The autoimmune disease-associated transcription factors EOMES and TBX21 are dysregulated in multiple sclerosis and define a molecular subtype of disease

Clinical Immunology

Volumn 151, Issue 1, 2014, Pages 16-24

  Parnell, Grant P ^a   Gatt, Prudence N ^a   Krupa, Malgorzata ^b   Nickles, Dorothee ^c   McKay, Fiona C ^a   Schibeci, Stephen D ^a   Batten, Marcel ^d   Baranzini, Sergio ^c   Henderson, Andrew ^a   Barnett, Michael ^a   Slee, Mark ^b   Vucic, Steve ^e   Stewart, Graeme J ^a   Booth, David R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e University of Sydney   (Australia)

Author keywords

EOMES; Gene expression; Multiple sclerosis; TBX21; Transcription factors

Indexed keywords

RANTES; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EOMES; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; COHORT ANALYSIS; COMPUTER MODEL; CONTROLLED STUDY; DISABILITY; DISEASE COURSE; DOWN REGULATION; EXPANDED DISABILITY STATUS SCALE; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC REGULATION; HUMAN; IMMUNOCOMPETENT CELL; LYMPHOCYTE DIFFERENTIATION; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NATURAL KILLER CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STABLE EXPRESSION; T LYMPHOCYTE; YOUNG ADULT;

EOMES; GENE EXPRESSION; MULTIPLE SCLEROSIS; TBX21; TRANSCRIPTION FACTORS;

ADOLESCENT; ADULT; AGED; B-LYMPHOCYTES; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CHEMOKINE CCL5; COHORT STUDIES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; KILLER CELLS, NATURAL; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTES;

EID: 84893349476     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2014.01.003     Document Type: Article

References (49)

1. Beecham A.H., Patsopoulos N.A., Xifara D.K., Davis M.F., Kemppinen A., Cotsapas C., et al. Analysis of immune-related loci identifies 48 new susceptibility variants for multiple sclerosis. Nat. Genet. 2013, 45:1353-1360.
2. Parkes M., Cortes A., van Heel D.A., Brown M.A. Genetic insights into common pathways and complex relationships among immune-mediated diseases. Nat. Rev. Genet. 2013, 14:661-673.
3. Network-based multiple sclerosis pathway analysis with GWAS data from 15,000 cases and 30,000 controls. Am. J. Hum. Genet. 2013, 92(6):854-865.
4. Engelhardt B., Ransohoff R.M. Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol. 2012, 33:579-589.
5. Bruck W., Gold R., Lund B.T., Oreja-Guevara C., Prat A., Spencer C.M., et al. Therapeutic decisions in multiple sclerosis: moving beyond efficacy. JAMA Neurol. 2013, 70(10):1315-1324.
6. Bielekova B., Becker B.L. Monoclonal antibodies in MS: mechanisms of action. Neurology 2010, 74(Suppl. 1):S31-S40.
7. Mehling M., Kappos L., Derfuss T. Fingolimod for multiple sclerosis: mechanism of action, clinical outcomes, and future directions. Curr. Neurol. Neurosci. Rep. 2011, 11:492-497.
8. Trojano M., Pellegrini F., Paolicelli D., Fuiani A., Zimatore G.B., Tortorella C., et al. Real-life impact of early interferon beta therapy in relapsing multiple sclerosis. Ann. Neurol. 2009, 66:513-520.
9. Cohen J.A., Reingold S.C., Polman C.H., Wolinsky J.S. Disability outcome measures in multiple sclerosis clinical trials: current status and future prospects. Lancet Neurol. 2012, 11:467-476.
10. Sawcer S., Hellenthal G., Pirinen M., Spencer C.C., Patsopoulos N.A., Moutsianas L., et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011, 476:214-219.
11. Cotsapas C., Voight B.F., Rossin E., Lage K., Neale B.M., Wallace C., et al. Pervasive sharing of genetic effects in autoimmune disease. PLoS Genet. 2011, 7:e1002254.
12. Lazarevic V., Glimcher L.H., Lord G.M. T-bet: a bridge between innate and adaptive immunity. Nat. Rev. Immunol. 2013, 13:777-789.
13. Parnell G.P., Gatt P.N., McKay F.C., Schibeci S., Krupa M., Powell J.E., et al. Ribosomal protein S6 mRNA is a biomarker upregulated in multiple sclerosis, downregulated by interferon treatment, and affected by season. Mult. Scler. 2013, 10.1177/1352458513507819.
14. Nickles D., Chen H.P., Li M.M., Khankhanian P., Madireddy L., Caillier S.J., et al. Blood RNA profiling in a large cohort of multiple sclerosis patients and healthy controls. Hum. Mol. Genet. 2013, 22:4194-4205.
15. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
16. Vaquerizas J.M., Kummerfeld S.K., Teichmann S.A., Luscombe N.M. A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 2009, 10:252-263.
17. Whitney A.R., Diehn M., Popper S.J., Alizadeh A.A., Boldrick J.C., Relman D.A., et al. Individuality and variation in gene expression patterns in human blood. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:1896-1901.
18. Maes M., Stevens W., Scharpe S., Bosmans E., De Meyer F., D'Hondt P., et al. Seasonal variation in peripheral blood leukocyte subsets and in serum interleukin-6, and soluble interleukin-2 and -6 receptor concentrations in normal volunteers. Experientia 1994, 50:821-829.
19. Khoo A.L., Koenen H.J., Chai L.Y., Sweep F.C., Netea M.G., van der Ven A.J., et al. Seasonal variation in vitamin D(3) levels is paralleled by changes in the peripheral blood human T cell compartment. PLoS ONE 2012, 7:e29250.
20. Karlovich C., Duchateau-Nguyen G., Johnson A., McLoughlin P., Navarro M., Fleurbaey C., et al. A longitudinal study of gene expression in healthy individuals. BMC Med. Genet. 2009, 2:33.
21. Muroi S., Naoe Y., Miyamoto C., Akiyama K., Ikawa T., Masuda K., et al. Cascading suppression of transcriptional silencers by ThPOK seals helper T cell fate. Nat. Immunol. 2008, 9:1113-1121.
22. Hirahara K., Poholek A., Vahedi G., Laurence A., Kanno Y., Milner J.D., et al. Mechanisms underlying helper T-cell plasticity: implications for immune-mediated disease. J. Allergy Clin. Immunol. 2013, 131:1276-1287.
23. Westra H.J., Peters M.J., Esko T., Yaghootkar H., Schurmann C., Kettunen J., et al. Systematic identification of trans eQTLs as putative drivers of known disease associations. Nat. Genet. 2013, 45:1238-1243.
24. Kurtzke J.F. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983, 33:1444-1452.
25. Roxburgh R.H., Seaman S.R., Masterman T., Hensiek A.E., Sawcer S.J., Vukusic S., et al. Multiple Sclerosis Severity Score: using disability and disease duration to rate disease severity. Neurology 2005, 64:1144-1151.
26. Maurano M.T., Humbert R., Rynes E., Thurman R.E., Haugen E., Wang H., et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 2012, 337:1190-1195.
27. Axtell R.C., de Jong B.A., Boniface K., van der Voort L.F., Bhat R., De Sarno P., et al. T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nat. Med. 2010, 16:406-412.
28. Dominguez-Villar M., Baecher-Allan C.M., Hafler D.A. Identification of T helper type 1-like, Foxp3+ regulatory T cells in human autoimmune disease. Nat. Med. 2011, 17:673-675.
29. Astier A.L., Hafler D.A. Abnormal Tr1 differentiation in multiple sclerosis. J. Neuroimmunol. 2007, 191:70-78.
30. Martinez-Forero I., Garcia-Munoz R., Martinez-Pasamar S., Inoges S., Lopez-Diaz de Cerio A., Palacios R., et al. IL-10 suppressor activity and ex vivo Tr1 cell function are impaired in multiple sclerosis. Eur. J. Immunol. 2008, 38:576-586.
31. Costantino C.M., Baecher-Allan C., Hafler D.A. Multiple sclerosis and regulatory T cells. J. Clin. Immunol. 2008, 28:697-706.
32. Gandhi K.S., McKay F.C., Cox M., Riveros C., Armstrong N., Heard R.N., et al. The multiple sclerosis whole blood mRNA transcriptome and genetic associations indicate dysregulation of specific T cell pathways in pathogenesis. Hum. Mol. Genet. 2010, 19(11):2134-2143.
33. Chanvillard C., Jacolik R.F., Infante-Duarte C., Nayak R.C. The role of natural killer cells in multiple sclerosis and their therapeutic implications. Front. Immunol. 2013, 4:63.
34. De Jager P.L., Rossin E., Pyne S., Tamayo P., Ottoboni L., Viglietta V., et al. Cytometric profiling in multiple sclerosis uncovers patient population structure and a reduction of CD8low cells. Brain 2008, 131:1701-1711.
35. Fox R.J., Kivisakk P., Lee J.C., Tucky B., Lucchinetti C., Rudick R.A., et al. Chemokine receptors as biomarkers in multiple sclerosis. Dis. Markers 2006, 22:227-233.
36. Evans D.M., Frazer I.H., Martin N.G. Genetic and environmental causes of variation in basal levels of blood cells. Twin Res. 1999, 2:250-257.
37. Ubogu E.E., Callahan M.K., Tucky B.H., Ransohoff R.M. Determinants of CCL5-driven mononuclear cell migration across the blood-brain barrier. Implications for therapeutically modulating neuroinflammation. J. Neuroimmunol. 2006, 179:132-144.
38. Bartosik-Psujek H., Stelmasiak Z. The levels of chemokines CXCL8, CCL2 and CCL5 in multiple sclerosis patients are linked to the activity of the disease. Eur. J. Neurol. 2005, 12:49-54.
39. Martinez-Caceres E.M., Espejo C., Brieva L., Pericot I., Tintore M., Saez-Torres I., et al. Expression of chemokine receptors in the different clinical forms of multiple sclerosis. Mult. Scler. 2002, 8:390-395.
40. Mahad D.J., Trebst C., Kivisakk P., Staugaitis S.M., Tucky B., Wei T., et al. Expression of chemokine receptors CCR1 and CCR5 reflects differential activation of mononuclear phagocytes in pattern II and pattern III multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 2004, 63:262-273.
41. Matsui M., Weaver J., Proudfoot A.E., Wujek J.R., Wei T., Richer E., et al. Treatment of experimental autoimmune encephalomyelitis with the chemokine receptor antagonist Met-RANTES. J. Neuroimmunol. 2002, 128:16-22.
42. Jia Y., Li H., Chen W., Li M., Lv M., Feng P., et al. Prevention of murine experimental autoimmune encephalomyelitis by in vivo expression of a novel recombinant immunotoxin DT390-RANTES. Gene Ther. 2006, 13:1351-1359.
43. Oral presentations: ECTRIMS Lecture. Mult. Scler. J. 2013, 19:18-73.
44. Coles A.J., Fox E., Vladic A., Gazda S.K., Brinar V., Selmaj K.W., et al. Alemtuzumab more effective than interferon beta-1a at 5-year follow-up of CAMMS223 clinical trial. Neurology 2012, 78:1069-1078.
45. Gold R., Giovannoni G., Selmaj K., Havrdova E., Montalban X., Radue E.W., et al. Daclizumab high-yield process in relapsing-remitting multiple sclerosis (SELECT): a randomised, double-blind, placebo-controlled trial. Lancet 2013, 381:2167-2175.
46. Devonshire V., Havrdova E., Radue E.W., O'Connor P., Zhang-Auberson L., Agoropoulou C., et al. Relapse and disability outcomes in patients with multiple sclerosis treated with fingolimod: subgroup analyses of the double-blind, randomised, placebo-controlled FREEDOMS study. Lancet Neurol. 2012, 11:420-428.
47. Hauser S.L., Waubant E., Arnold D.L., Vollmer T., Antel J., Fox R.J., et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 2008, 358:676-688.
48. Kappos L., Li D., Calabresi P.A., O'Connor P., Bar-Or A., Barkhof F., et al. Ocrelizumab in relapsing-remitting multiple sclerosis: a phase 2, randomised, placebo-controlled, multicentre trial. Lancet 2011, 378:1779-1787.
49. Bourdette D., Gilden D. Fingolimod and multiple sclerosis: four cautionary tales. Neurology 2012, 79:1942-1943.