Lack of host gut microbiota alters immune responses and intestinal granuloma formation during schistosomiasis

Clinical and Experimental Immunology

Volumn 175, Issue 2, 2014, Pages 246-257

  Holzscheiter, M ^a   Layland, L E ^a,c   Loffredo Verde, E ^a   Mair, K ^b   Vogelmann, R ^b   Langer, R ^b   Wagner, H ^a   Prazeres da Costa, C ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Gut microbiota; Host parasite interaction; Immunopathology; Schistosomiasis; Th responses

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; ANTIFUNGAL AGENT; CIPROFLOXACIN; CYTOKINE; FLUCONAZOLE; IMIPENEM; METRONIDAZOLE; VANCOMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; EGG; ENTERITIS; FECES; FEMALE; GRANULOMA; HOST PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNOPATHOLOGY; INTESTINE FLORA; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI;

GUT-MICROBIOTA; HOST-PARASITE INTERACTION; IMMUNOPATHOLOGY; SCHISTOSOMIASIS; TH RESPONSES;

ANIMALS; ANTI-BACTERIAL AGENTS; FECES; FEMALE; GRANULOMA; HOST-PARASITE INTERACTIONS; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-13; INTESTINES; LIVER; MICE; MICE, INBRED C57BL; MICROBIOTA; PARASITE LOAD; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TH1 CELLS;

EID: 84891608339     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12230     Document Type: Article

References (44)

1. Pearce EJ, MacDonald AS. The immunobiology of schistosomiasis. Nat Rev Immunol 2002; 2:499-511.
2. Wilson MS, Mentink-Kane MM, Pesce JT etal. Immunopathology of schistosomiasis. Immunol Cell Biol 2007; 85:148-154.
3. Wilson S, Vennervald BJ, Kadzo H etal. Health implications of chronic hepatosplenomegaly in Kenyan school-aged children chronically exposed to malarial infections and Schistosoma mansoni. Trans R Soc Trop Med Hyg 2010; 104:110-111.
4. Mountford AP, Coulson PS, Pemberton RM etal. The generation of interferon-gamma-producing T lymphocytes in skin-draining lymph nodes, and their recruitment to the lungs, is associated with protective immunity to Schistosoma mansoni. Immunology 1992; 75:250-256.
5. Wynn TA, Oswald IP, Eltoum IA etal. Elevated expression of Th1 cytokines and nitric oxide synthase in the lungs of vaccinated mice after challenge infection with Schistosoma mansoni. J Immunol 1994; 153:5200-5209.
6. -/- mice. Eur J Immunol 2005; 35:3248-3257.
7. Layland LE, Rad R, Wagner H etal. Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur J Immunol 2007; 37:2174-2184.
8. Layland LE, Mages J, Loddenkemper C etal. Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J Immunol 2010; 184:713-724.
9. Pearce EJ, Kane CM, Sun J etal. Th2 polarisation during infection with the helminth parasite Schistosoma mansoni. Immunol Rev 2004; 201:117-126.
10. Pearce EJ. Priming of the immune response by schistosome eggs. Parasite Immunol 2005; 27:265-270.
11. Cheever AW, Duvall RH, Hallack TA Jr etal. Variation of hepatic fibrosis and granuloma size among mouse strains infected with Schistosoma mansoni. Am J Trop Med Hyg 1987; 37:85-97.
12. Rutitzky LI, Hernandez HJ, Stadecker MJ. Th1-polarizing immunization with egg antigens correlates with severe exacerbation of immunopathology and death in schistosome infection. Proc Natl Acad Sci USA 2001; 98:13243-13248.
13. Fallon PG, Richardson EJ, McKenzie GJ etal. Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J Immunol 2000; 164:2585-2591.
14. King CH, Sturrock RF, Kariuki HC. Transmission control for schistosomiasis - why it matters now. Trends Parasitol 2006; 22:575-582.
15. Kane CM, Cervi L, Sun J etal. Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 2004; 173:7454-7461.
16. van Liempt E, van Vliet SJ, Engering A etal. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol Immunol 2007; 44:2605-2615.
17. Correale J, Farez M. Helminth antigens modulate immune responses in cells from multiple sclerosis patients through TLR2-dependent mechanisms. J Immunol 2009; 183:5999-6012.
18. Ritter M, Gross O, Kays S etal. Schistosoma mansoni triggers Dectin-2 which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc Natl Acad Sci USA 2010; 107:20459-20464.
19. Niess JH, Adler G. Enteric flora expands gut lamina propria CX3CR1+ dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions. J Immunol 2010; 184:2026-2237.
20. Marchiando AM, Graham WV, Turner JR. Epithelial barriers in homeostasis and disease. Annu Rev Pathol 2010; 5:119-144.
21. Heimesaat MM, Bereswill S, Fischer A etal. Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J Immunol 2006; 177:8785-8795.
22. Heimesaat MM, Fischer A, Siegmund B etal. Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4. PLOS ONE 2007; 2:662.
23. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F etal. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 2004; 118:229-241.
24. Dixon MF, Genta RM, Yardley JH etal. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol 1996; 10:1161-1181.
25. Whitehead RH, Robinson PS, Williams JA etal. Conditionally immortalized colonic epithelial cell line from a Ptk6 null mouse that polarizes and differentiates in vitro. J Gastroenterol Hepatol 2008; 23:1119-1124.
26. Nobre V, Serufo JC, Carvalho Odos S etal. Alteration in the endogenous intestinal flora of Swiss Webster mice by experimental Angiostrongylus costaricensis infection. Mem Inst Oswaldo Cruz 2004; 99:717-720.
27. Hamilton CM, Dowling DJ, Loscher CE etal. The Fasciola hepatica tegumental antigen suppresses dendritic cell maturation and function. Infect Immun 2009; 6:2488-2498.
28. Benson A, Pifer R, Behrendt CL etal. Gut commensal bacteria direct a protective immune response against Toxoplasma gondii. Cell Host Microbe 2009; 6:187-196.
29. Karanja DM, Colley DG, Nahlen BL etal. Studies on schistosomiasis in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 1997; 56:515-521.
30. Doenhoff M, Musallam R, Bain J etal. Studies on the host-parasite relationship in Schistosoma mansoni-infected mice: the immunological dependence of parasite egg excretion. Immunology 1978; 35:771-778.
31. Amiri P, Locksley RM, Parslow TG etal. Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature 1992; 356:604-607.
32. Cheever AW, Poindexter RW, Wynn TA. Egg laying is delayed but worm fecundity is normal in SCID mice infected with Schistosoma japonicum and S. mansoni with or without recombinant tumor necrosis factor alpha treatment. Infect Immun 1999; 67:2201-2208.
33. Boros DL. Immunopathology of Schistosoma mansoni infection. Clin Microbiol Rev 1989; 2:250-269.
34. Silva LM, Fernandes AL, Barbosa A etal. Significance of schistosomal granuloma modulation. Mem Inst Oswaldo Cruz 2000; 95:353-361.
35. Oliveira VR, El-Cheikh MC, Aguiar AM etal. Schistosoma mansoni egg-induced hepatic granulomas in mice deficient for the interferon-gamma receptor have altered populations of macrophages, lymphocytes and connective tissue cells. Microbes Infect 2000; 2:1817-1826.
36. Rezende SA, Oliveira VR, Silva AM etal. Mice lacking the gamma interferon receptor have an impaired granulomatous reaction to Schistosoma mansoni infection. Infect Immun 1997; 65:3457-3461.
37. Grove DI, Mahmound AA, Warren KS. Suppression of cell-mediated immunity by metronidazole. Int Arch Allergy Appl Immunol 1977; 54:422-427.
38. Viera LQ, Moraes-Santos T. Schistosomiasis mansoni: evidence for a milder response in germfree mice. Rev Inst Med Trop Sao Paulo 1987; 29:37-42.
39. Vieira LQ, Moraes-Santos T, Vieira EC. Alterations in cell number, size and collagen content in livers of conventional and germfree mice bearing Schistosoma mansoni. Prog Clin Biol Res 1985; 181:235-238.
40. Wynn TA, Thompson RW, Cheever AW etal. Immunopathogenesis of schistosomiasis. Immunol Rev 2004; 201:156-167.
41. Lukacs NW, Boros DL. Lymphokine regulation of granuloma formation in murine Schistosomiasis mansoni. Clin Immunol Immunopathol 1993; 68:57-63.
42. Boros DL. The role of cytokines in the formation of the schistosome egg granuloma. Immunobiology 1994; 191:441-450.
43. Chensue SW, Warmington KS, Ruth J etal. Cross-regulatory role of interferon-gamma (IFN-gamma), interleukin (IL)-4 and IL-10 in schistosome egg granuloma formation: in-vivo regulation of T helper activity and inflammation. Clin Exp Immunol 1994; 98:395-400.
44. Hayes KS, Bancroft AJ, Goldrick M etal. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 2010; 328:1391-1394.