Skip to main content

Advertisement

SpringerLink
Log in

Bioactive borate glass triggers phenotypic changes in adipose stem cells

  • Tissue Engineering Constructs and Cell Substrates
  • Original Research
  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

A bioactive borate glass, 13-93B3 (B3), has been used successfully in the clinic to treat chronic, nonhealing wounds without scarring. However, the mechanism by which B3 stimulates wound healing is poorly understood. Because adipose stem cells (ASCs) have been shown to have multiple roles in wound repair, we hypothesized that B3 triggers ASCs. In this study, we evaluate the effects of B3 on ASC survival, migration, differentiation, and protein secretion in vitro. In concentrations ≤10 mg/ml, B3 did not affect ASC viability under static conditions. B3 promoted the migration of ASCs but did not increase differentiation into bone or fat. B3 also decreased ASCs secretion of collagen I, PAI-1, MCP-1, DR6, DKK-1, angiogenin, IL-1, IGFBP-6, VEGF, and TIMP-2; increased expression of IL-1R and E-selectin; had a transient decrease in IL-6 secretion; and had a transient increase in bFGF secretion. Together, these results show that B3 alters the protein secretion of ASCs.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ASC:

Adipose stem cells

B3:

Borate bioactive glass

CCM:

Complete culture medium

ECM:

Extracellular matrix

VEGF:

Vascular endothelial growth factor

bFGF:

Basic fibroblast growth factor

TIMP-2:

Tissue inhibitor of metalloproteinases

IGFBP:

Insulin-like growth factor-binding protein 6

IL-1:

Interleukin 1

IL-6:

Interleukin 6

PAI:

Plasminogen activator inhibitor

MCP:

Monocyte chemoattractant protein, also known as CCL2

DR6:

Death receptor 6

DKK-1:

Dickkopf-related protein 1

PBS:

Phosphate buffer saline

References

  1. Järbrink K, Ni G, Sönnergren H. Prevalence and incidence of chronic wounds and related complications: a protocol for a systematic review. Syst Rev. 2016;5. https://doi.org/10.1186/s13643-016-0329-y.

  2. Sen CK. Human wounds and its burden: an updated compendium of estimates. Adv Wound Care. 2019;8:39–48. https://doi.org/10.1089/wound.2019.0946.

    Article  Google Scholar 

  3. Wang P-H, Huang B-S, Horng H-C, et al. Wound healing. J Chinese Med Assoc. 2018;81:94–101. https://doi.org/10.1016/j.jcma.2017.11.002.

    Article  Google Scholar 

  4. Shah J, Mohd Y, Omar E, Pai DR, Sood S. Cellular events and biomarkers of wound healing. Indian J Plast Surg. 2012;45:220–8. https://doi.org/10.4103/0970-0358.101282.

    Article  Google Scholar 

  5. Mendonça RJ, de, Coutinho-Netto J. Cellular aspects of wound healing. Anais Brasileiros de Dermatol. 2009;84:257–62. https://doi.org/10.1590/S0365-05962009000300007.

    Article  Google Scholar 

  6. Lombardi F, Palumbo P, Augello FR, et al. Secretome of adipose tissue-derived stem cells (ASCs) as a novel trend in chronic non-healing wounds: an overview of experimental in vitro and in vivo studies and methodological variables. Int J Mol Sci. 2019;20:3721 https://doi.org/10.3390/ijms20153721.

    Article  CAS  Google Scholar 

  7. Cherubino M, Rubin JP, Miljkovic N, et al. Adipose-derived stem cells for wound healing applications. Ann Plast Surg. 2011;66:210–5. https://doi.org/10.1097/SAP.0b013e3181e6d06c.

    Article  CAS  Google Scholar 

  8. Fromm-Dornieden C, Koenen P. Adipose-derived stem cells in wound healing: recent results in vitro and in vivo. OA Mol Cell Biol. 2013;1:8.

    Article  Google Scholar 

  9. Chen S, Yang Q, Brow RK, et al. In vitro stimulation of vascular endothelial growth factor by borate-based glass fibers under dynamic flow conditions. Mater Sci Eng C Mater Biol Appl. 2017;73:447–55. https://doi.org/10.1016/j.msec.2016.12.099.

    Article  CAS  Google Scholar 

  10. Gadelkarim M, Abushouk AI, Ghanem E, et al. Adipose-derived stem cells: effectiveness and advances in delivery in diabetic wound healing. Biomed Pharmacother. 2018;107:625–33. https://doi.org/10.1016/j.biopha.2018.08.013.

    Article  CAS  Google Scholar 

  11. Li P, Guo X. A review: therapeutic potential of adipose-derived stem cells in cutaneous wound healing and regeneration. Stem Cell Res Ther. 2018;9. https://doi.org/10.1186/s13287-018-1044-5.

  12. Strong AL, Bowles AC, MacCrimmon CP, et al. Adipose stromal cells repair pressure ulcers in both young and elderly mice: potential role of adipogenesis in skin repair. Stem Cells Transl Med. 2015;4:632–42. https://doi.org/10.5966/sctm.2014-0235.

    Article  CAS  Google Scholar 

  13. Shingyochi Y, Orbay H, Mizuno H. Adipose-derived stem cells for wound repair and regeneration. Expert Opin Biol Ther. 2015;15:1285–92. https://doi.org/10.1517/14712598.2015.1053867.

    Article  CAS  Google Scholar 

  14. D’Andrea F, De Francesco F, Ferraro GA, et al. Large-scale production of human adipose tissue from stem cells: a new tool for regenerative medicine and tissue banking. Tissue Eng Part C. 2008;14:233–42. https://doi.org/10.1089/ten.tec.2008.0108.

    Article  CAS  Google Scholar 

  15. Casteilla L, Dani C. Adipose tissue-derived cells: from physiology to regenerative medicine. Diabetes Metab. 2006;32:393–401. https://doi.org/10.1016/s1262-3636(07)70297-5.

    Article  CAS  Google Scholar 

  16. van Dongen JA, Harmsen MC, van der Lei B, Stevens HP. Augmentation of dermal wound healing by adipose tissue-derived stromal cells (ASC). Bioengineering. 2018;5. https://doi.org/10.3390/bioengineering5040091.

  17. Miguez-Pacheco V, Hench LL, Boccaccini AR. Bioactive glasses beyond bone and teeth: emerging applications in contact with soft tissues. Acta Biomater. 2015;13:1–15. https://doi.org/10.1016/j.actbio.2014.11.004.

    Article  CAS  Google Scholar 

  18. Hench LL. The story of Bioglass®. J Mater Sci. 2006;17:967–78. https://doi.org/10.1007/s10856-006-0432-z.

    Article  CAS  Google Scholar 

  19. Kargozar S, Mozafari M, Hamzehlou S, Baino F. Using bioactive glasses in the management of burns. Front Bioeng Biotechnol. 2019;7:62. https://doi.org/10.3389/fbioe.2019.00062.

    Article  Google Scholar 

  20. Brauer DS. Bioactive glasses—structure and properties. Angew Chemie Int Ed. 2015;54:4160–81. https://doi.org/10.1002/anie.201405310.

    Article  CAS  Google Scholar 

  21. Naseri S, Lepry WC, Nazhat SN. Bioactive glasses in wound healing: hope or hype? J Mater Chem B. 2017;5:6167–74. https://doi.org/10.1039/C7TB01221G.

    Article  CAS  Google Scholar 

  22. Kargozar S, Baino F, Hamzehlou S, et al. Bioactive glasses: sprouting angiogenesis in tissue engineering. Trends Biotechnol. 2018;36:430–44. https://doi.org/10.1016/j.tibtech.2017.12.003.

    Article  CAS  Google Scholar 

  23. Lin Y, Brown RF, Jung SB, Day DE. Angiogenic effects of borate glass microfibers in a rodent model. J Biomed Mater Res A. 2014;102:4491–9. https://doi.org/10.1002/jbm.a.35120.

    Article  CAS  Google Scholar 

  24. Jung SB, Day DE. Revolution in wound care? Inexpensive, easy-to-use cotton candy-like glass fibers appear to speed healing in initial venous stasis wound trial. Am Ceram Soc Bull. 2011;90:25–9.

    Google Scholar 

  25. Jung SB. Borate based bioactive glass scaffolds for hard and soft tissue engineering. Rolla, MO, USA: PhD Dissertation, Missouri University of Science and Technology; 2010.

  26. Jung SB, Day DE. Wound Care Compositions. US patent 20170014542. 2017.

  27. Balasubramanian P, Büttner T, Miguez Pacheco V, Boccaccini AR. Boron-containing bioactive glasses in bone and soft tissue engineering. J Eur Ceram Soc. 2018;38:855–69. https://doi.org/10.1016/j.jeurceramsoc.2017.11.001.

    Article  CAS  Google Scholar 

  28. Zhao S, Li L, Wang H, et al. Wound dressings composed of copper-doped borate bioactive glass microfibers stimulate angiogenesis and heal full-thickness skin defects in a rodent model. Biomaterials. 2015;53:379–91. https://doi.org/10.1016/j.biomaterials.2015.02.112.

    Article  CAS  Google Scholar 

  29. Yang Q, Chen S, Shi H, et al. In vitro study of improved wound-healing effect of bioactive borate-based glass nano-/micro-fibers. Mater Sci Eng C Mater Biol Appl. 2015;55:105–17. https://doi.org/10.1016/j.msec.2015.05.049.

    Article  CAS  Google Scholar 

  30. Yao A, Wang D, Huang W, et al. In vitro bioactive characteristics of borate-based glasses with controllable degradation behavior. J Am Ceram Soc. 2007;90:303–6. https://doi.org/10.1111/j.1551-2916.2006.01358.x.

    Article  CAS  Google Scholar 

  31. Zhou J, Wang H, Zhao S, et al. In vivo and in vitro studies of borate based glass micro-fibers for dermal repairing. Mater Sci Eng C Mater Biol Appl. 2016;60:437–45. https://doi.org/10.1016/j.msec.2015.11.068.

    Article  CAS  Google Scholar 

  32. Bose S, Fielding G, Tarafder S, Bandyopadhyay A. Trace element doping in calcium phosphate ceramics to understand osteogenesis and angiogenesis. Trends Biotechnol. 2013;31: https://doi.org/10.1016/j.tibtech.2013.06.005.

  33. Saghiri MA, Asatourian A, Orangi J, et al. Functional role of inorganic trace elements in angiogenesis-Part II: Cr, Si, Zn, Cu, and S. Crit Rev Oncol Hematol. 2015;96:143–55. https://doi.org/10.1016/j.critrevonc.2015.05.011.

    Article  Google Scholar 

  34. Rath SN, Brandl A, Hiller D, et al. Bioactive copper-doped glass scaffolds can stimulate endothelial cells in co-culture in combination with mesenchymal stem cells. PLoS ONE. 2014;9:e113319. https://doi.org/10.1371/journal.pone.0113319.

    Article  CAS  Google Scholar 

  35. Gupta B, Papke JB, Mohammadkhah A, et al. Effects of chemically doped bioactive borate glass on neuron regrowth and regeneration. Ann Biomed Eng. 2016;44:3468–77. https://doi.org/10.1007/s10439-016-1689-0.

    Article  Google Scholar 

  36. Akdere ÖE, Shikhaliyeva İ, Gümüşderelioğlu M. Boron mediated 2D and 3D cultures of adipose derived mesenchymal stem cells. Cytotechnology. 2019;71:611–22. https://doi.org/10.1007/s10616-019-00310-9.

    Article  CAS  Google Scholar 

  37. Brown RF, Rahaman MN, Dwilewicz AB, et al. Effect of borate glass composition on its conversion to hydroxyapatite and on the proliferation of MC3T3-E1 cells. J Biomed Mater Res Part A. 2009;88A:392–400. https://doi.org/10.1002/jbm.a.31679.

    Article  CAS  Google Scholar 

  38. Modglin VC, Brown RF, Jung SB, Day DE. Cytotoxicity assessment of modified bioactive glasses with MLO-A5 osteogenic cells in vitro. J Mater Sci Mater Med. 2013;24:1191–9. https://doi.org/10.1007/s10856-013-4875-8.

    Article  CAS  Google Scholar 

  39. Ojansivu M, Mishra A, Vanhatupa S, et al. The effect of S53P4-based borosilicate glasses and glass dissolution products on the osteogenic commitment of human adipose stem cells. PLoS ONE. 2018;13:e0202740. https://doi.org/10.1371/journal.pone.0202740.

    Article  CAS  Google Scholar 

  40. Mahdavi FS, Salehi A, Seyedjafari E, et al. Bioactive glass ceramic nanoparticles-coated poly(l-lactic acid) scaffold improved osteogenic differentiation of adipose stem cells in equine. Tissue Cell. 2017;49:565–72. https://doi.org/10.1016/j.tice.2017.07.003.

    Article  CAS  Google Scholar 

  41. Saçak B, Certel F, Akdeniz ZD, et al. Repair of critical size defects using bioactive glass seeded with adipose-derived mesenchymal stem cells. J Biomed Mater Res Part B Appl Biomater. 2017;105:1002–8. https://doi.org/10.1002/jbm.b.33634.

    Article  CAS  Google Scholar 

  42. Larrañaga A, Alonso-Varona A, Palomares T, et al. Effect of bioactive glass particles on osteogenic differentiation of adipose-derived mesenchymal stem cells seeded on lactide and caprolactone based scaffolds. J Biomed Mater Res A. 2015;103:3815–24. https://doi.org/10.1002/jbm.a.35525.

    Article  CAS  Google Scholar 

  43. Haimi S, Suuriniemi N, Haaparanta A-M, et al. Growth and osteogenic differentiation of adipose stem cells on PLA/bioactive glass and PLA/beta-TCP scaffolds. Tissue Eng Part A. 2009;15:1473–80. https://doi.org/10.1089/ten.tea.2008.0241.

    Article  CAS  Google Scholar 

  44. Abdik EA, Abdik H, Taşlı PN, et al. Suppressive role of boron on adipogenic differentiation and fat deposition in human mesenchymal stem cells. Biol Trace Elem Res. 2019;188:384–92. https://doi.org/10.1007/s12011-018-1428-5.

    Article  CAS  Google Scholar 

  45. Lin Q, Fang D, Fang J, et al. Impaired wound healing with defective expression of chemokines and recruitment of myeloid cells in TLR3-deficient mice. J Immunol. 2011;186:3710–7. https://doi.org/10.4049/jimmunol.1003007.

    Article  CAS  Google Scholar 

  46. Cash JL, Martin P. Myeloid cells in cutaneous wound repair. Microbiol Spectr. 2016;4: https://doi.org/10.1128/microbiolspec.MCHD-0017-2015.

  47. Akita S, Akino K, Hirano A. Basic fibroblast growth factor in scarless wound healing. Adv Wound Care. 2013;2:44–49. https://doi.org/10.1089/wound.2011.0324.

    Article  Google Scholar 

  48. Barrientos S, Brem H, Stojadinovic O, Tomic-Canic M. Clinical application of growth factors and cytokines in wound healing. Wound Repair Regen. 2014;22:569–78. https://doi.org/10.1111/wrr.12205.

    Article  Google Scholar 

  49. Przybylski M. A review of the current research on the role of bFGF and VEGF in angiogenesis. J Wound Care. 2009;18:516–9. https://doi.org/10.12968/jowc.2009.18.12.45609.

    Article  CAS  Google Scholar 

  50. Zonari A, Martins TMM, Paula ACC, et al. Polyhydroxybutyrate-co-hydroxyvalerate structures loaded with adipose stem cells promote skin healing with reduced scarring. Acta Biomater. 2015;17:170–81. https://doi.org/10.1016/j.actbio.2015.01.043.

    Article  CAS  Google Scholar 

  51. Hebert TL, Wu X, Yu G, et al. Culture effects of epidermal growth factor (EGF) and basic fibroblast growth factor (bFGF) on cryopreserved human adipose-derived stromal/stem cell proliferation and adipogenesis. J Tissue Eng Regen Med. 2009;3:553–61. https://doi.org/10.1002/term.198.

    Article  CAS  Google Scholar 

  52. Lim CP, Phan TT, Lim IJ, Cao X. Cytokine profiling and Stat3 phosphorylation in epithelial-mesenchymal interactions between keloid keratinocytes and fibroblasts. J Invest Dermatol. 2009;129:851–61. https://doi.org/10.1038/jid.2008.337.

    Article  CAS  Google Scholar 

  53. Gong Z-H, Ji J-F, Yang J, et al. Association of plasminogen activator inhibitor-1 and vitamin D receptor expression with the risk of keloid disease in a Chinese population. Kaohsiung J Med Sci. 2017;33:24–29. https://doi.org/10.1016/j.kjms.2016.10.013.

    Article  Google Scholar 

  54. Patel S, Maheshwari A, Chandra A. Biomarkers for wound healing and their evaluation. J Wound Care. 2016;25:46–55. https://doi.org/10.12968/jowc.2016.25.1.46.

    Article  CAS  Google Scholar 

  55. Yukami T, Hasegawa M, Matsushita Y, et al. Endothelial selectins regulate skin wound healing in cooperation with L-selectin and ICAM-1. J Leukoc Biol. 2007;82:519–31. https://doi.org/10.1189/jlb.0307152.

    Article  CAS  Google Scholar 

  56. Liu ZJF, Tian R, An W, et al. Identification of E-selectin as a novel target for the regulation of postnatal neovascularization: implications for diabetic wound healing. Ann Surg. 2010;252:625–34. https://doi.org/10.1097/SLA.0b013e3181f5a079.

    Article  Google Scholar 

  57. Bach LA. Recent insights into the actions of IGFBP-6. J Cell Commun Signal. 2015;9:189–200. https://doi.org/10.1007/s12079-015-0288-4.

    Article  Google Scholar 

  58. Le AD, Zhang Q, Wu Y, et al. Elevated vascular endothelial growth factor in keloids: relevance to tissue fibrosis. Cells Tissues Organs. 2004;176:87–94. https://doi.org/10.1159/000075030.

    Article  CAS  Google Scholar 

  59. DiPietro LA. Angiogenesis and wound repair: when enough is enough. J Leukoc Biol. 2016;100:979–84. https://doi.org/10.1189/jlb.4MR0316-102R.

    Article  CAS  Google Scholar 

  60. Apdik H, Doğan A, Demirci S, Aydın S, Şahin F. Dose-dependent effect of boric acid on myogenic differentiation of human adipose-derived stem cells (hADSCs). Biol Trace Elem Res. 2015;165:123–30. https://doi.org/10.1007/s12011-015-0253-3.

    Article  CAS  Google Scholar 

  61. Li X, Wang X, Jiang X, et al. Boron nitride nanotube-enhanced osteogenic differentiation of mesenchymal stem cells. J Biomed Mater Res B Appl Biomater. 2016;104:323–9. https://doi.org/10.1002/jbm.b.33391.

    Article  CAS  Google Scholar 

  62. Shuai C, Gao C, Feng P, et al. Boron nitride nanotubes reinforce tricalcium phosphate scaffolds and promote the osteogenic differentiation of mesenchymal stem cells. J Biomed Nanotechnol. 2016;12:934–47.

    Article  CAS  Google Scholar 

  63. Abdik EA, Abdik H, Taşlı PN, Deniz AAH, Şahin F. Suppressive role of boron on adipogenic differentiation and fat deposition in human mesenchymal stem cells. Biol Trace Elem Res. 2019;188:384–92. https://doi.org/10.1007/s12011-018-1428-5.

    Article  CAS  Google Scholar 

  64. Demirci S, Doğan A, Şişli B, Sahin F. Boron increases the cell viability of mesenchymal stem cells after long-term cryopreservation. Cryobiology. 2014;68:139–46. https://doi.org/10.1016/j.cryobiol.2014.01.010.

    Article  CAS  Google Scholar 

  65. Natesan S, Wrice NL, Baer DG, Christy RJ. Debrided skin as a source of autologous stem cells for wound repair. Stem Cells. 2011;29:1219–30. https://doi.org/10.1002/stem.677.

    Article  CAS  Google Scholar 

  66. Gimble JM, Guilak F, Bunnell BA. Clinical and preclinical translation of cell-based therapies using adipose tissue-derived cells. Stem Cell Res Ther. 2010;1:19. https://doi.org/10.1186/scrt19.

    Article  Google Scholar 

  67. Schäffler A, Büchler C. Concise review: adipose tissue-derived stromal cells–basic and clinical implications for novel cell-based therapies. Stem Cells. 2007;25:818–27. https://doi.org/10.1634/stemcells.2006-0589.

    Article  CAS  Google Scholar 

  68. Lee RH, Hsu SC, Munoz J, et al. A subset of human rapidly self-renewing marrow stromal cells preferentially engraft in mice. Blood. 2006;107:2153–61. https://doi.org/10.1182/blood-2005-07-2701

    Article  CAS  Google Scholar 

  69. Ylöstalo J, Bazhanov N, Prockop DJ. Reversible commitment to differentiation by human multipotent stromal cells (MSCs) in single-cell derived colonies. Exp Hematol. 2008;36:1390–402. https://doi.org/10.1016/j.exphem.2008.05.003.

    Article  CAS  Google Scholar 

  70. Kilroy GE, Foster SJ, Wu X, et al. Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol. 2007;212:702–9. https://doi.org/10.1002/jcp.21068.

    Article  CAS  Google Scholar 

  71. Wulandari E, Jusman SWA, Moenadjat Y, et al. Expressions of collagen I and III in hypoxic keloid tissue. Kobe J Med Sci. 2016;62:E58–69.

    CAS  Google Scholar 

  72. da Silva IR, Tiveron LCR, da C, da Silva MV, et al. In situ cytokine expression and morphometric evaluation of total collagen and collagens type I and type III in keloid scars. Mediat Inflamm. 2017;2017:6573802. https://doi.org/10.1155/2017/6573802.

    Article  CAS  Google Scholar 

  73. Tejiram S, Zhang J, Travis TE, et al. Compression therapy affects collagen type balance in hypertrophic scar. J Surg Res. 2016;201:299–305. https://doi.org/10.1016/j.jss.2015.10.040.

    Article  Google Scholar 

  74. Xue M, Jackson CJ. Extracellular matrix reorganization during wound healing and its impact on abnormal scarring. Adv Wound Care. 2015;4:119–36. https://doi.org/10.1089/wound.2013.0485.

    Article  Google Scholar 

  75. Gauglitz GG, Korting HC, Pavicic T, et al. Hypertrophic scarring and keloids: pathomechanisms and current and emerging treatment strategies. Mol Med. 2011;17:113–25. https://doi.org/10.2119/molmed.2009.00153.

    Article  CAS  Google Scholar 

  76. Marieb EN, Smith LA Chapter 19: The cardiovascular system: blood vessels, human anatomy and physiology 11th ed. 2018. p. 706–65 London, England: Pearson.

  77. Dimmeler S. ATVB in focus: novel mediators and mechanisms in angiogenesis and vasculogenesis. Arterioscler Thromb Vasc Biol. 2005;25:2245. https://doi.org/10.1161/01.ATV.0000187471.06942.17.

    Article  CAS  Google Scholar 

  78. Heil M, Eitenmüller I, Schmitz-Rixen T, Schaper W. Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med. 2006;10:45–55. https://doi.org/10.1111/j.1582-4934.2006.tb00290.x.

    Article  CAS  Google Scholar 

  79. Buschmann I, Schaper W. Arteriogenesis versus angiogenesis: two mechanisms of vessel growth. News Physiol Sci. 1999;14:121–5. https://doi.org/10.1152/physiologyonline.1999.14.3.121.

    Article  Google Scholar 

  80. Sohni A, Verfaillie CM. Mesenchymal stem cells migration homing and tracking. Stem Cells Int. 2013;2013:130763. https://doi.org/10.1155/2013/130763.

    Article  CAS  Google Scholar 

  81. De Becker A, Riet IV. Homing and migration of mesenchymal stromal cells: how to improve the efficacy of cell therapy. World J Stem Cells. 2016;8:73–87. https://doi.org/10.4252/wjsc.v8.i3.73.

    Article  Google Scholar 

  82. Nitzsche F, Müller C, Lukomska B, et al. Concise review: MSC adhesion cascade-insights into homing and transendothelial migration. Stem Cells. 2017;35:1446–60. https://doi.org/10.1002/stem.2614.

    Article  Google Scholar 

  83. Lin W, Xu L, Zwingenberger S, et al. Mesenchymal stem cells homing to improve bone healing. J Orthop Translat. 2017;9:19–27. https://doi.org/10.1016/j.jot.2017.03.002.

    Article  Google Scholar 

  84. Naderi MH, Matin MM, Heirani‐Tabasi A, et al. Injectable hydrogel delivery plus preconditioning of mesenchymal stem cells: exploitation of SDF-1/CXCR4 axis toward enhancing the efficacy of stem cells’ homing. Cell Biol Int. 2016;40:730–41. https://doi.org/10.1002/cbin.10474.

    Article  CAS  Google Scholar 

  85. Frazier T, Lee S, Bowles A, et al. Gender and age-related cell compositional differences in C57BL/6 murine adipose tissue stromal vascular fraction. Adipocyte. 2018;7:183–9. https://doi.org/10.1080/21623945.2018.1460009.

    Article  CAS  Google Scholar 

  86. Zhang X, Bowles AC, Semon JA. Transplantation of autologous adipose stem cells lacks therapeutic efficacy in the experimental autoimmune encephalomyelitis model. PLoS ONE. 2014;9: https://doi.org/10.1371/journal.pone.0085007.

  87. Scruggs BA, Semon JA, Zhang X, et al. Age of the donor reduces the ability of human adipose-derived stem cells to alleviate symptoms in the experimental autoimmune encephalomyelitis mouse model. Stem Cells Transl Med. 2013;2:797–807. https://doi.org/10.5966/sctm.2013-0026.

    Article  CAS  Google Scholar 

  88. Strong AL, Strong TA, Rhodes LV, et al. Obesity associated alterations in the biology of adipose stem cells mediate enhanced tumorigenesis by estrogen dependent pathways. Breast Cancer Res. 2013;15:R102. https://doi.org/10.1186/bcr3569.

    Article  Google Scholar 

  89. Pandey AC, Semon JA, Kaushal D, et al. MicroRNA profiling reveals age-dependent differential expression of nuclear factor κB and mitogen-activated protein kinase in adipose and bone marrow-derived human mesenchymal stem cells. Stem Cell Res Ther. 2011;2:49. https://doi.org/10.1186/scrt90.

    Article  CAS  Google Scholar 

  90. Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res. 2009;29:313–26. https://doi.org/10.1089/jir.2008.0027.

    Article  CAS  Google Scholar 

  91. Fujikura D, Ikesue M, Endo T, et al. Death receptor 6 contributes to autoimmunity in lupus-prone mice. Nat Commun. 2017;8:13957. https://doi.org/10.1038/ncomms13957.

    Article  CAS  Google Scholar 

  92. Kasof GM, Lu JJ, Liu D, et al. Tumor necrosis factor-alpha induces the expression of DR6, a member of the TNF receptor family, through activation of NF-kappaB. Oncogene. 2001;20:7965–75. https://doi.org/10.1038/sj.onc.1204985.

    Article  CAS  Google Scholar 

  93. Rabieian R, Boshtam M, Zareei M, et al. Plasminogen activator inhibitor type-1 as a regulator of fibrosis. J Cell Biochem. 2018;119:17–27. https://doi.org/10.1002/jcb.26146.

    Article  CAS  Google Scholar 

  94. Brosius FC. New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy. Rev Endocr Metab Disord. 2008;9:245–54. https://doi.org/10.1007/s11154-008-9100-6.

    Article  CAS  Google Scholar 

  95. Choi SH, Kim H, Lee HG, et al. Dickkopf-1 induces angiogenesis via VEGF receptor 2 regulation independent of the Wnt signaling pathway. Oncotarget. 2017;8:58974–84. https://doi.org/10.18632/oncotarget.19769.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Missouri University of Science and Technology, Rolla, MO, USA

    Nathan J. Thyparambil, Lisa C. Gutgesell, Bradley A. Bromet, Lauren E. Flowers, Samantha Greaney & Julie A. Semon

  2. Department of Material Science and Engineering, Missouri University of Science and Technology, Rolla, MO, USA

    Delbert E. Day

  3. Center for Biomedical Science and Engineering, Missouri University of Science and Technology, Rolla, MO, USA

    Delbert E. Day & Julie A. Semon

Authors
  1. Nathan J. Thyparambil
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lisa C. Gutgesell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bradley A. Bromet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lauren E. Flowers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Samantha Greaney
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Delbert E. Day
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Julie A. Semon
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived and designed the experiments: DED, JAS; Data curation: Cell culture: LCG, NJT; Live/dead + analysis: BAB; CyQuant: BAB, LCG; Migration: LCG; Invasion: LCG; Differentiation: NJT; Alkaline Phosphatase: LCG; Immunocytochemistry: NJT; Bio-Rad: LCG; Formal analysis: NJT, LCG, BAB; Contributed reagents/materials/analysis tools: DED; Wrote - original draft: NJT, JAS; Writing - reviewing and editing: NJT, BAB, LCG, LEF, DED, JAS.

Corresponding author

Correspondence to Julie A. Semon.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thyparambil, N.J., Gutgesell, L.C., Bromet, B.A. et al. Bioactive borate glass triggers phenotypic changes in adipose stem cells. J Mater Sci: Mater Med 31, 35 (2020). https://doi.org/10.1007/s10856-020-06366-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-020-06366-w

Search

Navigation