Genetic interaction between genes involved in NF-κB signaling pathway in systemic lupus erythematosus

Molecular Immunology

Volumn 56, Issue 4, 2013, Pages 643-648

  Cen, Han ^a   Zhou, Mo ^a   Leng, Rui Xue ^a   Wang, Wei ^a   Feng, Chen Chen ^a   Li, Bao Zhu ^a   Zhu, Yan ^a   Yang, Xiao Ke ^a   Yang, Mei ^a   Zhai, Yu ^a   Zhang, Min ^a   Hu, Lin Feng ^a   Li, Rui ^a   Chen, Gui Mei ^a   Chen, Hong ^a   Pan, Hai Feng ^a   Li, Xiang Pei ^b   Ye, Dong Qing ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b ANHUI PROVINCIAL HOSPITAL   (China)

Author keywords

Gene; Interaction; NF B; Susceptibility; Systemic lupus erythematosus

Indexed keywords

I KAPPA B; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN 1; SYNAPSIN I; SYNAPSIN II; TRANSCRIPTION FACTOR REL; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA INDUCED PROTEIN 3; TUMOR NECROSIS FACTOR ALPHA INDUCED PROTEIN 3 INTERACTING PROTEIN 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CHINESE; CONTROLLED STUDY; FEMALE; GENE; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOTYPE; HUMAN; HYPOTHESIS; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS;

EID: 84881106721     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.07.006     Document Type: Article

References (42)

1. Alarcon-Segovia D., Alarcon-Riquelme M.E., Cardiel M.H., Caeiro F., Massardo L., Villa A.R., Pons-Estel B.A. Familial aggregation of systemic lupus erythematosus, rheumatoid arthritis, and other autoimmune diseases in 1177 lupus patients from the GLADEL cohort. Arthritis and Rheumatism 2005, 52:1138-1147.
2. Albertella M.R., Campbell R.D. Characterization of a novel gene in the human major histocompatibility complex that encodes a potential new member of the I kappa B family of proteins. Human Molecular Genetics 1994, 3:793-799.
3. Allanore Y., Saad M., Dieude P., Avouac J., Distler J.H., Amouyel P., Matucci-Cerinic M., Riemekasten G., Airo P., Melchers I., Hachulla E., Cusi D., Wichmann H.E., Wipff J., Lambert J.C., Hunzelmann N., Tiev K., Caramaschi P., Diot E., Kowal-Bielecka O., Valentini G., Mouthon L., Czirjak L., Damjanov N., Salvi E., Conti C., Muller M., Muller-Ladner U., Riccieri V., Ruiz B., Cracowski J.L., Letenneur L., Dupuy A.M., Meyer O., Kahan A., Munnich A., Boileau C., Martinez M. Genome-wide scan identifies TNIP1, PSORS1C1, and RHOB as novel risk loci for systemic sclerosis. PLoS Genetics 2011, 7:e1002091.
4. Andersson T., Alfredsson L., Kallberg H., Zdravkovic S., Ahlbom A. Calculating measures of biological interaction. European Journal of Epidemiology 2005, 20:575-579.
5. Castiblanco J., Anaya J.M. The IkappaBL gene polymorphism influences risk of acquiring systemic lupus erythematosus and Sjogren's syndrome. Human Immunology 2008, 69:45-51.
6. Castillejo-Lopez C., Delgado-Vega A.M., Wojcik J., Kozyrev S.V., Thavathiru E., Wu Y.Y., Sanchez E., Pollmann D., Lopez-Egido J.R., Fineschi S., Dominguez N., Lu R., James J.A., Merrill J.T., Kelly J.A., Kaufman K.M., Moser K.L., Gilkeson G., Frostegard J., Pons-Estel B.A., D'Alfonso S., Witte T., Callejas J.L., Harley J.B., Gaffney P.M., Martin J., Guthridge J.M., Alarcon-Riquelme M.E. Genetic and physical interaction of the B-cell systemic lupus erythematosus-associated genes BANK1 and BLK. Annals of the Rheumatic Diseases 2012, 71:136-142.
7. Chen Z.J. Ubiquitin signalling in the NF-kappaB pathway. Nature Cell Biology 2005, 7:758-765.
8. Cordell H.J. Detecting gene-gene interactions that underlie human diseases. Nature Reviews Genetics 2009, 10:392-404.
9. Deapen D., Escalante A., Weinrib L., Horwitz D., Bachman B., Roy-Burman P., Walker A., Mack T.M. A revised estimate of twin concordance in systemic lupus erythematosus. Arthritis and Rheumatism 1992, 35:311-318.
10. Gao L., Coope H., Grant S., Ma A., Ley S.C., Harhaj E.W. ABIN1 protein cooperates with TAX1BP1 and A20 proteins to inhibit antiviral signaling. Journal of Biological Chemistry 2011, 286:36592-36602.
11. Gao M., Wang C.H., Sima X., Han X.M. NFKB1-94 insertion/deletion ATTG polymorphism contributes to risk of systemic lupus erythematosus. DNA and Cell Biology 2012, 31:611-615.
12. Graham R.R., Hom G., Ortmann W., Behrens T.W. Review of recent genome-wide association scans in lupus. Journal of Internal Medicine 2009, 265:680-688.
13. Gregersen P.K., Amos C.I., Lee A.T., Lu Y., Remmers E.F., Kastner D.L., Seldin M.F., Criswell L.A., Plenge R.M., Holers V.M., Mikuls T.R., Sokka T., Moreland L.W., Bridges S.L., Xie G., Begovich A.B., Siminovitch K.A. REL, encoding a member of the NF-kappaB family of transcription factors, is a newly defined risk locus for rheumatoid arthritis. Nature Genetics 2009, 41:820-823.
14. Han J.W., Zheng H.F., Cui Y., Sun L.D., Ye D.Q., Hu Z., Xu J.H., Cai Z.M., Huang W., Zhao G.P., Xie H.F., Fang H., Lu Q.J., Li X.P., Pan Y.F., Deng D.Q., Zeng F.Q., Ye Z.Z., Zhang X.Y., Wang Q.W., Hao F., Ma L., Zuo X.B., Zhou F.S., Du W.H., Cheng Y.L., Yang J.Q., Shen S.K., Li J., Sheng Y.J., Zuo X.X., Zhu W.F., Gao F., Zhang P.L., Guo Q., Li B., Gao M., Xiao F.L., Quan C., Zhang C., Zhang Z., Zhu K.J., Li Y., Hu D.Y., Lu W.S., Huang J.L., Liu S.X., Li H., Ren Y.Q., Wang Z.X., Yang C.J., Wang P.G., Zhou W.M., Lv Y.M., Zhang A.P., Zhang S.Q., Lin D., Low H.Q., Shen M., Zhai Z.F., Wang Y., Zhang F.Y., Yang S., Liu J.J., Zhang X.J. Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nature Genetics 2009, 41:1234-1237.
15. Harley I.T., Kaufman K.M., Langefeld C.D., Harley J.B., Kelly J.A. Genetic susceptibility to SLE: new insights from fine mapping and genome-wide association studies. Nature Reviews Genetics 2009, 10:285-290.
16. Hellquist A., Jarvinen T.M., Koskenmies S., Zucchelli M., Orsmark-Pietras C., Berglind L., Panelius J., Hasan T., Julkunen H., D'Amato M., Saarialho-Kere U., Kere J. Evidence for genetic association and interaction between the TYK2 and IRF5 genes in systemic lupus erythematosus. Journal of Rheumatology 2009, 36:1631-1638.
17. Hochberg M.C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis and Rheumatism 1997, 40:1725.
18. Hughes T., Adler A., Kelly J.A., Kaufman K.M., Williams A.H., Langefeld C.D., Brown E.E., Alarcon G.S., Kimberly R.P., Edberg J.C., Ramsey-Goldman R., Petri M., Boackle S.A., Stevens A.M., Reveille J.D., Sanchez E., Martin J., Niewold T.B., Vila L.M., Scofield R.H., Gilkeson G.S., Gaffney P.M., Criswell L.A., Moser K.L., Merrill J.T., Jacob C.O., Tsao B.P., James J.A., Vyse T.J., Alarcon-Riquelme M.E., Harley J.B., Richardson B.C., Sawalha A.H. Evidence for gene-gene epistatic interactions among susceptibility loci for systemic lupus erythematosus. Arthritis and Rheumatism 2012, 64:485-492.
19. Karban A.S., Okazaki T., Panhuysen C.I., Gallegos T., Potter J.J., Bailey-Wilson J.E., Silverberg M.S., Duerr R.H., Cho J.H., Gregersen P.K., Wu Y., Achkar J.P., Dassopoulos T., Mezey E., Bayless T.M., Nouvet F.J., Brant S.R. Functional annotation of a novel NFKB1 promoter polymorphism that increases risk for ulcerative colitis. Human Molecular Genetics 2004, 13:35-45.
20. Kawasaki A., Ito I., Ito S., Hayashi T., Goto D., Matsumoto I., Takasaki Y., Hashimoto H., Sumida T., Tsuchiya N. Association of TNFAIP3 polymorphism with susceptibility to systemic lupus erythematosus in a Japanese population. Journal of Biomedicine and Biotechnology 2010, 2010:207-578.
21. Kawasaki A., Ito S., Furukawa H., Hayashi T., Goto D., Matsumoto I., Kusaoi M., Ohashi J., Graham R.R., Matsuta K., Behrens T.W., Tohma S., Takasaki Y., Hashimoto H., Sumida T., Tsuchiya N. Association of TNFAIP3 interacting protein 1 TNIP1 with systemic lupus erythematosus in a Japanese population: a case-control association study. Arthritis Research and Therapy 2010, 12:R174.
22. Kraft P. Curses - winner's and otherwise - in genetic epidemiology. Epidemiology 2008, 19:649-651. discussion 657-648.
23. Leng R.X., Wang W., Cen H., Zhou M., Feng C.C., Zhu Y., Yang X.K., Yang M., Zhai Y., Li B.Z., Wang X.S., Li R., Chen G.M., Chen H., Pan H.F., Ye D.Q. Gene-gene and gene-sex epistatic interactions of MiR146a, IRF5, IKZF1, ETS1 and IL21 in systemic lupus erythematosus. PLoS ONE 2012, 7:e51090.
24. Li Z.W., Chu W., Hu Y., Delhase M., Deerinck T., Ellisman M., Johnson R., Karin M. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. Journal of Experimental Medicine 1999, 189:1839-1845.
25. Lodolce J.P., Kolodziej L.E., Rhee L., Kariuki S.N., Franek B.S., McGreal N.M., Logsdon M.F., Bartulis S.J., Perera M.A., Ellis N.A., Adams E.J., Hanauer S.B., Jolly M., Niewold T.B., Boone D.L. African-derived genetic polymorphisms in TNFAIP3 mediate risk for autoimmunity. Journal of Immunology 2010, 184:7001-7009.
26. Moore J.H. The ubiquitous nature of epistasis in determining susceptibility to common human diseases. Human Heredity 2003, 56:73-82.
27. Moynagh P.N. The NF-kappaB pathway. Journal of Cell Science 2005, 118:4589-4592.
28. Musone S.L., Taylor K.E., Lu T.T., Nititham J., Ferreira R.C., Ortmann W., Shifrin N., Petri M.A., Kamboh M.I., Manzi S., Seldin M.F., Gregersen P.K., Behrens T.W., Ma A., Kwok P.Y., Criswell L.A. Multiple polymorphisms in the TNFAIP3 region are independently associated with systemic lupus erythematosus. Nature Genetics 2008, 40:1062-1064.
29. Namjou B., Choi C.B., Harley I.T., Alarcon-Riquelme M.E., Kelly J.A., Glenn S.B., Ojwang J.O., Adler A., Kim K., Gallant C.J., Boackle S.A., Criswell L.A., Kimberly R.P., Brown E.E., Edberg J., Alarcon G.S., Stevens A.M., Jacob C.O., Gilkeson G.S., Kamen D.L., Tsao B.P., Anaya J.M., Kim E.M., Park S.Y., Sung Y.K., Guthridge J.M., Merrill J.T., Petri M., Ramsey-Goldman R., Vila L.M., Niewold T.B., Martin J., Pons-Estel B.A., Vyse T.J., Freedman B.I., Moser K.L., Gaffney P.M., Williams A.H., Comeau M.E., Reveille J.D., Kang C., James J.A., Scofield R.H., Langefeld C.D., Kaufman K.M., Harley J.B., Bae S.C. Evaluation of TRAF6 in a large multiancestral lupus cohort. Arthritis and Rheumatism 2012, 64:1960-1969.
30. Okamoto K., Makino S., Yoshikawa Y., Takaki A., Nagatsuka Y., Ota M., Tamiya G., Kimura A., Bahram S., Inoko H. Identification of I kappa BL as the second major histocompatibility complex-linked susceptibility locus for rheumatoid arthritis. American Journal of Human Genetics 2003, 72:303-312.
31. Orozco G., Sanchez E., Collado M.D., Lopez-Nevot M.A., Paco L., Garcia A., Jimenez-Alonso J., Martin J. Analysis of the functional NFKB1 promoter polymorphism in rheumatoid arthritis and systemic lupus erythematosus. Tissue Antigens 2005, 65:183-186.
32. Sheng Y.J., Gao J.P., Li J., Han J.W., Xu Q., Hu W.L., Pan T.M., Cheng Y.L., Yu Z.Y., Ni C., Yao S., He C.F., Liu Y.S., Li Y., Ge H.M., Xiao F.L., Sun L.D., Yang S., Zhang X.J. Follow-up study identifies two novel susceptibility loci PRKCB and 8p11.21 for systemic lupus erythematosus. Rheumatology 2011, 50:682-688.
33. Shimane K., Kochi Y., Horita T., Ikari K., Amano H., Hirakata M., Okamoto A., Yamada R., Myouzen K., Suzuki A., Kubo M., Atsumi T., Koike T., Takasaki Y., Momohara S., Yamanaka H., Nakamura Y., Yamamoto K. The association of a nonsynonymous single-nucleotide polymorphism in TNFAIP3 with systemic lupus erythematosus and rheumatoid arthritis in the Japanese population. Arthritis and Rheumatism 2010, 62:574-579.
34. Tanaka M., Fuentes M.E., Yamaguchi K., Durnin M.H., Dalrymple S.A., Hardy K.L., Goeddel D.V. Embryonic lethality, liver degeneration, and impaired NF-kappa B activation in IKK-beta-deficient mice. Immunity 1999, 10:421-429.
35. Trynka G., Zhernakova A., Romanos J., Franke L., Hunt K.A., Turner G., Bruinenberg M., Heap G.A., Platteel M., Ryan A.W., de Kovel C., Holmes G.K., Howdle P.D., Walters J.R., Sanders D.S., Mulder C.J., Mearin M.L., Verbeek W.H., Trimble V., Stevens F.M., Kelleher D., Barisani D., Bardella M.T., McManus R., van Heel D.A., Wijmenga C. Coeliac disease-associated risk variants in TNFAIP3 and REL implicate altered NF-kappaB signalling. Gut 2009, 58:1078-1083.
36. Varade J., Palomino-Morales R., Ortego-Centeno N., Diaz-Rubio M., Fernandez-Gutierrez B., Gonzalez-Gay M.A., Pascual-Salcedo D., Balsa A., Iglesias A., Gomez-Garcia M., Witte T., Radstake T.R., Coenen M.J., Urcelay E., Martin J. Analysis of the REL polymorphism rs13031237 in autoimmune diseases. Annals of the Rheumatic Diseases 2011, 70:711-712.
37. Wertz I.E., O'Rourke K.M., Zhou H., Eby M., Aravind L., Seshagiri S., Wu P., Wiesmann C., Baker R., Boone D.L., Ma A., Koonin E.V., Dixit V.M. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004, 430:694-699.
38. Yang W., Shen N., Ye D.Q., Liu Q., Zhang Y., Qian X.X., Hirankarn N., Ying D., Pan H.F., Mok C.C., Chan T.M., Wong R.W., Lee K.W., Mok M.Y., Wong S.N., Leung A.M., Li X.P., Avihingsanon Y., Wong C.M., Lee T.L., Ho M.H., Lee P.P., Chang Y.K., Li P.H., Li R.J., Zhang L., Wong W.H., Ng I.O., Lau C.S., Sham P.C., Lau Y.L. Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genetics 2010, 6:e1000841.
39. Yu H.H., Liu P.H., Lin Y.C., Chen W.J., Lee J.H., Wang L.C., Yang Y.H., Chiang B.L. Interleukin 4 and STAT6 gene polymorphisms are associated with systemic lupus erythematosus in Chinese patients. Lupus 2010, 19:1219-1228.
40. Zhong H., Li X.L., Li M., Hao L.X., Chen R.W., Xiang K., Qi X.B., Ma R.Z., Su B. Replicated associations of TNFAIP3, TNIP1 and ETS1 with systemic lupus erythematosus in a southwestern Chinese population. Arthritis Research and Therapy 2011, 13:R186.
41. Zhou X.J., Lu X.L., Nath S.K., Lv J.C., Zhu S.N., Yang H.Z., Qin L.X., Zhao M.H., Su Y., Shen N., Li Z.G., Zhang H. Gene-gene interaction of BLK, TNFSF4, TRAF1 TNFAIP3, and REL in systemic lupus erythematosus. Arthritis and Rheumatism 2012, 64:222-231.
42. Zou G.Y. On the estimation of additive interaction by use of the four-by-two table and beyond. American Journal of Epidemiology 2008, 168:212-224.