Skip to main content

Advertisement

Log in

Role of Matricellular Proteins in Disorders of the Central Nervous System

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Matricellular proteins (MCPs) are actively expressed non-structural proteins present in the extracellular matrix, which rapidly turnover and possess regulatory roles, as well as mediate cell–cell interactions. MCPs characteristically contain binding sites for other extracellular proteins, cell surface receptors, growth factors, cytokines and proteases, that provide structural support for surrounding cells. MCPs are present in most organs, including brain, and play a major role in cell–cell interactions and tissue repair. Among the MCPs found in brain include thrombospondin-1/2, secreted protein acidic and rich in cysteine family (SPARC), including Hevin/SC1, Tenascin C and CYR61/Connective Tissue Growth Factor/Nov family of proteins, glypicans, galectins, plasminogen activator inhibitor (PAI-1), autotaxin, fibulin and perisostin. This review summarizes the potential role of MCPs in the pathogenesis of major neurological disorders, including Alzheimer’s disease, amyotrophic lateral sclerosis, ischemia, trauma, hepatic encephalopathy, Down’s syndrome, autism, multiple sclerosis, brain neoplasms, Parkinson’s disease and epilepsy. Potential therapeutic opportunities of MCP’s for these disorders are also considered in this review.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Hay ED (1981) Extracellular matrix. J Cell Biol 91(3):205s–223s

    Article  CAS  PubMed  Google Scholar 

  2. Edgar D (1985) Nerve growth factors and molecules of the extracellular matrix in neuronal development. J Cell Sci Suppl 3:107–113

    Article  CAS  PubMed  Google Scholar 

  3. Novak U, Kaye AH (2000) Extracellular matrix and the brain: components and function. J Clin Neurosci 7(4):280–290

    Article  CAS  PubMed  Google Scholar 

  4. Martin GR, Kleinman HK (1985) The extracellular matrix in development and in disease. Semin Liver Dis 5(2):147–156

    Article  CAS  PubMed  Google Scholar 

  5. Sethi MK, Zaia J (2016) Extracellular matrix proteomics in schizophrenia and Alzheimer’s disease. Anal Bioanal Chem. doi:10.1007/s00216-016-9900-6

    PubMed  Google Scholar 

  6. Nicholson C, Syková E (1998) Extracellular space structure revealed by diffusion analysis. Trends Neurosci 21(5):207–215

    Article  CAS  PubMed  Google Scholar 

  7. Barros CS, Franco SJ, Müller U (2011) Extracellular matrix: functions in the nervous system. Cold Spring Harb Perspect Biol 3(1):a005108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130(3):503–506

    Article  CAS  PubMed  Google Scholar 

  9. Bornstein P, Sage EH (2002) Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol 14(5):608–616

    Article  CAS  PubMed  Google Scholar 

  10. Roberts DD (2011) Emerging functions of matricellular proteins. Cell Mol Life Sci 68(19):3133–3136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bornstein P (2009) Thrombospondins function as regulators of angiogenesis. J Cell Commun Signal 3(3–4):189–200

    Article  PubMed  PubMed Central  Google Scholar 

  12. Wolf FW, Eddy RL, Shows TB, Dixit VM (1990) Structure and chromosomal localization of the human thrombospondin gene. Genomics 6(4):685–691

    Article  CAS  PubMed  Google Scholar 

  13. Jaffe E, Bornstein P, Disteche CM (1990) Mapping of the thrombospondin gene to human chromosome 15 and mouse chromosome 2 by in situ hybridization. Genomics 7(1):123–126

    Article  CAS  PubMed  Google Scholar 

  14. Li Z, Calzada MJ, Sipes JM, Cashel JA, Krutzsch HC, Annis DS, Mosher DF, Roberts DD (2002) Interactions of thrombospondins with alpha4beta1 integrin and CD47 differentially modulate T cell behavior. J Cell Biol 157(3):509–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Asch AS, Leung LL, Shapiro J, Nachman RL (1986) Human brain glial cells synthesize thrombospondin. Proc Natl Acad Sci USA 83(9):2904–2908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jayakumar AR, Tong XY, Curtis KM, Ruiz-Cordero R, Shamaladevi N, Abuzamel M, Johnstone J, Gaidosh G, Rama Rao KV, Norenberg MD (2004) Decreased astrocytic thrombospondin-1 secretion after chronic ammonia treatment reduces the level of synaptic proteins: in vitro and in vivo studies. J Neurochem 131(3):333–347

    Article  CAS  Google Scholar 

  17. Lu Z, Kipnis J (2010) Thrombospondin 1–a key astrocyte-derived neurogenic factor. FASEB J 24(6):1925–1934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Rama Rao KV, Curtis KM, Johnstone JT, Norenberg MD (2013) Amyloid-β inhibits thrombospondin 1 release from cultured astrocytes: effects on synaptic protein expression. J Neuropathol Exp Neurol 72(8):735–744

    Article  CAS  PubMed  Google Scholar 

  19. Yonezawa T, Hattori S, Inagaki J, Kurosaki M, Takigawa T, Hirohata S, Miyoshi T, Ninomiya Y (2010) Type IV collagen induces expression of thrombospondin-1 that is mediated by integrin alpha1beta1 in astrocytes. Glia 58(7):755–767

    PubMed  Google Scholar 

  20. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120(3):421–433

    Article  CAS  PubMed  Google Scholar 

  21. Tran MD, Neary JT (2006) Purinergic signaling induces thrombospondin-1 expression in astrocytes. Proc Natl Acad Sci USA 103(24):9321–9326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Eroglu C, Allen NJ, Susman MW, O’Rourke NA, Park CY, Ozkan E, Chakraborty C, Mulinyawe SB, Annis DS, Huberman AD, Green EM, Lawler J, Dolmetsch R, Garcia KC, Smith SJ, Luo ZD, Rosenthal A, Mosher DF, Barres BA (2009) Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139(2):380–392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Xu J, Xiao N, Xia J (2010) Thrombospondin 1 accelerates synaptogenesis in hippocampal neurons through neuroligin 1. Nat Neurosci 13(1):22–24

    Article  CAS  PubMed  Google Scholar 

  24. Crawford DC, Jiang X, Taylor A, Mennerick S (2012) Astrocyte-derived thrombospondins mediate the development of hippocampal presynaptic plasticity in vitro. J Neurosci 32(38):13100–13110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Adams JC (2001) Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol 17:25–51

    Article  CAS  PubMed  Google Scholar 

  26. Petrik JJ, Gentry PA, Feige JJ, LaMarre J (2002) Expression and localization of thrombospondin-1 and -2 and their cell-surface receptor, CD36, during rat follicular development and formation of the corpus luteum. Biol Reprod 67(5):1522–1531

    Article  CAS  PubMed  Google Scholar 

  27. Goicoechea S, Pallero MA, Eggleton P, Michalak M, Murphy-Ullrich JE (2002) The anti-adhesive activity of thrombospondin is mediated by the N-terminal domain of cell surface calreticulin. J Biol Chem 277(40):37219–37228

    Article  CAS  PubMed  Google Scholar 

  28. Lopes N, Gregg D, Vasudevan S, Hassanain H, Goldschmidt-Clermont P, Kovacic H (2003) Thrombospondin 2 regulates cell proliferation induced by Rac1 redox-dependent signaling. Mol Cell Biol 23(15):5401–5408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lawler PR, Lawler J (2012) Molecular basis for the regulation of angiogenesis by thrombospondin-1 and -2. Cold Spring Harb Perspect Med 2(5):a006627

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Krady MM, Zeng J, Yu J, MacLauchlan S, Skokos EA, Tian W, Bornstein P, Sessa WC, Kyriakides TR (2008) Thrombospondin-2 modulates extracellular matrix remodeling during physiological angiogenesis. Am J Pathol 173(3):879–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ribeiro SM, Poczatek M, Schultz-Cherry S, Villain M, Murphy-Ullrich JE (1999) The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J Biol Chem 274(19):13586–13593

    Article  CAS  PubMed  Google Scholar 

  32. Carlson CB, Bernstein DA, Annis DS, Misenheimer TM, Hannah BL, Mosher DF, Keck JL (2005) Structure of the calcium-rich signature domain of human thrombospondin-2. Nat Struct Mol Biol 12(10):910–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Hoffmann BR, Liu Y, Mosher DF (2012) Modification of EGF-like module 1 of thrombospondin-1, an animal extracellular protein, by O-linked N-acetylglucosamine. PLoS One 7(3):e32762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kyriakides TR, Zhu YH, Smith LT, Bain SD, Yang Z, Lin MT, Danielson KG, Iozzo RV, LaMarca M, McKinney CE, Ginns EI, Bornstein P (1998) Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J Cell Biol 140(2):419–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Scott-Drew S (1997) Expression and function of thrombospondin-1 in myelinating glial cells of the central nervous system. J Neurosci Res 50(2):202–214

    Article  CAS  PubMed  Google Scholar 

  36. Son SM, Nam DW, Cha MY, Kim KH, Byun J, Ryu H, Mook-Jung I (2015) Thrombospondin-1 prevents amyloid beta-mediated synaptic pathology in Alzheimer’s disease. Neurobiol Aging 36(12):3214–3227

    Article  CAS  PubMed  Google Scholar 

  37. Buée L, Hof PR, Roberts DD, Delacourte A, Morrison JH, Fillit HM (1992) Immunohistochemical identification of thrombospondin in normal human brain and in Alzheimer’s disease. Am J Pathol 141:783–788

    PubMed  PubMed Central  Google Scholar 

  38. Norenberg MD, Rama Rao KV, Jayakumar AR (2009) Signaling factors in the mechanism of ammonia neurotoxicity. Metab Brain Dis 24(1):103–117

    Article  CAS  PubMed  Google Scholar 

  39. Jayakumar AR, Rama Rao KV, Norenberg MD (2015) Neuroinflammation in hepatic encephalopathy: mechanistic aspects. J Clin Exp Hepatol 5(Suppl 1):S21–S28

    Article  PubMed  Google Scholar 

  40. Jones EA, Weissenborn K (1997) Neurology and the liver. J Neurol Neurosurg Psychiatry 63:279–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hazell AS, Butterworth RF (1999) Hepatic encephalopathy: An update of pathophysiologic mechanisms. Proc Soc Exp Biol Med 222:99–112

    Article  CAS  PubMed  Google Scholar 

  42. Norenberg MD (1981) The astrocyte in liver disease. In: Fedoroff S, Hertz L (eds) Advances in cellular neurobiology, vol 2. Academic Press, New York, pp 303–352

    Google Scholar 

  43. Martin H, Voss K, Hufnagl P, Wack R, Wassilew G (1987) Morphometric and densitometric investigations of protoplasmic astrocytes and neurons in human hepatic encephalopathy. Exp Pathol 32:241–250

    Article  CAS  PubMed  Google Scholar 

  44. Pfrieger FW (2010) Role of glial cells in the formation and maintenance of synapses. Brain Res Rev 63(1–2):39–46

    Article  CAS  PubMed  Google Scholar 

  45. Gibson G, Zimber A, Krook L, Richardson EJ, Visek W (1974) Brain histology and behaviour of mice injected with urease. J Neuropathol 33:201–211

    Article  CAS  Google Scholar 

  46. Norenberg MD (1998) Astroglial dysfunction in hepatic encephalopathy. Metab Brain Dis 13(4):319–335

    Article  CAS  PubMed  Google Scholar 

  47. Albrecht J, Zielińska M (2014) Deficit of astroglia-derived thrombospondin-1 and loss of synaptic proteins in hepatic encephalopathy: do ammonia-overexposed astrocytes derange the synaptic hardware? J Neurochem 131(3):265–277

    Article  CAS  PubMed  Google Scholar 

  48. Lin TN, Kim GM, Chen JJ, Cheung WM, He YY, Hsu CY (2003) Differential regulation of thrombospondin-1 and thrombospondin-2 after focal cerebral ischemia/reperfusion. Stroke 34(1):177–186

    Article  CAS  PubMed  Google Scholar 

  49. Hayashi T, Noshita N, Sugawara T, Chan PH (2003) Temporal profile of angiogenesis and expression of related genes in the brain after ischemia. J Cereb Blood Flow Metab 23(2):166–180

    Article  CAS  PubMed  Google Scholar 

  50. Hu CJ, Chen SD, Yang DI, Lin TN, Chen CM, Huang TH, Hsu CY (2006) Promoter region methylation and reduced expression of thrombospondin-1 after oxygen-glucose deprivation in murine cerebral endothelial cells. J Cereb Blood Flow Metab 26(12):1519–1526

    Article  CAS  PubMed  Google Scholar 

  51. Liauw J, Hoang S, Choi M, Eroglu C, Choi M, Sun GH, Percy M, Wildman-Tobriner B, Bliss T, Guzman RG, Barres BA, Steinberg GK (2008) Thrombospondins 1 and 2 are necessary for synaptic plasticity and functional recovery after stroke. J Cereb Blood Flow Metab 28(10):1722–1732

    Article  CAS  PubMed  Google Scholar 

  52. Faulcon LM, Fu Z, Dulloor P, Barron-Casella E, Savage W, Jennings JM, Van Eyk JE, Debaun M, Casella JF, Everett A (2013) Thrombospondin-1 and L-selectin are associated with silent cerebral infarct in children with sickle cell anaemia. Br J Haematol 162(3):421–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Jiang Y, Wang LP, Dong XH, Cai J, Jiang GJ, Zhang C, Xie HH (2015) Trace amounts of copper in drinking water aggravate cerebral ischemic injury via impairing endothelial progenitor cells in mice. CNS Neurosci Ther 21(8):677–680

    Article  PubMed  Google Scholar 

  54. Gao JB, Tang WD, Wang HX, Xu Y (2015) Predictive value of thrombospondin-1 for outcomes in patients with acute ischemic stroke. Clin Chim Acta 450:176–180

    Article  CAS  PubMed  Google Scholar 

  55. Cekanaviciute E, Fathali N, Doyle KP, Williams AM, Han J, Buckwalter MS (2014) Astrocytic transforming growth factor-beta signaling reduces subacute neuroinflammation after stroke in mice. Glia 62(8):1227–1240

    Article  PubMed  PubMed Central  Google Scholar 

  56. Xing C, Wang X, Cheng C, Montaner J, Mandeville E, Leung W, van Leyen K, Lok J, Wang X, Lo EH (2014) Neuronal production of lipocalin-2 as a help-me signal for glial activation. Stroke 45(7):2085–2092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Tran MD, Furones-Alonso O, Sanchez-Molano J, Bramlett HM (2012) Trauma-induced expression of astrocytic thrombospondin-1 is regulated by P2 receptors coupled to protein kinase cascades. Neuroreport 23(12):721–726

    Article  CAS  PubMed  Google Scholar 

  58. Garcia O, Torres M, Helguera P, Coskun P, Busciglio J (2010) A role for thrombospondin-1 deficits in astrocyte-mediated spine and synaptic pathology in Down’s syndrome. PLoS One 5(12):e14200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lu L, Guo H, Peng Y, Xun G, Liu Y, Xiong Z, Tian D, Liu Y, Li W, Xu X, Zhao J, Hu Z, Xia K (2014) Common and rare variants of the THBS1 gene associated with the risk for autism. Psychiatr Genet 24(6):235–240

    Article  CAS  PubMed  Google Scholar 

  60. Proschel C, Stripay JL, Shih CH, Munger JC, Noble MD (2014) Delayed transplantation of precursor cell-derived astrocytes provides multiple benefits in a rat model of Parkinsons. EMBO Mol Med 6(4):504–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Reiher FK, Volpert OV, Jimenez B, Crawford SE, Dinney CP, Henkin J, Haviv F, Bouck NP, Campbell SC (2002) Inhibition of tumor growth by systemic treatment with thrombospondin-1 peptide mimetics. Int J Cancer 98(5):682–689

    Article  CAS  PubMed  Google Scholar 

  62. Naganuma H, Satoh E, Asahara T, Amagasaki K, Watanabe A, Satoh H, Kuroda K, Zhang L, Nukui H (2004) Quantification of thrombospondin-1 secretion and expression of alphavbeta3 and alpha3beta1 integrins and syndecan-1 as cell-surface receptors for thrombospondin-1 in malignant glioma cells. J Neurooncol 70(3):309–317

    Article  PubMed  Google Scholar 

  63. Bogdanov A Jr, Marecos E, Cheng HC, Chandrasekaran L, Krutzsch HC, Roberts DD, Weissleder R (1999) Treatment of experimental brain tumors with trombospondin-1 derived peptides: an in vivo imaging study. Neoplasia 1(5):438–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hsu SC, Volpert OV, Steck PA, Mikkelsen T, Polverini PJ, Rao S, Chou P, Bouck NP (1996) Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1. Cancer Res 56(24):5684–5691

    CAS  PubMed  Google Scholar 

  65. Pijuan-Thompson V, Grammer JR, Stewart J, Silverstein RL, Pearce SF, Tuszynski GP, Murphy-Ullrich JE, Gladson CL (1999) Retinoic acid alters the mechanism of attachment of malignant astrocytoma and neuroblastoma cells to thrombospondin-1. Exp Cell Res 249(1):86–101

    Article  CAS  PubMed  Google Scholar 

  66. Harada H, Nakagawa K, Saito M, Kohno S, Nagato S, Furukawa K, Kumon Y, Hamada K, Ohnishi T (2003) Introduction of wild-type p53 enhances thrombospondin-1 expression in human glioma cells. Cancer Lett 191(1):109–119

    Article  CAS  PubMed  Google Scholar 

  67. Anderson JC, Grammer JR, Wang W, Nabors LB, Henkin J, Stewart JE Jr, Gladson CL (2007) ABT-510, a modified type 1 repeat peptide of thrombospondin, inhibits malignant glioma growth in vivo by inhibiting angiogenesis. Cancer Biol Ther 6(3):454–462

    Article  CAS  PubMed  Google Scholar 

  68. Cho S, Kim E (2009) CD36: a multi-modal target for acute stroke therapy. J Neurochem 109(Suppl 1):126–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Chiquet-Ehrismann R (2004) Tenascins. Int J Biochem Cell Biol 36(6):986–990

    Article  CAS  PubMed  Google Scholar 

  70. Karus M, Denecke B, Wiese S, Faissner A (2011) The extracellular matrix molecule tenascin C modulates expression levels and territories of key patterning genes during spinal cord astrocyte specification. Development 138(24):5321–5331

    Article  CAS  PubMed  Google Scholar 

  71. Pesheva P, Gloor S, Probstmeier R (2001) Tenascin-R as a regulator of CNS glial cell function. Prog Brain Res 132:103–114

    Article  CAS  PubMed  Google Scholar 

  72. Jones EV, Bouvier DS (2014) Astrocyte-secreted matricellular proteins in CNS remodelling during development and disease. Neural Plast 2014. doi:10.1155/2014/321209

    Google Scholar 

  73. Garcion E, Faissner A (2001) Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 128(13):2485–2496

    CAS  PubMed  Google Scholar 

  74. Garwood J, Garcion E, Dobbertin A, Heck N, Calco V Faissner A (2004) The extracellular matrix glycoprotein Tenascin-C is expressed by oligodendrocyte precursor cells and required for the regulation of maturation rate, survival and responsiveness to platelet-derived growth factor. Eur J Neurosci 20(10):2524–2540

    Article  PubMed  Google Scholar 

  75. Czopka T, Von Holst A, Schmidt G Faissner A (2009) Tenascin C and tenascin R similarly prevent the formation of myelin membranes in a RhoA-dependent manner, but antagonistically regulate the expression of myelin basic protein via a separate pathway. Glia 57(16):1790–1801

    Article  PubMed  Google Scholar 

  76. Moritz S, Lehmann S, Faissner A, von Holst A (2008) An induction gene trap screen in neural stem cells reveals an instructive function of the niche and identifies the splicing regulator sam68 as a tenascin-C-regulated target gene. Stem Cells 26(9):2321–2331

    Article  CAS  PubMed  Google Scholar 

  77. Faissner A, Kruse J (1990) J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5(5):627–637

    Article  CAS  PubMed  Google Scholar 

  78. Lochter A, Vaughan L, Kaplony A, Prochiantz A, Schachner M, Faissner A (1991) J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J Cell Biol 113(5):1159–1171

    Article  CAS  PubMed  Google Scholar 

  79. Husmann K, Faissner A, Schachner M (1992) Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J Cell Biol 116(6):1475–1486

    Article  CAS  PubMed  Google Scholar 

  80. Götz B, Scholze A, Clement A, Joester A, Schütte K, Wigger F, Frank R, Spiess E, Ekblom P, Faissner A (1996) Tenascin-C contains distinct adhesive, anti-adhesive, and neurite outgrowth promoting sites for neurons. J Cell Biol 132(4):681–699

    Article  PubMed  Google Scholar 

  81. Götz M, Bolz J, Joester A, Faissner A (1997) Tenascin-C synthesis and influence on axonal growth during rat cortical development. Eur J Neurosci 9(3):496–506

    Article  PubMed  Google Scholar 

  82. Meiners S, Geller HM (1997) Long and short splice variants of human tenascin differentially regulate neurite outgrowth. Mol Cell Neurosci 10(1–2):100–116

    Article  CAS  PubMed  Google Scholar 

  83. Meiners S, Powell EM, Geller HM (1999) Neurite outgrowth promotion by the alternatively spliced region of tenascin-C is influenced by cell-type specific binding. Matrix Biol 18(1):75–87

    Article  CAS  PubMed  Google Scholar 

  84. Erickson HP (1993) Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions. Curr Opin Cell Biol 5(5):869–876

    Article  CAS  PubMed  Google Scholar 

  85. Wiese S, Karus M, Faissner A (2012) Astrocytes as a source for extracellular matrix molecules and cytokines. Front Pharmacol 3:120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Laywell ED, Dörries U, Bartsch U, Faissner A, Schachner M, Steindler DA (1992) Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc Natl Acad Sci U S A 89(7):2634–2638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Hausmann R, Betz P (2000) The time course of the vascular response to human brain injury–an immunohistochemical study. Int J Legal Med 113(5):288–292

    Article  CAS  PubMed  Google Scholar 

  88. Nishio T, Kawaguchi S, Yamamoto M, Iseda T, Kawasaki T, Hase T (2005) Tenascin-C regulates proliferation and migration of cultured astrocytes in a scratch wound assay. Neuroscience 132(1):87–102

    Article  CAS  PubMed  Google Scholar 

  89. Wanner IB, Deik A, Torres M, Rosendahl A, Neary JT, Lemmon VP, Bixby JL (2008) A new in vitro model of the glial scar inhibits axon growth. Glia 56(15):1691–1709. doi:10.1002/glia.20721

    Article  PubMed  PubMed Central  Google Scholar 

  90. Lin HW, Basu A, Druckman C, Cicchese M, Krady JK, Levison SW (2006) Astrogliosis is delayed in type 1 interleukin-1 receptor-null mice following a penetrating brain injury. J Neuroinflammation 30(3):15

    Article  CAS  Google Scholar 

  91. Yu YM, Cristofanilli M, Valiveti A, Ma L, Yoo M, Morellini F, Schachner M (2011) The extracellular matrix glycoprotein tenascin-C promotes locomotor recovery after spinal cord injury in adult zebrafish. Neuroscience 183:238–250

    Article  CAS  PubMed  Google Scholar 

  92. Jakovcevski I, Miljkovic D, Schachner M, Andjus PR (2013) Tenascins and inflammation in disorders of the nervous system. Amino Acids 44(4):1115–1127

    Article  CAS  PubMed  Google Scholar 

  93. Zhang Y, Winterbottom JK, Schachner M, Lieberman AR, Anderson PN (1997) Tenascin-C expression and axonal sprouting following injury to the spinal dorsal columns in the adult rat. J Neurosci Res 49(4):433–450

    Article  CAS  PubMed  Google Scholar 

  94. Deller T, Haas CA, Naumann T, Joester A, Faissner A, Frotscher M (1997) Up-regulation of astrocyte-derived tenascin-C correlates with neurite outgrowth in the rat dentate gyrus after unilateral entorhinal cortex lesion. Neuroscience 81(3):829–846

    Article  CAS  PubMed  Google Scholar 

  95. Ikeshima-Kataoka H, Shen JS, Eto Y, Saito S, Yuasa S (2008) Alteration of inflammatory cytokine production in the injured central nervous system of tenascin-deficient mice. In Vivo 22(4):409–413

    PubMed  Google Scholar 

  96. Gates MA, Fillmore H, Steindler DA (1996) Chondroitin sulfate proteoglycan and tenascin in the wounded adult mouse neostriatum in vitro: dopamine neuron attachment and process outgrowth. J Neurosci 16(24):8005–8018

    CAS  PubMed  Google Scholar 

  97. Soares HD, Potter WZ, Pickering E, Kuhn M, Immermann FW, Shera DM, Ferm M, Dean RA, Simon AJ, Swenson F, Siuciak JA, Kaplow J, Thambisetty M, Zagouras P, Koroshetz WJ, Wan HI, Trojanowski JQ, Shaw LM (2012) Plasma biomarkers associated with the apolipoprotein E genotype and Alzheimer disease. Biomarkers consortium Alzheimer’s disease plasma proteomics project. Arch Neurol 69(10):1310–1317

    Article  PubMed  PubMed Central  Google Scholar 

  98. Mi Z, Halfter W, Abrahamson EE, Klunk WE, Mathis CA, Mufson EJ, Ikonomovic MD (2016) Tenascin-C Is associated with cored amyloid-β plaques in Alzheimer disease and pathology burdened cognitively normal elderly. J Neuropathol Exp Neurol 75(9):868–876

    Article  PubMed  Google Scholar 

  99. Xie K, Liu Y, Hao W, Walter S, Penke B, Hartmann T, Schachner M, Fassbender K (2013) Tenascin-C deficiency ameliorates Alzheimer’s disease-related pathology in mice. Neurobiol Aging 34(10):2389–2398

    Article  CAS  PubMed  Google Scholar 

  100. Gutowski NJ, Newcombe J, Cuzner ML (1999) Tenascin-R and C in multiple sclerosis lesions: relevance to extracellular matrix remodelling. Neuropathol Appl Neurobiol 25(3):207–214

    Article  CAS  PubMed  Google Scholar 

  101. Harada M, Kamimura D, Arima Y, Kohsaka H, Nakatsuji Y, Nishida M, Atsumi T, Meng J, Bando H, Singh R, Sabharwal L, Jiang JJ, Kumai N, Miyasaka N, Sakoda S, Yamauchi-Takihara K, Ogura H, Hirano T, Murakami M (2015) Temporal expression of growth factors triggered by epiregulin regulates inflammation development. J Immunol 194(3):1039–1046

    Article  CAS  PubMed  Google Scholar 

  102. Holley JE, Gveric D, Whatmore JL, Gutowski NJ (2005) Tenascin C induces a quiescent phenotype in cultured adult human astrocytes. Glia 52(1):53–58

    Article  PubMed  Google Scholar 

  103. Zendedel A, Kashani IR, Azimzadeh M, Pasbakhsh P, Omidi N, Golestani A, Beyer C, Clarner T (2016) Regulatory effect of triiodothyronine on brain myelination and astrogliosis after cuprizone-induced demyelination in mice. Metab Brain Dis 31(2):425–433

    Article  CAS  PubMed  Google Scholar 

  104. Niquet J, Jorquera I, Faissner A, Ben-Ari Y, Represa A (1995) Gliosis and axonal sprouting in the hippocampus of epileptic rats are associated with an increase of tenascin-C immunoreactivity. J Neurocytol 24(8):611–624

    Article  CAS  PubMed  Google Scholar 

  105. Nakic M, Mitrovic N, Sperk G, Schachner M (1996) Kainic acid activates transient expression of tenascin-C in the adult rat hippocampus. J Neurosci Res 44(4):355–362

    Article  CAS  PubMed  Google Scholar 

  106. Ferhat L, Chevassus-Au-Louis N, Khrestchatisky M, Ben-Ari Y, Represa A (1996) Seizures induce tenascin-C mRNA expression in neurons. J Neurocytol 25(9):535–546

    Article  CAS  PubMed  Google Scholar 

  107. Mahler M, Ferhat L, Gillian A, Ben-Ari Y, Represa A (1996) Tenascin-C mRNA and tenascin-C protein immunoreactivity increase in astrocytes after activation by bFGF. Cell Adhes Commun 4(3):175–186

    Article  CAS  PubMed  Google Scholar 

  108. Represa A, Ben-Ari Y (1997) Molecular and cellular cascades in seizure-induced neosynapse formation. Adv Neurol 72:25–34

    CAS  PubMed  Google Scholar 

  109. Blümcke I, Beck H, Lie AA, Wiestler OD (1999) Molecular neuropathology of human mesial temporal lobe epilepsy. Epilepsy Res 36(2–3):205–223

    Article  PubMed  Google Scholar 

  110. Heck N, Garwood J, Loeffler JP, Larmet Y, Faissner A (2004) Differential upregulation of extracellular matrix molecules associated with the appearance of granule cell dispersion and mossy fiber sprouting during epileptogenesis in a murine model of temporal lobe epilepsy. Neuroscience 129(2):309–324

    Article  CAS  PubMed  Google Scholar 

  111. Mercado-Gómez O, Landgrave-Gómez J, Arriaga-Avila V, Nebreda-Corona A, Guevara-Guzmán R (2014) Role of TGF-β signaling pathway on Tenascin C protein upregulation in a pilocarpine seizure model. Epilepsy Res 108(10):1694–1704

    Article  PubMed  CAS  Google Scholar 

  112. Brenneke F, Bukalo O, Dityatev A, Lie AA (2004a) Mice deficient for the extracellular matrix glycoprotein tenascin-r show physiological and structural hallmarks of increased hippocampal excitability, but no increased susceptibility to seizures in the pilocarpine model of epilepsy. Neuroscience 124(4):841–855

    Article  CAS  PubMed  Google Scholar 

  113. Brenneke F, Schachner M, Elger CE, Lie AA (2004b) Up-regulation of the extracellular matrix glycoprotein tenascin-R during axonal reorganization and astrogliosis in the adult rat hippocampus. Epilepsy Res 58(2–3):133–143

    Article  CAS  PubMed  Google Scholar 

  114. Hoffmann K, Sivukhina E, Potschka H, Schachner M, Löscher W, Dityatev A (2009) Retarded kindling progression in mice deficient in the extracellular matrix glycoprotein tenascin-R. Epilepsia 50(4):859–869

    Article  CAS  PubMed  Google Scholar 

  115. Lee Y, Bullard DE, Humphrey PA, Colapinto EV, Friedman HS, Zalutsky MR, Coleman RE, Bigner DD (1988a) Treatment of intracranial human glioma xenografts with 131I-labeled anti-tenascin monoclonal antibody 81C6. Cancer Res 48(10):2904–2910

    CAS  PubMed  Google Scholar 

  116. Lee YS, Bullard DE, Zalutsky MR, Coleman RE, Wikstrand CJ, Friedman HS, Colapinto EV, Bigner DD (1988b) Therapeutic efficacy of antiglioma mesenchymal extracellular matrix 131I-radiolabeled murine monoclonal antibody in a human glioma xenograft model. Cancer Res 48(3):559–566

    CAS  PubMed  Google Scholar 

  117. Higuchi M, Ohnishi T, Arita N, Hiraga S, Hayakawa T (1993) Expression of tenascin in human gliomas: its relation to histological malignancy, tumor dedifferentiation and angiogenesis. Acta Neuropathol 85(5):481–487

    Article  CAS  PubMed  Google Scholar 

  118. Yoshida J, Wakabayashi T, Okamoto S, Kimura S, Washizu K, Kiyosawa K, Mokuno K (1994) Tenascin in cerebrospinal fluid is a useful biomarker for the diagnosis of brain tumour. J Neurol Neurosurg Psychiatry 57(10):1212–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Donato G, Lavano A, Volpentesta G, Chirchiglia D, Signorelli CD, Tucci L (1997) Expression of tenascin in astrocytic tumours: too much ado about nothing? J Neurol Neurosurg Psychiatry 63(3):413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Jallo GI, Friedlander DR, Kelly PJ, Wisoff JH, Grumet M, Zagzag D (1997) Tenascin-C expression in the cyst wall and fluid of human brain tumors correlates with angiogenesis. Neurosurgery 41(5):1052–1059

    Article  CAS  PubMed  Google Scholar 

  121. Nie S, Gurrea M, Zhu J, Thakolwiboon S, Heth JA, Muraszko KM, Fan X, Lubman DM (2015) Tenascin-C: a novel candidate marker for cancer stem cells in glioblastoma identified by tissue microarrays. J Proteome Res 14(2):814–822

    Article  CAS  PubMed  Google Scholar 

  122. Sarkar S, Zemp FJ, Senger D, Robbins SM, Yong VW (2015) ADAM-9 is a novel mediator of tenascin-C-stimulated invasiveness of brain tumor-initiating cells. Neuro-oncology 17(8):1095–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Vitolo D, Paradiso P, Uccini S, Ruco LP, Baroni CD (1996) Expression of adhesion molecules and extracellular matrix proteins in glioblastomas: relation to angiogenesis and spread. Histopathology 28(6):521–528

    Article  CAS  PubMed  Google Scholar 

  124. Zagzag D, Friedlander DR, Dosik J, Chikramane S, Chan W, Greco MA, Allen JC, Dorovini-Zis K, Grumet M (1996) Tenascin-C expression by angiogenic vessels in human astrocytomas and by human brain endothelial cells in vitro. Cancer Res 56(1):182–189

    CAS  PubMed  Google Scholar 

  125. Castellani P, Siri A, Zardi L, Barbanera A, Dorcaratto A, Viale G (1997) Distribution of tenascin in human malignant gliomas is not related to cell proliferation. J Neurol Neurosurg Psychiatry 62(3):290–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Hasegawa K, Yoshida T, Matsumoto K, Katsuta K, Waga S, Sakakura T (1997) Differential expression of tenascin-C and tenascin-X in human astrocytomas. Acta Neuropathol 93(5):431–437

    Article  CAS  PubMed  Google Scholar 

  127. Badruddoja MA, Black KL (2006) Improving the delivery of therapeutic agents to CNS neoplasms: a clinical review. Front Biosci 11:1466–1478

    Article  CAS  PubMed  Google Scholar 

  128. Brösicke N, Faissner A (2015) Role of tenascins in the ECM of gliomas. Cell Adh Migr 9(1–2):131–140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  129. Gladson CL (1999) The extracellular matrix of gliomas: modulation of cell function. J Neuropathol Exp Neurol 58(10):1029–1040

    Article  CAS  PubMed  Google Scholar 

  130. Leprini A, Querzé G, Zardi L (1994) Tenascin isoforms: possible targets for diagnosis and therapy of cancer and mechanisms regulating their expression. Perspect Dev Neurobiol 2(1):117–123

    CAS  PubMed  Google Scholar 

  131. Kurpad SN, Zhao XG, Wikstrand CJ, Batra SK, McLendon RE, Bigner DD (1995) Tumor antigens in astrocytic gliomas. Glia 15(3):244–256

    Article  CAS  PubMed  Google Scholar 

  132. Ruoslahti E (1996) Brain extracellular matrix. Glycobiology 6(5):489–492

    Article  CAS  PubMed  Google Scholar 

  133. Zamecnik J (2005) The extracellular space and matrix of gliomas. Acta Neuropathol 110(5):435–442

    Article  PubMed  Google Scholar 

  134. Kong X, Ma W, Li Y, Wang Y, Guan J, Gao J, Wei J, Yao Y, Lian W, Xu Z, Dou W, Xing B, Ren Z, Su C, Yang Y, Wang R (2015) Does Tenascin have clinical implications in pathological grade of glioma patients?: a systematic meta-analysis. Medicine 94(32):e1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Hau P, Kunz-Schughart LA, Rümmele P, Arslan F, Dörfelt A, Koch H, Lohmeier A, Hirschmann B, Müller A, Bogdahn U, Bosserhoff AK (2006) Tenascin-C protein is induced by transforming growth factor-beta1 but does not correlate with time to tumor progression in high-grade gliomas. J Neurooncol 77(1):1–7

    Article  CAS  PubMed  Google Scholar 

  136. Xia S, Lal B, Tung B, Wang S, Goodwin CR, Laterra J (2016) Tumor microenvironment tenascin-C promotes glioblastoma invasion and negatively regulates tumor proliferation. Neuro-oncology 18(4):507–517

    Article  PubMed  Google Scholar 

  137. Brack SS, Silacci M, Birchler M, Neri D (2006) Tumor-targeting properties of novel antibodies specific to the large isoform of tenascin-C. Clin Cancer Res 12(10):3200–3208

    Article  CAS  PubMed  Google Scholar 

  138. Herold-Mende C, Mueller MM, Bonsanto MM, Schmitt HP, Kunze S, Steiner HH (2002) Clinical impact and functional aspects of tenascin-C expression during glioma progression. Int J Cancer 98(3):362–369

    Article  CAS  PubMed  Google Scholar 

  139. Mai J, Sameni M, Mikkelsen T, Sloane BF (2002) Degradation of extracellular matrix protein tenascin-C by cathepsin B: an interaction involved in the progression of gliomas. Biol Chem 383(9):1407–1413

    Article  CAS  PubMed  Google Scholar 

  140. Maiuri F, Cappabianca P, Gangemi M, De Caro Mdel B, Esposito F, Pettinato G, de Divitiis O, Mignogna C, Strazzullo V, de Divitiis E (2006) Clinical progression and familial occurrence of cerebral cavernous angiomas: the role of angiogenic and growth factors. Neurosurg Focus 21(1):e3

    Article  PubMed  Google Scholar 

  141. Taga T, Suzuki A, Gonzalez-Gomez I, Gilles FH, Stins M, Shimada H, Barsky L, Weinberg KI, Laug WE (2002) alpha v-Integrin antagonist EMD 121974 induces apoptosis in brain tumor cells growing on vitronectin and tenascin. Int J Cancer 98(5):690-

    Article  CAS  PubMed  Google Scholar 

  142. Viale G, Dorcaratto A, Castellani P, Zardi L (2002) Tenascin-C in astrocytic tumors. Surg Neurol 57(4):286

    Article  PubMed  Google Scholar 

  143. Bigner DD, Brown MT, Friedman AH, Coleman RE, Akabani G, Friedman HS, Thorstad WL, McLendon RE, Bigner SH, Zhao XG, Pegram CN, Wikstrand CJ, Herndon JE 2nd, Vick NA, Paleologos N, Cokgor I, Provenzale JM, Zalutsky MR (1998) Iodine-131-labeled antitenascin monoclonal antibody 81C6 treatment of patients with recurrent malignant gliomas: phase I trial results. J Clin Oncol 16(6):2202–2212

    Article  CAS  PubMed  Google Scholar 

  144. Hirata E, Arakawa Y, Shirahata M, Yamaguchi M, Kishi Y, Okada T, Takahashi JA, Matsuda M, Hashimoto N (2009) Endogenous tenascin-C enhances glioblastoma invasion with reactive change of surrounding brain tissue. Cancer Sci 100(8):1451–1459

    Article  CAS  PubMed  Google Scholar 

  145. Marriott CJ, Thorstad W, Akabani G, Brown MT, McLendon RE, Hanson MW, Coleman RE (1998) Locally increased uptake of fluorine-18-fluorodeoxyglucose after intracavitary administration of iodine-131-labeled antibody for primary brain tumors. J Nucl Med 39(8):1376–1380

    CAS  PubMed  Google Scholar 

  146. Onishi M, Ichikawa T, Kurozumi K, Date I (2011) Angiogenesis and invasion in glioma. Brain Tumor Pathol 28(1):13–24

    Article  CAS  PubMed  Google Scholar 

  147. Sarkar S, Nuttall RK, Liu S, Edwards DR, Yong VW (2006) Tenascin-C stimulates glioma cell invasion through matrix metalloproteinase-12. Cancer Res 66(24):11771–11780

    Article  CAS  PubMed  Google Scholar 

  148. Sarkar S, Yong VW (2010) Reduction of protein kinase C delta attenuates tenascin-C stimulated glioma invasion in three-dimensional matrix. Carcinogenesis 31(2):311–317

    Article  CAS  PubMed  Google Scholar 

  149. Silacci M, Brack SS, Späth N, Buck A, Hillinger S, Arni S, Weder W, Zardi L, Neri D (2006) Human monoclonal antibodies to domain C of tenascin-C selectively target solid tumors in vivo. Protein Eng Des Sel 19(10):471–478

    Article  CAS  PubMed  Google Scholar 

  150. Zalutsky MR, Archer GE, Garg PK, Batra SK, Bigner DD (1996) Chimeric anti-tenascin antibody 81C6: increased tumor localization compared with its murine parent. Nucl Med Biol 23(4):449–458

    Article  CAS  PubMed  Google Scholar 

  151. Zukiel R, Nowak S, Wyszko E, Rolle K, Gawronska I, Barciszewska MZ, Barciszewski J (2006) Suppression of human brain tumor with interference RNA specific for tenascin-C. Cancer Biol Ther 5(8):1002–1007

    Article  CAS  PubMed  Google Scholar 

  152. Riva P, Arista A, Franceschi G, Frattarelli M, Sturiale C, Riva N, Casi M, Rossitti R (1995) Local treatment of malignant gliomas by direct infusion of specific monoclonal antibodies labeled with 131I: comparison of the results obtained in recurrent and newly diagnosed tumors. Cancer Res 55(23 Suppl):5952s–5956s

    CAS  PubMed  Google Scholar 

  153. Vincent AJ, Lau PW, Roskams AJ (2008) SPARC is expressed by macroglia and microglia in the developing and mature nervous system. Dev Dyn 237(5):1449–1462

    Article  PubMed  Google Scholar 

  154. Mendis DB, Malaval L, Brown IR (1995) SPARC, an extracellular matrix glycoprotein containing the follistatin module, is expressed by astrocytes in synaptic enriched regions of the adult brain. Brain Res 676(1):69–79

    Article  CAS  PubMed  Google Scholar 

  155. Mendis DB, Brown IR (1994) Expression of the gene encoding the extracellular matrix glycoprotein SPARC in the developing and adult mouse brain. Brain Res Mol Brain Res 24(1–4):11–19

    Article  CAS  PubMed  Google Scholar 

  156. Mendis DB, Ivy GO, Brown IR (1996) SC1, a brain extracellular matrix glycoprotein related to SPARC and follistatin, is expressed by rat cerebellar astrocytes following injury and during development. Brain Res 730(1–2):95–106

    Article  CAS  PubMed  Google Scholar 

  157. Murphy-Ullrich JE (2001) The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? J Clin Invest 107(7):785–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Brekken RA, Sage EH (2001) SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol 19(8):816–827

    Article  CAS  PubMed  Google Scholar 

  159. Yan Q, Sage EH (1999) SPARC, a matricellular glycoprotein with important biological functions. J Histochem Cytochem 47(12):1495–1506

    Article  CAS  PubMed  Google Scholar 

  160. Ikemoto M, Takita M, Imamura T, Inoue K (2000) Increased sensitivity to the stimulant effects of morphine conferred by anti-adhesive glycoprotein SPARC in amygdala. Nat Med 6(8):910–915

    Article  CAS  PubMed  Google Scholar 

  161. Kupprion C, Motamed K, Sage EH (1998) SPARC (BM-40, osteonectin) inhibits the mitogenic effect of vascular endothelial growth factor on microvascular endothelial cells. J Biol Chem 273(45):29635–29640

    Article  CAS  PubMed  Google Scholar 

  162. Vafadar-Isfahani B, Ball G, Coveney C, Lemetre C, Boocock D, Minthon L, Hansson O, Miles AK, Janciauskiene SM, Warden D, Smith AD, Wilcock G, Kalsheker N, Rees R, Matharoo-Ball B, Morgan K (2012) Identification of SPARC-like 1 protein as part of a biomarker panel for Alzheimer’s disease in cerebrospinal fluid. J Alzheimers Dis 28(3):625–636

    CAS  PubMed  Google Scholar 

  163. Richens JL, Vere KA, Light RA, Soria D, Garibaldi J, Smith AD, Warden D, Wilcock G, Bajaj N, Morgan K, O’Shea P (2014) Practical detection of a definitive biomarker panel for Alzheimer’s disease; comparisons between matched plasma and cerebrospinal fluid. Int J Mol Epidemiol Genet 5(2):53–70

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Lloyd-Burton SM, York EM, Anwar MA, Vincent AJ, Roskams AJ (2013) SPARC regulates microgliosis and functional recovery following cortical ischemia. J Neurosci 33(10):4468–4481

    Article  CAS  PubMed  Google Scholar 

  165. Baumann E, Preston E, Slinn J, Stanimirovic D (2009) Post-ischemic hypothermia attenuates loss of the vascular basement membrane proteins, agrin and SPARC, and the blood–brain barrier disruption after global cerebral ischemia. Brain Res 1269:185–197

    Article  CAS  PubMed  Google Scholar 

  166. Mendis DB, Ivy GO, Brown IR (2000) Induction of SC1 mRNA encoding a brain extracellular matrix glycoprotein related to SPARC following lesioning of the adult rat forebrain. Neurochem Res 25(12):1637–1644

    Article  CAS  PubMed  Google Scholar 

  167. Turtoi A, Musmeci D, Naccarato AG, Scatena C, Ortenzi V, Kiss R, Murtas D, Patsos G, Mazzucchelli G, De Pauw E, Bevilacqua G, Castronovo V (2012) Sparc-like protein 1 is a new marker of human glioma progression. J Proteome Res 11(10):5011–5021

    Article  CAS  PubMed  Google Scholar 

  168. Schultz C, Lemke N, Ge S, Golembieski WA, Rempel SA (2002) Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res 62(21):6270–6277

    CAS  PubMed  Google Scholar 

  169. Golembieski WA, Thomas SL, Schultz CR, Yunker CK, McClung HM, Lemke N, Cazacu S, Barker T, Sage EH, Brodie C, Rempel SA (2008) HSP27 mediates SPARC-induced changes in glioma morphology, migration, and invasion. Glia 56(10):1061–1075

    Article  PubMed  Google Scholar 

  170. Thomas SL, Alam R, Lemke N, Schultz LR, Gutiérrez JA, Rempel SA (2010) PTEN augments SPARC suppression of proliferation and inhibits SPARC-induced migration by suppressing SHC-RAF-ERK and AKT signaling. Neuro-oncology 12(9):941–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Thomas SL, Schultz CR, Mouzon E, Golembieski WA, El Naili R, Radakrishnan A, Lemke N, Poisson LM, Gutiérrez JA, Cottingham S, Rempel SA (2015) Loss of sparc in p53-null astrocytes promotes macrophage activation and phagocytosis resulting in decreased tumor size and tumor cell survival. Brain Pathol 25(4):391–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. McClung HM, Golembieski WA, Schultz CR, Jankowski M, Schultz LR, Rempel SA (2012) Deletion of the SPARC acidic domain or EGF-like module reduces SPARC-induced migration and signaling through p38 MAPK/HSP27 in glioma. Carcinogenesis 33(2):275–284

    Article  CAS  PubMed  Google Scholar 

  173. Shi Q, Bao S, Song L, Wu Q, Bigner DD, Hjelmeland AB, Rich JN (2007) Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 26(28):4084–4094

    Article  CAS  PubMed  Google Scholar 

  174. Yunker CK, Golembieski W, Lemke N, Schultz CR, Cazacu S, Brodie C, Rempel SA (2008) SPARC-induced increase in glioma matrix and decrease in vascularity are associated with reduced VEGF expression and secretion. Int J Cancer 122(12):2735–2743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Liu H, Xu Y, Chen Y, Zhang H, Fan S, Feng S, Liu F (2011) RNA interference against SPARC promotes the growth of U-87MG human malignant glioma cells. Oncol Lett 2(5):985–990

    CAS  PubMed  PubMed Central  Google Scholar 

  176. Capper D, Mittelbronn M, Goeppert B, Meyermann R, Schittenhelm J (2010) Secreted protein, acidic and rich in cysteine (SPARC) expression in astrocytic tumour cells negatively correlates with proliferation, while vascular SPARC expression is associated with patient survival. Neuropathol Appl Neurobiol 36(3):183–197

    Article  CAS  PubMed  Google Scholar 

  177. Seno T, Harada H, Kohno S, Teraoka M, Inoue A, Ohnishi T (2009) Downregulation of SPARC expression inhibits cell migration and invasion in malignant gliomas. Int J Oncol 34(3):707–715

    Article  CAS  PubMed  Google Scholar 

  178. Kucukdereli H, Allen NJ, Lee AT, Feng A, Ozlu MI, Conatser LM, Chakraborty C, Workman G, Weaver M, Sage EH, Barres BA, Eroglu C (2011) Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc Natl Acad Sci USA 108(32):E440–E449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Jones EV, Bernardinelli Y, Tse YC, Chierzi S, Wong TP, Murai KK (2011) Astrocytes control glutamate receptor levels at developing synapses through SPARC-beta-integrin interactions. J Neurosci 31(11):4154–4165

    Article  CAS  PubMed  Google Scholar 

  180. Au E, Richter MW, Vincent AJ, Tetzlaff W, Aebersold R, Sage EH, Roskams AJ (2007) SPARC from olfactory ensheathing cells stimulates Schwann cells to promote neurite outgrowth and enhances spinal cord repair. J Neurosci 27(27):7208–7221

    Article  CAS  PubMed  Google Scholar 

  181. Lorber B, Chew DJ, Hauck SM, Chong RS, Fawcett JW, Martin KR (2015) Retinal glia promote dorsal root ganglion axon regeneration. PLoS One 10(3):e0115996

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  182. Filmus J, Capurro M, Rast J (2008) Glypicans. Genome Biol 9(5):224

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  183. Svensson G, Awad W, Håkansson M, Mani K, Logan DT (2012) Crystal structure of N-glycosylated human glypican-1 core protein: structure of two loops evolutionarily conserved in vertebrate glypican-1. J Biol Chem 287(17):14040–14051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. David G, Lories V, Decock B, Marynen P, Cassiman JJ, Van den Berghe H (1990) Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J Cell Biol 111(6 Pt 2):3165–3176

    Article  CAS  PubMed  Google Scholar 

  185. Karthikeyan L, Maurel P, Rauch U, Margolis RK, Margolis RU (1992) Cloning of a major heparan sulfate proteoglycan from brain and identification as the rat form of glypican. Biochem Biophys Res Commun 188(1):395–401

    Article  CAS  PubMed  Google Scholar 

  186. Karthikeyan L, Flad M, Engel M, Meyer-Puttlitz B, Margolis RU, Margolis RK (1994) Immunocytochemical and in situ hybridization studies of the heparan sulfate proteoglycan, glypican, in nervous tissue. J Cell Sci 107(Pt 11):3213–3222

    CAS  PubMed  Google Scholar 

  187. Ivins JK, Litwack ED, Kumbasar A, Stipp CS, Lander AD (1997) Cerebroglycan, a developmentally regulated cell-surface heparan sulfate proteoglycan, is expressed on developing axons and growth cones. Dev Biol 184(2):320–332

    Article  CAS  PubMed  Google Scholar 

  188. Veugelers M, Vermeesch J, Reekmans G, Steinfeld R, Marynen P, David G (1997) Characterization of glypican-5 and chromosomal localization of human GPC5, a new member of the glypican gene family. Genomics 40(1):24–30

    Article  CAS  PubMed  Google Scholar 

  189. Saunders S, Paine-Saunders S, Lander AD (1997) Expression of the cell surface proteoglycan glypican-5 is developmentally regulated in kidney, limb, and brain. Dev Biol 190(1):78–93

    Article  CAS  PubMed  Google Scholar 

  190. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80(4):1267–1290

    CAS  PubMed  Google Scholar 

  191. Wang W, Dow KE (1997) Differential regulation of neuronal proteoglycans by activation of excitatory amino acid receptors. Neuroreport 8(3):659–663

    Article  CAS  PubMed  Google Scholar 

  192. Akita K, Toda M, Hosoki Y, Inoue M, Fushiki S, Oohira A, Okayama M, Yamashina I, Nakada H (2004) Heparan sulphate proteoglycans interact with neurocan and promote neurite outgrowth from cerebellar granule cells. Biochem J 383(Pt 1):129–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Rawson JM, Dimitroff B, Johnson KG, Rawson JM, Ge X, Van Vactor D, Selleck SB (2005) The heparan sulfate proteoglycans Dally-like and Syndecan have distinct functions in axon guidance and visual-system assembly in Drosophila. Curr Biol 15(9):833–838

    Article  CAS  PubMed  Google Scholar 

  194. Luxardi G, Galli A, Forlani S, Lawson K, Maina F, Dono R (2007) Glypicans are differentially expressed during patterning and neurogenesis of early mouse brain. Biochem Biophys Res Commun 352(1):55–60

    Article  CAS  PubMed  Google Scholar 

  195. Qiao D, Yang X, Meyer K, Friedl A (2008) Glypican-1 regulates anaphase promoting complex/cyclosome substrates and cell cycle progression in endothelial cells. Mol Biol Cell 19(7):2789–2801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Jen YH, Musacchio M, Lander AD (2009) Glypican-1 controls brain size through regulation of fibroblast growth factor signaling in early neurogenesis. Neural Dev 4:33. doi:10.1186/1749-8104-4-33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  197. van Horssen J, Otte-Höller I, David G, Maat-Schieman ML, van den Heuvel LP, Wesseling P, de Waal RM, Verbeek MM (2001) Heparan sulfate proteoglycan expression in cerebrovascular amyloid beta deposits in Alzheimer’s disease and hereditary cerebral hemorrhage with amyloidosis (Dutch) brains. Acta Neuropathol 102(6):604–614

    Article  PubMed  CAS  Google Scholar 

  198. van Horssen J, Kleinnijenhuis J, Maass CN, Rensink AA, Otte-Höller I, David G, van den Heuvel LP, Wesseling P, de Waal RM, Verbeek MM (2002) Accumulation of heparan sulfate proteoglycans in cerebellar senile plaques. Neurobiol Aging 23(4):537–545

    Article  PubMed  Google Scholar 

  199. Watanabe N, Araki W, Chui DH, Makifuchi T, Ihara Y, Tabira T (2004) Glypican-1 as an Abeta binding HSPG in the human brain: its localization in DIG domains and possible roles in the pathogenesis of Alzheimer’s disease. FASEB J 18(9):1013–1015

    CAS  PubMed  Google Scholar 

  200. Verbeek MM, Otte-Höller I, van den Born J, van den Heuvel LP, David G, Wesseling P, de Waal RM (1999) Agrin is a major heparan sulfate proteoglycan accumulating in Alzheimer’s disease brain. Am J Pathol 155(6):2115–2125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Williamson TG, Mok SS, Henry A, Cappai R, Lander AD, Nurcombe V, Beyreuther K, Masters CL, Small DH (1996) Secreted glypican binds to the amyloid precursor protein of Alzheimer’s disease (APP) and inhibits APP-induced neurite outgrowth. J Biol Chem 271(49):31215–31221

    Article  CAS  PubMed  Google Scholar 

  202. Cappai R, Cheng F, Ciccotosto GD, Needham BE, Masters CL, Multhaup G, Fransson LA, Mani K (2005) The amyloid precursor protein (APP) of Alzheimer disease and its paralog, APLP2, modulate the Cu/Zn-Nitric Oxide-catalyzed degradation of glypican-1 heparan sulfate in vivo. J Biol Chem 280(14):13913–13920

    Article  CAS  PubMed  Google Scholar 

  203. O’Callaghan P, Sandwall E, Li JP, Yu H, Ravid R, Guan ZZ, van Kuppevelt TH, Nilsson LN, Ingelsson M, Hyman BT, Kalimo H, Lindahl U, Lannfelt L, Zhang X (2008) Heparan sulfate accumulation with Abeta deposits in Alzheimer’s disease and Tg2576 mice is contributed by glial cells. Brain Pathol 18(4):548–561

    PubMed  PubMed Central  Google Scholar 

  204. Timmer NM, van Horssen J, Otte-Holler I, Wilhelmus MM, David G, van Beers J, de Waal RM, Verbeek MM (2009) Amyloid beta induces cellular relocalization and production of agrin and glypican-1. Brain Res 1260:38–46

    Article  CAS  PubMed  Google Scholar 

  205. Qiao D, Meyer K, Mundhenke C, Drew SA, Friedl A (2003) Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 signaling in brain endothelial cells. Specific role for glypican-1 in glioma angiogenesis. J Biol Chem 278(18):16045–16053

    Article  CAS  PubMed  Google Scholar 

  206. Qiao D, Meyer K, Friedl A (2013) Glypican 1 stimulates S phase entry and DNA replication in human glioma cells and normal astrocytes. Mol Cell Biol 33(22):4408–4421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Hill JJ, Jin K, Mao XO, Xie L, Greenberg DA (2012) Intracerebral chondroitinase ABC and heparan sulfate proteoglycan glypican improve outcome from chronic stroke in rats. Proc Natl Acad Sci USA 109(23):9155–9160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Fico A, de Chevigny A, Melon C, Bohic M, Kerkerian-Le Goff L, Maina F, Dono R, Cremer H (2014) Reducing glypican-4 in ES cells improves recovery in a rat model of Parkinson’s disease by increasing the production of dopaminergic neurons and decreasing teratoma formation. J Neurosci 34(24):8318–8323

    Article  PubMed  CAS  Google Scholar 

  209. Allen NJ, Bennett ML, Foo LC, Wang GX, Chakraborty C, Smith SJ, Barres BA (2012) Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486(7403):410–414

    CAS  PubMed  PubMed Central  Google Scholar 

  210. de Wit J, O’Sullivan ML, Savas JN, Condomitti G, Caccese MC, Vennekens KM, Yates JR 3rd, Ghosh A (2013) Unbiased discovery of glypican as a receptor for LRRTM4 in regulating excitatory synapse development. Neuron 79(4):696–711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  211. Ko JS, Pramanik G, Um JW, Shim JS, Lee D, Kim KH, Chung GY, Condomitti G, Kim HM, Kim H, de Wit J, Park KS, Tabuchi K, Ko J (2015) PTPσ functions as a presynaptic receptor for the glypican-4/LRRTM4 complex and is essential for excitatory synaptic transmission. Proc Natl Acad Sci USA 112(6):1874–1879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  212. Li J, Ye L, Owen S, Weeks HP, Zhang Z, Jiang WG (2015) Emerging role of CCN family proteins in tumorigenesis and cancer metastasis (Review). Int J Mol Med 36(6):1451–1463

    CAS  PubMed  PubMed Central  Google Scholar 

  213. Ishida J, Kurozumi K, Ichikawa T, Otani Y, Onishi M, Fujii K, Shimazu Y, Oka T, Shimizu T, Date I (2015) Evaluation of extracellular matrix protein CCN1 as a prognostic factor for glioblastoma. Brain Tumor Pathol 32(4):245–252

    Article  CAS  PubMed  Google Scholar 

  214. Albrecht C, von Der Kammer H, Mayhaus M, Klaudiny J, Schweizer M, Nitsch RM (2000) Muscarinic acetylcholine receptors induce the expression of the immediate early growth regulatory gene CYR61. J Biol Chem 275(37):28929–28936

    Article  CAS  PubMed  Google Scholar 

  215. Malik AR, Liszewska E, Jaworski J (2015) Matricellular proteins of the Cyr61/CTGF/NOV (CCN) family and the nervous system. Front Cell Neurosci 9:237

    Article  PubMed  PubMed Central  Google Scholar 

  216. Kondo Y, Nakanishi T, Takigawa M, Ogawa N (1999) Immunohistochemical localization of connective tissue growth factor in the rat central nervous system. Brain Res 834(1–2):146–151

    Article  CAS  PubMed  Google Scholar 

  217. Le Dréau G, Kular L, Nicot AB, Calmel C, Melik-Parsadaniantz S, Kitabgi P, Laurent M, Martinerie C (2010) NOV/CCN3 upregulates CCL2 and CXCL1 expression in astrocytes through beta1 and beta5 integrins. Glia 58(12):1510–1521

    PubMed  Google Scholar 

  218. Guo J, Cheng C, Chen CS, Xing X, Xu G, Feng J, Qin X (2016) Overexpression of Fibulin-5 attenuates ischemia/reperfusion injury after middle cerebral artery occlusion in rats. Mol Neurobiol 53(5):3154–3167

    Article  CAS  PubMed  Google Scholar 

  219. Guadall A, Orriols M, Rodríguez-Calvo R, Calvayrac O, Crespo J, Aledo R, Martínez-González J, Rodríguez C (2011) Fibulin-5 is up-regulated by hypoxia in endothelial cells through a hypoxia-inducible factor-1 (HIF-1α)-dependent mechanism. J Biol Chem 286(9):7093–7103

    Article  CAS  PubMed  Google Scholar 

  220. Yanagisawa H, Schluterman MK, Brekken RA (2009) Fibulin-5, an integrin-binding matricellular protein: its function in development and disease. J Cell Commun Signal 3(3–4):337–347

    Article  PubMed  PubMed Central  Google Scholar 

  221. Walther M, Kuklinski S, Pesheva P, Guntinas-Lichius O, Angelov DN, Neiss WF, Asou H, Probstmeier R (2000) Galectin-3 is upregulated in microglial cells in response to ischemic brain lesions, but not to facial nerve axotomy. J Neurosci Res 61(4):430–435

    Article  CAS  PubMed  Google Scholar 

  222. Hu L, Dong MX, Zhao H, Xu GH, Qin XY (2016) Fibulin-5: a novel biomarker for evaluating severity and predicting prognosis in patients with acute intracerebral haemorrhage. Eur J Neurol 23(7):1195–1201

    Article  CAS  PubMed  Google Scholar 

  223. Sirko S, Irmler M, Gascón S, Bek S, Schneider S, Dimou L, Obermann J, De Souza Paiva D, Poirier F, Beckers J, Hauck SM, Barde YA, Götz M (2015) Astrocyte reactivity after brain injury-: the role of galectins 1 and 3. Glia 63(12):2340–2361

    Article  PubMed  PubMed Central  Google Scholar 

  224. Qu WS, Wang YH, Ma JF, Tian DS, Zhang Q, Pan DJ, Yu ZY, Xie MJ, Wang JP, Wang W (2011) Galectin-1 attenuates astrogliosis-associated injuries and improves recovery of rats following focal cerebral ischemia. J Neurochem 116(2):217–226

    Article  CAS  PubMed  Google Scholar 

  225. Venkatesan C, Chrzaszcz M, Choi N, Wainwright MS (2010) Chronic upregulation of activated microglia immunoreactive for galectin-3/Mac-2 and nerve growth factor following diffuse axonal injury. J Neuroinflammation 7:32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  226. Endo T (2005) Glycans and glycan-binding proteins in brain: galectin-1-induced expression of neurotrophic factors in astrocytes. Curr Drug Targets 6(4):427–436

    Article  CAS  PubMed  Google Scholar 

  227. Imbe H, Okamoto K, Kadoya T, Horie H, Senba E (2003) Galectin-1 is involved in the potentiation of neuropathic pain in the dorsal horn. Brain Res 993(1–2):72–83

    Article  CAS  PubMed  Google Scholar 

  228. McGraw J, Oschipok LW, Liu J, Hiebert GW, Mak CF, Horie H, Kadoya T, Steeves JD, Ramer MS, Tetzlaff W (2004) Galectin-1 expression correlates with the regenerative potential of rubrospinal and spinal motoneurons. Neuroscience 128(4):713–719

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a Merit Review from the US Department of Veterans Affairs and by a National Institutes of Health grant (DK063311).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. D. Norenberg.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jayakumar, A.R., Apeksha, A. & Norenberg, M.D. Role of Matricellular Proteins in Disorders of the Central Nervous System. Neurochem Res 42, 858–875 (2017). https://doi.org/10.1007/s11064-016-2088-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-016-2088-5

Keywords

Navigation