The regulation of sarco(endo)plasmic reticulum calcium-ATPases (SERCA)
Publication: Canadian Journal of Physiology and Pharmacology
19 January 2015
Abstract
The sarco(endo)plasmic reticulum calcium ATPase (SERCA) is responsible for transporting calcium (Ca2+) from the cytosol into the lumen of the sarcoplasmic reticulum (SR) following muscular contraction. The Ca2+ sequestering activity of SERCA facilitates muscular relaxation in both cardiac and skeletal muscle. There are more than 10 distinct isoforms of SERCA expressed in different tissues. SERCA2a is the primary isoform expressed in cardiac tissue, whereas SERCA1a is the predominant isoform expressed in fast-twitch skeletal muscle. The Ca2+ sequestering activity of SERCA is regulated at the level of protein content and is further modified by the endogenous proteins phospholamban (PLN) and sarcolipin (SLN). Additionally, several novel mechanisms, including post-translational modifications and microRNAs (miRNAs) are emerging as integral regulators of Ca2+ transport activity. These regulatory mechanisms are clinically relevant, as dysregulated SERCA function has been implicated in the pathology of several disease states, including heart failure. Currently, several clinical trials are underway that utilize novel therapeutic approaches to restore SERCA2a activity in humans. The purpose of this review is to examine the regulatory mechanisms of the SERCA pump, with a particular emphasis on the influence of exercise in preventing the pathological conditions associated with impaired SERCA function.
Résumé
L’ATPase SERCA (« sarco(endoplasmic) reticulum calcium ATPase ») est responsable du transport du calcium (Ca2+) du cytosol à la lumière du réticulum sarcoplasmique (RS) à la suite de la contraction musculaire. L’activité de séquestration de Ca2+ de SERCA facilite la relaxation musculaire tant dans le muscle cardiaque que dans le muscle squelettique. Il existe plus de 10 formes distinctes de SERCA exprimées dans différents tissus. SERCA2a est la principale isoforme exprimée dans le tissu cardiaque alors que SERCA1a est l’isoforme prédominante du muscle squelettique à contraction rapide. L’activité de séquestration de Ca2+ de SERCA est régulée au niveau du contenu en protéine, et elle est modifiée en plus par deux protéines endogènes, le phospholamban (PLN) et la sarcolipine (SLN). En outre, plusieurs mécanismes nouveaux, dont les modifications post-traductionnelles et les microARN (miARN) émergent maintenant en tant que régulateurs intégraux de l’activité de transport du Ca2+. Ces mécanismes régulateurs sont pertinents sur le plan clinique, car la dérégulation de la fonction de SERCA a été impliquée dans plusieurs pathologies incluant l’insuffisance cardiaque. Actuellement, plusieurs essais cliniques en cours utilisent de nouvelles approches thérapeutiques afin de rétablir l’activité de SERCA2a chez l’humain. Le but de cet article de revue est d’examiner les mécanismes régulateurs de la pompe SERCA, en mettant l’emphase sur l’influence de l’exercice dans la prévention des conditions pathologiques associées à une déficience de la fonction de SERCA. [Traduit par la Rédaction]
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References
Adachi, T. 2010. Modulation of vascular sarco/endoplasmic reticulum calcium atpase in cardiovascular pathophysiology. In Advances in pharmacology. Edited by Paul M. Vanhoutte. Academic Press. pp. 165–195. [Available from www.sciencedirect.com/science/article/pii/S1054358910590069; accessed 1 October 2014].
Adachi T., Weisbrod R.M., Pimentel D.R., Ying J., Sharov V.S., Schöneich C., et al. 2004. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat. Med. 10(11): 1200–1207.
Ahn W., Lee M.G., Kim K.H., and Muallem S. 2003. Multiple effects of SERCA2b mutations associated with Darier’s disease. J. Biol. Chem. 278(23): 20795–20801.
Arai M., Alpert N.R., MacLennan D.H., Barton P., and Periasamy M. 1993. Alterations in sarcoplasmic reticulum gene expression in human heart failure. A possible mechanism for alterations in systolic and diastolic properties of the failing myocardium. Circ. Res. 72(2): 463–469.
Aronson D. and Krum H. 2012. Novel therapies in acute and chronic heart failure. Pharmacol. Ther. 135(1): 1–17.
Asahi M., Sugita Y., Kurzydlowski K., De Leon S., Tada M., Toyoshima C., et al. 2003. Sarcolipin regulates sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA) by binding to transmembrane helices alone or in association with phospholamban. Proc. Natl. Acad. Sci. U.S.A. 100(9): 5040–5045.
Babu G.J., Zheng Z., Natarajan P., Wheeler D., Janssen P.M., and Periasamy M. 2005. Overexpression of sarcolipin decreases myocyte contractility and calcium transient. Cardiovasc. Res. 65(1): 177–186.
Babu G.J., Bhupathy P., Carnes C.A., Billman G.E., and Periasamy M. 2007. Differential expression of sarcolipin protein during muscle development and cardiac pathophysiology. J. Mol. Cell. Cardiol. 43(2): 215–222.
Baker D.L., Dave V., Reed T., and Periasamy M. 1996. Multiple Sp1 binding sites in the cardiac/slow twitch muscle sarcoplasmic reticulum Ca2+-ATPase gene promoter are required for expression in Sol8 muscle cells. J. Biol. Chem. 271(10): 5921–5928.
Bal N.C., Maurya S.K., Sopariwala D.H., Sahoo S.K., Gupta S.C., Shaikh S.A., et al. 2012. Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat. Med. 18(10): 1575–1579.
Balagopal P., George D., Yarandi H., Funanage V., and Bayne E. 2005. Reversal of obesity-related hypoadiponectinemia by lifestyle intervention: a controlled, randomized study in obese adolescents. J. Clin. Endocrinol. Metab. 90(11): 6192–6197.
Ballal K., Wilson C.R., Harmancey R., and Taegtmeyer H. 2010. Obesogenic high fat western diet induces oxidative stress and apoptosis in rat heart. Mol. Cell. Biochem. 344(1–2): 221–230.
Barnes M., Gibson L.M., and Stephenson D.G. 2001. Increased muscle glycogen content is associated with increased capacity to respond to T-system depolarisation in mechanically skinned skeletal muscle fibres from the rat. Pflugers Arch. 442(1): 101–106.
Belke D.D. 2011. Swim-exercised mice show a decreased level of protein O-GlcNAcylation and expression of O-GlcNAc transferase in heart. J. Appl. Physiol. 111(1): 157–162.
Bennett C.E., Johnsen V.L., Shearer J., and Belke D.D. 2013. Exercise training mitigates aberrant cardiac protein O-GlcNAcylation in streptozotocin-induced diabetic mice. Life Sci. 92(11): 657–663.
Bers D.M. 1997. Ca transport during contraction and relaxation in mammalian ventricular muscle. Basic Res. Cardiol. 92(1): 1–10.
Bers D.M. 2002. Cardiac excitation–contraction coupling. Nature, 415(6868): 198–205.
Bhupathy P., Babu G.J., and Periasamy M. 2007. Sarcolipin and phospholamban as regulators of cardiac sarcoplasmic reticulum Ca2+ ATPase. J. Mol. Cell. Cardiol. 42(5): 903–911.
Bhupathy P., Babu G.J., Ito M., and Periasamy M. 2009. Threonine-5 at the N-terminus can modulate sarcolipin function in cardiac myocytes. J. Mol. Cell. Cardiol. 47(5): 723–729.
Bidasee K.R., Zhang Y., Shao C.H., Wang M., Patel K.P., Dincer Ü.D., et al. 2004. Diabetes increases formation of advanced glycation end products on sarco(endo)plasmic reticulum Ca2+-ATPase. Diabetes, 53(2): 463–473.
Boddu N.J., Theus S., Luo S., Wei J.Y., and Ranganathan G. 2014. Is the lack of adiponectin associated with increased ER/SR stress and inflammation in the heart? Adipocyte, 3(1): 10–18.
Bokník P., Unkel C., Kirchhefer U., Kleideiter U., Klein-Wiele O., Knapp J., et al. 1999. Regional expression of phospholamban in the human heart. Cardiovasc. Res. 43(1): 67–76.
Bombardier E., Smith I.C., Vigna C., Fajardo V.A., and Tupling A.R. 2013. Ablation of sarcolipin decreases the energy requirements for Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases in resting skeletal muscle. FEBS Lett. 587(11): 1687–1692.
Brandl C.J., deLeon S., Martin D.R., and MacLennan D.H. 1987. Adult forms of the Ca2+ATPase of sarcoplasmic reticulum. Expression in developing skeletal muscle. J. Biol. Chem. 262(8): 3768–3774. [accessed 2 October 2014].
Briggs F.N., Lee K.F., Wechsler A.W., and Jones L.R. 1992. Phospholamban expressed in slow-twitch and chronically stimulated fast-twitch muscles minimally affects calcium affinity of sarcoplasmic reticulum Ca(2+)-ATPase. J. Biol. Chem. 267(36): 26056–26061.
Bupha-Intr T., Laosiripisan J., and Wattanapermpool J. 2009. Moderate intensity of regular exercise improves cardiac SR Ca2+ uptake activity in ovariectomized rats. J. Appl. Physiol. 107(4): 1105–1112.
Callen D.F., Baker E., Lane S., Nancarrow J., Thompson A., Whitmore S.A., et al. 1991. Regional mapping of the Batten disease locus (CLN3) to human chromosome 16p12. Am. J. Hum. Genet. 49(6): 1372–1377.
Carneiro-Júnior M.A., Quintão-Júnior J.F., Drummond L.R., Lavorato V.N., Drummond F.R., da Cunha D.N.Q., et al. 2013. The benefits of endurance training in cardiomyocyte function in hypertensive rats are reversed within four weeks of detraining. J. Mol. Cell. Cardiol. 57: 119–128.
Chang K.C., Figueredo V.M., Schreur J.H., Kariya K., Weiner M.W., Simpson P.C., et al. 1997. Thyroid hormone improves function and Ca2+ handling in pressure overload hypertrophy. Association with increased sarcoplasmic reticulum Ca2+-ATPase and alpha-myosin heavy chain in rat hearts. J. Clin. Invest. 100(7): 1742–1749.
Choi Y.S., Kim S., and Pak Y.K. 2001. Mitochondrial transcription factor A (mtTFA) and diabetes. Diabetes Res. Clin. Pract. 54(Suppl. 2): S3–S9.
Ciloglu F., Peker I., Pehlivan A., Karacabey K., Ilhan N., Saygin O., et al. 2005. Exercise intensity and its effects on thyroid hormones. Neuro Endocrinol. Lett. 26(6): 830–834.
Clark R.J., McDonough P.M., Swanson E., Trost S.U., Suzuki M., Fukuda M., et al. 2003. Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J. Biol. Chem. 278(45): 44230–44237.
Cuenda A., Centeno F., and Gutierrez-Merino C. 1991. Modulation by phosphorylation of glycogen phosphorylase–sarcoplasmic reticulum interaction. FEBS Lett. 283(2): 273–276.
Dally S., Bredoux R., Corvazier E., Andersen J.P., Clausen J.D., Dode L., et al. 2006. Ca2+-ATPases in non-failing and failing heart: evidence for a novel cardiac sarco/endoplasmic reticulum Ca2+-ATPase 2 isoform (SERCA2c). Biochem. J. 395(2): 249.
De Maio A. 1999. Heat shock proteins: facts, thoughts, and dreams. Shock, 11(1): 1–12.
Del Monte F., Harding S.E., Schmidt U., Matsui T., Kang Z.B., Dec G.W., et al. 1999. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation, 100(23): 2308–2311.
Del Monte F., Harding S.E., Dec G.W., Gwathmey J.K., and Hajjar R.J. 2002. Targeting phospholamban by gene transfer in human heart failure. Circulation, 105(8): 904–907.
Dhitavat J., Dode L., Leslie N., Sakuntabhai A., Lorette G., and Hovnanian A. 2003. Mutations in the sarcoplasmic/endoplasmic reticulum Ca2+ ATPase isoform cause Darier’s disease. J. Invest. Dermatol. 121(3): 486–489.
Duhamel T.A., Green H.J., Perco J.G., and Ouyang J. 2005. Metabolic and sarcoplasmic reticulum Ca2+ cycling responses in human muscle 4 days following prolonged exercise. Can. J. Physiol. Pharmacol. 83(7): 643–655.
Duhamel T.A., Green H.J., Perco J.G., and Ouyang J. 2006. Comparative effects of a low-carbohydrate diet and exercise plus a low-carbohydrate diet on muscle sarcoplasmic reticulum responses in males. Am. J. Physiol. Cell Physiol. 291(4): C607–C617.
Entman M.L., Bornet E.P., Barber A.J., Schwartz A., Levey G.S., Lehotay D.C., et al. 1977a. The cardiac sarcoplasmic reticulum–glycogenolytic complex. A possible effector site for cyclic AMP. Biochim. Biophys. Acta, 499(2): 228–237.
Entman M.L., Bornet E.P., Van Winkle W.B., Goldstein M.A., and Schwartz A. 1977b. Association of glycogenolysis with cardiac sarcoplasmic reticulum: II. Effect of glycogen depletion, deoxycholate solubilization and cardiac ischemia: evidence for a phorphorylase kinase membrane complex. J. Mol. Cell. Cardiol. 9(7): 515–528.
Entman M.L., Keslensky S.S., Chu A., and Van Winkle W.B. 1980. The sarcoplasmic reticulum–glycogenolytic complex in mammalian fast twitch skeletal muscle. Proposed in vitro counterpart of the contraction-activated glycogenolytic pool. J. Biol. Chem. 255(13): 6245–6252.
Fabiato A. 1983. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol. 245(1): C1–C14.
Favero T.G., Colter D., Hooper P.F., and Abramson J.J. 1998. Hypochlorous acid inhibits Ca2+-ATPase from skeletal muscle sarcoplasmic reticulum. J. Appl. Physiol. 84(2): 425–430. [accessed 17 November 2014].
Flesch M. 2001. On the trail of cardiac specific transcription factors. Cardiovasc. Res. 50(1): 3–6.
Foster D.B., Liu T., Rucker J., O’Meally R.N., Devine L.R., Cole R.N., et al. 2013. The cardiac acetyl-lysine proteome. PLoS One, 8(7): e67513.
Gamu D., Bombardier E., Smith I.C., Fajardo V.A., and Tupling A.R. 2014. Sarcolipin provides a novel muscle-based mechanism for adaptive thermogenesis. Exerc. Sport Sci. Rev. 42(3): 136–142.
Gehrig S.M., van der Poel C., Sayer T.A., Schertzer J.D., Henstridge D.C., Church J.E., et al. 2012. Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature, 484(7394): 394–398.
Gélébart P., Martin V., Enouf J., and Papp B. 2003. Identification of a new SERCA2 splice variant regulated during monocytic differentiation. Biochem. Biophys. Res. Commun. 303(2): 676–684.
Gheorghiade M., Blair J.E.A., Filippatos G.S., Macarie C., Ruzyllo W., Korewicki J., et al. 2008. Hemodynamic, echocardiographic, and neurohormonal effects of istaroxime, a novel intravenous inotropic and lusitropic agent: a randomized controlled trial in patients hospitalized with heart failure. J. Am. Coll. Cardiol. 51(23): 2276–2285.
Ghezzi P. 2005. Oxidoreduction of protein thiols in redox regulation. Biochem. Soc. Trans. 33(6): 1378.
Gleyzer N., Vercauteren K., and Scarpulla R.C. 2005. Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol. Cell. Biol. 25(4): 1354–1366.
Gramolini A.O., Trivieri M.G., Oudit G.Y., Kislinger T., Li W., Patel M.M., et al. 2006. Cardiac-specific overexpression of sarcolipin in phospholamban null mice impairs myocyte function that is restored by phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 103(7): 2446–2451.
Green H.J., Ballantyne C.S., MacDougall J.D., Tarnopolsky M.A., and Schertzer J.D. 2003. Adaptations in human muscle sarcoplasmic reticulum to prolonged submaximal training. J. Appl. Physiol. 94(5): 2034–2042.
Green H.J., Burnett M., Kollias H., Ouyang J., Smith I., and Tupling S. 2011. Malleability of human skeletal muscle sarcoplasmic reticulum to short-term training. Appl. Physiol. Nutr. Metab. 36(6): 904–912.
Gunteski-Hamblin A.M., Greeb J., and Shull G.E. 1988. A novel Ca2+ pump expressed in brain, kidney, and stomach is encoded by an alternative transcript of the slow-twitch muscle sarcoplasmic reticulum Ca-ATPase gene. Identification of cDNAs encoding Ca2+ and other cation-transporting ATPases using an oligonucleotide probe derived from the ATP-binding site. J. Biol. Chem. 263(29): 15032–15040.
Guo J., Bian Y., Bai R., Li H., Fu M., and Xiao C. 2013. Globular adiponectin attenuates myocardial ischemia/reperfusion injury by upregulating endoplasmic reticulum Ca2+-ATPase activity and inhibiting endoplasmic reticulum stress. J. Cardiovasc. Pharmacol. 62(2): 143–153.
Gurha P., Abreu-Goodger C., Wang T., Ramirez M.O., Drumond A.L., van Dongen S., et al. 2012. Targeted deletion of microRNA-22 promotes stress-induced cardiac dilation and contractile dysfunction. Circulation, 125(22): 2751–2761.
Hartong R., Wang N., Kurokawa R., Lazar M.A., Glass C.K., Apriletti J.W., et al. 1994. Delineation of three different thyroid hormone-response elements in promoter of rat sarcoplasmic reticulum Ca2+ATPase gene. Demonstration that retinoid X receptor binds 5′ to thyroid hormone receptor in response element 1. J. Biol. Chem. 269(17): 13021–13029.
Hasenfuss G. 1998. Alterations of calcium-regulatory proteins in heart failure. Cardiovasc. Res. 37(2): 279–289.
Hovnanian A. 2007. SERCA pumps and human diseases. Subcell. Biochem. 45: 337–363.
Hu Y., Belke D., Suarez J., Swanson E., Clark R., Hoshijima M., et al. 2005. Adenovirus-mediated overexpression of O-GlcNAcase improves contractile function in the diabetic heart. Circ. Res. 96(9): 1006–1013.
Ikeuchi M., Matsusaka H., Kang D., Matsushima S., Ide T., Kubota T., et al. 2005. Overexpression of mitochondrial transcription factor a ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation, 112(5): 683–690.
Jardim-Messeder D., Camacho-Pereira J., and Galina A. 2012. 3-Bromopyruvate inhibits calcium uptake by sarcoplasmic reticulum vesicles but not SERCA ATP hydrolysis activity. Int. J. Biochem. Cell Biol. 44(5): 801–807.
Jaski B.E., Jessup M.L., Mancini D.M., Cappola T.P., Pauly D.F., Greenberg B., et al. 2009. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID Trial), a first-in-human phase 1/2 clinical trial. J. Card. Fail. 15(3): 171–181.
Jessup M., Greenberg B., Mancini D., Cappola T., Pauly D.F., Jaski B., et al. 2011. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID): a phase 2 trial of intracoronary gene therapy of sarcoplasmic reticulum Ca2+-ATPase in patients with advanced heart failure. Circulation, 124(3): 304–313.
Johnsen V.L., Belke D.D., Hughey C.C., Hittel D.S., Hepple R.T., Koch L.G., et al. 2013. Enhanced cardiac protein glycosylation (O-GlcNAc) of selected mitochondrial proteins in rats artificially selected for low running capacity. Physiol. Genomics, 45(1): 17–25.
Kalyanasundaram A., Lacombe V.A., Belevych A.E., Brunello L., Carnes C.A., Janssen P.M.L., et al. 2013. Up-regulation of sarcoplasmic reticulum Ca(2+) uptake leads to cardiac hypertrophy, contractile dysfunction and early mortality in mice deficient in CASQ2. Cardiovasc. Res. 98(2): 297–306.
Kawase Y. and Hajjar R.J. 2008. The cardiac sarcoplasmic/endoplasmic reticulum calcium ATPase: a potent target for cardiovascular diseases. Nat. Clin. Pract. Cardiovasc. Med. 5(9): 554–565.
Kaye D.M., Preovolos A., Marshall T., Byrne M., Hoshijima M., Hajjar R., et al. 2007. Percutaneous cardiac recirculation-mediated gene transfer of an inhibitory phospholamban peptide reverses advanced heart failure in large animals. J. Am. Coll. Cardiol. 50(3): 253–260.
Kemi O.J., Ellingsen O., Ceci M., Grimaldi S., Smith G.L., Condorelli G., et al. 2007. Aerobic interval training enhances cardiomyocyte contractility and Ca2+ cycling by phosphorylation of CaMKII and Thr-17 of phospholamban. J. Mol. Cell. Cardiol. 43(3): 354–361.
Kemi O.J., Ceci M., Condorelli G., Smith G.L., and Wisloff U. 2008. Myocardial sarcoplasmic reticulum Ca2+ ATPase function is increased by aerobic interval training. Eur. J. Cardiovasc. Prev. Rehabil. 15(2): 145–148.
Kho C., Lee A., Jeong D., Oh J.G., Chaanine A.H., Kizana E., et al. 2011. SUMO1-dependent modulation of SERCA2a in heart failure. Nature, 477(7366): 601–605.
Kimura Y., Otsu K., Nishida K., Kuzuya T., and Tada M. 1994. Thyroid hormone enhances Ca2+ pumping activity of the cardiac sarcoplasmic reticulum by increasing Ca2+ ATPase and decreasing phospholamban expression. J. Mol. Cell. Cardiol. 26(9): 1145–1154.
Kinnunen S. and Mänttäri S. 2012. Specific effects of endurance and sprint training on protein expression of calsequestrin and SERCA in mouse skeletal muscle. J. Muscle Res. Cell Motil. 33(2): 123–130.
Kiss E., Jakab G., Kranias E.G., and Edes I. 1994. Thyroid hormone-induced alterations in phospholamban protein expression. Regulatory effects on sarcoplasmic reticulum Ca2+ transport and myocardial relaxation. Circ. Res. 75(2): 245–251.
Koss K.L., Ponniah S., Jones W.K., Grupp I.L., and Kranias E.G. 1995. Differential phospholamban gene expression in murine cardiac compartments. Molecular and physiological analyses. Circ. Res. 77(2): 342–353.
Kubo H., Libonati J.R., Kendrick Z.V., Paolone A., Gaughan J.P., and Houser S.R. 2003. Differential effects of exercise training on skeletal muscle SERCA gene expression. Med. Sci. Sports Exerc. 35(1): 27–31. [Accessed 5 October 2014].
Kumarswamy R., Lyon A.R., Volkmann I., Mills A.M., Bretthauer J., Pahuja A., et al. 2012. SERCA2a gene therapy restores microRNA-1 expression in heart failure via an Akt/FoxO3A-dependent pathway. Eur. Heart J. 33(9): 1067–1075.
Lalli M.J., Yong J., Prasad V., Hashimoto K., Plank D., Babu G.J., et al. 2001. Sarcoplasmic reticulum Ca2+ ATPase (SERCA) 1a structurally substitutes for SERCA2a in the cardiac sarcoplasmic reticulum and increases cardiac Ca2+ handling capacity. Circ. Res. 89(2): 160–167.
Lancel S., Zhang J., Evangelista A., Trucillo M.P., Tong X., Siwik D.A., et al. 2009. Nitroxyl activates SERCA in cardiac myocytes via glutathiolation of cysteine 674. Circ. Res. 104(6): 720–723.
Leberer E., Härtner K.T., Brandl C.J., Fujii J., Tada M., MacLennan D.H., et al. 1989. Slow/cardiac sarcoplasmic reticulum Ca2+-ATPase and phospholamban mRNAs are expressed in chronically stimulated rabbit fast-twitch muscle. Eur. J. Biochem. 185(1): 51–54.
Lees S.J., Franks P.D., Spangenburg E.E., and Williams J.H. 2001. Glycogen and glycogen phosphorylase associated with sarcoplasmic reticulum: effects of fatiguing activity. J. Appl. Physiol. 91(4): 1638–1644.
Leppik J.A., Aughey R.J., Medved I., Fairweather I., Carey M.F., and McKenna M.J. 2004. Prolonged exercise to fatigue in humans impairs skeletal muscle Na+-K+-ATPase activity, sarcoplasmic reticulum Ca2+ release, and Ca2+ uptake. J. Appl. Physiol. 97(4): 1414–1423.
Levitzki A. 1988. From epinephrine to cyclic AMP. Science, 241(4867): 800–806.
Liu J. and Brautigan D.L. 2000. Insulin-stimulated phosphorylation of the protein phosphatase-1 striated muscle glycogen-targeting subunit and activation of glycogen synthase. J. Biol. Chem. 275(21): 15940–15947.
Lokuta A.J., Maertz N.A., Meethal S.V., Potter K.T., Kamp T.J., Valdivia H.H., et al. 2005. Increased nitration of sarcoplasmic reticulum Ca2+-ATPase in human heart failure. Circulation, 111(8): 988–995.
Lompré A.M., Anger M., and Levitsky D. 1994. Sarco(endo)plasmic reticulum calcium pumps in the cardiovascular system: function and gene expression. J. Mol. Cell. Cardiol. 26(9): 1109–1121.
Loukianov E., Ji Y., Grupp I.L., Kirkpatrick D.L., Baker D.L., Loukianova T., et al. 1998. Enhanced myocardial contractility and increased Ca2+ transport function in transgenic hearts expressing the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+-ATPase. Circ. Res. 83(9): 889–897.
Lumini-Oliveira J., Magalhães J., Pereira C.V., Moreira A.C., Oliveira P.J., and Ascensão A. 2011. Endurance training reverts heart mitochondrial dysfunction, permeability transition and apoptotic signaling in long-term severe hyperglycemia. Mitochondrion, 11(1): 54–63.
MacDonnell S.M., Kubo H., Crabbe D.L., Renna B.F., Reger P.O., Mohara J., et al. 2005. Improved myocardial beta-adrenergic responsiveness and signaling with exercise training in hypertension. Circulation, 111(25): 3420–3428.
MacLennan D.H. and Kranias E.G. 2003. Phospholamban: a crucial regulator of cardiac contractility. Nat. Rev. Mol. Cell Biol. 4(7): 566–577.
Mercadier J.J., Lompré A.M., Duc P., Boheler K.R., Fraysse J.B., Wisnewsky C., et al. 1990. Altered sarcoplasmic reticulum Ca(2+)-ATPase gene expression in the human ventricle during end-stage heart failure. J. Clin. Invest. 85(1): 305–309.
Minamisawa S., Wang Y., Chen J., Ishikawa Y., Chien K.R., and Matsuoka R. 2003. Atrial chamber-specific expression of sarcolipin is regulated during development and hypertrophic remodeling. J. Biol. Chem. 278(11): 9570–9575.
Morissette M.P., Susser S.E., Stammers A.N., O’Hara K.A., Gardiner P.F., Sheppard P., et al. 2014. Differential regulation of the fiber type-specific gene expression of the sarcoplasmic reticulum calcium-ATPase isoforms induced by exercise training. J. Appl. Physiol. 117(5): 544–555.
Morris T.E. and Sulakhe P.V. 1997. Sarcoplasmic reticulum Ca(2+)-pump dysfunction in rat cardiomyocytes briefly exposed to hydroxyl radicals. Free Radic. Biol. Med. 22(1–2): 37–47.
Nagai R., Zarain-Herzberg A., Brandl C.J., Fujii J., Tada M., MacLennan D.H., et al. 1989. Regulation of myocardial Ca2+-ATPase and phospholamban mRNA expression in response to pressure overload and thyroid hormone. Proc. Natl. Acad. Sci. U.S.A. 86(8): 2966–2970.
Norby F.L., Wold L.E., Duan J., Hintz K.K., and Ren J. 2002. IGF-I attenuates diabetes-induced cardiac contractile dysfunction in ventricular myocytes. Am. J. Physiol. Endocrinol. Metab. 283(4): E658–E666.
Norrbom J., Sundberg C.J., Ameln H., Kraus W.E., Jansson E., and Gustafsson T. 2004. PGC-1alpha mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. J. Appl. Physiol. 96(1): 189–194.
Norrbom J., Wallman S.E., Gustafsson T., Rundqvist H., Jansson E., and Sundberg C.J. 2010. Training response of mitochondrial transcription factors in human skeletal muscle. Acta Physiol. (Oxf.), 198(1): 71–79.
Odermatt A., Taschner P.E., Khanna V.K., Busch H.F., Karpati G., Jablecki C.K., et al. 1996. Mutations in the gene-encoding SERCA1, the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+ ATPase, are associated with Brody disease. Nat. Genet. 14(2): 191–194.
Ørtenblad N., Nielsen J., Saltin B., and Holmberg H.-C. 2011. Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J. Physiol. 589(3): 711–725.
Otsu K., Fujii J., Periasamy M., Difilippantonio M., Uppender M., Ward D.C., et al. 1993. Chromosome mapping of five human cardiac and skeletal muscle sarcoplasmic reticulum protein genes. Genomics, 17(2): 507–509.
Park W.J. and Oh J.G. 2013. SERCA2a: a prime target for modulation of cardiac contractility during heart failure. BMB Rep. 46(5): 237–243.
Periasamy M. and Kalyanasundaram A. 2007. SERCA pump isoforms: Their role in calcium transport and disease. Muscle Nerve, 35(4): 430–442.
Periasamy M., Bhupathy P., and Babu G.J. 2008. Regulation of sarcoplasmic reticulum Ca2+ ATPase pump expression and its relevance to cardiac muscle physiology and pathology. Cardiovasc. Res. 77(2): 265–273.
Peters D.G., Mitchell-Felton H., and Kandarian S.C. 1999. Unloading induces transcriptional activation of the sarco(endo)plasmic reticulum Ca2+-ATPase 1 gene in muscle. Am. J. Physiol. 276(5): C1218–C1225.
Pischon T., Girman C.J., Hotamisligil G.S., Rifai N., Hu F.B., and Rimm E.B. 2004. Plasma adiponectin levels and risk of myocardial infarction in men. JAMA, 291(14): 1730–1737.
Reed T.D., Babu G.J., Ji Y., Zilberman A., Ver Heyen M., Wuytack F., et al. 2000. The expression of SR calcium transport ATPase and the Na(+)/Ca(2+)Exchanger are antithetically regulated during mouse cardiac development and in hypo/hyperthyroidism. J. Mol. Cell. Cardiol. 32(3): 453–464.
Rohrer D. and Dillmann W.H. 1988. Thyroid hormone markedly increases the mRNA coding for sarcoplasmic reticulum Ca2+-ATPase in the rat heart. J. Biol. Chem. 263(15): 6941–6944.
Sack M.N. 2011. Emerging characterization of the role of SIRT3-mediated mitochondrial protein deacetylation in the heart. Am. J. Physiol. Heart Circ. Physiol. 301(6): H2191–H2197.
Safwat Y., Yassin N., Gamal El Din M., and Kassem L. 2013. Modulation of skeletal muscle performance and SERCA by exercise and adiponectin gene therapy in insulin-resistant rat. DNA Cell Biol. 32(7): 378–385.
Sahoo S.K., Shaikh S.A., Sopariwala D.H., Bal N.C., and Periasamy M. 2013. Sarcolipin protein interaction with sarco(endo)plasmic reticulum Ca2+ ATPase (SERCA) is distinct from phospholamban protein, and only sarcolipin can promote uncoupling of the SERCA pump. J. Biol. Chem. 288(10): 6881–6889.
Schulte L.M., Navarro J., and Kandarian S.C. 1993. Regulation of sarcoplasmic reticulum calcium pump gene expression by hindlimb unweighting. Am. J. Physiol. 264(5): C1308–C1315.
Simpson K.A. and Singh M.A.F. 2008. Effects of exercise on adiponectin: a systematic review. Obesity (Silver Spring), 16(2): 241–256.
Smith I.C., Bombardier E., Vigna C., and Tupling A.R. 2013. ATP consumption by sarcoplasmic reticulum Ca2+ pumps accounts for 40–50% of resting metabolic rate in mouse fast and slow twitch skeletal muscle. PLoS One, 8(7): e68924.
Suarez J., Hu Y., Makino A., Fricovsky E., Wang H., and Dillmann W.H. 2008a. Alterations in mitochondrial function and cytosolic calcium induced by hyperglycemia are restored by mitochondrial transcription factor A in cardiomyocytes. Am. J. Physiol. Cell Physiol. 295(6): C1561–C1568.
Suarez J., Scott B., and Dillmann W.H. 2008b. Conditional increase in SERCA2a protein is able to reverse contractile dysfunction and abnormal calcium flux in established diabetic cardiomyopathy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(5): R1439–R1445.
Sulaiman M., Matta M.J., Sunderesan N.R., Gupta M.P., Periasamy M., and Gupta M. 2010. Resveratrol, an activator of SIRT1, upregulates sarcoplasmic calcium ATPase and improves cardiac function in diabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 298(3): H833–H843.
Takizawa T., Arai M., Tomaru K., Koitabashi N., Baker D.L., Periasamy M., et al. 2003. Transcription factor Sp1 regulates SERCA2 gene expression in pressure-overloaded hearts: a study using in vivo direct gene transfer into living myocardium. J. Mol. Cell. Cardiol. 35(7): 777–783.
Tang W.H., Cheng W.T., Kravtsov G.M., Tong X.Y., Hou X.Y., Chung S.K., et al. 2010. Cardiac contractile dysfunction during acute hyperglycemia due to impairment of SERCA by polyol pathway-mediated oxidative stress. Am. J. Physiol. Cell Physiol. 299(3): C643–C653.
Tilemann L., Lee A., Ishikawa K., Aguero J., Rapti K., Santos-Gallego C., et al. 2013. SUMO-1 gene transfer improves cardiac function in a large-animal model of heart failure. Sci. Transl. Med. 5(211): 211ra159.
Tong X., Ying J., Pimentel D.R., Trucillo M., Adachi T., and Cohen R.A. 2008. High glucose oxidizes SERCA cysteine-674 and prevents inhibition by nitric oxide of smooth muscle cell migration. J. Mol. Cell. Cardiol. 44(2): 361–369.
Toyoshima C. 2009. How Ca2+-ATPase pumps ions across the sarcoplasmic reticulum membrane. Biochim. Biophys. Acta, 1793(6): 941–946.
Toyoshima C. and Inesi G. 2004. Structural basis of ion pumping by Ca2+-ATPase of the sarcoplasmic reticulum. Annu. Rev. Biochem. 73: 269–292.
Tsien R.W. 1977. Cyclic AMP and contractile activity in heart. Adv. Cyclic Nucleotide Res. 8: 363–420.
Tsuji T., Del Monte F., Yoshikawa Y., Abe T., Shimizu J., Nakajima-Takenaka C., et al. 2009. Rescue of Ca2+ overload-induced left ventricular dysfunction by targeted ablation of phospholamban. Am. J. Physiol. Heart Circ. Physiol. 296(2): H310–H317.
Tupling A.R., Gramolini A.O., Duhamel T.A., Kondo H., Asahi M., Tsuchiya S.C., et al. 2004. HSP70 Binds to the fast-twitch skeletal muscle sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA1a) and prevents thermal inactivation. J. Biol. Chem. 279(50): 52382–52389.
Van Rechem C., Boulay G., Pinte S., Stankovic-Valentin N., Guérardel C., and Leprince D. 2010. Differential regulation of HIC1 target genes by CtBP and NuRD, via an acetylation/SUMOylation switch, in quiescent versus proliferating cells. Mol. Cell. Biol. 30(16): 4045–4059.
Villarreal-Molina M.T. and Antuna-Puente B. 2012. Adiponectin: anti-inflammatory and cardioprotective effects. Biochimie, 94(10): 2143–2149.
Wahlquist C., Jeong D., Rojas-Muñoz A., Kho C., Lee A., Mitsuyama S., et al. 2014. Inhibition of miR-25 improves cardiac contractility in the failing heart. Nature, 508(7497): 531–535.
Wang Y., Tao L., Yuan Y., Lau W.B., Li R., Lopez B.L., et al. 2009. Cardioprotective effect of adiponectin is partially mediated by its AMPK-independent antinitrative action. Am. J. Physiol. Endocrinol. Metab. 297(2): E384–E391.
Watanabe A., Arai M., Koitabashi N., Niwano K., Ohyama Y., Yamada Y., et al. 2011. Mitochondrial transcription factors TFAM and TFB2M regulate Serca2 gene transcription. Cardiovasc. Res. 90(1): 57–67.
Wisløff U., Loennechen J.P., Currie S., Smith G.L., and Ellingsen Ø. 2002. Aerobic exercise reduces cardiomyocyte hypertrophy and increases contractility, Ca2+ sensitivity and SERCA-2 in rat after myocardial infarction. Cardiovasc. Res. 54(1): 162–174.
Wuytack F., Raeymaekers L., and Missiaen L. 2002. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium, 32(5–6): 279–305.
Xu K.Y. and Becker L.C. 1998. Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesticles. J. Histochem. Cytochem. 46(4): 419–427.
Xu K.Y., Zweier J.L., and Becker L.C. 1995. Functional coupling between glycolysis and sarcoplasmic reticulum Ca2+ transport. Circ. Res. 77(1): 88–97.
Xu K.Y., Zweier J.L., and Becker L.C. 1997. Hydroxyl radical inhibits sarcoplasmic reticulum Ca2+-ATPase function by direct attack on the ATP binding site. Circ. Res. 80(1): 76–81.
Yokoe S., Asahi M., Takeda T., Otsu K., Taniguchi N., Miyoshi E., et al. 2010. Inhibition of phospholamban phosphorylation by O-GlcNAcylation: implications for diabetic cardiomyopathy. Glycobiology, 20(10): 1217–1226.
Zarain-Herzberg A., Marques J., Sukovich D., and Periasamy M. 1994. Thyroid hormone receptor modulates the expression of the rabbit cardiac sarco (endo) plasmic reticulum Ca(2+)-ATPase gene. J. Biol. Chem. 269(2): 1460–1467.
Zhang Y., Fujii J., Phillips M.S., Chen H.-S., Karpati G., Yee W.-C., et al. 1995. Characterization of cDNA and Genomic DNA Encoding SERCA1, the Ca2+-ATPase of human fast-twitch skeletal muscle sarcoplasmic reticulum, and its elimination as a candidate gene for Brody Disease. Genomics, 30(3): 415–424.
Zhao W., Frank K.F., Chu G., Gerst M.J., Schmidt A.G., Ji Y., et al. 2003. Combined phospholamban ablation and SERCA1a overexpression result in a new hyperdynamic cardiac state. Cardiovasc. Res. 57(1): 71–81.
Zhao Y., Koebis M., Suo S., Ohno S., and Ishiura S. 2012. Regulation of the alternative splicing of sarcoplasmic reticulum Ca2+-ATPase1 (SERCA1) by phorbol 12-myristate 13-acetate (PMA) via a PKC pathway. Biochem. Biophys. Res. Commun. 423(2): 212–217.
Zheng J., Yancey D.M., Ahmed M.I., Wei C.-C., Powell P.C., Shanmugam M., et al. 2014. Increased sarcolipin expression and adrenergic drive in humans with preserved left ventricular ejection fraction and chronic isolated mitral regurgitation. Circ. Heart Fail. 7(1): 194–202.
Zsebo K., Yaroshinsky A., Rudy J.J., Wagner K., Greenberg B., Jessup M., et al. 2014. Long-term effects of AAV1/SERCA2a gene transfer in patients with severe heart failure: analysis of recurrent cardiovascular events and mortality. Circ. Res. 114(1): 101–108.
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Published In
Canadian Journal of Physiology and Pharmacology
Volume 93 • Number 10 • October 2015
Pages: 843 - 854
History
Received: 20 November 2014
Accepted: 8 January 2015
Accepted manuscript online: 19 January 2015
Version of record online: 19 January 2015
Notes
This Invited Review is part of a Special Issue entitled “2nd Cardiovascular Forum for Promoting Centers of Excellence and Young Investigators.”
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© 2015.
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Andrew N. Stammers, Shanel E. Susser, Naomi C. Hamm, Michael W. Hlynsky, Dustin E. Kimber, D. Scott Kehler, and Todd A. Duhamel. 2015. The regulation of sarco(endo)plasmic reticulum calcium-ATPases (SERCA). Canadian Journal of Physiology and Pharmacology.
93(10): 843-854. https://doi.org/10.1139/cjpp-2014-0463
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