1932

Abstract

Helminth parasites are a highly successful group of pathogens that challenge the immune system in a manner distinct from rapidly replicating infectious agents. Of this group, roundworms (nematodes) that dwell in the intestines of humans and other animals are prevalent worldwide. Currently, more than one billion people are infected by at least one species, often for extended periods of time. Thus, host-protective immunity is rarely complete. The reasons for this are complex, but laboratory investigation of tractable model systems in which protective immunity is effective has provided a mechanistic understanding of resistance that is characterized almost universally by a type 2/T helper 2 response. Greater understanding of the mechanisms of susceptibility has also provided the basis for defining host immunoregulation and parasite-evasion strategies, helping place in context the changing patterns of immunological disease observed worldwide.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-immunol-032713-120218
2015-03-21
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/immunol/33/1/annurev-immunol-032713-120218.html?itemId=/content/journals/10.1146/annurev-immunol-032713-120218&mimeType=html&fmt=ahah

Literature Cited

  1. Lamshead PJD, Boucher G. 1.  2003. Marine nematode deep-sea biodiversity—hyperdiverse or hype?. J. Biogeogr. 30:475–85 [Google Scholar]
  2. Blaxter M. 2.  2011. Nematodes: the worm and its relatives. PLOS Biol. 9:4e1001050 [Google Scholar]
  3. Anderson RM, May RM. 3.  1985. Helminth infections of humans: mathematical models, population dynamics, and control. Adv. Parasitol. 24:1–101 [Google Scholar]
  4. Balic A, Bowles VM, Meeusen EN. 4.  2000. The immunobiology of gastrointestinal nematode infections in ruminants. Adv. Parasitol. 45:181–241 [Google Scholar]
  5. Miller HR. 5.  1996. Prospects for the immunological control of ruminant gastrointestinal nematodes: Natural immunity, can it be harnessed?. Int. J. Parasitol. 26:8–9801–11 [Google Scholar]
  6. Kaplan RM, Vidyashankar AN. 6.  2012. An inconvenient truth: global worming and anthelmintic resistance. Vet. Parasitol. 186:1–270–78 [Google Scholar]
  7. Babu S, Nutman TB. 7.  2012. Immunopathogenesis of lymphatic filarial disease. Semin. Immunopathol. 34:6847–61 [Google Scholar]
  8. Pearce EJ, MacDonald AS. 8.  2002. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2:7499–511 [Google Scholar]
  9. Flynn RJ, Mulcahy G, Elsheikha HM. 9.  2010. Coordinating innate and adaptive immunity in Fasciola hepatica infection: implications for control. Vet. Parasitol. 169:3–4235–40 [Google Scholar]
  10. Lightowlers MW. 10.  2010. Fact or hypothesis: concomitant immunity in taeniid cestode infections. Parasite Immunol. 32:8582–89 [Google Scholar]
  11. Grencis RK, Humphreys NE, Bancroft AJ. 11.  2014. Immunity to gastrointestinal nematodes: mechanisms and myths. Immunol. Rev. 260:1183–205 [Google Scholar]
  12. Zaph C, Cooper PJ, Harris NL. 12.  2014. Mucosal immune responses following intestinal nematode infection. Parasite Immunol. 2014:1–14 [Google Scholar]
  13. Grencis RK. 13.  1997. Th2-mediated host protective immunity to intestinal nematode infections. Philos. Trans. R. Soc. Lond. B 352:13591377–84 [Google Scholar]
  14. Maizels RM, Hewitson JP, Smith KA. 14.  2012. Susceptibility and immunity to helminth parasites. Curr. Opin. Immunol. 24:4459–66 [Google Scholar]
  15. Africa CM. 15.  1931. Studies on the host relations of Nippostrongylus muris, with special reference to age resistance and acquired immunity. J. Parasitol. 18:1–14 [Google Scholar]
  16. Sarles MP, Taliaferro WH. 16.  1936. The local points of defense and the passive transfer of acquired immunity to Nippostrongylus muris in rats. J. Infect. Dis. 59:207–220 [Google Scholar]
  17. Taliaferro WH, Sarles MP. 17.  1939. The cellular reactions in the skin, lungs and intestine of normal and immune rats after infection with Nippostrongylus muris. J. Infect. Dis. 64:2157–92 [Google Scholar]
  18. Taliaferro WH, Sarles MP. 18.  1942. The histopathology of skin, lungs and intestine of rats during passive immunity to Nippostrongylus muris. J. Infect. Dis. 71:169–82 [Google Scholar]
  19. Chandler CA. 19.  1932. Experiments on resistance of rats to superinfection with the nematode Nippostrongylus muris. Am. J. Hyg. 16:750–82 [Google Scholar]
  20. Chandler CA. 20.  1935. Studies on the nature of immunity to intestinal helminths. I. The local nature of the immunity of white rats to Nippostrongylus infection. Am. J. Hyg. 22:157–68 [Google Scholar]
  21. Klion AD, Nutman TB. 21.  2004. The role of eosinophils in host defense against helminth parasites. J. Allergy Clin. Immunol. 113:130–37 [Google Scholar]
  22. Ogilvie BM, Love RJ. 22.  1974. Co-operation between antibodies and cells in immunity to a nematode parasite. Transplant Rev. 19:0147–69 [Google Scholar]
  23. Ogilvie BM, Jones VE. 23.  1968. Passive protection with cells or antiserum against Nippostrongylus brasiliensis in the rat. Parasitology 58:4939–49 [Google Scholar]
  24. Love RJ, Ogilvie BM, McLaren DJ. 24.  1975. Nippostrongylus brasiliensis: further properties of antibody-damaged worms and induction of comparable damage by maintaining worms in vitro. Parasitology 71:2275–83 [Google Scholar]
  25. Dineen JK, Wagland BM. 25.  1966. The dynamics of the host-parasite relationship. IV. The response of sheep to graded and to repeated infection with Haemonchus contortus. Parasitology 56:4639–50 [Google Scholar]
  26. Wagland BM, Dineen JK. 26.  1965. The cellular transfer of immunity to Trichostrongylus colubriformis in an isogenic strain of guinea-pig. Aust. J. Exp. Biol. Med. Sci. 43:429–38 [Google Scholar]
  27. Dineen JK, Ronai PM, Wagland BM. 27.  1968. The cellular transfer of immunity to Trichostrongylus colubriformis in an isogenic strain of guinea-pig. IV. The localization of immune lymphocytes in small intestine in infected and non-infected guinea-pigs. Immunology 15:5671–79 [Google Scholar]
  28. Nawa Y, Miller HR, Hall E, Jarrett EE. 28.  1981. Adoptive transfer of total and parasite-specific IgE responses in rats infected with Nippostrongylus brasiliensis. Immunology 44:1119–23 [Google Scholar]
  29. Ogilvie BM. 29.  1964. Reagin-like antibodies in animals immune to helminth parasites. Nature 204:91–92 [Google Scholar]
  30. Alba-Hurtado F, Munoz-Guzman MA. 30.  2013. Immune responses associated with resistance to haemonchosis in sheep. Biomed. Res. Int. 2013:162158 [Google Scholar]
  31. Dineen JK, Adams DB. 31.  1971. The role of the recirculating thymus-dependent lymphocyte in resistance to Trichostrongylus colubriformis in the guinea-pig. Immunology 20:1109–13 [Google Scholar]
  32. Ogilvie BM, Hockley DJ. 32.  1968. Effects of immunity on Nippostrongylus brasiliensis adult worms: reversible and irreversible changes in infectivity, reproduction, and morphology. J. Parasitol. 54:61073–84 [Google Scholar]
  33. Wakelin D. 33.  1978. Immunity to intestinal parasites. Nature 273:5664617–20 [Google Scholar]
  34. Castro GA, Harari Y. 34.  1991. Immunoregulation of endometrial and jejunal epithelia sensitized by infection. Int. Arch. Allergy Appl. Immunol. 95:2–3184–90 [Google Scholar]
  35. Bell RG, Appleton JA, Negrao-Correa DA, Adams LS. 35.  1992. Rapid expulsion of Trichinella spiralis in adult rats mediated by monoclonal antibodies of distinct IgG isotypes. Immunology 75:3520–27 [Google Scholar]
  36. Appleton JA, McGregor DD. 36.  1987. Characterization of the immune mediator of rapid expulsion of Trichinella spiralis in suckling rats. Immunology 62:3477–84 [Google Scholar]
  37. Grencis RK, Wakelin D. 37.  1982. Short lived, dividing cells mediate adoptive transfer of immunity to Trichinella spiralis in mice. I. Availability of cells in primary and secondary infections in relation to cellular changes in the mesenteric lymph node. Immunology 46:2443–50 [Google Scholar]
  38. Alizadeh H, Wakelin D. 38.  1982. Genetic factors controlling the intestinal mast cell response in mice infected with Trichinella spiralis. Clin. Exp. Immunol. 49:2331–37 [Google Scholar]
  39. Woodbury RG, Miller HR, Huntley JF, Newlands GF, Palliser AC, Wakelin D. 39.  1984. Mucosal mast cells are functionally active during spontaneous expulsion of intestinal nematode infections in rat. Nature 312:5993450–52 [Google Scholar]
  40. McKenzie GJ, Bancroft A, Grencis RK, McKenzie AN. 40.  1998. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr. Biol. 8:6339–42 [Google Scholar]
  41. Hasnain SZ, Wang H, Ghia JE, Haq N, Deng Y. 41.  et al. 2010. Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection. Gastroenterology 138:51763–71 [Google Scholar]
  42. Hasnain SZ, Evans CM, Roy M, Gallagher AL, Kindrachuk KN. 42.  et al. 2011. Muc5ac: a critical component mediating the rejection of enteric nematodes. J. Exp. Med. 208:5893–900 [Google Scholar]
  43. Jones VE, Edwards AJ, Ogilvie BM. 43.  1970. The circulating immunoglobulins involved in protective immunity to the intestinal stage of Nippostrongylus brasiliensis in the rat. Immunology 18:5621–33 [Google Scholar]
  44. Love RJ, Ogilvie BM, McLaren DJ. 44.  1976. The immune mechanism which expels the intestinal stage of Trichinella spiralis from rats. Immunology 30:17–15 [Google Scholar]
  45. Jungery M, Ogilvie BM. 45.  1982. Antibody response to stage-specific Trichinella spiralis surface antigens in strong and weak responder mouse strains. J. Immunol. 129:2839–43 [Google Scholar]
  46. Behnke JM, Parish HA. 46.  1979. Expulsion of Nematospiroides dubius from the intestine of mice treated with immune serum. Parasite Immunol. 1:113–26 [Google Scholar]
  47. Pritchard DI, Williams DJ, Behnke JM, Lee TD. 47.  1983. The role of IgG1 hypergammaglobulinaemia in immunity to the gastrointestinal nematode Nematospiroides dubius. The immunochemical purification, antigen-specificity and in vivo anti-parasite effect of IgG1 from immune serum. Immunology 49:2353–65 [Google Scholar]
  48. McCoy KD, Stoel M, Stettler R, Merky P, Fink K. 48.  et al. 2008. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4:4362–73 [Google Scholar]
  49. Harris NL, Pleass R, Behnke JM. 49.  2014. Understanding the role of antibodies in murine infections with Heligmosomoides (polygyrus) bakeri: 35 years ago, now and 35 years ahead. Parasite Immunol. 36:3115–24 [Google Scholar]
  50. Esser-von Bieren J, Mosconi I, Guiet R, Piersgilli A, Volpe B. 50.  et al. 2013. Antibodies trap tissue migrating helminth larvae and prevent tissue damage by driving IL-4Rα-independent alternative differentiation of macrophages. PLOS Pathog. 9:11e1003771 [Google Scholar]
  51. Filbey KJ, Grainger JR, Smith KA, Boon L, van Rooijen N. 51.  et al. 2014. Innate and adaptive type 2 immune cell responses in genetically controlled resistance to intestinal helminth infection. Immunol. Cell Biol. 92:436–48 [Google Scholar]
  52. Harris N, Gause WC. 52.  2011. To B or not to B: B cells and the Th2-type immune response to helminths. Trends Immunol. 32:280–88 [Google Scholar]
  53. Else KJ, Grencis RK. 53.  1996. Antibody-independent effector mechanisms in resistance to the intestinal nematode parasite Trichuris muris. Infect. Immun. 64:82950–54 [Google Scholar]
  54. Miller HR, Huntley JF, Wallace GR. 54.  1981. Immune exclusion and mucus trapping during the rapid expulsion of Nippostrongylus brasiliensis from primed rats. Immunology 44:2419–29 [Google Scholar]
  55. Spits H, Artis D, Colonna M, Diefenbach A. Santo JP. 55. , Di et al. 2013. Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:2145–49 [Google Scholar]
  56. Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M. 56.  et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464:72931367–70 [Google Scholar]
  57. Price AE, Liang HE, Sullivan BM, Reinhardt RL, Eisley CJ. 57.  et al. 2010. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. PNAS 107:2511489–94 [Google Scholar]
  58. Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T. 58.  et al. 2010. Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells. Nature 463:7280540–44 [Google Scholar]
  59. Saenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban JF Jr. 59.  2010. IL25 elicits a multipotent progenitor cell population that promotes TH2 cytokine responses. Nature 464:72931362–66 [Google Scholar]
  60. Turner JE, Morrison PJ, Wilhelm C, Wilson M, Ahlfors H. 60.  et al. 2013. IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J. Exp. Med. 210:132951–65 [Google Scholar]
  61. Hepworth MR, Grencis RK. 61.  2009. Disruption of Th2 immunity results in a gender-specific expansion of IL-13 producing accessory NK cells during helminth infection. J. Immunol. 183:63906–14 [Google Scholar]
  62. Inagaki-Ohara K, Sakamoto Y, Dohi T, Smith AL. 62.  2011. γδ T cells play a protective role during infection with Nippostrongylus brasiliensis by promoting goblet cell function in the small intestine. Immunology 134:4448–58 [Google Scholar]
  63. Hwang YY, McKenzie AN. 63.  2013. Innate lymphoid cells in immunity and disease. Adv. Exp. Med. Biol. 785:9–26 [Google Scholar]
  64. Saenz SA, Noti M, Artis D. 64.  2010. Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends Immunol. 31:11407–13 [Google Scholar]
  65. Neill DR, McKenzie AN. 65.  2011. Nuocytes and beyond: new insights into helminth expulsion. Trends Parasitol. 27:5214–21 [Google Scholar]
  66. Wong SH, Walker JA, Jolin HE, Drynan LF, Hams E. 66.  et al. 2012. Transcription factor RORα is critical for nuocyte development. Nat. Immunol. 13:3229–36 [Google Scholar]
  67. Zaiss MM, Maslowski KM, Mosconi I, Guenat N, Marsland BJ, Harris NL. 67.  2013. IL-1β suppresses innate IL-25 and IL-33 production and maintains helminth chronicity. PLOS Pathog. 9:8e1003531 [Google Scholar]
  68. Kang Z, Swaidani S, Yin W, Wang C, Barlow JL. 68.  et al. 2012. Epithelial cell-specific Act1 adaptor mediates interleukin-25-dependent helminth expulsion through expansion of Linc-Kit+ innate cell population. Immunity 36:5821–33 [Google Scholar]
  69. Zaph C, Troy AE, Taylor BC, Berman-Booty LD, Guild KJ. 69.  et al. 2007. Epithelial-cell-intrinsic IKK-β expression regulates intestinal immune homeostasis. Nature 446:7135552–56 [Google Scholar]
  70. Wills-Karp M, Rani R, Dienger K, Lewkowich I, Fox JG. 70.  et al. 2012. Trefoil factor 2 rapidly induces interleukin 33 to promote type 2 immunity during allergic asthma and hookworm infection. J. Exp. Med. 209:3607–22 [Google Scholar]
  71. Klose CS, Flach M, Möhle L, Rogell L, Hoyler T. 71.  et al. 2014. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157:2340–56 [Google Scholar]
  72. Yagi R, Zhong C, Northrup DL, Yu F, Bouladoux N. 72.  et al. 2014. The transcription factor GATA3 is critical for the development of all IL-7Rα-expressing innate lymphoid cells. Immunity 40:3378–88 [Google Scholar]
  73. Faulkner H, Renauld JC, Van Snick J, Grencis RK. 73.  1998. Interleukin-9 enhances resistance to the intestinal nematode Trichuris muris. Infect. Immun. 66:83832–40 [Google Scholar]
  74. Faulkner H, Humphreys N, Renauld JC, Van Snick J, Grencis R. 74.  1997. Interleukin-9 is involved in host protective immunity to intestinal nematode infection. Eur. J. Immunol. 27:102536–40 [Google Scholar]
  75. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E. 75.  et al. 2005. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23:5479–90 [Google Scholar]
  76. Humphreys NE, Xu D, Hepworth MR, Liew FY, Grencis RK. 76.  2008. IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J. Immunol. 180:42443–49 [Google Scholar]
  77. Yasuda K, Muto T, Kawagoe T, Matsumoto M, Sasaki Y. 77.  et al. 2012. Contribution of IL-33-activated type II innate lymphoid cells to pulmonary eosinophilia in intestinal nematode-infected mice. PNAS 109:93451–56 [Google Scholar]
  78. Haraldsen G, Balogh J, Pollheimer J, Sponheim J, Küchler AM. 78.  2009. Interleukin-33—cytokine of dual function or novel alarmin?. Trends Immunol. 30:5227–33 [Google Scholar]
  79. Townsend MJ, Fallon PG, Matthews DJ, Jolin HE, McKenzie AN. 79.  2000. T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J. Exp. Med. 191:61069–76 [Google Scholar]
  80. Hung LY, Lewkowich IP, Dawson LA, Downey J, Yang Y. 80.  et al. 2013. IL-33 drives biphasic IL-13 production for noncanonical type 2 immunity against hookworms. PNAS 110:1282–87 [Google Scholar]
  81. Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A. 81.  et al. 2006. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J. Exp. Med. 203:41105–16 [Google Scholar]
  82. Owyang AM, Zaph C, Wilson EH, Guild KJ, McClanahan T. 82.  et al. 2006. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J. Exp. Med. 203:4843–49 [Google Scholar]
  83. Hepworth MR, Monticelli LA, Fung TC, Ziegler CG, Grunberg S. 83.  et al. 2013. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498:7452113–17 [Google Scholar]
  84. Spencer SP, Wilhelm C, Yang Q, Hall JA, Bouladoux N. 84.  et al. 2014. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 343:6169432–37 [Google Scholar]
  85. Oliphant CJ, Hwang YY, Walker JA, Salimi M, Wong SH. 85.  et al. 2014. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4+ T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 41:2283–95 [Google Scholar]
  86. Ziegler SF, Artis D. 86.  2010. Sensing the outside world: TSLP regulates barrier immunity. Nat. Immunol. 11:4289–93 [Google Scholar]
  87. Taylor BC, Zaph C, Troy AE, Du Y, Guild KJ. 87.  et al. 2009. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J. Exp. Med. 206:3655–67 [Google Scholar]
  88. Massacand JC, Stettler RC, Meier R, Humphreys NE, Grencis RK. 88.  et al. 2009. Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function. PNAS 106:3313968–73 [Google Scholar]
  89. Klementowicz JE, Travis MA, Grencis RK. 89.  2012. Trichuris muris: a model of gastrointestinal parasite infection. Semin. Immunopathol. 34:6815–28 [Google Scholar]
  90. Cliffe LJ, Grencis RK. 90.  2004. The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection. Adv. Parasitol. 57:255–307 [Google Scholar]
  91. Persson EK, Scott CL, Mowat AM, Agace WW. 91.  2013. Dendritic cell subsets in the intestinal lamina propria: ontogeny and function. Eur. J. Immunol. 43:123098–107 [Google Scholar]
  92. Bekiaris V, Persson EK, Agace WW. 92.  2014. Intestinal dendritic cells in the regulation of mucosal immunity. Immunol. Rev. 260:186–101 [Google Scholar]
  93. Balic A, Smith KA, Harcus Y, Maizels RM. 93.  2009. Dynamics of CD11c+ dendritic cell subsets in lymph nodes draining the site of intestinal nematode infection. Immunol. Lett. 127:168–75 [Google Scholar]
  94. Gao Y, Nish SA, Jiang R, Hou L, Licona-Limón P. 94.  et al. 2013. Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39:4722–32 [Google Scholar]
  95. Smith KA, Hochweller K, Hämmerling GJ, Boon L, MacDonald AS, Maizels RM. 95.  2011. Chronic helminth infection promotes immune regulation in vivo through dominance of CD11cloCD103 dendritic cells. J. Immunol. 186:127098–109 [Google Scholar]
  96. Cruickshank SM, Deschoolmeester ML, Svensson M, Howell G, Bazakou A. 96.  et al. 2009. Rapid dendritic cell mobilization to the large intestinal epithelium is associated with resistance to Trichuris muris infection. J. Immunol. 182:53055–62 [Google Scholar]
  97. Worthington JJ, Klementowicz JE, Rahman S, Czajkowska BI, Smedley C. 97.  et al. 2013. Loss of the TGFβ-activating integrin αvβ8 on dendritic cells protects mice from chronic intestinal parasitic infection via control of type 2 immunity. PLOS Pathog. 9:10e1003675 [Google Scholar]
  98. Siracusa MC, Perrigoue JG, Comeau MR, Artis D. 98.  2010. New paradigms in basophil development, regulation and function. Immunol. Cell Biol. 88:3275–84 [Google Scholar]
  99. Voehringer D. 99.  2011. Basophils in immune responses against helminths. Microbes Infect. 13:11881–87 [Google Scholar]
  100. McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V. 100.  et al. 2012. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 483:7389345–49 [Google Scholar]
  101. Shan M, Gentile M, Yeiser JR, Walland AC, Bornstein VU. 101.  et al. 2013. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 342:6157447–53 [Google Scholar]
  102. Hepworth MR, Daniłowicz-Luebert E, Rausch S, Metz M, Klotz C. 102.  et al. 2012. Mast cells orchestrate type 2 immunity to helminths through regulation of tissue-derived cytokines. PNAS 109:176644–49 [Google Scholar]
  103. Svensson M, Bell L, Little MC, DeSchoolmeester M, Locksley RM, Else KJ. 103.  2011. Accumulation of eosinophils in intestine-draining mesenteric lymph nodes occurs after Trichuris muris infection. Parasite Immunol. 33:11–11 [Google Scholar]
  104. Nussbaum JC, Van Dyken SJ, von Moltke J, Cheng LE, Mohapatra A. 104.  et al. 2013. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502:7470245–48 [Google Scholar]
  105. Zigmond E, Jung S. 105.  2013. Intestinal macrophages: well educated exceptions from the rule. Trends Immunol. 34:4162–68 [Google Scholar]
  106. Bain CC, Mowat AM. 106.  2014. Macrophages in intestinal homeostasis and inflammation. Immunol. Rev. 260:1102–17 [Google Scholar]
  107. Reyes JL, Terrazas LI. 107.  2007. The divergent roles of alternatively activated macrophages in helminthic infections. Parasite Immunol 29:12609–19 [Google Scholar]
  108. Jenkins SJ, Allen JE. 108.  2010. Similarity and diversity in macrophage activation by nematodes, trematodes, and cestodes. J. Biomed. Biotechnol 2010:262609 doi: 10.1155/2010/262609 [Google Scholar]
  109. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD. 109.  et al. 2011. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332:60351284–88 [Google Scholar]
  110. Jenkins SJ, Ruckerl D, Thomas GD, Hewitson JP, Duncan S. 110.  et al. 2013. IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J. Exp. Med. 210:112477–91 [Google Scholar]
  111. Davies LC, Jenkins SJ, Allen JE, Taylor PR. 111.  2013. Tissue-resident macrophages. Nat. Immunol. 14:10986–95 [Google Scholar]
  112. Duffield JS, Lupher M, Thannickal VJ, Wynn TA. 112.  2013. Host responses in tissue repair and fibrosis. Annu. Rev. Pathol. Mech. Dis. 8:241–76 [Google Scholar]
  113. Else KJ, Finkelman FD. 113.  1998. Intestinal nematode parasites, cytokines and effector mechanisms. Int. J. Parasitol. 28:81145–58 [Google Scholar]
  114. Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC. 114.  et al. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15:505–33 [Google Scholar]
  115. Gause WC, Ekkens M, Nguyen D, Mitro V, Liu Q. 115.  et al. 1999. The development of CD4+ T effector cells during the type 2 immune response. Immunol. Res. 20:155–65 [Google Scholar]
  116. Bell LV, Else KJ. 116.  2008. Mechanisms of leucocyte recruitment to the inflamed large intestine: redundancy in integrin and addressin usage. Parasite Immunol. 30:3163–70 [Google Scholar]
  117. Humphreys NE, Worthington JJ, Little MC, Rice EJ, Grencis RK. 117.  2004. The role of CD8+ cells in the establishment and maintenance of a Trichuris muris infection. Parasite Immunol. 26:4187–96 [Google Scholar]
  118. Miller HR. 118.  1987. Gastrointestinal mucus, a medium for survival and for elimination of parasitic nematodes and protozoa. Parasitology 94:Suppl.S77–100 [Google Scholar]
  119. McGuckin MA, Lindén SK, Sutton P, Florin TH. 119.  2011. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9:4265–78 [Google Scholar]
  120. Hansson GC. 120.  2012. Role of mucus layers in gut infection and inflammation. Curr. Opin. Microbiol. 15:157–62 [Google Scholar]
  121. Johansson ME, Sjovall H, Hansson GC. 121.  2013. The gastrointestinal mucus system in health and disease. Nat. Rev. Gastroenterol. Hepatol. 10:6352–61 [Google Scholar]
  122. Corfield AP. 122.  2014. Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim. Biophys. Acta 1850:236–52 [Google Scholar]
  123. Turner JE, Stockinger B, Helmby H. 123.  2013. IL-22 mediates goblet cell hyperplasia and worm expulsion in intestinal helminth infection. PLOS Pathog. 9:10e1003698 [Google Scholar]
  124. Miller HR, Nawa Y, Parish CR. 124.  1979. Intestinal goblet cell differentiation in Nippostrongylus-infected rats after transfer of fractionated thoracic duct lymphocytes. Int. Arch. Allergy Appl. Immunol. 59:3281–85 [Google Scholar]
  125. Hasnain SZ, McGuckin MA, Grencis RK, Thornton DJ. 125.  2012. Serine protease(s) secreted by the nematode Trichuris muris degrade the mucus barrier. PLOS Negl. Trop. Dis. 6:10e1856 [Google Scholar]
  126. Foth BJ, Tsai IJ, Reid AJ, Bancroft AJ, Nichol S. 126.  et al. 2014. Whipworm genome and dual-species transcriptome analyses provide molecular insights into an intimate host-parasite interaction. Nat. Genet 46:7693–700 [Google Scholar]
  127. Jex AR, Nejsum P, Schwarz EM, Hu L, Young ND. 127.  et al. 2014. Genome and transcriptome of the porcine whipworm Trichuris suis. Nat. Genet. 46:7701–6 [Google Scholar]
  128. Herbert DR, Yang JQ, Hogan SP, Groschwitz K, Khodoun M. 128.  et al. 2009. Intestinal epithelial cell secretion of RELM-β protects against gastrointestinal worm infection. J. Exp. Med. 206:132947–57 [Google Scholar]
  129. Nair MG, Guild KJ, Du Y, Zaph C, Yancopoulos GD. 129.  et al. 2008. Goblet cell-derived resistin-like molecule β augments CD4+ T cell production of IFN-γ and infection-induced intestinal inflammation. J. Immunol. 181:74709–15 [Google Scholar]
  130. Khan WI, Richard M, Akiho H, Blennerhasset PA, Humphreys NE. 130.  et al. 2003. Modulation of intestinal muscle contraction by interleukin-9 (IL-9) or IL-9 neutralization: correlation with worm expulsion in murine nematode infections. Infect. Immun. 71:52430–38 [Google Scholar]
  131. Bell LV, Else KJ. 131.  2011. Regulation of colonic epithelial cell turnover by IDO contributes to the innate susceptibility of SCID mice to Trichuris muris infection. Parasite Immunol. 33:4244–49 [Google Scholar]
  132. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK. 132.  2005. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308:57271463–65 [Google Scholar]
  133. Zaiss DM, Yang L, Shah PR, Kobie JJ, Urban JF, Mosmann TR. 133.  2006. Amphiregulin, a TH2 cytokine enhancing resistance to nematodes. Science 314:58061746 [Google Scholar]
  134. Alizadeh H, Urban JF Jr, Katona IM, Finkelman FD. 134.  1986. Cells containing IgE in the intestinal mucosa of mice infected with the nematode parasite Trichinella spiralis are predominantly of a mast cell lineage. J. Immunol. 137:82555–60 [Google Scholar]
  135. Jarrett EE, Miller HR. 135.  1982. Production and activities of IgE in helminth infection. Prog. Allergy 31:178–233 [Google Scholar]
  136. Pritchard DI. 136.  1993. Immunity to helminths: Is too much IgE parasite- rather than host-protective?. Parasite Immunol. 15:15–9 [Google Scholar]
  137. Fitzsimmons CM, Falcone FH, Dunne DW. 137.  2014. Helminth allergens, parasite-specific IgE, and its protective role in human immunity. Front. Immunol. 5:61 [Google Scholar]
  138. Betts CJ, Else KJ. 138.  1999. Mast cells, eosinophils and antibody-mediated cellular cytotoxicity are not critical in resistance to Trichuris muris. Parasite Immunol. 21:145–52 [Google Scholar]
  139. Crowle PK, Reed ND. 139.  1981. Rejection of the intestinal parasite Nippostrongylus brasiliensis by mast cell-deficient W/Wv anemic mice. Infect. Immun. 33:154–58 [Google Scholar]
  140. Hayes KS, Bancroft AJ, Grencis RK. 140.  2004. Immune-mediated regulation of chronic intestinal nematode infection. Immunol. Rev. 201:75–88 [Google Scholar]
  141. Pennock JL, Grencis RK. 141.  2004. In vivo exit of c-kit+/CD49dhi/β7+ mucosal mast cell precursors from the bone marrow following infection with the intestinal nematode Trichinella spiralis. Blood 103:72655–60 [Google Scholar]
  142. Lantz CS, Boesiger J, Song CH, Mach N, Kobayashi T. 142.  et al. 1998. Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites. Nature 392:667190–93 [Google Scholar]
  143. Donaldson LE, Schmitt E, Huntley JF, Newlands GF, Grencis RK. 143.  1996. A critical role for stem cell factor and c-kit in host protective immunity to an intestinal helminth. Int. Immunol. 8:4559–67 [Google Scholar]
  144. Knight PA, Wright SH, Lawrence CE, Paterson YY, Miller HR. 144.  2000. Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. J. Exp. Med. 192:121849–56 [Google Scholar]
  145. McDermott JR, Bartram RE, Knight PA, Miller HR, Garrod DR, Grencis RK. 145.  2003. Mast cells disrupt epithelial barrier function during enteric nematode infection. PNAS 100:137761–66 [Google Scholar]
  146. Gurish MF, Bryce PJ, Tao H, Kisselgof AB, Thornton EM. 146.  et al. 2004. IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. J. Immunol. 172:21139–45 [Google Scholar]
  147. Obata-Ninomiya K, Ishiwata K, Tsutsui H, Nei Y, Yoshikawa S. 147.  et al. 2013. The skin is an important bulwark of acquired immunity against intestinal helminths. J. Exp. Med. 210:122583–95 [Google Scholar]
  148. Yasuda K, Matsumoto M, Nakanishi K. 148.  2014. Importance of both innate immunity and acquired immunity for rapid expulsion of S. venezuelensis. Front. Immunol. 5:118 [Google Scholar]
  149. Thawer SG, Horsnell WG, Darby M, Hoving JC, Dewals B. 149.  et al. 2014. Lung-resident CD4+ T cells are sufficient for IL-4Rα-dependent recall immunity to Nippostrongylus brasiliensis infection. Mucosal Immunol. 7:2239–48 [Google Scholar]
  150. Chen F, Wu W, Millman A, Craft JF, Chen E. 150.  et al. 2014. Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat. Immunol. 15:10938–46 [Google Scholar]
  151. Sutherland TE, Logan N, Rückerl D, Humbles AA, Allan SM. 151.  et al. 2014. Chitinase-like proteins promote IL-17-mediated neutrophilia in a tradeoff between nematode killing and host damage. Nat. Immunol. 15:121116–25 [Google Scholar]
  152. Marsland BJ, Kurrer M, Reissmann R, Harris NL, Kopf M. 152.  2008. Nippostrongylus brasiliensis infection leads to the development of emphysema associated with the induction of alternatively activated macrophages. Eur. J. Immunol. 38:2479–88 [Google Scholar]
  153. Knott ML, Matthaei KI, Foster PS, Dent LA. 153.  2009. The roles of eotaxin and the STAT6 signalling pathway in eosinophil recruitment and host resistance to the nematodes Nippostrongylus brasiliensis and Heligmosomoides bakeri. Mol. Immunol. 46:132714–22 [Google Scholar]
  154. Gebreselassie NG, Moorhead AR, Fabre V, Gagliardo LF, Lee NA. 154.  et al. 2012. Eosinophils preserve parasitic nematode larvae by regulating local immunity. J. Immunol. 188:1417–25 [Google Scholar]
  155. Patnode ML, Bando JK, Krummel MF, Locksley RM, Rosen SD. 155.  2014. Leukotriene B4 amplifies eosinophil accumulation in response to nematodes. J. Exp. Med. 211:71281–88 [Google Scholar]
  156. Moqbel R, King SJ, MacDonald AJ, Miller HR, Cromwell O. 156.  et al. 1986. Enteral and systemic release of leukotrienes during anaphylaxis of Nippostrongylus brasiliensis-primed rats. J. Immunol. 137:1296–301 [Google Scholar]
  157. Bowcutt R, Bell LV, Little M, Wilson J, Booth C. 157.  et al. 2011. Arginase-1-expressing macrophages are dispensable for resistance to infection with the gastrointestinal helminth Trichuris muris. Parasite Immunol. 33:7411–20 [Google Scholar]
  158. Anthony RM, Urban JF Jr, Alem F, Hamed HA, Rozo CT. 158.  et al. 2006. Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12:8955–60 [Google Scholar]
  159. Palm NW, Rosenstein RK, Medzhitov R. 159.  2012. Allergic host defences. Nature 484:7395465–72 [Google Scholar]
  160. Maizels RM, Bundy DA, Selkirk ME, Smith DF, Anderson RM. 160.  1993. Immunological modulation and evasion by helminth parasites in human populations. Nature 365:6449797–805 [Google Scholar]
  161. Fitzsimmons CM, Jones FM, Pinot de Moira A, Protasio AV, Khalife J. 161.  et al. 2012. Progressive cross-reactivity in IgE responses: an explanation for the slow development of human immunity to schistosomiasis?. Infect. Immun. 80:124264–70 [Google Scholar]
  162. Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA. 162.  1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349:6306243–45 [Google Scholar]
  163. Hopkin J. 163.  2009. Immune and genetic aspects of asthma, allergy and parasitic worm infections: evolutionary links. Parasite Immunol. 31:5267–73 [Google Scholar]
  164. Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM. 164.  et al. 2004. T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J. Infect. Dis. 190:101804–11 [Google Scholar]
  165. Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM. 165.  et al. 2004. Cytokine response profiles predict species-specific infection patterns in human GI nematodes. Int. J. Parasitol. 34:111237–44 [Google Scholar]
  166. Cooper PJ. 166.  2009. Mucosal immunology of geohelminth infections in humans. Mucosal Immunol. 2:4288–99 [Google Scholar]
  167. McSorley HJ, Loukas A. 167.  2010. The immunology of human hookworm infections. Parasite Immunol. 32:8549–59 [Google Scholar]
  168. Quinnell RJ, Woolhouse ME, Walsh EA, Pritchard DI. 168.  1995. Immunoepidemiology of human necatoriasis: correlations between antibody responses and parasite burdens. Parasite Immunol. 17:6313–18 [Google Scholar]
  169. Diemert DJ, Pinto AG, Freire J, Jariwala A, Santiago H. 169.  et al. 2012. Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. J. Allergy Clin. Immunol. 130:1169–76.e6 [Google Scholar]
  170. Tang YT, Gao X, Rosa BA, Abubucker S, Hallsworth-Pepin K. 170.  et al. 2014. Genome of the human hookworm Necator americanus. Nat. Genet. 46:3261–69 [Google Scholar]
  171. Wright V, Bickle Q. 171.  2005. Immune responses following experimental human hookworm infection. Clin. Exp. Immunol. 142:2398–403 [Google Scholar]
  172. Gaze S, McSorley HJ, Daveson J, Jones D, Bethony JM. 172.  et al. 2012. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLOS Pathog. 8:2e1002520 [Google Scholar]
  173. Broadhurst MJ, Leung JM, Kashyap V, McCune JM, Mahadevan U. 173.  et al. 2010. IL-22+ CD4+ T cells are associated with therapeutic Trichuris trichiura infection in an ulcerative colitis patient. Sci. Transl. Med. 2:6060ra88 [Google Scholar]
  174. Bancroft AJ, Else KJ, Humphreys NE, Grencis RK. 174.  et al. 2001. The effect of challenge and trickle Trichuris muris infections on the polarisation of the immune response. Int. J. Parasitol. 31:141627–37 [Google Scholar]
  175. Barger IA, Le Jambre LF, Georgi JR, Davies HI. 175.  1985. Regulation of Haemonchus contortus populations in sheep exposed to continuous infection. Int. J. Parasitol. 15:5529–33 [Google Scholar]
  176. Barnes EH, Dobson RJ. 176.  1990. Population dynamics of Trichostrongylus colubriformis in sheep: model to predict the worm population over time as a function of infection rate and host age. Int. J. Parasitol. 20:3365–73 [Google Scholar]
  177. Meeusen EN, Balic A, Bowles V. 177.  2005. Cells, cytokines and other molecules associated with rejection of gastrointestinal nematode parasites. Vet. Immunol. Immunopathol. 108:1–2121–25 [Google Scholar]
  178. McClure SJ, Davey RJ, Lloyd JB, Emery DL. 178.  1995. Depletion of IFN-γ, CD8+ or Tcrγδ+ cells in vivo during primary infection with an enteric parasite (Trichostrongylus colubriformis) enhances protective immunity. Immunol. Cell Biol. 73:6552–55 [Google Scholar]
  179. Finlay CM, Walsh KP, Mills KH. 179.  2014. Induction of regulatory cells by helminth parasites: exploitation for the treatment of inflammatory diseases. Immunol. Rev. 259:1206–30 [Google Scholar]
  180. Smits HH, Yazdanbakhsh M. 180.  2007. Chronic helminth infections modulate allergen-specific immune responses: protection against development of allergic disorders?. Ann. Med. 39:6428–39 [Google Scholar]
  181. Rausch S, Huehn J, Loddenkemper C, Hepworth MR, Klotz C. 181.  et al. 2009. Establishment of nematode infection despite increased Th2 responses and immunopathology after selective depletion of Foxp3+ cells. Eur. J. Immunol. 39:113066–77 [Google Scholar]
  182. Finney CA, Taylor MD, Wilson MS, Maizels RM. 182.  2007. Expansion and activation of CD4+CD25+ regulatory T cells in Heligmosomoides polygyrus infection. Eur. J. Immunol. 37:71874–86 [Google Scholar]
  183. Redpath SA, van der Werf N, Cervera AM, MacDonald AS, Gray D. 183.  et al. 2013. ICOS controls Foxp3+ regulatory T-cell expansion, maintenance and IL-10 production during helminth infection. Eur. J. Immunol. 43:3705–15 [Google Scholar]
  184. Rausch S, Huehn J, Kirchhoff D, Rzepecka J, Schnoeller C. 184.  et al. 2008. Functional analysis of effector and regulatory T cells in a parasitic nematode infection. Infect. Immun. 76:51908–19 [Google Scholar]
  185. Grainger JR, Smith KA, Hewitson JP, McSorley HJ, Harcus Y. 185.  et al. 2010. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J. Exp. Med. 207:112331–41 [Google Scholar]
  186. Smith KA, Maizels RM. 186.  2014. IL-6 controls susceptibility to helminth infection by impeding Th2 responsiveness and altering the Treg phenotype in vivo. Eur. J. Immunol. 44:1150–61 [Google Scholar]
  187. D'Elia R, Behnke JM, Bradley JE, Else KJ. 187.  2009. Regulatory T cells: a role in the control of helminth-driven intestinal pathology and worm survival. J. Immunol. 182:42340–48 [Google Scholar]
  188. Blankenhaus B, Klemm U, Eschbach ML, Sparwasser T. 188.  et al. 2011. Strongyloides ratti infection induces expansion of Foxp3+ regulatory T cells that interfere with immune response and parasite clearance in BALB/c mice. J. Immunol. 186:74295–305 [Google Scholar]
  189. Ince MN, Elliott DE, Setiawan T, Metwali A, Blum A. 189.  et al. 2009. Role of T cell TGF-β signaling in intestinal cytokine responses and helminthic immune modulation. Eur. J. Immunol. 39:71870–78 [Google Scholar]
  190. Bollrath J, Powrie FM. 190.  2013. Controlling the frontier: regulatory T-cells and intestinal homeostasis. Semin. Immunol. 25:5352–57 [Google Scholar]
  191. Schopf LR, Hoffmann KF, Cheever AW, Urban JF Jr, Wynn TA. 191.  et al. 2002. IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J. Immunol. 168:52383–92 [Google Scholar]
  192. Fasnacht N, Greweling MC, Bollati-Fogolín M, Schippers A, Müller W. 192.  2009. T-cell-specific deletion of gp130 renders the highly susceptible IL-10-deficient mouse resistant to intestinal nematode infection. Eur. J. Immunol. 39:82173–83 [Google Scholar]
  193. Levison SE, McLaughlin JT, Zeef LA, Fisher P, Grencis RK, Pennock JL. 193.  2010. Colonic transcriptional profiling in resistance and susceptibility to trichuriasis: phenotyping a chronic colitis and lessons for iatrogenic helminthosis. Inflamm. Bowel Dis. 16:122065–79 [Google Scholar]
  194. Kominsky DJ, Campbell EL, Ehrentraut SF, Wilson KE, Kelly CJ. 194.  et al. 2014. IFN-γ-mediated induction of an apical IL-10 receptor on polarized intestinal epithelia. J. Immunol. 192:31267–76 [Google Scholar]
  195. Zaccone P, Fehervari Z, Phillips JM, Dunne DW, Cooke A. 195.  2006. Parasitic worms and inflammatory diseases. Parasite Immunol. 28:10515–23 [Google Scholar]
  196. Elliott DE, Weinstock JV. 196.  2012. Helminth-host immunological interactions: prevention and control of immune-mediated diseases. Ann. N.Y. Acad. Sci. 1247:83–96 [Google Scholar]
  197. Bancroft AJ, Hayes KS, Grencis RK. 197.  2012. Life on the edge: the balance between macrofauna, microflora and host immunity. Trends Parasitol. 28:393–98 [Google Scholar]
  198. Honda K, Littman DR. 198.  2012. The microbiome in infectious disease and inflammation. Annu. Rev. Immunol. 30:759–95 [Google Scholar]
  199. Walk ST, Blum AM, Ewing SA, Weinstock JV, Young VB. 199.  2010. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm. Bowel Dis. 16:111841–49 [Google Scholar]
  200. Rausch S, Held J, Fischer A, Heimesaat MM, Kühl AA. 200.  et al. 2013. Small intestinal nematode infection of mice is associated with increased enterobacterial loads alongside the intestinal tract. PLOS ONE 8:9e74026 [Google Scholar]
  201. Li RW, Wu S, Li W, Navarro K, Couch RD. 201.  et al. 2012. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect. Immun. 80:62150–57 [Google Scholar]
  202. Wu S, Li RW, Li W, Beshah E, Dawson HD, Urban JF Jr. 202.  2012. Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLOS ONE 7:4e35470 [Google Scholar]
  203. Cooper P, Walker AW, Reyes J, Chico M, Salter SJ. 203.  et al. 2013. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLOS ONE 8:10e76573 [Google Scholar]
  204. Lee SC, Tang MS, Lim YA, Choy SH, Kurtz ZD. 204.  et al. 2014. Helminth colonization is associated with increased diversity of the gut microbiota. PLOS Negl. Trop. Dis. 8:5e2880 [Google Scholar]
  205. Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM. 205.  et al. 2012. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLOS Pathog. 8:11e1003000 [Google Scholar]
  206. Hayes KS, Bancroft AJ, Goldrick M, Portsmouth C, Roberts IS, Grencis RK. 206.  2010. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328:59841391–94 [Google Scholar]
  207. Everts B, Pearce EJ. 207.  2014. Metabolic control of dendritic cell activation and function: recent advances and clinical implications. Front. Immunol. 5:203 [Google Scholar]
  208. Pearce EL, Poffenberger MC, Chang CH, Jones RG. 208.  2013. Fueling immunity: insights into metabolism and lymphocyte function. Science 342:61551242454 [Google Scholar]
  209. Worthington JJ, Samuelson LC, Grencis RK, McLaughlin JT. 209.  2013. Adaptive immunity alters distinct host feeding pathways during nematode induced inflammation, a novel mechanism in parasite expulsion. PLOS Pathog. 9:1e1003122 [Google Scholar]
  210. McDermott JR, Leslie FC, D'Amato M, Thompson DG, Grencis RK, McLaughlin JT. 210.  2006. Immune control of food intake: enteroendocrine cells are regulated by CD4+ T lymphocytes during small intestinal inflammation. Gut 55:4492–97 [Google Scholar]
/content/journals/10.1146/annurev-immunol-032713-120218
Loading
/content/journals/10.1146/annurev-immunol-032713-120218
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error