Interleukin-22 and CD160 play additive roles in the host mucosal response to Clostridium difficile infection in mice

Immunology

Volumn 144, Issue 4, 2015, Pages 587-597

  Sadighi Akha, Amir A ^a   Mcdermott, Andrew J ^a   Theriot, Casey M ^a   Carlson, Paul E ^a   Frank, Charles R ^a   Mcdonald, Roderic ^a   Falkowski, Nicole R ^a   Bergin, Ingrid L ^a   Young, Vincent B ^a   Huffnagle, Gary B ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

CD160; Clostridium difficile; Interleukin 22; PSTAT3; RegIII

Indexed keywords

ANTIBIOTIC AGENT; CARBON TETRACHLORIDE; CCAAT ENHANCER BINDING PROTEIN DELTA; CD 160 ANTIBODY; CEPHOPERAZONE; CXCL2 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GAMMA INTERFERON RECEPTOR 1; INTERLEUKIN 22 ANTIBODY; MESSENGER RNA; PROTEIN ANTIBODY; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; STAT3 PROTEIN; UNCLASSIFIED DRUG; ANTIBODY; ANTIINFECTIVE AGENT; CD160 PROTEIN, MOUSE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; LEUKOCYTE ANTIGEN; STAT3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; CLOSTRIDIUM DIFFICILE INFECTION; COMPARATIVE STUDY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNE RESPONSE; LIMIT OF DETECTION; LIMIT OF QUANTITATION; MALE; MOUSE; MUCOSAL IMMUNITY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE; SURVIVAL FACTOR; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; ENTEROCOLITIS, PSEUDOMEMBRANOUS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PEPTOCLOSTRIDIUM DIFFICILE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME FACTOR;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBODIES; ANTIGENS, CD; CLOSTRIDIUM DIFFICILE; DISEASE MODELS, ANIMAL; ENTEROCOLITIS, PSEUDOMEMBRANOUS; GENE EXPRESSION REGULATION; GPI-LINKED PROTEINS; IMMUNITY, MUCOSAL; INTERLEUKINS; INTESTINAL MUCOSA; MALE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; PHOSPHORYLATION; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS;

EID: 84924390107     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12414     Document Type: Article

References (56)

1. Hall I, O'Toole E. Intestinal flora in newborn infants with description of a new pathogenic anaerobe. Am J Dis Child 1935; 49:390-402.
2. Kelly CP, LaMont JT. Clostridium difficile infection. Annu Rev Med 1998; 49:375-90.
3. Rupnik M, Wilcox MH, Gerding DN. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 2009; 7:526-36.
4. Britton RA, Young VB. Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol 2012; 20:313-9.
5. Eyre DW, Cule ML, Wilson DJ et al. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 2013; 369:1195-205.
6. Just I, Selzer J, von Eichel-Streiber C, Aktories K. The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile. J Clin Invest 1995; 95:1026-31.
7. Just I, Selzer J, Wilm M, von Eichel-Streiber C, Mann M, Aktories K. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 1995; 375:500-3.
8. Hecht G, Pothoulakis C, LaMont JT, Madara JL. Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers. J Clin Invest 1988; 82:1516-24.
9. Hecht G, Koutsouris A, Pothoulakis C, LaMont JT, Madara JL. Clostridium difficile toxin B disrupts the barrier function of T84 monolayers. Gastroenterology 1992; 102:416-23.
10. Pothoulakis C, Lamont JT. Microbes and microbial toxins: paradigms for microbial-mucosal interactions II. The integrated response of the intestine to Clostridium difficile toxins. Am J Physiol Gastrointest Liver Physiol 2001; 280:G178-83.
11. Johnson S, Gerding DN. Clostridium difficile-associated diarrhea. Clin Infect Dis 1998; 26:1027-34; quiz 35-6.
12. Lawley TD, Clare S, Walker AW et al. Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun 2009; 77:3661-9.
13. Ryan A, Lynch M, Smith SM et al. A role for TLR4 in Clostridium difficile infection and the recognition of surface layer proteins. PLoS Pathog 2011; 7:e1002076.
14. Hasegawa M, Yamazaki T, Kamada N, Tawaratsumida K, Kim YG, Nunez G, Inohara N. Nucleotide-binding oligomerization domain 1 mediates recognition of Clostridium difficile and induces neutrophil recruitment and protection against the pathogen. J Immunol 2011; 186:4872-80.
15. Hasegawa M, Kamada N, Jiao Y, Liu MZ, Nunez G, Inohara N. Protective role of commensals against Clostridium difficile infection via an IL-1β-mediated positive-feedback loop. J Immunol 2012; 189:3085-91.
16. Jarchum I, Liu M, Lipuma L, Pamer EG. Toll-like receptor 5 stimulation protects mice from acute Clostridium difficile colitis. Infect Immun 2011; 79:1498-503.
17. Jarchum I, Liu M, Shi C, Equinda M, Pamer EG. Critical role for MyD88-mediated neutrophil recruitment during C. difficile colitis. Infect Immun 2012; 80:2989-96.
18. Sadighi Akha AA, Theriot CM, Erb-Downward JR et al. Acute infection of mice with Clostridium difficile leads to eIF2α phosphorylation and pro-survival signalling as part of the mucosal inflammatory response. Immunology 2013; 140:111-22.
19. Montgomery RI, Warner MS, Lum BJ, Spear PG. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 1996; 87:427-36.
20. Anderson CA, Boucher G, Lees CW et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 2011; 43:246-52.
21. Steinberg MW, Turovskaya O, Shaikh RB et al. A crucial role for HVEM and BTLA in preventing intestinal inflammation. J Exp Med 2008; 205:1463-76.
22. Schaer C, Hiltbrunner S, Ernst B, Mueller C, Kurrer M, Kopf M, Harris NL. HVEM signalling promotes colitis. PLoS ONE 2011; 6:e18495.
23. Whitbeck JC, Peng C, Lou H et al. Glycoprotein D of herpes simplex virus (HSV) binds directly to HVEM, a member of the tumor necrosis factor receptor superfamily and a mediator of HSV entry. J Virol 1997; 71:6083-93.
24. Mauri DN, Ebner R, Montgomery RI et al. LIGHT, a new member of the TNF superfamily, and lymphotoxin α are ligands for herpesvirus entry mediator. Immunity 1998; 8:21-30.
25. Sedy JR, Gavrieli M, Potter KG et al. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat Immunol 2005; 6:90-8.
26. + T cells through interaction with herpesvirus entry mediator. Nat Immunol 2008; 9:176-85.
27. Cheung TC, Steinberg MW, Oborne LM et al. Unconventional ligand activation of herpesvirus entry mediator signals cell survival. Proc Natl Acad Sci USA 2009; 106:6244-9.
28. + T cells. Nat Immunol 2008; 9:122-4.
29. Cai G, Freeman GJ. The CD160, BTLA, LIGHT/HVEM pathway: a bidirectional switch regulating T-cell activation. Immunol Rev 2009; 229:244-58.
30. Ware CF, Sedy JR. TNF Superfamily Networks: bidirectional and interference pathways of the herpesvirus entry mediator (TNFSF14). Curr Opin Immunol 2011; 23:627-31.
31. Shui JW, Larange A, Kim G, Vela JL, Zahner S, Cheroutre H, Kronenberg M. HVEM signalling at mucosal barriers provides host defence against pathogenic bacteria. Nature 2012; 488:222-5.
32. Perez J, Springthorpe VS, Sattar SA. Clospore: a liquid medium for producing high titers of semi-purified spores of Clostridium difficile. J AOAC Int 2011; 94:618-26.
33. Theriot CM, Koumpouras CC, Carlson PE, Bergin II, Aronoff DM, Young VB. Cefoperazone-treated mice as an experimental platform to assess differential virulence of Clostridium difficile strains. Gut Microbes 2011; 2:326-34.
34. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 2009; 77:2367-75.
35. Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, Young VB. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes 2011; 2:145-58.
36. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3:1101-8.
37. Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB. Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect Immun 2012; 80:3786-94.
38. Sadighi Akha AA, Harper JM, Salmon AB, Schroeder BA, Tyra HM, Rutkowski DT, Miller RA. Heightened induction of proapoptotic signals in response to endoplasmic reticulum stress in primary fibroblasts from a mouse model of longevity. J Biol Chem 2011; 286:30344-51.
39. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3:RESEARCH0034.
40. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001; 98:5116-21.
41. Krzywinski M, Altman N. Points of significance: comparing samples - part II. Nat Methods 2014; 11:355-6.
42. Dumoutier L, de Meester C, Tavernier J, Renauld JC. New activation modus of STAT3: a tyrosine-less region of the interleukin-22 receptor recruits STAT3 by interacting with its coiled-coil domain. J Biol Chem 2009; 284:26377-84.
43. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004; 21:241-54.
44. Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, Fouser LA. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006; 203:2271-9.
45. Zheng Y, Valdez PA, Danilenko DM et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008; 14:282-9.
46. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 2011; 29:71-109.
47. Sonnenberg GF, Fouser LA, Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 2011; 12:383-90.
48. Pickert G, Neufert C, Leppkes M et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med 2009; 206:1465-72.
49. Vaishnava S, Yamamoto M, Severson KM et al. The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 2011; 334:255-8.
50. Franze E, Rizzo A, Caruso R, Pallone F, Monteleone G. Interleukin-25 negatively controls pathogenic responses in the gut. Inflamm Allergy Drug Targets 2011; 10:187-91.
51. Steinberg MW, Cheung TC, Ware CF. The signaling networks of the herpesvirus entry mediator (TNFRSF14) in immune regulation. Immunol Rev 2011; 244:169-87.
52. D'Addio F, Ueno T, Clarkson M et al. CD160Ig fusion protein targets a novel costimulatory pathway and prolongs allograft survival. PLoS ONE 2013; 8:e60391.
53. Maeda M, Carpenito C, Russell RC et al. Murine CD160, Ig-like receptor on NK cells and NKT cells, recognizes classical and nonclassical MHC class I and regulates NK cell activation. J Immunol 2005; 175:4426-32.
54. Park SY, Gupta D, Hurwich R, Kim CH, Dziarski R. Peptidoglycan recognition protein Pglyrp2 protects mice from psoriasis-like skin inflammation by promoting regulatory T cells and limiting Th17 responses. J Immunol 2011; 187:5813-23.
55. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 2013; 13:790-801.
56. Moreno JA, Radford H, Peretti D et al. Sustained translational repression by eIF2α-P mediates prion neurodegeneration. Nature 2012; 485:507-11.