Disrupted Ca
Calcium signalling
Primary immunodeficiency
Whole exome sequencing
Journal
Cellular & molecular immunology
ISSN: 2042-0226
Titre abrégé: Cell Mol Immunol
Pays: China
ID NLM: 101242872
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
received:
28
04
2022
accepted:
12
09
2022
pubmed:
28
10
2022
medline:
30
12
2022
entrez:
27
10
2022
Statut:
ppublish
Résumé
Calcium signaling is essential for lymphocyte activation, with genetic disruptions of store-operated calcium (Ca
Identifiants
pubmed: 36302985
doi: 10.1038/s41423-022-00928-4
pii: 10.1038/s41423-022-00928-4
pmc: PMC9794825
doi:
Substances chimiques
Calcium
SY7Q814VUP
Inositol 1,4,5-Trisphosphate Receptors
0
ITPR3 protein, human
0
Protein Isoforms
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11-25Subventions
Organisme : NIDCR NIH HHS
ID : R01 DE014756
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM072804
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM080139
Pays : United States
Organisme : NIDCR NIH HHS
ID : T90 DE021985
Pays : United States
Commentaires et corrections
Type : ErratumIn
Type : CommentIn
Informations de copyright
© 2022. The Author(s).
Références
Partiseti M, Le Deist F, Hivroz C, Fischer A, Korn H, Choquet D. The calcium current activated by T cell receptor and store depletion in human lymphocytes is absent in a primary immunodeficiency. J Biol Chem. 1994;269:32327–35.
doi: 10.1016/S0021-9258(18)31639-9
Le Deist F, Hivroz C, Partiseti M, Thomas C, Buc HA, Oleastro M, et al. A primary T-cell immunodeficiency associated with defective transmembrane calcium influx. Blood 1995;85:1053–62.
doi: 10.1182/blood.V85.4.1053.bloodjournal8541053
Bootman MD, Bultynck G. Fundamentals of cellular calcium signaling: a primer. Cold Spring Harb Perspect Biol. 2020;12:a038802.
doi: 10.1101/cshperspect.a038802
Arige V, Yule DI. Spatial and temporal crosstalk between the cAMP and Ca
doi: 10.1016/j.bbamcr.2022.119293
Scharenberg AM, Humphries LA, Rawlings DJ. Calcium signalling and cell-fate choice in B cells. Nat Rev Immunol. 2007;7:778–89.
doi: 10.1038/nri2172
Trebak M, Kinet J-P. Calcium signalling in T cells. Nat Rev Immunol. 2019;19:154–69.
doi: 10.1038/s41577-018-0110-7
Braiman A, Barda-Saad M, Sommers CL, Samelson LE. Recruitment and activation of PLCgamma1 in T cells: a new insight into old domains. EMBO J. 2006;25:774–84.
doi: 10.1038/sj.emboj.7600978
Jayaraman T, Ondriasová E, Ondrias K, Harnick DJ, Marks AR. The inositol 1,4,5-trisphosphate receptor is essential for T-cell receptor signaling. Proc Natl Acad Sci USA. 1995;92:6007–11.
doi: 10.1073/pnas.92.13.6007
Mikoshiba K. IP3 receptor/Ca
doi: 10.1111/j.1471-4159.2007.04825.x
Liou J, Fivaz M, Inoue T, Meyer T. Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca
doi: 10.1073/pnas.0702866104
Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, et al. STIM1 is a Ca
doi: 10.1038/nature04147
Lunz V, Romanin C, Frischauf I. STIM1 activation of Orai1. Cell Calcium. 2019;77:29–38.
doi: 10.1016/j.ceca.2018.11.009
Feske S. Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol. 2007;7:690–702.
doi: 10.1038/nri2152
Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI. Differential activation of transcription factors induced by Ca
doi: 10.1038/386855a0
Berridge MJ. The inositol trisphosphate/calcium signaling pathway in health and disease. Physiol Rev. 2016;96:1261–96.
doi: 10.1152/physrev.00006.2016
Parys JB, Bultynck G. Calcium signaling in health, disease and therapy. Biochim Biophys Acta Mol Cell Res. 2018;1865:1657–9.
doi: 10.1016/j.bbamcr.2018.08.019
Pchitskaya E, Popugaeva E, Bezprozvanny I. Calcium signaling and molecular mechanisms underlying neurodegenerative diseases. Cell Calcium 2018;70:87–94.
doi: 10.1016/j.ceca.2017.06.008
Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006;441:179–85.
doi: 10.1038/nature04702
Picard C, McCarl CA, Papolos A, Khalil S, Lüthy K, Hivroz C, et al. STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N Engl J Med. 2009;360:1971–80.
doi: 10.1056/NEJMoa0900082
Silva-Rojas R, Laporte J, Böhm J. STIM1/ORAI1 loss-of-function and gain-of-function mutations inversely impact on SOCE and calcium homeostasis and cause multi-systemic mirror diseases. Front Physiol. 2020;11:604941.
doi: 10.3389/fphys.2020.604941
Feske S, Draeger R, Peter H-H, Eichmann K, Rao A. The duration of nuclear residence of NFAT determines the pattern of cytokine expression in human SCID T cells. J Immunol. 2000;165:297–305.
doi: 10.4049/jimmunol.165.1.297
Milner JD, Fasth A, Etzioni A. Autoimmunity in severe combined immunodeficiency (SCID): lessons from patients and experimental models. J Clin Immunol. 2008;28:S29–33.
doi: 10.1007/s10875-007-9159-y
Fischer A, Provot J, Jais JP, Alcais A, Mahlaoui N. Members of the CEREDIH French PID Study Group Autoimmune and inflammatory manifestations occur frequently in patients with primary immunodeficiencies. J Allergy Clin Immunol. 2017;140:1388–93.e8.
doi: 10.1016/j.jaci.2016.12.978
Liston A, Enders A, Siggs OM. Unravelling the association of partial T-cell immunodeficiency and immune dysregulation. Nat Rev Immunol. 2008;8:545–58.
doi: 10.1038/nri2336
Schmidt RE, Grimbacher B, Witte T. Autoimmunity and primary immunodeficiency: two sides of the same coin? Nat Rev Rheumatol. 2018;14:7–18.
doi: 10.1038/nrrheum.2017.198
Kerkhofs M, Seitaj B, Ivanova H, Monaco G, Bultynck G, Parys JB, et al. Pathophysiological consequences of isoform-specific IP3 receptor mutations. Biochim Biophys Acta Mol Cell Res. 2018;1865:1707–17.
doi: 10.1016/j.bbamcr.2018.06.004
Terry LE, Alzayady KJ, Furati E, Yule DI. Inositol 1,4,5-trisphosphate receptor mutations associated with human disease. Messenger (Los Angeles). 2018;6:29–44.
Parolin Schnekenberg R, Perkins EM, Miller JW, Davies WI, D'Adamo MC, Pessia M, et al. De novo point mutations in patients diagnosed with ataxic cerebral palsy. Brain 2015;138:1817–32.
doi: 10.1093/brain/awv117
Tada M, Nishizawa M, Onodera O. Roles of inositol 1,4,5-trisphosphate receptors in spinocerebellar ataxias. Neurochem Int. 2016;94:1–8.
doi: 10.1016/j.neuint.2016.01.007
Klar J, Hisatsune C, Baig SM, Tariq M, Johansson AC, Rasool M, et al. Abolished InsP3R2 function inhibits sweat secretion in both humans and mice. J Clin Invest. 2014;124:4773–80.
doi: 10.1172/JCI70720
Rönkkö J, Molchanova S, Revah-Politi A, Pereira EM, Auranen M, Toppila J, et al. Dominant mutations in ITPR3 cause Charcot-Marie-Tooth disease. Ann Clin Transl Neurol. 2020;7:1962–72.
doi: 10.1002/acn3.51190
Sugawara H. Genetic evidence for involvement of type 1,type 2and type 3inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 1997;16:3078–88.
doi: 10.1093/emboj/16.11.3078
Ouyang K, Leandro Gomez-Amaro R, Stachura DL, Tang H, Peng X, Fang X, et al. Loss of IP3R-dependent Ca
doi: 10.1038/ncomms5814
Tang H, Wang H, Lin Q, Fan F, Zhang F, Peng X, et al. Loss of IP 3 receptor–mediated Ca 2+ release in mouse B cells results in abnormal B cell development and function. J Immunol. 2017;199:570–80.
doi: 10.4049/jimmunol.1700109
Foskett JK, White C, Cheung K-H, Mak D-OD. Inositol trisphosphate receptor Ca
doi: 10.1152/physrev.00035.2006
Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010;66:486–501.
doi: 10.1107/S0907444910007493
Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010;66:213–21.
doi: 10.1107/S0907444909052925
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera? A visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–12.
doi: 10.1002/jcc.20084
Parys JB, de Smedt H, Missiaen L, Bootman MD, Sienaert I, Casteels R. Rat basophilic leukemia cells as model system for inositol 1,4,5-trisphosphate receptor IV, a receptor of the type II family: functional comparison and immunological detection. Cell Calcium 1995;17:239–49.
doi: 10.1016/0143-4160(95)90070-5
Ma H-T, Venkatachalam K, Parys JB, Gill DL. Modification of store-operated channel coupling and inositol trisphosphate receptor function by 2-aminoethoxydiphenyl borate in DT40 lymphocytes. J Biol Chem. 2002;277:6915–22.
doi: 10.1074/jbc.M107755200
Bultynck G, Szlufcik K, Kasri NN, Assefa Z, Callewaert G, Missiaen L, et al. Thimerosal stimulates Ca
doi: 10.1042/BJ20040072
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–82.
doi: 10.1038/nmeth.2019
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012;9:671–5.
doi: 10.1038/nmeth.2089
Alzayady KJ, Wang L, Chandrasekhar R, Wagner LE, Van Petegem F, Yule DI. Defining the stoichiometry of inositol 1,4,5-trisphosphate binding required to initiate Ca 2+ release. Sci Signal 2016;9:ra35–ra35.
doi: 10.1126/scisignal.aad6281
Vaser R, Adusumalli S, Leng SN, Sikic M, Ng PC. SIFT missense predictions for genomes. Nat Protoc. 2016;11:1–9.
doi: 10.1038/nprot.2015.123
Quang D, Chen Y, Xie X. DANN: a deep learning approach for annotating the pathogenicity of genetic variants. Bioinformatics. 2015;31:761–3.
doi: 10.1093/bioinformatics/btu703
Zhang P, Bigio B, Rapaport F, Zhang SY, Casanova JL, Abel L, et al. PopViz: a webserver for visualizing minor allele frequencies and damage prediction scores of human genetic variations. Bioinformatics 2018;34:4307–9.
doi: 10.1093/bioinformatics/bty536
Paknejad N, Hite RK. Structural basis for the regulation of inositol trisphosphate receptors by Ca
doi: 10.1038/s41594-018-0089-6
Azumaya CM, Linton EA, Risener CJ, Nakagawa T, Karakas E. Cryo-EM structure of human type-3 inositol triphosphate receptor reveals the presence of a self-binding peptide that acts as an antagonist. J Biol Chem. 2020;295:1743–53.
doi: 10.1074/jbc.RA119.011570
Soulsby MD, Wojcikiewicz RJH. The type III inositol 1,4,5-trisphosphate receptor is phosphorylated by cAMP-dependent protein kinase at three sites. Biochem J. 2005;392:493–7.
doi: 10.1042/BJ20051325
Hornbeck PV, Zhang B, Murray B, Kornhauser JM, Latham V, Skrzypek E. PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res. 2015;43:D512–D520.
doi: 10.1093/nar/gku1267
Fan G, Baker MR, Wang Z, Seryshev AB, Ludtke SJ, Baker ML, et al. Cryo-EM reveals ligand induced allostery underlying InsP3R channel gating. Cell Res. 2018;28:1158–70.
doi: 10.1038/s41422-018-0108-5
Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol. 1997;15:707–47.
doi: 10.1146/annurev.immunol.15.1.707
Park Y-J, Yoo S-A, Kim M, Kim W-U. The role of calcium-calcineurin-NFAT signaling pathway in health and autoimmune diseases. Front Immunol. 2020;11:195.
doi: 10.3389/fimmu.2020.00195
Jasiulewicz A, Lisowska KA, Pietruczuk K, Frąckowiak J, Fulop T, Witkowski JM. Homeostatic ‘bystander’ proliferation of human peripheral blood B cells in response to polyclonal T-cell stimulation in vitro. Int Immunol. 2015;27:579–88.
doi: 10.1093/intimm/dxv032
Feske S. CRAC channelopathies. Pflug Arch. 2010;460:417–35.
doi: 10.1007/s00424-009-0777-5
Newton CL, Mignery GA, Südhof TC. Co-expression in vertebrate tissues and cell lines of multiple inositol 1,4,5-trisphosphate (InsP3) receptors with distinct affinities for InsP3. J Biol Chem. 1994;269:28613–9.
doi: 10.1016/S0021-9258(19)61949-6
Monkawa T, Miyawaki A, Sugiyama T, Yoneshima H, Yamamoto-Hino M, Furuichi T, et al. Heterotetrameric complex formation of inositol 1,4,5-trisphosphate receptor subunits. J Biol Chem. 1995;270:14700–4.
doi: 10.1074/jbc.270.24.14700
Chandrasekhar R, Alzayady KJ, Yule DI. Using concatenated subunits to investigate the functional consequences of heterotetrameric inositol 1,4,5-trisphosphate receptors. Biochem Soc Trans. 2015;43:364–70.
doi: 10.1042/BST20140287
Futatsugi A. IP3 receptor types 2 and 3 mediate exocrine secretion underlying energy metabolism. Science 2005;309:2232–4.
doi: 10.1126/science.1114110
Uchida K, Aramaki M, Nakazawa M, Yamagishi C, Makino S, Fukuda K, et al. Gene knock-outs of inositol 1,4,5-trisphosphate receptors types 1 and 2 result in perturbation of cardiogenesis. PLoS One. 2010;5:e12500.
doi: 10.1371/journal.pone.0012500
Prole DL, Taylor CW. Inositol 1,4,5‐trisphosphate receptors and their protein partners as signalling hubs. J Physiol. 2016;594:2849–66.
doi: 10.1113/JP271139
Parys JB, Vervliet T. New insights in the IP3 receptor and its regulation. Adv Exp Med Biol. 2020;1131:243–70. https://doi.org/10.1007/978-3-030-12457-1_10 .
Taylor CW, Genazzani AA, Morris SA. Expression of inositol trisphosphate receptors. Cell Calcium. 1999;26:237–51.
doi: 10.1054/ceca.1999.0090
Marchant JS, Taylor CW. Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca
doi: 10.1016/S0960-9822(06)00222-3
Wu B, Rice L, Shrimpton J, Lawless D, Walker K, Carter C, et al. Biallelic mutations in calcium release activated channel regulator 2A (CRACR2A) cause a primary immunodeficiency disorder. Elife 2021;10:e72559.
Des Georges A, Clarke OB, Zalk R, Yuan Q, Condon KJ, Grassucci RA, et al. Structural basis for gating and activation of RyR1. Cell. 2016;167:145–57.e17.
doi: 10.1016/j.cell.2016.08.075
Schmitz EA, Takahashi H, Karakas E. Structural basis for activation and gating of IP3 receptors. Nat Commun. 2022;13:1408.
doi: 10.1038/s41467-022-29073-2
Bhanumathy C, da Fonseca PCA, Morris EP, Joseph SK. Identification of functionally critical residues in the channel domain of inositol trisphosphate receptors. J Biol Chem. 2012;287:43674–84.
doi: 10.1074/jbc.M112.415786
Feske S, Müller JM, Graf D, Kroczek RA, Dräger R, Niemeyer C, et al. Severe combined immunodeficiency due to defective binding of the nuclear factor of activated T cells in T lymphocytes of two male siblings. Eur J Immunol. 1996;26:2119–26.
doi: 10.1002/eji.1830260924
Lian J, Cuk M, Kahlfuss S, Kozhaya L, Vaeth M, Rieux-Laucat F, et al. ORAI1 mutations abolishing store-operated Ca
doi: 10.1016/j.jaci.2017.10.031
Schaballie H, Rodriguez R, Martin E, Moens L, Frans G, Lenoir C, et al. A novel hypomorphic mutation in STIM1 results in a late-onset immunodeficiency. J Allergy Clin Immunol. 2015;136:816–9.e4.
doi: 10.1016/j.jaci.2015.03.009
Parry DA, Holmes TD, Gamper N, El-Sayed W, Hettiarachchi NT, Ahmed M, et al. A homozygous STIM1 mutation impairs store-operated calcium entry and natural killer cell effector function without clinical immunodeficiency. J Allergy Clin Immunol. 2016;137:955–7.e8.
doi: 10.1016/j.jaci.2015.08.051
Fuchs S, Rensing-Ehl A, Speckmann C, Bengsch B, Schmitt-Graeff A, Bondzio I, et al. Antiviral and regulatory T cell immunity in a patient with stromal interaction molecule 1 deficiency. J Immunol. 2012;188:1523–33.
doi: 10.4049/jimmunol.1102507
Rice L, Stockdale C, Berry I, O'Riordan S, Pysden K, Anwar R, et al. A report of novel STIM1 deficiency and 6-year follow-up of two previous cases associated with mild immunological phenotype. J Clin Immunol. 2019;39:249–56.
doi: 10.1007/s10875-019-00618-3
Hajnóczky G, Csordás G, Madesh M, Pacher P. Control of apoptosis by IP(3) and ryanodine receptor driven calcium signals. Cell Calcium. 2000;28:349–63.
doi: 10.1054/ceca.2000.0169
Decuypere J-P, Monaco G, Bultynck G, Missiaen L, De Smedt H, Parys JB. The IP3 receptor–mitochondria connection in apoptosis and autophagy. Biochim Biophys Acta Mol Cell Res. 2011;1813:1003–13.
doi: 10.1016/j.bbamcr.2010.11.023