Parasite proximity drives the expansion of regulatory T cells in Peyer's patches following intestinal helminth infection

Infection and Immunity

Volumn 83, Issue 9, 2015, Pages 3657-3665

  Mosconi, Ilaria ^a   Dubey, Lalit Kumar ^a   Volpe, Beatrice ^a   Esser von Bieren, Julia ^a   Zaiss, Mario M ^a   Lebon, Luc ^a   Massacand, Joanna C ^a   Harris, Nicola L ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; CLAVULANIC ACID; ENROFLOXACIN; RNA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; CELL EXPANSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; HELIGMOSOMOIDES POLYGYRUS; HELMINTHIASIS; INTESTINE INFECTION; LARVA; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TH2 CELL; ANIMAL; C57BL MOUSE; DISEASE MODEL; FLOW CYTOMETRY; IMMUNOLOGY; REAL TIME POLYMERASE CHAIN REACTION; STRONGYLE INFECTION;

ANIMALS; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; HELMINTHIASIS; INTESTINAL DISEASES, PARASITIC; MICE; MICE, INBRED C57BL; NEMATOSPIROIDES DUBIUS; PEYER'S PATCHES; REAL-TIME POLYMERASE CHAIN REACTION; STRONGYLIDA INFECTIONS; T-LYMPHOCYTES, REGULATORY; TH2 CELLS;

EID: 84939548413     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00266-15     Document Type: Article

References (46)

1. Krolewiecki A, Lammie P, Jacobson J, Gabrielli A-F, Levecke B, Socias E, Arias L, Sosa N, Abraham D, Cimino R, Echazú A, Crudo F, Vercruysse J, Albonico M. 2013. A public health response against Strongyloides stercoralis: time to look at soil-transmitted helminthiasis in full. PLoS Negl Trop Dis 7:e2165. http://dx.doi.org/10.1371/journal.pntd.0002165.
2. Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli A-F, Savioli L. 2008. Controlling soil-transmitted helminthiasis in pre-school-age children through preventive chemotherapy. PLoS Negl Trop Dis 2:e126. http://dx.doi.org/10.1371/journal.pntd.0000126.
3. Hotez P, Brindley P, Bethony J, King C, Pearce E, Jacobson J. 2008. Helminth infections: the great neglected tropical diseases. J Clin Invest 118:1311-1321. http://dx.doi.org/10.1172/JCI34261.
4. Pulendran B, Artis D. 2012. New paradigms in type 2 immunity. Science 337:431-435. http://dx.doi.org/10.1126/science.1221064.
5. Maizels R, Hewitson J, Murray J, Harcus Y, Dayer B, Filbey K, Grainger J, McSorley H, Reynolds L, Smith K. 2012. Immune modulation and modulators in Heligmosomoides polygyrus infection. Exp Parasitol 132:76-89. http://dx.doi.org/10.1016/j.exppara.2011.08.011.
6. Reynolds L, Filbey K, Maizels R. 2012. Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus. Semin Immunopathol 34:829-846. http://dx.doi.org/10.1007/s00281-012-0347-3.
7. McSorley H, Maizels R. 2012. Helminth infections and host immune regulation. Clin Microbiol Rev 25:585-608. http://dx.doi.org/10.1128/CMR.05040-11.
8. Camberis M, Le Gros G, Urban J. 2003. Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus. Curr Protoc Immunol Chapter 19:Unit 19.12. http://dx.doi.org/10.1002/0471142735.im1912s55.
9. Esser-von Bieren J, Mosconi I, Guiet R, Piersgilli A, Volpe B, Chen F, Gause WC, Seitz A, Verbeek JS, Harris NL. 2013. Antibodies trap tissue migrating helminth larvae and prevent tissue damage by driving IL-4Rα-independent alternative differentiation of macrophages. PLoS Pathog 9:e1003771. http://dx.doi.org/10.1371/journal.ppat.1003771.
10. Anthony R, Rutitzky L, Urban J, Stadecker M, Gause W. 2007. Protective immune mechanisms in helminth infection. Nat Rev Immunol 7:975-987. http://dx.doi.org/10.1038/nri2199.
11. Harris N, Gause W. 2011. To B or not to B: B cells and the Th2-type immune response to helminths. Trends Immunol 32:80-88. http://dx.doi.org/10.1016/j.it.2010.11.005.
12. Monroy F, Enriquez F. 1992. Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitol Today 8:49-54. http://dx.doi.org/10.1016/0169-4758(92)90084-F.
13. Anthony R, Urban J, Alem F, Hamed H, Rozo C, Boucher J-L, Van Rooijen N, Gause W. 2006. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med 12:955-960. http://dx.doi.org/10.1038/nm1451.
14. Massacand J, Stettler R, Meier R, Humphreys N, Grencis R, Marsland B, Harris N. 2009. Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function. Proc Natl Acad Sci U S A 106:13968-13973. http://dx.doi.org/10.1073/pnas.0906367106.
15. McCoy K, Stoel M, Stettler R, Merky P, Fink K, Senn B, Schaer C, Massacand J, Odermatt B, Oettgen H, Zinkernagel R, Bos N, Hengartner H, Macpherson A, Harris N. 2008. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4:362-373. http://dx.doi.org/10.1016/j.chom.2008.08.014.
16. Zaiss M, Maslowski K, Mosconi I, Guenat N, Marsland B, Harris N. 2013. IL-1ß suppresses innate IL-25 and IL-33 production and maintains helminth chronicity. PLoS Pathog 9:e1003531. http://dx.doi.org/10.1371/journal.ppat.1003531.
17. + CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur J Immunol 40:1682-1696. http://dx.doi.org/10.1002/eji.200939721.
18. McSorley H, O'Gorman M, Blair N, Sutherland T, Filbey K, Maizels R. 2012. Suppression of type 2 immunity and allergic airway inflammation by secreted products of the helminth Heligmosomoides polygyrus. Eur J Immunol 42:2667-2682. http://dx.doi.org/10.1002/eji.201142161.
19. Blum A, Hang L, Setiawan T, Urban J, Stoyanoff K, Leung J, Weinstock J. 2012. Heligmosomoides polygyrus bakeri induces tolerogenic dendritic cells that block colitis and prevent antigen-specific gut T cell responses. J Immunol 189:2512-2520. http://dx.doi.org/10.4049/jimmunol.1102892.
20. Grainger J, Smith K, Hewitson J, McSorley H, Harcus Y, Filbey K, Finney C, Greenwood E, Knox D, Wilson M, Belkaid Y, Rudensky A, Maizels R. 2010. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-ß pathway. J Exp Med 207:2331-2341. http://dx.doi.org/10.1084/jem.20101074.
21. Jung C, Hugot J-P, Barreau F. 2010. Peyer's patches: the immune sensors of the intestine. Int J Inflam 2010:823710. http://dx.doi.org/10.4061/2010/823710.
22. Taylor R, Williams I. 2005. Lymphoid organogenesis in the intestine. Immunol Res 33:167-181. http://dx.doi.org/10.1385/IR:33:2:167.
23. MacPherson G, Milling S, Yrlid U, Cousins L, Turnbull E, Huang F-P. 2004. Uptake of antigens from the intestine by dendritic cells. Ann N Y Acad Sci 1029:75-82. http://dx.doi.org/10.1196/annals.1309.010.
24. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869-877. http://dx.doi.org/10.1016/0092-8674(92)90030-G.
25. Zhu J, Min B, Hu-Li J, Watson C, Grinberg A, Wang Q, Killeen N, Urban J, Guo L, Paul W. 2004. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat Immunol 5:1157-1165. http://dx.doi.org/10.1038/ni1128.
26. Finney C, Taylor M, Wilson M, Maizels R. 2007. Expansion and activation of CD4(+)CD25(+) regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol 37:1874-1886. http://dx.doi.org/10.1002/eji.200636751.
27. Wilson M, Taylor M, Balic A, Finney C, Lamb J, Maizels R. 2005. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 202:1199-1212. http://dx.doi.org/10.1084/jem.20042572.
28. Rausch S, Huehn J, Kirchhoff D, Rzepecka J, Schnoeller C, Pillai S, Loddenkemper C, Scheffold A, Hamann A, Lucius R, Hartmann S. 2008. Functional analysis of effector and regulatory T cells in a parasitic nematode infection. Infect Immun 76:1908-1919. http://dx.doi.org/10.1128/IAI.01233-07.
29. Rötzschke O, Borsellino G, Battistini L, Falk K, Kleinewietfeld M. 2009. In vivo-activated CD103+ Foxp3+ Tregs: of men and mice. Blood 113:2119-2120. http://dx.doi.org/10.1182/blood-2008-11-188847.
30. Thornton AM, Korty PE, Tran DQ, Wohlfert EA, Murray PE, Belkaid Y, Shevach EM. 2010. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J Immunol 184:3433-3441. http://dx.doi.org/10.4049/jimmunol.0904028.
31. Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, McCoy KD, Macpherson AJ. 2011. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34:794-806. http://dx.doi.org/10.1016/j.immuni.2011.03.021.
32. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, Taniguchi T, Takeda K, Hori S, Ivanov II, Umesaki Y, Itoh K, Honda K. 2011. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331:337-341. http://dx.doi.org/10.1126/science.1198469.
33. Lathrop S, Bloom S, Rao S, Nutsch K, Lio C-W, Santacruz N, Peterson D, Stappenbeck T, HsiehCS. 2011. Peripheral education of the immune system by colonic commensal microbiota. Nature 478:250-254. http://dx.doi.org/10.1038/nature10434.
34. Sommer F, Bäckhed F. 2013. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 11:227-238. http://dx.doi.org/10.1038/nrmicro2974.
35. Round J, Lee S, Li J, Tran G, Jabri B, Chatila T, Mazmanian S. 2011. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332:974-977. http://dx.doi.org/10.1126/science.1206095.
36. Gaboriau-Routhiau V, Rakotobe S, Lécuyer E, Mulder I, Lan A, Bridonneau C, Rochet V, Pisi A, De Paepe M, Brandi G, Eberl G, Snel J, Kelly D, Cerf-Bensussan N. 2009. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31:677-689. http://dx.doi.org/10.1016/j.immuni.2009.08.020.
37. Ivanov I, Atarashi K, Manel N, Brodie E, Shima T, Karaoz U, Wei D, Goldfarb K, Santee C, Lynch S, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman D. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485-498. http://dx.doi.org/10.1016/j.cell.2009.09.033.
38. Cording S, Fleissner D, Heimesaat M, Bereswill S, Loddenkemper C, Uematsu S, Akira S, Hamann A, Huehn J. 2013. Commensal microbiota drive proliferation of conventional and Foxp3(+) regulatory CD4(+) T cells in mesenteric lymph nodes and Peyer's patches. Eur J Microbiol Immunol 3:1-10. http://dx.doi.org/10.3923/mj.2013.1.11.
39. Massacand JC, Kaiser P, Ernst B, Tardivel A, Burki K, Schneider P, Harris NL. 2008. Intestinal bacteria condition dendritic cells to promote IgA production. PLoS One 3:e2588. http://dx.doi.org/10.1371/journal.pone.0002588.
40. Schlüter C, Duchrow M, Wohlenberg C, Becker M, Key G, Flad H, Gerdes J. 1993. The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123:513-522. http://dx.doi.org/10.1083/jcb.123.3.513.
41. Hisaeda H, Maekawa Y, Iwakawa D, Okada H, Himeno K, Kishihara K, Tsukumo S, Yasutomo K. 2004. Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells. Nat Med 10:29-30. http://dx.doi.org/10.1038/nm975.
42. Taylor M, LeGoff L, Harris A, Malone E, Allen J, Maizels R. 2005. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol 174:4924-4933. http://dx.doi.org/10.4049/jimmunol.174.8.4924.
43. Kullberg M, Jankovic D, Gorelick P, Caspar P, Letterio J, Cheever A, Sher A. 2002. Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J Exp Med 196:505-515. http://dx.doi.org/10.1084/jem.20020556.
44. Hesse M, Piccirillo C, Belkaid Y, Prufer J, Mentink-Kane M, Leusink M, Cheever A, Shevach E, Wynn T. 2004. The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol 172:3157-3166. http://dx.doi.org/10.4049/jimmunol.172.5.3157.
45. Rausch S, Huehn J, Loddenkemper C, Hepworth M, Klotz C, Sparwasser T, Hamann A, Lucius R, Hartmann S. 2009. Establishment of nematode infection despite increased Th2 responses and immunopathology after selective depletion of Foxp3+ cells. Eur J Immunol 39:3066-3077. http://dx.doi.org/10.1002/eji.200939644.
46. Jan MH, Sougawa N, Tanaka T, Jirata T, Hiroi T, Tohya K, Guo Z, Umemoto E, Ebisuno Y, Yang BG, Seoh JY, Lipp M, Kiqono H, Miyasaka M. 2006. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J Immunol 176:803-810. http://www.jimmunol.org/content/176/2/803.