B cell signature during inactive systemic lupus is heterogeneous: Toward a biological dissection of lupus

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Garaud, Jean Claude ^a   Schickel, Jean Nicolas ^a   Blaison, Gilles ^b   Knapp, Anne Marie ^a,e   Dembele, Doulaye ^c   Ruer Laventie, Julie ^a   Korganow, Anne Sophie ^a,d,e   Martin, Thierry ^a,d,e   Soulas Sprauel, Pauline ^a,d,e   Pasquali, Jean Louis ^a,d,e  

^a INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b HÔPITAL CIVIL   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^e UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; B LYMPHOCYTE; CD1C GENE; CELL DIFFERENTIATION; CELL FUNCTION; CELL HETEROGENEITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISSECTION; EGR1 GENE; ENDOPLASMIC RETICULUM; FEMALE; GENE; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; LDOC1L GENE; MALE; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PMEPA 1 GENE; SYSTEMIC LUPUS ERYTHEMATOSUS; TLR 10 GENE; TRAF3IP2 GENE; TRANSCRIPTOMICS; CASE CONTROL STUDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOTYPE; UNFOLDED PROTEIN RESPONSE;

ANIMALIA; MUS;

INTERLEUKIN 4;

B-LYMPHOCYTES; CASE-CONTROL STUDIES; ENDOPLASMIC RETICULUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-4; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICROARRAY ANALYSIS; PHENOTYPE; UNFOLDED PROTEIN RESPONSE;

EID: 80051983086     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023900     Document Type: Article

References (51)

1. Hochberg MC, (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40 doi:10.1002/art.1780400928.
2. Reininger L, Winkler TH, Kalberer CP, Jourdan M, Melchers F, et al. (1996) Intrinsic B cell defects in NZB and NZW mice contribute to systemic lupus erythematosus in (NZB x NZW)F1 mice. J Exp Med 184: 853-861.
3. Odendahl M, Jacobi A, Hansen A, Feist E, Hiepe F, et al. (2000) Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol 165: 5970-5979.
4. Jacobi AM, Odendahl M, Reiter K, Bruns A, Burmester GR, et al. (2003) Correlation between circulating CD27high plasma cells and disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 48: 1332-1342 doi:10.1002/art.10949.
5. Grammer AC, Lipsky PE, (2003) B cell abnormalities in systemic lupus erythematosus. Arthritis Res Ther 5 (Suppl 4): S22-7 doi:10.1186/ar1009.
6. Dörner T, Lipsky PE, (2004) Correlation of circulating CD27high plasma cells and disease activity in systemic lupus erythematosus. Lupus 13: 283-289.
7. Jacobi AM, Reiter K, Mackay M, Aranow C, Hiepe F, et al. (2008) Activated memory B cell subsets correlate with disease activity in systemic lupus erythematosus: delineation by expression of CD27, IgD, and CD95. Arthritis Rheum 58: 1762-1773 doi:10.1002/art.23498.
8. Youinou P, Renaudineau Y, (2007) The paradox of CD5-expressing B cells in systemic lupus erythematosus. Autoimmun Rev 7: 149-154 doi:10.1016/j.autrev.2007.02.016.
9. Lipsky PE, (2001) Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2: 764-766 doi:10.1038/ni0901-764.
10. Mackay F, Silveira PA, Brink R, (2007) B cells and the BAFF/APRIL axis: fast-forward on autoimmunity and signaling. Current Opinion in Immunology 19: 327-336 doi:10.1016/j.coi.2007.04.008.
11. Banchereau J, Pascual V, (2006) Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 25: 383-392 doi:10.1016/j.immuni.2006.08.010.
12. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH, (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35: 630-640.
13. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80 doi:10.1186/gb-2004-5-10-r80.
14. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B (Methodological) 57: 289-300.
15. Benjamini Y, Yekutieli D, (2001) The control of the false discovery rate in multiple testing under dependency. Annals of Statistics 29: 1165-88.
16. Schwender H, Krause A, Ickstadt K, (2006) Identifying Interesting Genes with siggenes. Rnews 6: 45-50.
17. Zhu X, Hart R, Chang MS, Kim J-W, Lee SY, et al. (2004) Analysis of the major patterns of B cell gene expression changes in response to short-term stimulation with 33 single ligands. J Immunol 173: 7141-7149.
18. Simon JL, Bruce P, (1995) The new biostatistics of resampling. MD Comput 12: 115-21, 141.
19. Gao J, Ade AS, Tarcea VG, Weymouth TE, Mirel BR, et al. (2009) Integrating and annotating the interactome using the MiMI plugin for cytoscape. Bioinformatics 25: 137-138 doi:10.1093/bioinformatics/btn501.
20. Qian Y, Qin J, Cui G, Naramura M, Snow EC, et al. (2004) Act1, a negative regulator in CD40- and BAFF-mediated B cell survival. Immunity 21: 575-587 doi:10.1016/j.immuni.2004.09.001.
21. Qian Y, Liu C, Hartupee J, Altuntas CZ, Gulen MF, et al. (2007) The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 8: 247-256 doi:10.1038/ni1439.
22. Doreau A, Belot A, Bastid J, Riche B, Trescol-Biemont M-C, et al. (2009) Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat Immunol 10: 778-785 doi:10.1038/ni.1741.
23. Weller S, Braun MC, Tan BK, Rosenwald A, Cordier C, et al. (2004) Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104: 3647-3654 doi:10.1182/blood-2004-01-0346.
24. Korganow A-S, Knapp A-M, Nehme-Schuster H, Soulas-Sprauel P, Poindron V, et al. (2010) Peripheral B cell abnormalities in patients with systemic lupus erythematosus in quiescent phase: decreased memory B cells and membrane CD19 expression. J Autoimmun 34: 426-434 doi:10.1016/j.jaut.2009.11.002.
25. Hasan U, Chaffois C, Gaillard C, Saulnier V, Merck E, et al. (2005) Human TLR10 is a functional receptor, expressed by B cells and plasmacytoid dendritic cells, which activates gene transcription through MyD88. J Immunol 174: 2942-2950.
26. Guan Y, Ranoa DRE, Jiang S, Mutha SK, Li X, et al. (2010) Human TLRs 10 and 1 share common mechanisms of innate immune sensing but not signaling. J Immunol 184: 5094-5103 doi:10.4049/jimmunol.0901888.
27. Mora-López F, Pedreño-Horrillo N, Delgado-Pérez L, Brieva JA, Campos-Caro A, (2008) Transcription of PRDM1, the master regulator for plasma cell differentiation, depends on an SP1/SP3/EGR-1 GC-box. Eur J Immunol 38: 2316-2324 doi:10.1002/eji.200737861.
28. Iwakoshi NN, Lee A-H, Vallabhajosyula P, Otipoby KL, Rajewsky K, et al. (2003) Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 4: 321-329 doi:10.1038/ni907.
29. Lisbona F, Rojas-Rivera D, Thielen P, Zamorano S, Todd D, et al. (2009) BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol Cell 33: 679-691 doi:10.1016/j.molcel.2009.02.017.
30. Lyons PA, McKinney EF, Rayner TF, Hatton A, Woffendin HB, et al. (2010) Novel expression signatures identified by transcriptional analysis of separated leucocyte subsets in systemic lupus erythematosus and vasculitis. Annals of the Rheumatic Diseases 69: 1208-1213 doi:10.1136/ard.2009.108043.
31. Breitling R, (2006) Biological microarray interpretation: the rules of engagement. Biochim. Biophys. Acta 1759: 319-327 doi:10.1016/j.bbaexp.2006.06.003.
32. Hom G, Graham RR, Modrek B, Taylor KE, Ortmann W, et al. (2008) Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX. N Engl J Med 358: 900-909 doi:10.1056/NEJMoa0707865.
33. Tao J, Dong J, Li Y, Liu Y-Q, Yang J, et al. (2009) Up-regulation of cellular FLICE-inhibitory protein in peripheral blood B lymphocytes in patients with systemic lupus erythematosus is associated with clinical characteristics. J Eur Acad Dermatol Venereol 23: 433-437 doi:10.1111/j.1468-3083.2009.03095.x.
34. Wong CK, Ho CY, Li EK, Lam CW, (2000) Elevation of proinflammatory cytokine (IL-18, IL-17, IL-12) and Th2 cytokine (IL-4) concentrations in patients with systemic lupus erythematosus. Lupus 9: 589-593.
35. Nagy G, Pállinger E, Antal-Szalmás P, Aleksza M, Marschalkó M, et al. (2000) Measurement of intracellular interferon-gamma and interleukin-4 in whole blood T lymphocytes from patients with systemic lupus erythematosus. Immunol Lett 74: 207-210.
36. Yu H-H, Liu P-H, Lin Y-C, Chen WJ, Lee J-H, et al. (2010) Interleukin 4 and STAT6 gene polymorphisms are associated with systemic lupus erythematosus in Chinese patients. Lupus 19: 1219-1228 doi:10.1177/0961203310371152.
37. Yu CC, Yen TS, Lowell CA, DeFranco AL, (2001) Lupus-like kidney disease in mice deficient in the Src family tyrosine kinases Lyn and Fyn. Curr Biol 11: 34-38.
38. Engel P, Eck MJ, Terhorst C, (2003) The SAP and SLAM families in immune responses and X-linked lymphoproliferative disease. Nat Rev Immunol 3: 813-821 doi:10.1038/nri1202.
39. Luciano F, Ricci JE, Auberger P, (2001) Cleavage of Fyn and Lyn in their N-terminal unique regions during induction of apoptosis: a new mechanism for Src kinase regulation. Oncogene 20: 4935-4941 doi:10.1038/sj.onc.1204661.
40. Wary KK, Mariotti A, Zurzolo C, Giancotti FG, (1998) A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94: 625-634.
41. Li S, Couet J, Lisanti MP, (1996) Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 271: 29182-29190.
42. Xu Y, Yang G, Hu G, (2009) Binding of IFITM1 enhances the inhibiting effect of caveolin-1 on ERK activation. Acta Biochim Biophys Sin (Shanghai) 41: 488-494.
43. Gao Y, Howard A, Ban K, Chandra J, (2009) Oxidative stress promotes transcriptional up-regulation of Fyn in BCR-ABL1-expressing cells. J Biol Chem 284: 7114-7125 doi:10.1074/jbc.M804801200.
44. Maltzman JS, Carmen JA, Monroe JG, (1996) Transcriptional regulation of the Icam-1 gene in antigen receptor- and phorbol ester-stimulated B lymphocytes: role for transcription factor EGR1. J Exp Med 183: 1747-1759.
45. Maltzman JS, Carman JA, Monroe JG, (1996) Role of EGR1 in regulation of stimulus-dependent CD44 transcription in B lymphocytes. Mol Cell Biol 16: 2283-2294.
46. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee A-H, Qian S-B, et al. (2004) XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21: 81-93 doi:10.1016/j.immuni.2004.06.010.
47. Calame K, (2008) Activation-dependent induction of Blimp-1. Current Opinion in Immunology 20: 259-264 doi:10.1016/j.coi.2008.04.010.
48. Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, et al. (2009) A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41: 1228-1233 doi:10.1038/ng.468.
49. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K, (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
50. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96 doi:10.1038/415092a.
51. Chaussabel D, Quinn C, Shen J, Patel P, Glaser C, et al. (2008) A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 29: 150-164 doi:10.1016/j.immuni.2008.05.012.