Enhanced trophic factor secretion by mesenchymal stem/stromal cells with Glycine-Histidine-Lysine (GHK)-modified alginate hydrogels

Acta Biomaterialia

Volumn 10, Issue 5, 2014, Pages 1955-1964

  Jose, Soumia ^a   Hughbanks, Marissa L ^a   Binder, Bernard Y K ^a   Ingavle, Ganesh C ^a   Leach, J Kent ^a,b  

^a University of California Davis   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alginate; Angiogenesis; GHK; Hydrogel; Vascular endothelial growth factor

Indexed keywords

ALGINATE; CELL CULTURE; CELL ENGINEERING; CELL PROLIFERATION; CYTOTOXICITY; ENDOTHELIAL CELLS; GELS; HYDROGELS; RECOMBINANT PROTEINS;

ALGINATE HYDROGELS; ANGIOGENESIS; CELL-BE; CELL/B.E; CELL/BE; CLINICAL INVESTIGATION; CYTOKINES; GHK; STROMAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

AMINO ACIDS;

ALGINIC ACID; ALPHA6 INTEGRIN; BETA1 INTEGRIN; CYANAMIDE; FIBROBLAST GROWTH FACTOR 2; GLYCYLHISTIDYLLYSINE; VASCULOTROPIN; CULTURE MEDIUM; GLUCURONIC ACID; HEXURONIC ACID; HYDROGEL; INTEGRIN; MITOGENIC AGENT; OLIGOPEPTIDE; VASCULOTROPIN A;

APOPTOSIS; ARTICLE; CELL ADHESION; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CYTOTOXICITY; DNA CONTENT; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HYDROGEL; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; MONOLAYER CULTURE; PRIORITY JOURNAL; PROTEIN SECRETION; PROTON NUCLEAR MAGNETIC RESONANCE; UPREGULATION; CELL DEATH; CELL MOTION; CELL SURVIVAL; CFU COUNTING; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECTS; METABOLISM; PHARMACOLOGY; SECRETION (PROCESS);

ALGINATES; CELL ADHESION; CELL DEATH; CELL MOVEMENT; CELL SURVIVAL; COLONY-FORMING UNITS ASSAY; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; GLUCURONIC ACID; HEXURONIC ACIDS; HUMANS; HYDROGELS; INTEGRINS; MESENCHYMAL STROMAL CELLS; MITOGENS; OLIGOPEPTIDES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84898059527     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.01.020     Document Type: Article

References (44)

1. M. Potente, H. Gerhardt, and P. Carmeliet Basic and therapeutic aspects of angiogenesis Cell 146 2011 873 887
2. N. Ferrara Role of vascular endothelial growth factor in regulation of physiological angiogenesis Am J Physiol Cell Physiol 280 2001 C1358 C1366
3. D. Ribatti, and S. Baiguera Phase II angiogenesis stimulators Expert Opin Investig Drugs 22 2013 1157 1166
4. S. Mitsos, K. Katsanos, E. Koletsis, G.C. Kagadis, N. Anastasiou, and A. Diamantopoulos et al. Therapeutic angiogenesis for myocardial ischemia revisited: basic biological concepts and focus on latest clinical trials Angiogenesis 15 2012 1 22
5. A.I. Caplan, and D. Correa The MSC: an injury drugstore Cell Stem Cell 9 2011 11 15
6. G.P. Duffy, T. Ahsan, T. O'Brien, F. Barry, and R.M. Nerem Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time- and dose-dependent manner in vitro Tissue Eng Part A 15 2009 2459 2470
7. J. He, M.L. Decaris, and J.K. Leach Bioceramic-mediated trophic factor secretion by mesenchymal stem cells enhances in vitro endothelial cell persistence and in vivo angiogenesis Tissue Eng Part A 18 2012 1520 1528
8. B.J. Capoccia, D.L. Robson, K.D. Levac, D.J. Maxwell, S.A. Hohm, and M.J. Neelamkavil et al. Revascularization of ischemic limbs after transplantation of human bone marrow cells with high aldehyde dehydrogenase activity Blood 113 2009 5340 5351
9. I. Rosova, M. Dao, B. Capoccia, D. Link, and J.A. Nolta Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells Stem Cells 26 2008 2007-1104
10. B.Y. Binder, C.S. Sondergaard, J.A. Nolta, and J.K. Leach Lysophosphatidic acid enhances stromal cell-directed angiogenesis PLoS One 8 2013 e82134
11. C.J. Kearney, and D.J. Mooney Macroscale delivery systems for molecular and cellular payloads Nat Mater 12 2013 1004 1017
12. E. Alsberg, H.J. Kong, Y. Hirano, M.K. Smith, A. Albeiruti, and D.J. Mooney Regulating bone formation via controlled scaffold degradation J Dent Res 82 2003 903 908
13. J.L. Drury, and D.J. Mooney Hydrogels for tissue engineering: scaffold design variables and applications Biomaterials 24 2003 4337 4351
14. E. Alsberg, K.W. Anderson, A. Albeiruti, J.A. Rowley, and D.J. Mooney Engineering growing tissues Proc Natl Acad Sci U S A 99 2002 12025 12030
15. J.A. Rowley, G. Madlambayan, and D.J. Mooney Alginate hydrogels as synthetic extracellular matrix materials Biomaterials 20 1999 45 53
16. A. Bhat, A.I. Hoch, M.L. Decaris, and J.K. Leach Alginate hydrogels containing cell-interactive beads for bone formation FASEB J 27 2013 4844 4852
17. M. Rafat, L.S. Rotenstein, J.L. Hu, and D.T. Auguste Engineered endothelial cell adhesion via VCAM1 and E-selectin antibody-presenting alginate hydrogels Acta Biomater 8 2012 2697 2703
18. O. Tsur-Gang, E. Ruvinov, N. Landa, R. Holbova, M.S. Feinberg, and J. Leor et al. The effects of peptide-based modification of alginate on left ventricular remodeling and function after myocardial infarction Biomaterials 30 2009 189 195
19. L. Pickart, J.H. Freedman, W.J. Loker, J. Peisach, C.M. Perkins, and R.E. Stenkamp et al. Growth-modulating plasma tripeptide may function by facilitating copper uptake into cells Nature 288 1980 715 717
20. L. Mazurowska, and M. Mojski Biological activities of selected peptides: skin penetration ability of copper complexes with peptides J Cosmet Sci 59 2008 59 69
21. L.B. Rivera, A.D. Bradshaw, and R.A. Brekken The regulatory function of SPARC in vascular biology Cell Mol Life Sci 68 2011 3165 3173
22. L. Pickart The human tri-peptide GHK and tissue remodeling J Biomater Sci 19 2008 969 988
23. I.M. Conboy, M.J. Conboy, A.J. Wagers, E.R. Girma, I.L. Weissman, and T.A. Rando Rejuvenation of aged progenitor cells by exposure to a young systemic environment Nature 433 2005 760 764
24. 2+ Life Sci 51 1992 1049 1056
25. P.J. Huang, Y.C. Huang, M.F. Su, T.Y. Yang, J.R. Huang, and C.P. Jiang In vitro observations on the influence of copper peptide aids for the LED photoirradiation of fibroblast collagen synthesis Photomed Laser Surg 25 2007 183 190
26. 2+ FEBS Lett 238 1988 343 346
27. J.D. Pollard, S. Quan, T. Kang, and R.J. Koch Effects of copper tripeptide on the growth and expression of growth factors by normal and irradiated fibroblasts Arch Facial Plast Surg 7 2005 27 31
28. N.L. Henry, R. Dunn, S. Merjaver, Q. Pan, K.J. Pienta, and G. Brewer et al. Phase II trial of copper depletion with tetrathiomolybdate as an antiangiogenesis strategy in patients with hormone-refractory prostate cancer Oncology 71 2006 168 175
29. S.A. Lowndes, H.V. Sheldon, S. Cai, J.M. Taylor, and A.L. Harris Copper chelator ATN-224 inhibits endothelial function by multiple mechanisms Microvas Res 77 2009 314 326
30. B.Y. Binder, D.C. Genetos, and J.K. Leach Lysophosphatidic acid protects human mesenchymal stromal cells from differentiation-dependent vulnerability to apoptosis Tissue Eng Part A 2013 [Epub ahead of print]
31. M.C. Yoder, L.E. Mead, D. Prater, T.R. Krier, K.N. Mroueh, and F. Li et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals Blood 109 2007 1801 1809
32. M.L. Decaris, C.I. Lee, M.C. Yoder, A.F. Tarantal, and J.K. Leach Influence of the oxygen microenvironment on the proangiogenic potential of human endothelial colony forming cells Angiogenesis 12 2009 303 311
33. A.I. Hoch, B.Y. Binder, D.C. Genetos, and J.K. Leach Differentiation- dependent secretion of proangiogenic factors by mesenchymal stem cells PLoS One 7 2012 e35579
34. F.A. Fierro, S. Kalomoiris, C.S. Sondergaard, and J.A. Nolta Effects on proliferation and differentiation of multipotent bone marrow stromal cells engineered to express growth factors for combined cell and gene therapy Stem Cells 29 2011 1727 1737
35. X. Hu, S.P. Yu, J.L. Fraser, Z. Lu, M.E. Ogle, and J.-A. Wang et al. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis J Thorac Cardiovasc Surg 135 2008 799 808
36. H. Pohunkova, J. Stehlik, J. Vachal, O. Cech, and M. Adam Morphological features of bone healing under the effect of collagen-graft-glycosaminoglycan copolymer supplemented with the tripeptide Gly-His-Lys Biomaterials 17 1996 1567 1574
37. H. Pohunkova, and M. Adam Reactivity and the fate of some composite bioimplants based on collagen in connective tissue Biomaterials 16 1995 67 71
38. M.A. Buerkle, S.A. Pahernik, A. Sutter, A. Jonczyk, K. Messmer, and M. Dellian Inhibition of the alpha-nu integrins with a cyclic RGD peptide impairs angiogenesis, growth and metastasis of solid tumours in vivo Br J Cancer 86 2002 788 795
39. J.R. Sheu, M.H. Yen, Y.C. Kan, W.C. Hung, P.T. Chang, and H.N. Luk Inhibition of angiogenesis in vitro and in vivo: comparison of the relative activities of triflavin, an Arg-Gly-Asp-containing peptide and anti-alpha(v)beta3 integrin monoclonal antibody Biochim Biophys Acta 1336 1997 445 454
40. A. Trabocchi, G. Menchi, N. Cini, F. Bianchini, S. Raspanti, and A. Bottoncetti et al. Click-chemistry-derived triazole ligands of arginine-glycine-aspartate (RGD) integrins with a broad capacity to inhibit adhesion of melanoma cells and both in vitro and in vivo angiogenesis J Med Chem 53 2010 7119 7128
41. C. Kim, F. Ye, and M.H. Ginsberg Regulation of integrin activation Annu Rev Cell Dev Biol 27 2011 321 345
42. S.E. Funk, and E.H. Sage Differential effects of SPARC and cationic SPARC peptides on DNA synthesis by endothelial cells and fibroblasts J Cell Physiol 154 1993 53 63
43. T.F. Lane, M.L. Iruela-Arispe, R.S. John, and E.H. Sage SPARC is a source of copper-binding peptides that stimulate angiogenesis J Cell Biol 125 1994 929 943
44. L. Leroux, B. Descamps, N.F. Tojais, B. Seguy, P. Oses, and C. Moreau et al. Hypoxia preconditioned mesenchymal stem cells improve vascular and skeletal muscle fiber regeneration after ischemia through a Wnt4-dependent pathway Mol Ther 18 2010 1545 1552