Exploitation of the Intestinal Microflora by the Parasitic Nematode Trichuris Muris

Overview

Journal Science

Specialty Science

Date 2010 Jun 12

PMID 20538949

Citations 161

Authors

K S Hayes

A J Bancroft

M Goldrick

C Portsmouth

I S Roberts

R K Grencis

Affiliations

Soon will be listed here.

Abstract

The inhabitants of the mammalian gut are not always relatively benign commensal bacteria but may also include larger and more parasitic organisms, such as worms and protozoa. At some level, all these organisms are capable of interacting with each other. We found that successful establishment of the chronically infecting parasitic nematode Trichuris muris in the large intestine of mice is dependent on microflora and coincident with modulation of the host immune response. By reducing the number of bacteria in the host animal, we significantly reduced the number of hatched T. muris eggs. Critical interactions between bacteria (microflora) and parasites (macrofauna) introduced a new dynamic to the intestinal niche, which has fundamental implications for our current concepts of intestinal homeostasis and regulation of immunity.

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References

Ofek I, Beachey E . Mannose binding and epithelial cell adherence of Escherichia coli. Infect Immun. 1978; 22(1):247-54. PMC: 422142. DOI: 10.1128/iai.22.1.247-254.1978. View

Fumagalli M, Pozzoli U, Cagliani R, Comi G, Riva S, Clerici M . Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J Exp Med. 2009; 206(6):1395-408. PMC: 2715056. DOI: 10.1084/jem.20082779. View

Ley R, Hamady M, Lozupone C, Turnbaugh P, Ramey R, Bircher J . Evolution of mammals and their gut microbes. Science. 2008; 320(5883):1647-51. PMC: 2649005. DOI: 10.1126/science.1155725. View

Eto D, Jones T, Sundsbak J, Mulvey M . Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog. 2007; 3(7):e100. PMC: 1914067. DOI: 10.1371/journal.ppat.0030100. View

Backhed F, Ley R, Sonnenburg J, Peterson D, Gordon J . Host-bacterial mutualism in the human intestine. Science. 2005; 307(5717):1915-20. DOI: 10.1126/science.1104816. View

Wold A . The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora?. Allergy. 1998; 53(46 Suppl):20-5. DOI: 10.1111/j.1398-9995.1998.tb04953.x. View

Reisner A, Haagensen J, Schembri M, Zechner E, Molin S . Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol. 2003; 48(4):933-46. DOI: 10.1046/j.1365-2958.2003.03490.x. View

. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser. 2003; 912:i-vi, 1-57, back cover. View

Ivanov I, Atarashi K, Manel N, Brodie E, Shima T, Karaoz U . Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009; 139(3):485-98. PMC: 2796826. DOI: 10.1016/j.cell.2009.09.033. View

10.

Hooper L, Stappenbeck T, Hong C, Gordon J . Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003; 4(3):269-73. DOI: 10.1038/ni888. View

11.

Breines D, Burnham J . Modulation of Escherichia coli type 1 fimbrial expression and adherence to uroepithelial cells following exposure of logarithmic phase cells to quinolones at subinhibitory concentrations. J Antimicrob Chemother. 1994; 34(2):205-21. DOI: 10.1093/jac/34.2.205. View

12.

Hooper L, Gordon J . Commensal host-bacterial relationships in the gut. Science. 2001; 292(5519):1115-8. DOI: 10.1126/science.1058709. View

13.

Edelman S, Kasper D . Symbiotic commensal bacteria direct maturation of the host immune system. Curr Opin Gastroenterol. 2009; 24(6):720-4. DOI: 10.1097/MOG.0b013e32830c4355. View

14.

Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C . The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009; 31(4):677-89. DOI: 10.1016/j.immuni.2009.08.020. View

15.

Ivanov I, de Llanos Frutos R, Manel N, Yoshinaga K, Rifkin D, Sartor R . Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008; 4(4):337-49. PMC: 2597589. DOI: 10.1016/j.chom.2008.09.009. View

16.

Yazdanbakhsh M, Matricardi P . Parasites and the hygiene hypothesis: regulating the immune system?. Clin Rev Allergy Immunol. 2004; 26(1):15-24. DOI: 10.1385/CRIAI:26:1:15. View

17.

Chaudhry A, Rudra D, Treuting P, Samstein R, Liang Y, Kas A . CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science. 2009; 326(5955):986-91. PMC: 4408196. DOI: 10.1126/science.1172702. View

18.

Thumbikat P, Berry R, Zhou G, Billips B, Yaggie R, Zaichuk T . Bacteria-induced uroplakin signaling mediates bladder response to infection. PLoS Pathog. 2009; 5(5):e1000415. PMC: 2669708. DOI: 10.1371/journal.ppat.1000415. View

19.

Bouckaert J, Mackenzie J, de Paz J, Chipwaza B, Choudhury D, Zavialov A . The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes. Mol Microbiol. 2006; 61(6):1556-68. PMC: 1618777. DOI: 10.1111/j.1365-2958.2006.05352.x. View

20.

Maizels R, Yazdanbakhsh M . Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003; 3(9):733-44. DOI: 10.1038/nri1183. View