Skip to main content

Advertisement

SpringerLink
Log in

Proteins of the corneal stroma: importance in visual function

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The human cornea, consisting of five layers, is the transparent tissue that refracts and transmits light to the lens and retina, providing about two thirds of the refractive power of the eye. The stroma layer comprises nearly 90 % of the thickness of the cornea and thus plays a pivotal role in normal visual function. The bulk of this layer is constituted by proteins in the extracellular martrix secreted by the corneal epithelial, stroma, and endothelial cells. Clinical research has shown that corneal stroma diseases are common and involve conditions such as infections, injuries, and genetic defects, which cause severe visual disturbances or even blindness. To improve our understanding of the basic molecular mechanisms involved in the physiological and pathological activities of the corneal stroma, its proteins have been brought into the limelight to determine their crucial and irreplaceable roles. The data presented in a previous study have demonstrated the presence of 1679 proteins in the stroma, and this data set has subsequently been perfected by utilizing a highly sensitive isobaric peptide-labeling approach. According to their manifestations, these proteins can be classified as a gel-like organic material composed of proteoglycans, enzymes, and hemocyanin-binding proteins and a network of filaments composed of collagen, elastin, keratin, vimentin, and interconnected filaments comprising fibronectin and laminin. The aim of this review is to describe some corneal stroma proteins by highlighting their major functions and valuable applications in ophthalmologic research toward the better characterization and treatment of eye diseases.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ali S, Saik JE, Gould DJ, Dickinson ME, West JL (2013) Immobilization of cell-adhesive laminin peptides in degradable PEGDA hydrogels influences endothelial cell tubulogenesis. Biores Open Access 2:241–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amjadi S, Mai K, McCluskey P, Wakefield D (2013) The role of lumican in ocular disease. ISRN Ophthalmol 2013:632302

    Article  PubMed  PubMed Central  Google Scholar 

  • Becerra SP, Dass CR, Yabe T, Crawford SE (2012) Pigment epithelium-derived factor: chemistry, structure, biology, and applications. J Biomed Biotechnol 2012:830975

    Article  PubMed  PubMed Central  Google Scholar 

  • Beecher N, Carlson C, Allen BR, Kipchumba R, Conrad GW, Meek KM, Quantock AJ (2005) An X-ray diffraction study of corneal structure in mimecan-deficient mice. Invest Ophthalmol Vis Sci 46:4046–4049

    Article  PubMed  Google Scholar 

  • Boot-Handford RP, Tuckwell DS (2003) Fibrillar collagen: the key to vertebrate evolution? A rate of molecular incest. Bioessays 25:142–151

    Article  CAS  PubMed  Google Scholar 

  • Borrelli M, Joepen N, Reichl S, Finis D, Schoppe M, Geerling G, Schrader S (2015) Keratin films for ocular surface reconstruction: evaluation of biocompatibility in an in-vivo model. Biomaterials 42:112–120

    Article  CAS  PubMed  Google Scholar 

  • Bouhenni R, Hart M, Al-Jastaneiah S, AlKatan H, Edward DP (2013) Immunohistochemical expression and distribution of proteoglycans and collagens in sclerocornea. Int Ophthalmol 33:691–700

    Article  PubMed  Google Scholar 

  • Boulze Pankert M, Goyer B, Zaguia F, Bareille M, Perron MC, Liu X, Cameron JD, Proulx S, Brunette I (2014) Biocompatibility and functionality of a tissue-engineered living corneal stroma transplanted in the feline eye. Invest Ophthalmol Vis Sci 55:6908–6920

    Article  PubMed  Google Scholar 

  • Bredrup C, Stang E, Bruland O, Palka BP, Young RD, Haavik J, Knappskog PM, Rødahl E (2010) Decorin accumulation contributes to the stromal opacities found in congenital stromal corneal dystrophy. Invest Ophthalmol Vis Sci 51:5578–5582

    Article  PubMed  Google Scholar 

  • Broadhead ML, Choong PF, Dass CR (2012) Efficacy of continuously administered PEDF-derived synthetic peptides against osteosarcoma growth and metastasis. J Biomed Biotechnol 2012:230298

    Article  PubMed  PubMed Central  Google Scholar 

  • Byström B, Carracedo S, Behndig A, Gullberg D, Pedrosa-Domellöf F (2009) Alpha11 integrin in the human cornea: importance in development and disease. Invest Ophthalmol Vis Sci 50:5044–5053

    Article  PubMed  Google Scholar 

  • Carlson EC, Sun Y, Auletta J, Kao WW, Liu CY, Perez VL, Pearlman E (2010) Regulation of corneal inflammation by neutrophil-dependent cleavage of keratan sulfate proteoglycans as a model for breakdown of the chemokine gradient. J Leukoc Biol 88:517–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaerkady R, Shao H, Scott SG, Pandey A, Jun AS, Chakravarti S (2013) The keratoconus corneal proteome: loss of epithelial integrity and stromal degeneration. J Proteome 87:122–131

    Article  CAS  Google Scholar 

  • Chaurasia SS, Kaur H, Medeiros FW de, Smith SD, Wilson SE (2009) Reprint of “Dynamics of the expression of intermediate filaments vimentin and desmin during myofibroblast differentiation after corneal injury”. Exp Eye Res 89:590–596

  • Chen S, Sun M, Meng X, Iozzo RV, Kao WW, Birk DE (2011) Pathophysiological mechanisms of autosomal dominant congenital stromal corneal dystrophy: C-terminal-truncated decorin results in abnormal matrix assembly and altered expression of small leucine-rich proteoglycans. Am J Pathol 179:2409–2419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Sun M, Iozzo RV, Kao WW, Birk DE (2013) Intracellularly-retained decorin lacking the C-terminal ear repeat causes ER stress: a cell-based etiological mechanism for congenital stromal corneal dystrophy. Am J Pathol 183:247–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Young MF, Chakravarti S, Birk DE (2014) Interclass small leucine-rich repeat proteoglycan interactions regulate collagen fibrillogenesis and corneal stromal assembly. Matrix Biol 35:103–111

    Article  PubMed  PubMed Central  Google Scholar 

  • Choi JS, Kim EY, Kim MJ, Giegengack M, Khan FA, Khang G, Soker S (2013) In vitro evaluation of the interactions between human corneal endothelial cells and extracellular matrix proteins. Biomed Mater 8:014108

    Article  PubMed  Google Scholar 

  • Conrad AH, Zhang Y, Tasheva ES, Conrad GW (2010) Proteomic analysis of potential keratan sulfate, chondroitin sulfate A, and hyaluronic acid molecular interactions. Invest Ophthalmol Vis Sci 51:4500–4515

    Article  PubMed  PubMed Central  Google Scholar 

  • Corpuz LM, Funderburgh JL, Funderburgh ML, Bottomley GS, Prakash S, Conrad GW (1996) Molecular cloning and tissue distribution of keratocan. Bovine corneal keratan sulfate proteoglycan 37A. J Biol Chem 271:9759–9763

    Article  CAS  PubMed  Google Scholar 

  • Cortina MS, He J, Li N, Bazan NG, Bazan HE (2012) Recovery of corneal sensitivity, calcitonin gene-related peptide-positive nerves, and increased wound healing induced by pigment epithelial-derived factor plus docosahexaenoic acid after experimental surgery. Arch Ophthalmol 130:76–83

    Article  CAS  PubMed  Google Scholar 

  • Courtney DG, Atkinson SD, Allen EH, Moore JE, Walsh CP, Pedrioli DM, MacEwen CJ, Pellegrini G, Maurizi E, Serafini C, Fantacci M, Liao H, Irvine AD, McLean WH, Moore CB (2014) siRNA silencing of the mutant keratin 12 allele in corneal limbal epithelial cells grown from patients with Meesmann's epithelial corneal dystrophy. Invest Ophthalmol Vis Sci 55:3352–3360

    Article  CAS  PubMed  Google Scholar 

  • Das SK, Gupta I, Cho YK, Zhang X, Uehara H, Muddana SK, Bernhisel AA, Archer B, Ambati BK (2014) Vimentin knockdown decreases corneal opacity. Invest Ophthalmol Vis Sci 55:4030–4040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dassati S, Waldner A, Schweigreiter R (2014) Apolipoprotein D takes center stage in the stress response of the aging and degenerative brain. Neurobiol Aging 35:1632–1642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Iorio E, Barbaro V, Volpi N, Bertolin M, Ferrari B, Fasolo A, Arnaldi R, Brusini P, Prosdocimo G, Ponzin D, Ferrari S (2010) Localization and expression of CHST6 and keratan sulfate proteoglycans in the human cornea. Exp Eye Res 91:293–299

  • Du L, Wu X (2011) Development and characterization of a full-thickness acellular porcine cornea matrix for tissue engineering. Artif Organs 35:691–705

    Article  CAS  PubMed  Google Scholar 

  • Du Y, Carlson EC, Funderburgh ML, Birk DE, Pearlman E, Guo N, Kao WW, Funderburgh JL (2009) Stem cell therapy restores transparency to defective murine corneas. Stem Cells 27:1635–1642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dyrlund TF, Poulsen ET, Scavenius C, Nikolajsen CL, Thøgersen IB, Vorum H, Enghild JJ (2012) Human cornea proteome: identification and quantitation of the proteins of the three main layers including epithelium, stroma, and endothelium. J Proteome Res 11:4231–4239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Exposito JY, Cluzel C, Garrone R, Lethias C (2002) Evolution of collagens. Anat Rec 268:302–316

    Article  CAS  PubMed  Google Scholar 

  • Fuchsluger T, Salehi S, Petsch C, Bachmann B (2014) New possibilities for ocular surface reconstruction : collagen membranes and biocompatible elastomer nanofibers. Ophthalmologe 111:1019–1026

    Article  CAS  PubMed  Google Scholar 

  • Funderburgh JL, Corpuz LM, Roth MR, Funderburgh ML, Tasheva ES, Conrad GW (1997) Mimecan, the 25-kDa corneal keratan sulfate proteoglycan, is a product of the gene producing osteoglycin. J Biol Chem 272:28089–28095

    Article  CAS  PubMed  Google Scholar 

  • Funderburgh ML, Mann MM, Funderburgh JL (2008) Keratocyte phenotype is enhanced in the absence of attachment to the substratum. Mol Vis 14:308–317

    CAS  PubMed  PubMed Central  Google Scholar 

  • Georgakopoulos CD, Exarchou AM, Gartaganis SP, Kolonitsiou F, Anastassiou ED, Dimitracopoulos G, Hjerpe A, Theocharis AD, Karamanos NK (2006) Immunization with specific polysaccharide antigen reduces alterations in corneal proteoglycans during experimental slime-producing Staphylococcus epidermidis keratitis. Curr Eye Res 31:137–146

  • Gil ES, Mandal BB, Park SH, Marchant JK, Omenetto FG, Kaplan DL (2010) Helicoidal multi-lamellar features of RGD-functionalized silk biomaterials for corneal tissue engineering. Biomaterials 31:8953–8963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon SR (2014) Fibronectin antibody labels corneal stromal collagen fibrils in situ along their length and circumference and demonstrates distinct staining along the cell and stromal interfaces of Descemet's membrane. Curr Eye Res 39:312–316

    Article  CAS  PubMed  Google Scholar 

  • Hanlon SD, Behzad AR, Sakai LY, Burns AR (2015) Corneal stroma microfibrils. Exp Eye Res 132C:198–207

    Article  Google Scholar 

  • Hassell JR, Birk DE (2010) The molecular basis of corneal transparency. Exp Eye Res 91:326–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi Y, Call MK, Chikama T, Liu H, Carlson EC, Sun Y, Pearlman E, Funderburgh JL, Babcock G, Liu CY, Ohashi Y, Kao WW (2010) Lumican is required for neutrophil extravasation following corneal injury and wound healing. J Cell Sci 123:2987–2995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemmavanh C, Koch M, Birk DE, Espana EM (2013) Abnormal corneal endothelial maturation in collagen XII and XIV null mice. Invest Ophthalmol Vis Sci 54:3297–3308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Järveläinen H, Sainio A, Wight TN (2015) Pivotal role for decorin in angiogenesis. Matrix Biol 43:15–26

    Article  PubMed  PubMed Central  Google Scholar 

  • Jing Y, Kumar PR, Zhu L, Edward DP, Tao S, Wang L, Chuck R, Zhang C (2014) Novel decorin mutation in a Chinese family with congenital stromal corneal dystrophy. Cornea 33:288–293

    Article  PubMed  Google Scholar 

  • Kaarniranta K, Szalai E, Smedowski A, Hegyi Z, Kivinen N, Viiri J, Wowra B, Dobrowolski D, Módis L Jr, Berta A, Wylegala E, Felszeghy S (2015) A novel proteotoxic stress associated mechanism for macular corneal dystrophy. Histol Histopathol 30:921–930

    CAS  PubMed  Google Scholar 

  • Knupp C, Pinali C, Lewis PN, Parfitt GJ, Young RD, Meek KM, Quantock AJ (2009) The architecture of the cornea and structural basis of its transparency. Adv Protein Chem Struct Biol 78:25–49

    Article  CAS  PubMed  Google Scholar 

  • Kuo CN, Yang LC, Yang CT, Lai CH, Chen MF, Chen CY, Chen CH, Wu PC, Kou HK, Chen YJ, Hung CH, Tsai CB (2009) Inhibition of corneal neovascularization with plasmid pigment epithelium-derived factor (p-PEDF) delivered by synthetic amphiphile INTeraction-18 (SAINT-18) vector in an experimental model of rat corneal angiogenesis. Exp Eye Res 89:678–685

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Ki CS, Chung ES, Chung TY (2012) A novel decorin gene mutation in congenital hereditary stromal dystrophy: a Korean family. Korean J Ophthalmol 26:301–305

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ho D, Meng H, Chan TR, An B, Yu H, Brodsky B, Jun AS, Michael Yu S (2013) Direct detection of collagenous proteins by fluorescently labeled collagen mimetic peptides. Bioconjug Chem 24:9–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu CY, Birk DE, Hassell JR, Kane B, Kao WW (2003) Keratocan-deficient mice display alterations in corneal structure. J Biol Chem 278:21672–21677

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Zhang J, Liu CY, Wang IJ, Sieber M, Chang J, Jester JV, Kao WW (2010) Cell therapy of congenital corneal diseases with umbilical mesenchymal stem cells: lumican null mice. PLoS One 5:e10707

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu XY, Chen J, Zhou Q, Wu J, Zhang XL, Wang L, Qin XY (2013) In vitro tissue engineering of lamellar cornea using human amniotic epithelial cells and rabbit cornea stroma. Int J Ophthalmol 6:425–429

    PubMed  PubMed Central  Google Scholar 

  • Livny E, Livnat T, Yakimov M, Masoud M, Weinberger D, Bahar I (2013) Effect of erythropoietin on healing of corneal epithelial defects in rabbits. Ophthalmic Res 50:129–133

    CAS  PubMed  Google Scholar 

  • Ljubimov AV, Saghizadeh M (2015) Progress in corneal wound healing. Prog Retin Eye Res 49:17–45

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Zimek A, Chen J, Hesse M, Büssow H, Weber K, Magin TM (2006) Keratin 5 knockout mice reveal plasticity of keratin expression in the corneal epithelium. Eur J Cell Biol 85:803–811

    Article  CAS  PubMed  Google Scholar 

  • Mankus C, Chi C, Rich C, Ren R, Trinkaus-Randall V (2012) The P2X(7) receptor regulates proteoglycan expression in the corneal stroma. Mol Vis 18:128–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meek KM, Quantock AJ, Boote C, Liu CY, Kao WW (2003) An X-ray scattering investigation of corneal structure in keratocan-deficient mice. Matrix Biol 22:467–475

    Article  CAS  PubMed  Google Scholar 

  • Mellgren AE, Bruland O, Vedeler A, Saraste J, Schönheit J, Bredrup C, Knappskog PM, Rødahl E (2015) Development of congenital stromal corneal dystrophy is dependent on export and extracellular deposition of truncated decorin. Invest Ophthalmol Vis Sci 56:2909–2915

    Article  CAS  PubMed  Google Scholar 

  • Mi S, Connon CJ (2013) The formation of a tissue-engineered cornea using plastically compressed collagen scaffolds and limbal stem cells. Methods Mol Biol 1014:143–155

    Article  CAS  PubMed  Google Scholar 

  • Mohan RR, Gupta R, Mehan MK, Cowden JW, Sinha S (2010) Decorin transfection suppresses profibrogenic genes and myofibroblast formation in human corneal fibroblasts. Exp Eye Res 91:238–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohan RR, Tovey JC, Gupta R, Sharma A, Tandon A (2011a) Decorin biology, expression, function and therapy in the cornea. Curr Mol Med 11:110–128

    Article  CAS  PubMed  Google Scholar 

  • Mohan RR, Tandon A, Sharma A, Cowden JW, Tovey JC (2011b) Significant inhibition of corneal scarring in vivo with tissue-selective, targeted AAV5 decorin gene therapy. Invest Ophthalmol Vis Sci 52:4833–4841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohan RR, Tovey JC, Sharma A, Schultz GS, Cowden JW, Tandon A (2011c) Targeted decorin gene therapy delivered with adeno-associated virus effectively retards corneal neovascularization in vivo. PLoS One 6:e26432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moncayo-Arlandi J, López-García A, Fernández MC, Durán AC, Fernández B (2014) Osteoglycin deficiency does not affect atherosclerosis in mice. Atherosclerosis 237:418–425

    Article  CAS  PubMed  Google Scholar 

  • Morishige N, Shin-Gyou-Uchi R, Azumi H, Ohta H, Morita Y, Yamada N, Kimura K, Takahara A, Sonoda KH (2014) Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy. Invest Ophthalmol Vis Sci 55:8377–8385

    Article  PubMed  Google Scholar 

  • Musselmann K, Kane B, Alexandrou B, Hassell JR (2006) Stimulation of collagen synthesis by insulin and proteoglycan accumulation by ascorbate in bovine keratocytes in vitro. Invest Ophthalmol Vis Sci 47:5260–5266

    Article  PubMed  Google Scholar 

  • Musselmann K, Kane BP, Alexandrou B, Hassell JR (2008) IGF-II is present in bovine corneal stroma and activates keratocytes to proliferate in vitro. Exp Eye Res 86:506–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nees DW, Fariss RN, Piatigorsky J (2003) Serum albumin in mammalian cornea: implications for clinical application. Invest Ophthalmol Vis Sci 44:3339–3345

    Article  PubMed  Google Scholar 

  • Nishida T, Inui M, Nomizu M (2015) Peptide therapies for ocular surface disturbances based onfibronectin-integrin interactions. Prog Retin Eye Res 47:38–63

    Article  CAS  PubMed  Google Scholar 

  • Petsche SJ, Pinsky PM (2013) The role of 3-D collagen organization in stromal elasticity: a model based on X-ray diffraction data and second harmonic-generated images. Biomech Model Mechanobiol 12:1101–1113

    Article  PubMed  Google Scholar 

  • Ren R, Hutcheon AE, Guo XQ, Saeidi N, Melotti SA, Ruberti JW, Zieske JD, Trinkaus-Randall V (2008) Human primary corneal fibroblasts synthesize and deposit proteoglycans in long-term 3-D cultures. Dev Dyn 237:2705–2715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rødahl E, Van Ginderdeuren R, Knappskog PM, Bredrup C, Boman H (2006) A second decorin frame shift mutation in a family with congenital stromal corneal dystrophy. Am J Ophthalmol 142:520–521

    Article  PubMed  Google Scholar 

  • Saika S, Yamanaka O, Okada Y, Sumioka T (2016) Modulation of Smad signaling by non-TGFβ components in myofibroblast generation during wound healing in corneal stroma. Exp Eye Res 142:40–48

    Article  CAS  PubMed  Google Scholar 

  • Schönherr E, Sunderkötter C, Schaefer L, Thanos S, Grässel S, Oldberg A, Iozzo RV, Young MF, Kresse H (2004) Decorin deficiency leads to impaired angiogenesis in injured mouse cornea. J Vasc Res 41:499–508

    Article  PubMed  Google Scholar 

  • Sciandra F, Morlacchi S, Allamand V, De Benedetti G, Macchia G, Petrucci TC, Bozzi M, Brancaccio A (2008) First molecular characterization and immunolocalization of keratoepithelin in adult human skeletal muscle. Matrix Biol 27:360–370

    Article  CAS  PubMed  Google Scholar 

  • Shao H, Chaerkady R, Chen S, Pinto SM, Sharma R, Delanghe B, Birk DE, Pandey A, Chakravarti S (2011) Proteome profiling of wild type and lumican-deficient mouse corneas. J Proteome 74:1895–1905

    Article  CAS  Google Scholar 

  • Subramanian P, Notario PM, Becerra SP (2010) Pigment epithelium-derived factor receptor (PEDF-R): a plasma membrane-linked phospholipase with PEDF binding affinity. Adv Exp Med Biol 664:29–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subramanian P, Deshpande M, Locatelli-Hoops S, Moghaddam-Taaheri S, Gutierrez D, Fitzgerald DP, Guerrier S, Rapp M, Notario V, Becerra SP (2012) Identification of pigment epithelium-derived factor protein forms with distinct activities on tumor cell lines. J Biomed Biotechnol 2012:425907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanihara H, Inatani M, Koga T, Yano T, Kimura A (2002) Proteoglycans in the eye. Cornea 21:S62–S69

    Article  PubMed  Google Scholar 

  • Torricelli AA, Santhanam A, Wu J, Singh V, Wilson SE (2016) The corneal fibrosis response to epithelial-stromal injury. Exp Eye Res 142:110–118

    Article  CAS  PubMed  Google Scholar 

  • Uzunalli G, Soran Z, Erkal TS, Dagdas YS, Dinc E, Hondur AM, Bilgihan K, Aydin B, Guler MO, Tekinay AB (2014) Bioactive self-assembled peptide nanofibers for corneal stroma regeneration. Acta Biomater 10:1156–1166

    Article  CAS  PubMed  Google Scholar 

  • Vázquez N, Chacón M, Meana Á, Menéndez-Menéndez Y, Ferrero-Gutierrez A, Cereijo-Martín D, Naveiras M, Merayo-Lloves J (2015) Keratin-chitosan membranes as scaffold for tissue engineering of human cornea. Histol Histopathol 30:813–821

    PubMed  Google Scholar 

  • Wei X, Cai SP, Zhang X, Li X, Chen X, Liu X (2012) Is low dose of estrogen beneficial for prevention of glaucoma? Med Hypotheses 79:377–380

    Article  CAS  PubMed  Google Scholar 

  • Weyers A, Yang B, Solakyildirim K, Yee V, Li L, Zhang F, Linhardt RJ (2013) Isolation of bovine corneal keratan sulfate and its growth factor and morphogen binding. FEBS J 280:2285–2293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wojcik KA, Blasiak J, Szaflik J, Szaflik JP (2014) Role of biochemical factors in the pathogenesis of keratoconus. Acta Biochim Pol 61:55–62

    PubMed  Google Scholar 

  • Wu J, Du Y, Mann MM, Yang E, Funderburgh JL, Wagner WR (2013) Bioengineering organized, multilamellar human corneal stromal tissue by growth factor supplementation on highly aligned synthetic substrates. Tissue Eng Part A 19:2063–2075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamanaka O, Sumioka T, Saika S (2013) The role of extracellular matrix in corneal wound healing. Cornea 32(suppl):s43–s45 (retracted in Cornea 33:100)

    Article  PubMed  Google Scholar 

  • Yang CH, Culshaw GJ, Liu MM, Lu CC, French AT, Clements DN, Corcoran BM (2012) Canine tissue-specific expression of multiple small leucine rich proteoglycans. Vet J 193:374–380

    Article  CAS  PubMed  Google Scholar 

  • Yeh LK, Liu CY, Kao WW, Huang CJ, Hu FR, Chien CL, Wang IJ (2010) Knockdown of zebrafish lumican gene (zlum) causes scleral thinning and increased size of scleral coats. J Biol Chem 285:28141–28155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeo GC, Aghaei-Ghareh-Bolagh B, Brackenreg EP, Hiob MA, Lee P, Weiss AS (2015) Fabricated elastin. Adv Healthc Mater 4:2530–2556. doi:10.1002/adhm.201400781

    Article  CAS  PubMed  Google Scholar 

  • Yuan X, Hua X, Wilhelmus KR (2010) Expression of small leucine-rich proteoglycans during experimental fungal keratitis. Cornea 29:674–679

    PubMed  Google Scholar 

  • Zhang G, Chen S, Goldoni S, Calder BW, Simpson HC, Owens RT, McQuillan DJ, Young MF, Iozzo RV, Birk DE (2009) Genetic evidence for the coordinated regulation of collagen fibrillogenesis in the cornea by decorin and biglycan. J Biol Chem 284:8888–8897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Conrad AH, Conrad GW (2011) Effects of ultraviolet-A and riboflavin on the interaction of collagen and proteoglycans during corneal cross-linking. J Biol Chem 286:13011–13022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Mao X, Schwend T, Littlechild S, Conrad GW (2013) Resistance of corneal RFUVA–cross-linked collagens and small leucine-rich proteoglycans to degradation by matrix metalloproteinases. Invest Ophthalmol Vis Sci 54:1014–1025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Yang L, Qu M, Wang Y, Chen P, Wang Y, Shi W (2012) Role of senescent fibroblasts on alkali-induced corneal neovascularization. J Cell Physiol 227:1148–1156

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

    Authors and Affiliations

    1. Department of Ophthalmology, The 2nd Teaching Hospital of Jilin University, 218 Ziqiang Street, Nanguan District, Changchun, 130041, Jilin, China

      Meng Xuan, Shurong Wang, Xin Liu, Yuxi He, Ying Li & Yan Zhang

    Authors
    1. Meng Xuan
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Shurong Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Xin Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Yuxi He
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Ying Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Yan Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Yan Zhang.

    Ethics declarations

    Author contributions

    Meng Xuan and Shurong Wang gathered the materials and wrote the preliminary draft; Yan Zhang, Xin Liu, Yuxi He, and Ying Li critically reviewed and revised the manuscript; Yan Zhang provided overall supervision, direction, and leadership during the preparation of this manuscript.

    Conflict of interest

    The authors declare no conflicts of interest.

    Additional information

    Authors are grateful for funding support from Jilin University (2015791162), the Science and Technology Department of Jilin Province (20130413025GH), China.

    Meng Xuan and Shurong Wang contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Xuan, M., Wang, S., Liu, X. et al. Proteins of the corneal stroma: importance in visual function. Cell Tissue Res 364, 9–16 (2016). https://doi.org/10.1007/s00441-016-2372-3

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00441-016-2372-3

    Keywords

    Search

    Navigation