IL-10 in humans: Lessons from the Gut, IL-10/IL-10 receptor deficiencies, and IL-10 polymorphisms

Current Topics in Microbiology and Immunology

Volumn 380, Issue , 2014, Pages 1-18

  Engelhardt, Karin R ^a   Grimbacher, Bodo ^a  

^a Molecular Epidemiology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; AZATHIOPRINE; CORTICOSTEROID; METHOTREXATE; THALIDOMIDE; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

3' UNTRANSLATED REGION; ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL LINEAGE; CLINICAL FEATURE; CROHN DISEASE; DISEASE SEVERITY; DOWN REGULATION; GENOTYPE PHENOTYPE CORRELATION; HAPLOTYPE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HETEROZYGOSITY; HOMEOSTASIS; HOMOZYGOSITY; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; MACROPHAGE; MISSENSE MUTATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN PHOSPHORYLATION; PROTEIN POLYMORPHISM; PROTEIN SECRETION; QUALITY OF LIFE; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE; ULCERATIVE COLITIS; ADOLESCENCE; ADULTHOOD; ANUS FISTULA; ARTHRITIS; BLOODY DIARRHEA; COLON; COMMENSAL; DISEASE COURSE; ENTEROCOLITIS; ENVIRONMENTAL FACTOR; FAILURE TO THRIVE; FOLLICULITIS; GENETIC ASSOCIATION; GRANULOMA; HEREDITY; IMMUNE DEFICIENCY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; INTERLEUKIN 10 DEFICIENCY; INTERLEUKIN 10 RECEPTOR DEFICIENCY; INTESTINE FLORA; LOSS OF FUNCTION MUTATION; PERIANAL ABSCESS; RECURRENT FEVER; RESPIRATORY TRACT INFECTION; SMALL INTESTINE; ULCER;

ANIMALS; GASTROINTESTINAL TRACT; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; POLYMORPHISM, GENETIC; RECEPTORS, INTERLEUKIN-10;

EID: 84958539762     PISSN: 0070217X     EISSN: 21969965     Source Type: Book Series    
DOI: 10.1007/978-3-662-43492-5_1     Document Type: Article

References (83)

1. Abraham C, Cho JH (2009) Inflammatory bowel disease. N Engl J Med 361:2066-2078. doi:10. 1056/NEJMra0804647
2. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915-1920
3. Barnes MJ, Powrie F (2009) Regulatory T cells reinforce intestinal homeostasis. Immunity 31:401-411. doi:10.1016/j.immuni.2009.08.011
4. Barrett JC, Hansoul S, Nicolae DL, Cho JH, Duerr RH, Rioux JD et al (2008) Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 40:955-962. doi:10.1038/ng.175
5. Baumgart DC, Carding SR (2007) Inflammatory bowel disease: cause and immunobiology. Lancet 369:1627-1640
6. Begue B, Verdier J, Rieux-Laucat F, Goulet O, Morali A, Canioni D et al (2011) Defective IL-10 signaling defining a subgroup of patients with inflammatory bowel disease. Am J Gastroenterol 106:1544-1555. doi:10.1038/ajg.2011.112
7. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP et al (2006) A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol 4:754-759
8. Chaudhry A, Samstein RM, Treuting P, Liang Y, Pils MC, Heinrich JM et al (2011) Interleukin-10 signaling in regulatory T cells is required for suppression of th17 cell-mediated inflammation. Immunity 34:566-578. doi:10.1016/j.immuni.2011.03.018
9. Cheng LE, Kanwar B, Tcheurekdjian H, Grenert JP, Muskat M, Heyman MB et al (2009) Persistent systemic inflammation and atypical enterocolitis in patients with NEMO syndrome. Clin Immunol 132:124-131. doi:10.1016/j.clim.2009. 03.514
10. Cho JH (2008) The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol 8:458-466. doi:10.1038/nri2340
11. Commins S, Steinke JW, Borish L (2008) The extended IL-10 superfamily: IL-10, IL-19, IL-20, IL-22, IL-24, IL-26, IL-28, and IL-29. J Allergy Clin Immunol 121:1108-1111. doi:10.1016/j.jaci.2008.02.026
12. Donnelly RP, Dickensheets H, Finbloom DS (1999) The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 19:563-573
13. Donnelly RP, Sheikh F, Kotenko SV, Dickensheets H (2004) The expanded family of class II cytokines that share the IL-10 receptor-2 (IL-10R2) chain. J Leukoc Biol 76:314-321
14. Elson CO, Cong Y, McCracken VJ, Dimmitt RA, Lorenz RG, Weaver CT (2005) Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev 206:60-76
15. Elson CO, Cong Y, Weaver CT, Schoeb TR, McClanahan TK, Fick RB, Kastelein RA (2007) Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice. Gastroenterology 132:2359-2370
16. Engel MA, Neurath MF (2010) New pathophysiological insights and modern treatment of IBD. J Gastroenterol 45:571-583. doi:10.1007/s00535-010-0219-3
17. Engelhardt KR, Shah N, Faizura-Yeop I, Kocacik Uygun DF, Frede N, Muise AM et al (2013) Clinical outcome in IL-10- and IL-10 receptor-deficient patients with or without hematopoietic stem cell transplantation. J Allergy Clin Immunol 131:825-830. doi:10.1016/j.jaci.2012.09.025
18. Fava F, Danese S (2011) Intestinal microbiota in inflammatory bowel disease: friend or foe? World J Gastroenterol 17:557-566. doi:10.3748/wjg.v17. i5.557
19. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A (1991a) IL-10 inhibits cytokine production by activated macrophages. J Immunol 147:3815-3822
20. Fiorentino DF, Zlotnik A, Vieira P, Mosmann TR, Howard M, Moore KW, O'Garra A (1991b) IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol 146:3444-3451
21. Franke A, Balschun T, Karlsen TH, Hedderich J, May S, Lu T et al (2008a) Replication of signals from recent studies of Crohn's disease identifies previously unknown disease loci for ulcerative colitis. Nat Genet 40:713-715. doi:10.1038/ng.(a)
22. Franke A, Balschun T, Karlsen TH, Sventoraityte J, Nikolaus S, Mayr G et al (2008b) Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat Genet 40:1319-1323. doi:10.1038/ng.221.(b)
23. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T et al (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 42:1118-1125. doi:10.1038/ng.717
24. Glocker EO, Kotlarz D, Boztug K, Gertz EM, Schäffer AA, Noyan F et al (2009) Inflammatory bowel disease and mutations affecting the Interleukin-10 Receptor. N Engl J Med 361: 2033-2045. doi:10.1056/NEJMoa0907206
25. Glocker EO, Frede N, Perro M, Sebire N, Elawad M, Shah N et al (2010) Infant colitis - it's in the genes. Lancet 376:1272. doi:10.1016/S0140-6736(10) 61008-2
26. Goyette P, Labbé C, Trinh TT, Xavier RJ, Rioux JD (2007) Molecular pathogenesis of inflammatory bowel disease: genotypes, phenotypes and personalized medicine. Ann Med 39:177-199
27. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, Huse K et al (2007) A genome-wide association scan of non-synonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 39:207-211
28. Holland SM, DeLeo FR, Elloumi HZ, Hsu AP, Uzel G, Brodsky N et al (2007) STAT3 mutations in the hyper-IgE syndrome. N Engl J Med 357:1608-1619
29. Huber S, Gagliani N, Esplugues E, O'Connor W Jr, Huber FJ, Chaudhry A et al (2011) Th17 cells express interleukin-10 receptor and are controlled by Foxp3(-) and Foxp3(+) regulatory CD4(+) T cells in an interleukin-10-dependent manner. Immunity 34:554-565. doi:10.1016/j.immuni.2011.01.020
30. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cézard JP, Belaiche J et al (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411:599-603
31. Imielinski M, Baldassano RN, Griffiths A, Russell RK, Annese V, Dubinsky M et al (2009) Common variants at five new loci associated with early-onset inflammatory bowel disease. Nat Genet 41:1335-1340. doi:10.1038/ng.489
32. Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA et al (2007) Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 204:105-115
33. Izcue A, Coombes JL, Powrie F (2006) Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol Rev 212:256-271
34. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY et al (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491:119-124. doi:10.1038/nature11582
35. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H et al (2008) XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134:743-756. doi:10.1016/j.cell.2008.07. 021
36. Kaser A, Flak MB, Tomczak MF, Blumberg RS (2011) The unfolded protein response and its role in intestinal homeostasis and inflammation. Exp Cell Res 317:2772-2779. doi:10.1016/j.yexcr.2011.07.008
37. Kotenko SV, Krause CD, Izotova LS, Pollack BP, Wu W, Pestka S (1997) Identification and functional characterization of a second chain of the interleukin-10 receptor complex. EMBO J 16:5894-5903
38. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK et al (2003) IFNlambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4:69-77
39. Kotlarz D, Beier R, Murugan D, Diestelhorst J, Jensen O, Boztug K et al (2012) Loss of interleukin- 10 signaling and infantile inflammatory bowel disease - implications for diagnosis and therapy. Gastroenterology 143:347-355. doi:10.1053/j.gastro.2012.04.045
40. Kühn R, Löhler J, Rennick D, Rajewsky K, Müller W (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263-274
41. Levine A, Griffiths A, Markowitz J, Wilson DC, Turner D, Russell RK et al (2011) Pediatric modification of the Montreal classification for inflammatory bowel disease: the Paris classification. Inflamm Bowel Dis 17:1314-1321. doi:10.1002/ibd.21493
42. Liu Y, Wei SH, Ho AS, de Waal R, Malefyt, Moore KW (1994) Expression cloning and characterization of a human IL-10 receptor. J Immunol 152:1821-1829
43. Makita S, Kanai T, Oshima S, Uraushihara K, Totsuka T, Sawada T et al (2004) CD4 + CD25bright T cells in human intestinal lamina propria as regulatory cells. J Immunol 173:3119-3130
44. Mao H, Yang W, Lee PP, Ho MH, Yang J, Zeng S et al (2012) Exome sequencing identifies novel compound heterozygous mutations of IL-10 receptor 1 in neonatal-onset Crohn's disease. Genes Immun 13:437-442. doi:10.1038/gene. 2012.8
45. Marks DJ, Segal AW (2008) Innate immunity in inflammatory bowel disease: a disease hypothesis. J Pathol 214:260-266
46. Marks DJ, Miyagi K, Rahman FZ, Novelli M, Bloom SL, Segal AW (2009) Inflammatory bowel disease in CGD reproduces the clinicopathological features of Crohn's disease. Am J Gastroenterol 104:117-124. doi:10.1038/ajg.2008.72
47. Maxwell JR, Viney JL (2009) Overview of mouse models of inflammatory bowel disease and their use in drug discovery. Curr Protoc Pharmacol Chapter 5: Unit5.57. doi: 10.1002/0471141755.ph0557s47
48. Maynard CL, Harrington LE, Janowski KM, Oliver JR, Zindl CL, Rudensky AY, Weaver CT (2007) Regulatory T cells expressing interleukin 10 develop from Foxp3 + and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol 8:931-941
49. Mizoguchi A, Mizoguchi E (2008) Inflammatory bowel disease, past, present, and future: lessons from animal models. J Gastroenterol 43:1-17. doi:10.1007/s00535-007-2111-3
50. Moore KW, O'Garra A, de Waal Malefyt R, Vieira P, Mosmann TR (1993) Interleukin-10. Annu Rev Immunol 11:165-90
51. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A (2001) Interleukin-10 and the interleukin- 10 receptor. Annu Rev Immunol 19:683-765
52. Moraes-Vasconcelos D, Costa-Carvalho BT, Torgerson TR, Ochs HD (2008) Primary immune deficiency disorders presenting as autoimmune diseases: IPEX and APECED. J Clin Immunol 28(Suppl 1):S11-S19. doi:10.1007/s10875-008-9176-5
53. Moran CJ, Walters TD, Guo CH, Kugathasan S, Klein C, Turner D et al (2013) IL10R polymorphisms are associated with very-early-onset ulcerative colitis. Inflamm Bowel Dis 19:115-123
54. Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H et al (2009) Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 10:1178-1184. doi:10.1038/ni.1791
55. Neirynck S, Steidler L (2006) Delivery of therapeutic proteins through Lactococcus lactis. Biotechnol Genet Eng Rev 22:253-266
56. Neufert C, Pickert G, Zheng Y, Wittkopf N, Warntjen M, Nikolaev A et al (2010) Activation of epithelial STAT3 regulates intestinal homeostasis. Cell Cycle 9:652-655
57. Neuman MG, Nanau RM (2012) Inflammatory bowel disease: role of diet, microbiota, life style. Transl Res 160:29-44. doi:10.1016/j.trsl.2011.09.001
58. Ng SC, Woodrow S, Patel N, Subhani J, Harbord M (2012) Role of genetic and environmental factors in British twins with inflammatory bowel disease. Inflamm Bowel Dis 18:725-736. doi:10.1002/ibd.21747
59. O'Garra A, Murphy KM (2009) From IL-10 to IL-12: how pathogens and their products stimulate APCs to induce T(H)1 development. Nat Immunol 10(9):929-932. doi:10.1038/ni0909-929
60. Pachlopnik Schmid J, Canioni D, Moshous D, Touzot F, Mahlaoui N, Hauck F et al (2011) Clinical similarities and differences of patients with X-linked lymphoproliferative syndrome type 1 (XLP-1/SAP deficiency) vs type 2 (XLP-2/XIAP deficiency). Blood 117:1522-1529. doi:10.1182/blood-2010-07-298372
61. Parkes M, Barrett JC, Prescott NJ, Tremelling M, Anderson CA, Fisher SA et al(2007) Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat Genet 39:830-832
62. Pestka S, Krause CD, Sarkar D, Walter MR, Shi Y, Fisher PB (2004) Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 22:929-979
63. Podolsky DK (2002) Inflammatory bowel disease. N Engl J Med 347:417-429
64. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, Huett A et al (2007) Genomewide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 39:596-604
65. Sanchez R, Levy E, Costea F, Sinnett D (2009) IL-10 and TNF-alpha promoter haplotypes are associated with childhood Crohn's disease location. World J Gastroenterol 15:3776-3782
66. Satsangi J, Jewell DP, Rosenberg WM, Bell JI (1994) Genetics of inflammatory bowel disease. Gut 35:696-700
67. Sawczenko A, Sandhu BK (2003) Presenting features of inflammatory bowel disease in Great Britain and Ireland. Arch Dis Child 88:995-1000
68. Segal BH, Veys P, Malech H, Cowan MJ (2011) Chronic granulomatous disease: lessons from a rare disorder. Biol Blood Marrow Transplant 17(1 Suppl):S123-S131. doi:10.1016/j.bbmt.2010.09.008
69. Spencer SD, Di Marco F, Hooley J, Pitts-Meek S, Bauer M, Ryan AM et al (1998) The orphan receptor CRF2-4 is an essential subunit of the interleukin 10 receptor. J Exp Med 187:571-578
70. Stoll M, Corneliussen B, Costello CM, Waetzig GH, Mellgard B, Koch WA et al (2004) Genetic variation in DLG5 is associated with inflammatory bowel disease. Nat Genet 36:476-480
71. Taupin D, Podolsky DK (2003) Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 4:721-732
72. Thrasher AJ, Burns SO (2010) WASP: a key immunological multitasker. Nat Rev Immunol 10:182-192. doi:10.1038/nri2724
73. Torgerson TR, Ochs HD (2007) Immune dysregulation, polyendocrinopathy, enteropathy, X-linked: forkhead box protein 3 mutations and lack of regulatory T cells. J Allergy Clin Immunol 120:744-750
74. Turner JR (2006) Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 169:1901-1909
75. Uhlig HH, Powrie F (2005) The role of mucosal T lymphocytes in regulating intestinal inflammation. Springer Semin Immunopathol 27:167-180
76. Van Limbergen J, Wilson DC, Satsangi J (2009) The genetics of Crohn's disease. Annu Rev Genomics Hum Genet 10:89-116. doi:10.1146/annurev-genom- 082908-150013
77. Weber-Nordt RM, Riley JK, Greenlund AC, Moore KW, Darnell JE, Schreiber RD (1996) Stat3 recruitment by two distinct ligand-induced, tyrosine- phosphorylated docking sites in the interleukin-10 receptor intracellular domain. J Biol Chem 271:27954-27961
78. Williams L, Bradley L, Smith A, Foxwell B (2004) Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J Immunol 172:567-576
79. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R (2004) IL-22 increases the innate immunity of tissues. Immunity 21:241-254
80. Wolk K, Witte E, Wallace E, Döcke WD, Kunz S, Asadullah K et al (2006) IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis. Eur J Immunol 36:1309-1323
81. Xavier RJ, Podolsky DK (2007) Unraveling the pathogenesis of inflammatory bowel disease. Nature 448:427-434
82. Yong PF, Freeman AF, Engelhardt KR, Holland S, Puck JM, Grimbacher B (2012) An update on the hyper-IgE syndromes. Arthritis Res Ther 14:228
83. Zaki MH, Lamkanfi M, Kanneganti TD (2011) The Nlrp3 inflammasome: contributions to intestinal homeostasis. Trends Immunol 32:171-179. doi:10.1016/j.it.2011.02.002