Highly Efficient Derivation of Ventricular Cardiomyocytes from Induced Pluripotent Stem Cells with a Distinct Epigenetic Signature

Overview

Journal Cell Res

Specialty Cell Biology

Date 2011 Nov 9

PMID 22064699

Citations 36

Authors

Huansheng Xu

B Alexander Yi

Hao Wu

Christoph Bock

Hongcang Gu

Kathy O Lui

Joo-Hye C Park

Ying Shao

Alyssa K Riley

Ibrahim J Domian

Erding Hu

Robert Willette

John Lepore

Alexander Meissner

Zhong Wang

Kenneth R Chien

Affiliations

Soon will be listed here.

Abstract

Cardiomyocytes derived from pluripotent stem cells can be applied in drug testing, disease modeling and cell-based therapy. However, without procardiogenic growth factors, the efficiency of cardiomyogenesis from pluripotent stem cells is usually low and the resulting cardiomyocyte population is heterogeneous. Here, we demonstrate that induced pluripotent stem cells (iPSCs) can be derived from murine ventricular myocytes (VMs), and consistent with other reports of iPSCs derived from various somatic cell types, VM-derived iPSCs (ViPSCs) exhibit a markedly higher propensity to spontaneously differentiate into beating cardiomyocytes as compared to genetically matched embryonic stem cells (ESCs) or iPSCs derived from tail-tip fibroblasts. Strikingly, the majority of ViPSC-derived cardiomyocytes display a ventricular phenotype. The enhanced ventricular myogenesis in ViPSCs is mediated via increased numbers of cardiovascular progenitors at early stages of differentiation. In order to investigate the mechanism of enhanced ventricular myogenesis from ViPSCs, we performed global gene expression and DNA methylation analysis, which revealed a distinct epigenetic signature that may be involved in specifying the VM fate in pluripotent stem cells.

Citing Articles

Advances in Genetic Reprogramming: Prospects from Developmental Biology to Regenerative Medicine.

Dhanjal D, Singh R, Sharma V, Nepovimova E, Adam V, Kuca K Curr Med Chem. 2023; 31(13):1646-1690.

PMID: 37138422 DOI: 10.2174/0929867330666230503144619.

Harshening stem cell research and precision medicine: The states of human pluripotent cells stem cell repository diversity, and racial and sex differences in transcriptomes.

Nguyen T, Lac Q, Abdi L, Banerjee D, Deng Y, Zhang Y Front Cell Dev Biol. 2023; 10:1071243.

PMID: 36684445 PMC: 9848738. DOI: 10.3389/fcell.2022.1071243.

Advances in Manufacturing Cardiomyocytes from Human Pluripotent Stem Cells.

Floy M, Shabnam F, Simmons A, Bhute V, Jin G, Friedrich W Annu Rev Chem Biomol Eng. 2022; 13:255-278.

PMID: 35320695 PMC: 9197878. DOI: 10.1146/annurev-chembioeng-092120-033922.

Transient reprogramming of postnatal cardiomyocytes to a dedifferentiated state.

Kisby T, de Lazaro I, Stylianou M, Cossu G, Kostarelos K PLoS One. 2021; 16(5):e0251054.

PMID: 33951105 PMC: 8099115. DOI: 10.1371/journal.pone.0251054.

Induced pluripotent stem cells derived from the developing striatum as a potential donor source for cell replacement therapy for Huntington disease.

Choompoo N, Bartley O, Precious S, Vinh N, Schnell C, Garcia A Cytotherapy. 2020; 23(2):111-118.

PMID: 33246883 PMC: 7822401. DOI: 10.1016/j.jcyt.2020.06.001.

References

Chen J, Kubalak S, Minamisawa S, Price R, Becker K, Hickey R . Selective requirement of myosin light chain 2v in embryonic heart function. J Biol Chem. 1998; 273(2):1252-6. DOI: 10.1074/jbc.273.2.1252. View

Ng S, Wong C, Tsang S . Differential gene expressions in atrial and ventricular myocytes: insights into the road of applying embryonic stem cell-derived cardiomyocytes for future therapies. Am J Physiol Cell Physiol. 2010; 299(6):C1234-49. DOI: 10.1152/ajpcell.00402.2009. View

Gu H, Bock C, Mikkelsen T, Jager N, Smith Z, Tomazou E . Genome-scale DNA methylation mapping of clinical samples at single-nucleotide resolution. Nat Methods. 2010; 7(2):133-6. PMC: 2860480. DOI: 10.1038/nmeth.1414. View

Laugwitz K, Moretti A, Caron L, Nakano A, Chien K . Islet1 cardiovascular progenitors: a single source for heart lineages?. Development. 2007; 135(2):193-205. DOI: 10.1242/dev.001883. View

Ieda M, Fu J, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau B . Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell. 2010; 142(3):375-86. PMC: 2919844. DOI: 10.1016/j.cell.2010.07.002. View

Li H, Ruan J, Durbin R . Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 2008; 18(11):1851-8. PMC: 2577856. DOI: 10.1101/gr.078212.108. View

Laflamme M, Chen K, Naumova A, Muskheli V, Fugate J, Dupras S . Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol. 2007; 25(9):1015-24. DOI: 10.1038/nbt1327. View

Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P . Epigenetic memory in induced pluripotent stem cells. Nature. 2010; 467(7313):285-90. PMC: 3150836. DOI: 10.1038/nature09342. View

Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R . Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation. 2003; 107(21):2733-40. DOI: 10.1161/01.CIR.0000068356.38592.68. View

10.

Polo J, Liu S, Figueroa M, Kulalert W, Eminli S, Tan K . Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol. 2010; 28(8):848-55. PMC: 3148605. DOI: 10.1038/nbt.1667. View

11.

Moore J, Fu J, Chan Y, Lin D, Tran H, Tse H . Distinct cardiogenic preferences of two human embryonic stem cell (hESC) lines are imprinted in their proteomes in the pluripotent state. Biochem Biophys Res Commun. 2008; 372(4):553-8. PMC: 2665880. DOI: 10.1016/j.bbrc.2008.05.076. View

12.

Palacios D, Puri P . The epigenetic network regulating muscle development and regeneration. J Cell Physiol. 2005; 207(1):1-11. DOI: 10.1002/jcp.20489. View

13.

Epstein J . Franklin H. Epstein Lecture. Cardiac development and implications for heart disease. N Engl J Med. 2010; 363(17):1638-47. DOI: 10.1056/NEJMra1003941. View

14.

Qyang Y, Martin-Puig S, Chiravuri M, Chen S, Xu H, Bu L . The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell. 2008; 1(2):165-79. DOI: 10.1016/j.stem.2007.05.018. View

15.

Narazaki G, Uosaki H, Teranishi M, Okita K, Kim B, Matsuoka S . Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation. 2008; 118(5):498-506. DOI: 10.1161/CIRCULATIONAHA.108.769562. View

16.

Laflamme M, Murry C . Regenerating the heart. Nat Biotechnol. 2005; 23(7):845-56. DOI: 10.1038/nbt1117. View

17.

Wernig M, Lengner C, Hanna J, Lodato M, Steine E, Foreman R . A drug-inducible transgenic system for direct reprogramming of multiple somatic cell types. Nat Biotechnol. 2008; 26(8):916-24. PMC: 2654269. DOI: 10.1038/nbt1483. View

18.

Ohi Y, Qin H, Hong C, Blouin L, Polo J, Guo T . Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat Cell Biol. 2011; 13(5):541-9. PMC: 3987913. DOI: 10.1038/ncb2239. View

19.

Fijnvandraat A, Lekanne Deprez R, Moorman A . Development of heart muscle-cell diversity: a help or a hindrance for phenotyping embryonic stem cell-derived cardiomyocytes. Cardiovasc Res. 2003; 58(2):303-12. DOI: 10.1016/s0008-6363(03)00246-3. View

20.

He J, Ma Y, Lee Y, Thomson J, Kamp T . Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res. 2003; 93(1):32-9. DOI: 10.1161/01.RES.0000080317.92718.99. View