Trichinella spiralis immunomodulation: an interactive multifactorial process

References

• Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 296(5567), 490–494 (2002).
   PubMed Web of Science ®Google Scholar
• Strachan DP. Family size, infection and atopy: the first decade of the “hygiene hypothesis”. Thorax 55(Suppl. 1), S2–S10 (2000).
   PubMed Web of Science ®Google Scholar
• Weinstock JV, Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thompson R. The possible link between de-worming and the emergence of immunological disease. J. Lab. Clin. Med. 139(6), 334–338 (2002).
   PubMed Web of Science ®Google Scholar
• Belkaid Y, Blank RB, Suffia I. Natural regulatory T cells and parasites: a common quest for host homeostasis. Immunol. Rev. 212, 287–300 (2006).
   PubMed Web of Science ®Google Scholar
• Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites–masters of regulation. Immunol. Rev. 201, 89–116 (2004).
   PubMed Web of Science ®Google Scholar
• Ilic N, Gruden-Movsesijan A, Sofronic-Milosavljevic L. Trichinella spiralis: shaping the immune response. Immunol. Res. 52(1-2), 111–119 (2012).
   PubMed Web of Science ®Google Scholar
• McDermott JR, Grencis RK, Else KJ. Leucocyte recruitment during enteric nematode infection. Immunology 103(4), 505–510 (2001).
   PubMed Web of Science ®Google Scholar
• Helmby H, Grencis RK. IFN-γ-independent effects of IL-12 during intestinal nematode infection. J. Immunol. 171(7), 3691–3696 (2003).
   PubMed Web of Science ®Google Scholar
• Bruschi F, Chiumiento L. Trichinella inflammatory myopathy: host or parasite strategy? Parasit. Vectors 4, 42 (2011).
   PubMed Web of Science ®Google Scholar
• Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, Wynn TA. Immunopathology of schistosomiasis. Immunol. Cell Biol. 85(2), 148–154 (2007).
   PubMed Web of Science ®Google Scholar
• Park HK, Cho MK, Choi SH, Kim YS, Yu HS. Trichinella spiralis: infection reduces airway allergic inflammation in mice. Exp. Parasitol. 127(2), 539–544 (2011).
   PubMed Web of Science ®Google Scholar
• Khan WI, Blennerhasset PA, Varghese AK et al. Intestinal nematode infection ameliorates experimental colitis in mice. Infect. Immun. 70(11), 5931–5937 (2002).
   PubMed Web of Science ®Google Scholar
• Ashour DS, Othman AA, Shareef MM, Gaballah HH, Mayah WW. Interactions between Trichinella spiralis infection and induced colitis in mice. J. Helminthol. doi:10.1017/S0022149X13000059, 1–9 (2013) (Epub ahead of print).
   Web of Science ®Google Scholar
• Saunders KA, Raine T, Cooke A, Lawrence CE. Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect. Immun. 75(1), 397–407 (2007).
   PubMed Web of Science ®Google Scholar
• Gruden-Movsesijan A, Ilic N, Mostarica-Stojkovic M, Stosic-Grujicic S, Milic M, Sofronic-Milosavljevic L. Mechanisms of modulation of experimental autoimmune encephalomyelitis by chronic Trichinella spiralis infection in Dark Agouti rats. Parasite Immunol. 32(6), 450–459 (2010).
   PubMed Web of Science ®Google Scholar
• Liu Q, Sundar K, Mishra PK et al. Helminth infection can reduce insulitis and Type 1 diabetes through CD25- and IL-10-independent mechanisms. Infect. Immun. 77(12), 5347–5358 (2009).
   PubMed Web of Science ®Google Scholar
• Freeman CM, Chiu BC, Stolberg VR et al. CCR8 is expressed by antigen-elicited, IL-10-producing CD4+CD25+ T cells, which regulate Th2-mediated granuloma formation in mice. J. Immunol. 174(4), 1962–1970 (2005).
   PubMed Web of Science ®Google Scholar
• Cho MK, Park MK, Kang SA, Choi SH, Ahn SC, Yu HS. Trichinella spiralis infection suppressed gut inflammation with CD4(+)CD25(+)Foxp3(+) T cell recruitment. Korean J. Parasitol. 50(4), 385–390 (2012).
   PubMed Web of Science ®Google Scholar
• Aranzamendi C, de Bruin A, Kuiper R et al. Protection against allergic airway inflammation during the chronic and acute phases of Trichinella spiralis infection. Clin. Exp. Allergy 43(1), 103–115 (2013).
   PubMed Web of Science ®Google Scholar
• Grainger JR, Smith KA, Hewitson JP et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J. Exp. Med. 207(11), 2331–2341 (2010).
   PubMed Web of Science ®Google Scholar
• McKay DM. The therapeutic helminth? Trends Parasitol. 25(3), 109–114 (2009).
   PubMed Web of Science ®Google Scholar
• Beiting DP, Gagliardo LF, Hesse M, Bliss SK, Meskill D, Appleton JA. Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-β. J. Immunol. 178(2), 1039–1047 (2007).
   PubMed Web of Science ®Google Scholar
• Mills KH, McGuirk P. Antigen-specific regulatory T cells–their induction and role in infection. Semin. Immunol. 16(2), 107–117 (2004).
   PubMed Web of Science ®Google Scholar
• Liu B, Tonkonogy SL, Sartor RB. Antigen-presenting cell production of IL-10 inhibits T-helper 1 and 17 cell responses and suppresses colitis in mice. Gastroenterology 141(2), 653–662, 662.e1 (2011).
   PubMed Web of Science ®Google Scholar
• Chen Z, Lin F, Gao Y et al. FOXP3 and RORγt: transcriptional regulation of Treg and Th17. Int. Immunopharmacol. 11(5), 536–542 (2011).
   PubMed Web of Science ®Google Scholar
• Elliott DE, Weinstock JV. Helminth-host immunological interactions: prevention and control of immune-mediated diseases. Ann. N. Y. Acad. Sci. 1247, 83–96 (2012).
   PubMed Web of Science ®Google Scholar
• Ilic N, Worthington JJ, Gruden-Movsesijan A, Travis MA, Sofronic-Milosavljevic L, Grencis RK. Trichinella spiralis antigens prime mixed Th1/Th2 response but do not induce de novo generation of Foxp3+ T cells in vitro. Parasite Immunol. 33(10), 572–582 (2011).
   PubMed Web of Science ®Google Scholar
• Pape KA, Catron DM, Itano AA, Jenkins MK. The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity 26(4), 491–502 (2007).
   PubMed Web of Science ®Google Scholar
• Harris DP, Haynes L, Sayles PC et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat. Immunol. 1(6), 475–482 (2000).
   PubMed Web of Science ®Google Scholar
• Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 3(10), 944–950 (2002).
   PubMed Web of Science ®Google Scholar
• DiLillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann. N. Y. Acad. Sci. 1183, 38–57 (2010).
   PubMed Web of Science ®Google Scholar
• van der Vlugt LE, Labuda LA, Ozir-Fazalalikhan A et al. Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. PLoS ONE 7(2), e30883 (2012).
   PubMed Web of Science ®Google Scholar
• Everts B, Adegnika AA, Kruize YC, Smits HH, Kremsner PG, Yazdanbakhsh M. Functional impairment of human myeloid dendritic cells during Schistosoma haematobium infection. PLoS Negl. Trop. Dis. 4(4), e667 (2010).
   PubMed Web of Science ®Google Scholar
• Anthony RM, Nimmerjahn F, Ashline DJ, Reinhold VN, Paulson JC, Ravetch JV. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 320(5874), 373–376 (2008).
   PubMed Web of Science ®Google Scholar
• Hussaarts L, van der Vlugt LE, Yazdanbakhsh M, Smits HH. Regulatory B-cell induction by helminths: implications for allergic disease. J. Allergy Clin. Immunol. 128(4), 733–739 (2011).
   PubMed Web of Science ®Google Scholar
• Ronet C, Hauyon-La Torre Y, Revaz-Breton M et al. Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J. Immunol. 184(2), 886–894 (2010).
   PubMed Web of Science ®Google Scholar
• Mizoguchi A, Mizoguchi E, Takedatsu H, Blumberg RS, Bhan AK. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16(2), 219–230 (2002).
   PubMed Web of Science ®Google Scholar
• Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 197(4), 489–501 (2003).
   PubMed Web of Science ®Google Scholar
• Wolf SD, Dittel BN, Hardardottir F, Janeway CA Jr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J. Exp. Med. 184(6), 2271–2278 (1996).
   PubMed Web of Science ®Google Scholar
• Hernandez HJ, Wang Y, Stadecker MJ. In infection with Schistosoma mansoni, B cells are required for T helper type 2 cell responses but not for granuloma formation. J. Immunol. 158(10), 4832–4837 (1997).
   PubMed Web of Science ®Google Scholar
• Wilson MS, Taylor MD, O’Gorman MT et al. Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur. J. Immunol. 40(6), 1682–1696 (2010).
   PubMed Web of Science ®Google Scholar
• Lipscomb MF, Masten BJ. Dendritic cells: immune regulators in health and disease. Physiol. Rev. 82(1), 97–130 (2002).
   PubMed Web of Science ®Google Scholar
• Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 3(12), 984–993 (2003).
   PubMed Web of Science ®Google Scholar
• Duez C, Gosset P, Tonnel AB. Dendritic cells and toll-like receptors in allergy and asthma. Eur. J. Dermatol. 16(1), 12–16 (2006).
   PubMed Web of Science ®Google Scholar
• MacDonald AS, Maizels RM. Alarming dendritic cells for Th2 induction. J. Exp. Med. 205(1), 13–17 (2008).
   PubMed Web of Science ®Google Scholar
• Segura M, Su Z, Piccirillo C, Stevenson MM. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur. J. Immunol. 37(7), 1887–1904 (2007).
   PubMed Web of Science ®Google Scholar
• Ferret-Bernard S, Curwen RS, Mountford AP. Proteomic profiling reveals that Th2-inducing dendritic cells stimulated with helminth antigens have a ‘limited maturation’ phenotype. Proteomics 8(5), 980–993 (2008).
   PubMed Web of Science ®Google Scholar
• Barton GM, Medzhitov R. Control of adaptive immune responses by Toll-like receptors. Curr. Opin. Immunol. 14(3), 380–383 (2002).
   PubMed Web of Science ®Google Scholar
• Kane CM, Cervi L, Sun J et al. Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173(12), 7454–7461 (2004).
   PubMed Web of Science ®Google Scholar
• Pulendran B, Tang H, Manicassamy S. Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat. Immunol. 11(8), 647–655 (2010).
   PubMed Web of Science ®Google Scholar
• Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21, 685–711 (2003).
   PubMed Web of Science ®Google Scholar
• Klaver EJ, Kuijk LM, Laan LC et al. Trichuris suis-induced modulation of human dendritic cell function is glycan-mediated. Int. J. Parasitol. 43(3-4), 191–200 (2013).
   PubMed Web of Science ®Google Scholar
• Sofronic-Milosavljevic L, Radovic I, Ilic N, Majstorovic I, Cvetkovic J, Gruden-Movsesijan A. Application of dendritic cells stimulated with Trichinella spiralis excretory-secretory antigens alleviates experimental autoimmune encephalomyelitis. Med. Microbiol. Immunol. doi:10.1007/s00430-012-0286-6 (2013) (Epub ahead of print).
   PubMed Web of Science ®Google Scholar
• Langelaar M, Aranzamendi C, Franssen F et al. Suppression of dendritic cell maturation by Trichinella spiralis excretory/secretory products. Parasite Immunol. 31(10), 641–645 (2009).
   PubMed Web of Science ®Google Scholar
• Ilic N, Colic M, Gruden-movsesijan A, Majstorovic I, Vasilev S, Sofronic-Milosavljevic Lj. Characterization of rat bone marrow dendritic cells initially primed by Trichinella spiralis antigens. Parasite Immunol. 30(9), 491–495 (2008).
   PubMed Web of Science ®Google Scholar
• Gruden-Movsesijan A, Ilic N, Colic M et al. The impact of Trichinella spiralis excretory-secretory products on dendritic cells. Comp. Immunol. Microbiol. Infect. Dis. 34(5), 429–439 (2011).
   PubMed Web of Science ®Google Scholar
• Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front. Biosci. 13, 453–461 (2008).
   PubMed Web of Science ®Google Scholar
• Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164(12), 6166–6173 (2000).
   PubMed Web of Science ®Google Scholar
• Brown BN, Valentin JE, Stewart-Akers AM, McCabe GP, Badylak SF. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30(8), 1482–1491 (2009).
   PubMed Web of Science ®Google Scholar
• Horsnell WG, Brombacher F. Genes associated with alternatively activated macrophages discretely regulate helminth infection and pathogenesis in experimental mouse models. Immunobiology 215(9-10), 704–708 (2010).
   PubMed Web of Science ®Google Scholar
• Reynolds LA, Filbey KJ, Maizels RM. Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus. Semin. Immunopathol. 34(6), 829–846 (2012).
   PubMed Web of Science ®Google Scholar
• Semnani RT, Mahapatra L, Moore V, Sanprasert V, Nutman TB. Functional and phenotypic characteristics of alternative activation induced in human monocytes by interleukin-4 or the parasitic nematode Brugia malayi. Infect. Immun. 79(10), 3957–3965 (2011).
   PubMed Web of Science ®Google Scholar
• Loke P, MacDonald AS, Allen JE. Antigen-presenting cells recruited by Brugia malayi induce Th2 differentiation of naïve CD4(+) T cells. Eur. J. Immunol. 30(4), 1127–1135 (2000).
   PubMed Web of Science ®Google Scholar
• Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5(12), 953–964 (2005).
   PubMed Web of Science ®Google Scholar
• Reese TA, Liang HE, Tager AM et al. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature 447(7140), 92–96 (2007).
   PubMed Web of Science ®Google Scholar
• Bai X, Wu X, Wang X et al. Regulation of cytokine expression in murine macrophages stimulated by excretory/secretory products from Trichinella spiralis in vitro. Mol. Cell. Biochem. 360(1-2), 79–88 (2012).
   PubMed Web of Science ®Google Scholar
• Hesse M, Modolell M, La Flamme AC et al. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of l-arginine metabolism. J. Immunol. 167(11), 6533–6544 (2001).
   PubMed Web of Science ®Google Scholar
• Du L, Tang H, Ma Z et al. The protective effect of the recombinant 53-kDa protein of Trichinella spiralis on experimental colitis in mice. Dig. Dis. Sci. 56(10), 2810–2817 (2011).
   PubMed Web of Science ®Google Scholar
• Strowig T, Brilot F, Münz C. Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J. Immunol. 180(12), 7785–7791 (2008).
   PubMed Web of Science ®Google Scholar
• Mallevaey T, Fontaine J, Breuilh L et al. Invariant and noninvariant natural killer T cells exert opposite regulatory functions on the immune response during murine schistosomiasis. Infect. Immun. 75(5), 2171–2180 (2007).
   PubMed Web of Science ®Google Scholar
• Bany J, Janiak MK, Budzynski W. Activity of natural killer (NK) cells in the course of experimental trichinellosis in mice. Wiad. Parazytol. 38(3–4), 117–126 (1992).
   PubMedGoogle Scholar
• McDermott JR, Humphreys NE, Forman SP, Donaldson DD, Grencis RK. Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. J. Immunol. 175(5), 3207–3213 (2005).
   PubMed Web of Science ®Google Scholar
• Nielsen N, Ødum N, Ursø B, Lanier LL, Spee P. Cytotoxicity of CD56(bright) NK cells towards autologous activated CD4+ T cells is mediated through NKG2D, LFA-1 and TRAIL and dampened via CD94/NKG2A. PLoS ONE 7(2), e31959 (2012).
   Google Scholar
• Hall LJ, Murphy CT, Quinlan A et al. Natural killer cells protect mice from DSS-induced colitis by regulating neutrophil function via the NKG2A receptor. Mucosal Immunol. doi:10.1038/mi.2012.140 (2013) (Epub ahead of print).
   PubMed Web of Science ®Google Scholar
• Zaccone P, Fehérvári Z, Jones FM et al. Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of Type 1 diabetes. Eur. J. Immunol. 33(5), 1439–1449 (2003).
   PubMed Web of Science ®Google Scholar
• Oettgen HC, Geha RS. IgE regulation and roles in asthma pathogenesis. J. Allergy Clin. Immunol. 107(3), 429–440 (2001).
   PubMed Web of Science ®Google Scholar
• Erb KJ. Helminths, allergic disorders and IgE-mediated immune responses: where do we stand? Eur. J. Immunol. 37(5), 1170–1173 (2007).
   PubMed Web of Science ®Google Scholar
• Wang CC, Nolan TJ, Schad GA, Abraham D. Infection of mice with the helminth Strongyloides stercoralis suppresses pulmonary allergic responses to ovalbumin. Clin. Exp. Allergy 31(3), 495–503 (2001).
   PubMed Web of Science ®Google Scholar
• Hussain R, Poindexter RW, Ottesen EA. Control of allergic reactivity in human filariasis. Predominant localization of blocking antibody to the IgG4 subclass. J. Immunol. 148(9), 2731–2737 (1992).
   PubMed Web of Science ®Google Scholar
• Motomura Y, Wang H, Deng Y, El-Sharkawy RT, Verdu EF, Khan WI. Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clin. Exp. Immunol. 155(1), 88–95 (2009).
   PubMed Web of Science ®Google Scholar