A nondenatured, noncrosslinked collagen matrix to deliver stem cells to the heart

Regenerative Medicine

Volumn 6, Issue 5, 2011, Pages 569-582

  Kouris, Nicholas A ^a   Squirrell, Jayne M ^a   Jung, Jangwook P ^a   Pehlke, Carolyn A ^a   Hacker, Timothy ^b   Eliceiri, Kevin W ^a   Ogle, Brenda M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

biomaterial; cardiac patch; cardiac regeneration; collagen; mesenchymal stem cells

Indexed keywords

BIOMATERIAL; COLLAGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCOMPATIBILITY; CELL ADHESION; CELL COUNT; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; CROSS LINKING; DENATURATION; HEART INFARCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; TISSUE REPAIR;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; COLLAGEN; HEART; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MYOCARDIAL INFARCTION; MYOCARDIUM; REGENERATION;

EID: 80052888669     PISSN: 17460751     EISSN: 1746076X     Source Type: Journal    
DOI: 10.2217/rme.11.48     Document Type: Article

References (91)

1. Orsini E, Zito GB. Matching pathophysiology and evidence-based medicine for optimal management of ischemic heart disease. J. Cardiovasc. Med. (Hagerstown) 11(6), 469-479 (2010).
2. Baig MK, Mahon N, McKenna WJ, et al. The pathophysiology of advanced heart failure. Am. Heart J. 135(6 Pt 2 Su), S216-S230 (1998). (Pubitemid 28350124)
3. Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, Ashraf M. Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc. Res. 77(1), 134-142 (2008). (Pubitemid 351195153)
4. Zhang D, Fan GC, Zhou X, et al. Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. J. Mol. Cell. Cardiol. 44(2), 281-292 (2008).
5. Wolf D, Reinhard A, Seckinger A, Gross L, Katus HA, Hansen A. Regenerative capacity of intravenous autologous, allogeneic and human mesenchymal stem cells in the infarcted pig myocardium - complicated by myocardial tumor formation. Scand. Cardiovasc. J. 43(1), 39-45 (2009).
6. Xu YL, Gao YH, Liu Z, et al. Myocardium-targeted transplantation of mesenchymal stem cells by diagnostic ultrasound-mediated microbubble destruction improves cardiac function in myocardial infarction of New Zealand rabbits. Int. J. Cardiol. 138(2), 182-195 (2010).
7. Guddati AK, Otero JJ, Kessler E, et al. Embryonic stem cells overexpressing Pitx2c engraft in infarcted myocardium and improve cardiac function. Int. Heart J. 50(6), 783-799 (2009).
8. Schneider C, Jaquet K, Geidel S, et al. Transplantation of bone marrow-derived stem cells improves myocardial diastolic function: strain rate imaging in a model of hibernating myocardium. J. Am. Soc. Echocardiogr. 22(10), 1180-1189 (2009).
9. Qiao H, Surti S, Choi SR, et al. Death and proliferation time course of stem cells transplanted in the myocardium. Mol. Imaging Biol. 11(6), 408-414 (2009).
10. Simpson D, Liu H, Fan TH, Nerem R, Dudley SC Jr. A tissue engineering approach to progenitor cell delivery results in significant cell engraftment and improved myocardial remodeling. Stem Cells 25(9), 2350-2357 (2007). (Pubitemid 47480494)
11. Li M, Yu J, Li Y, Li D, Yan D, Ruan Q. CXCR4+ progenitors derived from bone mesenchymal stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Cell. Reprogram. 12(4), 405-415 (2010).
12. Chakraborty S, Kang B, Huang F, Guo YL. Mouse embryonic stem cells lacking p38a and p38d can differentiate to endothelial cells, smooth muscle cells, and epithelial cells. Differentiation 78(2-3), 143-150 (2009).
13. Guo YL, Ye J, Huang F. p38a MAP kinase-deficient mouse embryonic stem cells can differentiate to endothelial cells, smooth muscle cells, and neurons. Dev. Dyn. 236(12), 3383-3392 (2007). (Pubitemid 350276394)
14. Xiao Q, Zeng L, Zhang Z, et al. Sca-1+ progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler. Thromb. Vasc. Biol. 26(10), 2244-2251 (2006). (Pubitemid 44465718)
15. Silva GV, Litovsky S, Assad JA, et al. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 111(2), 150-156 (2005). (Pubitemid 40139725)
16. Dawn B, Stein AB, Urbanek K, et al. Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc. Natl Acad. Sci. USA 102(10), 3766-3771 (2005). (Pubitemid 40354686)
17. Zhang M, Methot D, Poppa V, Fujio Y, Walsh K, Murry CE. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J. Mol. Cell. Cardiol. 33(5), 907-921 (2001). (Pubitemid 32545326)
18. Suzuki K, Murtuza B, Beauchamp JR, et al. Dynamics and mediators of acute graft attrition after myoblast transplantation to the heart. FASEB J. 18(10), 1153-1155 (2004). (Pubitemid 39561554)
19. Yasuda T, Weisel RD, Kiani C, Mickle DA, Maganti M, Li RK. Quantitative analysis of survival of transplanted smooth muscle cells with real-time polymerase chain reaction. J. Thorac. Cardiovasc. Surg. 129(4), 904-911 (2005). (Pubitemid 40487896)
20. Mazo M, Planat-Benard V, Abizanda G, et al. Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur. J. Heart Fail. 10(5), 454-462 (2008).
21. Schneider C, Krause K, Jaquet K, et al. Intramyocardial transplantation of bone marrow-derived stem cells: ultrasonic strain rate imaging in a model of hibernating myocardium. J. Card. Fail. 14(10), 861-872 (2008).
22. Wang T, Tang W, Sun S, et al. Mesenchymal stem cells improve outcomes of cardiopulmonary resuscitation in myocardial infarcted rats. J. Mol. Cell. Cardiol. 46(3), 378-384 (2009).
23. Lee J, Stagg MA, Fukushima S, et al. Adult progenitor cell transplantation influences contractile performance and calcium handling of recipient cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 296(4), H927-H936 (2009).
24. Zhao T, Zhang D, Millard RW, Ashraf M, Wang Y. Stem cell homing and angiomyogenesis in transplanted hearts are enhanced by combined intramyocardial SDF-1a delivery and endogenous cytokine signaling. Am. J. Physiol. Heart Circ. Physiol. 296(4), H976-H986 (2009).
25. Krause K, Jaquet K, Schneider C, et al. Percutaneous intramyocardial stem cell injection in patients with acute myocardial infarction: first-in-man study. Heart 95(14), 1145-1152 (2009).
26. Wang T, Jiang XJ, Lin T, et al. The inhibition of postinfarct ventricle remodeling without polycythaemia following local sustained intramyocardial delivery of erythropoietin within a supramolecular hydrogel. Biomaterials 30(25), 4161-4167 (2009).
27. Makela J, Anttila V, Ylitalo K, et al. Acute homing of bone marrow-derived mononuclear cells in intramyocardial vs. intracoronary transplantation. Scand. Cardiovasc. J. 43(6), 366-373 (2009).
28. Zhou Y, Wang S, Yu Z, et al. Direct injection of autologous mesenchymal stromal cells improves myocardial function. Biochem. Biophys. Res. Commun. 390(3), 902-907 (2009).
29. Kenar H, Kose GT, Hasirci V. Design of a 3D aligned myocardial tissue construct from biodegradable polyesters. J. Mater. Sci. Mater. Med. 21(3), 989-997 (2010).
30. Zhou Q, Zhou JY, Zheng Z, Zhang H, Hu SS. A novel vascularized patch enhances cell survival and modifies ventricular remodeling in a rat myocardial infarction model. J. Thorac. Cardiovasc. Surg. 140(6), 1388-1396.e1-3 (2010).
31. Bursac N, Loo Y, Leong K, Tung L. Novel anisotropic engineered cardiac tissues: studies of electrical propagation. Biochem. Biophys. Res. Commun. 361(4), 847-853 (2007). (Pubitemid 47259017)
32. Kochupura PV, Azeloglu EU, Kelly DJ, et al. Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function. Circulation 112(Suppl. 9), I144-I149 (2005). (Pubitemid 41266666)
33. Kumbar SG, James R, Nukavarapu SP, Laurencin CT. Electrospun nanofiber scaffolds: engineering soft tissues. Biomed. Mater. 3(3), 034002 (2008).
34. Potapova IA, Doronin SV, Kelly DJ, et al. Enhanced recovery of mechanical function in the canine heart by seeding an extracellular matrix patch with mesenchymal stem cells committed to a cardiac lineage. Am. J. Physiol. Heart Circ. Physiol. 295(6), H2257-H2263 (2008).
35. Hou D, Youssef EA, Brinton TJ, et al. Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation 112(Suppl. 9), I150-I156 (2005). (Pubitemid 41266667)
36. Freyman T, Polin G, Osman H, et al. A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur. Heart J. 27(9), 1114-1122 (2006).
37. Sui R, Liao X, Zhou X, Tan Q. The current status of engineering myocardial tissue. Stem Cell Rev. 7(1), 172-180 (2011).
38. Shapira K, Dikovsky D, Habib M, Gepstein L, Seliktar D. Hydrogels for cardiac tissue regeneration. Biomed. Mater. Eng. 18(4-5), 309-314 (2008).
39. Akhyari P, Kamiya H, Haverich A, Karck M, Lichtenberg A. Myocardial tissue engineering: the extracellular matrix. Eur. J. Cardiothorac. Surg. 34(2), 229-241 (2008).
40. Horton RE, Millman JR, Colton CK, Auguste DT. Engineering microenvironments for embryonic stem cell differentiation to cardiomyocytes. Regen. Med. 4(5), 721-732 (2009).
41. Jawad H, Ali NN, Lyon AR, Chen QZ, Harding SE, Boccaccini AR. Myocardial tissue engineering: a review. J. Tissue Eng. Regen. Med. 1(5), 327-342 (2007).
42. Wang F, Guan J. Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy. Adv. Drug Deliv. Rev. 62(7-8), 784-797 (2010).
43. Wang T, Jiang XJ, Tang QZ, et al. Bone marrow stem cells implantation with a-cyclodextrin/MPEG-PCL-MPEG hydrogel improves cardiac function after myocardial infarction. Acta Biomater. 5(8), 2939-2944 (2009).
44. Bryant SJ, Nicodemus GD, Villanueva I. Designing 3D photopolymer hydrogels to regulate biomechanical cues and tissue growth for cartilage tissue engineering. Pharm. Res. 25(10), 2379-2386 (2008).
45. Zhu J, Tang C, Kottke-Marchant K, Marchant RE. Design and synthesis of biomimetic hydrogel scaffolds with controlled organization of cyclic RGD peptides. Bioconjug. Chem. 20(2), 333-339 (2009).
46. Benton JA, Fairbanks BD, Anseth KS. Characterization of valvular interstitial cell function in three dimensional matrix metalloproteinase degradable PEG hydrogels. Biomaterials 30(34), 6593-6603 (2009).
47. Varghese S, Hwang NS, Canver AC, Theprungsirikul P, Lin DW, Elisseeff J. Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol. 27(1), 12-21 (2008).
48. Roche S, Ronziere MC, Herbage D, Freyria AM. Native and DPPA cross-linked collagen sponges seeded with fetal bovine epiphyseal chondrocytes used for cartilage tissue engineering. Biomaterials 22(1), 9-18 (2001).
49. Ma L, Gao C, Mao Z, et al. Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials 24(26), 4833-4841 (2003). (Pubitemid 37188662)
50. Park SN, Park JC, Kim HO, Song MJ, Suh H. Characterization of porous collagen/hyaluronic acid scaffold modified by 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide cross-linking. Biomaterials 23(4), 1205-1212 (2002). (Pubitemid 33109052)
51. Marijianowski MM, Teeling P, Mann J, Becker AE. Dilated cardiomyopathy is associated with an increase in the type I/type III collagen ratio: a quantitative assessment. J. Am. Coll. Cardiol. 25(6), 1263-1272 (1995).
52. Trivedi P, Hematti P. Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells. Exp. Hematol. 36(3), 350-359 (2008).
53. Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 248(4951), 73-76 (1990).
54. Mohler W, Millard AC, Campagnola PJ. Second harmonic generation imaging of endogenous structural proteins. Methods 29(1), 97-109 (2003). (Pubitemid 36259916)
55. Kenealey JD, Subramanian L, Van Ginkel PR, et al. Resveratrol metabolites do not elicit early pro-apoptotic mechanisms in neuroblastoma cells. J. Agric. Food Chem. 59(9), 4979-4986 (2011).
56. Sung KE, Yang N, Pehlke C, et al. Transition to invasion in breast cancer: a microfluidic in vitro model enables examination of spatial and temporal effects. Integr. Biol. (Camb.) 3(4), 439-450 (2011).
57. Provenzano PP, Inman DR, Eliceiri KW, Keely PJ. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28(49), 4326-4343 (2009).
58. Abbi S, Ueda H, Zheng C, et al. Regulation of focal adhesion kinase by a novel protein inhibitor FIP200. Mol. Biol. Cell 13(9), 3178-3191 (2002). (Pubitemid 35034254)
59. Michael LH, Entman ML, Hartley CJ, et al. Myocardial ischemia and reperfusion: a murine model. Am. J. Physiol. 269(6 Pt 2), H2147-H2154 (1995). (Pubitemid 26023233)
60. Ogle BM, Butters KA, Plummer TB, et al. Spontaneous fusion of cells between species yields transdifferentiation and retroviral transfer in vivo. FASEB J. 18(3), 548-550 (2004).
61. Chaudhuri S, Nguyen H, Rangayyan RM, Walsh S, Frank CB. A Fourier domain directional filtering method for analysis of collagen alignment in ligaments. IEEE Trans. Biomed. Eng. 34(7), 509-518 (1987). (Pubitemid 17632200)
62. Marquez JP. Fourier analysis and automated measurement of cell and fiber angular orientation distributions. Int. J. Solids Struct. 43(21), 6413-6423 (2006). (Pubitemid 44389853)
63. Candes EJ, Donoho DL. Curvelets - a surprisingly effective nonadaptive representation for objects with edges. In:Curves and Surface Fitting: St-Malo 1999. Cohen A, Rabut C, Schumaker LL (Eds). Vanderbilt University Press, Nashville, TN, USA (2000).
64. Tse JR, Engler AJ. Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS One 6(1), e15978 (2011).
65. Jiang G, Huang AH, Cai Y, Tanase M, Sheetz MP. Rigidity sensing at the leading edge through avb3 integrins and RPTPa. Biophys. J. 90(5), 1804-1809 (2006).
66. Lo CM, Wang HB, Dembo M, Wang YL. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79(1), 144-152 (2000). (Pubitemid 30436733)
67. Eitan Y, Sarig U, Dahan N, Machluf M. Acellular cardiac extracellular matrix as a scaffold for tissue engineering: in vitro cell support, remodeling, and biocompatibility. Tissue Eng. Part C Methods 16(4), 671-683 (2010).
68. Choi EW, Shin IS, Lee HW, et al. Transplantation of CTLA4Ig gene-transduced adipose tissue-derived mesenchymal stem cells reduces inflammatory immune response and improves Th1/Th2 balance in experimental autoimmune thyroiditis. J. Gene Med. 13(1), 3-16 (2011).
69. Bunnell BA, Betancourt AM, Sullivan DE. New concepts on the immune modulation mediated by mesenchymal stem cells. Stem Cell Res. Ther. 1(5), 34 (2010).
70. Haddad E, Chen C, Greenberger E. The role of important non-parental adults (VIPs) in the lives of older adolescents: a comparison of three ethnic groups. J. Youth Adolesc. 40(3), 310-319 (2011).
71. Li FR, Wang XG, Deng CY, Qi H, Ren LL, Zhou HX. Immune modulation of co-transplantation mesenchymal stem cells with islet on T and dendritic cells. Clin. Exp. Immunol. 161(2), 357-363 (2010).
72. Fibbe WE, Nauta AJ, Roelofs H. Modulation of immune responses by mesenchymal stem cells. Ann. NY Acad. Sci. 1106, 272-278 (2007). (Pubitemid 47443061)
73. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105(4), 1815-1822 (2005). (Pubitemid 40223708)
74. Goldsmith EC, Hoffman A, Morales MO, et al. Organization of fibroblasts in the heart. Dev. Dyn. 230(4), 787-794 (2004). (Pubitemid 38993878)
75. Camelliti P, Borg TK, Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc. Res. 65(1), 40-51 (2005). (Pubitemid 40038477)
76. Rabani V, Shahsavani M, Gharavi M, Piryaei A, Azhdari Z, Baharvand H. Mesenchymal stem cell infusion therapy in a carbon tetrachloride-induced liver fibrosis model affects matrix metalloproteinase expression. Cell Biol. Int. 34(6), 601-605 (2010).
77. Ma J, Ge J, Zhang S, et al. Time course of myocardial stromal cell-derived factor 1 expression and beneficial effects of intravenously administered bone marrow stem cells in rats with experimental myocardial infarction. Basic Res. Cardiol. 100(3), 217-223 (2005). (Pubitemid 41348812)
78. Shake JG, Gruber PJ, Baumgartner WA, et al. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann. Thorac. Surg. 73(6), 1919-1925; discussion 1926 (2002).
79. Nagaya N, Fujii T, Iwase T, et al. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am. J. Physiol. Heart Circ. Physiol. 287(6), H2670-H2676 (2004). (Pubitemid 39557139)
80. Vunjak-Novakovic G, Tandon N, Godier A, et al. Challenges in cardiac tissue engineering. Tissue Eng. Part B Rev. 16(2), 169-187 (2010).
81. Lieber SC, Aubry N, Pain J, Diaz G, Kim SJ, Vatner SF. Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. Am. J. Physiol. Heart Circ. Physiol. 287(2), H645-H651 (2004). (Pubitemid 38955295)
82. Bhana B, Iyer RK, Chen WL, et al. Influence of substrate stiffness on the phenotype of heart cells. Biotechnol. Bioeng. 105(6), 1148-1160 (2010).
83. van der Loo JJ, Jakot J, Bovendeerd PHM. The development in cardiac stiffness in embryonic, neonatal and adult mice evaluated with atomic force microscopy. BMTE 08.45, internal report, Technische Universiteit Eindhoven (2008).
84. Berry MF, Engler AJ, Woo YJ, et al. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart Circ. Physiol. 290(6), H2196-H2203 (2006). (Pubitemid 43846045)
85. Zhang S, Sun A, Ma H, et al. Infarcted myocardium-like stiffness contributes to endothelial progenitor lineage commitment of bone marrow mononuclear cells. J. Cell. Mol. Med. DOI: 10.1111/j.1582-4934.2010.01217.x (2010) (Epub ahead of print).
86. Aurora A, McCarron J, Iannotti JP, Derwin K. Commercially available extracellular matrix materials for rotator cuff repairs: state of the art and future trends. J. Shoulder Elbow Surg. 16(Suppl. 5), S171-S178 (2007). (Pubitemid 47446298)
87. Valentin JE, Badylak JS, McCabe GP, Badylak SF. Extracellular matrix bioscaffolds for orthopaedic applications. A comparative histologic study. J. Bone Joint Surg. Am. 88(12), 2673-2686 (2006). (Pubitemid 44901955)
88. Agrawal V, Johnson SA, Reing J, et al. Epimorphic regeneration approach to tissue replacement in adult mammals. Proc. Natl Acad. Sci. USA 107(8), 3351-3355 (2010).
89. Mayo Clinic: definition of heart disease by Mayo Clinic staff www.mayoclinic.com/health/heart-disease/DS01120
90. American Heart Association www.americanheart.org
91. Stryker: TissueMend® www.stryker.com/en-us/products/Orthopaedics/ SoftTissueRepair/index.htm