Molecular effects of autoimmune-risk promoter polymorphisms on expression, exon choice, and translational efficiency of interferon regulatory factor 5

Journal of Interferon and Cytokine Research

Volumn 34, Issue 5, 2014, Pages 354-365

  Clark, Daniel N ^a   Lambert, Jared P ^a   Till, Rodney E ^a   Argueta, Lissenya B ^a   Greenhalgh, Kathryn E ^a   Henrie, Brandon ^a   Bills, Trieste ^a   Hawkley, Tyson F ^a   Roznik, Marinya G ^a   Sloan, Jason M ^a   Mayhew, Vera ^a   Woodland, Loc ^a   Nelson, Eric P ^a   Tsai, Meng Hsuan ^a   Poole, Brian D ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; INTERFERON REGULATORY FACTOR 5; MESSENGER RNA; INTERFERON REGULATORY FACTOR; IRF5 PROTEIN, HUMAN;

AFRICAN AMERICAN; ALLELE; ALTERNATIVE RNA SPLICING; ANALYSIS; ARTICLE; ASIAN; AUTOIMMUNE DISEASE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EUROPEAN AMERICAN; EXON; FEMALE; GENE EXPRESSION; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HISPANIC; HUMAN; HUMAN CELL; MALE; MUTATIONAL ANALYSIS; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; QUANTITATIVE ANALYSIS; RNA FOLDING; RNA SEQUENCE; RNA SPLICING; RNA STABILITY; RNA TRANSCRIPTION; RNA TRANSLATION; SINGLE NUCLEOTIDE POLYMORPHISM; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; PROTEIN SYNTHESIS; RISK FACTOR;

AUTOIMMUNE DISEASES; CELL LINE; EXONS; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; HEALTHY VOLUNTEERS; HEK293 CELLS; HUMANS; INTERFERON REGULATORY FACTORS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; RISK FACTORS; RNA, MESSENGER;

EID: 84900316872     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2012.0105     Document Type: Article

References (60)

1. Agarwal SK. 2010. The genetics of systemic sclerosis. Discov Med 10(51):134-143.
2. Alonso-Perez E, Suarez-Gestal M, Calaza M, Kwan T, Majewski J, Gomez-Reino JJ, Gonzalez A. 2011. Cis-regulation of IRF5 expression is unable to fully account for systemic lupus erythematosus association: analysis of multiple experiments with lymphoblastoid cell lines. Arthritis Res Ther 13(3):R80.
3. Balkhi MY, Fitzgerald KA, Pitha PM. 2010. IKKa negatively regulates IRF-5 function in a MyD88-TRAF6 pathway. Cell Signal 22(1):117-127.
4. Barnes BJ, Kellum MJ, Field AE, Pitha PM. 2002. Multiple regulatory domains of IRF-5 control activation, cellular localization, and induction of chemokines that mediate recruitment of T lymphocytes. Mol Cell Biol 22(16):5721-5740.
5. Barnes BJ, Kellum MJ, Pinder KE, Frisancho JA, Pitha PM. 2003. Interferon regulatory factor 5, a novel mediator of cell cycle arrest and cell death. Cancer Res 63(19):6424-6431.
6. Brogna S, Wen J. 2009. Nonsense-mediated mRNA decay (NMD) mechanisms. Nat Struct Mol Biol 16(2):107-113.
7. Cahir-McFarland ED, Carter K, Rosenwald A, Giltnane JM, Henrickson SE, Staudt LM, Kieff E. 2004. Role of NF-kappa B in cell survival and transcription of latent membrane protein 1-expressing or Epstein-Barr virus latency III-infected cells. J Virol 78(8):4108-4119.
8. Dideberg V, Kristjansdottir G, Milani L, Libioulle C, Sigurdsson S, Louis E, Wiman AC, Vermeire S, Rutgeerts P, Belaiche J, Franchimont D, Van Gossum A, Bours V, Syvanen AC. 2007. An insertion-deletion polymorphism in the interferon regulatory Factor 5 (IRF5) gene confers risk of inflammatory bowel diseases. Hum Mol Genet 16(24):3008-3016.
9. Dieguez-Gonzalez R, Calaza M, Perez-Pampin E, de la Serna AR, Fernandez-Gutierrez B, Castaneda S, Largo R, Joven B, Narvaez J, Navarro F, Marenco JL, Vicario JL, Blanco FJ, Fernandez-Lopez JC, Caliz R, Collado-Escobar MD, Carreno L, Lopez-Longo J, Canete JD, Gomez-Reino JJ, Gonzalez A. 2008. Association of interferon regulatory factor 5 haplotypes, similar to that found in systemic lupus erythematosus, in a large subgroup of patients with rheumatoid arthritis. Arthritis Rheum 58(5):1264-1274.
10. Dieude P, Guedj M, Wipff J, Avouac J, Fajardy I, Diot E, Granel B, Sibilia J, Cabane J, Mouthon L, Cracowski JL, Carpentier PH, Hachulla E, Meyer O, Kahan A, Boileau C, Allanore Y. 2009. Association between the IRF5 rs2004640 functional polymorphism and systemic sclerosis. Arthritis Rheum 60(1): 225-233.
11. Emilie D, Llorente L, Galanaud P. 1996. Cytokines and systemic lupus erythematosus. Ann Med Interne 147(7):480-484.
12. Fan JH, Gao LB, Pan XM, Li C, Liang WB, Liu J, Li Y, Zhang L. 2010. Association between IRF-5 polymorphisms and risk of acute coronary syndrome. DNA Cell Biol 29(1):19-23.
13. Feng D, Stone RC, Eloranta M-L, Sangster-Guity N, Nordmark G, Sigurdsson S, Wang C, Alm G, Syvänen A-C, Rönnblom L, Barnes BJ. 2010. Genetic variants and disease-associated factors contribute to enhanced interferon regulatory factor 5 expression in blood cells of patients with systemic lupus erythematosus. Arthritis Rheum 62(2):562-573.
14. Graham RR, Kozyrev SV, Baechler EC, Reddy MV, Plenge RM, Bauer JW, Ortmann WA, Koeuth T, Gonzalez Escribano MF, Pons-Estel B, Petri M, Daly M, Gregersen PK, Martin J, Altshuler D, Behrens TW, Alarcon-Riquelme ME. 2006. A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat Genet 38(5):550-555.
15. Graham RR, Kyogoku C, Sigurdsson S, Vlasova IA, Davies LRL, Baechler EC, Plenge RM, Koeuth T, Ortmann WA, Hom G, Bauer JW, Gillett C, Burtt N, Graham DSC, Onofrio R, Petri M, Gunnarsson I, Svenungsson E, Ronnblom L, Nordmark G, Gregersen PK, Moser K, Gaffney PM, Criswell LA, Vyse TJ, Syvanen AC, Bohjanen PR, Daly MJ, Behrens TW, Altshuler D. 2007. Three functional variants of IFN regulatory factor 5 (IRF5) define risk and protective haplotypes for human lupus. Proc Natl Acad Sci U S A 104(16):6758-6763.
16. Grievink H, Stowell K. 2010. Allele-specific differences in ryanodine receptor 1 mRNA expression levels may contribute to phenotypic variability in malignant hyperthermia. Orphanet J Rare Dis 5(1):10.
17. Hedl M, Abraham C. 2012. IRF5 risk polymorphisms contribute to interindividual variance in pattern recognition receptormediated cytokine secretion in human monocyte-derived cells. J Immunol 188(11):5348-5356.
18. Hu G, Barnes BJ. 2009. IRF-5 Is a mediator of the death receptorinduced apoptotic signaling pathway. J Biol Chem 284(5): 2767-2777.
19. Hu G, Mancl ME, Barnes BJ. 2005. Signaling through IFN regulatory factor-5 sensitizes p53-deficient tumors to DNA damageinduced apoptosis and cell death. Cancer Res 65(16):7403-7412.
20. Kaplan MJ. 2004. Apoptosis in systemic lupus erythematosus. Clin Immunol 112(3):210-218.
21. Kawasaki A, Kyogoku C, Ohashi J, Miyashita R, Hikami K, Kusaoi M, Tokunaga K, Takasaki Y, Hashimoto H, Behrens TW, Tsuchiya N. 2008. Association of IRF5 polymorphisms with systemic lupus erythematosus in a Japanese population: support for a crucial role of intron 1 polymorphisms. Arthritis Rheum 58(3):826-834.
22. Kelly JA, Kelley JM, Kaufman KM, Kilpatrick J, Bruner GR, Merrill JT, James JA, Frank SG, Reams E, Brown EE, Gibson AW, Marion MC, Langefeld CD, Li QZ, Karp DR, Wakeland EK, Petri M, Ramsey-Goldman R, Reveille JD, Vila LM, Alarcon GS, Kimberly RP, Harley JB, Edberg JC. 2008. Interferon regulatory factor-5 is genetically associated with systemic lupus erythematosus in African Americans. Genes Immun 9(3):187-194.
23. Kim YJ, Park JH, Kim I, Kim JO, Bae JS, Shin HD, Bae SC. 2008. Putative role of functional interferon regulatory factor 5 (IRF5) polymorphism in rheumatoid arthritis in a Korean population. J Rheumatol 35(11):2106-2118.
24. Kozak M. 1999. Initiation of translation in prokaryotes and eukaryotes. Gene 234(2):187-208.
25. Kozyrev SV, Lewen S, Reddy PM, Pons-Estel B, Witte T, Junker P, Laustrup H, Gutierrez C, Suarez A, Francisca Gonzalez- Escribano M, Martin J, Alarcon-Riquelme ME. 2007. Structural insertion/deletion variation in IRF5 is associated with a risk haplotype and defines the precise IRF5 isoforms expressed in systemic lupus erythematosus. Arthritis Rheum 56(4):1234-1241.
26. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, Hussell T, Feldmann M, Udalova IA. 2011. IRF5 promotes inflammatory macrophage polarization and T(H)1- T(H)17 responses. Nat Immunol 12(3):231-238.
27. Kristjansdottir G, Sandling JK, Bonetti A, Roos IM, Milani L, Wang C, Gustafsdottir SM, Sigurdsson S, Lundmark A, Tienari PJ, Koivisto K, Elovaara I, Pirttila T, Reunanen M, Peltonen L, Saarela J, Hillert J, Olsson T, Landegren U, Alcina A, Fernandez O, Leyva L, Guerrero M, Lucas M, Izquierdo G, Matesanz F, Syvanen AC. 2008. Interferon regulatory factor 5 (IRF5) gene variants are associated with multiple sclerosis in three distinct populations. J Med Genet 45(6):362-369.
28. Lien CY, Fang CM, Huso D, Livak F, Lu RQ, Pitha PM. 2010. Critical role of IRF-5 in regulation of B-cell differentiation. Proc Natl Acad Sci U S A 107(10):4664-4668.
29. Lin R, Yang L, Arguello M, Penafuerte C, Hiscott J. 2005. A CRM1-dependent nuclear export pathway is involved in the regulation of IRF-5 subcellular localization. J Biol Chem 280(4):3088-3095.
30. Liu HF, An XJ, Yang Y, Yang L, Li Y, Huang CZ, Tao J, Tu YT. 2013. Association of rs10954213 polymorphisms and haplotype diversity in interferon regulatory factor 5 with systemic lupus erythematosus: a meta-analysis. J Huazhong Univ Sci Technolog Med Sci 33(1):15-21.
31. Londin ER, Keller MA, D'Andrea MR, Delgrosso K, Ertel A, Surrey S, Fortina P. 2011. Whole-exome sequencing of DNA from peripheral blood mononuclear cells (PBMC) and EBVtransformed lymphocytes from the same donor. BMC Genomics 12:464.
32. Mancl ME, Hu G, Sangster-Guity N, Olshalsky SL, Hoops K, Fitzgerald-Bocarsly P, Pitha PM, Pinder K, Barnes BJ. 2005. Two discrete promoters regulate the alternatively spliced human interferon regulatory factor-5 isoforms. Multiple isoforms with distinct cell type-specific expression, localization, regulation, and function. J Biol Chem 280(22):21078-21090.
33. Martin HJ, Lee JM, Walls D, Hayward SD. 2007. Manipulation of the toll-like receptor 7 signaling pathway by Epstein-Barr virus. J Virol 81(18):9748-9758.
34. Mellor J. 2005. The dynamics of chromatin remodeling at promoters. Mol Cell 19(2):147-157.
35. Miceli-Richard C, Comets E, Loiseau P, Puechal X, Hachulla E, Mariette X. 2007. Association of an IRF5 gene functional polymorphism with Sjogren's syndrome. Arthritis Rheum 56(12):3989-3994.
36. Niewold TB, Clark DN, Salloum R, Poole BD. 2010. Interferon alpha in systemic lupus erythematosus. J Biomed Biotechnol 2010:Article ID 948364.
37. Niewold TB, Kelly JA, Flesch MH, Espinoza LR, Harley JB, Crow MK. 2008. Association of the IRF5 risk haplotype with high serum interferon-a activity in systemic lupus erythematosus patients. Arthritis Rheum 58(8):2481-2487.
38. Niewold TB, Kelly JA, Kariuki SN, Franek BS, Kumar AA, Kaufman KM, Thomas K, Walker D, Kamp S, Frost JM, Wong AK, Merrill JT, Alarcón-Riquelme ME, Tikly M, Ramsey- Goldman R, Reveille JD, Petri MA, Edberg JC, Kimberly RP, Alarcón GS, Kamen DL, Gilkeson GS, Vyse TJ, James JA, Gaffney PM, Moser KL, Crow MK, Harley JB. 2012. IRF5 haplotypes demonstrate diverse serological associations which predict serum interferon alpha activity and explain the majority of the genetic association with systemic lupus erythematosus. Ann Rheum Dis 71(3):463-469.
39. Nordang GBN, Viken MK, Amundsen SS, Sanchez ES, Flatø B, Førre ØT, Martin J, Kvien TK, Lie BA. 2012. Interferon regulatory factor 5 gene polymorphism confers risk to several rheumatic diseases and correlates with expression of alternative thymic transcripts. Rheumatology 51(4):619-626.
40. Nordmark G, Kristjansdottir G, Theander E, Eriksson P, Brun JG, Wang C, Padyukov L, Truedsson L, Alm G, Eloranta ML, Jonsson R, Ronnblom L, Syvanen AC. 2008. Additive effects of the major risk alleles of IRF5 and STAT4 in primary Sjogren's syndrome. Genes Immun 10(1):68-76.
41. Qin L, Lv J, Zhou X, Hou P, Yang H, Zhang H. 2010. Association of IRF5 gene polymorphisms and lupus nephritis in a Chinese population. Nephrology (Carlton) 15(7):710-713.
42. Rullo OJ, Woo JMP, Wu H, Hoftman ADC, Maranian P, Brahn BA, McCurdy D, Cantor R, Tsao B. 2010. Association of IRF5 polymorphisms with activation of the Interferon-alpha pathway. Ann Rheum Dis 69:611-617.
43. Savitsky DA, Yanai H, Tamura T, Taniguchi T, Honda K. 2010. Contribution of IRF5 in B cells to the development of murine SLE-like disease through its transcriptional control of the IgG2a locus. Proc Natl Acad Sci U S A 107(22):10154-10159.
44. Shin SH, Kim B-h, Jang J-J, Suh KS, Kang GH. 2010. Identification of novel methylation markers in hepatocellular carcinoma using a methylation array. J Korean Med Sci 25(8):1152-1159.
45. Sie L, Loong S, Tan EK. 2009. Utility of lymphoblastoid cell lines. J Neurosci Res 87(9):1953-1959.
46. Sigurdsson S, Gö ring HHH, Kristjansdottir G, Milani L, Nordmark G, Sandling JK, Eloranta M-L, Feng D, Sangster-Guity N, Gunnarsson I, Svenungsson E, Sturfelt G, Jönsen A, Truedsson L, Barnes BJ, Alm G, Rönnblom L, Syvänen A-C. 2008. Comprehensive evaluation of the genetic variants of interferon regulatory factor 5 (IRF5) reveals a novel 5 bp length polymorphism as strong risk factor for systemic lupus erythematosus. Hum Mol Genet 17(6):872-881.
47. Sigurdsson S, Nordmark G, Goring HH, Lindroos K, Wiman AC, Sturfelt G, Jonsen A, Rantapaa-Dahlqvist S, Moller B, Kere J, Koskenmies S, Widen E, Eloranta ML, Julkunen H, Kristjansdottir H, Steinsson K, Alm G, Ronnblom L, Syvanen AC. 2005. Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus. Am J Hum Genet 76(3):528-537.
48. Sigurdsson S, Padyukov L, Kurreeman FA, Liljedahl U, Wiman AC, Alfredsson L, Toes R, Ronnelid J, Klareskog L, Huizinga TW, Alm G, Syvanen AC, Ronnblom L. 2007. Association of a haplotype in the promoter region of the interferon regulatory factor 5 gene with rheumatoid arthritis. Arthritis Rheum 56(7):2202-2210.
49. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101(16):6062-6067.
50. Tada Y, Kondo S, Aoki S, Koarada S, Inoue H, Suematsu R, Ohta A, Mak TW, Nagasawa K. 2011. Interferon regulatory factor 5 is critical for the development of lupus in MRL/lpr mice. Arthritis Rheum 63(3):738-748.
51. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596-1599.
52. Tsuchiya N, Ito I, Kawasaki A. 2010. Association of IRF5, STAT4 and BLK with systemic lupus erythematosus and other rheumatic diseases. Nihon Rinsho Meneki Gakkai Kaishi 33(2):57-65.
53. Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A. 2011. Determinants of nucleosome organization in primary human cells. Nature 474(7352):516-520.
54. Vosslamber S, van der Voort LF, van den Elskamp IJ, Heijmans R, Aubin C, Uitdehaag BM, Crusius JB, van der PouwKraan TC, Comabella M, Montalban X, Hafler DA, De Jager PL, Killestein J, Polman CH, Verweij CL. 2011. Interferon regulatory factor 5 gene variants and pharmacological and clinical outcome of Interferonbeta therapy in multiple sclerosis. Genes Immun 12(6):466-472.
55. Xu Y, Lee PY, Li Y, Liu C, Zhuang H, Han S, Nacionales DC, Weinstein J, Mathews CE, Moldawer LL, Li SW, Satoh M, Yang LJ, Reeves WH. 2012. Pleiotropic IFN-dependent and -independent effects of IRF5 on the pathogenesis of experimental lupus. J Immunol 188(8):4113-4121.
56. Yamashita M, Toyota M, Suzuki H, Nojima M, Yamamoto E, Kamimae S, Watanabe Y, Kai M, Akashi H, Maruyama R, Sasaki Y, Yamano H, Sugai T, Shinomura Y, Imai K, Tokino T, Itoh F. 2010. DNA methylation of interferon regulatory factors in gastric cancer and noncancerous gastric mucosae. Cancer Sci 101(7):1708-1716.
57. Yanagimachi M, Naruto T, Miyamae T, Hara T, Kikuchi M, Hara R, Imagawa T, Mori M, Sato H, Goto H, Yokota S. 2011. Association of IRF5 polymorphisms with susceptibility to macrophage activation syndrome in patients with juvenile idiopathic arthritis. J Rheumatol. 38(4):769-774.
58. Yanai H, Chen HM, Inuzuka T, Kondo S, Mak TW, Takaoka A, Honda K, Taniguchi T. 2007. Role of IFN regulatory factor 5 transcription factor in antiviral immunity and tumor suppression. Proc Natl Acad Sci U S A 104(9):3402-3407.
59. Yang L, Feng D, Bi X, Stone RC, Barnes BJ. 2012. Monocytes from Irf5 - / - mice have an intrinsic defect in their response to pristane-induced lupus. J Immunol 189(7):3741-3750.
60. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406-3415.