The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
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Increased store-operated Ca2+ entry mediated by GNB5 and STIM1

  • Kang, Namju (Department of Oral Biology, BK21 PLUS Project, Yonsei University College of Dentistry) ;
  • Kang, Jung Yun (Department of Oral Biology, BK21 PLUS Project, Yonsei University College of Dentistry) ;
  • Park, Soonhong (Department of Oral Biology, BK21 PLUS Project, Yonsei University College of Dentistry) ;
  • Shin, Dong Min (Department of Oral Biology, BK21 PLUS Project, Yonsei University College of Dentistry)
  • Received : 2017.12.20
  • Accepted : 2018.02.19
  • Published : 2018.05.01
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Abstract

Recent human genetic studies have shown that $G{\beta}5$ is related to various clinical symptoms, such as sinus bradycardia, cognitive disability, and attention deficit hyperactivity disorder. Although the calcium signaling cascade is closely associated with a heterotrimeric G-protein, the function of $G{\beta}5$ in calcium signaling and its relevance to clinical symptoms remain unknown. In this study, we investigated the in vitro changes of store-operated calcium entry (SOCE) with exogenous expression of $G{\beta}5$. The cells expressing $G{\beta}5$ had enhanced SOCE after depletion of calcium ion inside the endoplasmic reticulum. $G{\beta}5$ also augmented Stim1- and Orai1-dependent SOCE. An ORAI1 loss-of-function mutant did not show inhibition of $G{\beta}5$-induced SOCE, and a STIM1-ERM truncation mutant showed no enhancement of SOCE. These results suggested a novel role of GNB5 and Stim1, and provided insight into the regulatory mechanism of SOCE.

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References

  1. Logothetis DE, Kurachi Y, Galper J, Neer EJ, Clapham DE. The beta gamma subunits of GTP-binding proteins activate the muscarinic $K^{+}$ channel in heart. Nature. 1987;325:321-326. https://doi.org/10.1038/325321a0
  2. Dupre DJ, Robitaille M, Rebois RV, Hebert TE. The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes. Annu Rev Pharmacol Toxicol. 2009;49:31-56. https://doi.org/10.1146/annurev-pharmtox-061008-103038
  3. Smrcka AV. G protein ${\beta}{\gamma}$ subunits: central mediators of G proteincoupled receptor signaling. Cell Mol Life Sci. 2008;65:2191-2214. https://doi.org/10.1007/s00018-008-8006-5
  4. Kisselev O, Ermolaeva M, Gautam N. Efficient interaction with a receptor requires a specific type of prenyl group on the G protein gamma subunit. J Biol Chem. 1995;270:25356-25358. https://doi.org/10.1074/jbc.270.43.25356
  5. Macrez-Lepretre N, Kalkbrenner F, Morel JL, Schultz G, Mironneau J. G protein heterotrimer Galpha13beta1gamma3 couples the angiotensin AT1A receptor to increases in cytoplasmic $Ca^{2+}$ in rat portal vein myocytes. J Biol Chem. 1997;272:10095-10102. https://doi.org/10.1074/jbc.272.15.10095
  6. Lodder EM, De Nittis P, Koopman CD, Wiszniewski W, Moura de Souza CF, Lahrouchi N, Guex N, Napolioni V, Tessadori F, Beekman L, Nannenberg EA, Boualla L, Blom NA, de Graaff W, Kamermans M, Cocciadiferro D, Malerba N, Mandriani B, Akdemir ZHC, Fish RJ, Eldomery MK, Ratbi I, Wilde AAM, de Boer T, Simonds WF, Neerman-Arbez M, Sutton VR, Kok F, Lupski JR, Reymond A, Bezzina CR, Bakkers J, Merla G. GNB5 mutations cause an autosomalrecessive multisystem syndrome with sinus bradycardia and cognitive disability. Am J Hum Genet. 2016;99:704-710. https://doi.org/10.1016/j.ajhg.2016.06.025
  7. Shamseldin HE, Masuho I, Alenizi A, Alyamani S, Patil DN, Ibrahim N, Martemyanov KA, Alkuraya FS. GNB5 mutation causes a novel neuropsychiatric disorder featuring attention deficit hyperactivity disorder, severely impaired language development and normal cognition. Genome Biol. 2016;17:195. https://doi.org/10.1186/s13059-016-1061-6
  8. Xie K, Allen KL, Kourrich S, Colon-Saez J, Thomas MJ, Wickman K, Martemyanov KA. Gbeta5 recruits R7 RGS proteins to GIRK channels to regulate the timing of neuronal inhibitory signaling. Nat Neurosci. 2010;13:661-663. https://doi.org/10.1038/nn.2549
  9. Xie K, Ge S, Collins VE, Haynes CL, Renner KJ, Meisel RL, Lujan R, Martemyanov KA. $G{\beta}5$-RGS complexes are gatekeepers of hyperactivity involved in control of multiple neurotransmitter systems. Psychopharmacology (Berl). 2012;219:823-834. https://doi.org/10.1007/s00213-011-2409-y
  10. 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:H446-458. https://doi.org/10.1152/ajpheart.00104.2013
  11. Kar P, Parekh A. STIM proteins, Orai1 and gene expression. Channels (Austin). 2013;7:374-378. https://doi.org/10.4161/chan.25298
  12. Ruhle B, Trebak M. Emerging roles for native Orai $Ca^{2+}$ channels in cardiovascular disease. Curr Top Membr. 2013;71:209-235.
  13. Shaikh S, Troncoso R, Criollo A, Bravo-Sagua R, Garcia L, Morselli E, Cifuentes M, Quest AF, Hill JA, Lavandero S. Regulation of cardiomyocyte autophagy by calcium. Am J Physiol Endocrinol Metab. 2016;310:E587-596. https://doi.org/10.1152/ajpendo.00374.2015
  14. Russell VA, Sagvolden T, Johansen EB. Animal models of attentiondeficit hyperactivity disorder. Behav Brain Funct. 2005;1:9. https://doi.org/10.1186/1744-9081-1-9
  15. Lehohla M, Kellaway L, Russell VA. NMDA receptor function in the prefrontal cortex of a rat model for attention-deficit hyperactivity disorder. Metab Brain Dis. 2004;19:35-42. https://doi.org/10.1023/B:MEBR.0000027415.75432.ad
  16. Lehohla M, Russell V, Kellaway L. NMDA-stimulated $Ca^{2+}$ uptake into barrel cortex slices of spontaneously hypertensive rats. Metab Brain Dis. 2001;16:133-141. https://doi.org/10.1023/A:1012532709306
  17. Horn JL, Janicki PK, Franks JJ. Diminished brain synaptic plasma membrane $Ca^{2+}$-ATPase activity in spontaneously hypertensive rats: association with reduced anesthetic requirements. Life Sci. 1995;56:PL427-432.
  18. Liao Y, Erxleben C, Abramowitz J, Flockerzi V, Zhu MX, Armstrong DL, Birnbaumer L. Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci U S A. 2008;105:2895-2900. https://doi.org/10.1073/pnas.0712288105
  19. Lee KP, Yuan JP, Hong JH, So I, Worley PF, Muallem S. An endoplasmic reticulum/plasma membrane junction: STIM1/Orai1/TRPCs. FEBS Lett. 2010;584:2022-2027. https://doi.org/10.1016/j.febslet.2009.11.078
  20. Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T. STIM is a $Ca^{2+}$ sensor essential for $Ca^{2+}$-store-depletion-triggered $Ca^{2+}$ influx. Curr Biol. 2005;15:1235-1241. https://doi.org/10.1016/j.cub.2005.05.055
  21. Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF. STIM1 carboxyl-terminus activates native SOC, Icrac and TRPC1 channels. Nat Cell Biol. 2006;8:1003-1010. https://doi.org/10.1038/ncb1454
  22. Hogan PG, Rao A. Store-operated calcium entry: Mechanisms and modulation. Biochem Biophys Res Commun. 2015;460:40-49. https://doi.org/10.1016/j.bbrc.2015.02.110
  23. Nieto Gutierrez A, McDonald PH. GPCRs: Emerging anti-cancer drug targets. Cell Signal. 2018;41:65-74. https://doi.org/10.1016/j.cellsig.2017.09.005
  24. Berridge MJ. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta. 2009;1793:933-940. https://doi.org/10.1016/j.bbamcr.2008.10.005
  25. Myung CS, Garrison JC. Role of C-terminal domains of the G protein beta subunit in the activation of effectors. Proc Natl Acad Sci U S A. 2000;97:9311-9316. https://doi.org/10.1073/pnas.97.16.9311
  26. Rebres RA, Roach TI, Fraser ID, Philip F, Moon C, Lin KM, Liu J, Santat L, Cheadle L, Ross EM, Simon MI, Seaman WE. Synergistic $Ca^{2+}$ responses by Gai- and Gaq-coupled G-protein-coupled receptors require a single PLCb isoform that is sensitive to both Gbg and Gaq. J Biol Chem. 2011;286:942-951. https://doi.org/10.1074/jbc.M110.198200
  27. Zeng W, Mak DO, Li Q, Shin DM, Foskett JK, Muallem S. A new mode of $Ca^{2+}$ signaling by G protein-coupled receptors: gating of IP3 receptor $Ca^{2+}$ release channels by $G{\beta}{\gamma}$. Curr Biol. 2003;13:872-876. https://doi.org/10.1016/S0960-9822(03)00330-0
  28. Schindl R, Muik M, Fahrner M, Derler I, Fritsch R, Bergsmann J, Romanin C. Recent progress on STIM1 domains controlling Orai activation. Cell Calcium. 2009;46:227-232. https://doi.org/10.1016/j.ceca.2009.08.003
  29. Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S. SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol. 2009;11:337-343. https://doi.org/10.1038/ncb1842
  30. Sondek J, Bohm A, Lambright DG, Hamm HE, Sigler PB. Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature. 1996;379:369-374. https://doi.org/10.1038/379369a0
  31. Cao X, Choi S, Maleth JJ, Park S, Ahuja M, Muallem S. The ER/PM microdomain, PI(4,5)P2 and the regulation of STIM1-Orai1 channel function. Cell Calcium. 2015;58:342-348. https://doi.org/10.1016/j.ceca.2015.03.003
  32. Jing J, He L, Sun A, Quintana A, Ding Y, Ma G, Tan P, Liang X, Zheng X, Chen L, Shi X, Zhang SL, Zhong L, Huang Y, Dong MQ, Walker CL, Hogan PG, Wang Y, Zhou Y. Proteomic mapping of ERPM junctions identifies STIMATE as a regulator of $Ca^{2+}$ influx. Nat Cell Biol. 2015;17:1339-1347. https://doi.org/10.1038/ncb3234
  33. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP. CRACM1 is a plasma membrane protein essential for store-operated $Ca^{2+}$ entry. Science. 2006;312:1220-1223. https://doi.org/10.1126/science.1127883
  34. Shin DM, Son A, Park S, Kim MS, Ahuja M, Muallem S. The TRPCs, Orais and STIMs in ER/PM Junctions. Adv Exp Med Biol. 2016;898:47-66.
  35. Kim MS, Lee KP, Yang D, Shin DM, Abramowitz J, Kiyonaka S, Birnbaumer L, Mori Y, Muallem S. Genetic and pharmacologic inhibition of the $Ca^{2+}$ influx channel TRPC3 protects secretory epithelia from $Ca^{2+}$-dependent toxicity. Gastroenterology. 2011;140:2107-2115, 2115.e1-4. https://doi.org/10.1053/j.gastro.2011.02.052