The NLRP12 Sensor Negatively Regulates Autoinflammatory Disease by Modulating Interleukin-4 Production in T Cells

Immunity

Volumn 42, Issue 4, 2015, Pages 654-664

  Lukens, John R ^a,b   Gurung, Prajwal ^a   Shaw, Patrick J ^a   Barr, Maggie J ^a   Zaki, Md Hasan ^c   Brown, Scott A ^a   Vogel, Peter ^a   Chi, Hongbo ^a   Kanneganti, Thirumala Devi ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR 12; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; NLRP12 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; ATAXIA; ATOPIC DERMATITIS; AUTOINFLAMMATORY DISEASE; BONE MARROW CELL; CELL DEATH; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; DISEASE EXACERBATION; DNA SYNTHESIS; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FLOW CYTOMETRY; GENE DELETION; IMMUNIZATION; INFLAMMATORY CELL; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PARALYSIS; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH2 CELL; THYMOCYTE; ANIMAL; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ATAXIA; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; COLITIS; DENDRITIC CELLS; DERMATITIS, ATOPIC; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE EXPRESSION REGULATION; IMMUNITY, CELLULAR; INTERLEUKIN-4; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MICE; MICE, KNOCKOUT; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84928196080     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.03.006     Document Type: Article

References (47)

1. Allen I.C., Wilson J.E., Schneider M., Lich J.D., Roberts R.A., Arthur J.C., Woodford R.M., Davis B.K., Uronis J.M., Herfarth H.H., et al. NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-κB signaling. Immunity 2012, 36:742-754.
2. Anand P.K., Malireddi R.K., Lukens J.R., Vogel P., Bertin J., Lamkanfi M., Kanneganti T.D. NLRP6 negatively regulates innate immunity and host defence against bacterial pathogens. Nature 2012, 488:389-393.
3. Bettelli E., Das M.P., Howard E.D., Weiner H.L., Sobel R.A., Kuchroo V.K. IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J.Immunol. 1998, 161:3299-3306.
4. Boirivant M., Fuss I.J., Chu A., Strober W. Oxazolone colitis: a murine model of T helper cell type 2 colitis treatable with antibodies to interleukin 4. J.Exp. Med. 1998, 188:1929-1939.
5. Borghini S., Tassi S., Chiesa S., Caroli F., Carta S., Caorsi R., Fiore M., Delfino L., Lasigliè D., Ferraris C., et al. Clinical presentation and pathogenesis of cold-induced autoinflammatory disease in a family with recurrence of an NLRP12 mutation. Arthritis Rheum. 2011, 63:830-839.
6. Chen G.Y., Liu M., Wang F., Bertin J., Núñez G. A functional role for Nlrp6 in intestinal inflammation and tumorigenesis. J.Immunol. 2011, 186:7187-7194.
7. Cho J.H. The genetics and immunopathogenesis of inflammatory bowel disease. Nat. Rev. Immunol. 2008, 8:458-466.
8. Davenport C.M., McAdams H.A., Kou J., Mascioli K., Eichman C., Healy L., Peterson J., Murphy S., Coppola D., Truneh A. Inhibition of pro-inflammatory cytokine generation by CTLA4-Ig in the skin and colon of mice adoptively transplanted with CD45RBhi CD4+ Tcells correlates with suppression of psoriasis and colitis. Int. Immunopharmacol. 2002, 2:653-672.
9. Delgoffe G.M., Pollizzi K.N., Waickman A.T., Heikamp E., Meyers D.J., Horton M.R., Xiao B., Worley P.F., Powell J.D. The kinase mTOR regulates the differentiation of helper Tcells through the selective activation of signaling by mTORC1 and mTORC2. Nat. Immunol. 2011, 12:295-303.
10. Elinav E., Strowig T., Kau A.L., Henao-Mejia J., Thaiss C.A., Booth C.J., Peaper D.R., Bertin J., Eisenbarth S.C., Gordon J.I., Flavell R.A. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011, 145:745-757.
11. Falcone M., Rajan A.J., Bloom B.R., Brosnan C.F. A critical role for IL-4 in regulating disease severity in experimental allergic encephalomyelitis as demonstrated in IL-4-deficient C57BL/6 mice and BALB/c mice. J.Immunol. 1998, 160:4822-4830.
12. Fort M., Lesley R., Davidson N., Menon S., Brombacher F., Leach M., Rennick D. IL-4 exacerbates disease in a Th1 cell transfer model of colitis. J.Immunol. 2001, 166:2793-2800.
13. Furlan R., Poliani P.L., Galbiati F., Bergami A., Grimaldi L.M., Comi G., Adorini L., Martino G. Central nervous system delivery of interleukin 4 by a nonreplicative herpes simplex type 1 viral vector ameliorates autoimmune demyelination. Hum. Gene Ther. 1998, 9:2605-2617.
14. Fuss I.J., Neurath M., Boirivant M., Klein J.S., de la Motte C., Strong S.A., Fiocchi C., Strober W. Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J.Immunol. 1996, 157:1261-1270.
15. Goverman J. Autoimmune Tcell responses in the central nervous system. Nat. Rev. Immunol. 2009, 9:393-407.
16. Hedegaard C.J., Krakauer M., Bendtzen K., Lund H., Sellebjerg F., Nielsen C.H. T helper cell type 1 (Th1), Th2 and Th17 responses to myelin basic protein and disease activity in multiple sclerosis. Immunology 2008, 125:161-169.
17. Heller F., Fuss I.J., Nieuwenhuis E.E., Blumberg R.S., Strober W. Oxazolone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells. Immunity 2002, 17:629-638.
18. Hohnoki K., Inoue A., Koh C.S. Elevated serum levels of IFN-gamma, IL-4 and TNF-alpha/unelevated serum levels of IL-10 in patients with demyelinating diseases during the acute stage. J.Neuroimmunol. 1998, 87:27-32.
19. Jéru I., Duquesnoy P., Fernandes-Alnemri T., Cochet E., Yu J.W., Lackmy-Port-Lis M., Grimprel E., Landman-Parker J., Hentgen V., Marlin S., et al. Mutations in NALP12 cause hereditary periodic fever syndromes. Proc. Natl. Acad. Sci. USA 2008, 105:1614-1619.
20. Jéru I., Le Borgne G., Cochet E., Hayrapetyan H., Duquesnoy P., Grateau G., Morali A., Sarkisian T., Amselem S. Identification and functional consequences of a recurrent NLRP12 missense mutation in periodic fever syndromes. Arthritis Rheum. 2011, 63:1459-1464.
21. Kanneganti T.D. Central roles of NLRs and inflammasomes in viral infection. Nat. Rev. Immunol. 2010, 10:688-698.
22. Kanneganti T.D., Dixit V.D. Immunological complications of obesity. Nat. Immunol. 2012, 13:707-712.
23. Kanneganti T.D., Lamkanfi M., Núñez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007, 27:549-559.
24. Kroenke M.A., Chensue S.W., Segal B.M. EAE mediated by a non-IFN-γ/non-IL-17 pathway. Eur. J. Immunol. 2010, 40:2340-2348.
25. Lamkanfi M., Vande Walle L., Kanneganti T.D. Deregulated inflammasome signaling in disease. Immunol. Rev. 2011, 243:163-173.
26. Lei Y., Wen H., Yu Y., Taxman D.J., Zhang L., Widman D.G., Swanson K.V., Wen K.W., Damania B., Moore C.B., et al. The mitochondrial proteins NLRX1 and TUFM form a complex that regulates type I interferon and autophagy. Immunity 2012, 36:933-946.
27. Leon F., Contractor N., Fuss I., Marth T., Lahey E., Iwaki S., la Sala A., Hoffmann V., Strober W., Kelsall B.L. Antibodies to complement receptor 3 treat established inflammation in murine models of colitis and a novel model of psoriasiform dermatitis. J.Immunol. 2006, 177:6974-6982.
28. Lich J.D., Williams K.L., Moore C.B., Arthur J.C., Davis B.K., Taxman D.J., Ting J.P. Monarch-1 suppresses non-canonical NF-kappaB activation and p52-dependent chemokine expression in monocytes. J.Immunol. 2007, 178:1256-1260.
29. Link J., Söderström M., Olsson T., Höjeberg B., Ljungdahl A., Link H. Increased transforming growth factor-beta, interleukin-4, and interferon-gamma in multiple sclerosis. Ann. Neurol. 1994, 36:379-386.
30. Lukens J.R., Dixit V.D., Kanneganti T.D. Inflammasome activation in obesity-related inflammatory diseases and autoimmunity. Discov. Med. 2011, 12:65-74.
31. Lukens J.R., Gross J.M., Kanneganti T.D. IL-1 family cytokines trigger sterile inflammatory disease. Front. Immunol. 2012, 3:315.
32. Macaluso F., Nothnagel M., Parwez Q., Petrasch-Parwez E., Bechara F.G., Epplen J.T., Hoffjan S. Polymorphisms in NACHT-LRR (NLR) genes in atopic dermatitis. Exp. Dermatol. 2007, 16:692-698.
33. Mizoguchi A., Mizoguchi E., Bhan A.K. The critical role of interleukin 4 but not interferon gamma in the pathogenesis of colitis in T-cell receptor alpha mutant mice. Gastroenterology 1999, 116:320-326.
34. Normand S., Delanoye-Crespin A., Bressenot A., Huot L., Grandjean T., Peyrin-Biroulet L., Lemoine Y., Hot D., Chamaillard M. Nod-like receptor pyrin domain-containing protein 6 (NLRP6) controls epithelial self-renewal and colorectal carcinogenesis upon injury. Proc. Natl. Acad. Sci. USA 2011, 108:9601-9606.
35. Ponomarev E.D., Maresz K., Tan Y., Dittel B.N. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J.Neurosci. 2007, 27:10714-10721.
36. Schön M.P., Detmar M., Parker C.M. Murine psoriasis-like disorder induced by naive CD4+ Tcells. Nat. Med. 1997, 3:183-188.
37. Shaw M.K., Lorens J.B., Dhawan A., DalCanto R., Tse H.Y., Tran A.B., Bonpane C., Eswaran S.L., Brocke S., Sarvetnick N., et al. Local delivery of interleukin 4 by retrovirus-transduced T lymphocytes ameliorates experimental autoimmune encephalomyelitis. J.Exp. Med. 1997, 185:1711-1714.
38. Shaw P.J., McDermott M.F., Kanneganti T.D. Inflammasomes and autoimmunity. Trends Mol. Med. 2011, 17:57-64.
39. Strober W., Murray P.J., Kitani A., Watanabe T. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 2006, 6:9-20.
40. Stromnes I.M., Cerretti L.M., Liggitt D., Harris R.A., Goverman J.M. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 2008, 14:337-342.
41. Strowig T., Henao-Mejia J., Elinav E., Flavell R. Inflammasomes in health and disease. Nature 2012, 481:278-286.
42. Vladimer G.I., Weng D., Paquette S.W., Vanaja S.K., Rathinam V.A., Aune M.H., Conlon J.E., Burbage J.J., Proulx M.K., Liu Q., et al. The NLRP12 inflammasome recognizes Yersinia pestis. Immunity 2012, 37:96-107.
43. Wensky A., Marcondes M.C., Lafaille J.J. The role of IFN-gamma in the production of Th2 subpopulations: implications for variable Th2-mediated pathologies in autoimmunity. J.Immunol. 2001, 167:3074-3081.
44. Williams K.L., Lich J.D., Duncan J.A., Reed W., Rallabhandi P., Moore C., Kurtz S., Coffield V.M., Accavitti-Loper M.A., Su L., et al. The CATERPILLER protein monarch-1 is an antagonist of toll-like receptor-, tumor necrosis factor alpha-, and Mycobacterium tuberculosis-induced pro-inflammatory signals. J.Biol. Chem. 2005, 280:39914-39924.
45. Xia X., Cui J., Wang H.Y., Zhu L., Matsueda S., Wang Q., Yang X., Hong J., Songyang Z., Chen Z.J., Wang R.F. NLRX1 negatively regulates TLR-induced NF-κB signaling by targeting TRAF6 and IKK. Immunity 2011, 34:843-853.
46. Zaki M.H., Vogel P., Malireddi R.K., Body-Malapel M., Anand P.K., Bertin J., Green D.R., Lamkanfi M., Kanneganti T.D. The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell 2011, 20:649-660.
47. Zaki M.H., Man S.M., Vogel P., Lamkanfi M., Kanneganti T.D. Salmonella exploits NLRP12-dependent innate immune signaling to suppress host defenses during infection. Proc. Natl. Acad. Sci. USA 2014, 111:385-390.