Platform technology for scalable assembly of instantaneously functional mosaic tissues

Science Advances

Volumn 1, Issue 7, 2015, Pages

  Zhang, Boyang ^a,b   Montgomery, Miles ^a,b   Davenport H, Locke ^a,b   Korolj, Anastasia ^a,b   Radisic, Milica ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; CUTTING; CYTOLOGY; ENDOTHELIAL CELLS; HISTOLOGY; TISSUE;

MATRIX DISSOLUTIONS; MATRIX REMODELING; MECHANICAL CUTTING; MULTIPLE CELL TYPES; PHYSICAL INTEGRITY; PLATFORM TECHNOLOGY; THREE DIMENSIONAL (3D) STRUCTURES; TOPOGRAPHICAL FEATURES;

SCAFFOLDS (BIOLOGY);

EID: 85040141461     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500423     Document Type: Article

References (54)

1. G. Macchiarelli, O. Ohtani, S. A. NottoI a, T. Stallone, A. Camboni, I. M. Prado, P. M. Motta, A micro-anatomical model of the distribution of myocardial endomysial collagen. Histol. Histopathol. 17,699-706 (2002).
2. P. J. Hanley, A. A. Young, I. J. LeGrice, S. G. Edgar, D. S. Loiselle, 3-Dimensional configuration of perimysial collagen fibres in rat cardiac muscle at resting and extended sarcomere lengths. J. Physiol. 517 (Pt. 3), 831-837 (1999).
3. J. W. Holmes, T. K. Borg, J. W. Covell, Structure and mechanics of healing myocardial infarcts. Anna. Rev. Biomed. Eng. 7, 223-253 (2005).
4. P. Camelliti, T. K. Borg, P. Kohl, Structural and functional characterisation of cardiac fibroblasts. Cardiovasc. Res. 65, 40-51 (2005).
5. P. Helm, M. F. Beg, M. I. Miller, R. L. Winslow, Measuring and mapping cardiac fiber and laminar architecture using diffusion tensor MR imaging. Ann. N. Y. Acad. Sci. 1047, 296-307 (2005).
6. M. Montgomery, B. Zhang, M. Radisic, Cardiac tissue vascularization: From angiogenesis to microfluidic blood vessels. J. Cardiovasc. Pharmacol. Ther. 19, 382-393 (2014).
7. M. E. Kolewe, H. Park, C. Gray, X. Ye, R. Langer, L. E. Freed, 3D structural patterns in scalable, elastomeric scaffolds guide engineered tissue architecture. Adv. Mater. 25, 4459-4465 (2013).
8. G. C. Engelmayr Jr., M. Cheng, C. J. Bettinger, J. T. Borenstein, R. Langer, L. E. Freed, Accordionlike honeycombs for tissue engineering of cardiac anisotropy. Nat. Mater. 7, 1003-1010 (2008).
9. M. E. Kolewe, H. Park, C. Gray, X. Ye, R. Langer, L. E. Freed, 3D structural patterns in scalable, elastomeric scaffolds guide engineered tissue architecture. Adv. Mater. 25, 4459-4465 (2013) .
10. W. L. Stoppel, D. Hu, I. J. Domian, D. L. Kaplan, L. D. Black III, Anisotropic silk biomaterials containing cardiac extracellular matrix for cardiac tissue engineering. Biomed. Mater. 10, 034105 (2015).
11. S. R. Shin, B. Aghaei-Ghareh-Bolagh, X. Gao, M. Nikkhah, S. M. Jung, A. Dolatshahi-Pirouz, S. B. Kim, S. M. Kim, M. R. Dokmeci, X. S. Tang, A. Khademhosseini, Layer-by-layer assembly of 3D tissue constructs with functionalized graphene. Adv. Funct. Mater. 24, 6136-6144 (2014) .
12. N. Thavandiran, N. Dubois, A. Mikryukov, S. Masse, B. Beca, C. A. Simmons, V. S. Deshpande, J. P. McGarry, C. S. Chen, K. Nanthakumar, G. M. Keller, M. Radisic, P. W. Zandstra, Design and formulation of functional pluripotent stem cell-derived cardiac microtissues. Proc. Natl. Acad. Sci. USA. 110, E4698-E4707 (2013).
13. M. Radisic, H. Park, H. Shing, T. Consi, F. J. Schoen, R. Langer, L. E. Freed, G. Vunjak-Novakovic, Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl. Acad. Sci. U.S.A. 101, 18129-18134 (2004).
14. N. K. Paschos, W. E. Brown, R. Eswaramoorthy, J. C. Hu, K. A. Athanasiou, Advances in tissue engineering through stem cell-based co-culture. J. Tissue Eng. Regen. Med. 9, 488-503 (2015).
15. T. Xu, W. Zhao, J.-M. Zhu, M. Z. Albanna, J. J. Yoo, A. Atala, Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials 34, 130-139 (2013).
16. L. Leng, A. McAllister, B. Zhang, M. Radisic, A. Gunther, Mosaic hydrogels: One-step formation of multiscale soft materials. Adv. Mater. 24, 3650-3658 (2012).
17. R. Derda, A. Laromaine, A. Mammoto, S. K. Tang, T. Mammoto, D. E. Ingber, G. M. Whitesides, Paper-supported 3D cell culture for tissue-based bioassays. Proc. Natl. Acad. Sci. U.S.A. 106, 18457-18462 (2009).
18. B. Mosadegh, B. E. Dabiri, M. R. Lockett, R. Derda, P. Campbell, K. K. Parker, G. M. Whitesides, Three-dimensional paper-based model for cardiac ischemia. Adv. Healthc. Mater. 3,1036-1043 (2014) .
19. R. T. Tran, P. Thevenot, D. Gyawali, J. C. Chiao, L. Tang, J. Yang, Synthesis and characterization of a biodegradable elastomer featuring a dual crosslinking mechanism. Soft Matter 6, 2449-2461 (2010).
20. C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, T. G. Reese, W. J. Kostis, A. Thiagalingam, P. Maurovich-Horvat, J. N. Ruskin, U. Hoffmann, M. P. Jackowski, D. E. Sosnovik, Fiber architecture in remodeled myocardium revealed with a quantitative diffusion CMRtractography framework and histological validation. J. Cardiovasc. Magn. Reson. 14, 70 (2012).
21. S. S. Nunes, J. W. Miklas, J. Liu, R. Aschar-Sobbi, Y. Xiao, B. Zhang, J. Jiang, S. Masse, M. Gagliardi, A. Hsieh, N. Thavandiran, M. A. Laflamme, K. Nanthakumar, G. J. Gross, P. H. Backx, G. Keller, M. Radisic, Biowire: A platform for maturation of human pluripotent stem cell-derived cardio-myocytes. Nat. Methods 10, 781-787 (2013).
22. V. H. Barocas, R. T. Tranquillo, An anisotropic biphasic theory of tissue-equivalent mechanics: The interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance. J. Biomech. Eng. 119, 137-145 (1997).
23. W. Bian, N. Badie, H. D. Himel IV, N. Bursac, Robust T-tubulation and maturation of cardio-myocytes using tissue-engineered epicardial mimetics. Biomaterials 35, 3819-3828 (2014).
24. A. M. Blakely, K. L. Manning, A. Tripathi, J. R. Morgan, Bio-pick, place, and perfuse: A new instrument for three-dimensional tissue engineering. Tissue Eng. Part C Methods 21, 737-746 (2015) .
25. X. Ye, L. Lu, M. E. Kolewe, K. Hearon, K. M. Fischer, J. Coppeta, L. E. Freed, Scalable units for building cardiac tissue. Adv. Mater. 26, 7202-7208 (2014).
26. S. F. Nagueh, G. Shah, Y. Wu, G. Torre-Amione, N. M. P. King, S. Lahmers, C. C. Witt, K. Becker, S. Labeit, H. L. Granzier, Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110, 155-162 (2004).
27. S. M. Weis, J. L. Emery, K. D. Becker, D. J. McBride Jr., J. H. Omens, A. D. McCulloch, Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (o/m). Ore. Res. 87, 663-669 (2000).
28. C. Coirault, J.-L. Samuel, D. Chemla, J.-C. Pourny, F. Lambert, F. Marotte, Y. Lecarpentier, Increased compliance in diaphragm muscle of the cardiomyopathic Syrian hamster. J. Appl. Physiol. 85, 1762-1769 (1998).
29. J. H. Omens, Stress and strain as regulators of myocardial growth. Prog. Biophys. Mol. Biol. 69, 559-572 (1998).
30. D. A. Narmoneva, R. Vukmirovic, M. E. Davis, R. D. Kamm, R. T. Lee, Endothelial cells promote cardiac myocyte survival and spatial reorganization: Implications for cardiac regeneration. Circulation 110, 962-968 (2004).
31. R. K. Iyer, D. Odedra, L. L. Chiu, G. Vunjak-Novakovic, M. Radisic, Vascular endothelial growth factor secretion by nonmyocytes modulates Connexin-43 levels in cardiac organoids. Tissue Eng. Part A 18, 1771-1783 (2012).
32. B. Korecky, C. M. Hai, K. Rakusan, Functional capillary density in normal and transplanted rat hearts. Can. J. Physiol. Pharmacol. 60, 23-32 (1982).
33. K. Rakusan, B. Korecky, The effect of growth and aging on functional capillary supply of the rat heart. Growth 46, 275-281 (1982).
34. S. Bhatia, U. Balis, M. Yarmush, M. Toner, Effect of cell-cell interactions in preservation of cellular phenotype: Cocultivation of hepatocytes and nonparenchymal cells. FASEB J. 13, 1883-1900 (1999).
35. R. K. Iyer, L. L. Y. Chiu, M. Radisic, Microfabricated poly(ethylene glycol) templates enable rapid screening of triculture conditions for cardiac tissue engineering. J. Biomed. Mater. Res. A 89A, 616-631 (2009).
36. M. D. Chamberlain, R. Gupta, M. V. Sefton, Chimeric vessel tissue engineering driven by endothelialized modules in immunosuppressed Sprague-Dawley rats. Tissue Eng. Part A 17, 151-160 (2011).
37. M. D. Chamberlain, R. Gupta, M. V. Sefton, Bone marrow-derived mesenchymal stromal cells enhance chimeric vessel development driven by endothelial cell-coated microtissues. Tissue Eng. Part A 18, 285-294 (2012).
38. W. Wu, R. A. Allen, Y. Wang, Fast-degrading elastomer enables rapid remodeling of a cell-free synthetic graft into a neoartery. Nat. Med. 18, 1148-1153 (2012).
39. H. Sekine, T. Shimizu, K. Hobo, S. Sekiya, J. Yang, M. Yamato, H. Kurosawa, E. Kobayashi, T. Okano, Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118, S145-S152 (2008) .
40. O. Caspi, A. Lesman, Y. Basevitch, A. Gepstein, G. Arbel, I. H. M. Habib, L. Gepstein, S. Levenberg, Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Ore. Res. 100, 263-272 (2007).
41. K. R. Stevens, K. L. Kreutziger, S. K. Dupras, F. S. Korte, M. Regnier, V. Muskheli, M. B. Nourse, K. Bendixen, H. Reinecke, C. E. Murry, Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc. Natl. Acad. Sci. USA. 106,16568-16573 (2009) .
42. R. J. Lee, A. Hinson, S. Helgerson, R. Bauernschmitt, H. N. Sabbah, Polymer-based restoration of left ventricular mechanics. Cell Transplant. 22, 529-533 (2013).
43. R. Hashizume, K. L. Fujimoto,Y. Hong,J. Guan, CToma, K.Tobita,W. R.Wagner, Biodegradable elastic patch plasty ameliorates left ventricular adverse remodeling after ischemia-reperfusion injury: A preclinical study of a porous polyurethane material in a porcine model. J. Thorac. Cardiovasc. Surg. 146, 391-399.e391 (2013).
44. G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, J. W. Holmes, Model-based design of mechanical therapies for myocardial infarction. J. Cardiovasc. Transl. Res. 4, 82-91 (2011).
45. G. M. Fomovsky, S. A. Clark, K. M. Parker, G. Ailawadi, J. W. Holmes, Anisotropic reinforcement of acute anteroapical infarcts improves pump function. Circ. Heart Fail. 5, 515-522 (2012).
46. B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, M. Radisic, Influence of substrate stiffness on the phenotype of heart cells. Biotechnol. Bioeng. 105, 1148-1160 (2010).
47. J. Yang, M. Yamato, T. Shimizu, H. Sekine, K. Ohashi, M. Kanzaki, T. Ohki, K. Nishida, T. Okano, Reconstruction of functional tissues with cell sheet engineering. Biomaterials 28, 5033-5043 (2007).
48. B. Zhang, J. V. Green, S. K. Murthy, M. Radisic, Label-free enrichment of functional cardio-myocytes using microfluidic deterministic lateral flow displacement. PLOS One 7, e37619 (2012).
49. M. S. Sacks, C. J. Chuong, Biaxial mechanical properties of passive right ventricular free wall myocardium. J. Biomech. Eng. 115, 202-205 (1993).
50. D. Rappaport, D. Adam, P. Lysyansky, S. Riesner, Assessment of myocardial regional strain and strain rate by tissue tracking in B-mode echocardiograms. Ultrasound Med. Biol. 32, 1181-1192 (2006).
51. C. J. Chuong, M. S. Sacks, G. Templeton, F. Schwiep, R. L. Johnson Jr., Regional deformation and contractile function in canine right ventricular free wall. Am. J. Physiol. 260, H1224-H1235 (1991).
52. R. Rezakhaniha, A. Agianniotis, J. T. C Schrauwen, A. Griffa, D. Sage, C V. C Bouten, F. N. van de Vosse, M. Unser, N. Stergiopulos, Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech. Model. Mechanobiol. 11,461-473 (2012).
53. J. W. Miklas, S. M. Dallabrida, L. A. Reis, N. Ismail, M. Rupnick, M. Radisic, QHREDGS enhances tube formation, metabolism and survival of endothelial cells in collagen-chitosan hydrogels. PLOS One 8, e72956 (2013).
54. P. Simpson, Stimulation of hypertrophy of cultured neonatal rat heart cells through an a-|-adrenergic receptor and induction of beating through an arand pradrenergic receptor interaction. Evidence for independent regulation of growth and beating. Circ. Res. 56,884-894 (1985).