The dual effect of the lupus-associated polymorphism rs10516487 on BANK1 gene expression and protein localization

Genes and Immunity

Volumn 13, Issue 2, 2012, Pages 129-138

  Kozyrev, S V ^a   Bernal Quiros M ^b   Alarcon Riquelme M E ^b,c   Castillejo Lopez C ^b  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF GRANADA   (Spain)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

BANK1; cytoplasmic punctae; isoforms; SLE; splicing; sub cellular localization

Indexed keywords

DIMER; ISOPROTEIN; MESSENGER RNA;

ANIMAL CELL; ARTICLE; BANK1 GENE; CELLULAR DISTRIBUTION; CONSENSUS SEQUENCE; CONTROLLED STUDY; CYTOPLASM; ENHANCER REGION; EXON; GENE; GENE EXPRESSION; GENE FUNCTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA SPLICING; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALTERNATIVE SPLICING; BASE SEQUENCE; EXONS; GENE EXPRESSION REGULATION; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; RNA, MESSENGER;

EID: 84857792996     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2011.62     Document Type: Article

References (42)

1. Delgado-Vega A, Sanchez E, Lofgren S, Castillejo-Lopez C, Alarcon-Riquelme ME. Recent findings on genetics of systemic autoimmune diseases. Curr Opin Immunol 2010; 22: 698-705.
2. Kozyrev SV, Abelson AK, Wojcik J, Zaghlool A, Linga Reddy MV, Sanchez E et al. Functional variants in the B-cell gene BANK1 are associated with systemic lupus erythematosus. Nat Genet 2008; 40: 211-216.
3. Guo L, Deshmukh H, Lu R, Vidal GS, Kelly JA, Kaufman KM et al. Replication of the BANK1 genetic association with systemic lupus erythematosus in a European-derived population. Genes Immun 2009; 10: 531-538.
4. Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X et al. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 2009; 41: 1228-1233.
5. Yang W, Shen N, Ye DQ, Liu Q, Zhang Y, Qian XX et al. Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet 2010; 6: e1000841.
6. Chang YK, Yang W, Zhao M, Mok CC, Chan TM, Wong RW et al. Association of BANK1 and TNFSF4 with systemic lupus erythematosus in Hong Kong Chinese. Genes Immun 2009; 10: 414-420.
7. Wilbe M, Jokinen P, Truve K, Seppala EH, Karlsson EK, Biagi T et al. Genome-wide association mapping identifies multiple loci for a canine SLE-related disease complex. Nat Genet 2010; 42: 250-254.
8. Yokoyama K, Su Ih IH, Tezuka T, Yasuda T, Mikoshiba K, Tarakhovsky A et al. BANK regulates BCR-induced calcium mobilization by promoting tyrosine phosphorylation of IP(3) receptor. Embo J 2002; 21: 83-92.
9. Battersby A, Csiszar A, Leptin M, Wilson R. Isolation of proteins that interact with the signal transduction molecule Dof and identification of a functional domain conserved between Dof and vertebrate BCAP. J Mol Biol 2003; 329: 479-493.
10. Okada T, Maeda A, Iwamatsu A, Gotoh K, Kurosaki T. BCAP: the tyrosine kinase substrate that connects B cell receptor to phosphoinositide 3-kinase activation. Immunity 2000; 13: 817-827.
11. Aiba Y, Yamazaki T, Okada T, Gotoh K, Sanjo H, Ogata M et al. BANK negatively regulates Akt activation and subsequent B cell responses. Immunity 2006; 24: 259-268.
12. Krainer AR. Pre-mRNA splicing by complementation with purified human U1, U2, U4/U6 and U5 snRNPs. Nucleic Acids Res 1988; 16: 9415-9429.
13. Cartegni L,Wang J, Zhu Z, Zhang MQ, Krainer AR. ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res 2003; 31: 3568-3571.
14. Ibrahim EC, Schaal TD, Hertel KJ, Reed R, Maniatis T. Serine/arginine-rich protein-dependent suppression of exon skipping by exonic splicing enhancers. Proc Natl Acad Sci USA 2005; 102: 5002-5007.
15. Matlin AJ, Clark F, Smith CW. Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol 2005; 6: 386-398.
16. Cartegni L, Chew SL, Krainer AR. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet 2002; 3: 285-298.
17. Pagani F, Baralle FE. Genomic variants in exons and introns: identifying the splicing spoilers. Nat Rev Genet 2004; 5: 389-396.
18. Hertel KJ. Combinatorial control of exon recognition. J Biol Chem 2008; 283: 1211-1215.
19. Kuivenhoven JA, Weibusch H, Pritchard PH, Funke H, Benne R, Assmann G et al. An intronic mutation in a lariat branchpoint sequence is a direct cause of an inherited human disorder (fish-eye disease). J Clin Invest 1996; 98: 358-364.
20. Li M, Pritchard PH. Characterization of the effects of mutations in the putative branchpoint sequence of intron on the splicing within the human lecithin:cholesterol acyltransferase gene. J Biol Chem 2000; 275: 18079-18084.
21. Burrows NP, Nicholls AC, Richards AJ, Luccarini C, Harrison JB, Yates JR et al. A point mutation in an intronic branch site results in aberrant splicing of COL5A1 and in Ehlers-Danlos syndrome type II in two British families. Am J Hum Genet 1998; 63: 390-398.
22. Janssen RJ, Wevers RA, Haussler M, Luyten JA, Steenbergen-Spanjers GC, Hoffmann GF et al. A branch site mutation leading to aberrant splicing of the human tyrosine hydroxylase gene in a child with a severe extrapyramidal movement disorder. Ann Hum Genet 2000; 64 (Pt 5): 375-382.
23. Webb JC, Patel DD, Shoulders CC, Knight BL, Soutar AK. Genetic variation at a splicing branch point in intron 9 of the low density lipoprotein (LDL)-receptor gene: a rare mutation that disrupts mRNA splicing in a patient with familial hypercholesterolaemia and a common polymorphism. Hum Mol Genet 1996; 5: 1325-1331.
24. Chavanas S, Gache Y, Vailly J, Kanitakis J, Pulkkinen L, Uitto J et al. Splicing modulation of integrin beta4 pre-mRNA carrying a branch point mutation underlies epidermolysis bullosa with pyloric atresia undergoing spontaneous amelioration with ageing. Hum Mol Genet 1999; 8: 2097-2105.
25. Kralovicova J, Houngninou-Molango S, Kramer A, Vorechovsky I. Branch site haplotypes that control alternative splicing. Hum Mol Genet 2004; 13: 3189-3202.
26. Liu HX, Cartegni L, Zhang MQ, Krainer AR. A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nat Genet 2001; 27: 55-58.
27. Cartegni L, Krainer AR. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat Genet 2002; 30: 377-384.
28. Kashima T, Manley JL. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat Genet 2003; 34: 460-463.
29. Teraoka SN, Telatar M, Becker-Catania S, Liang T, Onengut S, Tolun A et al. Splicing defects in the ataxia-telangiectasia gene, ATM: underlying mutations and consequences. Am J Hum Genet 1999; 64: 1617-1631.
30. Pagani F, Stuani C, Tzetis M, Kanavakis E, Efthymiadou A, Doudounakis S et al. New type of disease causing mutations: the example of the composite exonic regulatory elements of splicing in CFTR exon 12. Hum Mol Genet 2003; 12: 1111-1120.
31. Liu HX, Zhang M, Krainer AR. Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev 1998; 12: 1998-2012.
32. Graveley BR. Sorting out the complexity of SR protein functions. RNA 2000; 6: 1197-1211.
33. Wu Y, Zhang Y, Zhang J. Distribution of exonic splicing enhancer elements in human genes. Genomics 2005; 86: 329-336.
34. Okajima K, Warman ML, Byrne LC, Kerr DS. Somatic mosaicism in a male with an exon skipping mutation in PDHA1 of the pyruvate dehydrogenase complex results in a milder phenotype. Mol Genet Metab 2006; 87: 162-168.
35. Ibrahim EC, Schaal TD, Hertel KJ, Reed R, Maniatis T. Serine/arginine-rich protein-dependent suppression of exon skipping by exonic splicing enhancers. Proc Natl Acad Sci USA 2005; 102: 5002-5007.
36. Kuo BA, Uporova TM, Liang H, Bennett VD, Tuan RS, Norton PA. Alternative splicing during chondrogenesis: modulation of fibronectin exon EIIIA splicing by SR proteins. J Cell Biochem 2002; 86: 45-55.
37. Wang J, Smith PJ, Krainer AR, Zhang MQ. Distribution of SR protein exonic splicing enhancer motifs in human protein-coding genes. Nucleic Acids Res 2005; 33: 5053-5062.
38. Liang H, Tuan RS, Norton PA. Overexpression of SR proteins and splice variants modulates chondrogenesis. Exp Cell Res 2007; 313: 1509-1517.
39. Tyson-Capper AJ, Bailey J, Krainer AR, Robson SC, Europe-Finner GN. The switch in alternative splicing of cyclic AMP-response element modulator protein CREM{tau}2{alpha} (activator) to CREM{alpha} (repressor) in human myometrial cells is mediated by SRp40. J Biol Chem 2005; 280: 34521-34529.
40. Wilson R, Battersby A, Csiszar A, Vogelsang E, Leptin M. A functional domain of Dof that is required for fibroblast growth factor signaling. Mol Cell Biol 2004; 24: 2263-2276.
41. Ma H, Xiong H, Liu T, Zhang L, Godzik A, Zhang Z. Aggregate formation and synaptic abnormality induced by DSCR1. J Neurochem 2004; 88: 1485-1496.
42. Taher TE, Parikh K, Flores-Borja F, Mletzko S, Isenberg DA, Peppelenbosch MP et al. Protein phosphorylation and kinome profiling reveal altered regulation of multiple signaling pathways in B lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum 2010; 62: 2412-2423.