Engineering microenvironments for embryonic stem cell differentiation to cardiomyocytes

Regenerative Medicine

Volumn 4, Issue 5, 2009, Pages 721-732

  Horton, Renita E ^a   Millman, Jeffrey R ^b   Colton, Clark K ^b   Auguste, Debra T ^a  

^a HARVARD UNIVERSITY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Bioreactor; Cardiomyocyte; Embryonic stem cell; Extracellular matrix; Induced pluripotent stem cell; Scaffold

Indexed keywords

ACTIVIN A; ASCORBIC ACID; AZACITIDINE; BONE MORPHOGENETIC PROTEIN; COLLAGEN; DIMETHYL SULFOXIDE; FIBRONECTIN; FIBRONECTIN RECEPTOR; KRUPPEL LIKE FACTOR 4; LAMININ 1; MOLECULAR SCAFFOLD; MYC PROTEIN; MYOCYTE ENHANCER FACTOR 2; NOTCH RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; POLYMER; RETINOIC ACID; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

BASEMENT MEMBRANE; BIOREACTOR; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; HYPOXIA; MATRIX ATTACHMENT REGION; MICROENVIRONMENT; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BIOMEDICAL ENGINEERING; BIOREACTORS; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL HYPOXIA; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX; HUMANS; MICE; MYOCYTES, CARDIAC;

EID: 70350776947     PISSN: 17460751     EISSN: None     Source Type: Journal    
DOI: 10.2217/rme.09.48     Document Type: Review

References (71)

1. Lloyd-Jones D, Adams R, Carnethon M et al.: Heart disease and stroke statistics - 2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 119(3), E21-E181 (2009).
2. Maltsev VA, Rohwedel J, Hescheler J, Wobus AM: Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech. Dev. 44(1), 41-50 (1993).
3. Kehat I, Khimovich L, Caspi O et al.: Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat. Biotechnol. 22(10), 1282-1289 (2004).
4. Xue T, Cho HC, Akar FG et al.: Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation 111(1), 11-20 (2005).
5. Laflamme MA, Chen KY, Naumova AV et al.: Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 25(9), 1015-1024 (2007).
6. Caulfield JB, Leinbach R, Gold H: The relationship of myocardial infarct size and prognosis. Circulation 53(Suppl. 3), 1141-1144 (1976).
7. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al.: Embryonic stem cell lines derived from human blastocysts. Science 282(5391), 1145-1147 (1998).
8. Baharvand H, Azarnia M, Parivar K, Ashtiani SK: The effect of extracellular matrix on embryonic stem cell-derived cardiomyocytes. J Mol. Cell. Cardiol. 38 (3), 495-503 (2005).
9. Hovatta O: Derivation of human embryonic stem cell lines, towards clinical quality. Reprod. Fertil. Dev. 18(8), 823-828 (2006).
10. Keller GM: In vitro differentiation of embryonic stem cells. Curr. Opin. Cell Biol. 7(6), 862-869 (1995).
11. Itskovitz-Eldor J, Schuldiner M, Karsenti D et al.: Differentiation of human embryonic stem cells into embryoid bodies comprising the three embryonic germ layers. Mol. Med. 6(2), 88-95 (2000).
12. Passier R, Oostwaard DW-V, Snapper J et al.: Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 23(6), 772-780 (2005).
13. Takahashi T, Lord B, Schulze PC et al.: Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 107(14), 1912-1916 (2003).
14. Ventura C, Maioli M: Opioid peptide gene expression primes cardiogcnesis in embryonal pluripotent stem cells. Circ. Res. 87(3), 189-194 (2000).
15. Yoon BS, Yoo SJ, Lee JE, You S, Lee HT, Yoon HS: Enhanced differentiation of human embryonic stem cells into cardiomyocytes by combining hanging drop culture and 5-azacytidine treatment. Differentiation 74(4), 149-159 (2006).
16. Wobus AM, Kaomei G, Shan J et al.: Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 29 (6), 1525-1539 (1997).
17. Chen Y, Amende I, Hampton TG et al.: Vascular endothelial growth factor promotes cardiomyocyte differentiation of embryonic stem cells. Am. J. Physiol. Heart Circ. Physiol. 291(4), H1653-H1658 (2006).
18. Sachinidis A, Fleischmann BK, Kolossov E, Wartenberg M, Sauer H, Hescheler J: Cardiac specific differentiation of mouse embryonic stem cells. Cardiovasc. Res. 58(2), 278-291 (2003).
19. Fukuda K, Yuasa S: Stem cells as a source of regenerative cardiomyocytes. Circ. Res. 98 (8), 1002-1013 (2006).
20. Behfar A, Zingman LV, Hodgson DM et al.: Stem cell differentiation requires a paracrine pathway in the heart. FASEB J. 16(12), 1558-1566 (2002).
21. Feng B, Ng JH, Heng JCD, Ng HH: Molecules that promote or enhance reprogramming of somatic cells to induced pluripotent stem cells. Cell Stem Cell 4(4), 301-312 (2009).
22. Narazaki G, Uosaki H, Teranishi M et al.: Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 118(5), 498-506 (2008).
23. Mauritz C, Schwanke K, Reppel M et al.: Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 118(5), 507-517 (2008).
24. Schenke-Layland K, Rhodes KE, Angelis E et al.: Reprogrammed mouse fibroblasts differentiate into cells of the cardiovascular and hematopoietic lineages. Stem Cells 26(6), 1537-1546 (2008).
25. Zhang J, Wilson GF, Soerens Ag et al.: Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ. Res. 104(4), E30-E41 (2009).
26. Battista S, Guarnieri D, Borselli C et al.: The effect of matrix composition of 3D constructs on embryonic stem cell differentiation. Biomaterials 26(31), 6194-6207 (2005).
27. Miyamoto S, Katz BZ, Lafrenie RM, Yamada KM: Fibronectin and integrins in cell adhesion, signaling, and morphogenesis. Ann. NY Acad. Sci. 857, 119-129 (1998).
28. Fujiwara H, Hayashi Y, Sanzen N et al.: Regulation of mesodermal differentiation of mouse embryonic stem cells by basement membranes. J. Biol. Chem. 282 (40), 29701-29711 (2007).
29. Kumar D, Sun B: Transforming growth factor-β2 enhances differentiation of cardiac myocytes from embryonic stem cells. Biochem. Biophys. Res. Commun. 332(1), 135-141 (2005).
30. Sachlos E, Auguste DT: Embryoid body morphology influences diffusive transport of inductive biochemicals: a strategy for stem cell differentiation. Biomaterials 29 (34), 4471-4480 (2008).
31. Vanwinkle WB, Snuggs MB, Buja LM: Cardiogel: a biosynthetic extracellular matrix for cardiomyocyte culture. In Vitro Cell. Dev. Biol. Anim. 32(8), 478-485 (1996).
32. Yan Q, Sage EH: Sparc, a matricellular glycoprotein with important biological functions. J. Histochem. Cytochem. 47(12), 1495-1506 (1999).
33. Stary M, Pasteiner W, Summer A, Hrdina A, Eger A, Weitzer G: Parietal endoderm secreted SPARC promotes early cardiomyogenesis in vitro. Exp. Cell Res. 310(2), 331-343 (2005).
34. Hrabchak C, Ringuette M, Woodhouse K: Recombinant mouse sparc promotes parietal endoderm differentiation and cardiomyogenesis in embryoid bodies. Biochem. Cell Biol. 86(6), 487-499 (2008).
35. Sugahara H, Kanakura Y, Furitsu T et al.: Induction of programmed cell death in human hematopoietic cell lines by fibronectin via its interaction with very late antigen 5. J. Exp. Med. 179(6), 1757-1766 (1994).
36. Park JS, Huang NF, Kurpinski KT, Patel S, Hsu S, Li S: Mechanobiology of mesenchymal stem cells and their use in cardiovascular repair. Front. Biosci. 12, 5098-5116 (2007).
37. Kutschka I, Chen IY, Kofidis T et al.: Collagen matrices enhance survival of transplanted ' cardiomyoblasts and contribute to functional improvement of ischemic rat hearts. Circulation 114(Suppl. 1), 1167-1173 (2006).
38. Hynes RO: Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 5, 32-40 (2007).
39. Xiang Z, Liao R, Kelly MS, Spector M: Collagen-GAG scaffolds grafted onto myocardial infarcts in a rat model: a delivery vehicle for mesenchymal stem cells. Tissue Eng. 12(9), 2467-2478 (2006).
40. Flanagan TC, Wilkins B, Black A, Jockenhoevel S, Smith TJ, Pandit AS: A collagen-glycosaminoglycan co-culture model for heart valve tissue engineering applications. Biomaterials 27(10), 2233-2246 (2006).
41. Guo XM, Zhao YS, Chang HX et al.: Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation 113(18), 2229-2237 (2006).
42. Passier R, Mummery C: Cardiomyocyte differentiation from embryonic and adult stem cells. Curr. Opin. Biotechnol. 16(5), 498-502 (2005).
43. Sato H, Takahashi M, Ise H et al.: Collagen synthesis is required for ascorbic acid-enhanced differentiation of mouse embryonic stem cells into cardiomyocytes. Biochem. Biophys. Res. Commun. 342(1), 107-112(2006).
44. Stupack DG, Cheresh DA: ECM remodeling regulates angiogenesis: endothelial integrins look for new ligands. Sci. STKE 2002 (119), PE7 (2002).
45. Jakobsson L, Domogatskaya A, Tryggvason K, Edgar D, Claesson-Welsh L: Laminin deposition is dispensable for vasculogénesis but regulates blood vessel diameter independent of flow. FASEB J. 22 (5), 1530-1539 (2008).
46. Malan D, Reppel M, Dobrowolski R et al.: Lack of laminin γ1 in embryonic stem cell-derived cardiomyocytes causes inhomogeneous electrical spreading despite intact differentiation and function. Stem Cells 27(1), 88-99 (2009).
47. Zhang WJ, Liu W, Cui L, Cao Y: Tissue engineering of blood vessel. J. Cell. Mol. Med. 11(5), 945-957 (2007).
48. Engler AJ, Carag-Krieger C, Johnson CP et al.: Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell. Sci. 121(22), 3794-3802 (2008).
49. Nair R, Shukla S, Mcdevitt TC: Acellular matrices derived from differentiating embryonic stem cells. J. Biomed. Mater. Res. A 87(4), 1075-1085 (2008).
50. Ngangan AV, Mcdevitt TC: Acellularization of embryoid bodies via physical disruption methods. Biomaterials 30(6), 1143-1149 (2009).
51. Ott HC, Matthiesen TS, Gob SK et al.: Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14(2), 213-221 (2008).
52. Bauwens CL, Raheem P, Niebruegge S et al.: Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26(9), 2300-2310 (2008).
53. Burridge PW, Anderson D, Priddle H et al.: Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells 25 (4), 929-938 (2007).
54. Dang SM, Gerecht-Nir S, Chen J, Itskovitz-Eldor J, Zandstra PW: Controlled, scalable embryonic stem cell differentiation culture. Stem Cells 22(3), 275-282 (2004).
55. Ng ES, Davis RP, Azzola L, Stanley EG, Elefanty AG: Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106(5), 1601-1603 (2005).
56. Karp JM, Yeh J, Eng G et al.: Controlling size, shape and homogeneity of embryoid bodies using poly(ethylene glycol) microwells. Lab Chip 7(6), 786-794 (2007).
57. Singhvi R, Kumar A, Lopez GP et al.: Engineering cell shape and function. Science 264(5159), 696-698 (1994).
58. Tan JL, Liu W, Nelson CM, Raghavan S, Chen CS: Simple approach to micropattern cells on common culture substrates by tuning substrate wettability. Tissue Eng. 10(5-6), 865-872 (2004).
59. Niebruegge S, Bauwens CL, Peerani R et al: Generation of human embryonic stem cell-derived mesoderm and cardiac cells using size-specified aggregates in an oxygen-controlled bioreactor. Biotechnol. Bioeng. 102(2), 493-507 (2009).
60. Discher DE, Mooney DJ, Zandstra PW: Growth factors, matrices, and forces combine and control stem cells. Science 324(5935), 1673-1677 (2009).
61. Cameron CM, Hu WS, Kaufman DS: Improved development of human embryonic stem cell-derived embryoid bodies by stirred vessel cultivation. Biotechnol. Bioeng. 94(5), 938-948 (2006).
62. Sargent CY, Berguig GY, Mcdevitt TC: Cardiomyogenic differentiation of embryoid bodies is promoted by rotary orbital suspension culture. Tissue Eng. Part A 15 (2), 331-342 (2009).
63. Lu S, Liu S, He W et al.: Bioreactor cultivation enhances NTEB formation and differentiation of NTES cells into cardiomyocytes. Cloning Stem Cells 10(3), 363-370 (2008).
64. Niebruegge S, Nehring A, Bar H, Schroeder M, Zweigerdt R, Lehmann J: Cardiomyocyte production in mass suspension culture: embryonic stem cells as a source for great amounts of functional cardiomyocytes. Tissue Eng. Part A 14(10), 1591-1601 (2008).
65. Zur Nieden NI, Cormier JT, Rancourt DE, Kallos MS: Embryonic stem cells remain highly pluripotent following long term expansion as aggregates in suspension bioreactors. J. Biotechnol. 129 (3), 421-432 (2007).
66. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12(2), 149-162 (1998).
67. Lee YM, Jeong CH, Koo SY et al.: Determination of hypoxic region by hypoxia marker in developing mduse embryos in vivo: a possible signal for vessel development. Dev. Dyn. 220(2), 175-186 (2001).
68. Bauwens C, Yin T, Dang S, Peerani R, Zandstra PW: Development of a perfusion fed bioreactor for embryonic stem cell-derived cardiomyocyte generation: oxygen-mediated enhancement of cardiomyocyte output. Biotechnol. Bioeng. 90 (4), 452-461 (2005).
69. Fromstein JD, Zandstra PW, Alperin C, Rockwood D, Rabolt JF, Woodhouse KA: Seeding bioreactor-produced embryonic stem cell-derived cardiomyocytes on different porous, degradable, polyurethane scaffolds reveals the effect of scaffold architecture on cell morphology. Tissue Eng. Part A 14 (3), 369-378 (2008).
70. Figallo E, Cannizzaro C, Gerecht S et al.: Micro-bioreactor array for controlling cellular microenvironments. Lab Chip 7(6), 710-719 (2007).
71. Kim L, Vahey MD, Lee HY, Voldman J: Microfluidic arrays for logarithmically perfused embryonic stem cell culture. Lab Chip 6(3), 394-406 (2006).