The orphan solute carrier SLC10A7 is a novel negative regulator of intracellular calcium signaling.
Amino Acid Sequence
Calcium
/ metabolism
Calcium Signaling
Cell Line
Humans
Mutation
Neoplasm Proteins
/ metabolism
ORAI1 Protein
/ metabolism
Organic Anion Transporters, Sodium-Dependent
/ chemistry
RNA, Messenger
/ genetics
Sarcoplasmic Reticulum Calcium-Transporting ATPases
/ metabolism
Stromal Interaction Molecule 1
/ metabolism
Symporters
/ chemistry
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
29 04 2020
29 04 2020
Historique:
received:
23
01
2020
accepted:
07
04
2020
entrez:
1
5
2020
pubmed:
1
5
2020
medline:
7
1
2021
Statut:
epublish
Résumé
SLC10A7 represents an orphan member of the Solute Carrier Family SLC10. Recently, mutations in the human SLC10A7 gene were associated with skeletal dysplasia, amelogenesis imperfecta, and decreased bone mineral density. However, the exact molecular function of SLC10A7 and the mechanisms underlying these pathologies are still unknown. For this reason, the role of SLC10A7 on intracellular calcium signaling was investigated. SLC10A7 protein expression was negatively correlated with store-operated calcium entry (SOCE) via the plasma membrane. Whereas SLC10A7 knockout HAP1 cells showed significantly increased calcium influx after thapsigargin, ionomycin and ATP/carbachol treatment, SLC10A7 overexpression reduced this calcium influx. Intracellular Ca
Identifiants
pubmed: 32350310
doi: 10.1038/s41598-020-64006-3
pii: 10.1038/s41598-020-64006-3
pmc: PMC7190670
doi:
Substances chimiques
Neoplasm Proteins
0
ORAI1 Protein
0
ORAI1 protein, human
0
Organic Anion Transporters, Sodium-Dependent
0
RNA, Messenger
0
STIM1 protein, human
0
Slc10a7 protein, human
0
Stromal Interaction Molecule 1
0
Symporters
0
Sarcoplasmic Reticulum Calcium-Transporting ATPases
EC 3.6.3.8
ATP2A2 protein, human
EC 7.2.2.10
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7248Références
Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517–529, https://doi.org/10.1038/nrm1155 (2003).
doi: 10.1038/nrm1155
pubmed: 12838335
Zhang, S. L. et al. STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437, 902–905, https://doi.org/10.1038/nature04147 (2005).
doi: 10.1038/nature04147
pubmed: 16208375
pmcid: 1618826
Roos, J. et al. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 169, 435–445, https://doi.org/10.1083/jcb.200502019 (2005).
doi: 10.1083/jcb.200502019
pubmed: 15866891
pmcid: 2171946
Choi, S. et al. The TRPCs-STIM1-Orai interaction. Handb. Exp. Pharmacol. 223, 1035–1054, https://doi.org/10.1007/978-3-319-05161-1_13 (2014).
doi: 10.1007/978-3-319-05161-1_13
pubmed: 24961979
Liou, J. et al. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 15, 1235–1241, https://doi.org/10.1016/j.cub.2005.05.055 (2005).
doi: 10.1016/j.cub.2005.05.055
pubmed: 16005298
pmcid: 3186072
Lewis, R. S. The molecular choreography of a store-operated calcium channel. Nature 446, 284–287, https://doi.org/10.1038/nature05637 (2007).
doi: 10.1038/nature05637
pubmed: 17361175
Wang, Y. et al. STIM protein coupling in the activation of Orai channels. Proc. Natl Acad. Sci. U S A 106, 7391–7396, https://doi.org/10.1073/pnas.0900293106 (2009).
doi: 10.1073/pnas.0900293106
pubmed: 19376967
pmcid: 2678612
Zweifach, A. & Lewis, R. S. Slow calcium-dependent inactivation of depletion-activated calcium current. Store-dependent and -independent mechanisms. J. Biol. Chem. 270, 14445–14451, https://doi.org/10.1074/jbc.270.24.14445 (1995).
doi: 10.1074/jbc.270.24.14445
pubmed: 7540169
Fierro, L. & Parekh, A. B. Fast calcium-dependent inactivation of calcium releaseactivated calcium current (CRAC) in RBL-1 cells. J. Membr. Biol. 168, 9–17 (1999).
doi: 10.1007/s002329900493
Brini, M. & Carafoli, E. Calcium pumps in health and disease. Physiol. Rev. 89, 1341–1378, https://doi.org/10.1152/physrev.00032.2008 (2009).
doi: 10.1152/physrev.00032.2008
pubmed: 19789383
MacLennan, D. H. & Kranias, E. G. Phospholamban: a crucial regulator of cardiac contractility. Nat. Rev. Mol. Cell Biol. 4, 566–577, https://doi.org/10.1038/nrm1151 (2003).
doi: 10.1038/nrm1151
pubmed: 12838339
Vangheluwe, P. et al. Intracellular Ca2+- and Mn2+-transport ATPases. Chem. Rev. 109, 4733–4759, https://doi.org/10.1021/cr900013m (2009).
doi: 10.1021/cr900013m
pubmed: 19678701
Srikanth, S. et al. A novel EF-hand protein, CRACR2A, is a cytosolic Ca2+ sensor that stabilizes CRAC channels in T cells. Nat. Cell Biol. 12, 436–446, https://doi.org/10.1038/ncb2045 (2010).
doi: 10.1038/ncb2045
pubmed: 20418871
pmcid: 2875865
Srikanth, S. et al. A large Rab GTPase encoded by CRACR2A is a component of subsynaptic vesicles that transmit T cell activation signals. Sci. Signal. 9, ra31, https://doi.org/10.1126/scisignal.aac9171 (2016).
doi: 10.1126/scisignal.aac9171
pubmed: 27016526
pmcid: 5013727
Palty, R., Raveh, A., Kaminsky, I., Meller, R. & Reuveny, E. SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 149, 425–438, https://doi.org/10.1016/j.cell.2012.01.055 (2012).
doi: 10.1016/j.cell.2012.01.055
pubmed: 22464749
Ashikov, A. et al. Integrating glycomics and genomics uncovers SLC10A7 as essential factor for bone mineralization by regulating post-Golgi protein transport and glycosylation. Hum. Mol. Genet. 27, 3029–3045, https://doi.org/10.1093/hmg/ddy213 (2018).
doi: 10.1093/hmg/ddy213
pubmed: 29878199
Dubail, J. et al. SLC10A7 mutations cause a skeletal dysplasia with amelogenesis imperfecta mediated by GAG biosynthesis defects. Nat. Commun. 9, 3087, https://doi.org/10.1038/s41467-018-05191-8 (2018).
doi: 10.1038/s41467-018-05191-8
pubmed: 30082715
pmcid: 6078967
Laugel-Haushalter, V. et al. A New SLC10A7 Homozygous Missense Mutation Responsible for a Milder Phenotype of Skeletal Dysplasia With Amelogenesis Imperfecta. Front. Genet. 10, 504, https://doi.org/10.3389/fgene.2019.00504 (2019).
doi: 10.3389/fgene.2019.00504
pubmed: 31191616
pmcid: 6546871
Godoy, J. R. et al. Molecular and phylogenetic characterization of a novel putative membrane transporter (SLC10A7), conserved in vertebrates and bacteria. Eur. J. Cell Biol. 86, 445–460, https://doi.org/10.1016/j.ejcb.2007.06.001 (2007).
doi: 10.1016/j.ejcb.2007.06.001
pubmed: 17628207
Geyer, J., Wilke, T. & Petzinger, E. The solute carrier family SLC10: more than a family of bile acid transporters regarding function and phylogenetic relationships. Naunyn Schmiedebergs Arch. Pharmacol. 372, 413–431, https://doi.org/10.1007/s00210-006-0043-8 (2006).
doi: 10.1007/s00210-006-0043-8
pubmed: 16541252
Geyer, J. et al. Cloning and functional characterization of human sodium-dependent organic anion transporter (SLC10A6). J. Biol. Chem. 282, 19728–19741, https://doi.org/10.1074/jbc.M702663200 (2007).
doi: 10.1074/jbc.M702663200
pubmed: 17491011
Jiang, L. et al. The Candida albicans plasma membrane protein Rch1p, a member of the vertebrate SLC10 carrier family, is a novel regulator of cytosolic Ca2+ homoeostasis. Biochem. J. 444, 497–502, https://doi.org/10.1042/BJ20112166 (2012).
doi: 10.1042/BJ20112166
pubmed: 22530691
Alber, J., Jiang, L. & Geyer, J. CaRch1p does not functionally interact with the high-affinity Ca(2+) influx system (HACS) of Candida albicans. Yeast 30, 449–457, https://doi.org/10.1002/yea.2981 (2013).
doi: 10.1002/yea.2981
pubmed: 24123457
Zhao, Y. Y. et al. The plasma membrane protein Rch1 is a negative regulator of cytosolic calcium homeostasis and positively regulated by the calcium/calcineurin signaling pathway in budding yeast. Eur. J. Cell Biol. 95, 164–174, https://doi.org/10.1016/j.ejcb.2016.01.001 (2016).
doi: 10.1016/j.ejcb.2016.01.001
pubmed: 26832117
Morgan, A. J. & Jacob, R. Ionomycin enhances Ca2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane. Biochem. J. 300, 665–672, https://doi.org/10.1042/bj3000665 (1994).
doi: 10.1042/bj3000665
pubmed: 8010948
pmcid: 1138219
Nusse, O. et al. Store-operated Ca2+ influx and stimulation of exocytosis in HL-60 granulocytes. J. Biol. Chem. 272, 28360–28367, https://doi.org/10.1074/jbc.272.45.28360 (1997).
doi: 10.1074/jbc.272.45.28360
pubmed: 9353293
Decuypere, J. P. et al. mTOR-Controlled Autophagy Requires Intracellular Ca2+ Signaling. PLoS One 8, e61020, https://doi.org/10.1371/journal.pone.0061020 (2013).
doi: 10.1371/journal.pone.0061020
pubmed: 23565295
pmcid: 3614970
Mogami, H., Tepikin, A. V. & Petersen, O. H. Termination of cytosolic Ca2+ signals: Ca2+ reuptake into intracellular stores is regulated by free Ca2+ concentration in the store lumen. EMBO J. 17, 435–442 (1998).
doi: 10.1093/emboj/17.2.435
Srikanth, S. et al. The Ca2+ sensor STIM1 regulates the type I interferon response by retaining the signaling adaptor STING at the endoplasmic reticulum. Nat. Immunol. 20, 152–162, https://doi.org/10.1038/s41590-018-0287-8 (2019).
doi: 10.1038/s41590-018-0287-8
pubmed: 30643259
pmcid: 6340781
Yazbeck, P. et al. STIM1 Phosphorylation at Y361 Recruits Orai1 to STIM1 Puncta and Induces Ca2+ Entry. Sci. Rep. 7, 42758, https://doi.org/10.1038/srep42758 (2017).
doi: 10.1038/srep42758
pubmed: 28218251
pmcid: 5316956
Brandman, O., Liou, J., Park, W. S. & Meyer, T. STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131, 1327–1339, https://doi.org/10.1016/j.cell.2007.11.039 (2007).
doi: 10.1016/j.cell.2007.11.039
pubmed: 18160041
pmcid: 2680164
Bittremieux, M. et al. DPB162-AE, an inhibitor of store-operated Ca2+ entry, can deplete the endoplasmic reticulum Ca2+ store. Cell Calcium 62, 60–70, https://doi.org/10.1016/j.ceca.2017.01.015 (2017).
doi: 10.1016/j.ceca.2017.01.015
pubmed: 28196740
Smyth, J. T., Dehaven, W. I., Bird, G. S. & Putney, J. W. Jr. Ca2+-store-dependent and -independent reversal of Stim1 localization and function. J. Cell Sci. 121, 762–772, https://doi.org/10.1242/jcs.023903 (2008).
doi: 10.1242/jcs.023903
pubmed: 18285445
pmcid: 2587154
Putney, J. W. Pharmacology of store-operated calcium channels. Mol. Interv. 10, 209–218, https://doi.org/10.1124/mi.10.4.4 (2010).
doi: 10.1124/mi.10.4.4
pubmed: 20729487
pmcid: 2965610
Tang, T. H. et al. Oxidative stress disruption of receptor-mediated calcium signaling mechanisms. J. Biomed. Sci. 20, 48, https://doi.org/10.1186/1423-0127-20-48 (2013).
doi: 10.1186/1423-0127-20-48
pubmed: 23844974
pmcid: 3716919
Palmer, A. E., Jin, C., Reed, J. C. & Tsien, R. Y. Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc. Natl Acad. Sci. USA 101, 17404–17409, https://doi.org/10.1073/pnas.0408030101 (2004).
doi: 10.1073/pnas.0408030101
pubmed: 15585581
Albarran, L., Lopez, J. J., Woodard, G. E., Salido, G. M. & Rosado, J. A. Store-operated Ca2+ Entry-associated Regulatory factor (SARAF) Plays an Important Role in the Regulation of Arachidonate-regulated Ca2+ (ARC) Channels. J. Biol. Chem. 291, 6982–6988, https://doi.org/10.1074/jbc.M115.704940 (2016).
doi: 10.1074/jbc.M115.704940
pubmed: 26817842
pmcid: 4807282
Toyoshima, C. et al. Crystal structures of the calcium pump and sarcolipin in the Mg2+-bound E1 state. Nature 495, 260–264, https://doi.org/10.1038/nature11899 (2013).
doi: 10.1038/nature11899
pubmed: 23455422
pmcid: 23455422
Sahoo, S. K. et al. The N Terminus of Sarcolipin Plays an Important Role in Uncoupling Sarco-endoplasmic Reticulum Ca2+-ATPase (SERCA) ATP Hydrolysis from Ca2+ Transport. J. Biol. Chem. 290, 14057–14067, https://doi.org/10.1074/jbc.M115.636738 (2015).
doi: 10.1074/jbc.M115.636738
pubmed: 25882845
pmcid: 4447977
Winther, A. M. et al. The sarcolipin-bound calcium pump stabilizes calcium sites exposed to the cytoplasm. Nature 495, 265–269, https://doi.org/10.1038/nature11900 (2013).
doi: 10.1038/nature11900
pubmed: 23455424
pmcid: 23455424
Glitsch, M. D., Bakowski, D. & Parekh, A. B. Store-operated Ca2+ entry depends on mitochondrial Ca2+ uptake. EMBO J. 21, 6744–6754, https://doi.org/10.1093/emboj/cdf675 (2002).
doi: 10.1093/emboj/cdf675
pubmed: 12485995
pmcid: 139095
Kirichok, Y., Krapivinsky, G. & Clapham, D. E. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360–364, https://doi.org/10.1038/nature02246 (2004).
doi: 10.1038/nature02246
pubmed: 14737170
Prydz, K. Determinants of Glycosaminoglycan (GAG) Structure. Biomolecules 5, 2003–2022, https://doi.org/10.3390/biom5032003 (2015).
doi: 10.3390/biom5032003
pubmed: 26308067
pmcid: 4598785
Eckstein, M. et al. Store-operated Ca2+ entry controls ameloblast cell function and enamel development. JCI Insight 2, e91166, https://doi.org/10.1172/jci.insight.91166 (2017).
doi: 10.1172/jci.insight.91166
pubmed: 28352661
pmcid: 5358480
Wang, S. et al. STIM1 and SLC24A4 Are Critical for Enamel Maturation. J. Dent. Res. 93, 94S–100S, https://doi.org/10.1177/0022034514527971 (2014).
doi: 10.1177/0022034514527971
pubmed: 24621671
pmcid: 4107542
McCarl, C. A. et al. ORAI1 deficiency and lack of store-operated Ca2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J. Allergy Clin. Immunol. 124, 1311–1318 e1317, https://doi.org/10.1016/j.jaci.2009.10.007 (2009).
doi: 10.1016/j.jaci.2009.10.007
pubmed: 20004786
pmcid: 2829767
Picard, C. et al. STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N. Engl. J. Med. 360, 1971–1980, https://doi.org/10.1056/NEJMoa0900082 (2009).
doi: 10.1056/NEJMoa0900082
pubmed: 19420366
pmcid: 2851618
Lacruz, R. S. & Feske, S. Diseases caused by mutations in ORAI1 and STIM1. Ann. N. Y. Acad. Sci. 1356, 45–79, https://doi.org/10.1111/nyas.12938 (2015).
doi: 10.1111/nyas.12938
pubmed: 26469693
pmcid: 4692058
Noppes, S. et al. Homo- and heterodimerization is a common feature of the solute carrier family SLC10 members. Biol. Chem. 400, 1371–1384, https://doi.org/10.1515/hsz-2019-0148 (2019).
doi: 10.1515/hsz-2019-0148
pubmed: 31256060
Bindels, D. S. et al. mScarlet: a bright monomeric red fluorescent protein for cellular imaging. Nat. Methods 14, 53–56, https://doi.org/10.1038/nmeth.4074 (2017).
doi: 10.1038/nmeth.4074
pubmed: 27869816
Gröer, C. et al. LC-MS/MS-based quantification of clinically relevant intestinal uptake and efflux transporter proteins. J. Pharm. Biomed. Anal. 85, 253–261, https://doi.org/10.1016/j.jpba.2013.07.031 (2013).
doi: 10.1016/j.jpba.2013.07.031
pubmed: 23973632