Glucocorticoid stimulation increases cardiac contractility by SGK1-dependent SOCE-activation in rat cardiac myocytes

English version

Autoři: Michael Wester ^aff001; Anton Heller ^aff001; Michael Gruber ^aff002; Lars S. Maier ^aff001; Christian Schach ^aff001; Stefan Wagner ^aff001
Působiště autorů: University Heart Center Regensburg, University Hospital Regensburg, Regensburg, Germany ^aff001; Clinic for Anesthesiology, University Hospital Regensburg, Regensburg, Germany ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222341

Souhrn

Aims

Glucocorticoid (GC) stimulation has been shown to increase cardiac contractility by elevated intracellular [Ca] but the sources for Ca entry are unclear. This study aims to determine the role of store-operated Ca entry (SOCE) for GC-mediated inotropy.

Methods and results

Dexamethasone (Dex) pretreatment significantly increased cardiac contractile force ex vivo in Langendorff-perfused Sprague-Dawley rat hearts (2 mg/kg BW i.p. Dex 24 h prior to experiment). Moreover, Ca transient amplitude as well as fractional shortening were significantly enhanced in Fura-2-loaded isolated rat ventricular myocytes exposed to Dex (1 mg/mL Dex, 24 h). Interestingly, these Dex-dependent effects could be abolished in the presence of SOCE-inhibitors SKF-96356 (SKF, 2 μM) and BTP2 (5 μM). Ca transient kinetics (time to peak, decay time) were not affected by SOCE stimulation. Direct SOCE measurements revealed a negligible magnitude in untreated myocytes but a dramatic increase in SOCE upon Dex-pretreatment. Importantly, the Dex-dependent stimulation of SOCE could be blocked by inhibition of serum and glucocorticoid-regulated kinase 1 (SGK1) using EMD638683 (EMD, 50 μM). Dex preincubation also resulted in increased mRNA expression of proteins involved in SOCE (stromal interaction molecule 2, STIM2, and transient receptor potential cation channels 3/6, TRPC 3/6), which were also prevented in the presence of EMD.

Conclusion

Short-term GC-stimulation with Dex improves cardiac contractility by a SOCE-dependent mechanism, which appears to involve increased SGK1-dependent expression of the SOCE-related proteins. Since Ca transient kinetics were unaffected, SOCE appears to influence Ca cycling more by an integrated response across multiple cardiac cycles but not on a beat-to-beat basis.

Klíčová slova:

Biology and life sciences – Cell biology – Biochemistry – Physical sciences – Chemistry – Research and analysis methods – Proteins – Molecular biology – Neuroscience – Molecular biology techniques – Cellular types – Animal cells – Anatomy – Medicine and health sciences – Chemical compounds – Physiology – Molecular biology assays and analysis techniques – Gene expression and vector techniques – Physics – Biological tissue – Surgical and invasive medical procedures – Calcium channels – Electrophysiology – Neurophysiology – Protein expression – Muscle tissue – Muscle cells – Cardiomyocytes – Myofibrils – Sarcomeres – Cardiovascular anatomy – Heart – Functional electrical stimulation – Biophysics – Alkaloids – Caffeine

Zdroje

1. Libby P, Maroko PR, Bloor CM, Sobel BE, Braunwald E. Reduction of experimental myocardial infarct size by corticosteroid administration. J. Clin. Invest. 1973; 52: 599–607. doi: 10.1172/JCI107221 4685084

2. Spath JA, Lane DL, Lefer AM. Protective action of methylprednisolone on the myocardium during experimental myocardial ischemia in the cat. Circ. Res. 1974; 35: 44–51. doi: 10.1161/01.res.35.1.44 4841252

3. Valen G, Kawakami T, Tahepold P, Dumitrescu A, Lowbeer C, Vaage J. Glucocorticoid pretreatment protects cardiac function and induces cardiac heat shock protein 72. Am. J. Physiol. Heart Circ. Physiol. 2000; 279: H836–43. doi: 10.1152/ajpheart.2000.279.2.H836 10924084

4. Enc Y, Karaca P, Ayoglu U, Camur G, Kurc E, Cicek S. The acute cardioprotective effect of glucocorticoid in myocardial ischemia-reperfusion injury occurring during cardiopulmonary bypass. Heart Vessels. 2006; 21: 152–156. doi: 10.1007/s00380-005-0887-8 16715189

5. Checchia PA, Backer CL, Bronicki RA, Baden HP, Crawford SE, Green TP, et al. Dexamethasone reduces postoperative troponin levels in children undergoing cardiopulmonary bypass. Crit Care Med. 2003; 31: 1742–1745. doi: 10.1097/01.CCM.0000063443.32874.60 12794414

6. Liakopoulos OJ, Schmitto JD, Kazmaier S, Brauer A, Quintel M, Schoendube FA, et al. Cardiopulmonary and systemic effects of methylprednisolone in patients undergoing cardiac surgery. Ann Thorac Surg. 2007; 84: 110–8; discussion 118–9. doi: 10.1016/j.athoracsur.2007.01.003 17588396

7. Katzung BG, editor. Basic & clinical pharmacology. [New York]: McGraw-Hill; 2018.

8. Xue Q, Patterson AJ, Xiao D, Zhang L. Glucocorticoid modulates angiotensin II receptor expression patterns and protects the heart from ischemia and reperfusion injury. PLoS ONE. 2014; 9: e106827. doi: 10.1371/journal.pone.0106827 25265380

9. Pearl JM, Plank DM, McLean KM, Wagner CJ, Duffy JY. Glucocorticoids improve calcium cycling in cardiac myocytes after cardiopulmonary bypass. J Surg Res. 2011; 167: 279–286. doi: 10.1016/j.jss.2009.05.001 19726057

10. Itagaki K, Menconi M, Antoniu B, Zhang Q, Gonnella P, Soybel D, et al. Dexamethasone stimulates store-operated calcium entry and protein degradation in cultured L6 myotubes through a phospholipase2-dependent mechanism. Am. J. Physiol., Cell Physiol. 2010; 298: C1127–39. doi: 10.1152/ajpcell.00309.2009 20107037

11. Borst O, Schmidt E-M, Münzer P, Schönberger T, Towhid ST, Elvers M, et al. The serum- and glucocorticoid-inducible kinase 1 (SGK1) influences platelet calcium signaling and function by regulation of Orai1 expression in megakaryocytes. Blood. 2012; 119: 251–261. doi: 10.1182/blood-2011-06-359976 22031864

12. Eylenstein A, Schmidt S, Gu S, Yang W, Schmid E, Schmidt E-M, et al. Transcription factor NF-κB regulates expression of pore-forming Ca2+ channel unit, Orai1, and its activator, STIM1, to control Ca2+ entry and affect cellular functions. J. Biol. Chem. 2012; 287: 2719–2730. doi: 10.1074/jbc.M111.275925 22110130

13. Collins HE, Zhu-Mauldin X, Marchase RB, Chatham JC. STIM1/Orai1-mediated SOCE: current perspectives and potential roles in cardiac function and pathology. Am. J. Physiol. Heart Circ. Physiol. 2013; 305: H446–58. doi: 10.1152/ajpheart.00104.2013 23792674

14. Avila-Medina J, Mayoral-Gonzalez I, Dominguez-Rodriguez A, Gallardo-Castillo I, Ribas J, Ordoñez A, et al. The complex role of store operated calcium entry pathways and related proteins in the function of cardiac, skeletal and vascular smooth muscle cells. Front Physiol. 2018; 9: 257. doi: 10.3389/fphys.2018.00257 29618985

15. Bootman MD, Rietdorf K. Tissue specificity. Store-operated Ca2+ entry in cardiac myocytes. Adv Exp Med Biol. 2017; 993: 363–387. doi: 10.1007/978-3-319-57732-6_19 28900924

16. Luo X, Hojayev B, Jiang N, Wang ZV, Tandan S, Rakalin A, et al. STIM1-dependent store-operated Ca2+ entry is required for pathological cardiac hypertrophy. J. Mol. Cell. Cardiol. 2012; 52: 136–147. doi: 10.1016/j.yjmcc.2011.11.003 22108056

17. Hulot J-S, Fauconnier J, Ramanujam D, Chaanine A, Aubart F, Sassi Y, et al. Critical role for stromal interaction molecule 1 in cardiac hypertrophy. Circulation. 2011; 124: 796–805. doi: 10.1161/CIRCULATIONAHA.111.031229 21810664

18. Parekh AB, Putney JW. Store-operated calcium channels. Physiol. Rev. 2005; 85: 757–810. doi: 10.1152/physrev.00057.2003 15788710

19. Wagner S, Ruff HM, Weber SL, Bellmann S, Sowa T, Schulte T, et al. Reactive oxygen species-activated Ca/calmodulin kinase II δ is required for late INa augmentation leading to cellular Na and Ca overload. Circ. Res. 2011; 108: 555–565. doi: 10.1161/CIRCRESAHA.110.221911 21252154

20. Bers DM. Excitation-contraction coupling and cardiac contractile force. Dordrecht: Springer Netherlands; 2001.

21. Oakley RH, Cidlowski JA. Glucocorticoid signaling in the heart. A cardiomyocyte perspective. J Steroid Biochem Mol Biol. 2015; 153: 27–34. doi: 10.1016/j.jsbmb.2015.03.009 25804222

22. Sainte-Marie Y, Nguyen Dinh Cat A, Perrier R, Mangin L, Soukaseum C, Peuchmaur M, et al. Conditional glucocorticoid receptor expression in the heart induces atrio-ventricular block. FASEB J. 2007; 21: 3133–3141. doi: 10.1096/fj.07-8357com 17517920

23. Gardner JP, Zhang L. Glucocorticoid modulation of Ca2+ homeostasis in human B lymphoblasts. J. Physiol. (Lond.). 1999; 514: 385–396. doi: 10.1111/j.1469-7793.1999.385ae.x 9852321

24. Feske S. CRAC channelopathies. Pflugers Arch. 2010; 460: 417–435. doi: 10.1007/s00424-009-0777-5 20111871

25. Stiber J, Hawkins A, Zhang Z-S, Wang S, Burch J, Graham V, et al. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol. 2008; 10: 688–697. doi: 10.1038/ncb1731 18488020

26. Bartoli F, Sabourin J. Cardiac remodeling and disease. Current understanding of STIM1/Orai1-mediated store-operated Ca2+ entry in cardiac function and pathology. Adv Exp Med Biol. 2017; 993: 523–534. doi: 10.1007/978-3-319-57732-6_26 28900931

27. Collins HE, He L, Zou L, Qu J, Zhou L, Litovsky SH, et al. Stromal interaction molecule 1 is essential for normal cardiac homeostasis through modulation of ER and mitochondrial function. Am. J. Physiol. Heart Circ. Physiol. 2014; 306: H1231–9. doi: 10.1152/ajpheart.00075.2014 24585777

28. Parks C, Alam MA, Sullivan R, Mancarella S. STIM1-dependent Ca(2+) microdomains are required for myofilament remodeling and signaling in the heart. Sci Rep. 2016; 6: 25372. doi: 10.1038/srep25372 27150728

29. Völkers M, Dolatabadi N, Gude N, Most P, Sussman MA, Hassel D. Orai1 deficiency leads to heart failure and skeletal myopathy in zebrafish. J. Cell. Sci. 2012; 125: 287–294. doi: 10.1242/jcs.090464 22302996

30. Kiviluoto S, Decuypere J-P, de Smedt H, Missiaen L, Parys JB, Bultynck G. STIM1 as a key regulator for Ca2+ homeostasis in skeletal-muscle development and function. Skelet Muscle. 2011; 1: 16. doi: 10.1186/2044-5040-1-16 21798093

31. Sedova M, Klishin A, Huser J, Blatter LA. Capacitative Ca2+ entry is graded with degree of intracellular Ca2+ store depletion in bovine vascular endothelial cells. J. Physiol.(Lond.). 2000; 523 Pt 3: 549–559. doi: 10.1111/j.1469-7793.2000.t01-3-00549.x

32. Sweeney ZK, Minatti A, Button DC, Patrick S. Small-molecule inhibitors of store-operated calcium entry. ChemMedChem. 2009; 4: 706–718. doi: 10.1002/cmdc.200800452 19330784

33. Merritt JE, Armstrong WP, Benham CD, Hallam TJ, Jacob R, Jaxa-Chamiec A, et al. SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochemical Journal. 1990; 271: 515–522. doi: 10.1042/bj2710515 2173565

34. Gao H, Wang F, Wang W, Makarewich CA, Zhang H, Kubo H, et al. Ca2+ influx through L-type Ca2+ channels and transient receptor potential channels activates pathological hypertrophy signaling. J. Mol. Cell. Cardiol. 2012; 53: 657–667. doi: 10.1016/j.yjmcc.2012.08.005 22921230

35. Jairaman A, Prakriya M. Molecular pharmacology of store-operated CRAC channels. Channels (Austin). 2013; 7: 402–414. doi: 10.4161/chan.25292 23807116

36. Ji Y, Guo X, Zhang Z, Huang Z, Zhu J, Chen Q-H, et al. CaMKIIδ meditates phenylephrine induced cardiomyocyte hypertrophy through store-operated Ca2+ entry. Cardiovasc Pathol. 2017; 27: 9–17. doi: 10.1016/j.carpath.2016.11.004 27940402

37. Zhao G, Li T, Brochet DXP, Rosenberg PB, Lederer WJ. STIM1 enhances SR Ca2+ content through binding phospholamban in rat ventricular myocytes. Proc Natl Acad Sci U S A. 2015; 112: E4792–801. doi: 10.1073/pnas.1423295112 26261328

38. Troupes CD, Wallner M, Borghetti G, Zhang C, Mohsin S, Lewinski D von, et al. Role of STIM1 (Stromal Interaction Molecule 1) in Hypertrophy-Related Contractile Dysfunction. Circ. Res. 2017; 121: 125–136. doi: 10.1161/CIRCRESAHA.117.311094 28592415

39. Obejero-Paz CA, Lakshmanan M, Jones SW, Scarpa A. Effects of dexamethasone on L-type calcium currents in the A7r5 smooth muscle-derived cell line. FEBS Lett. 1993; 333: 73–77. doi: 10.1016/0014-5793(93)80377-7 8224174

40. Wang L, Feng ZP, Duff HJ. Glucocorticoid regulation of cardiac K+ currents and L-type Ca2+ current in neonatal mice. Circ. Res. 1999; 85: 168–173. doi: 10.1161/01.res.85.2.168 10417398

41. De P, Roy SG, Kar D, Bandyopadhyay A. Excess of glucocorticoid induces myocardial remodeling and alteration of calcium signaling in cardiomyocytes. J Endocrinol. 2011; 209: 105–114. doi: 10.1530/JOE-10-0431 21282255

42. Eisner V, Csordas G, Hajnoczky G. Interactions between sarco-endoplasmic reticulum and mitochondria in cardiac and skeletal muscle—pivotal roles in Ca2+ and reactive oxygen species signaling. J. Cell. Sci. 2013; 126: 2965–2978. doi: 10.1242/jcs.093609 23843617

43. Spurgeon HA, Stern MD, Baartz G, Raffaeli S, Hansford RG, Talo A, et al. Simultaneous measurement of Ca2+, contraction, and potential in cardiac myocytes. Am J Physiol. 1990; 258: H574–86. doi: 10.1152/ajpheart.1990.258.2.H574 2309919

44. Endoh M. Cardiac α1-adrenoceptors and inotropy. Myofilament Ca2+ sensitivity, intracellular Ca2+ mobilization, signaling pathway, and pathophysiological relevance. Circ. Res. 2016; 119: 587–590. doi: 10.1161/CIRCRESAHA.116.309502 27539971

45. Lang F, Eylenstein A, Shumilina E. Regulation of Orai1/STIM1 by the kinases SGK1 and AMPK. Cell Calcium. 2012; 52: 347–354. doi: 10.1016/j.ceca.2012.05.005 22682960

46. Lang F, Böhmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V. (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol. Rev. 2006; 86: 1151–1178. doi: 10.1152/physrev.00050.2005 17015487

47. Ackermann TF, Boini KM, Beier N, Scholz W, Fuchss T, Lang F. EMD638683, a novel SGK inhibitor with antihypertensive potency. Cell Physiol Biochem. 2011; 28: 137–146. doi: 10.1159/000331722 21865856

48. Voelkl J, Pasham V, Ahmed MSE, Walker B, Szteyn K, Kuhl D, et al. SGK1-dependent stimulation of cardiac Na+/H+ exchanger NHE-1 by dexamethasone. Cell Physiol Biochem. 2013; 32: 25–38. doi: 10.1159/000350120 23860121

49. Correll RN, Goonasekera SA, van Berlo JH, Burr AR, Accornero F, Zhang H, et al. STIM1 elevation in the heart results in aberrant Ca2+ handling and cardiomyopathy. J. Mol. Cell. Cardiol. 2015; 87: 38–47. doi: 10.1016/j.yjmcc.2015.07.032 26241845

50. Voelkers M, Salz M, Herzog N, Frank D, Dolatabadi N, Frey N, et al. Orai1 and STIM1 regulate normal and hypertrophic growth in cardiomyocytes. J. Mol. Cell. Cardiol. 2010; 48: 1329–1334. doi: 10.1016/j.yjmcc.2010.01.020 20138887

51. Park CY, Shcheglovitov A, Dolmetsch R. The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science. 2010; 330: 101–105. doi: 10.1126/science.1191027 20929812

52. Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S, Soboloff J, et al. The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science. 2010; 330: 105–109. doi: 10.1126/science.1191086 20929813

53. Soboloff J, Rothberg BS, Madesh M, Gill DL. STIM proteins. Dynamic calcium signal transducers. Nat Rev Mol Cell Biol. 2012; 13: 549–565. doi: 10.1038/nrm3414 22914293

54. Cheng KT, Ong HL, Liu X, Ambudkar IS. Contribution and regulation of TRPC channels in store-operated Ca2+ entry. Curr Top Membr. 2013; 71: 149–179. doi: 10.1016/B978-0-12-407870-3.00007-X 23890115

55. Eder P, Molkentin JD. TRPC channels as effectors of cardiac hypertrophy. Circ. Res. 2011; 108: 265–272. doi: 10.1161/CIRCRESAHA.110.225888 21252153

56. Watanabe H, Murakami M, Ohba T, Takahashi Y, Ito H. TRP channel and cardiovascular disease. Pharmacology & Therapeutics. 2008; 118: 337–351. doi: 10.1016/j.pharmthera.2008.03.008 18508125

57. Bush EW, Hood DB, Papst PJ, Chapo JA, Minobe W, Bristow MR, et al. Canonical transient receptor potential channels promote cardiomyocyte hypertrophy through activation of calcineurin signaling. J. Biol. Chem. 2006; 281: 33487–33496. doi: 10.1074/jbc.M605536200 16950785

58. Niizeki T, Takeishi Y, Kitahara T, Arimoto T, Ishino M, Bilim O, et al. Diacylglycerol kinase-ε restores cardiac dysfunction under chronic pressure overload. A new specific regulator of Gαq signaling cascade. Am. J. Physiol. Heart Circ. Physiol. 2008; 295: H245–55. doi: 10.1152/ajpheart.00066.2008 18487437

59. Kuwahara K, Wang Y, McAnally J, Richardson JA, Bassel-Duby R, Hill JA, et al. TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J. Clin. Invest. 2006; 116: 3114–3126. doi: 10.1172/JCI27702 17099778

60. Zannas AS, Jia M, Hafner K, Baumert J, Wiechmann T, Pape JC, et al. Epigenetic upregulation of FKBP5 by aging and stress contributes to NF-κB-driven inflammation and cardiovascular risk. Proc Natl Acad Sci U S A. 2019; 116: 11370–11379. doi: 10.1073/pnas.1816847116 31113877

61. Song R, Hu X, Zhang L. Glucocorticoids and programming of the microenvironment in heart. J Endocrinol. 2019. doi: 10.1530/JOE-18-0672 31018174

62. Gao X, Wu X, Yan J, Zhang J, Zhao W, DeMarco D, et al. Transcriptional regulation of stress kinase JNK2 in pro-arrhythmic CaMKIIδ expression in the aged atrium. Cardiovasc Res. 2018; 114: 737–746. doi: 10.1093/cvr/cvy011 29360953

63. Yan J, Thomson JK, Zhao W, Gao X, Huang F, Chen B, et al. Role of Stress Kinase JNK in Binge Alcohol-Evoked Atrial Arrhythmia. J Am Coll Cardiol. 2018; 71: 1459–1470. doi: 10.1016/j.jacc.2018.01.060 29598867

64. Wolkowicz PE, Huang J, Umeda PK, Sharifov OF, Tabengwa E, Halloran BA, et al. Pharmacological evidence for Orai channel activation as a source of cardiac abnormal automaticity. Eur. J. Pharmacol. 2011; 668: 208–216. doi: 10.1016/j.ejphar.2011.06.025 21745466