Helicobacter saguini, a novel helicobacter isolated from cotton-top tamarins with ulcerative colitis, has proinflammatory properties and induces typhlocolitis and dysplasia in gnotobiotic IL-10-/- Mice

Infection and Immunity

Volumn 84, Issue 8, 2016, Pages 2307-2316

  Shen, Z ^a   Mannion, A ^a   Whary, M T ^a   Muthupalani, S ^a   Sheh, A ^a   Feng, Y ^a   Gong, G ^b   Vandamme, P ^c   Holcombe, H R ^a   Paster, B J ^d   Fox, J G ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c GHENT UNIVERSITY   (Belgium)

^d FORSYTH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; CATALASE; CEFOPERAZONE; CXCL1 CHEMOKINE; CYTOLETHAL DISTENDING TOXIN; GAMMA INTERFERON; HISTONE H2AX; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; OXIDOREDUCTASE; TUMOR NECROSIS FACTOR ALPHA; UREASE; VANCOMYCIN; AUTACOID; BACTERIUM ANTIBODY; CYTOKINE; HISTONE; RNA 16S;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENOME; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; COTTON TOP TAMARIN; DYSPLASIA; ENZYME LINKED IMMUNOSORBENT ASSAY; GNOTOBIOTICS; HELICOBACTER; HELICOBACTER SAGUINI; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMATE; PRIORITY JOURNAL; ULCERATIVE COLITIS; ANIMAL; CELL LINE; CLASSIFICATION; COLITIS; DEFICIENCY; DISEASE MODEL; FECES; GENE EXPRESSION; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MONKEY DISEASE; PATHOLOGY; PHYLOGENY; PHYSIOLOGY; VETERINARY;

ANIMALS; ANTIBODIES, BACTERIAL; CELL LINE; COLITIS; COLITIS, ULCERATIVE; CYTOKINES; DISEASE MODELS, ANIMAL; FECES; GENE EXPRESSION; GENOME, BACTERIAL; HELICOBACTER; HISTONES; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-10; MICE; MICE, KNOCKOUT; MONKEY DISEASES; PHYLOGENY; RNA, RIBOSOMAL, 16S;

EID: 84979779178     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00235-16     Document Type: Article

References (52)

1. Johnson LD, Ausman LM, Sehgal PK, King NW, Jr. 1996. A prospective study of the epidemiology of colitis and colon cancer in cotton-top tamarins (Saguinus oedipus). Gastroenterology 110:102-115. http://dx.doi.org /10.1053/gast.1996.v110.pm8536845.
2. Wood JD, Peck OC, Tefend KS, Rodriguez MM, Rodriguez MJ, Hernandez CJ, Stonerook MJ, Sharma HM. 1998. Colitis and colon cancer in cotton-top tamarins (Saguinus oedipus oedipus) living wild in their natural habitat. Dig Dis Sci 43:1443-1453. http://dx.doi.org/10 .1023/A:1018842210330.
3. Mansfield KG, Lin KC, Xia D, Newman JV, Schauer DB, MacKey J, Lackner AA, Carville A. 2001. Enteropathogenic Escherichia coli and ulcerative colitis in cotton-top tamarins (Saguinus oedipus). J Infect Dis 184:803-807. http://dx.doi.org/10.1086/322990.
4. Johnson LD, Ausman LM, Rolland RM, Chalifoux LV, Russell RG. 2001. Campylobacter-induced enteritis and diarrhea in captive cotton-top tamarins (Saguinus oedipus) during the first year of life. Comp Med 51: 257-261.
5. Saunders KE, Shen Z, Dewhirst FE, Paster BJ, Dangler CA, Fox JG. 1999. Novel intestinal Helicobacter species isolated from cotton-top tamarins (Saguinus oedipus) with chronic colitis. J Clin Microbiol 37:146-151.
6. Hansen R, Thomson JM, Fox JG, El-Omar EM, Hold GL. 2011. Could Helicobacter organisms cause inflammatory bowel disease? FEMS Immunol Med Microbiol 61:1-14. http://dx.doi.org/10.1111/j.1574-695X.2010 .00744.x.
7. Yu Q, Zhang S, Li L, Xiong L, Chao K, Zhong B, Li Y, Wang H, Chen M. 2015. Enterohepatic Helicobacter species as a potential causative factor in inflammatory bowel disease: a meta-analysis. Medicine 94:e1773. http: //dx.doi.org/10.1097/MD.0000000000001773.
8. + regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 162:691-702. http://dx.doi.org/10.1016/S0002-9440(10)63863-1.
9. Erdman SE, Rao VP, Poutahidis T, Rogers AB, Taylor CL, Jackson EA, Ge Z, Lee CW, Schauer DB, Wogan GN, Tannenbaum SR, Fox JG. 2009. Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc Natl Acad Sci U S A 106:1027-1032. http://dx.doi.org/10.1073/pnas .0812347106.
10. Mangerich A, Knutson CG, Parry NM, Muthupalani S, Ye W, Prestwich E, Cui L, McFaline JL, Mobley M, Ge Z, Taghizadeh K, Wishnok JS, Wogan GN, Fox JG, Tannenbaum SR, Dedon PC. 2012. Infectioninduced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc Natl Acad Sci U S A 109:E1820-E1829. http://dx.doi.org/10.1073/pnas.1207829109.
11. Nguyen DD, Muthupalani S, Goettel JA, Eston MA, Mobley M, Taylor NS, McCabe A, Marin R, Snapper SB, Fox JG. 2013. Colitis and colon cancer in WASP-deficient mice require helicobacter species. Inflamm Bowel Dis 19:2041-2050. http://dx.doi.org/10.1097/MIB .0b013e318295fd8f.
12. Lertpiriyapong K, Handt L, Feng Y, Mitchell TW, Lodge KE, Shen Z, Dewhirst FE, Muthupalani S, Fox JG. 2014. Pathogenic properties of enterohepatic Helicobacter spp. isolated from rhesus macaques with intestinal adenocarcinoma. J Med Microbiol 63:1004-1016. http://dx.doi.org/10.1099/jmm.0.072462-0.
13. Marini RP, Muthupalani S, Shen Z, Buckley EM, Alvarado C, Taylor NS, Dewhirst FE, Whary MT, Patterson MM, Fox JG. 2010. Persistent infection of rhesus monkeys with "Helicobacter macacae" and its isolation from an animal with intestinal adenocarcinoma. J Med Microbiol 59:961-969. http://dx.doi.org/10.1099/jmm.0.019117-0.
14. Fox JG, Boutin SR, Handt LK, Taylor NS, Xu S, Rickman B, Marini RP, Dewhirst FE, Paster BJ, Motzel S, Klein HJ. 2007. Isolation and characterization of a novel helicobacter species, "Helicobacter macacae," from rhesus monkeys with and without chronic idiopathic colitis. J Clin Microbiol 45:4061-4063. http://dx.doi.org/10.1128/JCM.01100-07.
15. Totten PA, Fennell CL, Tenover FC, Wezenberg JM, Perine PL, Stamm WE, Holmes KK. 1985. Campylobacter cinaedi (sp. nov.) and Campylobacter fennelliae (sp. nov.): two new Campylobacter species associated with enteric disease in homosexual men. J Infect Dis 151:131-139. http://dx.doi.org/10.1093/infdis/151.1.131.
16. Flores BM, Fennell CL, Kuller L, Bronsdon MA, Morton WR, Stamm WE. 1990. Experimental infection of pig-tailed macaques (Macaca nemestrina) with Campylobacter cinaedi and Campylobacter fennelliae. Infect Immun 58:3947-3953.
17. Thomson JM, Hansen R, Berry SH, Hope ME, Murray GI, Mukhopadhya I, McLean MH, Shen Z, Fox JG, El-Omar E, Hold GL. 2011. Enterohepatic helicobacter in ulcerative colitis: potential pathogenic entities? PLoS One 6:e17184. http://dx.doi.org/10.1371/journal.pone.0017184.
18. Fox JG, Dewhirst FE, Shen Z, Feng Y, Taylor NS, Paster BJ, Ericson RL, Lau CN, Correa P, Araya JC, Roa I. 1998. Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 114:755-763. http://dx.doi.org/10.1016/S0016-5085(98)70589-X.
19. Shen Z, Xu S, Dewhirst FE, Paster BJ, Pena JA, Modlin IM, Kidd M, Fox JG. 2005. A novel enterohepatic Helicobacter species "Helicobacter mastomyrinus" isolated from the liver and intestine of rodents. Helicobacter 10:59-70. http://dx.doi.org/10.1111/j.1523-5378.2005.00292.x.
20. Kaur T, Singh J, Huffman MA, Petrzelkova KJ, Taylor NS, Xu S, Dewhirst FE, Paster BJ, Debruyne L, Vandamme P, Fox JG. 2011. Campylobacter troglodytis sp. nov., isolated from feces of humanhabituated wild chimpanzees (Pan troglodytes schweinfurthii) in Tanzania. Appl Environ Microbiol 77:2366-2373. http://dx.doi.org/10.1128/AEM .01840-09.
21. Shen Z, Feng Y, Sheh A, Everitt J, Bertram F, Paster BJ, Fox JG. 2015. Isolation and characterization of a novel Helicobacter species, Helicobacter jaachi sp. nov., from common marmosets (Callithrix jaachus). J Med Microbiol 64:1063-1073. http://dx.doi.org/10.1099/jmm.0.000113.
22. Sheh A, Piazuelo MB, Wilson KT, Correa P, Fox JG. 2013. Draft genome sequences of Helicobacter pylori strains isolated from regions of low and high gastric cancer risk in Colombia. Genome Announc 1:e00736-13. http://dx.doi.org/10.1128/genomeA.00736-13.
23. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. http://dx.doi .org/10.1101/gr.074492.107.
24. Klimke W, Agarwala R, Badretdin A, Chetvernin S, Ciufo S, Fedorov B, Kiryutin B, O'Neill K, Resch W, Resenchuk S, Schafer S, Tolstoy I, Tatusova T. 2009. The National Center for Biotechnology Information's Protein Clusters Database. Nucleic Acids Res 37:D216-D223. http://dx .doi.org/10.1093/nar/gkn734.
25. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. http://dx.doi.org /10.1186/1471-2105-14-60.
26. Shen Z, Feng Y, Rogers AB, Rickman B, Whary MT, Xu S, Clapp KM, Boutin SR, Fox JG. 2009. Cytolethal distending toxin promotes Helicobacter cinaedi-associated typhlocolitis in interleukin-10-deficient mice. Infect Immun 77:2508-2516. http://dx.doi.org/10.1128/IAI.00166-09.
27. Chan V, Crocetti G, Grehan M, Zhang L, Danon S, Lee A, Mitchell H. 2005. Visualization of Helicobacter species within the murine cecal mucosa using specific fluorescence in situ hybridization. Helicobacter 10:114-124. http://dx.doi.org/10.1111/j.1523-5378.2005.00298.x.
28. Meier-Kolthoff JP, Klenk HP, Goker M. 2014. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 64:352-356. http://dx.doi.org/10.1099/ijs.0.056994-0.
29. Ivashkevich A, Redon CE, Nakamura AJ, Martin RF, Martin OA. 2012. Use of the gamma-H2AX assay to monitor DNA damage and repair in translational cancer research. Cancer Lett 327:123-133. http://dx.doi.org/10.1016/j.canlet.2011.12.025.
30. Turinetto V, Giachino C. 2015. Multiple facets of histone variant H2AX: aDNAdouble-strand-break marker with several biological functions. Nucleic Acids Res 43:2489-2498. http://dx.doi.org/10.1093/nar/gkv061.
31. Koeppel M, Garcia-Alcalde F, Glowinski F, Schlaermann P, Meyer TF. 2015. Helicobacter pylori infection causes characteristic DNA damage patterns in human cells. Cell Rep 11:1703-1713. http://dx.doi.org/10.1016/j .celrep.2015.05.030.
32. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263-274. http: //dx.doi.org/10.1016/0092-8674(93)80068-P.
33. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, Balish E, Rennick DM, Sartor RB. 1998. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 66:5224-5231.
34. + T regulatory cells suppress Helicobacter hepaticus-induced colitis. J Exp Med 196:505-515. http://dx.doi.org/10.1084/jem.20020556.
35. Kullberg MC, Jankovic D, Feng CG, Hue S, Gorelick PL, McKenzie BS, Cua DJ, Powrie F, Cheever AW, Maloy KJ, Sher A. 2006. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med 203:2485-2494. http://dx.doi.org/10.1084/jem.20061082.
36. Ray A, Basu S, Gharaibeh RZ, Cook LC, Kumar R, Lefkowitz EJ, Walker CR, Morrow CD, Franklin CL, Geiger TL, Salzman NH, Fodor A, Dittel BN. 2015. Gut microbial dysbiosis due to Helicobacter drives an increase in marginal zone B cells in the absence of IL-10 signaling in macrophages. J Immunol 195:3071-3085. http://dx.doi.org/10.4049/jimmunol.1500153.
37. Chichlowski M, Westwood GS, Abraham SN, Hale LP. 2010. Role of mast cells in inflammatory bowel disease and inflammation-associated colorectal neoplasia in IL-10-deficient mice. PLoS One 5:e12220. http://dx.doi.org/10.1371/journal.pone.0012220.
38. Fox JG, Gorelick PL, Kullberg MC, Ge Z, Dewhirst FE, Ward JM. 1999. A novel urease-negative Helicobacter species associated with colitis and typhlitis in IL-10-deficient mice. Infect Immun 67:1757-1762.
39. Shen Z, Feng Y, Rickman B, Fox JG. 2015. Helicobacter cinaedi induced typhlocolitis in Rag-2-deficient mice. Helicobacter 20:146-155. http://dx.doi.org/10.1111/hel.12179.
40. Eaton KA, Opp JS, Gray BM, Bergin IL, Young VB. 2011. Ulcerative typhlocolitis associated with Helicobacter mastomyrinus in telomerasedeficient mice. Vet Pathol 48:713-725. http://dx.doi.org/10.1177 /0300985810383876.
41. Dieleman LA, Arends A, Tonkonogy SL, Goerres MS, Craft DW, Grenther W, Sellon RK, Balish E, Sartor RB. 2000. Helicobacter hepaticus does not induce or potentiate colitis in interleukin-10-deficient mice. Infect Immun 68:5107-5113. http://dx.doi.org/10.1128/IAI.68.9.5107-5113.2000.
42. -/-) mice. Immunology 133:165-178. http://dx.doi.org/10.1111/j.1365-2567.2011.03423.x.
43. Floch P, Pey V, Castroviejo M, Dupuy JW, Bonneu M, de la Guardia AH, Pitard V, Megraud F, Lehours P. 2014. Role of Campylobacter jejuni gamma-glutamyl transpeptidase on epithelial cell apoptosis and lymphocyte proliferation. Gut Pathog 6:20. http://dx.doi.org/10.1186/1757-4749-6-20.
44. Javed S, Mejias-Luque R, Kalali B, Bolz C, Gerhard M. 2013. Helicobacter bilis gamma-glutamyltranspeptidase enhances inflammatory stress response via oxidative stress in colon epithelial cells. PLoS One 8:e73160. http://dx.doi.org/10.1371/journal.pone.0073160.
45. Rossi M, Bolz C, Revez J, Javed S, El-Najjar N, Anderl F, Hyytiainen H, Vuorela P, Gerhard M, Hanninen ML. 2012. Evidence for conserved function of gamma-glutamyltranspeptidase in Helicobacter genus. PLoS One 7:e30543. http://dx.doi.org/10.1371/journal.pone.0030543.
46. Zhang G, Ducatelle R, De Bruyne E, Joosten M, Bosschem I, Smet A, Haesebrouck F, Flahou B. 2015. Role of gamma-glutamyltranspeptidase in the pathogenesis of Helicobacter suis and Helicobacter pylori infections. Vet Res 46:31. http://dx.doi.org/10.1186/s13567-015-0163-6.
47. Grivennikov SI. 2013. Inflammation and colorectal cancer: colitisassociated neoplasia. Semin Immunopathol 35:229-244. http://dx.doi.org/10.1007/s00281-012-0352-6.
48. Francescone R, Hou V, Grivennikov SI. 2015. Cytokines, IBD, and colitis-associated cancer. Inflamm Bowel Dis 21:409-418. http://dx.doi.org/10.1097/MIB.0000000000000236.
49. Kiraly O, Gong G, Olipitz W, Muthupalani S, Engelward BP. 2015. Inflammation-induced cell proliferation potentiates DNA damageinduced mutations in vivo. PLoS Genet 11:e1004901. http://dx.doi.org/10.1371/journal.pgen.1004901.
50. Knutson CG, Mangerich A, Zeng Y, Raczynski AR, Liberman RG, Kang P, Ye W, Prestwich EG, Lu K, Wishnok JS, Korzenik JR, Wogan GN, Fox JG, Dedon PC, Tannenbaum SR. 2013. Chemical and cytokine features of innate immunity characterize serum and tissue profiles in inflammatory bowel disease. Proc Natl Acad Sci U S A 110:E2332-E2341. http://dx.doi.org/10.1073/pnas.1222669110.
51. Fox JG. 2002. The non-H. pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut 50:273-283. http://dx.doi.org/10.1136/gut.50.2.273.
52. Castano-Rodriguez N, Kaakoush NO, Lee WS, Mitchell HM. 27 October 2015. Dual role of Helicobacter and Campylobacter species in IBD: a systematic review and meta-analysis. Gut http://dx.doi.org/10.1136/gutjnl-2015-310545.