Regulation of endothelial cell activation and angiogenesis by injectable peptide nanofibers

Acta Biomaterialia

Volumn 8, Issue 1, 2012, Pages 154-164

  Cho, Hongkwan ^a   Balaji, Swathi ^d   Sheikh, Abdul Q ^a   Hurley, Jennifer R ^a   Tian, Ye F ^b,c   Collier, Joel H ^b   Crombleholme, Timothy M ^d   Narmoneva, Daria A ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c Illinois Institute of Technology   (United States)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Low affinity interactions; Self assembling peptide nanofibers; Vascular tissue engineering

Indexed keywords

BIOCOMPATIBILITY; BIOMECHANICS; CELL ENGINEERING; CYTOLOGY; ENDOTHELIAL CELLS; HYBRID MATERIALS; MAMMALS; MORPHOLOGY; PEPTIDES; PHOSPHORYLATION; SCAFFOLDS (BIOLOGY); TISSUE;

AFFINITY INTERACTIONS; ANGIOGENESIS; CAPILLARY MORPHOGENESIS; IN-VITRO; INTEGRINS; LOW-AFFINITY INTERACTION; MICROVASCULAR ENDOTHELIAL CELLS; SELF-ASSEMBLING PEPTIDE NANOFIBER; SELF-ASSEMBLING PEPTIDES; VASCULAR TISSUE ENGINEERING;

NANOFIBERS;

BETA3 INTEGRIN; ECHISTATIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NANOFIBER; RAD16 II PEPTIDE NANOFIBER; UNCLASSIFIED DRUG; VASCULOTROPIN;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOCOMPATIBILITY; CELL ACTIVATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIUM CELL; FEMALE; HYDROGEL; MOLECULAR INTERACTION; MORPHOGENESIS; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; VASCULAR TISSUE; WOUND HEALING;

EID: 84855954013     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2011.08.029     Document Type: Article

References (83)

1. R. Langer, and J.P. Vacanti Tissue engineering Science 260 1993 920 926 (Pubitemid 23209960)
2. L.G. Griffith, and G. Naughton Tissue engineering - current challenges and expanding opportunities Science 295 2002 1009 1014
3. G.D. Nicodemus, and S.J. Bryant Cell encapsulation in biodegradable hydrogels for tissue engineering applications Tissue Eng Part B Rev 14 2008 149 165 (Pubitemid 351839212)
4. F. Wang, Z. Li, M. Khan, K. Tamama, P. Kuppusamy, and W.R. Wagner Injectable, rapid gelling and highly flexible hydrogel composites as growth factor and cell carriers Acta Biomater 6 2010 1978 1991
5. L. Almany, and D. Seliktar Biosynthetic hydrogel scaffolds made from fibrinogen and polyethylene glycol for 3D cell cultures Biomaterials 26 2005 2467 2477 (Pubitemid 39600699)
6. J.E. Saik, D.J. Gould, E.M. Watkins, M.E. Dickinson, and J.L. West Covalently immobilized platelet-derived growth factor-BB promotes angiogenesis in biomimetic poly(ethylene glycol) hydrogels Acta Biomater 7 2011 133 143
7. J.E. Leslie-Barbick, C. Shen, C. Chen, and J.L. West Micron-scale spatially patterned, covalently immobilized vascular endothelial growth factor on hydrogels accelerates endothelial tubulogenesis and increases cellular angiogenic responses Tissue Eng Part A 17 2011 221 229
8. J. Kisiday, M. Jin, B. Kurz, H. Hung, C. Semino, and S. Zhang Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair Proc Natl Acad Sci USA 99 2002 9996 10001 (Pubitemid 34831161)
9. M.E. Davis, J.P. Motion, D.A. Narmoneva, T. Takahashi, D. Hakuno, and R.D. Kamm Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells Circulation 111 2005 442 450 (Pubitemid 40204428)
10. D.A. Narmoneva, O. Oni, A.L. Sieminski, S. Zhang, J.P. Gertler, and R.D. Kamm Self-assembling short oligopeptides and the promotion of angiogenesis Biomaterials 26 2005 4837 4846 (Pubitemid 40343031)
11. J. Liu, H. Song, L. Zhang, H. Xu, and X. Zhao Self-assembly-peptide hydrogels as tissue-engineering scaffolds for three-dimensional culture of chondrocytes in vitro Macromol Biosci 10 2010 1164 1170
12. S.A. Maher, R.L. Mauck, L. Rackwitz, and R.S. Tuan A nanofibrous cell-seeded hydrogel promotes integration in a cartilage gap model J Tissue Eng Regen Med 4 2010 25 29
13. M.R. Caplan, E.M. Schwartzfarb, S. Zhang, R.D. Kamm, and D.A. Lauffenburger Effects of systematic variation of amino acid sequence on the mechanical properties of a self-assembling, oligopeptide biomaterial J Biomater Sci Polym Ed 13 2002 225 236 (Pubitemid 34692830)
14. S. Zhang Fabrication of novel biomaterials through molecular self-assembly Nat Biotechnol 21 2003 1171 1178 (Pubitemid 37186173)
15. S. Zhang, T.C. Holmes, C.M. DiPersio, R.O. Hynes, X. Su, and A. Rich Self-complementary oligopeptide matrices support mammalian cell attachment Biomaterials 16 1995 1385 1393
16. I.R. Degano, L. Quintana, M. Vilalta, D. Horna, N. Rubio, and S. Borros The effect of self-assembling peptide nanofiber scaffolds on mouse embryonic fibroblast implantation and proliferation Biomaterials 30 2009 1156 1165
17. F. Gelain, A. Horii, and S. Zhang Designer self-assembling peptide scaffolds for 3-D tissue cell cultures and regenerative medicine Macromol Biosci 7 2007 544 551 (Pubitemid 47264628)
18. P. Jing, J.P. Jung, and J.H. Collier Nanostructured materials constructed from polypeptides D. Shi, Nanoscience in biomedicine 2009 Springer New York
19. E. Genove, S. Schmitmeier, A. Sala, S. Borros, A. Bader, and L.G. Griffith Functionalized self-assembling peptide hydrogel enhance maintenance of hepatocyte activity in vitro J Cell Mol Med 13 2009 3387 3397
20. Y. Chau, Y. Luo, A.C. Cheung, Y. Nagai, S. Zhang, and J.B. Kobler Incorporation of a matrix metalloproteinase-sensitive substrate into self-assembling peptides - a model for biofunctional scaffolds Biomaterials 29 2008 1713 1719
21. E. Genove, C. Shen, S. Zhang, and C.E. Semino The effect of functionalized self-assembling peptide scaffolds on human aortic endothelial cell function Biomaterials 26 2005 3341 3351 (Pubitemid 39647267)
22. J.P. Jung, J.Z. Gasiorowski, and J.H. Collier Fibrillar peptide gels in biotechnology and biomedicine Biopolymers 94 2010 49 59
23. S. Balaji, A.Q. Sheikh, S.S. Vaikunth, J.K. Parvadia, F.Y. Lim, and T.M. Crombleholme Wound treatment with angiogenic provisional matrix enhances wound neovascularization and improves healing in db/db mice Wound Repair Regen 17 2009 A15
24. D.A. Narmoneva, R. Vukmirovic, M.E. Davis, R.D. Kamm, and R.T. Lee Endothelial cells promote cardiac myocyte survival and spatial reorganization: implications for cardiac regeneration Circulation 110 2004 962 968 (Pubitemid 39136214)
25. A.L. Sieminski, C.E. Semino, H. Gong, and R.D. Kamm Primary sequence of ionic self-assembling peptide gels affects endothelial cell adhesion and capillary morphogenesis J Biomed Mater Res A 87 2008 494 504
26. A.L. Sieminski, A.S. Was, G. Kim, H. Gong, and R.D. Kamm The stiffness of three-dimensional ionic self-assembling peptide gels affects the extent of capillary-like network formation Cell Biochem Biophys 49 2007 73 83 (Pubitemid 47574999)
27. Y.D. Lin, M.L. Yeh, Y.J. Yang, D.C. Tsai, T.Y. Chu, and Y.Y. Shih Intramyocardial peptide nanofiber injection improves postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs Circulation 122 2010 S132 S141
28. P.C. Hsieh, M.E. Davis, J. Gannon, C. MacGillivray, and R.T. Lee Controlled delivery of PDGF-BB for myocardial protection using injectable self-assembling peptide nanofibers J Clin Invest 116 2006 237 248 (Pubitemid 43121809)
29. S. Koutsopoulos, L.D. Unsworth, Y. Nagai, and S. Zhang Controlled release of functional proteins through designer self-assembling peptide nanofiber hydrogel scaffold Proc Natl Acad Sci USA 106 2009 4623 4628
30. N. Ferrara, and R.S. Kerbel Angiogenesis as a therapeutic target Nature 438 2005 967 974 (Pubitemid 43093963)
31. B.P. Eliceiri, and D.A. Cheresh Adhesion events in angiogenesis Curr Opin Cell Biol 13 2001 563 568 (Pubitemid 32817014)
32. R.O. Hynes, B.L. Bader, and K. Hodivala-Dilke Integrins in vascular development Braz J Med Biol Res 32 1999 501 510 (Pubitemid 129540411)
33. D.G. Stupack, and D.A. Cheresh Integrins and angiogenesis Curr Top Dev Biol 64 2004 207 238 (Pubitemid 39752398)
34. E.F. Plow, T.A. Haas, L. Zhang, J. Loftus, and J.W. Smith Ligand binding to integrins J Biol Chem 275 2000 21785 21788 (Pubitemid 30621742)
35. C.J. Avraamides, B. Garmy-Susini, and J.A. Varner Integrins in angiogenesis and lymphangiogenesis Nat Rev Cancer 8 2008 604 617
36. P.R. Somanath, A. Ciocea, and T.V. Byzova Integrin and growth factor receptor alliance in angiogenesis Cell Biochem Biophys 53 2009 53 64
37. G.H. Mahabeleshwar, W. Feng, K. Reddy, E.F. Plow, and T.V. Byzova Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis Circ Res 101 2007 570 580 (Pubitemid 351325874)
38. I. Cascone, L. Napione, F. Maniero, G. Serini, and F. Bussolino Stable interaction between alpha5beta1 integrin and Tie2 tyrosine kinase receptor regulates endothelial cell response to Ang-1 J Cell Biol 170 2005 993 1004 (Pubitemid 41306298)
39. S.J. Shattil, and M.H. Ginsberg Integrin signaling in vascular biology J Clin Invest 100 1997 S91 S95
40. S.D. Blystone, M.P. Williams, S.E. Slater, and E.J. Brown Requirement of integrin beta3 tyrosine 747 for beta3 tyrosine phosphorylation and regulation of alphavbeta3 avidity J Biol Chem 272 1997 28757 28761 (Pubitemid 27517834)
41. A. Datta, F. Huber, and D. Boettiger Phosphorylation of beta3 integrin controls ligand binding strength J Biol Chem 277 2002 3943 3949 (Pubitemid 34968647)
42. G.H. Mahabeleshwar, W. Feng, D.R. Phillips, and T.V. Byzova Integrin signaling is critical for pathological angiogenesis J Exp Med 203 2006 2495 2507 (Pubitemid 44664619)
43. S.K. Chandhoke, M. Williams, E. Schaefer, L. Zorn, and S.D. Blystone Beta 3 integrin phosphorylation is essential for Arp3 organization into leukocyte alpha V beta 3-vitronectin adhesion contacts J Cell Sci 117 2004 1431 1441 (Pubitemid 38559819)
44. J.W. Smith, and D.A. Cheresh Integrin (alpha v beta 3)-ligand interaction. Identification of a heterodimeric RGD binding site on the vitronectin receptor J Biol Chem 265 1990 2168 2172
45. E. Ruoslahti RGD and other recognition sequences for integrins Annu Rev Cell Dev Biol 12 1996 697 715 (Pubitemid 26422728)
46. Y. Sun, S. Cressman, N. Fang, P.R. Cullis, and D.D.Y. Chen Capillary electrophoresis frontal analysis for characterization of alpha(v)beta(3) integrin binding interactions Anal Chem 80 2008 3105 3111 (Pubitemid 351620694)
47. T. Hermosilla, D. Munoz, R. Herrera-Molina, A. Valdivia, N. Munoz, and S.U. Nham Direct Thy-1/alphaVbeta3 integrin interaction mediates neuron to astrocyte communication Biochim Biophys Acta 1783 2008 1111 1120
48. J.R. Hurley, S. Balaji, and D.A. Narmoneva Complex temporal regulation of capillary morphogenesis by fibroblasts Am J Physiol Cell Physiol 299 2010 C444 C453
49. A.L. Sieminski, R.P. Hebbel, and K.J. Gooch The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro Exp Cell Res 297 2004 574 584 (Pubitemid 38798416)
50. B. Vailhe, D. Vittet, and J.J. Feige In vitro models of vasculogenesis and angiogenesis Lab Invest 81 2001 439 452 (Pubitemid 32298789)
51. M.F. Favata, K.Y. Horiuchi, E.J. Manos, A.J. Daulerio, D.A. Stradley, and W.S. Feeser Identification of a novel inhibitor of mitogen-activated protein kinase kinase J Biol Chem 273 1998 18623 18632 (Pubitemid 28334795)
52. S.G. Keswani, A.B. Katz, F.Y. Lim, P. Zoltick, A. Radu, and D. Alaee Adenoviral mediated gene transfer of PDGF-B enhances wound healing in type I and type II diabetic wounds Wound Repair Regen 12 2004 497 504 (Pubitemid 39314331)
53. M.D. Abramoff, P.J. Magelhaes, and S.J. Ram Image Processing with ImageJ Biophotonics Int 11 2004 36 42
54. C.M. Ghajar, X. Chen, J.W. Harris, V. Suresh, C.C. Hughes, and N.L. Jeon The effect of matrix density on the regulation of 3-D capillary morphogenesis Biophys J 94 2008 1930 1941
55. E. Kniazeva, and A.J. Putnam Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3-D Am J Physiol Cell Physiol 297 2009 C179 C187
56. L. Deshmukh, V. Gorbatyuk, and O. Vinogradova Integrin β3 phosphorylation dictates its complex with the Shc phosphotyrosine-binding (PTB) domain J Biol Chem 285 2010 34875 34884
57. R. Fukuda, K. Hirota, F. Fan, Y.D. Jung, L.M. Ellis, and G.L. Semenza Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells J Biol Chem 277 2002 38205 38211 (Pubitemid 35154674)
58. Y. Salem, S. Shpungin, O. Pasder, O. Pomp, M. Taler, and H. Malovani Fer kinase sustains the activation level of ERK1/2 and increases the production of VEGF in hypoxic cells Cell Signal 17 2005 341 353 (Pubitemid 39574695)
59. Balaji S, Sheikh AQ, Morris L, Lim FY, Crombleholme TM, Narmoneva DA. Angiogenic nanoscaffold accelerates diabetic wound healing and improves wound tissue strength in db/db mice. In: Proceedings of the ASME 2009 summer bioengineering conference2009.
60. K.M. Hodivala-Dilke, A.R. Reynolds, and L.E. Reynolds Integrins in angiogenesis: multitalented molecules in a balancing act Cell Tissue Res 314 2003 131 144 (Pubitemid 37409919)
61. H.D. Guo, G.H. Cui, H.J. Wang, and Y.Z. Tan Transplantation of marrow-derived cardiac stem cells carried in designer self-assembling peptide nanofibers improves cardiac function after myocardial infarction Biochem Biophys Res Commun 399 2010 42 48
62. S. Ahmed, H.K. Yang, A.E. Ozcam, K. Efimenko, M.C. Weiger, and J. Genzer Poly(vinylmethylsiloxane) elastomer networks as functional materials for cell adhesion and migration studies Biomacromolecules 12 2011 1265 1271
63. J. Zhu, C. Tang, K. Kottke-Marchant, and R.E. Marchant Design and synthesis of biomimetic hydrogel scaffolds with controlled organization of cyclic RGD peptides Bioconjug Chem 20 2009 333 339
64. S. Schiekofer, G. Galasso, K. Sato, B.J. Kraus, and K. Walsh Impaired revascularization in a mouse model of type 2 diabetes is associated with dysregulation of a complex angiogenic-regulatory network Arterioscler Thromb Vac Biol 25 2005 1603 1609 (Pubitemid 41098928)
65. M. Pfaff, M.A. McLane, L. Beviglia, S. Niewiarowski, and R. Timpl Comparison of disintegrins with limited variation in the RGD loop in their binding to purified integrins alpha IIb beta 3, alpha V beta 3 and alpha 5 beta 1 and in cell adhesion inhibition Cell Adhes Commun 2 1994 491 501
66. J.H. Collier, and T. Segura Evolving the use of peptides as components of biomaterials Biomaterials 32 2011 4198 4204
67. J.H. Collier, J.S. Rudra, J.Z. Gasiorowski, and J.P. Jung Multi-component extracellular matrices based on peptide self-assembly Chem Soc Rev 39 2010 3413 3424
68. M. Kushwaha, J.M. Anderson, C.A. Bosworth, A. Andukuri, W.P. Minor, and J.R. Lancaster Jr. A nitric oxide releasing, self assembled peptide amphiphile matrix that mimics native endothelium for coating implantable cardiovascular devices Biomaterials 31 2010 1502 1508
69. R. Soldi, S. Mitola, M. Strasly, P. Defilippi, G. Tarone, and F. Bussolino Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2 EMBO J 18 1999 882 892 (Pubitemid 29082268)
70. P.E. Depeille, Y. Ding, J.L. Bromberg-White, and N.S. Duesbery MKK signaling and vascularization Oncogene 26 2007 1290 1296 (Pubitemid 46328459)
71. S. Balaji, K. Marcotte, R. Helton, and D.A. Narmoneva Novel peptide scaffold promotes cell migration and angiogenesis through enhanced expression of angiogenic factors J Int Soc Thromb Haemost 4 Suppl. I 2006 69
72. K.K. Wary, G.D. Thakker, J.O. Humtsoe, and J. Yang Analysis of VEGF-responsive genes involved in the activation of endothelial cells Mol Cancer 2 2003 25
73. Y. Funahashi, C.J. Shawber, A. Sharma, E. Kanamaru, Y.K. Choi, and J. Kitajewski Notch modulates VEGF action in endothelial cells by inducing Matrix Metalloprotease activity Vasc Cell 3 2011 2
74. J.D. Humphries, A. Byron, and M.J. Humphries Integrin ligands at a glance J Cell Sci 119 2006 3901 3903 (Pubitemid 44650863)
75. N.J. Boudreau, and J.A. Varner The homeobox transcription factor Hox D3 promotes integrin alpha5beta1 expression and function during angiogenesis J Biol Chem 279 2004 4862 4868 (Pubitemid 38199081)
76. K.J. Bayless, R. Salazar, and G.E. Davis RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the alpha(v)beta(3) and alpha(5)beta(1) integrins Am J Pathol 156 2000 1673 1683 (Pubitemid 30646705)
77. J.J. Moon, M.S. Hahn, I. Kim, B.A. Nsiah, and J.L. West Micropatterning of poly(ethylene glycol) diacrylate hydrogels with biomolecules to regulate and guide endothelial morphogenesis Tissue Eng Part A 15 2009 579 585
78. P.A. DiMilla, K. Barbee, and D.A. Lauffenburger Mathematical model for the effects of adhesion and mechanics on cell migration speed Biophys J 60 1991 15 37
79. M.J. Powers, and L.G. Griffith Adhesion-guided in vitro morphogenesis in pure and mixed cell cultures Microsc Res Tech 43 1998 379 384 (Pubitemid 28565785)
80. S.P. Palecek, A. Huttenlocher, A.F. Horwitz, and D.A. Lauffenburger Physical and biochemical regulation of integrin release during rear detachment of migrating cells J Cell Sci 111 Pt. 7 1998 929 940 (Pubitemid 28196076)
81. J.S. Miller, C.J. Shen, W.R. Legant, J.D. Baranski, B.L. Blakely, and C.S. Chen Bioactive hydrogels made from step-growth derived PEG-peptide macromers Biomaterials 31 2010 3736 3743
82. S. Zhang Emerging biological materials through molecular self-assembly Biotechnol Adv 20 2002 321 339 (Pubitemid 35348279)
83. J. Kopecek, and J. Yang Peptide-directed self-assembly of hydrogels Acta Biomater 5 2009 805 816