Twenty one years of P19 cells: What an embryonal carcinoma cell line taught us about cardiomyocyte differentiation

Cardiovascular Research

Volumn 58, Issue 2, 2003, Pages 292-302

  Van Der Heyden, Marcel A G ^a   Defize, Libert H K ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b HUBRECHT INSTITUTE   (Netherlands)

Author keywords

Cell culture isolation; Developmental biology; Gene expression; Signal transduction; Stem cells

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR GATA 4;

CARCINOMA CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL LINE; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; EMBRYONAL CARCINOMA; GERM LAYER; HEART MUSCLE CELL; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TERATOCARCINOMA;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CARCINOMA, EMBRYONAL; CELL DIFFERENTIATION; CELL MEMBRANE; ELECTROPHYSIOLOGY; HEART; MICE; MYOCARDIAL CONTRACTION; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED; TUMOR STEM CELLS; WNT PROTEINS; ZEBRAFISH PROTEINS;

EID: 0038030931     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(02)00771-X     Document Type: Review

References (91)

1. Masters J.R. HeLa cells 50 years on: the good, the bad and the ugly. Nature Rev Cancer. 2:2002;315-319.
2. Stevens L.C. The biology of teratomas. Adv Morphol. 6:1967;1-31.
3. Solter S., Škreb N., Damjanov I. Extrauterine growth of mouse egg-cylinders results in malignant teratoma. Nature. 277:1970;503-504.
4. Stevens L. The development of transplantable teratocarcinomas from testicular grafts of pre- and postimplantation mouse embryos. Dev Biol. 21:1970;364-382.
5. Martin G.R., Evans M.J. The morphology and growth of a pluripotent teratocarcinoma cell line and its derivatives in tissue culture. Cell. 2:1974;163-172.
6. Martin G.R., Evans M.J. Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA. 72:1975;1441-1445.
7. Martin G.R. Teratocarcinomas as a model system for the study of embryogenesis and neoplasia. Cell. 5:1975;229-243.
8. Andrews P.W. Human teratocarcinomas. Biochim Biophys Acta. 948:1988;17-36.
9. Andrews P.W. Teratocarcinomas and human embryology: pluripotent human EC cell lines. APMIS. 1:1998;158-167.
10. Lehtonen E., Laasonen A., Tienari J. Teratocarcinoma stem cells as a model for differentiation in the mouse embryo. Int J Dev Biol. 33:1989;105-115.
11. Alonso A., Breuer B., Steuer B., Fischer J. The F9-EC cell line as a model for the analysis of differentiation. Int J Dev Biol. 35:1991;389-397.
12. Verheijen M.H.G., Defize L.H.K. Signals governing extraembryonic endoderm formation in the mouse: involvement of the type 1 parathyroid hormone-related peptide (PTHrP) receptor, p21Ras and cell adhesion molecules. Int J Dev Biol. 43:1999;711-721.
13. McBurney M.W. P19 embryonal carcinoma cells. Int J Dev Biol. 37:1993;135-140.
14. Skerjanc I.S. Cardiac and skeletal muscle development in P19 embryonal carcinoma cells. Trends Cardiovasc Med. 9:1999;139-143.
15. Bain G., Ray W.J., Yao M., Gottlieb D.I. From embryonal carcinoma cells to neurons: the P19 pathway. Bioessays. 16:1994;343-348.
16. McBurney M.W., Rogers B.J. Isolation of male murine embryonal carcinoma cells and their chromosome replication patterns. Dev Biol. 89:1982;503-508.
17. Rossant J., McBurney M.W. The developmental potential of a euploid male teratocarcinoma cell line after blastocyst injection. J Embryol Exp Morphol. 70:1982;99-112.
18. Edwards M.K.S., Harris J.F., McBurney M.W. Induced muscle differentiation in an embryonal carcinoma cell line. Mol Cell Biol. 3:1983;2280-2286.
19. Jones-Villeneuve E.M.C., Rudnicki M.A., Harris J.F., McBurney M.W. Retinoic acid induced neural differentiation of embryonal carcinoma cells. Mol Cell Biol. 3:1983;2271-2279.
20. Habara-Ohkubo A. Differentiation of beating cardiac muscle cells from a derivative of P19 embryonal carcinoma cells. Cell Struct Funct. 21:1996;101-110.
21. Mummery C.L., Feijen A., Van der Saag P.T., Van den Brink C.E., De Laat S.W. Clonal variants of differentiated P19 embryonal carcinoma cells exhibit epidermal growth factor receptor kinase activity. Dev Biol. 109:1985;402-410.
22. Mummery C.L., Feijen A., Moolenaar W.H., Van den Brink C.E., De Laat S.W. Establishment of a differentiated mesodermal line from P19 EC cells expressing functional PDGF and EGF receptors. Exp Cell Res. 165:1986;229-242.
23. Rudnicki M.A., Reuhl K.R., McBurney M.W. Cell lines with developmental potential restricted to mesodermal lineages isolated from differentiating cultures of pluripotential P19 embryonal carcinoma cells. Development. 107:1989;361-372.
24. Strickland S., Mahdavi V. The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell. 15:1978;393-403.
25. Jones-Villeneuve E.M., McBurney M.W., Rogers K.A., Kalnins V.I. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J Cell Biol. 94:1982;253-262.
26. McBurney M.W., Jones-Villeneuve E.M.V., Edwards M.K.S., Anderson P.J. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature. 299:1982;165-167.
27. Friend C., Scher W., Holland J.G., Sato T. Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethyl sulfoxide. Proc Natl Acad Sci USA. 68:1976;378-382.
28. Kimhi Y., Palfrey C., Spector I., Barak Y., Littauer U.Z. Maturation of neuroblastoma cells in the presence of dimethylsulfoxide. Proc Natl Acad Sci USA. 73:1976;462-466.
29. Tralka T.S., Rabson A.S. Cilia formation in cultures of human lung cancer cells treated with dimethyl sulfoxide. J Natl Cancer Inst. 57:1976;1383-1388.
30. Lako M., Lindsay S., Lincoln J., et al. Characterization of Wnt gene expression during the differentiation of murine embryonic stem cells in vitro: role of Wnt3 in enhancing haematopoietic differentiation. Mech Dev. 103:2001;49-59.
31. Morley P., Whitfield J.F. The differentiation inducer, dimethyl sulfoxide, transiently increases the intracellular calcium ion concentration in various cell types. J Cell Physiol. 156:1993;219-225.
32. Smith S.C., Reuhl K.R., Craig J., McBurney M.W. The role of aggregation in embryonal carcinoma cell differentiation. J Cell Physiol. 131:1987;74-84.
33. Belliveau D.J., Bechberger J.F., Rogers K.A., Naus C.C.G. Differential expression of gap junctions in neurons and astrocytes derived from P19 embryonal carcinoma cells. Dev Genet. 21:1997;187-200.
34. Van der Heyden M.A.G., Rook M.B., Hermans M.M.P., et al. Identification of connexin43 as a functional target for Wnt signalling. J Cell Sci. 111:1998;1741-1749.
35. Van der Heyden M.A.G., Veltmaat J.M., Hendriks J.A.A., Destrée O.H.J., Defize L.H.K. Dynamic connexin43 expression and gap junctional communication during endoderm differentiation of F9 embryonal carcinoma cells. Eur J Cell Biol. 79:2000;272-282.
36. Campione-Piccardo J., Sun J.J., Craig J., McBurney M.W. Cell-cell interaction can influence drug-induced differentiation of murine embryonal carcinoma cells. Dev Biol. 109:1985;25-31.
37. Armour C., Garson K., McBurney M.W. Cell-cell interaction modulates MyoD-induced skeletal myogenesis in pluripotent P19 cells in vitro. Exp Cell Res. 251:1999;79-91.
38. Mummery C.L., Van Achterberg T.A., Van den Eijnden-van Raaij A.J., et al. Visceral-endoderm-like cell lines induce differentiation of murine P19 embryonal carcinoma cells. Differentiation. 46:1991;51-60.
39. Van den Eijnden-van Raaij A.J., Van Achterberg T.A., Van der Kruijssen C.M., et al. Differentiation of aggregated murine P19 embryonal carcinoma cells is induced by a novel visceral endoderm-specific FGF-like factor and inhibited by activin A. Mech Dev. 33:1991;157-165.
40. Edwards M.K.S., McBurney M.W. The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev Biol. 98:1983;187-191.
41. Rodriguez E.R., Tan C.D., Onwuta U.S., et al. 3,5,3′-Triiodo-l-thyronine induces cardiac myocyte differentiation but not neuronal differentiation in P19 teratocarcinoma cells in a dose dependent manner. Biochem Biophys Res Commun. 205:1994;652-658.
42. 3) in P19 teratocarcinoma cells is accompanied by preferential binding of RGG(T/A)CA direct repeats spaced by 4 base pairs in the DNA. Biochem Biophys Res Commun. 205:1994;1899-1906.
43. Paquin J., Danalache B.A., Jankowski M., McCann S.M., Gutkowska J. Oxytocin induces differentiation of P19 embryonic stem cells to cardiomyocytes. Proc Natl Acad Sci USA. 99:2002;9550-9555.
44. Gimpl G., Fahrenholz F. The oxytocin receptor system: structure, function and regulation. Physiol Rev. 81:2001;629-683.
45. Azuma M., Hayashi Y., Yoshida H., et al. Emergence of differentiated subclones from a human salivary adenocarcinoma cell clone in culture after treatment with sodium butyrate. Cancer Res. 46:1986;770-777.
46. Adan R.A., Cox J.J., Van Kats J.P., Burbach J.P. Thyroid hormone regulates the oxytocin gene. J Biol Chem. 267:1992;3771-3777.
47. Adan R.A., Cox J.J., Beischlag T.V., Burbach J.P. A composite hormone response element mediates the transactivation of the rat oxytocin gene by different classes of nuclear hormone receptors. Mol Endocrinol. 7:1993;47-57.
48. Grépin C., Robitaille L., Antakly T., Nemer M. Inhibition of transcription factor GATA-4 expression blocks in vitro cardiac muscle differentiation. Mol Cell Biol. 15:1995;4095-4102.
49. Grépin C., Nemer G., Nemer M. Enhanced cardiogenesis in embryonic stem cells overexpressing the GATA-4 transcription factor. Development. 124:1997;2387-2395.
50. Skerjanc I.S., Petropoulos H., Ridgeway A.G., Wilton S. Myocyte enhancer 2C and Nkx2-5 up-regulate each other's expression and initiate cardiomyogenesis in P19 cells. J Biol Chem. 52:1998;34904-34910.
51. Jamali M., Rogerson P.J., Wilton S., Skerjanc I.S. Nkx2-5 activity is essential for cardiomyogenesis. J Biol Chem. 276:2001;42252-42258.
52. Li Q.Y., Newbury-Ecob R.A., Terrett J.A., et al. Holt-Oram syndrome is caused by mutations in Tbx5, a member of the Brachyury (T) gene family. Nature Genet. 15:1997;21-29.
53. Bruneau B.G., Nemer G., Schmitt J.P., et al. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell. 106:2001;709-721.
54. Hiroi Y., Kudoh S., Monzen K., et al. Tbx5 associates with Nkx2-5 and synergistically promotes cardiomyocyte differentiation. Nature Genet. 28:2002;276-280.
55. Hosoda T., Monzen K., Hiroi Y., et al. A novel myocyte-specific gene Midori promotes the differentiation of P19Cl6 cells into cardiomyocytes. J Biol Chem. 276:2001;35978-35989.
56. Schultheiss T.M., Burch J.B., Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11:1997;451-462.
57. Monzen K., Shiojima I., Hiroi Y., et al. Bone morphogenetic proteins induce cardiomyocyte differentiation through the mitogen-activated protein kinase kinase kinase TAK1 and cardiac transcription factors Csx/Nkx-2.5 and GATA-4. Mol Cell Biol. 19:1999;7096-7105.
58. Davidson S.M., Morange M. Hsp25 and the p38 MAPK pathway are involved in differentiation of cardiomyocytes. Dev Biol. 218:2000;146-160.
59. Eriksson M., Leppä S. Mitogen-activated protein kinases and activator protein 1 are required for proliferation and cardiomyocyte differentiation of P19 embryonal carcinoma cells. J Biol Chem. 277:2002;15992-16001.
60. Yang S.H., Galanis A., Sharrocks A.D. Targeting of p38 mitogen-activated protein kinases to MEF2 transcription factors. Mol Cell Biol. 19:1999;4028-4038.
61. Zhao M., New L., Kravchenko V.V., et al. Regulation of the MEF2 family of transcription factors by p38. Mol Cell Biol. 19:1999;21-30.
62. Raingeaud J., Gupta S., Rogers J.S., et al. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem. 270:1995;7420-7426.
63. Monzen K., Hiroi Y., Kudoh S., et al. Smads, TAK1, and their common target ATF-2 play a critical role in cardiomyocyte differentiation. J Cell Biol. 153:2001;687-698.
64. Von Bubnoff A., Cho K.W.Y. Intracellular BMP signaling regulation in vertebrates: pathway or network. Dev Biol. 239:2001;1-14.
65. Sano Y., Harada J., Tashiro S., et al. ATF-2 is a common nuclear target of Smad and TAK1 pathways in transforming growth factor-β signaling. J Biol Chem. 274:1999;8949-8957.
66. Jamali M., Karamboulas C., Rogerson P.J., Skerjanc I.S. BMP signaling regulates Nkx2-5 activity during cardiomyogenesis. FEBS Lett. 509:2001;126-130.
67. Pandur P., Läsche L., Eisenberg L.M., Kühl M. Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature. 418:2002;636-641.
68. Peng C.-F., Wei Y., Levsky J.M., et al. Microarray analysis of global changes in gene expression during cardiac myocyte differentiation. Physiol Genomics. 9:2002;145-155.
69. Anisimov S.V., Tarasov K.V., Riordon D., Wobus A.M., Boheler K.R. SAGE identification of differentiation responsive genes in P19 embryonic cells induced to form cardiomyocytes in vitro. Mech Dev. 117:2002;25-74.
70. Rudnicki M.A., Ruben M., McBurney M.W. Regulated expression of a transfected human cardiac actin gene during differentiation of multipotential murine embryonal carcinoma cells. Mol Cell Biol. 8:1988;406-417.
71. Rudnicki M.A., Jackowski G., Saggin L., McBurney M.W. Actin and myosin expression during development of cardiac muscle from cultured embryonal carcinoma cells. Dev Biol. 138:1990;348-358.
72. Fotheringham J., Xu F.Y., Nemer M., et al. Lysophophatidylethanolamine acyltransferase activity is elevated during cardiac cell differentiation. Biochim Biophys Acta. 1485:2000;1-10.
73. Reig J., Domingo E., Segura R., et al. Rat myocardial tissue lipids and their effects on ventricular electrical activity: influence of dietary lipids. Cardiovasc Res. 27:1993;364-370.
74. Post J.A., Verkleij A.J., Langer G.A. Organization and function of sarcolemmal phospholipids in control and ischemic/reperfused cardiomyocytes. J Mol Cell Cardiol. 27:1995;749-760.
75. Turnheim K., Gruber J., Wachter C., Ruiz-Gutierrez V. Membrane phospholipid composition affects function of potassium channels from rabbit colon epithelium. Am J Physiol. 277:1999;C83-C90.
76. Xu F.Y., Kardami E., Nemer M., Choy P.C., Hatch G.M. Elevation in phosphatidylethanolamine is an early but not essential event for cardiac cell differentiation. Exp Cell Res. 256:2000;358-364.
77. Xu F.Y., Fandrich R.R., Nemer M., Kardami E., Hatch G.M. The subcellular distribution of protein kinase Cα, -ε, and -ζ isoforms during cardiac cell differentiation. Arch Biochem Biophys. 367:1999;17-25.
78. + exchanger is constitutively activated in P19 embryonal carcinoma cells, but not in a differentiated derivative. J Biol Chem. 262:1987;9621-9628.
79. + channels in cardiac and neuronal cells derived from a mouse embryonal carcinoma cell line. J Physiol. 472:1993;289-303.
80. Van der Heyden M.A.G., Van Kempen M.J.A., Tsuji Y., et al. P19 embryonal carcinoma cells: a suitable model system for cardiac electrophysiological differentiation at the molecular and functional level. Cardiovasc Res. 44:2003;1 Issue manager: please supply correct volume number and pages.
81. 2+ channels. In Vitro Cell Dev Biol. 30A:1994;425-434.
82. Lipskaia L., Grépin C., Defer N., Hanoune J. Adenylyl cyclase activity and gene expression during mesodermal differentiation of the P19 embryonal carcinoma cells. J Cell Physiol. 176:1998;50-56.
83. 2+ channel blockers. Differentiation. 48:1991;173-182.
84. Maltsev V.A., Rohwedel J., Hescheler J., Wobus A.M. Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev. 44:1993;41-50.
85. Franco D., Lamers W.H., Moorman A.F.M. Patterns of expression in the developing myocardium: towards a morphologically integrated transcriptional model. Cardiovasc Res. 38:1998;25-53.
86. Wetzel G.T., Klitzner T. Developmental cardiac electrophysiology. Recent advances in cellular physiology. Cardiovasc Res. 31:1996;E52-E60.
87. Taylor W.A., Xu F.Y., Ma B.J., et al. Expression of monolysocardiolipin acyltransferase activity is regulated in concert with the level of cardiolipin and cardiolipin biosynthesis in the mammalian heart. BMC Biochem. 3:2002;9.
88. 4 mRNA in differentiating P19 embryonic cells and during development of cardiovascular tissues. Biochim Biophys Acta. 1306:1996;187-193.
89. Monge J.C., Stewart D.N., Cernacek P. Differentiation of embryonal carcinoma cells to a neural or cardiomyocyte lineage is associated with selective expression of endothelin receptors. J Biol Chem. 270:1995;15385-15390.
90. Hidaka K., Morisaki T., Byun S.H., et al. The MEF2B homologue differentially expressed in mouse embryonal carcinoma cells. Biochem Biophys Res Commun. 213:1995;555-560.
91. Ziman M.R., Thomas M., Jacobsen P., Beazley L. A key role for Pax7 transcripts in determination of muscle and nerve cells. Exp Cell Res. 268:2001;220-229.