A peptide-modified chitosan-collagen hydrogel for cardiac cell culture and delivery

Acta Biomaterialia

Volumn 8, Issue 3, 2012, Pages 1022-1036

  Reis, Lewis A ^a   Chiu, Loraine L Y ^b   Liang, Yan ^b   Hyunh, Kent ^a   Momen, Abdul ^c   Radisic, Milica ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Biomaterial; Cardiac; Hydrogel; Myocardial infarction; Peptide

Indexed keywords

BIOMATERIALS; BIOMECHANICS; CARDIOLOGY; CELL CULTURE; CHITOSAN; COLLAGEN; GELATION; HYDROGELS;

ANGIOPOIETINS; CARDIAC CELL; CARDIOMYOCYTES; COLLAGEN I; IN-VITRO; LOSS MODULI; MODIFIED CHITOSAN; MYOCARDIAL INFARCTION; SCAR FORMATION; THERMORESPONSIVE HYDROGELS;

PEPTIDES;

ANGIOPOIETIN 1; CHITOSAN; COLLAGEN TYPE 1; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CELL ENCAPSULATION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; DOSE RESPONSE; DRUG DELIVERY SYSTEM; GELATION; HEART INFARCTION; HEART MUSCLE CELL; IN VITRO STUDY; LEWIS RAT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

RATTUS;

EID: 84856538047     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2011.11.030     Document Type: Article

References (68)

1. Ontario HSFo. Statistics. 2010 [on-line].
2. M.A. Laflamme, and C.E. Murry Regenerating the heart Nat Biotechnol 23 2005 845 856 (Pubitemid 43093128)
3. H. Reinecke, G.H. MacDonald, S.D. Hauschka, and C.E. Murry Electromechanical coupling between skeletal and cardiac muscle. Implications for infarct repair J Cell Biol 149 2000 731 740 (Pubitemid 30252405)
4. H. Reinecke, V. Poppa, and C.E. Murry Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting J Mol Cell Cardiol 34 2002 241 249 (Pubitemid 35222833)
5. B. Bittira, J.-Q. Kuang, A. Al-Khaldi, D. Shum-Tim, and R.C.J. Chiu In vitro preprogramming of marrow stromal cells for myocardial regeneration Ann Thorac Surg 74 2002 1154 1159 discussion 9-60
6. S. Makino, K. Fukuda, S. Miyoshi, F. Konishi, H. Kodama, and J. Pan Cardiomyocytes can be generated from marrow stromal cells in vitro J Clin Invest 103 1999 697 705 (Pubitemid 29122423)
7. J.G. Shake, P.J. Gruber, W.A. Baumgartner, G. Senechal, J. Meyers, J.M. Redmond, M.F. Pittenger, and B.J. Martin Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects Ann Thorac Surg 73 2002 1919 1925 discussion 26
8. D. Orlic, J. Kajstura, S. Chimenti, I. Jakoniuk, S.M. Anderson, and B. Li Bone marrow cells regenerate infarcted myocardium Nature 410 2001 701 705 (Pubitemid 32290358)
9. C.E. Murry, M.H. Soonpaa, H. Reinecke, H. Nakajima, H.O. Nakajima, and M. Rubart Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts Nature 428 2004 664 668 (Pubitemid 38524810)
10. M.J. Lipinski, G.G. Biondi-Zoccai, A. Abbate, R. Khianey, I. Sheiban, and J. Bartunek Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: a collaborative systematic review and meta-analysis of controlled clinical trials J Am Coll Cardiol 50 2007 1761 1767 (Pubitemid 47600592)
11. J. Müller-Ehmsen, P. Whittaker, R.A. Kloner, J.S. Dow, T. Sakoda, T.I. Long, P.W. Laird, and L. Kedes Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium J Mol Cell Cardiol 34 2002 107 116 (Pubitemid 35229976)
12. M. Zhang, D. Methot, V. Poppa, Y. Fujio, K. Walsh, and C.E. Murry Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies J Mol Cell Cardiol 33 2001 907 921 (Pubitemid 32545326)
13. P. Menasché Current status and future prospects for cell transplantation to prevent congestive heart failure Semin Thorac Cardiovasc Surg 20 2008 131 137
14. N. Smart, Ca. Risebro, Melville. AaD, K. Moses, R.J. Schwartz, and K.R. Chien Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization Nature 445 2007 177 182 (Pubitemid 46095717)
15. I. Bock-Marquette, A. Saxena, M.D. White, J.M. Dimaio, and D. Srivastava Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair Nature 432 2004 466 472 (Pubitemid 39576522)
16. D. Crockford Development of thymosin beta4 for treatment of patients with ischemic heart disease Ann N. Y. Acad Sci 1112 2007 385 395 (Pubitemid 47598686)
17. J.M. Nygren, S. Jovinge, M. Breitbach, P. Säwén, W. Röll, and J. Hescheler Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation Nat Med 10 2004 494 501 (Pubitemid 38667908)
18. S. Minatoguchi, G. Takemura, X.-H. Chen, N. Wang, Y. Uno, and M. Koda Acceleration of the healing process and myocardial regeneration may be important as a mechanism of improvement of cardiac function and remodeling by postinfarction granulocyte colony-stimulating factor treatment Circulation 109 2004 2572 2580 (Pubitemid 38720559)
19. K.L. Christman, H.H. Fok, R.E. Sievers, Q. Fang, and R.J. Lee Fibrin glue alone and skeletal myoblasts in a fibrin scaffold preserve cardiac function after myocardial infarction Tissue Eng 10 2004 403 409 (Pubitemid 38580261)
20. K.L. Christman, A.J. Vardanian, Q. Fang, R.E. Sievers, H.H. Fok, and R.J. Lee Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium J Am Coll Cardiol 44 2004 654 660 (Pubitemid 39089073)
21. T. Kofidis, D.R. Lebl, E.C. Martinez, G. Hoyt, M. Tanaka, and R.C. Robbins Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury Circulation 112 2005 I173 I177
22. S.J. Yoon, Y.H. Fang, C.H. Lim, B.S. Kim, H.S. Son, and Y. Park Regeneration of ischemic heart using hyaluronic acid-based injectable hydrogel J Biomed Mater Res B Appl Biomater 91 2009 163 171
23. M.E. Davis, J.P.M. Motion, D.A. Narmoneva, T. Takahashi, D. Hakuno, R.D. Kamm, S. Zhang, and R.T. Lee Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells Circulation 111 2005 442 450 (Pubitemid 40204428)
24. E.J. Suuronen, J.P. Veinot, S. Wong, V. Kapila, J. Price, and M. Griffith Tissue-engineered injectable collagen-based matrices for improved cell delivery and vascularization of ischemic tissue using CD133+ progenitors expanded from the peripheral blood Circulation 114 2006 I138 I144
25. C. Deng, P. Zhang, B. Vulesevic, D. Kuraitis, F. Li, and A.F. Yang A collagen-chitosan hydrogel for endothelial differentiation and angiogenesis Tissue Eng Part A 16 2010 3099 3109
26. W.N. Lu, S.-H. Lü, H.-B. Wang, D.-X. Li, C.-M. Duan, and Z.-Q. Liu Functional improvement of infarcted heart by co-injection of embryonic stem cells with temperature-responsive chitosan hydrogel Tissue Eng Part A 15 2009 1437 1447
27. F. Rask, A. Mihic, L. Reis, S.M. Dallabrida, N.S. Ismail, and K. Sider Hydrogels modified with QHREDGS peptide support cardiomyocyte survival in vitro and after sub-cutaneous implantation Soft Matter 6 2010 5089 5099
28. J.A. DeQuach, V. Mezzano, A. Miglani, S. Lange, G.M. Keller, and F. Sheikh PLoS One 5 2010 e13039
29. Y. Duan, Z. Liu, J. O'Neill, L.Q. Wan, D.O. Freytes, and G. Vunjak-Novakovic Hybrid gel composed of native heart matrix and collagen induces cardiac differentiation of human embryonic stem cells without supplemental growth factors J Cardiovasc Transl Res 4 2011 605 615
30. Q.Z. Chen, S.E. Harding, N.N. Ali, A.R. Lyon, and A.R. Boccaccini Biomaterials in cardiac tissue engineering: ten years of research survey Mater Sci Eng R Rep 59 2008 1 37 (Pubitemid 351625614)
31. M. Prasitsilp, R. Jenwithisuk, K. Kongsuwan, N. Damrongchai, and P. Watts Cellular responses to chitosan in vitro: the importance of deacetylation J Mater Sci Mater Med 11 2000 773 778 (Pubitemid 32014530)
32. R.A.A. Muzzarelli Biochemical significance of exogenous chitins and chitosans in animals and patients Carbohydr Polym 20 1993 7 16
33. Q. Li, E.T. Dunn, E.W. Grandmaison, and M.F.A. Goosen Applications and properties of chitosan J Bioact Compat Polym 7 1992 370 397 (Pubitemid 23020214)
34. N.V. Majeti, and R. Kumar A review of chitin and chitosan applications React Funct Polym 46 2000 1 27
35. I.Y. Kim, S.-J. Seo, H.-S. Moon, M.-K. Yoo, I.-Y. Park, and B.-C. Kim Chitosan and its derivatives for tissue engineering applications Biotechnol Adv 26 2008 1 21 (Pubitemid 350138341)
36. S.M. Dallabrida, N. Ismail, J.R. Oberle, B.E. Himes, and M.A. Rupnick Angiopoietin-1 promotes cardiac and skeletal myocyte survival through integrins Circ Res 96 2005 e8 e24
37. F. Rask The development of an injectible hydrogel for the site-specific delivery of cardiomyocytes to the heart 2009 University of Toronto Toronto
38. F. Rask, S.M. Dallabrida, N.S. Ismail, Z. Amoozgar, Y. Yeo, and M.A. Rupnick Photocrosslinkable chitosan modified with angiopoietin-1 peptide, QHREDGS, promotes survival of neonatal rat heart cells J Biomed Mater Res A 95 2010 105 117
39. S.Y. Boateng, S.S. Lateef, W. Mosley, T.J. Hartman, L. Hanley, and B. Russell RGD and YIGSR synthetic peptides facilitate cellular adhesion identical to that of laminin and fibronectin but alter the physiology of neonatal cardiac myocytes Am J Physiol Cell Physiol 288 2005 C30 C38
40. S. Balasubramanian, and D. Kuppuswamy RGD-containing peptides activate S6K1 through beta3 integrin in adult cardiac muscle cells J Biol Chem 278 2003 42214 42224 (Pubitemid 37310488)
41. T. Eschenhagen, C. Fink, U. Remmers, H. Scholz, J. Wattchow, and J. Weil Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system FASEB J 11 1997 683 694 (Pubitemid 27318285)
42. M. Radisic, H. Park, H. Shing, T. Consi, F.J. Schoen, and R. Langer Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds Proc Nat Acad Sci U.S.A. 101 2004 18129 18134 (Pubitemid 40054085)
43. S. Pulapura, and J. Kohn Trends in the development of bioresorbable polymers for medical applications J Biomater Appl 6 1992 216 250
44. 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)
45. W. Tan, R. Krishnaraj, and T.A. Desai Evaluation of nanostructured composite collagen-chitosan matrices for tissue engineering Tissue Eng 7 2001 203 210 (Pubitemid 32295154)
46. M.L. Graber, D.C. DiLillo, B.L. Friedman, and E. Pastoriza-Munoz Characteristics of fluoroprobes for measuring intracellular pH Anal Biochem 156 1986 202 212 (Pubitemid 16044421)
47. M. Radisic, M. Euloth, L. Yang, R. Langer, L.E. Freed, and G. Vunjak-Novakovic High-density seeding of myocyte cells for cardiac tissue engineering Biotechnol Bioeng 82 2003 403 414 (Pubitemid 36505879)
48. R.K. Iyer, L.L.Y. Chiu, and M. Radisic Microfabricated poly(ethylene glycol) templates enable rapid screening of triculture conditions for cardiac tissue engineering J Biomed Mater Res A 89 2009 616 631
49. J. Dengler, H. Song, N. Thavandiran, S. Massé, G.A. Wood, K. Nanthakumar, P.A. Zandtsra, and M. Radisic Engineered heart tissue enables study of residual undifferentiated embryonic stem cell activity in a cardiac environment Biotechnol Bioeng 108 3 2011 704 719
50. E. Rossomacha, C.D. Hoemanni, and M.S. Shive Simple methods for staining chitosan in biotechnological applications J Histotechnol 27 2004 31 36 (Pubitemid 38451874)
51. L.L.Y. Chiu, and M. Radisic Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues Biomaterials 31 2010 226 241
52. B. Bhana, R.K. Iyer, W.L. Chen, R. Zhao, K.L. Sider, and M. Likhitpanichkul Influence of substrate stiffness on the phenotype of heart cells Biotechnol Bioeng 105 2010 1148 1160
53. L. Wang, and J.P. Stegemann Glyoxal crosslinking of cell-seeded chitosan/collagen hydrogels for bone regeneration Acta Biomater 7 2011 2410 2417
54. S. Ikeda, and E.A. Foegeding Measurement of gel rheology: dynamic tests R.E. Wrolstad, T.E. Acree, E.A. Decker, M.H. Penner, D.S. Reid, S.J. Schwartz, Current protocols in food analytical chemistry 2003 John Wiley & Sons Hoboken, NJ 1 9
55. P. Whittingstall Dynamic or oscillatory testing of complex fluids R.E. Wrolstad, T.E. Acree, E.A. Decker, M.H. Penner, D.S. Reid, S.J. Schwartz, Current protocols in food analytical chemistry 2003 John Wiley & Sons Hoboken, NJ 1 11
56. C.A. DeForest, E.A. Sims, and K.S. Anseth Peptide-functionalized click hydrogels with independently tunable mechanics and chemical functionality for 3D cell culture Chem Mater 22 2010 4783 4790
57. Y. Miyagi, L.L. Chiu, M. Cimini, R.D. Weisel, M. Radisic, and R.K. Li Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair Biomaterials 32 2011 1280 1290
58. W.H. Zimmermann, I. Melnychenko, and T. Eschenhagen Engineered heart tissue for regeneration of diseased hearts Biomaterials 25 2004 1639 1647 (Pubitemid 38091542)
59. J. Elisseeff, K. Anseth, D. Sims, W. McIntosh, M. Randolph, and R. Langer Transdermal photopolymerization for minimally invasive implantation Proc Nat Acad Sci U.S.A. 96 1999 3104 3107 (Pubitemid 29148851)
60. L.L.Y. Chiu, and M. Radisic Controlled release of thymosin β4 using collagen-chitosan composite hydrogels promotes epicardial cell migration and angiogenesis J Controlled Release 155 2011 376 385
61. M.J. van Luyn, I.M. Khouw, P.B. van Wachem, E.H. Blaauw, and J.A. Werkmeister Modulation of the tissue reaction to biomaterials. II. The function of T cells in the inflammatory reaction to crosslinked collagen implanted in T-cell-deficient rats J Biomed Mater Res 1998 398 406 (Pubitemid 28063455)
62. T.F. Krzemiński, J.K. Nozyński, J. Grzyb, and M. Porc Wide-spread myocardial remodeling after acute myocardial infarction in rat. Features for heart failure progression Vascul Pharmacol 48 2008 100 108
63. R. Patten, M. Aronovitz, L. Deras-Mejia, N.G. Pandian, G.G. Hanak, and J.J. Smith Am Physiol Soc 274 1998 H1812
64. S.T. Wall, J.C. Walker, K.E. Healy, M.B. Ratcliffe, and J.M. Guccione Theoretical impact of the injection of material into the myocardium: a finite element model simulation Circulation 114 2006 2627 2635 (Pubitemid 44967346)
65. K.L. Fujimoto, Z. Ma, D.M. Nelson, R. Hashizume, J. Guan, and K. Tobita Synthesis, characterization and therapeutic efficacy of a biodegradable, thermoresponsive hydrogel designed for application in chronic infarcted myocardium Biomaterials 30 2009 4357 4368
66. Y. Ito Covalently immobilized biosignal molecule materials for tissue engineering Soft Matter 4 2008 46 56
67. V.H. Fan, K. Tamama, A. Au, R. Littrell, L.B. Richardson, and J.W. Wright Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells Stem cells 25 2007 1241 1251 (Pubitemid 46684884)
68. J. Wu, F. Zeng, X.-P. Huang, J.C.-Y. Chung, F. Konecny, and R.D. Weisel Infarct stabilization and cardiac repair with a VEGF-conjugated, injectable hydrogel Biomaterials 32 2011 579 586