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

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

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.

Keywords

Plasma membrane calcium ATPase Signal transduction Calcium microdomain Genetically encoded calcium indicator GCaMP2 

Notes

Compliance with Ethical Standards

Conflict of Interest Statement

The authors declare that they have no conflict of interest.

References

  1. 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):30111–30114CrossRefPubMedGoogle Scholar
  2. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. 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 CrossRefPubMedGoogle Scholar
  5. Bers DM (2000) Calcium fluxes involved in control of cardiac myocyte contraction. Circ Res 87(4):275–281CrossRefPubMedGoogle Scholar
  6. 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 976:356–366CrossRefPubMedGoogle Scholar
  7. Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89(4):1341–1378. doi: 10.1152/physrev.00032.2008 CrossRefPubMedGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262(5134):740–744CrossRefPubMedGoogle Scholar
  11. 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 CrossRefPubMedGoogle Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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 CrossRefPubMedGoogle Scholar
  15. 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):17981–17986CrossRefPubMedGoogle Scholar
  16. 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):6425–6430PubMedGoogle Scholar
  17. 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):32461–32467CrossRefPubMedGoogle Scholar
  18. 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):2930–2936PubMedGoogle Scholar
  19. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 CrossRefPubMedGoogle Scholar
  21. 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 CrossRefPubMedGoogle Scholar
  22. Fujimoto T (1993) Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol 120(5):1147–1157CrossRefPubMedGoogle Scholar
  23. 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 986:461–471CrossRefPubMedGoogle Scholar
  24. 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 CrossRefPubMedGoogle Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. 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 CrossRefPubMedGoogle Scholar
  27. 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):877–888CrossRefPubMedGoogle Scholar
  28. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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 CrossRefPubMedGoogle Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. 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 CrossRefPubMedGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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):19717–19725PubMedGoogle Scholar
  34. 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 CrossRefPubMedGoogle Scholar
  35. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 CrossRefPubMedGoogle Scholar
  37. 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):1591–1595CrossRefPubMedGoogle Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. 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 CrossRefPubMedGoogle Scholar
  40. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 CrossRefPubMedGoogle Scholar
  42. 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 CrossRefPubMedGoogle Scholar
  43. 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 CrossRefPubMedGoogle Scholar
  44. 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 CrossRefPubMedGoogle Scholar
  45. 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 CrossRefPubMedGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. 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 CrossRefPubMedGoogle Scholar
  48. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 CrossRefPubMedGoogle Scholar
  50. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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 CrossRefPubMedGoogle Scholar
  52. 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):217–230CrossRefPubMedGoogle Scholar
  53. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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):215–228CrossRefPubMedPubMedCentralGoogle Scholar
  55. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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 CrossRefPubMedGoogle Scholar
  57. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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):8588–8592PubMedGoogle Scholar
  59. 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 CrossRefPubMedGoogle Scholar
  60. 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 CrossRefPubMedGoogle Scholar
  61. 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 CrossRefPubMedGoogle Scholar
  62. Pedersen PL, Carafoli E (1987) Ion motive ATPases. I. Ubiquity, properties, and significance to cell function. Trends Biochem Sci 12:146–150CrossRefGoogle Scholar
  63. 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 CrossRefPubMedGoogle Scholar
  64. Schatzmann HJ (1966) ATP-dependent Ca++ − extrusion from human red cells. Experientia 22(6):364–365CrossRefPubMedGoogle Scholar
  65. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 CrossRefPubMedGoogle Scholar
  67. 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 CrossRefPubMedGoogle Scholar
  68. 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 CrossRefPubMedGoogle Scholar
  69. 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 CrossRefPubMedGoogle Scholar
  70. 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 CrossRefPubMedGoogle Scholar
  71. Souders CA, Bowers SL, Baudino TA (2009) Cardiac fibroblast: the renaissance cell. Circ Res 105(12):1164–1176. doi: 10.1161/circresaha.109.209809 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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):25993–26003PubMedGoogle Scholar
  73. Strehler EE (1991) Recent advances in the molecular characterization of plasma membrane Ca2+ pumps. J Membr Biol 120(1):1–15CrossRefPubMedGoogle Scholar
  74. Strehler EE, Zacharias DA (2001) Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 81(1):21–50CrossRefPubMedGoogle Scholar
  75. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 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 CrossRefPubMedGoogle Scholar
  78. 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 CrossRefPubMedGoogle Scholar
  79. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 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 CrossRefPubMedGoogle Scholar
  82. 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 CrossRefPubMedGoogle Scholar
  83. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 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 PubMedPubMedCentralGoogle Scholar
  85. 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 CrossRefPubMedGoogle Scholar
  86. 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):397–405CrossRefPubMedGoogle Scholar
  87. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Nicholas Stafford
    • 1
  • Ludwig Neyses
    • 1
    • 2
  • Delvac Oceandy
    • 1
  1. 1.Division of Cardiovascular SciencesThe University of ManchesterManchesterUK
  2. 2.University of LuxembourgEsch-sur-AlzetteLuxembourg

Personalised recommendations