Nuanced Interactions between AKAP79 and STIM1 with Orai1 Ca²⁺ Channels at Endoplasmic Reticulum-Plasma Membrane Junctions Sustain NFAT Activation

REFERENCES

• Esseltine JL, Scott JD. 2013. AKAP signalling complexes: pointing towards the next generation of therapeutic targets. Trends Pharmacol Sci 34:648–655. https://doi.org/10.1016/j.tips.2013.10.005.
   PubMed Web of Science ®Google Scholar
• Klauck TM, Faux MC, Labudda K, Langeberg LK, Jaken S, Scott JD. 1996. Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 271:1589–1592. https://doi.org/10.1126/science.271.5255.1589.
   PubMed Web of Science ®Google Scholar
• Patel N, Stengel F, Aebersold R, Gold MG. 2017. Molecular basis of AKAP79 regulation by calmodulin. Nat Commun 8:1681. https://doi.org/10.1038/s41467-017-01715-w.
   PubMed Web of Science ®Google Scholar
• Kar P, Barak P, Zerio A, Lin Y-P, Parekh AJ, Watts VJ, Cooper DMF, Zaccolo M, Kramer H, Parekh AB. 2021. AKAP79 orchestrates a cyclic AMP signalosome adjacent to Orai1 Ca2+ channels. Function (Oxf) 2:zqab036. https://doi.org/10.1093/function/zqab036.
   PubMedGoogle Scholar
• Liu G, Papa A, Katchman AN, Zakharov SI, Roybal D, Hennessey JA, Kushner J, Yang L, Chen B-X, Kushnir A, Dangas K, Gygi SP, Pitt GS, Colecraft HM, Ben-Johny M, Kalocsay M, Marx SO. 2020. Mechanism of adrenergic Ca V 1.2 stimulation revealed by proximity proteomics. Nature 577:695–700. https://doi.org/10.1038/s41586-020-1947-z.
   PubMed Web of Science ®Google Scholar
• Donelson SF, Esseltine JL, Nygren PJ, Veesler D, Byrne DP, Vonderach M, Strashnov I, Eyers CE, Eyers PA, Langeberg LK, Scott JD. 2017. Local protein kinase A action proceeds through intact holoenzymes. Science 356:1288–1293. https://doi.org/10.1126/science.aaj1669.
   PubMed Web of Science ®Google Scholar
• Bers DM, Xiang YK, Zaccolo M. 2019. Whole-cell cAMP and PKA activity are epiphenomena, nanodomain signaling matters. Physiology (Bethesda) 34:240–249. https://doi.org/10.1152/physiol.00002.2019.
   PubMed Web of Science ®Google Scholar
• Bakowski D, Murray F, Parekh AB. 2021. Store-operated Ca2+ channels: mechanism, function, pharmacology, and therapeutic targets. Annu Rev Pharmacol Toxicol 61:629–654. https://doi.org/10.1146/annurev-pharmtox-031620-105135.
   PubMed Web of Science ®Google Scholar
• Prakriya M, Lewis RS. 2015. Store-operated calcium channels. Physiol Rev 95:1383–1436. https://doi.org/10.1152/physrev.00020.2014.
   PubMed Web of Science ®Google Scholar
• Amcheslavsky A, Wood ML, Yeromin AV, Parker I, Freites JA, Tobias DJ, Cahalan MD. 2015. Molecular biophysics of Orai store-operated Ca2+ channels. Biophys J 108:237–246. https://doi.org/10.1016/j.bpj.2014.11.3473.
   PubMed Web of Science ®Google Scholar
• Chiono M, Mahey R, Tate G, Cooper DMF. 1995. Capacitative calcium entry exclusively inhibits cAMP synthesis in C6-2B glioma cells. Evidence that physiologically activated Ca2+ entry regulates Ca2+-inhibitable adenylyl cyclase in non-excitable cells. J Biological Chemistry 270:1149–1155. https://doi.org/10.1074/jbc.270.3.1149.
   PubMed Web of Science ®Google Scholar
• Chang WC, Parekh AB. 2004. Close functional coupling between CRAC channels, arachidonic acid release and leukotriene secretion. J Biol Chem 279:29994–29999. https://doi.org/10.1074/jbc.M403969200.
   PubMed Web of Science ®Google Scholar
• Bautista DM, Lewis RS. 2004. Modulation of plasma membrane calcium-ATPase activity by local calcium microdomains near CRAC channels in human T cells. J Physiol 556:805–817. https://doi.org/10.1113/jphysiol.2003.060004.
   PubMed Web of Science ®Google Scholar
• Kar P, Parekh AB. 2015. Distinct spatial Ca2+ signatures selectively activate different NFAT transcription factor isoforms. Mol Cell 58:232–243. https://doi.org/10.1016/j.molcel.2015.02.027.
   PubMed Web of Science ®Google Scholar
• Kar P, Mirams GR, Christian HC, Parekh AB. 2016. Control of NFAT isoform activation and NFAT-dependent gene expression through two coincident and spatially segregated intracellular Ca2+ signals. Mol Cell 64:746–759. https://doi.org/10.1016/j.molcel.2016.11.011.
   PubMed Web of Science ®Google Scholar
• Somasundaram S, Shum AK, McBride HJ, Kessler JA, Feske S, Miller RJ, Prakriya M. 2014. Store-operated CRAC channels regulate gene expression and proliferation in neural progenitor cells. J Neuroscience 34:9107–9123. https://doi.org/10.1523/JNEUROSCI.0263-14.2014.
   PubMed Web of Science ®Google Scholar
• Kar P, Nelson C, Parekh AB. 2011. Selective activation of the transcription factor NFAT1 by calcium microdomains near Ca2+ release-activated Ca2+ (CRAC) channels. J Biol Chem 286:14795–14803. https://doi.org/10.1074/jbc.M111.220582.
   PubMed Web of Science ®Google Scholar
• Müller MR, Rao A. 2010. NFAT, immunity and cancer: a transcription factor comes of age. Nat Rev Immunol 10:645–656. https://doi.org/10.1038/nri2818.
   PubMed Web of Science ®Google Scholar
• Hogan PG, Chen L, Nardone J, Rao A. 2003. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 17:2205–2232. https://doi.org/10.1101/gad.1102703.
   PubMed Web of Science ®Google Scholar
• Murphy JG, Crosby KC, Dittmer PJ, Sather WA, Dell’Acqua ML. 2019. AKAP79/150 recruits the transcription factor NFAT to regulate signaling to the nucleus by neuronal L-type Ca2+ channels. Mol Biol Cell 30:1743–1756. https://doi.org/10.1091/mbc.E19-01-0060.
   PubMed Web of Science ®Google Scholar
• Kar P, Lin Y-P, Bhardwaj R, Tucker CJ, Bird GS, Hediger MA, Monico C, Amin N, Parekh AB. 2021. The N terminus of Orai1 couples to the AKAP79 signaling complex to drive NFAT1 activation by local Ca2+ entry. Proc Natl Acad Sci USA 118:e2012908118. https://doi.org/10.1073/pnas.2012908118.
   Google Scholar
• Kar P, Samanta K, Kramer H, Morris O, Bakowski D, Parekh AB. 2014. Dynamic assembly of a membrane signaling complex enables selective activation of NFAT by orai1. Curr Biol 24:1361–1368. https://doi.org/10.1016/j.cub.2014.04.046.
   PubMed Web of Science ®Google Scholar
• Dell’Acqua ML, Faux MC, Thorburn J, Thorburn A, Scott JD. 1998. Membrane-targeting sequences on AKAP79 bind phosphatidylinositol-4, 5-bisphosphate. EMBO J 17:2246–2260. https://doi.org/10.1093/emboj/17.8.2246.
   PubMed Web of Science ®Google Scholar
• Liou J, Fivaz M, Inoue T, Meyer T. 2007. Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after calcium store depletion. Proc Natl Acad Sci USA 104:9301–9306. https://doi.org/10.1073/pnas.0702866104.
   PubMed Web of Science ®Google Scholar
• Covington ED, Wu MM, Lewis RS. 2010. Essential role for the CRAC activation domain in store-dependent oligomerization of STIM1. Mol Biol Cell 21:1897–1907. https://doi.org/10.1091/mbc.e10-02-0145.
   PubMed Web of Science ®Google Scholar
• Zhang X, Pathak T, Yoast R, Emrich S, Xin P, Nwokonko RM, Johnson M, Wu S, Delierneux C, Gueguinou M, Hempel N, Putney JW, Gill DL, Trebak M. 2019. A calcium/cAMP signaling loop at the ORAI1 mouth drives channel inactivation to shape NFAT induction. Nat Commun 10:1971. https://doi.org/10.1038/s41467-019-09593-0.
   PubMed Web of Science ®Google Scholar
• Zweifach A, Lewis RS. 1995. Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. J Gen Physiol 105:209–226. https://doi.org/10.1085/jgp.105.2.209.
   PubMed Web of Science ®Google Scholar
• Fierro L, Parekh AB. 1999. Fast calcium-dependent inactivation of calcium release-activated calcium current (CRAC) in RBL-1 cells. J Membr Biol 168:9–17. https://doi.org/10.1007/s002329900493.
   PubMed Web of Science ®Google Scholar
• Fierro L, Parekh AB. 2000. Substantial depletion of the intracellular Ca2+ stores is required for macroscopic activation of the Ca2+ release-activated Ca2+ current in rat basophilic leukaemia cells. J Physiology (Lond) 522:247–257. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00247.x.
   PubMed Web of Science ®Google Scholar
• Neher E. 1988. The influence of intracellular calcium concentration on degranulation of dialyzed mast cells from rat peritoneum. J Physiology (Lond) 395:193–214. https://doi.org/10.1113/jphysiol.1988.sp016914.
   PubMed Web of Science ®Google Scholar
• Parekh AB. 2008. Ca2+ microdomains near plasma membrane Ca2+ channels: impact on cell function. J Physiol 586:3043–3054. https://doi.org/10.1113/jphysiol.2008.153460.
   PubMed Web of Science ®Google Scholar
• Clerx M, Robinson M, Lambert B, Lei CL, Ghosh S, Mirams GR, Gavaghan DJ. 2019. Probabilistic inference on noisy time series (PINTS). Jors 7:23. https://doi.org/10.5334/jors.252.
   Google Scholar
• Wu MM, Covington ED, Lewis RS. 2014. Single-molecule analysis of diffusion and trapping of STIM1 and Orai1 at endoplasmic reticulum-plasma membrane junctions. Mol Biol Cell 25:3672–3685. https://doi.org/10.1091/mbc.e14-06-1107.
   PubMed Web of Science ®Google Scholar
• Hodeify R, Selvaraj S, Wen J, Arredouani A, Hubrack S, dib M, Al-Thani SN, McGraw T, Machaca K. 2015. A STIM1-dependent 'trafficking trap' mechanism regulates Orai1 plasma membrane residence and Ca2+ influx levels. J Cell Sci 128:3143–3154. https://doi.org/10.1242/jcs.172320.
   PubMed Web of Science ®Google Scholar
• Pani B, Ong HL, Liu X, Rauser K, Ambudkar IS, Singh BB. 2008. Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of store-operated Ca2+ entry (SOCE). J Biol Chem 283:17333–17340. https://doi.org/10.1074/jbc.M800107200.
   PubMed Web of Science ®Google Scholar
• Delint-Ramirez I, Willoughby D, Hammond GRV, Hammond GVR, Ayling LJ, Cooper DMF. 2011. Palmitoylation targets AKAP79 protein to lipid rafts and promotes its regulation of calcium-sensitive adenylyl cyclase Type 8. J Biol Chem 286:32962–32975. https://doi.org/10.1074/jbc.M111.243899.
   PubMed Web of Science ®Google Scholar
• Son G-Y, Subedi KP, Ong H-L, Noyer L, Saadi H, Zheng C, Bhardwaj R, Feske S, Ambudkar IS. 2020. STIM2 targets Orai1/STIM1 to the AKAP79 signaling complex and confers coupling of Ca2+ entry with NFAT1 activation. Proc Natl Acad Sci USA 117:16638–16648. https://doi.org/10.1073/pnas.1915386117.
   PubMed Web of Science ®Google Scholar
• Al-Daraji WI, Grant KR, Ryan K, Saxton A, Reynolds NJ. 2002. Localization of calcineurin/NFAT in human skin and psoriasis and inhibition of calcineurin/NFAT activation in human keratinocytes by cyclosporin A. J Invest Dermatol 118:779–788. https://doi.org/10.1046/j.1523-1747.2002.01709.x.
   PubMed Web of Science ®Google Scholar
• Sharma S, Findlay GM, Bandukwala HS, Oberdoerffer S, Baust B, Li Z, Schmidt V, Hogan PG, Sacks DB, Rao A. 2011. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNA-protein scaffold complex. Proc Natl Acad Sci USA 108:11381–11386. https://doi.org/10.1073/pnas.1019711108.
   PubMed Web of Science ®Google Scholar
• Feliciello A, Li Y, Avvedimento EV, Gottesman ME, Rubin CS. 1997. A-kinase anchor protein 75 increases the rate and magnitude of cAMP signaling to the nucleus. Curr Biol 7:1011–1014. https://doi.org/10.1016/S0960-9822(06)00424-6.
   PubMed Web of Science ®Google Scholar
• Kang M, Day CA, Kenworthy AK, DiBenedetto E. 2012. Simplified equation to extract diffusion coefficients from confocal FRAP data. Traffic 13:1589–1600.
   PubMed Web of Science ®Google Scholar
• Yeh Y-C, Lin Y-P, Kramer H, Parekh AB. 2020. Single-nucleotide polymorphisms in Orai1 associated with atopic dermatitis inhibit protein turnover, decrease calcium entry and disrupt calcium-dependent gene expression. Hum Mol Genet 29:1808–1823. https://doi.org/10.1093/hmg/ddz223.
   PubMed Web of Science ®Google Scholar
• Gold M, Stengel F, Nygren PJ, Weisbrod CR, Bruce JE, Robinson CV, Barford D, Scott JD. 2011. Architecture and dynamics of an A-kinase anchoring protein 79 (AKAP79) signaling complex. Proc Natl Acad Sci USA 108:6426–6431. https://doi.org/10.1073/pnas.1014400108.
   PubMed Web of Science ®Google Scholar