Skip to main content

The Control of Sub-plasma Membrane Calcium Signalling by the Plasma Membrane Calcium ATPase Pump PMCA4

  • Chapter
  • First Online:
Microdomains in the Cardiovascular System

Part of the book series: Cardiac and Vascular Biology ((Abbreviated title: Card. vasc. biol.,volume 3))

  • 719 Accesses

Abstract

Within cardiomyocytes cytosolic calcium levels rise and fall by an order of magnitude in each cardiac cycle, yet amidst the noise of this “global” calcium, a separate pool of “local” calcium is able to act as a second messenger in a multitude of signalling networks. The cell is equipped to deal with this through utilising the calcium-binding messenger protein calmodulin which in turn activates calcium/calmodulin-dependent targets and through compartmentalisation. This allows decoding of the calcium signal within such subcellular microdomains as the mitochondrion, the nucleus, the sarcoplasmic reticulum and the plasma membrane. In recent years our group and others have identified isoform 4 of the plasma membrane calcium/calmodulin-dependent ATPase (PMCA4) as a major regulator of local subplasmalemmal calcium in a number of cardiovascular cell types including the cardiomyocyte. Here we review techniques developed for the study of calcium levels local to PMCA4, the protein interaction and signalling complexes formed and regulated by the pump and the physiological implications of these in the heart and vascular systems.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

References

  • Adamo HP, Filoteo AG, Enyedi A, Penniston JT (1995) Mutants in the putative nucleotide-binding region of the plasma membrane Ca(2+)-pump. A reduction in activity due to slow dephosphorylation. J Biol Chem 270(50):30111–30114

    Article  CAS  PubMed  Google Scholar 

  • Afroze T, Yang G, Khoshbin A, Tanwir M, Tabish T, Momen A, Husain M (2014) Calcium efflux activity of plasma membrane Ca2+ ATPase-4 (PMCA4) mediates cell cycle progression in vascular smooth muscle cells. J Biol Chem 289(10):7221–7231. doi:10.1074/jbc.M113.533638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armesilla AL, Williams JC, Buch MH, Pickard A, Emerson M, Cartwright EJ, Oceandy D, Vos MD, Gillies S, Clark GJ, Neyses L (2004) Novel functional interaction between the plasma membrane Ca2+ pump 4b and the proapoptotic tumor suppressor Ras-associated factor 1 (RASSF1). J Biol Chem 279(30):31318–31328. doi:10.1074/jbc.M307557200

    Article  CAS  PubMed  Google Scholar 

  • Baggott RR, Alfranca A, Lopez-Maderuelo D, Mohamed TM, Escolano A, Oller J, Ornes BC, Kurusamy S, Rowther FB, Brown JE, Oceandy D, Cartwright EJ, Wang W, Gomez-del Arco P, Martinez-Martinez S, Neyses L, Redondo JM, Armesilla AL (2014) Plasma membrane calcium ATPase isoform 4 inhibits vascular endothelial growth factor-mediated angiogenesis through interaction with calcineurin. Arterioscler Thromb Vasc Biol 34(10):2310–2320. doi:10.1161/atvbaha.114.304363

    Article  CAS  PubMed  Google Scholar 

  • Bers DM (2000) Calcium fluxes involved in control of cardiac myocyte contraction. Circ Res 87(4):275–281

    Article  CAS  PubMed  Google Scholar 

  • Blaustein MP, Juhaszova M, Golovina VA, Church PJ, Stanley EF (2002) Na/Ca exchanger and PMCA localization in neurons and astrocytes: functional implications. Ann N Y Acad Sci 976:356–366

    Article  CAS  PubMed  Google Scholar 

  • Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89(4):1341–1378. doi:10.1152/physrev.00032.2008

    Article  CAS  PubMed  Google Scholar 

  • Buch MH, Pickard A, Rodriguez A, Gillies S, Maass AH, Emerson M, Cartwright EJ, Williams JC, Oceandy D, Redondo JM, Neyses L, Armesilla AL (2005) 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 280(33):29479–29487. doi:10.1074/jbc.M501326200

    Article  CAS  PubMed  Google Scholar 

  • Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499(7458):295–300. doi:10.1038/nature12354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262(5134):740–744

    Article  CAS  PubMed  Google Scholar 

  • Damy T, Ratajczak P, Shah AM, Camors E, Marty I, Hasenfuss G, Marotte F, Samuel JL, Heymes C (2004) Increased neuronal nitric oxide synthase-derived NO production in the failing human heart. Lancet 363(9418):1365–1367. doi:10.1016/s0140-6736(04)16048-0

    Article  CAS  PubMed  Google Scholar 

  • DeMarco SJ, Strehler EE (2001) Plasma membrane Ca2 + −ATPase isoforms 2b and 4b interact promiscuously and selectively with members of the membrane-associated guanylate kinase family of PDZ (PSD95/Dlg/ZO-1) domain-containing proteins. J Biol Chem 276(24):21594–21600. doi:10.1074/jbc.M101448200

    Article  CAS  PubMed  Google Scholar 

  • Despa S, Shui B, Bossuyt J, Lang D, Kotlikoff MI, Bers DM (2014) Junctional cleft [Ca(2)(+)]i measurements using novel cleft-targeted Ca(2)(+) sensors. Circ Res 115(3):339–347. doi:10.1161/circresaha.115.303582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Leva F, Domi T, Fedrizzi L, Lim D, Carafoli E (2008) The plasma membrane Ca2+ ATPase of animal cells: structure, function and regulation. Arch Biochem Biophys 476(1):65–74. doi:10.1016/j.abb.2008.02.026

    Article  CAS  PubMed  Google Scholar 

  • Elwess NL, Filoteo AG, Enyedi A, Penniston JT (1997) Plasma membrane Ca2+ pump isoforms 2a and 2b are unusually responsive to calmodulin and Ca2+. J Biol Chem 272(29):17981–17986

    Article  CAS  PubMed  Google Scholar 

  • Enyedi A, Flura M, Sarkadi B, Gardos G, Carafoli E (1987) The maximal velocity and the calcium affinity of the red cell calcium pump may be regulated independently. J Biol Chem 262(13):6425–6430

    CAS  PubMed  Google Scholar 

  • Enyedi A, Verma AK, Filoteo AG, Penniston JT (1996) Protein kinase C activates the plasma membrane Ca2+ pump isoform 4b by phosphorylation of an inhibitory region downstream of the calmodulin-binding domain. J Biol Chem 271(50):32461–32467

    Article  CAS  PubMed  Google Scholar 

  • Falchetto R, Vorherr T, Brunner J, Carafoli E (1991) The plasma membrane Ca2+ pump contains a site that interacts with its calmodulin-binding domain. J Biol Chem 266(5):2930–2936

    CAS  PubMed  Google Scholar 

  • Falchetto R, Vorherr T, Carafoli E (1992) The calmodulin-binding site of the plasma membrane Ca2+ pump interacts with the transduction domain of the enzyme. Protein Sci 1(12):1613–1621. doi:10.1002/pro.5560011209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franchini KG (2012) Focal adhesion kinase—the basis of local hypertrophic signaling domains. J Mol Cell Cardiol 52(2):485–492. doi:10.1016/j.yjmcc.2011.06.021

    Article  CAS  PubMed  Google Scholar 

  • Frey N, McKinsey TA, Olson EN (2000) Decoding calcium signals involved in cardiac growth and function. Nat Med 6(11):1221–1227. doi:10.1038/81321

    Article  CAS  PubMed  Google Scholar 

  • Fujimoto T (1993) Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol 120(5):1147–1157

    Article  CAS  PubMed  Google Scholar 

  • Goellner GM, DeMarco SJ, Strehler EE (2003) Characterization of PISP, a novel single-PDZ protein that binds to all plasma membrane Ca2 + −ATPase b-splice variants. Ann N Y Acad Sci 986:461–471

    Article  CAS  PubMed  Google Scholar 

  • Gros R, Afroze T, You XM, Kabir G, Van Wert R, Kalair W, Hoque AE, Mungrue IN, Husain M (2003) Plasma membrane calcium ATPase overexpression in arterial smooth muscle increases vasomotor responsiveness and blood pressure. Circ Res 93(7):614–621. doi:10.1161/01.res.0000092142.19896.d9

    Article  CAS  PubMed  Google Scholar 

  • Guerini D, Zecca-Mazza A, Carafoli E (2000) Single amino acid mutations in transmembrane domain 5 confer to the plasma membrane Ca2+ pump properties typical of the Ca2+ pump of endo(sarco)plasmic reticulum. J Biol Chem 275(40):31361–31368. doi:10.1074/jbc.M003474200

    Article  CAS  PubMed  Google Scholar 

  • Guerini D, Pan B, Carafoli E (2003) Expression, purification, and characterization of isoform 1 of the plasma membrane Ca2+ pump: focus on calpain sensitivity. J Biol Chem 278(40):38141–38148. doi:10.1074/jbc.M302400200

    Article  CAS  PubMed  Google Scholar 

  • Hammes A, Oberdorf-Maass S, Rother T, Nething K, Gollnick F, Linz KW, Meyer R, Hu K, Han H, Gaudron P, Ertl G, Hoffmann S, Ganten U, Vetter R, Schuh K, Benkwitz C, Zimmer HG, Neyses L (1998) Overexpression of the sarcolemmal calcium pump in the myocardium of transgenic rats. Circ Res 83(9):877–888

    Article  CAS  PubMed  Google Scholar 

  • Hare JM, Stamler JS (2005) NO/redox disequilibrium in the failing heart and cardiovascular system. J Clin Invest 115(3):509–517. doi:10.1172/jci24459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey RD, Calaghan SC (2012) Caveolae create local signalling domains through their distinct protein content, lipid profile and morphology. J Mol Cell Cardiol 52(2):366–375. doi:10.1016/j.yjmcc.2011.07.007

    Article  CAS  PubMed  Google Scholar 

  • Heim N, Griesbeck O (2004) Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J Biol Chem 279(14):14280–14286. doi:10.1074/jbc.M312751200

    Article  CAS  PubMed  Google Scholar 

  • Heineke J, Ritter O (2012) Cardiomyocyte calcineurin signaling in subcellular domains: from the sarcolemma to the nucleus and beyond. J Mol Cell Cardiol 52(1):62–73. doi:10.1016/j.yjmcc.2011.10.018

    Article  CAS  PubMed  Google Scholar 

  • Higazi DR, Fearnley CJ, Drawnel FM, Talasila A, Corps EM, Ritter O, McDonald F, Mikoshiba K, Bootman MD, Roderick HL (2009) Endothelin-1-stimulated InsP3-induced Ca2+ release is a nexus for hypertrophic signaling in cardiac myocytes. Mol Cell 33(4):472–482. doi:10.1016/j.molcel.2009.02.005

    Article  CAS  PubMed  Google Scholar 

  • Hilfiker H, Strehler-Page MA, Stauffer TP, Carafoli E, Strehler EE (1993) Structure of the gene encoding the human plasma membrane calcium pump isoform 1. J Biol Chem 268(26):19717–19725

    CAS  PubMed  Google Scholar 

  • Holton M, Yang D, Wang W, Mohamed TM, Neyses L, Armesilla AL (2007) The interaction between endogenous calcineurin and the plasma membrane calcium-dependent ATPase is isoform specific in breast cancer cells. FEBS Lett 581(21):4115–4119. doi:10.1016/j.febslet.2007.07.054

    Article  CAS  PubMed  Google Scholar 

  • Holton M, Mohamed TM, Oceandy D, Wang W, Lamas S, Emerson M, Neyses L, Armesilla AL (2010) Endothelial nitric oxide synthase activity is inhibited by the plasma membrane calcium ATPase in human endothelial cells. Cardiovasc Res 87(3):440–448. doi:10.1093/cvr/cvq077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iguchi M, Kato M, Nakai J, Takeda T, Matsumoto-Ida M, Kita T, Kimura T, Akao M (2012) Direct monitoring of mitochondrial calcium levels in cultured cardiac myocytes using a novel fluorescent indicator protein, GCaMP2-mt. Int J Cardiol 158(2):225–234. doi:10.1016/j.ijcard.2011.01.034

    Article  PubMed  Google Scholar 

  • Kim E, DeMarco SJ, Marfatia SM, Chishti AH, Sheng M, Strehler EE (1998) Plasma membrane Ca2+ ATPase isoform 4b binds to membrane-associated guanylate kinase (MAGUK) proteins via their PDZ (PSD-95/Dlg/ZO-1) domains. J Biol Chem 273(3):1591–1595

    Article  CAS  PubMed  Google Scholar 

  • Kosiorek M, Podszywalow-Bartnicka P, Zylinska L, Zablocki K, Pikula S (2011) Interaction of plasma membrane Ca(2+)-ATPase isoform 4 with calcineurin A: implications for catecholamine secretion by PC12 cells. Biochem Biophys Res Commun 411(2):235–240. doi:10.1016/j.bbrc.2011.06.098

    Article  CAS  PubMed  Google Scholar 

  • Kritzer MD, Li J, Dodge-Kafka K, Kapiloff MS (2012) AKAPs: the architectural underpinnings of local cAMP signaling. J Mol Cell Cardiol 52(2):351–358. doi:10.1016/j.yjmcc.2011.05.002

    Article  CAS  PubMed  Google Scholar 

  • Lee MY, Song H, Nakai J, Ohkura M, Kotlikoff MI, Kinsey SP, Golovina VA, Blaustein MP (2006) Local subplasma membrane Ca2+ signals detected by a tethered Ca2+ sensor. Proc Natl Acad Sci U S A 103(35):13232–13237. doi:10.1073/pnas.0605757103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenaerts I, Bito V, Heinzel FR, Driesen RB, Holemans P, D'Hooge J, Heidbuchel H, Sipido KR, Willems R (2009) Ultrastructural and functional remodeling of the coupling between Ca2+ influx and sarcoplasmic reticulum Ca2+ release in right atrial myocytes from experimental persistent atrial fibrillation. Circ Res 105(9):876–885. doi:10.1161/circresaha.109.206276

    Article  CAS  PubMed  Google Scholar 

  • Little R, Cartwright EJ, Neyses L, Austin C (2016) Plasma membrane calcium ATPases (PMCAs) as potential targets for the treatment of essential hypertension. Pharmacol Ther 159:23–34. doi:10.1016/j.pharmthera.2016.01.013

    Article  CAS  PubMed  Google Scholar 

  • Magyar CE, White KE, Rojas R, Apodaca G, Friedman PA (2002) Plasma membrane Ca2 + −ATPase and NCX1 Na+/Ca2+ exchanger expression in distal convoluted tubule cells. Am J Physiol Renal Physiol 283(1):F29–F40. doi:10.1152/ajprenal.00252.2000

    Article  CAS  PubMed  Google Scholar 

  • Mangialavori I, Ferreira-Gomes M, Pignataro MF, Strehler EE, Rossi JP (2010) Determination of the dissociation constants for Ca2+ and calmodulin from the plasma membrane Ca2+ pump by a lipid probe that senses membrane domain changes. J Biol Chem 285(1):123–130. doi:10.1074/jbc.M109.076679

    Article  CAS  PubMed  Google Scholar 

  • Mank M, Reiff DF, Heim N, Friedrich MW, Borst A, Griesbeck O (2006) A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change. Biophys J 90(5):1790–1796. doi:10.1529/biophysj.105.073536

    Article  CAS  PubMed  Google Scholar 

  • Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, Stein V, Hendel T, Reiff DF, Levelt C, Borst A, Bonhoeffer T, Hubener M, Griesbeck O (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5(9):805–811. doi:10.1038/nmeth.1243

    Article  CAS  PubMed  Google Scholar 

  • Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388(6645):882–887. doi:10.1038/42264

    Article  CAS  PubMed  Google Scholar 

  • Mohamed TM, Oceandy D, Prehar S, Alatwi N, Hegab Z, Baudoin FM, Pickard A, Zaki AO, Nadif R, Cartwright EJ, Neyses L (2009) Specific role of neuronal nitric-oxide synthase when tethered to the plasma membrane calcium pump in regulating the beta-adrenergic signal in the myocardium. J Biol Chem 284(18):12091–12098. doi:10.1074/jbc.M809112200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohamed TM, Baudoin-Stanley FM, Abou-Leisa R, Cartwright E, Neyses L, Oceandy D (2010) Measurement of plasma membrane calcium-calmodulin-dependent ATPase (PMCA) activity. Methods Mol Biol 637:333–342. doi:10.1007/978-1-60761-700-6_18

    Article  CAS  PubMed  Google Scholar 

  • Mohamed TM, Oceandy D, Zi M, Prehar S, Alatwi N, Wang Y, Shaheen MA, Abou-Leisa R, Schelcher C, Hegab Z, Baudoin F, Emerson M, Mamas M, Di Benedetto G, Zaccolo M, Lei M, Cartwright EJ, Neyses L (2011) 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(48):41520–41529. doi:10.1074/jbc.M111.290411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohamed TM, Abou-Leisa R, Baudoin F, Stafford N, Neyses L, Cartwright EJ, Oceandy D (2013a) Development and characterization of a novel fluorescent indicator protein PMCA4-GCaMP2 in cardiomyocytes. J Mol Cell Cardiol 63:57–68. doi:10.1016/j.yjmcc.2013.07.007

    Article  CAS  PubMed  Google Scholar 

  • Mohamed TM, Zakeri SA, Baudoin F, Wolf M, Oceandy D, Cartwright EJ, Gul S, Neyses L (2013b) Optimisation and validation of a high throughput screening compatible assay to identify inhibitors of the plasma membrane calcium ATPase pump—a novel therapeutic target for contraception and malaria. J Pharm Pharm Sci 16(2):217–230

    Article  CAS  PubMed  Google Scholar 

  • Mohamed TM, Abou-Leisa R, Stafford N, Maqsood A, Zi M, Prehar S, Baudoin-Stanley F, Wang X, Neyses L, Cartwright EJ, Oceandy D (2016) The plasma membrane calcium ATPase 4 signalling in cardiac fibroblasts mediates cardiomyocyte hypertrophy. Nat Commun 7:11074. doi:10.1038/ncomms11074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93(2):215–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagai T, Sawano A, Park ES, Miyawaki A (2001) Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc Natl Acad Sci U S A 98(6):3197–3202. doi:10.1073/pnas.051636098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19(2):137–141. doi:10.1038/84397

    Article  CAS  PubMed  Google Scholar 

  • Nakayama H, Bodi I, Maillet M, DeSantiago J, Domeier TL, Mikoshiba K, Lorenz JN, Blatter LA, Bers DM, Molkentin JD (2010) The IP3 receptor regulates cardiac hypertrophy in response to select stimuli. Circ Res 107(5):659–666. doi:10.1161/circresaha.110.220038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niggli V, Adunyah ES, Carafoli E (1981) Acidic phospholipids, unsaturated fatty acids, and limited proteolysis mimic the effect of calmodulin on the purified erythrocyte Ca2+ − ATPase. J Biol Chem 256(16):8588–8592

    CAS  PubMed  Google Scholar 

  • Oceandy D, Cartwright EJ, Emerson M, Prehar S, Baudoin FM, Zi M, Alatwi N, Venetucci L, Schuh K, Williams JC, Armesilla AL, Neyses L (2007) Neuronal nitric oxide synthase signaling in the heart is regulated by the sarcolemmal calcium pump 4b. Circulation 115(4):483–492. doi:10.1161/circulationaha.106.643791

    Article  CAS  PubMed  Google Scholar 

  • Oceandy D, Mohamed TM, Cartwright EJ, Neyses L (2011) Local signals with global impacts and clinical implications: lessons from the plasma membrane calcium pump (PMCA4). Biochim Biophys Acta 1813(5):974–978. doi:10.1016/j.bbamcr.2010.12.007

    Article  CAS  PubMed  Google Scholar 

  • Ohkura M, Matsuzaki M, Kasai H, Imoto K, Nakai J (2005) Genetically encoded bright Ca2+ probe applicable for dynamic Ca2+ imaging of dendritic spines. Anal Chem 77(18):5861–5869. doi:10.1021/ac0506837

    Article  CAS  PubMed  Google Scholar 

  • Pedersen PL, Carafoli E (1987) Ion motive ATPases. I. Ubiquity, properties, and significance to cell function. Trends Biochem Sci 12:146–150

    Article  CAS  Google Scholar 

  • Rimessi A, Coletto L, Pinton P, Rizzuto R, Brini M, Carafoli E (2005) Inhibitory interaction of the 14-3-3 protein with isoform 4 of the plasma membrane Ca(2+)-ATPase pump. J Biol Chem 280(44):37195–37203. doi:10.1074/jbc.M504921200

    Article  CAS  PubMed  Google Scholar 

  • Schatzmann HJ (1966) ATP-dependent Ca++ − extrusion from human red cells. Experientia 22(6):364–365

    Article  CAS  PubMed  Google Scholar 

  • Schuh K, Uldrijan S, Telkamp M, Rothlein N, Neyses L (2001) The plasma membrane calmodulin-dependent calcium pump: a major regulator of nitric oxide synthase I. J Cell Biol 155(2):201–205. doi:10.1083/jcb.200104131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuh K, Quaschning T, Knauer S, Hu K, Kocak S, Roethlein N, Neyses L (2003a) Regulation of vascular tone in animals overexpressing the sarcolemmal calcium pump. J Biol Chem 278(42):41246–41252. doi:10.1074/jbc.M307606200

    Article  CAS  PubMed  Google Scholar 

  • Schuh K, Uldrijan S, Gambaryan S, Roethlein N, Neyses L (2003b) Interaction of the plasma membrane Ca2+ pump 4b/CI with the Ca2+/calmodulin-dependent membrane-associated kinase CASK. J Biol Chem 278(11):9778–9783. doi:10.1074/jbc.M212507200

    Article  CAS  PubMed  Google Scholar 

  • Schuh K, Cartwright EJ, Jankevics E, Bundschu K, Liebermann J, Williams JC, Armesilla AL, Emerson M, Oceandy D, Knobeloch KP, Neyses L (2004) Plasma membrane Ca2+ ATPase 4 is required for sperm motility and male fertility. J Biol Chem 279(27):28220–28226. doi:10.1074/jbc.M312599200

    Article  CAS  PubMed  Google Scholar 

  • Sgambato-Faure V, Xiong Y, Berke JD, Hyman SE, Strehler EE (2006) The Homer-1 protein Ania-3 interacts with the plasma membrane calcium pump. Biochem Biophys Res Commun 343(2):630–637. doi:10.1016/j.bbrc.2006.03.020

    Article  CAS  PubMed  Google Scholar 

  • Shang W, Lu F, Sun T, Xu J, Li LL, Wang Y, Wang G, Chen L, Wang X, Cannell MB, Wang SQ, Cheng H (2014) Imaging Ca2+ nanosparks in heart with a new targeted biosensor. Circ Res 114(3):412–420. doi:10.1161/circresaha.114.302938

    Article  CAS  PubMed  Google Scholar 

  • Souders CA, Bowers SL, Baudino TA (2009) Cardiac fibroblast: the renaissance cell. Circ Res 105(12):1164–1176. doi:10.1161/circresaha.109.209809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stauffer TP, Hilfiker H, Carafoli E, Strehler EE (1993) Quantitative analysis of alternative splicing options of human plasma membrane calcium pump genes. J Biol Chem 268(34):25993–26003

    CAS  PubMed  Google Scholar 

  • Strehler EE (1991) Recent advances in the molecular characterization of plasma membrane Ca2+ pumps. J Membr Biol 120(1):1–15

    Article  CAS  PubMed  Google Scholar 

  • Strehler EE, Zacharias DA (2001) Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 81(1):21–50

    Article  CAS  PubMed  Google Scholar 

  • Tallini YN, Ohkura M, Choi BR, Ji G, Imoto K, Doran R, Lee J, Plan P, Wilson J, Xin HB, Sanbe A, Gulick J, Mathai J, Robbins J, Salama G, Nakai J, Kotlikoff MI (2006) Imaging cellular signals in the heart in vivo: cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc Natl Acad Sci U S A 103(12):4753–4758. doi:10.1073/pnas.0509378103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tay LH, Dick IE, Yang W, Mank M, Griesbeck O, Yue DT (2012) Nanodomain Ca(2)(+) of Ca(2)(+) channels detected by a tethered genetically encoded Ca(2)(+) sensor. Nat Commun 3:778. doi:10.1038/ncomms1777

    Article  CAS  PubMed  Google Scholar 

  • Timmann C, Thye T, Vens M, Evans J, May J, Ehmen C, Sievertsen J, Muntau B, Ruge G, Loag W, Ansong D, Antwi S, Asafo-Adjei E, Nguah SB, Kwakye KO, Akoto AO, Sylverken J, Brendel M, Schuldt K, Loley C, Franke A, Meyer CG, Agbenyega T, Ziegler A, Horstmann RD (2012) Genome-wide association study indicates two novel resistance loci for severe malaria. Nature 489(7416):443–446. doi:10.1038/nature11334

    Article  CAS  PubMed  Google Scholar 

  • Trafford AW, Clarke JD, Richards MA, Eisner DA, Dibb KM (2013) Calcium signalling microdomains and the t-tubular system in atrial myocytes: potential roles in cardiac disease and arrhythmias. Cardiovasc Res 98(2):192–203. doi:10.1093/cvr/cvt018

    Article  CAS  PubMed  Google Scholar 

  • Tsui AK, Marsden PA, Mazer CD, Adamson SL, Henkelman RM, Ho JJ, Wilson DF, Heximer SP, Connelly KA, Bolz SS, Lidington D, El-Beheiry MH, Dattani ND, Chen KM, Hare GM (2011) Priming of hypoxia-inducible factor by neuronal nitric oxide synthase is essential for adaptive responses to severe anemia. Proc Natl Acad Sci U S A 108(42):17544–17549. doi:10.1073/pnas.1114026108

    Article  PubMed  PubMed Central  Google Scholar 

  • Ueda K, Valdivia C, Medeiros-Domingo A, Tester DJ, Vatta M, Farrugia G, Ackerman MJ, Makielski JC (2008) Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proc Natl Acad Sci U S A 105(27):9355–9360. doi:10.1073/pnas.0801294105

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Eerden BC, Weissgerber P, Fratzl-Zelman N, Olausson J, Hoenderop JG, Schreuders-Koedam M, Eijken M, Roschger P, de Vries TJ, Chiba H, Klaushofer K, Flockerzi V, Bindels RJ, Freichel M, van Leeuwen JP (2012) The transient receptor potential channel TRPV6 is dynamically expressed in bone cells but is not crucial for bone mineralization in mice. J Cell Physiol 227(5):1951–1959. doi:10.1002/jcp.22923

    Article  CAS  PubMed  Google Scholar 

  • Williams JC, Armesilla AL, Mohamed TM, Hagarty CL, McIntyre FH, Schomburg S, Zaki AO, Oceandy D, Cartwright EJ, Buch MH, Emerson M, Neyses L (2006) The sarcolemmal calcium pump, alpha-1 syntrophin, and neuronal nitric-oxide synthase are parts of a macromolecular protein complex. J Biol Chem 281(33):23341–23348. doi:10.1074/jbc.M513341200

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Zhang T, Bossuyt J, Li X, McKinsey TA, Dedman JR, Olson EN, Chen J, Brown JH, Bers DM (2006) Local InsP3-dependent perinuclear Ca2+ signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest 116(3):675–682. doi:10.1172/jci27374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu X, Chang B, Blair NS, Sargent M, York AJ, Robbins J, Shull GE, Molkentin JD (2009) Plasma membrane Ca2 + −ATPase isoform 4 antagonizes cardiac hypertrophy in association with calcineurin inhibition in rodents. J Clin Invest 119(4):976–985. doi:10.1172/jci36693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaccolo M (2006) Phosphodiesterases and compartmentalized cAMP signalling in the heart. Eur J Cell Biol 85(7):693–697. doi:10.1016/j.ejcb.2006.01.002

    Article  CAS  PubMed  Google Scholar 

  • Zacharias DA, Kappen C (1999) Developmental expression of the four plasma membrane calcium ATPase (Pmca) genes in the mouse. Biochim Biophys Acta 1428(2–3):397–405

    Article  CAS  PubMed  Google Scholar 

  • Zhang YH, Casadei B (2012) Sub-cellular targeting of constitutive NOS in health and disease. J Mol Cell Cardiol 52(2):341–350. doi:10.1016/j.yjmcc.2011.09.006

    Article  CAS  PubMed  Google Scholar 

Download references

Compliance with Ethical Standards

Conflict of Interest Statement

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Delvac Oceandy .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Stafford, N., Neyses, L., Oceandy, D. (2017). The Control of Sub-plasma Membrane Calcium Signalling by the Plasma Membrane Calcium ATPase Pump PMCA4. In: Nikolaev, V., Zaccolo, M. (eds) Microdomains in the Cardiovascular System. Cardiac and Vascular Biology, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-319-54579-0_16

Download citation

Publish with us

Policies and ethics