The plasma membrane calcium ATPase 4 signalling in cardiac fibroblasts mediates cardiomyocyte hypertrophy

Nature Communications

Volumn 7, Issue , 2016, Pages

  Mohamed, Tamer M A ^a,b,c   Abou Leisa, Riham ^a   Stafford, Nicholas ^a   Maqsood, Arfa ^a   Zi, Min ^a   Prehar, Sukhpal ^a   Baudoin Stanley, Florence ^a   Wang, Xin ^a   Neyses, Ludwig ^a   Cartwright, Elizabeth J ^a   Oceandy, Delvac ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b GLADSTONE INSTITUTES   (United States)

^c Zagazig University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

AURINTRICARBOXYLIC ACID; PLASMA MEMBRANE CALCIUM ATPASE 4; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SECRETED FRIZZLED RELATED PROTEIN 2; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE (CALCIUM); CONDITIONED MEDIUM; MEMBRANE PROTEIN; PMCA4 PROTEIN, MOUSE; SFRP2 PROTEIN, MOUSE;

CALCIUM; INHIBITOR; MEMBRANE; NEUROLOGY; PLASMA; PROTEIN; RODENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART FIBROBLAST; HEART MUSCLE INJURY; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE PRESSURE; MOUSE; NONHUMAN; PROTEIN TARGETING; RAT; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; AORTA; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CARDIOMEGALY; CELL MEMBRANE; COMPLICATION; CONDITIONED MEDIUM; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; FIBROBLAST; GENE DELETION; KNOCKOUT MOUSE; METABOLISM; NEWBORN; PATHOLOGY; PHARMACOLOGY; PRESSURE; SIGNAL TRANSDUCTION; STENOSIS, OCCLUSION AND OBSTRUCTION;

MUS;

ANIMALS; ANIMALS, NEWBORN; AORTA; AURINTRICARBOXYLIC ACID; CALCIUM-TRANSPORTING ATPASES; CARDIOMEGALY; CELL MEMBRANE; CONSTRICTION, PATHOLOGIC; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; FIBROBLASTS; GENE DELETION; MEMBRANE PROTEINS; MICE, KNOCKOUT; MYOCARDIUM; MYOCYTES, CARDIAC; PRESSURE; SIGNAL TRANSDUCTION;

EID: 84962715083     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11074     Document Type: Article

References (46)

1. Arad, M., Seidman, J. G., Seidman, C. E. Phenotypic diversity in hypertrophic cardiomyopathy. Hum. Mol. Genet. 11, 2499-2506 (2002).
2. Heineke, J., Molkentin, J. D. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat. Rev. Mol. Cell Biol. 7, 589-600 (2006).
3. Hill, J. A., Olson, E. N. Cardiac plasticity. N. Engl. J. Med. 358, 1370-1380 (2008).
4. Mathew, J. et al. Reduction of cardiovascular risk by regression of electrocardiographic markers of left ventricular hypertrophy by the angiotensin-converting enzyme inhibitor ramipril. Circulation 104, 1615-1621 (2001).
5. Klingbeil, A. U., Schneider, M., Martus, P., Messerli, F. H., Schmieder, R. E. A meta-analysis of the effects of treatment on left ventricular mass in essential hypertension. Am. J. Med. 115, 41-46 (2003).
6. Souders, C. A., Bowers, S. L., Baudino, T. A. Cardiac fibroblast: the renaissance cell. Circ. Res. 105, 1164-1176 (2009).
7. Kakkar, R., Lee, R. T. Intramyocardial fibroblast myocyte communication. Circ. Res. 106, 47-57 (2010).
8. Takeda, N. et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J. Clin. Invest. 120, 254-265 (2010).
9. Bang, C. et al. Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J. Clin. Invest. 124, 2136-2146 (2014).
10. Carafoli, E. Calcium signaling: a tale for all seasons. Proc. Natl Acad. Sci. USA 99, 1115-1122 (2002).
11. Zhang, X. et al. Calcium sensing receptor promotes cardiac fibroblast proliferation and extracellular matrix secretion. Cell Physiol. Biochem. 33, 557-568 (2014).
12. He, W. et al. Exogenously administered secreted frizzled related protein 2 (Sfrp2) reduces fibrosis and improves cardiac function in a rat model of myocardial infarction. Proc. Natl Acad. Sci. USA 107, 21110-21115 (2010).
13. Kobayashi, K. et al. Secreted Frizzled-related protein 2 is a procollagen C proteinase enhancer with a role in fibrosis associated with myocardial infarction. Nat. Cell Biol. 11, 46-55 (2009).
14. Brophy, P. D., Lang, K. M., Dressler, G. R. The secreted frizzled related protein 2 (SFRP2) gene is a target of the Pax2 transcription factor. J. Biol. Chem. 278, 52401-52405 (2003).
15. Qin, S., Taglienti, M., Cai, L., Zhou, J., Kreidberg, J. A. c-Met and NF-kappaB-dependent overexpression of Wnt7a and-7b and Pax2 promotes cystogenesis in polycystic kidney disease. J. Am. Soc. Nephrol. 23, 1309-1318 (2012).
16. Curry, M. C., Luk, N. A., Kenny, P. A., Roberts-Thomson, S. J., Monteith, G. R. Distinct regulation of cytoplasmic calcium signals and cell death pathways by different plasma membrane calcium ATPase isoforms in MDA-MB-231 breast cancer cells. J. Biol. Chem. 287, 28598-28608 (2012).
17. Altamirano, F. et al. Increased resting intracellular calcium modulates NF-kappaB-dependent inducible nitric-oxide synthase gene expression in dystrophic mdx skeletal myotubes. J. Biol. Chem. 287, 20876-20887 (2012).
18. Bergmann, M. W. WNT signaling in adult cardiac hypertrophy and remodeling: lessons learned from cardiac development. Circ. Res. 107, 1198-1208 (2010).
19. Veeman, M. T., Slusarski, D. C., Kaykas, A., Louie, S. H., Moon, R. T. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13, 680-685 (2003).
20. Schuh, K. et al. Plasma membrane Ca2\+ ATPase 4 is required for sperm motility and male fertility. J. Biol. Chem. 279, 28220-28226 (2004).
21. Mohamed, T. M. et al. Plasma membrane calcium pump (PMCA4)/neuronal nitric oxide synthase complex regulates cardiac contractility through modulation of a compartmentalized cyclic nucleotide microdomain. J. Biol. Chem. 286, 41520-41529 (2011).
22. Lindsley, A. et al. Identification and characterization of a novel Schwann and outflow tract endocardial cushion lineage-restricted periostin enhancer. Dev. Biol. 307, 340-355 (2007).
23. Qian, L. et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485, 593-598 (2012).
24. Mohamed, T. M. et al. Development and characterization of a novel fluorescent indicator protein PMCA4-GCaMP2 in cardiomyocytes. J. Mol. Cell. Cardiol. 63, 57-68 (2013).
25. Hallick, R. B., Chelm, B. K., Gray, P. W., Orozco, Jr E. M. Use of aurintricarboxylic acid as an inhibitor of nucleases during nucleic acid isolation. Nucleic Acids Res. 4, 3055-3064 (1977).
26. Posner, A., Raser, K. J., Hajimohammadreza, I., Yuen, P. W., Wang, K. K. Aurintricarboxylic acid is an inhibitor of mu-and m-calpain. Biochem. Mol. Biol. Int. 36, 291-299 (1995).
27. Hashem, A. M. et al. Aurintricarboxylic acid is a potent inhibitor of influenza A and B virus neuraminidases. PLoS ONE 4, e8350 (2009).
28. Kanekar, S., Hirozanne, T., Terracio, L., Borg, T. K. Cardiac fibroblasts: form and function. Cardiovasc. Pathol. 7, 127-133 (1998).
29. Pellieux, C. et al. Dilated cardiomyopathy and impaired cardiac hypertrophic response to angiotensin II in mice lacking FGF-2. J. Clin. Invest. 108, 1843-1851 (2001).
30. Sanada, S. et al. IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system. J. Clin. Invest. 117, 1538-1549 (2007).
31. Mohamed, T. M. et al. Specific role of neuronal nitric-oxide synthase when tethered to the plasma membrane calcium pump in regulating the betaadrenergic signal in the myocardium. J. Biol. Chem. 284, 12091-12098 (2009).
32. Oceandy, D. et al. Neuronal nitric oxide synthase signaling in the heart is regulated by the sarcolemmal calcium pump 4b. Circulation 115, 483-492 (2007).
33. Wu, X. et al. Plasma membrane Ca2\+-ATPase isoform 4 antagonizes cardiac hypertrophy in association with calcineurin inhibition in rodents. J. Clin. Invest. 119, 976-985 (2009).
34. Rao, T. P., Kuhl, M. An updated overview on Wnt signaling pathways: a prelude for more. Circ. Res. 106, 1798-1806 (2010).
35. Okunade, G. W. et al. Targeted ablation of plasma membrane Ca2\+-ATPase (PMCA) 1 and 4 indicates a major housekeeping function for PMCA1 and a critical role in hyperactivated sperm motility and male fertility for PMCA4. J. Biol. Chem. 279, 33742-33750 (2004).
36. Afroze, T. et al. Calcium efflux activity of plasma membrane Ca2\+ ATPase-4 (PMCA4) mediates cell cycle progression in vascular smooth muscle cells. J. Biol. Chem. 289, 7221-7231 (2014).
37. Prasad, V. et al. Ablation of plasma membrane Ca-ATPase isoform 4 prevents development of hypertrophy in a model of hypertrophic cardiomyopathy. J. Mol. Cell. Cardiol. 77C, 53-63 (2014).
38. Baggott, R. R. et al. Plasma membrane calcium ATPase isoform 4 inhibits vascular endothelial growth factor-mediated angiogenesis through interaction with calcineurin. Arterioscler. Thromb. Vasc. Biol. 34, 2310-2320 (2014).
39. Gros, R. et al. Plasma membrane calcium ATPase overexpression in arterial smooth muscle increases vasomotor responsiveness and blood pressure. Circ. Res. 93, 614-621 (2003).
40. Su, L., Mruk, D. D., Cheng, C. Y. Drug transporters, the blood-testis barrier, and spermatogenesis. J. Endocrinol. 208, 207-223 (2011).
41. Agah, R. et al. Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J. Clin. Invest. 100, 169-179 (1997).
42. Oceandy, D. et al. Tumor suppressor Ras-association domain family 1 isoform A is a novel regulator of cardiac hypertrophy. Circulation 120, 607-616 (2009).
43. Zi, M. et al. The mammalian Ste20-like kinase 2 (Mst2) modulates stress-induced cardiac hypertrophy. J. Biol. Chem. 289, 24275-24288 (2014).
44. O'Connell, T. D., Rodrigo, M. C., Simpson, P. C. Isolation and culture of adult mouse cardiac myocytes. Methods Mol. Biol. 357, 271-296 (2007).
45. Irizarry, R. A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003).
46. Liu, X., Milo, M., Lawrence, N. D., Rattray, M. Probe-level measurement error improves accuracy in detecting differential gene expression. Bioinformatics 22, 2107-2113 (2006).