CADPS functional mutations in patients with bipolar disorder increase the sensitivity to stress.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
07
03
2019
accepted:
29
04
2021
revised:
19
04
2021
pubmed:
17
2
2022
medline:
4
5
2022
entrez:
16
2
2022
Statut:
ppublish
Résumé
Bipolar disorder is a severe and chronic psychiatric disease resulting from a combination of genetic and environmental risk factors. Here, we identified a significant higher mutation rate in a gene encoding the calcium-dependent activator protein for secretion (CADPS) in 132 individuals with bipolar disorder, when compared to 184 unaffected controls or to 21,070 non-psychiatric and non-Finnish European subjects from the Exome Aggregation Consortium. We found that most of these variants resulted either in a lower abundance or a partial impairment in one of the basic functions of CADPS in regulating neuronal exocytosis, synaptic plasticity and vesicular transporter-dependent uptake of catecholamines. Heterozygous mutant mice for Cadps
Identifiants
pubmed: 35169262
doi: 10.1038/s41380-021-01151-9
pii: 10.1038/s41380-021-01151-9
doi:
Substances chimiques
CADPS protein, human
0
Cadps protein, mouse
0
Calcium-Binding Proteins
0
Nerve Tissue Proteins
0
Vesicular Transport Proteins
0
Calcium
SY7Q814VUP
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
1145-1157Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM119158
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Merikangas KR, Akiskal HS, Angst J, Greenberg PE, Hirschfeld RM, Petukhova M, et al. Lifetime and 12-month prevalence of bipolar spectrum disorder in the National Comorbidity Survey replication. Arch Gen psychiatry. 2007;64:543–52.
pubmed: 17485606
pmcid: 1931566
doi: 10.1001/archpsyc.64.5.543
Kieseppa T, Partonen T, Haukka J, Kaprio J, Lonnqvist J. High concordance of bipolar I disorder in a nationwide sample of twins. Am J psychiatry. 2004;161:1814–21.
pubmed: 15465978
doi: 10.1176/ajp.161.10.1814
Mathieu F, Dizier MH, Etain B, Jamain S, Rietschel M, Maier W, et al. European collaborative study of early-onset bipolar disorder: evidence for genetic heterogeneity on 2q14 according to age at onset. Am J Med Genet B Neuropsychiatr Genet. 2010;153B:1425–33.
pubmed: 20886542
doi: 10.1002/ajmg.b.31121
Lopez de Lara C, Jaitovich-Groisman I, Cruceanu C, Mamdani F, Lebel V, Yerko V, et al. Implication of synapse-related genes in bipolar disorder by linkage and gene expression analyses. Int J Neuropsychopharmacol. 2010;13:1397–410.
pubmed: 20667171
doi: 10.1017/S1461145710000714
Etain B, Mathieu F, Rietschel M, Maier W, Albus M, McKeon P, et al. Genome-wide scan for genes involved in bipolar affective disorder in 70 European families ascertained through a bipolar type I early-onset proband: supportive evidence for linkage at 3p14. Mol psychiatry. 2006;11:685–94.
pubmed: 16534504
pmcid: 1959341
doi: 10.1038/sj.mp.4001815
Breen G, Lewis CM, Vassos E, Pergadia ML, Blackwood DH, Boomsma DI, et al. Replication of association of 3p21.1 with susceptibility to bipolar disorder but not major depression. Nat Genet. 2011;43:3–5. Author reply 5
pubmed: 21217634
doi: 10.1038/ng0111-3
Chen DT, Jiang X, Akula N, Shugart YY, Wendland JR, Steele CJ, et al. Genome-wide association study meta-analysis of European and Asian-ancestry samples identifies three novel loci associated with bipolar disorder. Mol psychiatry. 2013;18:195–205.
pubmed: 22182935
doi: 10.1038/mp.2011.157
McMahon FJ, Akula N, Schulze TG, Muglia P, Tozzi F, Detera-Wadleigh SD, et al. Meta-analysis of genome-wide association data identifies a risk locus for major mood disorders on 3p21.1. Nat Genet. 2010;42:128–31.
pubmed: 20081856
pmcid: 2854040
doi: 10.1038/ng.523
Psychiatric GCBDWG. Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat Genet. 2011;43:977–83.
doi: 10.1038/ng.943
Scott LJ, Muglia P, Kong XQ, Guan W, Flickinger M, Upmanyu R, et al. Genome-wide association and meta-analysis of bipolar disorder in individuals of European ancestry. Proc Natl Acad Sci U.S.A. 2009;106:7501–6.
pubmed: 19416921
pmcid: 2678639
doi: 10.1073/pnas.0813386106
He K, Wang Q, Chen J, Li T, Li Z, Li W, et al. ITIH family genes confer risk to schizophrenia and major depressive disorder in the Han Chinese population. Prog Neuropsychopharmacol Biol Psychiatry. 2014;51:34–8.
pubmed: 24389398
doi: 10.1016/j.pnpbp.2013.12.004
Ament SA, Szelinger S, Glusman G, Ashworth J, Hou L, Akula N, et al. Rare variants in neuronal excitability genes influence risk for bipolar disorder. Proc Natl Acad Sci U.S.A. 2015;112:3576–81.
pubmed: 25730879
pmcid: 4371952
doi: 10.1073/pnas.1424958112
Cupertino RB, Kappel DB, Bandeira CE, Schuch JB, da Silva BS, Muller D, et al. SNARE complex in developmental psychiatry: neurotransmitter exocytosis and beyond. J Neural Transm. 2016;123:867–83.
pubmed: 26856328
doi: 10.1007/s00702-016-1514-9
Etain B, Dumaine A, Mathieu F, Chevalier F, Henry C, Kahn JP, et al. A SNAP25 promoter variant is associated with early-onset bipolar disorder and a high expression level in brain. Mol Psychiatry. 2010;15:748–55.
pubmed: 19125158
doi: 10.1038/mp.2008.148
Mertens J, Wang QW, Kim Y, Yu DX, Pham S, Yang B, et al. Differential responses to lithium in hyperexcitable neurons from patients with bipolar disorder. Nature. 2015;527:95–9.
pubmed: 26524527
pmcid: 4742055
doi: 10.1038/nature15526
Ferreira MA, O’Donovan MC, Meng YA, Jones IR, Ruderfer DM, Jones L, et al. Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder. Nat Genet. 2008;40:1056–8.
pubmed: 18711365
pmcid: 2703780
doi: 10.1038/ng.209
Speidel D, Varoqueaux F, Enk C, Nojiri M, Grishanin RN, Martin TF, et al. A family of Ca2+-dependent activator proteins for secretion: comparative analysis of structure, expression, localization, and function. J Biol Chem. 2003;278:52802–9.
pubmed: 14530279
doi: 10.1074/jbc.M304727200
Ann K, Kowalchyk JA, Loyet KM, Martin TF. Novel Ca2+-binding protein (CAPS) related to UNC-31 required for Ca2+-activated exocytosis. J Biol Chem. 1997;272:19637–40.
pubmed: 9289490
doi: 10.1074/jbc.272.32.19637
Jockusch WJ, Speidel D, Sigler A, Sorensen JB, Varoqueaux F, Rhee JS, et al. CAPS-1 and CAPS-2 are essential synaptic vesicle priming proteins. Cell. 2007;131:796–808.
pubmed: 18022372
doi: 10.1016/j.cell.2007.11.002
Kabachinski G, Kielar-Grevstad DM, Zhang X, James DJ, Martin TF. Resident CAPS on dense-core vesicles docks and primes vesicles for fusion. Mol Biol Cell. 2016;27:654–68.
pubmed: 26700319
pmcid: 4750925
doi: 10.1091/mbc.E15-07-0509
Speidel D, Bruederle CE, Enk C, Voets T, Varoqueaux F, Reim K, et al. CAPS1 regulates catecholamine loading of large dense-core vesicles. Neuron. 2005;46:75–88.
pubmed: 15820695
doi: 10.1016/j.neuron.2005.02.019
Brunk I, Blex C, Speidel D, Brose N, Ahnert-Hilger G. Ca2+-dependent activator proteins of secretion promote vesicular monoamine uptake. J Biol Chem. 2009;284:1050–6.
pubmed: 19008227
doi: 10.1074/jbc.M805328200
Liu Y, Schirra C, Stevens DR, Matti U, Speidel D, Hof D, et al. CAPS facilitates filling of the rapidly releasable pool of large dense-core vesicles. J Neurosci. 2008;28:5594–601.
pubmed: 18495893
pmcid: 6670619
doi: 10.1523/JNEUROSCI.5672-07.2008
Hattori K, Tanaka H, Wakabayashi C, Yamamoto N, Uchiyama H, Teraishi T, et al. Expression of Ca(2)(+)-dependent activator protein for secretion 2 is increased in the brains of schizophrenic patients. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35:1738–43.
pubmed: 21601610
doi: 10.1016/j.pnpbp.2011.05.004
Palo OM, Soronen P, Silander K, Varilo T, Tuononen K, Kieseppa T, et al. Identification of susceptibility loci at 7q31 and 9p13 for bipolar disorder in an isolated population. Am J Med Genet B Neuropsychiatr Genet. 2010;153B:723–35.
pubmed: 19851985
Sadakata T, Washida M, Iwayama Y, Shoji S, Sato Y, Ohkura T, et al. Autistic-like phenotypes in Cadps2-knockout mice and aberrant CADPS2 splicing in autistic patients. J Clin Investig. 2007;117:931–43.
pubmed: 17380209
pmcid: 1821065
doi: 10.1172/JCI29031
Daily NJ, Boswell KL, James DJ, Martin TF. Novel interactions of CAPS (Ca2+-dependent activator protein for secretion) with the three neuronal SNARE proteins required for vesicle fusion. J Biol Chem. 2010;285:35320–9.
pubmed: 20826818
pmcid: 2975156
doi: 10.1074/jbc.M110.145169
Fatemi SH, Earle JA, Stary JM, Lee S, Sedgewick J. Altered levels of the synaptosomal associated protein SNAP-25 in hippocampus of subjects with mood disorders and schizophrenia. Neuroreport. 2001;12:3257–62.
pubmed: 11711867
doi: 10.1097/00001756-200110290-00023
Scarr E, Gray L, Keriakous D, Robinson PJ, Dean B. Increased levels of SNAP-25 and synaptophysin in the dorsolateral prefrontal cortex in bipolar I disorder. Bipolar Disord. 2006;8:133–43.
pubmed: 16542183
doi: 10.1111/j.1399-5618.2006.00300.x
Jamain S, Cichon S, Etain B, Muhleisen TW, Georgi A, Zidane N, et al. Common and rare variant analysis in early-onset bipolar disorder vulnerability. PloS ONE. 2014;9:e104326.
pubmed: 25111785
pmcid: 4128749
doi: 10.1371/journal.pone.0104326
Bernstein DP, Fink L, Handelsman L, Foote J, Lovejoy M, Wenzel K, et al. Initial reliability and validity of a new retrospective measure of child abuse and neglect. Am J psychiatry. 1994;151:1132–6.
pubmed: 8037246
doi: 10.1176/ajp.151.8.1132
Paquette D, Laporte L, Bigras M, Zoccolillo M. Validation of the French version of the CTQ and prevalence of the history of maltreatment. Sante Ment au Que. 2004;29:201–20.
doi: 10.7202/008831ar
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–75.
pubmed: 17701901
pmcid: 1950838
doi: 10.1086/519795
Gubernator NG, Zhang H, Staal RG, Mosharov EV, Pereira DB, Yue M, et al. Fluorescent false neurotransmitters visualize dopamine release from individual presynaptic terminals. Science. 2009;324:1441–4.
pubmed: 19423778
pmcid: 6696931
doi: 10.1126/science.1172278
Brunk I, Blex C, Rachakonda S, Holtje M, Winter S, Pahner I, et al. The first luminal domain of vesicular monoamine transporters mediates G-protein-dependent regulation of transmitter uptake. J Biol Chem. 2006;281:33373–85.
pubmed: 16926160
doi: 10.1074/jbc.M603204200
Grishanin RN, Klenchin VA, Loyet KM, Kowalchyk JA, Ann K, Martin TF. Membrane association domains in Ca2+-dependent activator protein for secretion mediate plasma membrane and dense-core vesicle binding required for Ca2+-dependent exocytosis. The. J Biol Chem. 2002;277:22025–34.
pubmed: 11927595
doi: 10.1074/jbc.M201614200
Khodthong C, Kabachinski G, James DJ, Martin TF. Munc13 homology domain-1 in CAPS/UNC31 mediates SNARE binding required for priming vesicle exocytosis. Cell Metab. 2011;14:254–63.
pubmed: 21803295
pmcid: 3148490
doi: 10.1016/j.cmet.2011.07.002
Nojiri M, Loyet KM, Klenchin VA, Kabachinski G, Martin TF. CAPS activity in priming vesicle exocytosis requires CK2 phosphorylation. J Biol Chem. 2009;284:18707–14.
pubmed: 19460754
pmcid: 2707249
doi: 10.1074/jbc.M109.017483
Petrie M, Esquibel J, Kabachinski G, Maciuba S, Takahashi H, Edwardson JM, et al. The vesicle priming factor CAPS functions as a homodimer via C2 domain interactions to promote regulated vesicle exocytosis. J Biol Chem. 2016;291:21257–70.
pubmed: 27528604
pmcid: 5076532
doi: 10.1074/jbc.M116.728097
Aas M, Henry C, Andreassen OA, Bellivier F, Melle I, Etain B. The role of childhood trauma in bipolar disorders. Int J bipolar Disord. 2016;4:2.
pubmed: 26763504
pmcid: 4712184
doi: 10.1186/s40345-015-0042-0
Etain B, Henry C, Bellivier F, Mathieu F, Leboyer M. Beyond genetics: childhood affective trauma in bipolar disorder. Bipolar Disord. 2008;10:867–76.
pubmed: 19594502
doi: 10.1111/j.1399-5618.2008.00635.x
Sadakata T, Washida M, Morita N, Furuichi T. Tissue distribution of Ca2+-dependent activator protein for secretion family members CAPS1 and CAPS2 in mice. J Histochemistry Cytochemistry. 2007;55:301–11.
doi: 10.1369/jhc.6A7033.2006
Walent JH, Porter BW, Martin TF. A novel 145 kd brain cytosolic protein reconstitutes Ca(2+)-regulated secretion in permeable neuroendocrine cells. Cell. 1992;70:765–75.
pubmed: 1516133
doi: 10.1016/0092-8674(92)90310-9
Autry AE, Monteggia LM. Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol Rev. 2012;64:238–58.
pubmed: 22407616
pmcid: 3310485
doi: 10.1124/pr.111.005108
Grigoroiu-Serbanescu M, Martinez M, Nothen MM, Grinberg M, Sima D, Propping P, et al. Different familial transmission patterns in bipolar I disorder with onset before and after age 25. Am J Med Genet. 2001;105:765–73.
pubmed: 11803528
doi: 10.1002/ajmg.10047
Leboyer M, Bellivier F, McKeon P, Albus M, Borrman M, Perez-Diaz F, et al. Age at onset and gender resemblance in bipolar siblings. Psychiatry Res. 1998;81:125–31.
pubmed: 9858030
doi: 10.1016/S0165-1781(98)00087-0
Leboyer M, Henry C, Paillere-Martinot ML, Bellivier F. Age at onset in bipolar affective disorders: a review. Bipolar Disord. 2005;7:111–8.
pubmed: 15762851
doi: 10.1111/j.1399-5618.2005.00181.x
Lin PI, McInnis MG, Potash JB, Willour V, MacKinnon DF, DePaulo JR, et al. Clinical correlates and familial aggregation of age at onset in bipolar disorder. Am J psychiatry. 2006;163:240–6.
pubmed: 16449477
doi: 10.1176/appi.ajp.163.2.240
O’Mahony E, Corvin A, O’Connell R, Comerford C, Larsen B, Jones R, et al. Sibling pairs with affective disorders: resemblance of demographic and clinical features. Psychological Med. 2002;32:55–61.
doi: 10.1017/S0033291701004986
Schurhoff F, Bellivier F, Jouvent R, Mouren-Simeoni MC, Bouvard M, Allilaire JF, et al. Early and late onset bipolar disorders: two different forms of manic-depressive illness? J Affect Disord. 2000;58:215–21.
pubmed: 10802130
doi: 10.1016/S0165-0327(99)00111-1
Kennedy KP, Cullen KR, DeYoung CG, Klimes-Dougan B. The genetics of early-onset bipolar disorder: a systematic review. J Affect Disord. 2015;184:1–12.
pubmed: 26057335
pmcid: 5552237
doi: 10.1016/j.jad.2015.05.017
Chen HM, DeLong CJ, Bame M, Rajapakse I, Herron TJ, McInnis MG, et al. Transcripts involved in calcium signaling and telencephalic neuronal fate are altered in induced pluripotent stem cells from bipolar disorder patients. Transl psychiatry. 2014;4:e375.
pubmed: 25116795
pmcid: 3966040
doi: 10.1038/tp.2014.12
Wang JL, Shamah SM, Sun AX, Waldman ID, Haggarty SJ, Perlis RH. Label-free, live optical imaging of reprogrammed bipolar disorder patient-derived cells reveals a functional correlate of lithium responsiveness. Transl psychiatry. 2014;4:e428.
pubmed: 25158003
pmcid: 4150245
doi: 10.1038/tp.2014.72
Machado-Vieira R, Soeiro-De-Souza MG, Richards EM, Teixeira AL, Zarate CA Jr. Multiple levels of impaired neural plasticity and cellular resilience in bipolar disorder: developing treatments using an integrated translational approach. World J Biol Psychiatry. 2014;15:84–95.
pubmed: 23998912
doi: 10.3109/15622975.2013.830775
Anand A, Koller DL, Lawson WB, Gershon ES, Nurnberger JI, Bi GSC. Genetic and childhood trauma interaction effect on age of onset in bipolar disorder: an exploratory analysis. J Affect Disord. 2015;179:1–5.
pubmed: 25837715
pmcid: 5845791
doi: 10.1016/j.jad.2015.02.029
Viswanath B, Jose SP, Squassina A, Thirthalli J, Purushottam M, Mukherjee O, et al. Cellular models to study bipolar disorder: a systematic review. J Affect Disord. 2015;184:36–50.
pubmed: 26070045
doi: 10.1016/j.jad.2015.05.037
Renden R, Berwin B, Davis W, Ann K, Chin CT, Kreber R, et al. Drosophila CAPS is an essential gene that regulates dense-core vesicle release and synaptic vesicle fusion. Neuron. 2001;31:421–37.
pubmed: 11516399
doi: 10.1016/S0896-6273(01)00382-8
Manji HK, Quiroz JA, Payne JL, Singh J, Lopes BP, Viegas JS, et al. The underlying neurobiology of bipolar disorder. World Psychiatry. 2003;2:136–46.
pubmed: 16946919
pmcid: 1525098
Cannon M, Clarke MC, Cotter DR. Priming the brain for psychosis: maternal inflammation during fetal development and the risk of later psychiatric disorder. Am J Psychiatry. 2014;171:901–5.
pubmed: 25178744
doi: 10.1176/appi.ajp.2014.14060749
Haussleiter IS, Neumann E, Lorek S, Ueberberg B, Juckel G. Role of child maltreatment and gender for bipolar symptoms in young adults. Int J Bipolar Disord. 2020;8:10.
pubmed: 32115670
pmcid: 7049538
doi: 10.1186/s40345-019-0173-9
Zhang S, Lin X, Yang T, Zhang S, Pan Y, Lu J, et al. Prevalence of childhood trauma among adults with affective disorder using the Childhood Trauma Questionnaire: a meta-analysis. J Affect Disord. 2020;276:546–54.
pubmed: 32871685
doi: 10.1016/j.jad.2020.07.001