Display options
Share it on

Trends Cell Biol. 2017 May;27(5):352-364. doi: 10.1016/j.tcb.2016.11.010. Epub 2016 Dec 19.

Recreating the Cardiac Microenvironment in Pluripotent Stem Cell Models of Human Physiology and Disease.

Trends in cell biology

Ayhan Atmanli, Ibrahim John Domian

Affiliations

  1. Cardiovascular Research Center, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USA; Department of Biomedical Engineering, Tufts University, Medford, MA, USA.
  2. Cardiovascular Research Center, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USA; Harvard Stem Cell Institute, Cambridge, MA, USA. Electronic address: [email protected].

PMID: 28007424 PMCID: PMC5403626 DOI: 10.1016/j.tcb.2016.11.010

Abstract

The advent of human pluripotent stem cell (hPSC) biology has opened unprecedented opportunities for the use of tissue engineering to generate human cardiac tissue for in vitro study. Engineering cardiac constructs that recapitulate human development and disease requires faithful recreation of the cardiac niche in vitro. Here we discuss recent progress in translating the in vivo cardiac microenvironment into PSC models of the human heart. We review three key physiologic features required to recreate the cardiac niche and facilitate normal cardiac differentiation and maturation: the biochemical, biophysical, and bioelectrical signaling cues. Finally, we discuss key barriers that must be overcome to fulfill the promise of stem cell biology in preclinical applications and ultimately in clinical practice.

Copyright © 2016 Elsevier Ltd. All rights reserved.

Keywords: cardiac myocytes; cardiac niche; cellular microenvironment; disease modeling; pluripotent stem cells; tissue engineering

References

  1. J Clin Invest. 2001 Aug;108(3):407-14 - PubMed
  2. J Clin Invest. 1975 Jul;56(1):56-64 - PubMed
  3. J Cell Sci. 2003 Mar 1;116(Pt 5):875-85 - PubMed
  4. Circulation. 2003 Jun 3;107(21):2733-40 - PubMed
  5. Dev Biol. 2003 Jun 1;258(1):1-19 - PubMed
  6. Am J Physiol Heart Circ Physiol. 2004 Feb;286(2):H507-16 - PubMed
  7. Circ Res. 2004 Mar 19;94(5):642-9 - PubMed
  8. J Cell Biol. 1992 Sep;118(6):1411-20 - PubMed
  9. Circ Res. 2004 Oct 1;95(7):708-16 - PubMed
  10. J Am Coll Cardiol. 1992 Mar 1;19(3):619-29 - PubMed
  11. Proc Natl Acad Sci U S A. 2004 Dec 28;101(52):18129-34 - PubMed
  12. Stem Cells. 2005 Feb;23(2):288-96 - PubMed
  13. Stem Cells. 2005 Jun-Jul;23(6):772-80 - PubMed
  14. Nat Med. 2006 Apr;12(4):452-8 - PubMed
  15. Circulation. 2006 Jul 4;114(1 Suppl):I72-8 - PubMed
  16. Cell. 2006 Aug 25;126(4):677-89 - PubMed
  17. Acta Biomater. 2007 Jan;3(1):33-41 - PubMed
  18. Cell. 2006 Dec 15;127(6):1137-50 - PubMed
  19. Stem Cells. 2007 Apr;25(4):929-38 - PubMed
  20. Stem Cells. 2007 May;25(5):1136-44 - PubMed
  21. Cardiovasc Res. 2008 Mar 1;77(4):637-48 - PubMed
  22. Biomaterials. 2007 Oct;28(29):4277-93 - PubMed
  23. Nat Biotechnol. 2007 Sep;25(9):1015-24 - PubMed
  24. Science. 2007 Sep 7;317(5843):1366-70 - PubMed
  25. Nat Med. 2008 Feb;14(2):213-21 - PubMed
  26. Nature. 2008 May 22;453(7194):524-8 - PubMed
  27. Mol Cell Biochem. 2008 Jul;314(1-2):179-91 - PubMed
  28. Biochem Biophys Res Commun. 2008 Aug 8;372(4):553-8 - PubMed
  29. Circ Res. 1991 Sep;69(3):722-30 - PubMed
  30. Tissue Eng Part A. 2011 Jun;17(11-12):1465-77 - PubMed
  31. J Cell Sci. 2008 Nov 15;121(Pt 22):3794-802 - PubMed
  32. Circ Res. 2009 Feb 27;104(4):e30-41 - PubMed
  33. J Am Assoc Lab Anim Sci. 2009 Jan;48(1):23-7 - PubMed
  34. Tissue Eng Part A. 2009 Oct;15(10):3099-108 - PubMed
  35. Science. 2009 Apr 3;324(5923):98-102 - PubMed
  36. Proc Natl Acad Sci U S A. 2009 Jun 23;106(25):10097-102 - PubMed
  37. Eur Phys J E Soft Matter. 2009 Oct;30(2):175-9 - PubMed
  38. Nature. 2009 Jul 2;460(7251):113-7 - PubMed
  39. Tissue Eng Part B Rev. 2010 Apr;16(2):169-87 - PubMed
  40. Science. 2009 Oct 16;326(5951):426-9 - PubMed
  41. Nat Methods. 2010 Jan;7(1):61-6 - PubMed
  42. Science. 2009 Nov 27;326(5957):1216-9 - PubMed
  43. Biotechnol Bioeng. 2010 Apr 15;105(6):1148-60 - PubMed
  44. Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):565-70 - PubMed
  45. Biomaterials. 2010 May;31(13):3613-21 - PubMed
  46. Proteomics. 2010 May;10(9):1886-90 - PubMed
  47. Biointerphases. 2009 Dec;4(4):69-79 - PubMed
  48. J Phys Condens Matter. 2010 May 19;22(19):194116 - PubMed
  49. Circ Res. 2010 Sep 17;107(6):776-86 - PubMed
  50. Circulation. 2010 Sep 7;122(10):993-1003 - PubMed
  51. Physiol Genomics. 2010 Nov 29;42A(4):283-9 - PubMed
  52. Cell Res. 2011 Apr;21(4):579-87 - PubMed
  53. J Cell Sci. 2010 Dec 15;123(Pt 24):4195-200 - PubMed
  54. Eur J Heart Fail. 2011 Jan;13(1):1-10 - PubMed
  55. Cell Stem Cell. 2011 Feb 4;8(2):228-40 - PubMed
  56. Nature. 2011 Mar 10;471(7337):230-4 - PubMed
  57. PLoS One. 2011 Apr 08;6(4):e18293 - PubMed
  58. Biomaterials. 2011 Aug;32(24):5625-32 - PubMed
  59. Int J Biol Sci. 2011;7(6):708-14 - PubMed
  60. Nat Nanotechnol. 2011 Sep 25;6(11):720-5 - PubMed
  61. Cells Tissues Organs. 2012;195(1-2):82-93 - PubMed
  62. Nat Methods. 2011 Oct 23;8(12):1037-40 - PubMed
  63. Tissue Eng Part A. 2012 May;18(9-10):910-9 - PubMed
  64. PLoS One. 2011;6(11):e27417 - PubMed
  65. Circ Res. 2012 Feb 17;110(4):609-23 - PubMed
  66. Biomaterials. 2012 Aug;33(23):5732-41 - PubMed
  67. Proc Natl Acad Sci U S A. 2012 Jul 3;109(27):E1848-57 - PubMed
  68. Circulation. 2012 Jun 26;125(25):3079-91 - PubMed
  69. Circ Res. 2012 Jul 20;111(3):344-58 - PubMed
  70. Toxicol Sci. 2012 Nov;130(1):117-31 - PubMed
  71. Cell. 2012 Sep 28;151(1):206-20 - PubMed
  72. PLoS One. 2012;7(9):e45963 - PubMed
  73. Cell Stem Cell. 2013 Jan 3;12(1):127-37 - PubMed
  74. Nature. 2013 Jan 17;493(7432):433-6 - PubMed
  75. Biomaterials. 2013 Mar;34(10):2399-411 - PubMed
  76. Cell Stem Cell. 2013 Jan 3;12(1):101-13 - PubMed
  77. PLoS One. 2012;7(12):e52405 - PubMed
  78. Nat Med. 2013 Feb;19(2):193-201 - PubMed
  79. Cell. 2013 Jan 31;152(3):570-83 - PubMed
  80. Nature. 2013 Feb 7;494(7435):105-10 - PubMed
  81. Circ Res. 2013 Feb 1;112(3):534-48 - PubMed
  82. Circ Arrhythm Electrophysiol. 2013 Feb;6(1):191-201 - PubMed
  83. Circulation. 2013 Apr 23;127(16):1677-91 - PubMed
  84. J Vis Exp. 2013 Mar 19;(73):e50288 - PubMed
  85. Biomaterials. 2013 Jul;34(23):5813-20 - PubMed
  86. PeerJ. 2013 Jun 04;1:e82 - PubMed
  87. Nat Methods. 2013 Aug;10(8):781-7 - PubMed
  88. Acta Biomater. 2014 Jan;10(1):194-204 - PubMed
  89. Development. 2013 Oct;140(20):4165-76 - PubMed
  90. Acta Biomater. 2014 Feb;10(2):604-12 - PubMed
  91. Proc Natl Acad Sci U S A. 2013 Dec 3;110(49):E4698-707 - PubMed
  92. Proc Natl Acad Sci U S A. 2013 Dec 24;110(52):20923-8 - PubMed
  93. Stem Cell Reports. 2014 Feb 06;2(2):163-70 - PubMed
  94. Circulation. 2014 Apr 8;129(14):1483-92 - PubMed
  95. Adv Healthc Mater. 2014 Jul;3(7):1036-43 - PubMed
  96. Circ Res. 2014 Feb 28;114(5):916-27 - PubMed
  97. J Biomech Eng. 2014 May;136(5):051005 - PubMed
  98. Am J Physiol Heart Circ Physiol. 2014 Jun 1;306(11):H1525-39 - PubMed
  99. Proc Natl Acad Sci U S A. 2014 Apr 15;111(15):5580-5 - PubMed
  100. Biomaterials. 2014 Jul;35(21):5462-71 - PubMed
  101. Adv Healthc Mater. 2014 Nov;3(11):1759-64 - PubMed
  102. Nat Med. 2014 Jun;20(6):616-23 - PubMed
  103. Nat Commun. 2014 Jun 02;5:3935 - PubMed
  104. Nat Methods. 2014 Aug;11(8):855-60 - PubMed
  105. Circ Res. 2014 Aug 29;115(6):556-66 - PubMed
  106. Nat Biotechnol. 2014 Aug;32(8):773-85 - PubMed
  107. Nat Biotechnol. 2014 Oct;32(10):1026-35 - PubMed
  108. Sci Transl Med. 2014 Sep 24;6(255):255ra130 - PubMed
  109. Sci Rep. 2014 Oct 22;4:6716 - PubMed
  110. Stem Cell Reports. 2014 Oct 14;3(4):594-605 - PubMed
  111. Front Physiol. 2014 Oct 21;5:408 - PubMed
  112. Cell Rep. 2014 Nov 6;9(3):810-21 - PubMed
  113. Biochim Biophys Acta. 2015 Jan;1852(1):1-11 - PubMed
  114. Stem Cell Reports. 2015 Mar 10;4(3):340-7 - PubMed
  115. Biomaterials. 2015 May;51:138-150 - PubMed
  116. PLoS Comput Biol. 2015 Apr 07;11(4):e1004190 - PubMed
  117. Stem Cells. 2015 Jul;33(7):2148-57 - PubMed
  118. Biomaterials. 2015 Aug;60:82-91 - PubMed
  119. Nat Methods. 2015 Jul;12(7):595-6 - PubMed
  120. Biomaterials. 2015 Oct;67:52-64 - PubMed
  121. Stem Cell Reports. 2015 Oct 13;5(4):582-96 - PubMed
  122. Proc Natl Acad Sci U S A. 2015 Oct 13;112(41):12705-10 - PubMed
  123. Nat Commun. 2015 Oct 08;6:8526 - PubMed
  124. Circ Res. 2016 Jan 8;118(1):56-72 - PubMed
  125. Stem Cell Reports. 2015 Dec 8;5(6):1226-1238 - PubMed
  126. Cell Stem Cell. 2016 Mar 3;18(3):341-53 - PubMed
  127. Nat Commun. 2016 Jan 19;7:10312 - PubMed
  128. ACS Appl Mater Interfaces. 2016 Aug 31;8(34):21923-32 - PubMed
  129. Cell Rep. 2016 Feb 23;14(7):1662-1672 - PubMed
  130. J Pharmacol Toxicol Methods. 2016 Sep-Oct;81:240-50 - PubMed
  131. Science. 2016 Jul 8;353(6295):158-62 - PubMed
  132. J Bioeng Biomed Sci. 2015 Nov;5(3): - PubMed
  133. Cell Tissue Res. 1987 Aug;249(2):247-55 - PubMed
  134. Circ Res. 1994 Jun;74(6):1065-70 - PubMed
  135. FASEB J. 1997 Jul;11(8):683-94 - PubMed

MeSH terms

Publication Types

Grant support