Type I interferon receptor controls B-cell expression of nucleic acid-sensing Toll-like receptors and autoantibody production in a murine model of lupus

Arthritis Research and Therapy

Volumn 11, Issue 4, 2009, Pages

  Thibault, Donna L ^a,b   Graham, Kareem L ^a   Lee, Lowen Y ^a   Balboni, Imelda ^a   Hertzog, Paul J ^c   Utz, Paul J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GENENTECH INC   (United States)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; ALPHA INTERFERON RECEPTOR 1; ALPHA INTERFERON RECEPTOR 2; AUTOANTIBODY; AUTOANTIGEN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; PHOSPHOPROTEIN; PRISTANE; RIBONUCLEOPROTEIN; SINGLE STRANDED DNA; SM ANTIBODY; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; IFNAR2 PROTEIN, MOUSE; INTERLEUKIN 6; NUCLEIC ACID; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; BAGG ALBINO MOUSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA SYNTHESIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENOTYPE; HYPERGAMMAGLOBULINEMIA; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOPRECIPITATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEINURIA; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; UPREGULATION; ANIMAL; BIOSYNTHESIS; BLOOD; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PROTEIN MICROARRAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; B-LYMPHOCYTES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOPRECIPITATION; INTERLEUKIN-6; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; NUCLEIC ACIDS; PROTEIN ARRAY ANALYSIS; RECEPTOR, INTERFERON ALPHA-BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTORS;

EID: 68849105323     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2771     Document Type: Article

References (57)

1. Banchereau J Pascual V Type I interferon in systemic lupus erythematosus and other autoimmune diseases Immunity 2006, 25:383-392 10.1016/ j.immuni.2006.08.010 16979570
2. Marshak-Rothstein A Rifkin IR Immunologically active autoantigens: The role of toll-like receptors in the development of chronic inflammatory disease Annu Rev Immunol 2007, 25:419-441 10.1146/ annurev.immunol.22.012703.104514 17378763
3. Savarese E Chae OW Trowitzsch S Weber G Kastner B Akira S Wagner H Schmid RM Bauer S Krug A U1 small nuclear ribonucleoprotein immune complexes induce type I interferon in plasmacytoid dendritic cells through TLR7 Blood 2006, 107:3229-3234 10.1182/blood-2005-07-2650 16368889
4. Lovgren T Eloranta ML Kastner B Wahren-Herlenius M Alm GV Ronnblom L Induction of interferon-alpha by immune complexes or liposomes containing systemic lupus erythematosus autoantigen- and Sjogren's syndrome autoantigen-associated RNA Arthritis Rheum 2006, 54:1917-1927 10.1002/art.21893 16729300
5. Kelly KM Zhuang H Nacionales DC Scumpia PO Lyons R Akaogi J Lee P Williams B Yamamoto M Akira S Satoh M Reeves WH "Endogenous adjuvant" activity of the RNA components of lupus autoantigens Sm/ RNP and Ro 60 Arthritis Rheum 2006, 54:1557-1567 10.1002/art.21819 16645989
6. Vollmer J Tluk S Schmitz C Hamm S Jurk M Forsbach A Akira S Kelly KM Reeves WH Bauer S Krieg AM Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8 J Exp Med 2005, 202:1575-1585 2213330 16330816 10.1084/jem.20051696
7. Means TK Latz E Hayashi F Murali MR Golenbock DT Luster AD Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9 J Clin Invest 2005, 115:407-417 544604 15668740
8. Lau CM Broughton C Tabor AS Akira S Flavell RA Mamula MJ Christensen SR Shlomchik MJ Viglianti GA Rifkin IR Marshak-Rothstein A RNA-associated autoantigens activate B cells by combined B cell antigen receptor/ Toll-like receptor 7 engagement J Exp Med 2005, 202:1171-1177 2213226 16260486 10.1084/jem.20050630
9. Barrat FJ Meeker T Gregorio J Chan JH Uematsu S Akira S Chang B Duramad O Coffman RL Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus J Exp Med 2005, 202:1131-1139 2213213 16230478 10.1084/ jem.20050914
10. Hoffman RW Gazitt T Foecking MF Ortmann RA Misfeldt M Jorgenson R Young SL Greidinger EL U1 RNA induces innate immunity signaling Arthritis Rheum 2004, 50:2891-2896 1475509 15457457 10.1002/art.20428
11. Leadbetter EA Rifkin IR Hohlbaum AM Beaudette BC Shlomchik MJ Marshak-Rothstein A Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors Nature 2002, 416:603-607 10.1038/416603a 11948342
12. Yasuda K Richez C Maciaszek JW Agrawal N Akira S Marshak-Rothstein A Rifkin IR Murine dendritic cell type I IFN production induced by human IgG-RNA immune complexes is IFN regulatory factor (IRF)5 and IRF7 dependent and is required for IL-6 production J Immunol 2007, 178:6876-6885 17513736
13. Christensen SR Shupe J Nickerson K Kashgarian M Flavell RA Shlomchik MJ Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus Immunity 2006, 25:417-428 10.1016/j.immuni.2006.07.013 16973389
14. Savarese E Steinberg C Pawar RD Reindl W Akira S Anders HJ Krug A Requirement of Toll-like receptor 7 for pristane-induced production of autoantibodies and development of murine lupus nephritis Arthritis Rheum 2008, 58:1107-1115 10.1002/art.23407 18383384
15. Subramanian S Tus K Li QZ Wang A Tian XH Zhou J Liang C Bartov G McDaniel LD Zhou XJ Schultz RA Wakeland EK A Tlr7 translocation accelerates systemic autoimmunity in murine lupus Proc Natl Acad Sci USA 2006, 103:9970-9975 1502563 16777955 10.1073/pnas.0603912103
16. Pisitkun P Deane JA Difilippantonio MJ Tarasenko T Satterthwaite AB Bolland S Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication Science 2006, 312:1669-1672 10.1126/ science.1124978 16709748
17. Santiago-Raber ML Kikuchi S Borel P Uematsu S Akira S Kotzin BL Izui S Evidence for genes in addition to Tlr7 in the Yaa translocation linked with acceleration of systemic lupus erythematosus J Immunol 2008, 181:1556-1562 18606711
18. Fairhurst AM Hwang SH Wang A Tian XH Boudreaux C Zhou XJ Casco J Li QZ Connolly JE Wakeland EK Yaa autoimmune phenotypes are conferred by overexpression of TLR7 Eur J Immunol 2008, 38:1971-1978 10.1002/ eji.200838138 18521959
19. Ehlers M Fukuyama H McGaha TL Aderem A Ravetch JV TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE J Exp Med 2006, 203:553-561 2118244 16492804 10.1084/jem.20052438
20. Satoh M Reeves WH Induction of lupus-associated autoantibodies in BALB/c mice by intraperitoneal injection of pristane J Exp Med 1994, 180:2341-2346 2191761 7964507 10.1084/jem.180.6.2341
21. Craft J Antibodies to snRNPs in systemic lupus erythematosus Rheum Dis Clin North Am 1992, 18:311-335 1626072
22. Nacionales DC Kelly KM Lee PY Zhuang H Li Y Weinstein JS Sobel E Kuroda Y Akaogi J Satoh M Reeves WH Type I interferon production by tertiary lymphoid tissue developing in response to 2,6,10,14-tetramethyl-pentadecane (pristane) Am J Pathol 2006, 168:1227-1240 1606560 16565497 10.2353/ajpath.2006.050125
23. Zhuang H Narain S Sobel E Lee PY Nacionales DC Kelly KM Richards HB Segal M Stewart C Satoh M Reeves WH Association of anti-nucleoprotein autoantibodies with upregulation of Type I interferon-inducible gene transcripts and dendritic cell maturation in systemic lupus erythematosus Clin Immunol 2005, 117:238-250 10.1016/j.clim.2005.07.009 16126005
24. Kirou KA Lee C George S Louca K Papagiannis IG Peterson MG Ly N Woodward RN Fry KE Lau AY Prentice JG Wohlgemuth JG Crow MK Coordinate overexpression of interferon-alpha-induced genes in systemic lupus erythematosus Arthritis Rheum 2004, 50:3958-3967 10.1002/art.20798 15593221
25. Lee PY Kumagai Y Li Y Takeuchi O Yoshida H Weinstein J Kellner ES Nacionales D Barker T Kelly-Scumpia K van Rooijen N Kumar H Kawai T Satoh M Akira S Reeves WH TLR7-dependent and FcgammaR-independent production of type I interferon in experimental mouse lupus J Exp Med 2008, 205:2995-3006 2605237 19047436 10.1084/jem.20080462
26. Calvani N Caricchio R Tucci M Sobel ES Silvestris F Tartaglia P Richards HB Induction of apoptosis by the hydrocarbon oil pristane: Implications for pristane-induced lupus J Immunol 2005, 175:4777-4782 16177126
27. Hardy MP Owczarek CM Trajanovska S Liu X Kola I Hertzog PJ The soluble murine type I interferon receptor Ifnar-2 is present in serum, is independently regulated, and has both agonistic and antagonistic properties Blood 2001, 97:473-482 10.1182/blood.V97.2.473 11154225
28. Owczarek CM Hwang SY Holland KA Gulluyan LM Tavaria M Weaver B Reich NC Kola I Hertzog PJ Cloning and characterization of soluble and transmembrane isoforms of a novel component of the murine type I interferon receptor, IFNAR 2 J Biol Chem 1997, 272:23865-23870 10.1074/ jbc.272.38.23865 9295335
29. Rothlin CV Ghosh S Zuniga EI Oldstone MB Lemke G TAM receptors are pleiotropic inhibitors of the innate immune response Cell 2007, 131:1124-1136 10.1016/j.cell.2007.10.034 18083102
30. Fenner JE Starr R Cornish AL Zhang JG Metcalf D Schreiber RD Sheehan K Hilton DJ Alexander WS Hertzog PJ Suppressor of cytokine signaling 1 regulates the immune response to infection by a unique inhibition of type I interferon activity Nat Immunol 2006, 7:33-39 10.1038/ni1287 16311601
31. van Boxel-Dezaire AH Rani MR Stark GR Complex modulation of cell type-specific signaling in response to type I interferons Immunity 2006, 25:361-372 10.1016/j.immuni.2006.08.014 16979568
32. Thibault DL Chu AD Graham KL Balboni I Lee LY Kohlmoos C Landrigan A Higgins JP Tibshirani R Utz PJ IRF9 and STAT1 are required for IgG autoantibody production and B cell expression of TLR7 in mice J Clin Invest 2008, 118:1417-1426 2267033 18340381 10.1172/JCI30065
33. Nacionales DC Kelly-Scumpia KM Lee PY Weinstein JS Lyons R Sobel E Satoh M Reeves WH Deficiency of the type I interferon receptor protects mice from experimental lupus Arthritis Rheum 2007, 56:3770-3783 10.1002/ art.23023 17968932
34. Tusher VG Tibshirani R Chu G Significance analysis of microarrays applied to the ionizing radiation response Proc Natl Acad Sci USA 2001, 98:5116-5121 33173 11309499 10.1073/pnas.091062498
35. Eisen MB Spellman PT Brown PO Botstein D Cluster analysis and display of genome-wide expression patterns Proc Natl Acad Sci USA 1998, 95:14863-14868 24541 9843981 10.1073/pnas.95.25.14863
36. Saldanha AJ Java Treeview - extensible visualization of microarray data Bioinformatics 2004, 20:3246-3248 10.1093/bioinformatics/bth349 15180930
37. Protocols - The Utz Lab - Stanford University School of Medicine http://utzlab.stanford.edu/protocols
38. Satoh M Kumar A Kanwar YS Reeves WH Anti-nuclear antibody production and immune-complex glomerulonephritis in BALB/c mice treated with pristane Proc Natl Acad Sci USA 1995, 92:10934-10938 40545 7479913 10.1073/ pnas.92.24.10934
39. Hamilton KJ Satoh M Swartz J Richards HB Reeves WH Influence of microbial stimulation on hypergammaglobulinemia and autoantibody production in pristane-induced lupus Clin Immunol Immunopathol 1998, 86:271-279 10.1006/clin.1997.4481 9557160
40. Nimmerjahn F Bruhns P Horiuchi K Ravetch JV FcgammaRIV: A novel FcR with distinct IgG subclass specificity Immunity 2005, 23:41-51 10.1016/ j.immuni.2005.05.010 16039578
41. Jego G Palucka AK Blanck JP Chalouni C Pascual V Banchereau J Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6 Immunity 2003, 19:225-234 10.1016/ S1074-7613(03)00208-5 12932356
42. Le Bon A Schiavoni G D'Agostino G Gresser I Belardelli F Tough DF Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo Immunity 2001, 14:461-470 10.1016/S1074-7613(01)00126-1 11336691
43. Kattah MG Alemi GR Thibault DL Utz PJ A novel two-color Fab labeling method for autoantigen protein microarrays Nat Methods 2006, 3:745-51 10.1038/nmeth910 16929321
44. Graham KL Vaysberg M Kuo A Utz PJ Autoantigen arrays for multiplex analysis of antibody isotypes Proteomics 2006, 6:5720-5724 10.1002/ pmic.200600345 17068762
45. Sekine H Graham KL Zhao S Elliott MK Ruiz P Utz PJ Gilkeson GS Role of MHC-linked genes in autoantigen selection and renal disease in a murine model of systemic lupus erythematosus J Immunol 2006, 177:7423-7434 17082662
46. Robinson WH DiGennaro C Hueber W Haab BB Kamachi M Dean EJ Fournel S Fong D Genovese MC de Vegvar HE Skriner K Hirschberg DL Morris RI Muller S Pruijn GJ van Venrooij WJ Smolen JS Brown PO Steinman L Utz PJ Autoantigen microarrays for multiplex characterization of autoantibody responses Nat Med 2002, 8:295-301 10.1038/nm0302-295 11875502
47. Balboni I Chan SM Kattah M Tenenbaum JD Butte AJ Utz PJ Multiplexed protein array platforms for analysis of autoimmune diseases Annu Rev Immunol 2006, 24:391-418 10.1146/annurev.immunol.24.021605.090709 16551254
48. Bekeredjian-Ding IB Wagner M Hornung V Giese T Schnurr M Endres S Hartmann G Plasmacytoid dendritic cells control TLR7 sensitivity of naive B cells via type I IFN J Immunol 2005, 174:4043-4050 15778362
49. Hanada T Yoshida H Kato S Tanaka K Masutani K Tsukada J Nomura Y Mimata H Kubo M Yoshimura A Suppressor of cytokine signaling-1 is essential for suppressing dendritic cell activation and systemic autoimmunity Immunity 2003, 19:437-450 10.1016/S1074-7613(03)00240-1 14499118
50. Lu Q Lemke G Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family Science 2001, 293:306-311 10.1126/ science.1061663 11452127
51. Lee PY Weinstein JS Nacionales DC Scumpia PO Li Y Butfiloski E van Rooijen N Moldawer L Satoh M Reeves WH A novel type I IFN-producing cell subset in murine lupus J Immunol 2008, 180:5101-5108 18354236
52. Hua J Kirou K Lee C Crow MK Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies Arthritis Rheum 2006, 54:1906-1916 10.1002/art.21890 16736505
53. Bennett L Palucka AK Arce E Cantrell V Borvak J Banchereau J Pascual V Interferon and granulopoiesis signatures in systemic lupus erythematosus blood J Exp Med 2003, 197:711-723 2193846 12642603 10.1084/jem.20021553
54. Baechler EC Batliwalla FM Karypis G Gaffney PM Ortmann WA Espe KJ Shark KB Grande WJ Hughes KM Kapur V Gregersen PK Behrens TW Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus Proc Natl Acad Sci USA 2003, 100:2610-2615 151388 12604793 10.1073/pnas.0337679100
55. Tan EM Antinuclear antibodies: Diagnostic markers for autoimmune diseases and probes for cell biology Adv Immunol 1989, 44:93-151 10.1016/ S0065-2776(08)60641-0 2646863
56. Yoshida H Satoh M Behney KM Lee CG Richards HB Shaheen VM Yang JQ Singh RR Reeves WH Effect of an exogenous trigger on the pathogenesis of lupus in (NZB × NZW)F1 mice Arthritis Rheum 2002, 46:2235-2244 2291543 12209530 10.1002/art.10441
57. Gaipl US Voll RE Sheriff A Franz S Kalden JR Herrmann M Impaired clearance of dying cells in systemic lupus erythematosus Autoimmun Rev 2005, 4:189-194 10.1016/j.autrev.2004.10.007 15893710