Plasma membrane calcium ATPase isoform 4 inhibits vascular endothelial growth factor-mediated angiogenesis through interaction with calcineurin

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 10, 2014, Pages 2310-2320

  Baggott, Rhiannon R ^a   Alfranca, Arantzazu ^b,c   López Maderuelo, Dolores ^b   Mohamed, Tamer M A ^d,e   Escolano, Amelia ^b   Oller, Jorge ^b   Ornes, Beatriz C ^b   Kurusamy, Sathishkumar ^a   Rowther, Farjana B ^a   Brown, James E ^f   Oceandy, Delvac ^d   Cartwright, Elizabeth J ^d   Wang, Weiguang ^a   Gómez Del Arco, Pablo ^b,g   Martínez Martínez, Sara ^b   Neyses, Ludwig ^d,h   Redondo, Juan Miguel ^b   Armesilla, Angel Luis ^a  

^a UNIVERSITY OF WOLVERHAMPTON   (United Kingdom)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^c Instituto de Salud Carlos III   (Spain)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e Zagazig University   (Egypt)

^f ASTON UNIVERSITY   (United Kingdom)

^g UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^h UNIVERSITY OF LUXEMBOURG   (Luxembourg)

Author keywords

Angiogenesis effect; Calcineurin; Calcium; Nuclear factors of activated T cells; Plasma membrane calcium transporting ATPase

Indexed keywords

CALCINEURIN; CYCLOOXYGENASE 2; PEPTIDES AND PROTEINS; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 4; REGULATOR OF CALCINEURIN 1; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; VASCULOTROPIN; ADENOSINE TRIPHOSPHATASE (CALCIUM); ANGIOGENIC FACTOR; ATP2B4 PROTEIN, HUMAN; DSCR1 PROTEIN, MOUSE; MUSCLE PROTEIN; PMCA4 PROTEIN, MOUSE; PTGS2 PROTEIN, HUMAN; PTGS2 PROTEIN, MOUSE; RCAN1 PROTEIN, HUMAN; SIGNAL PEPTIDE; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL MOTION; CELL PROLIFERATION; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HINDLIMB; ISCHEMIA; KNOCKOUT MOUSE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIME; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; CALCINEURIN; CALCIUM-TRANSPORTING ATPASES; CELL MOVEMENT; CELL PROLIFERATION; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HEK293 CELLS; HINDLIMB; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISCHEMIA; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NFATC TRANSCRIPTION FACTORS; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84913590141     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304363     Document Type: Article

References (36)

1. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473:298-307.
2. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249-257.
3. Takahashi H, Shibuya M. The vascular endothelial growth factor (VEGF)/ VEGF receptor system and its role under physiological and pathological conditions. Clin Sci (Lond). 2005;109:227-241.
4. Armesilla AL, Lorenzo E, Gómez del Arco P, Martínez-Martínez S, Alfranca A, Redondo JM. Vascular endothelial growth factor activates nuclear factor of activated T cells in human endothelial cells: a role for tissue factor gene expression. Mol Cell Biol. 1999;19:2032-2043.
5. Hernández GL, Volpert OV, Iñiguez MA, Lorenzo E, Martínez-Martínez S, Grau R, Fresno M, Redondo JM. Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2. J Exp Med. 2001;193:607-620.
6. Zaichuk TA, Shroff EH, Emmanuel R, Filleur S, Nelius T, Volpert OV. Nuclear factor of activated T cells balances angiogenesis activation and inhibition. J Exp Med. 2004;199:1513-1522.
7. Ryeom S, Baek KH, Rioth MJ, Lynch RC, Zaslavsky A, Birsner A, Yoon SS, McKeon F. Targeted deletion of the calcineurin inhibitor DSCR1 suppresses tumor growth. Cancer Cell. 2008;13:420-431.
8. Klee CB, Ren H, Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem. 1998;273:13367-13370.
9. Hogan PG, Chen L, Nardone J, Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003;17:2205-2232.
10. Martínez-Martínez S, Redondo JM. Inhibitors of the calcineurin/NFAT pathway. Curr Med Chem. 2004;11:997-1007.
11. Buch MH, Pickard A, Rodriguez A, Gillies S, Maass AH, Emerson M, Cartwright EJ, Williams JC, Oceandy D, Redondo JM, Neyses L, Armesilla AL. The sarcolemmal calcium pump inhibits the calcineurin/ nuclear factor of activated T-cell pathway via interaction with the calcineurin A catalytic subunit. J Biol Chem. 2005;280:29479-29487.
12. Holton M, Yang D, Wang W, Mohamed TM, Neyses L, Armesilla AL. The interaction between endogenous calcineurin and the plasma membrane calcium-dependent ATPase is isoform specific in breast cancer cells. FEBS Lett. 2007;581:4115-4119.
13. Strehler EE, Zacharias DA. Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev. 2001;81:21-50.
14. Holton ML, Wang W, Emerson M, Neyses L, Armesilla AL. Plasma membrane calcium ATPase proteins as novel regulators of signal transduction pathways. World J Biol Chem. 2010;1:201-208.
15. Holton M, Mohamed TM, Oceandy D, Wang W, Lamas S, Emerson M, Neyses L, Armesilla AL. Endothelial nitric oxide synthase activity is inhibited by the plasma membrane calcium ATPase in human endothelial cells. Cardiovasc Res. 2010;87:440-448.
16. Wu X, Chang B, Blair NS, Sargent M, York AJ, Robbins J, Shull GE, Molkentin JD. Plasma membrane Ca2+-ATPase isoform 4 antagonizes cardiac hypertrophy in association with calcineurin inhibition in rodents. J Clin Invest. 2009;119:976-985.
17. Urso K, Alfranca A, Martínez-Martínez S, Escolano A, Ortega I, Rodríguez A, Redondo JM. NFATc3 regulates the transcription of genes involved in T-cell activation and angiogenesis. Blood. 2011;118:795-803.
18. Holmes K, Chapman E, See V, Cross MJ. VEGF stimulates RCAN1.4 expression in endothelial cells via a pathway requiring Ca2+/calcineurin and protein kinase C-delta. PLoS One. 2010;5:e11435.
19. Minami T, Yano K, Miura M, Kobayashi M, Suehiro J, Reid PC, Hamakubo T, Ryeom S, Aird WC, Kodama T. The Down syndrome critical region gene 1 short variant promoters direct vascular bed-specific gene expression during inflammation in mice. J Clin Invest. 2009;119:2257-2270.
20. Yu Y, Sato JD. MAP kinases, phosphatidylinositol 3-kinase, and p70 S6 kinase mediate the mitogenic response of human endothelial cells to vascular endothelial growth factor. J Cell Physiol. 1999;178:235-246.
21. Baggott RR, Mohamed TM, Oceandy D, Holton M, Blanc MC, Roux-Soro SC, Brown S, Brown JE, Cartwright EJ, Wang W, Neyses L, Armesilla AL. Disruption of the interaction between PMCA2 and calcineurin triggers apoptosis and enhances paclitaxel-induced cytotoxicity in breast cancer cells. Carcinogenesis. 2012;33:2362-2368.
22. Bir SC, Xiong Y, Kevil CG, Luo J. Emerging role of PKA/eNOS pathway in therapeutic angiogenesis for ischaemic tissue diseases. Cardiovasc Res. 2012;95:7-18.
23. Oliveria SF, Dell'Acqua ML, Sather WA. AKAP79/150 anchoring of calcineurin controls neuronal L-type Ca2+ channel activity and nuclear signaling. Neuron. 2007;55:261-275.
24. Nieves-Cintrón M, Amberg GC, Navedo MF, Molkentin JD, Santana LF. The control of Ca2+ influx and NFATc3 signaling in arterial smooth muscle during hypertension. Proc Natl Acad Sci USA. 2008;105:15623-15628.
25. Kim JY, Saffen D. Activation of M1 muscarinic acetylcholine receptors stimulates the formation of a multiprotein complex centered on TRPC6 channels. J Biol Chem. 2005;280:32035-32047.
26. Poteser M, Schleifer H, Lichtenegger M, Schernthaner M, Stockner T, Kappe CO, Glasnov TN, Romanin C, Groschner K. PKC-dependent coupling of calcium permeation through transient receptor potential canonical 3 (TRPC3) to calcineurin signaling in HL-1 myocytes. Proc Natl Acad Sci U S A. 2011;108:10556-10561.
27. 2+ channel antagonist inhibits hypertrophic signaling without reducing cardiac contractility. Circ Res. 2012;110:669-674.
28. Fujimoto T. Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol. 1993;120:1147-1157.
29. Hammes A, Oberdorf-Maass S, Rother T, et al. Overexpression of the sarcolemmal calcium pump in the myocardium of transgenic rats. Circ Res. 1998;83:877-888.
30. El-Yazbi AF, Cho WJ, Schulz R, Daniel EE. Calcium extrusion by plasma membrane calcium pump is impaired in caveolin-1 knockout mouse small intestine. Eur J Pharmacol. 2008;591:80-87.
31. Iizuka M, Abe M, Shiiba K, Sasaki I, Sato Y. Down syndrome candidate region 1,a downstream target of VEGF, participates in endothelial cell migration and angiogenesis. J Vasc Res. 2004;41:334-344.
32. Kim HJ, Prasad V, Hyung SW, Lee ZH, Lee SW, Bhargava A, Pearce D, Lee Y, Kim HH. Plasma membrane calcium ATPase regulates bone mass by fine-tuning osteoclast differentiation and survival. J Cell Biol. 2012;199:1145-1158.
33. Ewart MA, Kennedy S, Macmillan D, Raja AL, Watt IM, Currie S. Altered vascular smooth muscle function in the ApoE knockout mouse during the progression of atherosclerosis. Atherosclerosis. 2014;234:154-161.
34. Esteban V, Méndez-Barbero N, Jiménez-Borreguero LJ, Roqué M, Novensá L, García-Redondo AB, Salaices M, Vila L, Arbonés ML, Campanero MR, Redondo JM. Regulator of calcineurin 1 mediates pathological vascular wall remodeling. J Exp Med. 2011;208:2125-2139.
35. Méndez-Barbero N, Esteban V, Villahoz S, Escolano A, Urso K, Alfranca A, Rodríguez C, Sánchez SA, Osawa T, Andrés V, Martínez-González J, Minami T, Redondo JM, Campanero MR. A major role for RCAN1 in atherosclerosis progression. EMBO Mol Med. 2013;5:1901-1917.
36. Prasad V, Okunade GW, Miller ML, Shull GE. Phenotypes of SERCA and PMCA knockout mice. Biochem Biophys Res Commun. 2004;322:1192-1203.