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PMID: 22155237 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The human phospholamban Arg14-deletion mutant localizes to plasma membrane and interacts with the Na/K-ATPase.

Journal of molecular and cellular cardiology ·Vol. 52 ·No. 3 ·2012-03-00 ·Pages 773-82

Haghighi K, Pritchard T, Bossuyt J, Waggoner JR, Yuan Q, Fan GC, Osinska H, Anjak A, Rubinstein J, Robbins J, Bers DM, Kranias EG

Abstract

Depressed Ca-handling in cardiomyocytes is frequently attributed to impaired sarcoplasmic reticulum (SR) function in human and experimental heart failure. Phospholamban (PLN) is a key regulator of SR and cardiac function, and PLN mutations in humans have been associated with dilated cardiomyopathy (DCM). We previously reported the deletion of the highly conserved amino acid residue arginine 14 (nucleic acids 39, 40 and 41) in DCM patients. This basic amino acid is important in maintaining the upstream consensus sequence for PKA phosphorylation of Ser 16 in PLN. To assess the function of this mutant PLN, we introduced the PLN-R14Del in cardiac myocytes of the PLN null mouse. Transgenic lines expressing mutant PLN-R14Del at similar protein levels to wild types exhibited no inhibition of the initial rates of oxalate-facilitated SR Ca uptake compared to PLN-knockouts (PLN-KO). The contractile parameters and Ca-kinetics also remained highly stimulated in PLN-R14Del cardiomyocytes, similar to PLN-KO, and isoproterenol did not further stimulate these hyper-contractile basal parameters. Consistent with the lack of inhibition on SR Ca-transport and contractility, confocal microscopy indicated that the PLN-R14Del failed to co-localize with SERCA2a. Moreover, PLN-R14Del did not co-immunoprecipitate with SERCA2a (as did WT-PLN), but rather co-immunoprecipitated with the sarcolemmal Na/K-ATPase (NKA) and stimulated NKA activity. In addition, studies in HEK cells indicated significant fluorescence resonance energy transfer between PLN-R14Del-YFP and NKAα1-CFP, but not with the NKA regulator phospholemman. Despite the enhanced cardiac function in PLN-R14Del hearts (as in PLN-knockouts), there was cardiac hypertrophy (unlike PLN-KO) coupled with activation of Akt and the MAPK pathways. Thus, human PLN-R14Del is misrouted to the sarcolemma, in the absence of endogenous PLN, and alters NKA activity, leading to cardiac remodeling.

MeSH Terms
Animals Calcium/metabolism Calcium-Binding Proteins/genetics,metabolism Cardiomegaly/genetics,metabolism,pathology Cell Membrane/metabolism Enzyme Activation/genetics Humans Male Mice Mice, Transgenic Mutant Proteins/genetics,metabolism Myocytes, Cardiac/metabolism,pathology Protein Binding Protein Transport Sarcoplasmic Reticulum/metabolism Sequence Deletion Signal Transduction Sodium-Potassium-Exchanging ATPase/metabolism Ventricular Remodeling/genetics
Chemicals
Calcium-Binding Proteins Mutant Proteins phospholamban Sodium-Potassium-Exchanging ATPase Calcium
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Haghighi Kobra
Department of Pharmacology and Cell Biophysics, University of Cincinnati, College of Medicine, Cincinnati, OH 45267-0575, USA.
Pritchard Tracy
Bossuyt Julie
Waggoner Jason R
Yuan Qunying
Fan Guo-Chang
Osinska Hanna
Anjak Ahmad
Rubinstein Jack
Robbins Jeffrey
Bers Donald M
Kranias Evangelia G
References (45)
45 references, click to expand
  1. The presence of Lys27 instead of Asn27 in human phospholamban promotes sarcoplasmic reticulum Ca2+-ATPase superinhibition and cardiac remodeling.
    Circulation. 2006 Feb 21;113(7):995-1004 PMID: 16476846
  2. A single site (Ser16) phosphorylation in phospholamban is sufficient in mediating its maximal cardiac responses to beta -agonists.
    J Biol Chem. 2000 Dec 8;275(49):38938-43 PMID: 10988285
  3. Hypercholesterolemia and myocardial function evaluated via tissue doppler imaging.
    Cardiovasc Ultrasound. 2009 Nov 27;7:56 PMID: 19943937
  4. Phospholemman-phosphorylation mediates the beta-adrenergic effects on Na/K pump function in cardiac myocytes.
    Circ Res. 2005 Aug 5;97(3):252-9 PMID: 16002746
  5. Phospholamban and cardiac contractile function.
    J Mol Cell Cardiol. 2000 Dec;32(12):2131-9 PMID: 11112989
  6. The role of p38 in the regulation of Na+-Ca2+ exchanger expression in adult cardiomyocytes.
    J Mol Cell Cardiol. 2005 May;38(5):735-43 PMID: 15850567
  7. Regulation of Na/K-ATPase beta1-subunit gene expression by ouabain and other hypertrophic stimuli in neonatal rat cardiac myocytes.
    Mol Cell Biochem. 2000 Dec;215(1-2):65-72 PMID: 11204457
  8. Altered myocardial gene expression reveals possible maladaptive processes in heterozygous and homozygous cardiac myosin-binding protein C knockout mice.
    Genomics. 2008 Jan;91(1):52-60 PMID: 18060737
  9. A mutation in the human phospholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy.
    Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1388-93 PMID: 16432188
  10. Regulation of Ncx1 gene expression in the normal and hypertrophic heart.
    Ann N Y Acad Sci. 2007 Mar;1099:195-203 PMID: 17446459
  11. Cellular trafficking of phospholamban and formation of functional sarcoplasmic reticulum during myocyte differentiation.
    Am J Physiol Cell Physiol. 2007 Jun;292(6):C2084-94 PMID: 17287364
  12. Sodium-hydrogen exchange inhibition attenuates glycoside-induced hypertrophy in rat ventricular myocytes.
    Cardiovasc Res. 2010 Jan 1;85(1):79-89 PMID: 19687166
  13. Maximal inhibition of SERCA2 Ca(2+) affinity by phospholamban in transgenic hearts overexpressing a non-phosphorylatable form of phospholamban.
    J Biol Chem. 2000 Apr 21;275(16):12129-35 PMID: 10766848
  14. Na(+)/K(+)-ATPase as a signal transducer.
    Eur J Biochem. 2002 May;269(10):2434-9 PMID: 12027880
  15. Phospholamban ablation and compensatory responses in the mammalian heart.
    Ann N Y Acad Sci. 1998 Sep 16;853:49-62 PMID: 10603936
  16. Cardiotonic steroids: potential endogenous sodium pump ligands with diverse function.
    Exp Biol Med (Maywood). 2002 Sep;227(8):561-9 PMID: 12192097
  17. Calcium pumps in health and disease.
    Physiol Rev. 2009 Oct;89(4):1341-78 PMID: 19789383
  18. Regulation of cardiac excitation and contraction by p21 activated kinase-1.
    Prog Biophys Mol Biol. 2008 Oct-Nov;98(2-3):238-50 PMID: 19351515
  19. The cytoplasmic domains of phospholamban and phospholemman associate with phospholipid membrane surfaces.
    Biochemistry. 2005 Dec 27;44(51):17016-26 PMID: 16363815
  20. Regulation of Ca2+ transport by cyclic 3',5'-AMP-dependent and calcium-calmodulin-dependent phosphorylation of cardiac sarcoplasmic reticulum.
    Biochim Biophys Acta. 1985 Feb 21;844(2):193-9 PMID: 2982423
  21. Structural similarities of Na,K-ATPase and SERCA, the Ca(2+)-ATPase of the sarcoplasmic reticulum.
    Biochem J. 2001 Jun 15;356(Pt 3):685-704 PMID: 11389677
  22. Phospholamban: a prominent regulator of myocardial contractility.
    Circ Res. 1996 Dec;79(6):1059-63 PMID: 8943944
  23. Chronic SR Ca2+-ATPase inhibition causes adaptive changes in cellular Ca2+ transport.
    Circ Res. 2003 Apr 18;92(7):769-76 PMID: 12637367
  24. Effects of phospholamban phosphorylation catalyzed by adenosine 3':5'-monophosphate- and calmodulin-dependent protein kinases on calcium transport ATPase of cardiac sarcoplasmic reticulum.
    J Mol Cell Cardiol. 1983 May;15(5):335-46 PMID: 6310131
  25. Distribution and structure-function relationship of myosin heavy chain isoforms in the adult mouse heart.
    J Biol Chem. 2007 Aug 17;282(33):24057-64 PMID: 17575272
  26. Endoplasmic reticulum protein targeting of phospholamban: a common role for an N-terminal di-arginine motif in ER retention?
    PLoS One. 2010 Jul 09;5(7):e11496 PMID: 20634894
  27. Calcium cycling and signaling in cardiac myocytes.
    Annu Rev Physiol. 2008;70:23-49 PMID: 17988210
  28. Phospholemman: its role in normal cardiac physiology and potential as a druggable target in disease.
    Curr Opin Pharmacol. 2009 Apr;9(2):160-6 PMID: 19195931
  29. Phospholamban: a crucial regulator of cardiac contractility.
    Nat Rev Mol Cell Biol. 2003 Jul;4(7):566-77 PMID: 12838339
  30. Cardiac-specific overexpression of phospholamban alters calcium kinetics and resultant cardiomyocyte mechanics in transgenic mice.
    J Clin Invest. 1996 Jan 15;97(2):533-9 PMID: 8567978
  31. SERCA2a in heart failure: role and therapeutic prospects.
    J Bioenerg Biomembr. 2005 Dec;37(6):375-80 PMID: 16691468
  32. New roles for an old enzyme: Na,K-ATPase emerges as an interesting drug target.
    J Intern Med. 2007 Jan;261(1):44-52 PMID: 17222167
  33. Ouabain triggers preconditioning through activation of the Na+,K+-ATPase signaling cascade in rat hearts.
    Cardiovasc Res. 2007 Feb 1;73(3):488-96 PMID: 17157283
  34. Förster transfer recovery reveals that phospholamban exchanges slowly from pentamers but rapidly from the SERCA regulatory complex.
    Circ Res. 2007 Nov 26;101(11):1123-9 PMID: 17975108
  35. Na+/K+-ATPase-mediated signal transduction and Na+/K+-ATPase regulation.
    Fundam Clin Pharmacol. 2008 Dec;22(6):615-21 PMID: 19049666
  36. Phospholamban: protein structure, mechanism of action, and role in cardiac function.
    Physiol Rev. 1998 Oct;78(4):921-47 PMID: 9790566
  37. Transgenic mice expressing Na+-K+-ATPase in smooth muscle decreases blood pressure.
    Am J Physiol Heart Circ Physiol. 2007 Aug;293(2):H1172-82 PMID: 17468335
  38. The Na-K-ATPase and calcium-signaling microdomains.
    Physiology (Bethesda). 2008 Aug;23:205-11 PMID: 18697994
  39. Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation.
    Circ Res. 1994 Sep;75(3):401-9 PMID: 8062415
  40. Current concepts in the treatment of congestive heart failure.
    Cardiology. 1997;88 Suppl 2:2-6 PMID: 9142429
  41. Genetic deletion of arginine 14 in phospholamban causes dilated cardiomyopathy with attenuated electrocardiographic R amplitudes.
    Heart Rhythm. 2009 Apr;6(4):480-6 PMID: 19324307
  42. Isoform specificity of the Na/K-ATPase association and regulation by phospholemman.
    J Biol Chem. 2009 Sep 25;284(39):26749-57 PMID: 19638348
  43. Phospholamban gene dosage effects in the mammalian heart.
    Circ Res. 1996 May;78(5):839-47 PMID: 8620604
  44. Mitogen-activated protein kinases in heart development and diseases.
    Circulation. 2007 Sep 18;116(12):1413-23 PMID: 17875982
  45. The enhanced contractility of the phospholamban-deficient mouse heart persists with aging.
    J Mol Cell Cardiol. 2001 May;33(5):1031-40 PMID: 11343424
Article Info
Journal
Journal of molecular and cellular cardiology
Abbr.
J Mol Cell Cardiol
ISSN
1095-8584
Published
2012-03-00
Epub
2011-00-01
Pages
773-82
Language
English
Region
England
NLM ID
0262322
PMCID
PMC3376549
Subset
IM
Grants
NHLBI NIH HHS · R37 HL026057 · United States
NHLBI NIH HHS · P50 HL077101-05 · United States
NHLBI NIH HHS · R01 HL081562 · United States
NHLBI NIH HHS · R01 HL026057-30 · United States
NHLBI NIH HHS · HL-81562 · United States
NHLBI NIH HHS · HL-026057 · United States
NHLBI NIH HHS · T32 HL007382 · United States
NHLBI NIH HHS · P50 HL077101 · United States
NHLBI NIH HHS · R37 HL030077 · United States
NHLBI NIH HHS · R01 HL064018-11 · United States
NHLBI NIH HHS · HL007382 · United States
NHLBI NIH HHS · HL-64018 · United States
NHLBI NIH HHS · R01 HL026057 · United States
NHLBI NIH HHS · HL-77101 · United States
NHLBI NIH HHS · R01 HL064018 · United States
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