Atrial natriuretic peptide inhibits cell cycle activity of embryonic cardiac progenitor cells via its NPRA receptor signaling axis

American Journal of Physiology - Cell Physiology

Volumn 308, Issue 7, 2015, Pages C557-C569

  Hotchkiss, Adam ^a   Feridooni, Tiam ^a   Baguma Nibasheka, Mark ^a   McNeil, Kathleen ^a   Chinni, Sarita ^a   Pasumarthi, Kishore B S ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

ANP; Cardiac progenitor cells; Cardiomyocytes; Cell proliferation and differentiation; Embryonic heart; Gene expression; Knockin mice; Lineage tracking; Natriuretic peptide receptors

Indexed keywords

ADENYLATE CYCLASE; ATRIAL NATRIURETIC FACTOR; CYCLIC AMP; CYCLIC GMP; GENOMIC DNA; MESSENGER RNA; NATRIURETIC PEPTIDE RECEPTOR A; NATRIURETIC PEPTIDE RECEPTOR B; RNA; ATRIAL NATRIURETIC FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIAC STEM CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; HEART VENTRICLE WALL; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SECOND MESSENGER ASSAY; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; EMBRYONIC STEM CELL; HEART MUSCLE CELL; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

MAMMALIA; MUS;

ANIMALS; ATRIAL NATRIURETIC FACTOR; CELL CYCLE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC STEM CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCYTES, CARDIAC; RECEPTORS, ATRIAL NATRIURETIC FACTOR; SIGNAL TRANSDUCTION;

EID: 84926345039     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00323.2014     Document Type: Article

References (48)

1. Anand-Srivastava MB, Thibault G, Sola C, Fon E, Ballak M, Charbonneau C, Haile-Meskel H, Garcia R, Genest J, Cantin M. Atrial natriuretic factor in Purkinje fibers of rabbit heart. Hypertension 13: 789-798, 1989.
2. Baldini PM, De Vito P, D’Aquilio F, Vismara D, Zalfa F, Bagni C, Fiaccavento R, Di Nardo P. Role of atrial natriuretic peptide in the suppression of lysophosphatydic acid-induced rat aortic smooth muscle (RASM) cell growth. Mol Cell Biochem 272: 19-28, 2005.
3. Bloch KD, Seidman JG, Naftilan JD, Fallon JT, Seidman CE. Neonatal atria and ventricles secrete atrial natriuretic factor via tissue-specific secretory pathways. Cell 47: 695-702, 1986.
4. Brown J, Zuo Z. Natriuretic peptide receptors in the fetal rat. Am J Physiol Endocrinol Metab 269: E253-E268, 1995.
5. Bruneau BG, Nemer G, Schmitt JP, Charron F, Robitaille L, Caron S, Conner DA, Gessler M, Nemer M, Seidman CE, Seidman JG. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106: 709-721, 2001.
6. Cameron VA, Aitken GD, Ellmers LJ, Kennedy MA, Espiner EA. The sites of gene expression of atrial, brain, and C-type natriuretic peptides in mouse fetal development: temporal changes in embryos and placenta. Endocrinology 137: 817-824, 1996.
7. Cameron VA, Ellmers LJ. Minireview: natriuretic peptides during development of the fetal heart and circulation. Endocrinology 144: 2191-2194, 2003.
8. Cao L, Gardner DG. Natriuretic peptides inhibit DNA synthesis in cardiac fibroblasts. Hypertension 25: 227-234, 1995.
9. Church DJ, Braconi S, van der Bent V, Vallotton MB, Lang U. Protein kinase C-dependent prostaglandin production mediates angiotensin IIinduced atrial-natriuretic peptide release. Biochem J 298: 451-456, 1994.
10. Clerico A, Giannoni A, Vittorini S, Passino C. Thirty years of the heart as an endocrine organ: physiological role and clinical utility of cardiac natriuretic hormones. Am J Physiol Heart Circ Physiol 301: H12-H20, 2011.
11. Coqueret O. New roles for p21 and p27 cell-cycle inhibitors: a function for each cell compartment? Trends Cell Biol 13: 65-70, 2003.
12. Delporte C, Winand J, Poloczek P, Von Geldern T, Christophe J. Discovery of a potent atrial natriuretic peptide antagonist for ANPA receptors in the human neuroblastoma NB-OK-1 cell line. Eur J Pharmacol 224: 183-188, 1992.
13. DiCicco-Bloom E, Lelievre V, Zhou X, Rodriguez W, Tam J, Waschek JA. Embryonic expression and multifunctional actions of the natriuretic peptides and receptors in the developing nervous system. Dev Biol 271: 161-175, 2004.
14. Dobrivojevic M, Sindic A, Edemir B, Kalweit S, Forssmann WG, Hirsch JR. Interaction between bradykinin and natriuretic peptides via RGS protein activation in HEK-293 cells. Am J Physiol Cell Physiol 303: C1260-C1268, 2012.
15. Edwards BS, Zimmerman RS, Schwab TR, Heublein DM, Burnett JC Jr. Atrial stretch, not pressure, is the principal determinant controlling the acute release of atrial natriuretic factor. Circ Res 62: 191-195, 1988.
16. Ellmers LJ, Knowles JW, Kim HS, Smithies O, Maeda N, Cameron VA. Ventricular expression of natriuretic peptides in Npr1-/-mice with cardiac hypertrophy and fibrosis. Am J Physiol Heart Circ Physiol 283: H707-H714, 2002.
17. Feridooni T, Hotchkiss A, Remley-Carr S, Saga Y, Pasumarthi KB. Cardiomyocyte specific ablation of p53 is not sufficient to block doxorubicin induced cardiac fibrosis and associated cytoskeletal changes. PLoS One 6: e22801, 2011.
18. Glenn DJ, Rahmutula D, Nishimoto M, Liang F, Gardner DG. Atrial natriuretic peptide suppresses endothelin gene expression and proliferation in cardiac fibroblasts through a GATA4-dependent mechanism. Cardiovasc Res 84: 209-217, 2009.
19. Hersey RM, Nazir MA, Whitney KD, Klein RM, Sale RD, Hinton DA, Weisz J, Gattone VH 2nd. Atrial natriuretic peptide in heart and specific binding in organs from fetal and newborn rats. Cell Biochem Funct 7: 35-41, 1989.
20. Hotchkiss A, Feridooni T, Zhang F, Pasumarthi KB. The effects of calcium channel blockade on proliferation and differentiation of cardiac progenitor cells. Cell Calcium 55: 238-251, 2014.
21. Irons CE, Sei CA, Glembotski CC. Regulated secretion of atrial natriuretic factor from cultured ventricular myocytes. Am J Physiol Heart Circ Physiol 264: H282-H285, 1993.
22. Jankowski M, Rachelska G, Donghao W, McCann SM, Gutkowska J. Estrogen receptors activate atrial natriuretic peptide in the rat heart. Proc Natl Acad Sci USA 98: 11765-11770, 2001.
23. Koide M, Akins RE, Harayama H, Yasui K, Yokota M, Tuan RS. Atrial natriuretic peptide accelerates proliferation of chick embryonic cardiomyocytes in vitro. Differentiation 61: 1-11, 1996.
24. Kotlo KU, Rasenick MM, Danziger RS. Evidence for cross-talk between atrial natriuretic peptide and nitric oxide receptors. Mol Cell Biochem 338: 183-189, 2010.
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25: 402-408, 2001.
26. Lopez MJ, Wong SK, Kishimoto I, Dubois S, Mach V, Friesen J, Garbers DL, Beuve A. Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide. Nature 378: 65-68, 1995.
27. Lowe DG. Human natriuretic peptide receptor-A guanylyl cyclase is self-associated prior to hormone binding. Biochemistry 31: 10421-10425, 1992.
28. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Waldman SA. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 52: 375-414, 2000.
29. McGrath MF, de Bold ML, de Bold AJ. The endocrine function of the heart. Trends Endocrinol Metab 16: 469-477, 2005.
30. McMullen NM, Zhang F, Hotchkiss A, Bretzner F, Wilson JM, Ma H, Wafa K, Brownstone RM, Pasumarthi KB. Functional characterization of cardiac progenitor cells and their derivatives in the embryonic heart post-chamber formation. Dev Dyn 238: 2787-2799, 2009.
31. Nemer M, Lavigne JP, Drouin J, Thibault G, Gannon M, Antakly T. Expression of atrial natriuretic factor gene in heart ventricular tissue. Peptides 7: 1147-1152, 1986.
32. O’Tierney PF, Chattergoon NN, Louey S, Giraud GD, Thornburg KL. Atrial natriuretic peptide inhibits angiotensin II-stimulated proliferation in fetal cardiomyocytes. J Physiol 588: 2879-2889, 2010.
33. Ortola FV, Ballermann BJ, Anderson S, Mendez RE, Brenner BM. Elevated plasma atrial natriuretic peptide levels in diabetic rats. Potential mediator of hyperfiltration. J Clin Invest 80: 670-674, 1987.
34. Schulz S, Singh S, Bellet RA, Singh G, Tubb DJ, Chin H, Garbers DL. The primary structure of a plasma membrane guanylate cyclase demonstrates diversity within this new receptor family. Cell 58: 1155-1162, 1989.
35. Scott NJ, Ellmers LJ, Lainchbury JG, Maeda N, Smithies O, Richards AM, Cameron VA. Influence of natriuretic peptide receptor-1 on survival and cardiac hypertrophy during development. Biochim Biophys Acta 1792: 1175-1184, 2009.
36. Sei CA, Glembotski CC. Calcium dependence of phenylephrine-, endothelin-, and potassium chloride-stimulated atrial natriuretic factor secretion from long term primary neonatal rat atrial cardiocytes. J Biol Chem 265: 7166-7172, 1990.
37. Sharma GD, Nguyen HT, Antonov AS, Gerrity RG, von Geldern T, Pandey KN. Expression of atrial natriuretic peptide receptor-A antagonizes the mitogen-activated protein kinases (Erk2 and P38MAPK) in cultured human vascular smooth muscle cells. Mol Cell Biochem 233: 165-173, 2002.
38. Stanley EG, Biben C, Elefanty A, Barnett L, Koentgen F, Robb L, Harvey RP. Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5. Int J Dev Biol 46: 431-439, 2002.
39. Stastna M, Chimenti I, Marban E, Van Eyk JE. Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics 10: 245-253, 2010.
40. Sun Q, Zhang F, Wafa K, Baptist T, Pasumarthi KB. A splice variant of cyclin D2 regulates cardiomyocyte cell cycle through a novel protein aggregation pathway. J Cell Sci 122: 1563-1573, 2009.
41. Tripathi S, Pandey KN. Guanylyl cyclase/natriuretic peptide receptor-A signaling antagonizes the vascular endothelial growth factor-stimulated MAPKs and downstream effectors AP-1 and CREB in mouse mesangial cells. Mol Cell Biochem 368: 47-59, 2012.
42. Wafa K, MacLean J, Zhang F, Pasumarthi KB. Characterization of growth suppressive functions of a splice variant of cyclin D2. PLoS One 8: e53503, 2013.
43. Wei YF, Rodi CP, Day ML, Wiegand RC, Needleman LD, Cole BR, Needleman P. Developmental changes in the rat atriopeptin hormonal system. J Clin Invest 79: 1325-1329, 1987.
44. Yan W, Sheng N, Seto M, Morser J, Wu Q. Corin, a mosaic transmembrane serine protease encoded by a novel cDNA from human heart. J Biol Chem 274: 14926-14935, 1999.
45. Yan W, Wu F, Morser J, Wu Q. Corin, a transmembrane cardiac serine protease, acts as a pro-atrial natriuretic peptide-converting enzyme. Proc Natl Acad Sci USA 97: 8525-8529, 2000.
46. Zeller R, Bloch KD, Williams BS, Arceci RJ, Seidman CE. Localized expression of the atrial natriuretic factor gene during cardiac embryogenesis. Genes Dev 1: 693-698, 1987.
47. Zhang F, Feridooni T, Hotchkiss A, Pasumarthi KB. Divergent cell cycle kinetics of midgestation ventricular cells entail a higher engraftment efficiency after cell transplantation. Am J Physiol Cell Physiol 308: C220-C228, 2015.
48. Zhang F, Pasumarthi KB. Ultrastructural and immunocharacterization of undifferentiated myocardial cells in the developing mouse heart. J Cell Mol Med 11: 552-560, 2007.