Display options
Cite
Murphy SA, Chen EZ, Tung L, et al. Maturing heart muscle cells: Mechanisms and transcriptomic insights. Semin Cell Dev Biol. 2021;119:49-60doi: 10.1016/j.semcdb.2021.04.019.
Murphy, S. A., Chen, E. Z., Tung, L., Boheler, K. R., & Kwon, C. (2021). Maturing heart muscle cells: Mechanisms and transcriptomic insights. Seminars in cell & developmental biology, 11949-60. https://doi.org/10.1016/j.semcdb.2021.04.019
Murphy, Sean A, et al. "Maturing heart muscle cells: Mechanisms and transcriptomic insights." Seminars in cell & developmental biology vol. 119 (2021): 49-60. doi: https://doi.org/10.1016/j.semcdb.2021.04.019
Murphy SA, Chen EZ, Tung L, Boheler KR, Kwon C. Maturing heart muscle cells: Mechanisms and transcriptomic insights. Semin Cell Dev Biol. 2021 Nov;119:49-60. doi: 10.1016/j.semcdb.2021.04.019. Epub 2021 May 02. PMID: 33952430; PMCID: PMC8653577.
Copy Download .nbib Format: NLM
Share it on

Semin Cell Dev Biol. 2021 Nov;119:49-60. doi: 10.1016/j.semcdb.2021.04.019. Epub 2021 May 02.

Maturing heart muscle cells: Mechanisms and transcriptomic insights.

Seminars in cell & developmental biology

Sean A Murphy, Elaine Zhelan Chen, Leslie Tung, Kenneth R Boheler, Chulan Kwon

Affiliations

  1. Division of Cardiology, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Institute of Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Cellular and Molecular Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
  2. Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
  3. Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Electronic address: [email protected].
  4. Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Electronic address: [email protected].
  5. Division of Cardiology, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Institute of Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Cellular and Molecular Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Electronic address: [email protected].

PMID: 33952430 PMCID: PMC8653577 DOI: 10.1016/j.semcdb.2021.04.019

Abstract

Cardiomyocyte (CM) maturation is the transformation of differentiated fetal CMs into adult CMs that involves changes in morphology, cell function and metabolism, and the transcriptome. This process is, however, incomplete and ultimately arrested in pluripotent stem cell-derived CMs (PSC-CMs) in culture, which hinders their broad biomedical application. For this reason, enormous efforts are currently being made with the goal of generating mature PSC-CMs. In this review, we summarize key aspects of maturation observed in native CMs and discuss recent findings on the factors and mechanisms that regulate the process. Particular emphasis is put on transcriptional regulation and single-cell RNA-sequencing analysis that has emerged as a key tool to study time-series gene regulation and to determine the maturation state. We then discuss different biomimetic strategies to enhance PSC-CM maturation and discuss their effects at the single cell transcriptomic and functional levels.

Copyright © 2021 The Authors. Published by Elsevier Ltd.. All rights reserved.

Keywords: Cardiomyocyte maturation; Heart development; Maturation metrics; Pluripotent stem cells; Single-cell transcriptomics; Tissue engineering

References

  1. Development. 2015 Sep 15;142(18):3231-8 - PubMed
  2. Circ J. 2011;75(9):2071-9 - PubMed
  3. Life Sci. 2020 Aug 15;255:117817 - PubMed
  4. J Mol Cell Cardiol. 2013 Jul;60:36-46 - PubMed
  5. Cell Rep. 2015 Nov 24;13(8):1705-16 - PubMed
  6. Sci Rep. 2017 Aug 17;7(1):8590 - PubMed
  7. J Am Heart Assoc. 2017 Jul 24;6(7): - PubMed
  8. J Am Heart Assoc. 2018 Oct 16;7(20):e010378 - PubMed
  9. Am J Cardiovasc Dis. 2016 Sep 15;6(3):70-80 - PubMed
  10. Stem Cells Int. 2018 Jan 8;2018:6067096 - PubMed
  11. Sci Rep. 2020 Mar 6;10(1):4249 - PubMed
  12. Dev Cell. 2019 Oct 7;51(1):62-77.e5 - PubMed
  13. Circ Res. 2004 Mar 5;94(4):505-13 - PubMed
  14. Elife. 2016 Oct 11;5: - PubMed
  15. Dev Dyn. 1995 Dec;204(4):358-71 - PubMed
  16. Can J Physiol Pharmacol. 2017 Oct;95(10):1100-1107 - PubMed
  17. J Physiol. 2017 Aug 1;595(15):5129-5142 - PubMed
  18. Cell Stem Cell. 2013 Jan 3;12(1):127-37 - PubMed
  19. Nat Commun. 2021 Mar 12;12(1):1648 - PubMed
  20. Nat Rev Cardiol. 2020 Jun;17(6):341-359 - PubMed
  21. Histochemistry. 1983;77(4):485-94 - PubMed
  22. Anat Embryol (Berl). 2001 Sep;204(3):217-24 - PubMed
  23. Nat Clin Pract Cardiovasc Med. 2007 Feb;4 Suppl 1:S60-7 - PubMed
  24. Stem Cells. 2018 Aug;36(8):1198-1209 - PubMed
  25. Circ Res. 2020 Jun 5;126(12):1685-1702 - PubMed
  26. J Am Heart Assoc. 2020 Oct 20;9(20):e016528 - PubMed
  27. Circ Res. 1984 Jun;54(6):694-702 - PubMed
  28. J Membr Biol. 2007 Aug;218(1-3):13-28 - PubMed
  29. Cardiovasc Res. 1998 Feb;37(2):405-23 - PubMed
  30. Circ Res. 2020 Apr 10;126(8):1086-1106 - PubMed
  31. Cell Stem Cell. 2018 Oct 4;23(4):586-598.e8 - PubMed
  32. Aging (Albany NY). 2020 Apr 28;12(8):7411-7430 - PubMed
  33. J Mol Cell Cardiol. 2014 Jul;72:296-304 - PubMed
  34. Antioxid Redox Signal. 2014 Nov 10;21(14):2018-31 - PubMed
  35. Cell Stem Cell. 2011 Feb 4;8(2):228-40 - PubMed
  36. Cell Stem Cell. 2016 Jul 7;19(1):95-106 - PubMed
  37. Stem Cell Reports. 2017 Feb 14;8(2):278-289 - PubMed
  38. Stem Cells Dev. 2019 May 15;28(10):659-673 - PubMed
  39. PLoS Comput Biol. 2021 Sep 17;17(9):e1009305 - PubMed
  40. Nature. 2011 May 19;473(7347):326-35 - PubMed
  41. Semin Perinatol. 1996 Dec;20(6):482-509 - PubMed
  42. Mol Ther. 2018 Jul 5;26(7):1599-1609 - PubMed
  43. J Cardiovasc Pharmacol. 2010 Aug;56(2):130-40 - PubMed
  44. Nat Methods. 2017 Oct;14(10):979-982 - PubMed
  45. Circ Res. 2019 Jun 21;125(1):90-103 - PubMed
  46. Cell Stem Cell. 2020 Jun 4;26(6):862-879.e11 - PubMed
  47. Stem Cells. 2006 Aug;24(8):1956-67 - PubMed
  48. PLoS One. 2013 Oct 21;8(10):e77784 - PubMed
  49. Mol Cell Biochem. 1998 Nov;188(1-2):49-56 - PubMed
  50. Circ Res. 2017 Dec 8;121(12):1323-1330 - PubMed
  51. Genes Dev. 2018 Oct 1;32(19-20):1344-1357 - PubMed
  52. Circ Res. 2017 Jun 9;120(12):1874-1888 - PubMed
  53. Cell Death Differ. 2015 Jul;22(7):1106-16 - PubMed
  54. Circ Res. 2018 Oct 12;123(9):1066-1079 - PubMed
  55. Nat Commun. 2014 Mar 04;5:3416 - PubMed
  56. Proc Natl Acad Sci U S A. 2015 May 26;112(21):E2785-94 - PubMed
  57. Stem Cell Rev Rep. 2011 Nov;7(4):976-86 - PubMed
  58. Dev Cell. 2016 Nov 21;39(4):480-490 - PubMed
  59. Circ Res. 2003 Jun 13;92(11):1182-92 - PubMed
  60. Clin Transplant. 2019 Jun;33(6):e13573 - PubMed
  61. Stem Cell Reports. 2019 Oct 8;13(4):657-668 - PubMed
  62. Stem Cells Dev. 2015 May 1;24(9):1035-52 - PubMed
  63. PLoS One. 2008;3(10):e3474 - PubMed
  64. Dev Biol. 2006 Jan 15;289(2):430-41 - PubMed
  65. Nat Commun. 2018 Aug 7;9(1):3140 - PubMed
  66. Circ Res. 2014 Jan 31;114(3):511-23 - PubMed
  67. Am J Physiol Heart Circ Physiol. 2001 Apr;280(4):H1814-20 - PubMed
  68. Pharmacol Rev. 2020 Jan;72(1):320-342 - PubMed
  69. Proc Natl Acad Sci U S A. 2017 Oct 3;114(40):E8372-E8381 - PubMed
  70. EMBO J. 1998 Jun 15;17(12):3309-16 - PubMed
  71. Cell Rep. 2017 Jan 10;18(2):571-582 - PubMed
  72. J Mol Cell Cardiol. 2015 Apr;81:81-93 - PubMed
  73. Pharmacol Ther. 2018 Mar;183:127-136 - PubMed
  74. Stem Cell Res Ther. 2014 Jan 28;5(1):17 - PubMed
  75. Dev Biol. 1993 Mar;156(1):253-64 - PubMed
  76. J Biol Chem. 1994 Jun 17;269(24):16961-70 - PubMed
  77. Front Pharmacol. 2013 Jun 27;4:81 - PubMed
  78. J Mol Cell Cardiol. 1992 Sep;24(9):949-65 - PubMed
  79. Circ Res. 2018 Jul 6;123(2):224-243 - PubMed
  80. Front Physiol. 2013 May 10;4:102 - PubMed
  81. Biomaterials. 2015 Aug;60:82-91 - PubMed
  82. PLoS One. 2012;7(10):e46413 - PubMed
  83. Nat Protoc. 2017 Oct;12(10):2097-2109 - PubMed
  84. Pediatr Cardiol. 2009 Jul;30(5):588-96 - PubMed
  85. Cell Res. 2020 Jul;30(7):626-629 - PubMed
  86. Circulation. 2020 Jan 28;141(4):285-300 - PubMed
  87. Cardiovasc Res. 2001 Aug 1;51(2):217-29 - PubMed
  88. Circ Res. 2019 Aug 16;125(5):567-569 - PubMed
  89. Nat Biotechnol. 2020 Jun;38(6):737-746 - PubMed
  90. Stem Cell Reports. 2014 Oct 14;3(4):594-605 - PubMed
  91. Nat Commun. 2017 Feb 17;8:14495 - PubMed
  92. Anat Rec. 1994 Feb;238(2):199-206 - PubMed
  93. Cell Stem Cell. 2017 Aug 3;21(2):179-194.e4 - PubMed
  94. J Physiol. 2020 Jul;598(14):2941-2956 - PubMed
  95. J Mol Cell Cardiol. 2015 Aug;85:79-88 - PubMed
  96. Stem Cells. 2008 Jul;26(7):1831-40 - PubMed
  97. Cell. 2007 Nov 30;131(5):861-72 - PubMed
  98. PLoS One. 2011;6(8):e23657 - PubMed
  99. Sci Transl Med. 2016 Jun 8;8(342):342ps13 - PubMed
  100. Exp Mol Med. 2018 Aug 7;50(8):1-14 - PubMed
  101. Nat Commun. 2020 May 22;11(1):2585 - PubMed
  102. J Mol Cell Cardiol. 2020 Dec;149:115-122 - PubMed
  103. Proc Natl Acad Sci U S A. 2021 Jan 12;118(2): - PubMed
  104. J Mol Cell Cardiol. 2010 Apr;48(4):725-34 - PubMed
  105. Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2111-6 - PubMed
  106. Cell Stem Cell. 2011 Apr 8;8(4):376-88 - PubMed
  107. Eur Heart J. 1984 Dec;5 Suppl F:181-91 - PubMed
  108. J Tissue Eng Regen Med. 2021 May;15(5):503-512 - PubMed
  109. Int J Mol Sci. 2019 Aug 03;20(15): - PubMed
  110. Stem Cell Reports. 2019 May 14;12(5):967-981 - PubMed
  111. Nature. 2020 Jun;582(7811):271-276 - PubMed
  112. Cell Stem Cell. 2020 Jul 2;27(1):50-63.e5 - PubMed
  113. Prog Biophys Mol Biol. 2012 Oct-Nov;110(2-3):178-95 - PubMed
  114. J Physiol. 2020 Jul;598(14):2909-2922 - PubMed
  115. J Pharmacol Toxicol Methods. 2018 Mar - Apr;90:19-30 - PubMed
  116. Nat Med. 2016 May;22(5):547-56 - PubMed
  117. FASEB J. 2012 Jan;26(1):397-408 - PubMed
  118. Nature. 2002 Jan 10;415(6868):198-205 - PubMed
  119. Circ Cardiovasc Genet. 2013 Dec;6(6):624-33 - PubMed
  120. Circ Res. 2017 Jul 7;121(2):181-195 - PubMed
  121. Cardiovasc Res. 2004 Nov 1;64(2):198-207 - PubMed
  122. Nat Commun. 2017 Nov 28;8(1):1825 - PubMed
  123. Circulation. 1994 Aug;90(2):713-25 - PubMed
  124. Cardiovasc Res. 2018 May 1;114(6):894-906 - PubMed
  125. Cell Rep. 2015 Sep 29;12(12):1960-7 - PubMed
  126. Science. 2007 Dec 21;318(5858):1917-20 - PubMed
  127. Elife. 2017 Dec 12;6: - PubMed
  128. Int J Mol Sci. 2019 Sep 06;20(18): - PubMed
  129. Nat Commun. 2018 Sep 21;9(1):3837 - PubMed

Publication Types

Grant support