Suppression of inflammation by helminths: A role for the gut microbiota?

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1675, 2015, Pages

  Giacomin, Paul ^a   Croese, John ^b   Krause, Lutz ^c   Loukas, Alex ^a   Cantacessi, Cinzia ^d  

^a JAMES COOK UNIVERSITY   (Australia)

^b THE PRINCE CHARLES HOSPITAL   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Helminth induced suppression of inflammation; Hookworms; Host parasite interactions; Microbial richness; Microbiota; Whipworms

Indexed keywords

COMMENSAL; DISEASE TREATMENT; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; MICROBIAL COMMUNITY; PARASITE; PATHOGENICITY;

ANCYLOSTOMATOIDEA; VERMES;

ANIMAL; CELIAC DISEASE; DISEASE MODEL; HELMINTH; HOOKWORM; HOST PARASITE INTERACTION; HUMAN; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTESTINE FLORA; MICROBIOLOGY; PARASITOLOGY; PROCEDURES; TRICHURIS;

ANCYLOSTOMATOIDEA; ANIMALS; CELIAC DISEASE; DISEASE MODELS, ANIMAL; GASTROINTESTINAL MICROBIOME; HELMINTHS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOSUPPRESSION; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; TRICHURIS;

EID: 84936984348     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0296     Document Type: Review

References (54)

1. Lozupone CA, Stombaugh JI, Gordon JI, Jansoon JK, Knight R. 2012 Diversity, stability and resilience of the human gut microbiota. Nature 489, 242-249. (doi:10. 1038/nature11552)
2. Brestoff JR, Artis D. 2013 Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 14, 676-684. (doi:10. 1038/ ni. 2640)
3. McLean MH, Dieguez Jr D, Miller LM, Young HA. 2015 Does the microbiota play a role in the pathogenesis of autoimmune disease? Gut 64, 332-341. (doi:10. 1136/gutjnl-2014-308514)
4. Knights D, Lassen KG, Xavier RJ. 2013 Advances in inflammatory bowel disease pathogenesis: linking host genetics and the microbiome. Gut 62, 1505-1515. (doi:10. 1136/gutjnl-2012-303954)
5. de Sousa Moraes LF, Grzeskowiak LM, de Sales Teixeira TF, Gouveia Peluzio MC. 2014 Intestinal microbiota and probiotics in celiac disease. Clin. Microbiol. Rev. 27, 482-489. (doi:10. 1128/CMR. 00106-13)
6. M'Koma AE. 2013 Inflammatory bowel disease: an expanding global health problem. Clin. Med. Insights Gastroenterol. 14, 33-47. (doi:10. 4137/ CGast. S12731)
7. Podolski DK. 2002 Inflammatory bowel disease. N. Engl. J. Med. 347, 417-429. (doi:10. 1056/ NEJMra020831)
8. Sartor RB, Mazmanian SK. 2012 Intestinal microbes in inflammatory bowel disease. Am. J. Gastroenterol. Suppl. 1, 15-21. (doi:10. 1038/ajgsup. 2012. 4)
9. Olivares M, Laparra JM, Sanz Y. 2013 Host genotype, intestinal microbiota and inflammatory disorders. Br. J. Nutr. 109, S76-S80. (doi:10. 1017/ S0007114512005521)
10. Fasano A, Catassi C. 2012 Clinical practice. Celiac disease. N. Engl. J. Med. 367, 2419-2426. (doi:10. 1056/NEJMcp1113994)
11. Abadie V, Discepolo V, Jabri B. 2012 Intraepithelial lymphocytes in celiac disease immunopathology. Semin. Immunopathol. 34, 551-566. (doi:10. 1007/ s00281. 012. 0316. x)
12. Di Sabatino A, Vanoli A, Giuffrida P, Liunetti O, Solcia E, Corazza GR. 2012 The function of tissue transglutaminase in celiac disease. Autoimmun. Rev. 11, 746-753. (doi:10. 1016/j. autrev. 2012. 01. 007)
13. Nadal I, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. 2007 Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J. Med. Microbiol. 56, 1669-1674. (doi:10. 1099/jmm. 0. 47410-0)
14. Strachan DP. 1989 Hay fever, hygiene and household size. BMJ 299, 1259-1260. (doi:10. 1136/bmj. 299. 6710. 1259)
15. Navarro S, Ferreira I, Loukas A. 2013 The hookworm pharmacopoeia for inflammatory diseases. Int. J. Parasitol. 43, 225-231. (doi:10. 1016/j. ijpara. 2012. 11. 005)
16. Weinstock JV, Elliott DE. 2013 Translatability of helminth therapy in inflammatory bowel diseases. Int. J. Parasitol. 43, 245-251. (doi:10. 1016/j. ijpara. 2012. 10. 016)
17. Wammes LJ, Mpairwe H, Elliott AM, Yazdanbakhsh M. 2014 Helminth therapy or elimination: epidemiological, immunological, and clinical considerations. Lancet Infect. Dis. 14, 1150-1162. (doi:10. 1016/S1473-3099(14)70771-6)
18. Evans H, Mitre E. 2015 Worms as therapeutic agents for allergy and asthma: understanding why benefits in animal studies have not translated into clinical success. J. Allergy Clin. Immunol. 135, 343-353. (doi:10. 1016/j. jaci. 2014. 07. 007)
19. Croese J, Gaze ST, Loukas A. 2013 Changed gluten immunity in celiac disease by Necator americanus provides new insights into autoimmunity. Int. J. Parasitol. 43, 275-282. (doi:10. 1016/j. ijpara. 2012. 12. 005)
20. Anderson RC. 2000 Nematode parasites of vertebrates. Their development and transmission, 2nd edn. Wallingford, UK: CABI Publishing.
21. Hurst RJ, Else KJ. 2013 Trichuris muris research revisited: a journey through time. Parasitology 140, 1325-1339. (doi:10. 1017/S0031182013001054)
22. Hayes KS, Bancroft AJ, Goldrick M, Portsmouth IS, Grencis RK. 2010 Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328, 1391-1394. (doi:10. 1126/science. 1187703)
23. Ebner F et al. 2014 Therapeutic potential of larval excretory/secretory proteins of the pig whipworm Trichuris suis in allergic disease. Allergy 69, 1489-1497. (doi:10. 1111/all. 12496)
24. Summers RW, Elliott DE, Qadir K, Urban Jr JF, Thompson R, Weinstock JV. 2003 Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am. J. Gastroenterol. 98, 2034-2041. (doi:10. 1111/ j. 1572-0241. 2003. 07660. x)
25. Summers RW, Elliott DE, Urban Jr JF, Thompson RA, Weinstock JV. 2005 Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825-832. (doi:10. 1053/j. gastro. 2005. 01. 005)
26. Summers RW, Elliott DE, Urban Jr JF, Thompson R, Weinstock JV. 2005 Trichuris suis therapy in Crohn's disease. Gut 54, 87-90. (doi:10. 1136/gut. 2004. 041749)
27. Fleming JO, Isaak A, Lee JE, Luzzio CC, Carrithers MD, Cook TD, Field AS, Boland J, Fabry Z. 2011 Probiotic helminth administration in relapsingremitting multiple sclerosis: a phase 1 study. Mult. Scler. 17, 743-754. (doi:10. 1177/135245851 1398054)
28. Elliott DE, Weinstock JV. 2012 Helminth-host immunological interactions: prevention and control of immune-mediated disease. Ann. NY Acad. Sci. 1247, 83-96. (doi:10. 1111/j. 1749-6632. 2011. 06292. x)
29. Klementowicz JE, Travis MA, Grencis RK. 2012 Trichuris muris: a model of gastrointestinal parasite infection. Semin. Immunopathol. 34, 815-828. (doi:10. 1007/s00281-012-0348-2)
30. Glendinning L, Nausch N, Free A, Taylor DW, Mutapi F. 2014 The microbiota and helminths: sharing the same niche in the human host. Parasitology 141, 1255-1271. (doi:10. 1017/ S0031182014000699)
31. Walk ST, Blum AM, Ewing SAS, Weinstock JV, Young VB. 2010 Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm. Bowel Dis. 16, 1841-1849. (doi:10. 1002/ibd. 21299)
32. Reynolds LA et al. 2014 Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites. Gut Microbes 5, 522-532. (doi:10. 4161/gmic. 32155)
33. Wu S, Li RW, Beshah E, Dawson HD, Urban Jr JF. 2012 Worm-burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS ONE 7, e35470. (doi:10. 1371/journal. pone. 0035470)
34. Broadhurst MJ et al. 2012 Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog. 8, e1003000. (doi:10. 1371/journal. ppat. 1003000)
35. Wolff MJ, Broadhurst MJ, Loke P. 2012 Helminthic therapy: improving mucosal barrier function. Trends Parasitol. 28, 187-194. (doi:10. 1016/j. pt/2-12. 02. 008)
36. Leung JM, Loke P. 2013 A role for IL-22 in the relationship between intestinal helminths, gut microbiota and mucosal immunity. Int. J. Parasitol. 43, 253-257. (doi:10. 1016/j. ijpara. 2012. 10. 015)
37. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. 2004 Hookworm infection. N. Engl. J. Med. 351, 799-807. (doi:10. 1056/ NEJMra032492)
38. Gasser RB, Cantacessi C, Loukas A. 2008 DNA technological progress toward advanced diagnostic tools to support human hookworm control. Biotechnol. Adv. 26, 35-45. (doi:10. 1016/j. biotechadv. 2007. 09. 003)
39. Mortimer K, Brown A, Feary J, Jagger C, Lewis S, Antoniak M, Pritchard D, Britton J. 2006 Doseranging study for trials of therapeutic infection with Necator americanus in humans. Am. J. Trop. Med. Hyg. 75, 914-920.
40. Feary J, Venn A, Brown A, Hooi D, Falcone FH, Mortimer K, Pritchard DI, Britton J. 2009 Safety of hookworm infection in individuals with measurable airway responsiveness: a randomized placebocontrolled feasibility study. Clin. Exp. Allergy 39, 1060-1068. (doi:10. 1111/j. 1365-2222. 2009. 03187. x)
41. Daveson AJ et al. 2011 Effect of hookworm infection on wheat challenge in celiac disease-a randomised double-blinded placebo controlled trial. PLoS ONE 6, e17366. (doi:10. 1371/journal. pone. 0017366)
42. Gaze S et al. 2012 Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 8, e1002520. (doi:10. 1371/journal. ppat. 1002520)
43. Croese J et al. 2015 Experimental hookworm infection and gluten microchallenge promote tolerance in celiac disease. J. Allergy Clin. Immunol. 135, 508-516. (doi:10. 1016/j. jaci. 2014. 07. 022)
44. McSorley HJ et al. 2011 Suppression of inflammatory immune responses in celiac disease by experimental hookworm infection. PLoS ONE 6, e24092. (doi:10. 1371/journal. pone. 0024092)
45. + T cell responses and suppress pathology in a mouse model of colitis. Infect. Immun. 81, 2104-2111. (doi:10. 1128/iai. 00563-12)
46. Croese J, O'Neil J, Masson J, Cooke S, Melrose W, Pritchard D, Speare R. 2006 A proof-of-concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 55, 136-137. (doi:10. 1136/gut. 2005. 079129)
47. Cantacessi C et al. 2014 Impact of experimental hookworm infection on the human gut microbiota. J. Infect. Dis. 210, 1431-1434. (doi:10. 1093/infdis/ jiu256)
48. Lee SC et al. 2014 Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 8, e2880. (doi:10. 1371/journal. pntd. 0002880)
49. Sepehri S, Kotlowski R, Bernstein CN, Krause DO. 2007 Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflamm. Bowel Dis. 13, 675-683. (doi:10. 1002/ibd. 20101)
50. Monira S, Shabnam SA, Alam NH, Endtz HP, Cravioto A, Alam M. 2012 16S rRNA gene-targeted TTGE in determining diversity of the gut microbiota during acute diarrhoea and convalescence. J. Health Popul. Nutr. 30, 250-256. (doi:10. 3329/jhpn. v30i3. 12287)
51. Lin A, Bik EM, Costello EK, Dethlefsen L, Haque R, Relman DA, Singh U. 2013 Distinct distal gut microbiome diversity and composition in healthy children from Bangladesh and the United States. PLoS ONE 8, e53838. (doi:10. 1371/journal. pone. 0053838)
52. Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S. 2011 The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol. Rev. 35, 681-704. (doi:10. 1111/j. 1574. 6976. 2011. 00270. x)
53. Boyett D, Hsieh MH. 2014 Wormholes in host defense: how helminths manipulate host tissues to survive and reproduce. PLoS Pathog. 10, e1004014. (doi:10. 1371/journal. ppat. 1004014)
54. Li RW, Wu S, Weizhing L, Navarro K, Couch RD, Hill D, Urban Jr JF. 2012 Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect. Immun. 80, 2150-2157. (doi:10. 1120/iai. 00141-12)