Nitric oxide signaling in oxytocin-mediated cardiomyogenesis

Stem Cells

Volumn 25, Issue 3, 2007, Pages 679-688

  Danalache, Bogdan A ^a,b   Paquin, Joanne ^a   Donghao, Wang ^b   Grygorczyk, Ryszard ^b   Moore, Jennifer C ^c   Mummery, Christine L ^c   Gutkowska, Jolanta ^b   Jankowski, Marek ^b  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Embryonal carcinoma; Fluorescent protein reporter genes; In vitro differentiation; Myogenesis; Nitric oxide; Oxytocin

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; ALPHA ACTININ; ATRIAL NATRIURETIC FACTOR; CONTRACTILE PROTEIN; FETAL ANTIGEN; GREEN FLUORESCENT PROTEIN; MYOCYTE ENHANCER FACTOR 2; MYOGENIN; MYOSIN HEAVY CHAIN ALPHA; MYOSIN LIGHT CHAIN; N ACETYL S NITROSOPENICILLAMINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; OXYTOCIN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR MEF2C; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MUSCLE DEVELOPMENT; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ATRIAL NATRIURETIC FACTOR; DIMETHYL SULFOXIDE; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HEART; HUMANS; MUSCLE CELLS; MYOCARDIUM; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; OXYTOCIN; POLYMERASE CHAIN REACTION; RADIOIMMUNOASSAY; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 33847616638     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2005-0610     Document Type: Article

References (52)

1. Wobus AM, Boheler KR. Embryonic stem cells: Prospects for developmental biology and cell therapy. Physiol Rev 2005;85:635-678.
2. van der Heyden MA, Defize LH. Twenty one years of P19 cells: What an embryonal carcinoma cell line taught us about cardiomyocyte differentiation. Cardiovasc Res 2003;58:292-302.
3. Skerjanc IS. Cardiac and skeletal muscle development in P19 embryonal carcinoma cells. Trends Cardiovasc Med 1999;9:139-143.
4. van der Heyden MA, van Kempen MJ, Tsuji Y et al. P19 embryonal carcinoma cells: A suitable model system for cardiac electrophysiological differentiation at the molecular and functional level. Cardiovasc Res 2003;58:410-422.
5. Moore JC, Spijker R, Martens AC et al. A P19Cl6 GFP reporter line to quantify cardiomyocyte differentiation of stem cells. Int J Dev Biol 2004;48:47-55.
6. Habara-Ohkubo A. Differentiation of beating cardiac muscle cells from a derivative of P19 embryonal carcinoma cells. Cell Struct Funct 1996;21:101-110.
7. Gutkowska J, Jankowski M, Lambert C et al. Oxytocin releases atrial natriuretic peptide by combining with oxytocin receptors in the heart. Proc Natl Acad Sci U S A 1997;94:11704-11709.
8. Jankowski M, Hajjar F, Kawas SA et al. Rat heart: A site of oxytocin production and action. Proc Natl Acad Sci U S A 1998;95:14558-14563.
9. Paquin J, Danalache BA, Jankowski M et al. Oxytocin induces differentiation of P19 embryonic stem cells to cardiomyocytes. Proc Natl Acad Sci U S A 2002;99:9550-9555.
10. Jankowski M, Danalache B, Wang D et al. Oxytocin in cardiac ontogeny. Proc Natl Acad Sci U S A 2004;101:13074-13079.
11. Matsuura K, Nagai T, Nishigaki N et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 2004;279:11384-11391.
12. Gimpl G, Fahrenholz F. The oxytocin receptor system: Structure, function, and regulation. Physiol Rev 2001;81:629-683.
13. Thibonnier M, Conarty DM, Preston JA et al. Human vascular endothelial cells express oxytocin receptors. Endocrinology 1999;140:1301-1309.
14. Haraldsen L, Soderstrom-Lauritzsen V, Nilsson GE. Oxytocin stimulates cerebral blood flow in rainbow trout (Oncorhynchus mykiss) through a nitric oxide dependent mechanism. Brain Res 2002;929:10-14.
15. Chiodera P, Volpi R, Manfredi G et al. Effect of oxytocin on nitric oxide activity controlling gonadotropin secretion in humans. Eur J Clin Invest 2003;33:402-405.
16. Selvage DJ, Johnston CA. Interaction between norepinephrine, oxytocin, and nitric oxide in the stimulation of gonadotropin-releasing hormone release from proestrous rat basal hypothalamus explants. J Neuroendocrinol 2004;16:819-824.
17. Mukaddam-Daher S, Yin YL, Roy J et al. Negative inotropic and chronotropic effects of oxytocin. Hypertension 2001;38:292-296.
18. Jankowski M, Wang D, Mukaddam-Daher S et al. Pregnancy alters nitric oxide synthase and natriuretic peptide systems in the rat left ventricle. J Endocrinol 2005;184:209-217.
19. Bloch W, Fleischmann BK, Lorke DE et al. Nitric oxide synthase expression and role during cardiomyogenesis. Cardiovasc Res 1999;43:675-684.
20. Kanno S, Kim PK, Sallam K et al. Nitric oxide facilitates cardiomyogenesis in mouse embryonic stem cells. Proc Natl Acad Sci U S A 2004;101:12277-12281.
21. Laplante I, Paquin J, Beliveau R. RhoB expression is induced after the transient upregulation of RhoA and Cdc42 during neuronal differentiation and influenced by culture substratum and microtubule integrity. Dev Brain Res 2001;129:157-168.
22. Nemer G, Nemer M. Transcriptional activation of BMP-4 and regulation of mammalian organogenesis by GATA4 and -6. Dev Biol 2003;254:131-148.
23. Lefebvre DL, Giaid A, Bennett H et al. Oxytocin gene expression in rat uterus. Science 1992;256:1553-1555.
24. Ridgeway AG, Wilton S, Skerjanc IS. Myocyte enhancer factor 2C and myogenin up-regulate each other's expression and induce the development of skeletal muscle in P19 cells. J Biol Chem 2000;275:41-46.
25. Wilton S, Skerjanc IS. Factors in serum regulate muscle development in P19 cells. In Vitro Cell Dev Biol Anim 1999;35:175-177.
26. Jeng YJ, Soloff SL, Anderson GD, Soloff MS. Regulation of oxytocin receptor expression in cultured human myometrial cells by fetal bovine serum and lysophospholipids. Endocrinology 2003;144:61-68.
27. Garvey EP, Oplinger JA, Furfine ES et al. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 1997;272:4959-4963.
28. Garthwaite J, Southam E, Boulton CL et al. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4, 3-a]quinoxalin-1-one. Mol Pharmacol 1995;48:184-188.
29. Bogdan C. Nitric oxide and the regulation of gene expression. Trends Cell Biol 2001;11:66-75.
30. Braam B, de Roos R, Dijk A et al. Nitric oxide donor induces temporal and dose-dependent reduction of gene expression in human endothelial cells. Am J Physiol 2004;287:H1977-H1986.
31. Suzuki YJ, Nagase H, Day RM et al. GATA4 regulation of myocardial survival in the preconditioned heart. J Mol Cell Cardiol 2004;37:1195-1203.
32. Smith MP, Ayad VJ, Mundell SJ et al. Internalization and desensitization of the oxytocin receptor is inhibited by Dynamin and Clathrin mutants in HEK-293 cells. Mol Endocrinol 2006;20:379-388.
33. Phaneuf S, Asboth G, Carrasco MP et al. The desensitization of oxytocin receptors in human myometrial cells is accompanied by down-regulation of oxytocin receptor messenger RNA. J Endocrinol 1997;154:7-18.
34. Phaneuf S, Asboth G, Carrasco MP et al. Desensitization of oxytocin receptors in human myometrium. Hum Reprod Update 1998;4:625-633.
35. Xu W, Liu LZ, Loizidou M et al. The role of nitric oxide in cancer. Cell Res 2002;12:311-320.
36. Berg RW, McBurney MW. Cell density and cell cycle effects on retinoic acid-induced carcinoma cell differentiation. Dev Biol 1990;138:123-135.
37. Krumenacker JS, Katsuki S, Kots A et al. Differential expression of genes involved in cGMP-dependent nitric oxide signaling in murine embryonic stem (ES) cells and ES cell-derived cardiomyocytes. Nitric Oxide 2006;14:1-11.
38. Bu S, Xia G, Tao Y, Lei L, Zhou B. Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol Cell Endocrinol 2003;207:21-30.
39. Thaler CD, Epel D. Nitric oxide in oocyte maturation, ovulation, fertilization, cleavage and implantation: A little dab'll do ya. Curr Pharm Des 2003;9:399-409.
40. Sato N, Meijer L, Skaltsounis P et al. Maintenance of pluripotency in human and embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004;10:55-63.
41. Ahumada A, Slusarski DC, Liu X et al. Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP Science 2002;298:2006-2010.
42. Grépin C, Robitaille L, Antakly T et al. Inhibition of transcription factor GATA4 expression blocks in vitro cardiac muscle differentiation. Mol Cell Biol 1995;15:4095-4102.
43. Liu H, Harris TM, Kim HH et al. Cardiac myocyte differentiation: the Nkx2.5 and Cripto target genes in P19 clone 6 cells. Funct Integr Genomics 2005;5:218-239.
44. Weiss A, Leinwand LA. The mammalian myosin heavy chain gene family. Annu Rev Cell Dev Biol 12:417-439, 1996.
45. Morkin E. Control of cardiac myosin heavy chain gene expression. Microsc Res Tech 50:522-531, 2000.
46. Wobus AM, Kleppisch T, Maltsev V et al. Cardiomyocyte-like cells differentiated in vitro from embryonic carcinoma cells P19 are characterized by functional expression of adrenoceptors and Ca2+ channels. In Vitro Cell Dev Biol Anim 1994;30A:425-434.
47. Zheng Z, Wang ZM, Delbono O. Charge movement and transcription regulation of L-type calcium channel alpha (1S) in skeletal muscle cells. J Physiol 2002;540:397-409.
48. Small EM, Krieg PA. Transgenic analysis of the atrial natriuretic factor (ANF) promoter: Nkx2-5 and GATA-4 binding sites are required for atrial specific expression of ANF. Dev Biol 2003;261:116-131.
49. Uchida S, Fuke, Tsukahara T. Upregulations of Gata4 and oxytocin receptor are important in cardiomyocyte differentiation processes of P19CL6 cells. J Cell Biochem 2006;Sep 7; [Epub ahead of print].
50. Chun YS, Hyun IY, Kwak YG et al. Hypoxicactivation of the atrial natriuretic peptide gene promoter trough direct and indirect actions of hypoxia-inductible factor-1. Biochem J 2003;370:149-157.
51. Hagen T, Taylor CT, Lam F et al. Redistribution of intracellular oxygen in hypoxia by nitric oxide: Effect of HIF1alpha. Science 2003;302:1975-1978.
52. Schmelter M, Ateghang B, Helmig S et al. Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-indued cardiovascular differentiation. FASEB J 2006;20:1182-1184.