Genetic variations in the PSMA6 and PSMC6 proteasome genes are associated with multiple sclerosis and response to interferon‑β therapy in Latvians
- Authors:
- Natalia Paramonova
- Jolanta Kalnina
- Kristine Dokane
- Kristine Dislere
- Ilva Trapina
- Tatjana Sjakste
- Nikolajs Sjakste
-
Affiliations: Genomics and Bioinformatics, Institute of Biology of The University of Latvia, LV‑1004 Riga, Latvia - Published online on: March 12, 2021 https://doi.org/10.3892/etm.2021.9909
- Article Number: 478
-
Copyright: © Paramonova et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
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|
Compston A and Confavreux C: The distribution of multiple sclerosis. In: McAlPine's multiPle Sclerosis. 4th edition. Pioli S (ed). Churchill Livingstone/Elsevier, Philadelphia, pp69-180, 2006. | |
|
Bellavista E, Santoro A, Galimberti D, Comi C, Luciani F and Mishto M: Current understanding on the role of standard and immunoproteasomes in inflammatory/immunological pathways of multiple sclerosis. Autoimmune Dis. 2014(739705)2014.PubMed/NCBI View Article : Google Scholar | |
|
Miller AE: Multiple sclerosis: Where will we be in 2020? Mt Sinai J Med. 78:268–279. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Noseworthy JH, Lucchinetti C, Rodriguez M and Weinshenker BG: Multiple sclerosis. N Engl J Med. 343:938–952. 2000.PubMed/NCBI View Article : Google Scholar | |
|
Song GG, Choi SJ, Ji JD and Lee YH: Genome-wide pathway analysis of a genome-wide association study on multiple sclerosis. Mol Biol Rep. 40:2557–2564. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Nicoletti F, Patti F, Cocuzza C, Zaccone P, Nicoletti A, Di Marco R and Reggio A: Elevated serum levels of interleukin-12 in chronic progressive multiple sclerosis. J Neuroimmunol. 70:87–90. 1996.PubMed/NCBI View Article : Google Scholar | |
|
Nicoletti F, Di Marco R, Mangano K, Patti F, Reggio E, Nicoletti A, Bendtzen K and Reggio A: Increased serum levels of interleukin-18 in patients with multiple sclerosis. Neurology. 57:342–244. 2001.PubMed/NCBI View Article : Google Scholar | |
|
Cavalli E, Mazzon E, Basile MS, Mangano K, Di Marco R, Bramanti P, Nicoletti F, Fagone P and Petralia MC: Upregulated expression of macrophage migration inhibitory factor, its analogue D-dopachrome tautomerase, and the CD44 receptor in peripheral CD4 T cells from clinically isolated syndrome patients with rapid conversion to clinical defined multiple sclerosis. Medicina (Kaunas). 55(667)2019.PubMed/NCBI View Article : Google Scholar | |
|
Fagone P, Mazzon E, Cavalli E, Bramanti A, Petralia MC, Mangano K, Al-Abed Y, Bramati P and Nicoletti F: Contribution of the macrophage migration inhibitory factor superfamily of cytokines in the pathogenesis of preclinical and human multiple sclerosis: In silico and in vivo evidences. J Neuroimmunol. 322:46–56. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Govindarajan V, de Rivero Vaccari JP and Keane RW: Role of inflammasomes in multiple sclerosis and their potential as therapeutic targets. J Neuroinflammation. 17(260)2020.PubMed/NCBI View Article : Google Scholar | |
|
Cavalli E, Mazzon E, Basile MS, Mammana S, Pennisi M, Fagone P, Kalfin R, Martinovic V, Ivanovic J, Andabaka M, et al: In silico and in vivo analysis of IL37 in multiple sclerosis reveals its probable homeostatic role on the clinical activity, disability, and treatment with fingolimod. Molecules. 25(20)2019.PubMed/NCBI View Article : Google Scholar | |
|
Nicoletti F, Patti F, DiMarco R, Zaccone P, Nicoletti A, Meroni P and Reggio A: Circulating serum levels of IL-1ra in patients with relapsing remitting multiple sclerosis are normal during remission phases but significantly increased either during exacerbations or in response to IFN-beta treatment. Cytokine. 8:395–400. 1996.PubMed/NCBI View Article : Google Scholar | |
|
Dujmovic I, Mangano K, Pekmezovic T, Quattrocchi C, Mesaros S, Stojsavljevic N, Nicoletti F and Drulovic J: The analysis of IL-1 beta and its naturally occurring inhibitors in multiple sclerosis: The elevation of IL-1 receptor antagonist and IL-1 receptor type II after steroid therapy. J Neuroimmunol. 207:101–106. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Fagone P, Patti F, Mangano K, Mammana S, Coco M, Touil-Boukoffa C, Chikovani T, Di Marco R and Nicoletti F: Heme oxygenase-1 expression in peripheral blood mononuclear cells correlates with disease activity in multiple sclerosis. J Neuroimmunol. 261:82–86. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Australia and New Zealand Multiple Sclerosis Genetics Consortium (ANZgene) Genome-wide association study identifies new multiple sclerosis susceptibility loci on chromosomes 12 and 20. Nat Genet. 41:824–828. 2009.PubMed/NCBI View Article : Google Scholar | |
|
International Multiple Sclerosis Genetics Conssortium (IMSGC). IL12A, MPHOSPH9/CDK2AP1 and RGS1 are novel multiple sclerosis susceptibility loci. Genes Immun. 11:397–405. 2010.PubMed/NCBI View Article : Google Scholar | |
|
International Multiple Sclerosis Genetics Consortium. Hafler DA, Compston A, Sawcer S, Lander ES, Daly MJ, de Jager PL, de Bakker PI, Gabriel SB, Mirel DB, et al: Risk allels for multiple sclerosis identified by a genome wide study. N Engl J Med. 357:851–862. 2007.PubMed/NCBI View Article : Google Scholar | |
|
De Jager PL, Jia X, Wang J, de Bakker PI, Ottoboni L, Aggarwal NT, Piccio L, Raychaudhuri S, Tran D, Aubin C, et al: Meta-analysis of genome scans and replication identify CD6, IRF8 and TNFRSF1A as new multiple sclerosis susceptibility loci. Nat Genet. 41:776–782. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Kofler DM, Severson CA, Mousissian N, De Jager PL and Hafler DA: The CD6 multiple sclerosis susceptibility allele is associated with alterations in CD4+ T cell proliferation. J Immunol. 187:3286–3291. 2011.PubMed/NCBI View Article : Google Scholar | |
|
International Multiple Sclerosis Genetics Consortium; Wellcome Trust Case Control Consortium 2. Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, Dilthey A, Su Z, et al: Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature. 476:214–219. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Zhang K, Chang S, Cui S, Guo L, Zhang L and Wang J: ICSNPathway: Identify candidate causal SNPs and pathways from genome-wide association study by one analytical framework. Nucleic Acids Res. 39:W437–W443. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Fissolo N, Kraus M, Reich M, Ayturan M, Overkleeft H, Driessen C and Weissert R: Dual inhibition of proteasomal and lysosomal proteolysis ameliorates autoimmune central nervous system inflammation. Eur J Immunol. 38:2401–2411. 2008.PubMed/NCBI View Article : Google Scholar | |
|
Mayo I, Arribas J, Villoslada P, Alvarez DoForno R, Rodríguez-Vilariño S, Montalban X, De Sagarra MR and Castaño JG: The proteasome is a major autoantigen in multiple sclerosis. Brain. 125:2658–2667. 2002.PubMed/NCBI View Article : Google Scholar | |
|
Zheng J and Bizzozero OA: Decreased activity of the 20S proteasome in the brain white matter and gray matter of patients with multiple sclerosis. J Neurochem. 117:143–153. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Minagar A, Ma W, Zhang X, Wang X, Zhang K, Alexander JS, Gonzalez-Toledo E and Albitar M: Plasma ubiquitin-proteasome system profile in patients with multiple sclerosis: Correlation with clinical features, neuroimaging, and treatment with interferon-beta-1b. Neurol Res. 34:611–618. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Pardo G and Jones DE: The sequence of disease-modifying therapies in relapsing multiple sclerosis: Safety and immunologic considerations. J Neurol. 264:2351–2374. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Nicoletti F, Di Marco R, Patti F, Reggio E, Nicoletti A, Zaccone P, Stivala F, Meroni PL and Reggio A: Blood levels of transforming growth factor-beta 1 (TGF-beta1) are elevated in both relapsing remitting and chronic progressive multiple sclerosis (MS) patients and are further augmented by treatment with interferon-beta 1b (IFN-beta1b). Clin Exp Immunol. 113:96–99. 1998.PubMed/NCBI View Article : Google Scholar | |
|
Patti F, Cataldi ML, Nicoletti F, Reggio E, Nicoletti A and Reggio A: Combination of cyclophosphamide and interferon-beta halts progression in patients with rapidly transitional multiple sclerosis. J Neurol Neurosurg Psychiatry. 71:404–407. 2001.PubMed/NCBI View Article : Google Scholar | |
|
Fagone P, Mazzon E, Mammana S, Di Marco R, Spinasanta F, Basile MS, Petralia MC, Bramanti P, Nicoletti F and Mangano K: Identification of CD4+ T cell biomarkers for predicting the response of patients with relapsing-remitting multiple sclerosis to natalizumab treatment. Mol Med Rep. 20:678–684. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Derfuss T, Mehling M, Papadopoulou A, Bar-Or A, Cohen JA and Kappos L: Advances in oral immunomodulating therapies in relapsing multiple sclerosis. Lancet Neurol. 19:336–347. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Kulakova OG, Tsareva EY, Boyko AN, Shchur SG, Gusev EI, Lvovs D, Favorov AV, Vandenbroeck K and Favorova OO: Allelic combinations of immune-response genes as possible composite markers of IFN-β efficacy in multiple sclerosis patients. Pharmacogenomics. 13:1689–1700. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Kalnina J, Paramonova N, Sjakste N and Sjakste T: Study of association between polymorphisms in the PSMB5 (rs11543947) and PSMA3 (rs2348071) genes and multiple sclerosis in Latvians. Biopolymers Cell. 30:305–309. 2014. | |
|
Mishto M, Bellavista E, Ligorio C, Textoris-Taube K, Santoro A, Giordano M, D'Alfonso S, Listì F, Nacmias B, Cellini E, et al: Immunoproteasome LMP2 60HH variant alters MBP epitope generation and reduces the risk to develop multiple sclerosis in Italian female population. PLoS One. 5(e9287)2010.PubMed/NCBI View Article : Google Scholar | |
|
Sjakste T, Paramonova N, Rumba-Rozenfelde I, Trapina I, Sugoka O and Sjakste N: Juvenile idiopathic arthritis subtype- and sex-specific associations with genetic variants in the PSMA6/PSMC6/PSMA3 gene cluster. Pediatr Neonatol. 55:393–403. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Paramonova N, Wu LS, Rumba-Rozenfelde I, Wang JY, Sjakste N and Sjakste T: Genetic variants in the PSMA6, PSMC6 and PSMA3 genes associated with childhood asthma in Latvian and Taiwanese populations. Biopolymers Cell. 30:377–387. 2014. | |
|
Paramonova N, Kupca S, Rumba-Rozenfelde I, Sjakste N and Sjakste T: Association between the PSMB5 and PSMC6 genetic variations and children obesity in the Latvian population. Biopolymers Cell. 30:477–480. 2014. | |
|
Sjakste T, Kalis M, Poudziunas I, Pirags V, Lazdins M, Groop L and Sjakste N: Association of microsatellite polymorphisms of the human 14q13.2 region with type 2 diabetes mellitus in Latvian and Finnish populations. Ann Hum Genet. 71:772–776. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Sjakste T, Paramonova N, Osina K, Dokane K, Sokolovska J and Sjakste N: Genetic variations in the PSMA3, PSMA6 and PSMC6 genes are associated with type 1 diabetes in Latvians and with expression level of number of UPS-related and T1DM-susceptible genes in HapMap individuals. Mol Genet Genomics. 291:891–903. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Sjakste T, Poudziunas I, Ninio E, Perret C, Pirags V, Nicaud V, Lazdins M, Evanss A, Morrison C, Cambien F and Sjakste N: SNPs of PSMA6 gene-investigation of possible association with myocardial infarction and type 2 diabetes mellitus. Genetika. 43:553–559. 2007.PubMed/NCBI | |
|
Wang H, Jiang M, Zhu H, Chen Q, Gong P, Lin J, Lu J and Qiu J: Quantitative assessment of the influence of PSMA6 variant (rs1048990) on coronary artery disease risk. Mol Biol Rep. 40:1035–1041. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Sjakste T, Paramonova N, Wu LS, Zemeckiene Z, Sitkauskiene B, Sakalauskas R, Wang JY and Sjakste N: PSMA6 (rs2277460, rs1048990), PSMC6 (rs2295826, rs2295827) and PSMA3 (rs2348071) genetic diversity in Latvians, lithuanians and taiwanese. Meta Gene. 2:283–298. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Rojas-Villarraga A, Amaya-Amaya J, Rodriguez-Rodriguez A, Mantilla RD and Anaya JM: Introducing polyautoimmunity: Secondary autoimmune diseases no longer exist. Autoimmune Dis. 2012(254319)2012.PubMed/NCBI View Article : Google Scholar | |
|
Holm K, Melum E, Franke A and Karlsen TH: SNPexp-A web tool for calculating and visualizing correlation between HapMap genotypes and gene expression levels. BMC Bioinformatics. 11(600)2010.PubMed/NCBI View Article : Google Scholar | |
|
Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, et al: Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol. 69:292–302. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Stangel M, Penner IK, Kallmann BA, Lukas C and Kieseier BC: Towards the implementation of ‘no evidence of disease activity’ in multiple sclerosis treatment: The multiple sclerosis decision model. Ther Adv Neurol Disord. 8:3–13. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Lewis CM: Genetic association studies: Design, analysis and interpretation. Brief Bioinform. 3:146–153. 2002.PubMed/NCBI View Article : Google Scholar | |
|
Alsmadi O, Muiya P, Khalak H, Al-Saud H, Meyer BF, Al-Mohanna F, Alshahid M and Dzimiri N: Haplotypes encompassing the KIAA0391 and PSMA6 gene cluster confer a genetic link for myocardial infarction and coronary artery disease. Ann Hum Genet. 73:475–483. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Andreassen OA, Harbo HF, Wang Y, Thompson WK, Schork AJ, Mattingsdal M, Zuber V, Bettella F, Ripke S, Kelsoe JR, et al: Genetic pleiotropy between multiple sclerosis and schizophrenia but not bipolar disorder: Differential involvement of immune-related gene loci. Mol Psychiatry. 20:207–214. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Lee S, Xu L, Shin Y, Gardner L, Hartzes A, Dohan FC, Raine C, Homayouni R and Levin MC: A potential link between autoimmunity and neurodegeneration in immune-mediated neurological disease. J Neuroimmunol. 235:56–69. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Thompson SD, Barnes MG, Griffin TA, Grom AA and Glass DN: Heterogeneity in juvenile idiopathic arthritis: Impact of molecular profiling based on DNA polymorphism and gene expression patterns. Arthritis Rheum. 62:2611–2615. 2010.PubMed/NCBI View Article : Google Scholar | |
|
Sivakumaran S, Agakov F, Theodoratou E, Prendergast JG, Zgaga L, Manolio T, Rudan I, McKeigue P, Wilson JF and Campbell H: Abundant pleiotropy in human complex diseases and traits. Am J Hum Genet. 89:607–618. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Hallstrand TS, Fischer ME, Wurfel MM, Afari N, Buchwald D and Goldberg J: Genetic pleiotropy between asthma and obesity in a community-based sample of twins. J Allergy Clin Immunol. 116:1235–1241. 2005.PubMed/NCBI View Article : Google Scholar | |
|
Murphy A, Tantisira KG, Soto-Quirós ME, Avila L, Klanderman BJ, Lake S, Weiss ST and Celedón JC: PRKCA: A positional candidate gene for body mass index and asthma. Am J Hum Genet. 85:87–96. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Lee SH, Lee EB, Shin ES, Lee JE, Cho SH, Min KU and Park HW: The interaction between allelic variants of CD86 and CD40LG: A common risk factor of allergic asthma and rheumatoid arthritis. Allergy Asthma Immunol Res. 6:137–141. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Ramírez-Bello J, Jiménez-Morales S, Espinosa-Rosales F, Gómez-Vera J, Gutiérrez A, Velázquez Cruz R, Baca V and Orozco L: Juvenile rheumatoid arthritis and asthma, but not childhood-onset systemic lupus erythematosus are associated with FCRL3 polymorphisms in Mexicans. Mol Immunol. 53:374–378. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Johnson DA, Amirahmadi S, Ward C, Fabry Z and Johnson JA: The absence of the pro-antioxidant transcription factor Nrf2 exacerbates experimental autoimmune encephalomyelitis. Toxicol Sci. 114:237–246. 2010.PubMed/NCBI View Article : Google Scholar | |
|
Bekenstein U and Soreq H: Heterogeneous nuclear ribonucleoprotein A1 in health and neurodegenerative disease: From structural insights to post-transcriptional regulatory roles. Mol Cell Neurosci. 56:436–446. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Leibowitz SM and Yan J: NF-κB pathways in the pathogenesis of multiple sclerosis and the therapeutic implications. Front Mol Neurosci. 9(84)2016.PubMed/NCBI View Article : Google Scholar | |
|
Yue Y, Stone S and Lin W: Role of nuclear factor κB in multiple sclerosis and experimental autoimmune encephalomyelitis. Neural Regen Res. 13:1507–1515. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Wu ZH and Shi Y: When ubiquitin meets NF-κB: A trove for anti-cancer drug development. Curr Pharm Des. 19:3263–3275. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Fedorova OA, Moiseeva TN, Nikiforov AA, Tsimokha AS, Livinskaya VA, Hodson M, Bottrill A, Evteeva IN, Ermolayeva JB, Kuznetzova IM, et al: Proteomic analysis of the 20S proteasome (PSMA3)-interacting proteins reveals a functional link between the proteasome and mRNA metabolism. Biochem Biophys Res Commun. 416:258–265. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Wosik K, Antel J, Kuhlmann T, Brück W, Massie B and Nalbantoglu J: Oligodendrocyte injury in multiple sclerosis: A role for p53. J Neurochem. 85:635–644. 2003.PubMed/NCBI View Article : Google Scholar | |
|
Dozmorov M, Wu W, Chakrabarty K, Booth JL, Hurst RE, Coggeshall KM and Metcalf JP: Gene expression profiling of human alveolar macrophages infected by B. anthracis spores demonstrates TNF-alpha and NF-kappab are key components of the innate immune response to the pathogen. BMC Infect Dis. 9(152)2009.PubMed/NCBI View Article : Google Scholar | |
|
Gill GN: Decoding the LIM development code. Trans Am Clin Climatol Assoc. 114:179–189. 2003.PubMed/NCBI | |
|
Phillips K and Luisi B: The virtuoso of versatility: POU proteins that flex to fit. J Mol Biol. 302:1023–1039. 2000.PubMed/NCBI View Article : Google Scholar | |
|
She H and Mao Z: Regulation of myocyte enhancer factor-2 transcription factors by neurotoxins. Neurotoxicology. 32:563–566. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Uzumcu A, Karaman B, Toksoy G, Uyguner ZO, Candan S, Eris H, Tatli B, Geckinli B, Yuksel A, Kayserili H and Basaran S: Molecular genetic screening of MBS1 locus on chromosome 13 for microdeletions and exclusion of FGF9, GSH1 and CDX2 as causative genes in patients with Moebius syndrome. Eur J Med Genet. 52:315–320. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Ho B, Olson G, Figel S, Gelman I, Cance WG and Golubovskaya VM: Nanog increases focal adhesion kinase (FAK) promoter activity and expression and directly binds to FAK protein to be phosphorylated. J Biol Chem. 287:18656–18673. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Ozaki K, Sato H, Iida A, Mizuno H, Nakamura T, Miyamoto Y, Takahashi A, Tsunoda T, Ikegawa S, Kamatani N, et al: A functional SNP in PSMA6 confers risk of myocardial infarction in the Japanese population. Nat Genet. 38:921–925. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Caputi FF, Carboni L, Mazza D, Candeletti S and Romualdi P: Cocaine and ethanol target 26S proteasome activity and gene expression in neuroblastoma cells. Drug Alcohol Depend. 161:265–275. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Bedford L, Lowe J, Dick LR, Mayer RJ and Brownell JE: Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat Rev Drug Discov. 10:29–46. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Torkildsen Ø, Myhr KM and Bø L: Disease-modifying treatments for multiple sclerosis-a review of approved medications. Eur J Neurol. 23 (Suppl 1):S18–S27. 2016.PubMed/NCBI View Article : Google Scholar |
