{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T14:18:28Z","timestamp":1790432308115,"version":"4.1.0"},"reference-count":46,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,11,20]],"date-time":"2021-11-20T00:00:00Z","timestamp":1637366400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,11,20]],"date-time":"2021-11-20T00:00:00Z","timestamp":1637366400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100005888","name":"uniwersytet medyczny w lodzi","doi-asserted-by":"publisher","award":["2014\/15\/B\/NZ5\/01579"],"award-info":[{"award-number":["2014\/15\/B\/NZ5\/01579"]}],"id":[{"id":"10.13039\/501100005888","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005888","name":"uniwersytet medyczny w lodzi","doi-asserted-by":"publisher","award":["2015\/19\/B\/NZ5\/02243"],"award-info":[{"award-number":["2015\/19\/B\/NZ5\/02243"]}],"id":[{"id":"10.13039\/501100005888","id-type":"DOI","asserted-by":"publisher"}]},{"name":"polskie towarzystwo diabetologiczne","award":["no number"],"award-info":[{"award-number":["no number"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell Commun Signal"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Wolfram syndrome (WFS) is a rare autosomal recessive syndrome in which diabetes mellitus and neurodegenerative disorders occur as a result of Wolframin deficiency and increased ER stress. In addition, WFS1 deficiency leads to calcium homeostasis disturbances and can change mitochondrial dynamics. The aim of this study was to evaluate protein levels and changes in gene transcription on human WFS cell model under experimental ER stress.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      We performed transcriptomic and proteomic analysis on WFS human cell model\u2014skin fibroblasts reprogrammed into induced pluripotent stem (iPS) cells and then into neural stem cells (NSC) with subsequent ER stress induction using tunicamycin (TM). Results were cross-referenced with publicly available RNA sequencing data in hippocampi and hypothalami of mice with\n                      <jats:italic>WFS1<\/jats:italic>\n                      deficiency.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Proteomic analysis identified specific signal pathways that differ in NSC WFS cells from healthy ones. Next, detailed analysis of the proteins involved in the mitochondrial function showed the down-regulation of subunits of the respiratory chain complexes in NSC WFS cells, as well as the up-regulation of proteins involved in Krebs cycle and glycolysis when compared to the control cells. Based on pathway enrichment analysis we concluded that in samples from mice hippocampi the mitochondrial protein import machinery and OXPHOS were significantly down-regulated.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Our results show the functional and morphological secondary mitochondrial damage in patients with WFS.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Graphical Abstract<\/jats:title>\n                  <\/jats:sec>","DOI":"10.1186\/s12964-021-00791-2","type":"journal-article","created":{"date-parts":[[2021,11,20]],"date-time":"2021-11-20T02:04:33Z","timestamp":1637373873000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Multiomic analysis on human cell model of wolfram syndrome reveals changes in mitochondrial morphology and function"],"prefix":"10.1186","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8781-4469","authenticated-orcid":false,"given":"Agnieszka","family":"Zmyslowska","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miljan","family":"Kuljanin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Beata","family":"Malachowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcin","family":"Stanczak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominika","family":"Michalek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aneta","family":"Wlodarczyk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dagmara","family":"Grot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanna","family":"Taha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bart\u0142omiej","family":"Pawlik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magdalena","family":"Lebiedzi\u0144ska-Arciszewska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanna","family":"Nieznanska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariusz R.","family":"Wieckowski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Piotr","family":"Rieske","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph D.","family":"Mancias","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maciej","family":"Borowiec","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wojciech","family":"Mlynarski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wojciech","family":"Fendler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,11,20]]},"reference":[{"key":"791_CR1","doi-asserted-by":"crossref","first-page":"1605","DOI":"10.1002\/ajmg.a.31809","volume":"143","author":"A Cano","year":"2007","unstructured":"Cano A, Rouzier C, Monnot S, Chabrol B, Conrath J, Lecomte P, French Group of Wolfram Syndrome, Vialettes B, et al. Identification of novel mutations in WFS1 and genotype-phenotype correlation in Wolfram syndrome. Am J Med Genet. 2007;143:1605.","journal-title":"Am J Med Genet"},{"key":"791_CR2","doi-asserted-by":"crossref","first-page":"14731","DOI":"10.1038\/srep14731","volume":"5","author":"X Qian","year":"2015","unstructured":"Qian X, Qin L, Xing G, Cao X. Phenotype prediction of pathogenic nonsynonymous single nucleotide polymorphisms in WFS1. Sci Rep. 2015;5:14731.","journal-title":"Sci Rep"},{"key":"791_CR3","doi-asserted-by":"publisher","first-page":"e40604","DOI":"10.1371\/journal.pone.0040604","volume":"7","author":"T Hershey","year":"2012","unstructured":"Hershey T, Lugar HM, Shimony JS, Rutlin J, Koller JM, Perantie DC, Washington University Wolfram Study Group, et al. Early brain vulnerability in Wolfram syndrome. PLoS ONE. 2012;7:e40604. https:\/\/doi.org\/10.1371\/journal.pone.0040604.","journal-title":"PLoS ONE"},{"key":"791_CR4","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1172\/JCI39678","volume":"120","author":"SG Fonseca","year":"2010","unstructured":"Fonseca SG, Ishigaki S, Oslowski CM, Lu S, Lipson KL, Ghosh R, et al. WFS 1 gene negatively regulates ER stress signaling in rodent and human cells. J Clin Investig. 2010;120:744.","journal-title":"J Clin Investig"},{"key":"791_CR5","doi-asserted-by":"crossref","first-page":"39609","DOI":"10.1074\/jbc.M507426200","volume":"280","author":"SG Fonseca","year":"2005","unstructured":"Fonseca SG, Fukuma M, Lipson KL, Nguyen LX, Allen JR, Oka Y, et al. WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic-cells. J Biol Chem. 2005;280:39609.","journal-title":"J Biol Chem"},{"key":"791_CR6","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1186\/s12967-019-1993-1","volume":"17","author":"MT Pallotta","year":"2019","unstructured":"Pallotta MT, Tascini G, Crispoldi R, Orabona C, Mondanelli G, Grohmann U, et al. Wolfram syndrome, a rare neurodegenerative disease: from pathogenesis to future treatment perspectives. J Transl Med. 2019;17:238. https:\/\/doi.org\/10.1186\/s12967-019-1993-1.","journal-title":"J Transl Med"},{"key":"791_CR7","doi-asserted-by":"crossref","first-page":"19461","DOI":"10.18632\/oncotarget.25114","volume":"9","author":"D Rojas-Rivera","year":"2018","unstructured":"Rojas-Rivera D, Rodriguez DA, Sepulveda D, Hetz C. ER stress sensing mechanism: putting off the brake on UPR transducers. Oncotarget. 2018;9:19461.","journal-title":"Oncotarget"},{"key":"791_CR8","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1111\/acel.12599","volume":"16","author":"G Mart\u0131nez","year":"2017","unstructured":"Mart\u0131nez G, Duran-Aniotz C, Cabral-Miranda F, Vivar JP, Hetz C. Endoplasmic reticulum proteostasis impairment in aging. Aging Cell. 2017;16:615.","journal-title":"Aging Cell"},{"key":"791_CR9","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.exer.2014.04.015","volume":"125","author":"SX Zhang","year":"2014","unstructured":"Zhang SX, Sanders E, Fliesler SJ, Wang JJ. Endoplasmic reticulum stress and the unfolded protein responses in retinal degeneration. Exp Eye Res. 2014;125:30.","journal-title":"Exp Eye Res"},{"key":"791_CR10","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s13024-018-0250-z","volume":"13","author":"T McLaughlin","year":"2018","unstructured":"McLaughlin T, Falkowski M, Park JW, Keegan S, Elliott M, Wang JJ, et al. Loss of XBP1 accelerates age-related decline in retinal function and neurodegeneration. Mol Neurodegener. 2018;13:16.","journal-title":"Mol Neurodegener"},{"key":"791_CR11","doi-asserted-by":"crossref","first-page":"e1002511","DOI":"10.1371\/journal.pbio.1002511","volume":"14","author":"M Cagalinec","year":"2016","unstructured":"Cagalinec M, Liiv M, Hodurova Z, Hickey MA, Vaarmann A, Mandel M, et al. Role of mitochondrial dynamics in neuronal development: Mechanism for Wolfram syndrome. PLOS Biol. 2016;14:e1002511.","journal-title":"PLOS Biol"},{"key":"791_CR12","doi-asserted-by":"publisher","first-page":"eaaq1380","DOI":"10.1126\/scisignal.aaq1380","volume":"11","author":"C Angebault","year":"2018","unstructured":"Angebault C, Fauconnier J, Patergnani S, Rieusset J, Danese A, Affortit CA, et al. ER-mitochondria cross-talk is regulated by the Ca2+ sensor ncs1 and is impaired in Wolfram syndrome. Sci Signal. 2018;11:eaaq1380. https:\/\/doi.org\/10.1126\/scisignal.aaq1380.","journal-title":"Sci Signal."},{"key":"791_CR13","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.2337\/dc10-1937","volume":"34","author":"J Rohayem","year":"2011","unstructured":"Rohayem J, Ehlers C, Wiedemann B, Holl R, Oexle K, Kordonouri O, Wolfram Syndrome Diabetes Writing Group, et al. Diabetes and neurodegeneration in Wolfram syndrome: a multicenter study of phenotype and genotype. Diabetes Care. 2011;34:1503.","journal-title":"Diabetes Care"},{"issue":"8988","key":"791_CR14","doi-asserted-by":"crossref","first-page":"1458","DOI":"10.1016\/S0140-6736(95)92473-6","volume":"346","author":"TG Barrett","year":"1995","unstructured":"Barrett TG, Bundey SE, Macleod AF. Neurodegeneration and diabetes: UK nationwide study of Wolfram (DIDMOAD) syndrome. Lancet. 1995;346(8988):1458.","journal-title":"Lancet"},{"key":"791_CR15","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1111\/j.1365-2265.2011.04102.x","volume":"75","author":"A Zmyslowska","year":"2011","unstructured":"Zmyslowska A, Borowiec M, Antosik K, Szalecki M, Stefanski A, Iwaniszewska B, et al. Wolfram syndrome in the Polish population: novel mutations and genotype-phenotype correlation. Clin Endocrinol (Oxf). 2011;75:636.","journal-title":"Clin Endocrinol (Oxf)"},{"key":"791_CR16","doi-asserted-by":"crossref","first-page":"e0141688","DOI":"10.1371\/journal.pone.0141688","volume":"10","author":"M Winiecka-Klimek","year":"2015","unstructured":"Winiecka-Klimek M, Smolarz M, Walczak MP, Zieba J, Hulas-Bigoszewska K, Kmieciak B, et al. SOX2 and SOX2-MYC reprogramming process of fibroblasts to the neural stem cells compromised by senescence. PLoS ONE. 2015;10:e0141688.","journal-title":"PLoS ONE"},{"key":"791_CR17","first-page":"465","volume":"15","author":"JA Paulo","year":"2014","unstructured":"Paulo JA. Nicotine alters the proteome of two human pancreatic duct cell lines. JOP. 2014;15:465.","journal-title":"JOP"},{"key":"791_CR18","doi-asserted-by":"crossref","first-page":"1600319","DOI":"10.1002\/pmic.201600319","volume":"17","author":"JA Paulo","year":"2017","unstructured":"Paulo JA, Gygi SP. Nicotine-induced protein expression profiling reveals mutually altered proteins across four human cell lines. Proteomics. 2017;17:1600319.","journal-title":"Proteomics"},{"key":"791_CR19","doi-asserted-by":"crossref","first-page":"2226","DOI":"10.1021\/acs.jproteome.8b00217","volume":"17","author":"J Navarrete-Perea","year":"2018","unstructured":"Navarrete-Perea J, Yu Q, Gygi SP, Paulo JA. Streamlined tandem mass tag (SL-TMT) protocol: an efficient strategy for quantitative (phospho) proteome profiling using tandem mass tag-synchronous precursor selection-MS3. J Proteome Res. 2018;17:2226.","journal-title":"J Proteome Res"},{"key":"791_CR20","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1021\/acs.jproteome.8b00899","volume":"18","author":"BK Erickson","year":"2019","unstructured":"Erickson BK, Mintseris J, Schweppe DK, Navarrete-Perea J, Erickson AR, Nusinow DP, et al. Active instrument engagement combined with a real-time database search for improved performance of sample multiplexing workflows. J Proteome Res. 2019;18:1299.","journal-title":"J Proteome Res"},{"key":"791_CR21","doi-asserted-by":"crossref","first-page":"2026","DOI":"10.1021\/acs.jproteome.9b00860","volume":"19","author":"DK Schweppe","year":"2020","unstructured":"Schweppe DK, Eng JK, Qing Y, Bailey D, Rad R, Navarrete-Perea J, et al. Full-featured, real-time database searching platform enables fast and accurate multiplexed quantitative proteomics. J Proteome Res. 2020;19:2026.","journal-title":"J Proteome Res"},{"key":"791_CR22","doi-asserted-by":"crossref","first-page":"1865","DOI":"10.1007\/s13361-015-1179-x","volume":"26","author":"JK Eng","year":"2015","unstructured":"Eng JK, Hoopmann MR, Jahan TA, Egerton JD, Noble WS, MacCoss MJ. A deeper look into comet\u2014implementation and features. J Am Soc Mass Spectrom. 2015;26:1865.","journal-title":"J Am Soc Mass Spectrom"},{"key":"791_CR23","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1002\/pmic.201200439","volume":"13","author":"JK Eng","year":"2013","unstructured":"Eng JK, Jahan TA, Hoopmann MR. Comet: an open-source MS\/MS sequence database search tool. Proteomics. 2013;13:22.","journal-title":"Proteomics"},{"key":"791_CR24","doi-asserted-by":"crossref","first-page":"7469","DOI":"10.1021\/ac301572t","volume":"84","author":"GC McAlister","year":"2012","unstructured":"McAlister GC, Huttlin EL, Haas W, Ting L, Jedrychowski MP, Rogers JC, et al. Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses. Anal Chem. 2012;84:7469.","journal-title":"Anal Chem"},{"key":"791_CR25","doi-asserted-by":"crossref","first-page":"1285","DOI":"10.1038\/nbt1240","volume":"24","author":"SA Beausoleil","year":"2006","unstructured":"Beausoleil SA, Vill\u00e9n J, Gerber SA, Rush J, Gygi SP. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol. 2006;24:1285.","journal-title":"Nat Biotechnol"},{"key":"791_CR26","doi-asserted-by":"crossref","first-page":"1174","DOI":"10.1016\/j.cell.2010.12.001","volume":"143","author":"EL Huttlin","year":"2010","unstructured":"Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, et al. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell. 2010;143:1174.","journal-title":"Cell"},{"key":"791_CR27","doi-asserted-by":"crossref","first-page":"1295","DOI":"10.5858\/2005-129-1295-DOMRDI","volume":"129","author":"KK Abu-Amero","year":"2005","unstructured":"Abu-Amero KK, Bosley TM. Detection of mitochondrial respiratory dysfunction in circulating lymphocytes using Resazurin. Arch Pathol Lab Med. 2005;129:1295.","journal-title":"Arch Pathol Lab Med"},{"key":"791_CR28","doi-asserted-by":"crossref","first-page":"1112","DOI":"10.1038\/nprot.2006.179","volume":"1","author":"V Vichai","year":"2006","unstructured":"Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc. 2006;1:1112.","journal-title":"Nat Protoc"},{"key":"791_CR29","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1111\/febs.14608","volume":"286","author":"A Almanza","year":"2019","unstructured":"Almanza A, Carlesso A, Chintha C, Creedican S, Doultsinos D, Leuzzi B, et al. Endoplasmic reticulum stress signalling\u2014from basic mechanisms to clinical applications. FEBS J. 2019;286:241.","journal-title":"FEBS J"},{"key":"791_CR30","first-page":"1","volume":"4","author":"K Matsuhisa","year":"2016","unstructured":"Matsuhisa K, Saito A, Asada R, Kanemoto S, Kaneko M, Imaizumi K. The physiological roles of ER stress transducer BBF2H7\/CREB3L2 and its potential as a target of disease therapy. Med Res Arch. 2016;4:1.","journal-title":"Med Res Arch"},{"key":"791_CR31","doi-asserted-by":"crossref","first-page":"147","DOI":"10.3390\/cells8020147","volume":"8","author":"P Niewiadomski","year":"2019","unstructured":"Niewiadomski P, Niedzi\u00f3\u0142ka SM, Markiewicz \u0141, U\u015bpie\u0144ski T, Baran B, Chojnowska K. Gli proteins: regulation in development and cancer. Cells. 2019;8:147.","journal-title":"Cells"},{"key":"791_CR32","doi-asserted-by":"crossref","first-page":"31","DOI":"10.3233\/JPD-160921","volume":"7","author":"E Bentea","year":"2017","unstructured":"Bentea E, Verbruggen L, Massie A. The proteasome inhibition model of Parkinson\u2019s disease. J Parkinsons Dis. 2017;7:31.","journal-title":"J Parkinsons Dis"},{"key":"791_CR33","doi-asserted-by":"crossref","first-page":"3175313","DOI":"10.1155\/2018\/3175313","volume":"2018","author":"M Eimre","year":"2018","unstructured":"Eimre M, Paju K, Peet N, Kadaja L, Tarrend M, Kasvandik S, et al. Increased mitochondrial protein levels and bioenergetics in the musculus rectus femoris of Wfs1-deficient mice. Oxid Med Cell Longev. 2018;2018:3175313.","journal-title":"Oxid Med Cell Longev"},{"key":"791_CR34","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/j.cell.2008.11.046","volume":"136","author":"X Wang","year":"2009","unstructured":"Wang X, Schwarz TL. The mechanism of Ca2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell. 2009;136:163\u201374.","journal-title":"Cell"},{"key":"791_CR35","doi-asserted-by":"crossref","first-page":"4861","DOI":"10.1093\/hmg\/ddq419","volume":"9","author":"ME Gegg","year":"2010","unstructured":"Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1\/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet. 2010;9:4861.","journal-title":"Hum Mol Genet"},{"key":"791_CR36","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1152\/physiolgenomics.00122.2012","volume":"45","author":"S K\u00f5ks","year":"2013","unstructured":"K\u00f5ks S, Overall RW, Ivask M, Soomets U, Guha M, Vasar E, et al. Silencing of the WFS1 gene in HEK cells induces pathways related to neurodegeneration and mitochondrial damage. Physiol Genom. 2013;45:182.","journal-title":"Physiol Genom"},{"key":"791_CR37","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/j.bbamcr.2011.11.018","volume":"1823","author":"S Grimm","year":"2012","unstructured":"Grimm S. The ER-mitochondria interface: the social network of cell death. Biochim Biophys Acta. 2012;1823:327.","journal-title":"Biochim Biophys Acta"},{"key":"791_CR38","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.ceca.2017.05.003","volume":"69","author":"S Marchi","year":"2018","unstructured":"Marchi S, Patergnani S, Missiroli S, Morciano G, Rimessi A, Wieckowski MR, et al. Mitochondrial and endoplasmic reticulum calcium homeostasis and cell death. Cell Calcium. 2018;69:62.","journal-title":"Cell Calcium"},{"key":"791_CR39","doi-asserted-by":"crossref","first-page":"2005","DOI":"10.1007\/s11011-018-0308-1","volume":"33","author":"P J\u0119drak","year":"2018","unstructured":"J\u0119drak P, Mozolewski P, W\u0119grzyn G, Wi\u0119ckowski MR. Mitochondrial alterations accompanied by oxidative stress conditions in skin fibroblasts of Huntington\u2019s disease patients. Metab Brain Dis. 2018;33:2005.","journal-title":"Metab Brain Dis"},{"key":"791_CR40","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1038\/s41419-018-0406-3","volume":"9","author":"B Delprat","year":"2018","unstructured":"Delprat B, Maurice T, Delettre C. Wolfram syndrome: MAMs\u2019 connection? Cell Death Dis. 2018;9:364.","journal-title":"Cell Death Dis"},{"key":"791_CR41","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.3389\/fnins.2019.01028","volume":"13","author":"M Ramalingam","year":"2019","unstructured":"Ramalingam M, Huh YJ, Lee YI. The impairments of alpha-Synuclein and mechanistic target of Rapamycin in rotenone-induced SH-SY5Y cells and mice model of Parkinson\u2019s disease. Front Neurosci. 2019;13:1028.","journal-title":"Front Neurosci"},{"key":"791_CR42","doi-asserted-by":"crossref","first-page":"4106","DOI":"10.1038\/emboj.2012.202","volume":"31","author":"E Area-Gomez","year":"2012","unstructured":"Area-Gomez E, Castillo MDCL, Tambini MD, Guardia-Laguarta C, de Groof AJC, Madra M, et al. Upregulated function of mitochondria-associated ER membranes in Alzheimer disease. EMBO J. 2012;31:4106.","journal-title":"EMBO J"},{"key":"791_CR43","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1093\/hmg\/ddx060","volume":"26","author":"C Rouzier","year":"2017","unstructured":"Rouzier C, Moore D, Delorme C, Lacas-Gervais S, Ait-El-Mkadem S, Fragaki K, et al. A novel CISD2 mutation associated with a classical Wolfram syndrome phenotype alters Ca2+ homeostasis and ER-mitochondria interactions. Hum Mol Genet. 2017;26:1599.","journal-title":"Hum Mol Genet"},{"key":"791_CR44","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1093\/hmg\/ddu499","volume":"24","author":"M Zatyka","year":"2015","unstructured":"Zatyka M, Da Silva XG, Bellomo EA, Leadbeater W, Astuti D, Smith J, et al. Sarco(endo)plasmic reticulum ATPase is a molecular partner of Wolfram syndrome 1 protein, which negatively regulates its expression. Hum Mol Genet. 2015;24:814\u201327.","journal-title":"Hum Mol Genet"},{"key":"791_CR45","doi-asserted-by":"crossref","first-page":"934","DOI":"10.1111\/pedi.12513","volume":"18","author":"S Morikawa","year":"2017","unstructured":"Morikawa S, Tajima T, Nakamura A, Ishizu K, Ariga T. A novel heterozygous mutation of the WFS1 gene leading to constitutive endoplasmic reticulum stress is the cause of Wolfram syndrome. Pediatr Diabetes. 2017;18:934\u201341.","journal-title":"Pediatr Diabetes"},{"key":"791_CR46","doi-asserted-by":"crossref","first-page":"4785","DOI":"10.1038\/s41598-020-61735-3","volume":"10","author":"C La Morgia","year":"2020","unstructured":"La Morgia C, Maresca A, Amore G, Gramegna LL, Carbonelli M, Scimonelli E, et al. Calcium mishandling in absence of primary mitochondrial dysfunction drives cellular pathology in Wolfram Syndrome. Sci Rep. 2020;10:4785.","journal-title":"Sci Rep"}],"container-title":["Cell Communication and Signaling"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12964-021-00791-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12964-021-00791-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12964-021-00791-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,16]],"date-time":"2022-05-16T13:22:48Z","timestamp":1652707368000},"score":1,"resource":{"primary":{"URL":"https:\/\/biosignaling.biomedcentral.com\/articles\/10.1186\/s12964-021-00791-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,20]]},"references-count":46,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["791"],"URL":"https:\/\/doi.org\/10.1186\/s12964-021-00791-2","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-675651\/v1","asserted-by":"object"}]},"ISSN":["1478-811X"],"issn-type":[{"value":"1478-811X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,20]]},"assertion":[{"value":"6 July 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 October 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 November 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study protocol was approved by the University Bioethics Committee at the Medical University in Lodz, Poland (RNN\/73\/14\/KE).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Patients have written informed consent for participation in the study and publication. All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Declaration of Helsinki.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests in relation to this work.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"116"}}