MicroRNA-mediated regulation of immune responses to intestinal helminth infections

Parasite Immunology

Volumn 39, Issue 2, 2017, Pages

  Entwistle, L J ^a   Wilson, M S ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

Dendritic cell; Heligmosomoides polygyrus; Nippostrongylus brasiliensis; T lymphocyte; Th2 cell; Trichinella spiralis; Trichuris spp.

Indexed keywords

MICRORNA;

ADAPTIVE IMMUNITY; APOPTOSIS; CELL DIFFERENTIATION; DENDRITIC CELL; ENTEROENDOCRINE CELL; GENE EXPRESSION; HELIGMOSOMOIDES POLYGYRUS; HELMINTHIASIS; HUMAN; IMMUNOREGULATION; INTESTINE INFECTION; MUCOSAL IMMUNITY; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PARASITE IMMUNITY; PRIORITY JOURNAL; REVIEW; RNA TRANSLATION; TH2 CELL; TRICHINELLA SPIRALIS; TRICHURIS MURIS; ANIMAL; CD4+ T LYMPHOCYTE; DISEASE MODEL; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; MOUSE; NIPPOSTRONGYLUS; PARASITOLOGY; STRONGYLE INFECTION; TRICHINOSIS; TRICHURIASIS; TRICHURIS;

ADAPTIVE IMMUNITY; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HELMINTHIASIS; INTESTINAL DISEASES, PARASITIC; INTESTINAL MUCOSA; MICE; MICRORNAS; NEMATOSPIROIDES DUBIUS; NIPPOSTRONGYLUS; STRONGYLIDA INFECTIONS; TRICHINELLA SPIRALIS; TRICHINELLOSIS; TRICHURIASIS; TRICHURIS;

EID: 85015333029     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12406     Document Type: Review

References (137)

1. Bethony J, Brooker S, Albonico M, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–1532.
2. Hotez PJ, Molyneux DH, Fenwick A, et al. Control of neglected tropical diseases. N Engl J Med. 2007;357:1018–1027.
3. Albonico M, Bickle Q, Ramsan M, Montresor A, Savioli L, Taylor M. Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bull World Health Organ. 2003;81:343–352.
4. Taman A, Azab M. Present-day anthelmintics and perspectives on future new targets. Parasitol Res. 2014;113:2425–2433.
5. Kaplan RM, Vidyashankar AN. An inconvenient truth: global worming and anthelmintic resistance. Vet Parasitol. 2012;186:70–78.
6. Ambros V. A uniform system for microRNA annotation. RNA. 2003;9:277–279.
7. Zaph C, Troy AE, Taylor BC, et al. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature. 2007;446:552–556.
8. Howitt MR, Lavoie S, Michaud M, et al. Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science. 2016;351:1329–1333.
9. Gerbe F, Sidot E, Smyth DJ, et al. Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature. 2016;529:226–230.
10. von Moltke J, Ji M, Liang HE, Locksley RM. Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature. 2016;529:221–225.
11. Moro K, Yamada T, Tanabe M, et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010;463:540–544.
12. Neill DR, Wong SH, Bellosi A, et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010;464:1367–1370.
13. Price AE, Liang HE, Sullivan BM, et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci USA. 2010;107:11489–11494.
14. Oliphant CJ, Hwang YY, Walker JA, et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity. 2014;41:283–295.
15. Chieppa M, Rescigno M, Huang AY, Germain RN. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med. 2006;203:2841–2852.
16. Pelly VS, Kannan Y, Coomes SM, et al. IL-4-producing ILC2s are required for the differentiation of TH2 cells following Heligmosomoides polygyrus infection. Mucosal Immunol. 2016;9:1407–1417.
17. Grencis RK, Hültner L, Else KJ. Host protective immunity to Trichinella spiralis in mice: activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes. Immunology. 1991;74:329–332.
18. Hashimoto K, Uchikawa R, Tegoshi T, Takeda K, Yamada M, Arizono N. Depleted intestinal goblet cells and severe pathological changes in SCID mice infected with Heligmosomoides polygyrus. Parasite Immunol. 2009;31:457–465.
19. Oeser K, Schwartz C, Voehringer D. Conditional IL-4/IL-13-deficient mice reveal a critical role of innate immune cells for protective immunity against gastrointestinal helminths. Mucosal Immunol. 2015;8:672–682.
20. Fallon PG, Ballantyne SJ, Mangan NE, et al. 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. 2006;203:1105–1116.
21. Anthony RM, Urban JF Jr, Alem F, et al. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med. 2006;12:955–960.
22. Murray PJ, Allen JE, Biswas SK, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41:14–20.
23. Hepworth MR, Danilowicz-Luebert E, Rausch S, et al. Mast cells orchestrate type 2 immunity to helminths through regulation of tissue-derived cytokines. Proc Natl Acad Sci USA. 2012;109:6644–6649.
24. Schwartz C, Turqueti-Neves A, Hartmann S, Yu P, Nimmerjahn F, Voehringer D. Basophil-mediated protection against gastrointestinal helminths requires IgE-induced cytokine secretion. Proc Natl Acad Sci USA. 2014;111:E5169–E5177.
25. Cadman ET, Thysse KA, Bearder S, et al. Eosinophils are important for protection, immunoregulation and pathology during infection with nematode microfilariae. PLoS Pathog. 2014;10:e1003988.
26. Sutherland TE, Logan N, Ruckerl D, et al. Chitinase-like proteins promote IL-17-mediated neutrophilia in a tradeoff between nematode killing and host damage. Nat Immunol. 2014;15:1116–1125.
27. Chen F, Wu W, Millman A, et al. Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat Immunol. 2014;15:938–946.
28. McCoy KD, Stoel M, Stettler R, et al. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe. 2008;4:362–373.
29. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science. 2005;308:1463–1465.
30. Hasnain SZ, Evans CM, Roy M, et al. Muc5ac: a critical component mediating the rejection of enteric nematodes. J Exp Med. 2011;208:893–900.
31. Vallance BA, Blennerhassett PA, Collins SM. Increased intestinal muscle contractility and worm expulsion in nematode-infected mice. Am J Physiol. 1997;272(Pt 1):G321–G327.
32. Farmer SG, Brown JM, Pollock D. Increased responsiveness of intestinal and vascular smooth muscle to agonists in rats infected with Nippostrongylus brasiliensis. Arch Int Pharmacodyn Ther. 1983;263:217–227.
33. Herbert DR, Yang JQ, Hogan SP, et al. Intestinal epithelial cell secretion of RELM-β protects against gastrointestinal worm infection. J Exp Med. 2009;206:2947–2957.
34. Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004;23:4051–4060.
35. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003;17:3011–3016.
36. Hutvagner G, McLachlan J, Pasquinelli AE, Balint E, Tuschl T, Zamore PD. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science. 2001;293:834–838.
37. Cloonan N. Re-thinking miRNA-mRNA interactions: intertwining issues confound target discovery. BioEssays. 2015;37:379–388.
38. Abdelfattah AM, Park C, Choi MY. Update on non-canonical MicroRNAs. Biomol Concepts. 2014;5:275–287.
39. Martinez J, Patkaniowska A, Urlaub H, Tuschl T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell. 2002;110:563–574.
40. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 2009;10:126–139.
41. Eulalio A, Huntzinger E, Izaurralde E. Getting to the root of miRNA-mediated gene silencing. Cell. 2008;132:9–14.
42. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. 2010;11:597–610.
43. McKenna LB, Schug J, Vourekas A, et al. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology. 2010;139:1654–1664, 1664 e1651.
44. Biton M, Levin A, Slyper M, et al. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol. 2011;12:239–246.
45. Wu F, Zikusoka M, Trindade A, et al. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology. 2008;135:1624–1635 e1624.
46. Worthington JJ, Samuelson LC, Grencis RK, McLaughlin JT. Adaptive immunity alters distinct host feeding pathways during nematode induced inflammation, a novel mechanism in parasite expulsion. PLoS Pathog. 2013;9:e1003122.
47. Knudsen LA, Petersen N, Schwartz TW, Egerod KL. The MicroRNA repertoire in enteroendocrine cells: identification of miR-375 as a potential regulator of the enteroendocrine lineage. Endocrinology. 2015;156:3971–3983.
48. Gerbe F, van Es JH, Makrini L, et al. Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol. 2011;192:767–780.
49. Gerbe F, Legraverend C, Jay P. The intestinal epithelium tuft cells: specification and function. Cell Mol Life Sci. 2012;69:2907–2917.
50. Chunjie N, Huijuan N, Zhao Y, Jianzhao W, Xiaojian Z. Disease-specific signature of serum miR-20b and its targets IL-8 and IL-25, in myasthenia gravis patients. Eur Cytokine Netw. 2015;26:61–66.
51. Coskun M, Bjerrum JT, Seidelin JB, Troelsen JT, Olsen J, Nielsen OH. miR-20b, miR-98, miR-125b-1*, and let-7e* as new potential diagnostic biomarkers in ulcerative colitis. World J Gastroenterol. 2013;19:4289–4299.
52. Caruso R, Sarra M, Stolfi C, et al. Interleukin-25 inhibits interleukin-12 production and Th1 cell-driven inflammation in the gut. Gastroenterology. 2009;136:2270–2279.
53. Nakato G, Hase K, Sato T, et al. Epithelium-intrinsic MicroRNAs contribute to mucosal immune homeostasis by promoting M-Cell maturation. PLoS One. 2016;11:e0150379.
54. Zhou R, O'Hara SP, Chen XM. MicroRNA regulation of innate immune responses in epithelial cells. Cell Mol Immunol. 2011;8:371–379.
55. Czimmerer Z, Varga T, Kiss M, et al. The IL-4/STAT6 signaling axis establishes a conserved microRNA signature in human and mouse macrophages regulating cell survival via miR-342-3p. Genome Med. 2016;8:63.
56. Zhuang G, Meng C, Guo X, et al. A novel regulator of macrophage activation: miR-223 in obesity-associated adipose tissue inflammation. Circulation. 2012;125:2892–2903.
57. Ruckerl D, Jenkins SJ, Laqtom NN, et al. Induction of IL-4Ralpha-dependent microRNAs identifies PI3K/Akt signaling as essential for IL-4-driven murine macrophage proliferation in vivo. Blood. 2012;120:2307–2316.
58. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245–252.
59. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003;3:984–993.
60. Mehta A, Baltimore D. MicroRNAs as regulatory elements in immune system logic. Nat Rev Immunol. 2016;16:279–294.
61. Smith KA, Harcus Y, Garbi N, Hammerling GJ, MacDonald AS, Maizels RM. Type 2 innate immunity in helminth infection is induced redundantly and acts autonomously following CD11c(+) cell depletion. Infect Immun. 2012;80:3481–3489.
62. Smith KA, Hochweller K, Hammerling GJ, Boon L, MacDonald AS, Maizels RM. Chronic helminth infection promotes immune regulation in vivo through dominance of CD11cloCD103- dendritic cells. J Immunol. 2011;186:7098–7109.
63. Phythian-Adams AT, Cook PC, Lundie RJ, et al. CD11c depletion severely disrupts Th2 induction and development in vivo. J Exp Med. 2010;207:2089–2096.
64. Terrazas LI, Sanchez-Munoz F, Perez-Miranda M, et al. Helminth excreted/secreted antigens repress expression of LPS-induced Let-7i but not miR-146a and miR-155 in human dendritic cells. BioMed Res Int. 2013;2013:972506.
65. Zheng J, Jiang HY, Li J, et al. MicroRNA-23b promotes tolerogenic properties of dendritic cells in vitro through inhibiting Notch1/NF-kappaB signalling pathways. Allergy. 2012;67:362–370.
66. Dunand-Sauthier I, Irla M, Carnesecchi S, et al. Repression of arginase-2 expression in dendritic cells by microRNA-155 is critical for promoting T cell proliferation. J Immunol. 2014;193:1690–1700.
67. Zech A, Ayata CK, Pankratz F, et al. MicroRNA-155 modulates P2R signaling and Th2 priming of dendritic cells during allergic airway inflammation in mice. Allergy. 2015;70:1121–1129.
68. Okoye IS, Czieso S, Ktistaki E, et al. Transcriptomics identified a critical role for Th2 cell-intrinsic miR-155 in mediating allergy and antihelminth immunity. Proc Natl Acad Sci USA. 2014;111:E3081–E3090.
69. Tang H, Jiang H, Zheng J, et al. MicroRNA-106b regulates pro-allergic properties of dendritic cells and Th2 polarisation by targeting early growth response-2 in vitro. Int Immunopharmacol. 2015;28:866–874.
70. Johansson K, Malmhall C, Ramos-Ramirez P, Radinger M. MicroRNA-155 is a critical regulator of type 2 innate lymphoid cells and IL-33 signaling in experimental models of allergic airway inflammation. J Allergy Clin Immunol. 2016. pii: S0091-6749(16)30723-0.
71. Mohrs M, Shinkai K, Mohrs K, Locksley RM. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity. 2001;15:303–311.
72. Katona IM, Urban JF Jr, Finkelman FD. The role of L3T4+ and Lyt-2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J Immunol. 1988;140:3206–3211.
73. Bancroft AJ, Else KJ, Grencis RK. Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. Eur J Immunol. 1994;24:3113–3118.
74. Muljo SA, Ansel KM, Kanellopoulou C, Livingston DM, Rao A, Rajewsky K. Aberrant T cell differentiation in the absence of Dicer. J Exp Med. 2005;202:261–269.
75. Cobb BS, Nesterova TB, Thompson E, et al. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J Exp Med. 2005;201:1367–1373.
76. Baumjohann D, Ansel KM. MicroRNA-mediated regulation of T helper cell differentiation and plasticity. Nat Rev Immunol. 2013;13:666–678.
77. Rivera J, Proia RL, Olivera A. The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat Rev Immunol. 2008;8:753–763.
78. Cho S, Wu CJ, Yasuda T, et al. miR-23~27~24 clusters control effector T cell differentiation and function. J Exp Med. 2016;213:235–249.
79. Simpson LJ, Patel S, Bhakta NR, et al. A microRNA upregulated in asthma airway T cells promotes TH2 cytokine production. Nat Immunol. 2014;15:1162–1170.
80. Pua HH, Steiner DF, Patel S, et al. MicroRNAs 24 and 27 suppress allergic inflammation and target a network of regulators of T Helper 2 cell-associated cytokine production. Immunity. 2016;44:821–832.
81. Mavrakis KJ, Wolfe AL, Oricchio E, et al. Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol. 2010;12:372–379.
82. Lu TX, Hartner J, Lim EJ, et al. MicroRNA-21 limits in vivo immune response-mediated activation of the IL-12/IFN-gamma pathway, Th1 polarization, and the severity of delayed-type hypersensitivity. J Immunol. 2011;187:3362–3373.
83. Fu D, Yu W, Li M, et al. MicroRNA-138 regulates the balance of Th1/Th2 via targeting RUNX3 in psoriasis. Immunol Lett. 2015;166:55–62.
84. Abbas AK, Benoist C, Bluestone JA, et al. Regulatory T cells: recommendations to simplify the nomenclature. Nat Immunol. 2013;14:307–308.
85. Finney CA, Taylor MD, Wilson MS, Maizels RM. Expansion and activation of CD4(+)CD25(+) regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol. 2007;37:1874–1886.
86. Grainger JR, Smith KA, Hewitson JP, et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-beta pathway. J Exp Med. 2010;207:2331–2341.
87. Hang L, Blum AM, Setiawan T, Urban JP Jr, Stoyanoff KM, Weinstock JV. Heligmosomoides polygyrus bakeri infection activates colonic Foxp3+ T cells enhancing their capacity to prevent colitis. J Immunol. 2013;191:1927–1934.
88. Rausch S, Huehn J, Kirchhoff D, et al. Functional analysis of effector and regulatory T cells in a parasitic nematode infection. Infect Immun. 2008;76:1908–1919.
89. Liston A, Lu LF, O'Carroll D, Tarakhovsky A, Rudensky AY. Dicer-dependent microRNA pathway safeguards regulatory T cell function. J Exp Med. 2008;205:1993–2004.
90. Zhou X, Jeker LT, Fife BT, et al. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J Exp Med. 2008;205:1983–1991.
91. Chong MM, Rasmussen JP, Rudensky AY, Littman DR. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J Exp Med. 2008;205:2005–2017.
92. Li D, Kong C, Tsun A, et al. MiR-125a-5p decreases the sensitivity of Treg cells toward IL-6-mediated conversion by inhibiting IL-6R and STAT3 expression. Sci Rep. 2015;5:14615.
93. Li S, Fan Q, He S, Tang T, Liao Y, Xie J. MicroRNA-21 negatively regulates Treg cells through a TGF-beta1/Smad-independent pathway in patients with coronary heart disease. Cell Physiol Biochem. 2015;37:866–878.
94. Pan W, Zhu S, Dai D, et al. MiR-125a targets effector programs to stabilize Treg-mediated immune homeostasis. Nat Commun. 2015;6:7096.
95. van der Geest KS, Smigielska-Czepiel K, Park JA, et al. SF Treg cells transcribing high levels of Bcl-2 and microRNA-21 demonstrate limited apoptosis in RA. Rheumatology (Oxford). 2015;54:950–958.
96. Zhou Q, Haupt S, Kreuzer JT, et al. Decreased expression of miR-146a and miR-155 contributes to an abnormal Treg phenotype in patients with rheumatoid arthritis. Ann Rheum Dis. 2015;74:1265–1274.
97. Li W, Kong LB, Li JT, et al. MiR-568 inhibits the activation and function of CD4(+) T cells and Treg cells by targeting NFAT5. Int Immunol. 2014;26:269–281.
98. Jiang S, Li C, Olive V, et al. Molecular dissection of the miR-17-92 cluster's critical dual roles in promoting Th1 responses and preventing inducible Treg differentiation. Blood. 2011;118:5487–5497.
99. Rouas R, Fayyad-Kazan H, El Zein N, et al. Human natural Treg microRNA signature: role of microRNA-31 and microRNA-21 in FOXP3 expression. Eur J Immunol. 2009;39:1608–1618.
100. Singh Y, Garden OA, Lang F, Cobb BS. MicroRNA-15b/16 enhances the induction of regulatory T cells by regulating the expression of Rictor and mTOR. J Immunol. 2015;195:5667–5677.
101. Seddiki N, Swaminathan S, Phetsouphanh C, Kelleher AD. miR-155 is differentially expressed in Treg subsets, which may explain expression level differences of miR-155 in HIV-1 infected patients. Blood. 2012;119:6396–6397.
102. Lu LF, Thai TH, Calado DP, et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity. 2009;30:80–91.
103. Lu LF, Boldin MP, Chaudhry A, et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell. 2010;142:914–929.
104. Kelada S, Sethupathy P, Okoye IS, et al. miR-182 and miR-10a are key regulators of Treg specialisation and stability during schistosome and leishmania-associated inflammation. PLoS Pathog. 2013;9:e1003451.
105. Stittrich AB, Haftmann C, Sgouroudis E, et al. The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes. Nat Immunol. 2010;11:1057–1062.
106. Li YF, Ou X, Xu S, Jin ZB, Iwai N, Lam KP. Loss of miR-182 affects B-cell extrafollicular antibody response. Immunology. 2016;148:140–149.
107. Wojciechowski W, Harris DP, Sprague F, et al. Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity. 2009;30:421–433.
108. Liu Q, Kreider T, Bowdridge S, et al. B cells have distinct roles in host protection against different nematode parasites. J Immunol. 2010;184:5213–5223.
109. Blackwell NM, Else KJ. B cells and antibodies are required for resistance to the parasitic gastrointestinal nematode Trichuris muris. Infect Immun. 2001;69:3860–3868.
110. Leon B, Ballesteros-Tato A, Browning JL, Dunn R, Randall TD, Lund FE. Regulation of T(H)2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat Immunol. 2012;13:681–690.
111. Dixon H, Little MC, Else KJ. Characterisation of the protective immune response following subcutaneous vaccination of susceptible mice against Trichuris muris. Int J Parasitol. 2010;40:683–693.
112. Vigorito E, Perks KL, Abreu-Goodger C, et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity. 2007;27:847–859.
113. Thai TH, Calado DP, Casola S, et al. Regulation of the germinal center response by microRNA-155. Science. 2007;316:604–608.
114. Nakagawa R, Leyland R, Meyer-Hermann M, et al. MicroRNA-155 controls affinity-based selection by protecting c-MYC+ B cells from apoptosis. J Clin Invest. 2016;126:377–388.
115. Teng G, Hakimpour P, Landgraf P, et al. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity. 2008;28:621–629.
116. Sole C, Larrea E, Manterola L, et al. Aberrant expression of MicroRNAs in B-cell lymphomas. MicroRNA. 2016.
117. Eis PS, Tam W, Sun L, et al. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci USA. 2005;102:3627–3632.
118. Tsai DY, Hung KH, Lin IY, et al. Uncovering MicroRNA regulatory hubs that modulate plasma cell differentiation. Sci Rep. 2015;5:17957.
119. Porstner M, Winkelmann R, Daum P, et al. miR-148a promotes plasma cell differentiation and targets the germinal center transcription factors Mitf and Bach2. Eur J Immunol. 2015;45:1206–1215.
120. Gabler J, Wittmann J, Porstner M, et al. Contribution of microRNA 24-3p and Erk1/2 to interleukin-6-mediated plasma cell survival. Eur J Immunol. 2013;43:3028–3037.
121. Hayes KS, Bancroft AJ, Goldrick M, Portsmouth C, Roberts IS, Grencis RK. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science. 2010;328:1391–1394.
122. Zaiss MM, Rapin A, Lebon L, et al. The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity. 2015;43:998–1010.
123. Wescott RB, Todd AC. A comparison of the development of Nippostrongylus brasiliensis in Germ-free and conventioal mice. J Parasitol. 1964;50:138–143.
124. Chang J, Wescott RB. Infectivity, fecundity, and survival of Nematospiroides dubius in gnotobiotic mice. Exp Parasitol. 1972;32:327–334.
125. Stefanski W, Przyjalkowski Z. Effect of alimentary tract microorganisms on the development of Trichinella spiralis in mice. Exp Parasitol. 1965;16:167–173.
126. Reynolds LA, Smith KA, Filbey KJ, et al. Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites. Gut Microbes. 2014;5:522–532.
127. Dalmasso G, Nguyen HT, Yan Y, et al. Microbiota modulate host gene expression via microRNAs. PLoS One. 2011;6:e19293.
128. Singh N, Shirdel EA, Waldron L, Zhang RH, Jurisica I, Comelli EM. The murine caecal microRNA signature depends on the presence of the endogenous microbiota. Int J Biol Sci. 2012;8:171–186.
129. Liu S, da Cunha AP, Rezende RM, et al. The host shapes the gut microbiota via fecal MicroRNA. Cell Host Microbe. 2016;19:32–43.
130. Bautista-Garfias CR, Ixta-Rodríguez O, Martínez-Gómez F, López MG, Aguilar-Figueroa BR. Effect of viable or dead Lactobacillus casei organisms administered orally to mice on resistance against Trichinella spiralis infection. Parasite. 2001;8:S226–S228.
131. Hansen EP, Kringel H, Thamsborg SM, Jex A, Nejsum P. Profiling circulating miRNAs in serum from pigs infected with the porcine whipworm, Trichuris suis. Vet Parasitol. 2016;223:30–33.
132. Nowacki FC, Swain MT, Klychnikov OI, et al. Protein and small non-coding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni. J Extracell Vesicles. 2015;4:28665.
133. Quintana JF, Makepeace BL, Babayan SA, et al. Extracellular onchocerca-derived small RNAs in host nodules and blood. Parasit Vectors. 2015;8:58.
134. Hoy AM, Lundie RJ, Ivens A, et al. Parasite-derived microRNAs in host serum as novel biomarkers of helminth infection. PLoS Negl Trop Dis. 2014;8:e2701.
135. Buck AH, Coakley G, Simbari F, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun. 2014;5:5488.
136. Quintana JF, Babayan SA, Buck AH. Small RNAs and extracellular vesicles in filarial nematodes: from nematode development to diagnostics. Parasite Immunol. 2016. doi: 10.1111/pim.12395.
137. Fromm B, Ovchinnikov V, Hoye E, Bernal D, Hackenberg M, Marcilla A. On the presence and immunoregulatory functions of extracellular microRNAs in the trematode Fasciola hepatica. Parasite Immunol. 2016. doi: 10.1111/pim.12399.