Cardiac Fibroblasts Support Endothelial Cell Proliferation and Sprout Formation but not the Development of Multicellular Sprouts in a Fibrin Gel Co-Culture Model

Annals of Biomedical Engineering

Volumn 42, Issue 5, 2014, Pages 1074-1084

  Twardowski, Rachel L ^a   Black III, Lauren D ^a,b  

^a Tufts University   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

3D cell culture; Angiogenesis and vasculogenesis; Endothelial cells; Heart tissue engineering; Myocardium

Indexed keywords

CELL PROLIFERATION; ENDOTHELIAL CELLS; FIBROBLASTS; FLOWCHARTING; HEART; OPTIMIZATION; TISSUE ENGINEERING;

3-D CELL CULTURE; CARDIAC TISSUE ENGINEERING; HEART TISSUES; MECHANICAL FUNCTIONS; MESENCHYMAL STEM CELL; MYOCARDIUM; VASCULAR SMOOTH MUSCLE CELLS; VASCULOGENESIS;

CELL CULTURE;

FIBRIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL COUNT; CELL PROLIFERATION; CELL STRUCTURE; COCULTURE; CONTROLLED STUDY; DNA DETERMINATION; ENDOTHELIUM CELL; FIBROBLAST; FLOW CYTOMETRY; HEART; HYDROGEL; IMMUNOHISTOLOGY; IN VIVO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RAT; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL COUNT; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; FIBRIN; FIBROBLASTS; GELS; MESENCHYMAL STROMAL CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, SPRAGUE-DAWLEY; TISSUE ENGINEERING;

EID: 84898541404     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-014-0971-2     Document Type: Article

References (34)

1. Ahmann, K. A., J. S. Weinbaum, S. L. Johnson, and R. T. Tranquillo. Fibrin degradation enhances vascular smooth muscle cell proliferation and matrix deposition in fibrin-based tissue constructs fabricated in vitro. Tissue Eng. Part A. 16: 3261-3270, 2010.
2. Augustin, H. G., G. Y. Koh, G. Thurston, and K. Alitalo. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 10(3): 165-177, 2009.
3. Bergers, G., and S. Song. The role of pericytes in blood-vessel formation and maintenance. Neuro-Oncology 7: 452-464, 2005.
4. Black, L. D., J. D. Meyers, J. S. Weinbaum, Y. A. Shvelidze, and R. T. Tranquillo. Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng. Part A 15: 3099-3108, 2009.
5. Bootle-Wilbraham, C. A., S. Tazzyman, W. D. Thompson, C. M. Stirk, and C. E. Lewis. Fibrin fragment E stimulate the proliferation, migration and differentiation of human microvascular endothelial cells in vitro. Angiogenesis 4: 269-275, 2001.
6. Carmeliet, P., and R. K. Jain. Angiogenesis in cancer and other diseases. Nature 407: 249-257, 2000.
7. Chen, X., A. S. Aledia, C. M. Ghajar, C. K. Griffith, A. J. Putnam, C. C. W. Hughes, et al. Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng. Part A 15: 1363-1371, 2009.
8. Davis, D. R., E. Kizana, J. Terrovitis, A. S. Barth, Y. Zhang, R. P. Smith, et al. Isolation and expansion of functionally-competent cardiac progenitor cells directly from heart biopsies. J. Mol. Cell Cardiol. 49: 312-321, 2010.
9. Davis, G. E., and D. R. Senger. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ. Res. 97: 1093-1107, 2005.
10. Duffy, G. P., 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. Tissue Eng. Part A 15: 2459-2470, 2009.
11. Gai, G., E. L. Leung, P. D. Costantino, J. R. Aguila, D. M. Nguyen, L. M. Fink, et al. Generation and characterization of functional cardiomyocytes using induced pluripotent stem cells derived from human fibroblasts. Cell Biol. Int. 33: 1184-1193, 2009.
12. Gerhardt, H., and C. Betsholtz. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res. 314: 15-23, 2003.
13. Hinsbergh, V. W. M., A. Collen, and P. Koolwijk. Role of fibrin matrix in angiogenesis. Ann. N. Y. Acad. Sci. 936: 426-437, 2001.
14. Holderfield, M. T., and C. C. W. Hughes. Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-β in vascular morphogenesis. Circ. Res. 102: 637-652, 2008.
15. Jain, R. K., P. Au, J. Tam, D. G. Duda, and D. Fukumura. Engineering vascularized tissue. Nat. Biotechnol. 23: 821-823, 2005.
16. Laschke, M. W., Y. Harder, M. Amon, I. Martin, J. Farhadi, A. Ring, et al. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes. Tissue Eng. 12: 2093-2104, 2006.
17. Lesman, A., M. Habib, O. Caspi, A. Gepstein, G. Arbel, S. Levenberg, et al. Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng. Part A 16: 115-125, 2010.
18. Liau, B., N. Christoforou, K. W. Leong, and N. Bursac. Pluripotent stem cell-derived cardiac tissues with advanced structure and function. Biomaterials 32: 9180-9187, 2011.
19. Lovett, M., K. Lee, A. Edwards, and D. Kaplan. Vascularization strategies for tissue engineering. Tissue Eng. Part B Rev. 15: 353-370, 2009.
20. Naito, H., I. Melnychenko, M. Didié, K. Schneiderbanger, P. Schubert, S. Rosenkranz, et al. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114: I72-I78, 2006.
21. Nehls, V., R. Herrmann, M. Huhnken, and A. Palmetshofer. Contact-dependent inhibition of angiogenesis by cardiac fibroblasts in three-dimensional fibrin gels in vitro: implications for microvascular network remodeling and coronary collateral formation. Cell Tissue Res. 293: 479-488, 1998.
22. Neofytou, E. A., E. Chang, B. Patlola, L. M. Joubert, J. Rajadas, S. S. Gambhir, et al. Adipose tissue-derived stem cells display a proangiogenic phenotype on 3D scaffolds. J. Biomed. Mater. Res. Part A 98: 383-393, 2001.
23. Noseda, M., and M. D. Schneider. Fibroblasts inform the heart: control of cardiomyocyte cycling and size by age-dependent paracrine signals. Dev. Cell 16: 161-162, 2009.
24. Otsu, K., S. Das, S. D. Houser, S. K. Quadri, S. Bhattacharya, and J. Bhattacharya. Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells. Blood 113: 4197-4205, 2009.
25. Pons, J., Y. Huang, J. Arakawa-Hoyt, D. Washko, J. Takagawa, J. Ye, et al. VEGF improves survival of mesenchymal stem cells in infarcted hearts. Biochem. Biophys. Res. Commun. 376: 419-422, 2008.
26. Rickles, F. R., S. Patierno, and P. M. Fernandez. Tissue factor, thrombin, and cancer. Chest 124: 58S-68S, 2003.
27. Seif-Naraghi, S. B., M. A. Salvatore, P. J. Schup-Magoffin, D. P. Hu, and K. L. Christman. Design and characterization of an injectable pericardial matrix gel: a potentially autologous scaffold for cardiac tissue engineering. Tissue Eng. Part A 16: 2017-2027, 2010.
28. Sekine, H., T. Shimizu, K. Hobo, S. Sekiya, J. Yang, M. Yamato, et al. Endothelial cell co-culture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118: S145-S152, 2008.
29. Szabó, A., and A. Czirók. The role of cell-cell adhesion in the formation of multicellular sprouts. Math. Model. Nat. Phenom. 5: 106, 2010.
30. Tilling, T., C. Engelbertz, S. Decker, D. Korte, S. Huwel, and H. Galla. Expression and adhesive properties of basement membrane proteins in cerebral capillary endothelial cell cultures. Cell Tissue Res. 310: 19-29, 2002.
31. Valarmathi, M., J. Davis, M. Yost, R. Goodwin, and J. Potts. A three-dimensional model of vasculogenesis. Biomaterials 30: 1098-1112, 2009.
32. Williams, C., S. L. Johnson, P. S. Robinson, and R. T. Tranquillo. Cell sourcing and culture conditions for fibrin-based valve constructs. Tissue Eng. Part A 12: 1489-1502, 2006.
33. Ye, K. Y., K. E. Sullivan, and L. D. Black. Encapsulation of cardiomyocytes in a fibrin hydrogel for cardiac tissue engineering. J. Vis. Exp. 55: 3251, 2011.
34. Zhao, L., and M. Eghbali-Webb. Release of pro- and anti-angiogenic factors by human cardiac fibroblasts: effects on DNA synthesis and protection under hypoxia in human endothelial cells. BBA Mol. Cell Res. 1538: 273-282, 2001.