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PMID: 12595439 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Macrophage migration inhibitory factor plays a critical role in mediating protection against the helminth parasite Taenia crassiceps.

Infection and immunity ·Vol. 71 ·No. 3 ·2003-03-00 ·Pages 1247-54

Rodríguez-Sosa M, Rosas LE, David JR, Bojalil R, Satoskar AR, Terrazas LI

Abstract

To determine the role of endogenous migration inhibitory factor (MIF) in regulation of immune response during murine cysticercosis caused by the helminth parasite Taenia crassiceps, we analyzed the course of T. crassiceps infection in MIF(-/-) BALB/c mice. MIF(-/-) mice were highly susceptible to T. crassiceps and developed significantly higher parasite loads compared to similarly infected MIF(+/+) mice. Throughout the course of infection, Taenia crassiceps soluble antigen-stimulated spleen cells from both MIF(+/+) and MIF(-/-) mice produced significant and comparable levels of interleukin-4 (IL-4), but those from MIF(-/-) mice produced significantly more IL-13, as well as gamma interferon (IFN-gamma), suggesting that the susceptibility of MIF(-/-) mice to T. crassiceps was not due to the lack of IFN-gamma production. Interestingly, low levels of both total and specific immunoglobulin G2a were observed in MIF(-/-) cysticercotic mice despite the high IFN-gamma levels; in addition, peritoneal macrophages obtained from T. crassiceps-infected MIF(-/-) mice at different time points failed to respond efficiently to stimulation in vitro with lipopolysaccharide plus IFN-gamma and produced significantly lower levels of IL-12, tumor necrosis factor alpha, and NO compared to those from MIF(+/+) mice. These findings demonstrate that MIF plays a critical role in mediating protection against T. crassiceps in vivo. Moreover, these findings also suggest that impaired macrophage function rather than the lack of Th1 development may be responsible for mediating susceptibility to T. crassiceps.

MeSH Terms
Animals Antibodies, Helminth/blood Cysticercosis/immunology Female Immunoglobulin E/blood Immunoglobulin G/blood,classification Interferon-gamma/pharmacology Macrophage Migration-Inhibitory Factors/physiology Mice Mice, Inbred BALB C Nitric Oxide/biosynthesis Th1 Cells/immunology Th2 Cells/immunology
Chemicals
Antibodies, Helminth Immunoglobulin G Macrophage Migration-Inhibitory Factors Nitric Oxide Immunoglobulin E Interferon-gamma
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Rodríguez-Sosa Miriam
Department of Immunology, Instituto Nacional de Cardiología Ignacio Chávez, Mexico, D.F. 14080 Mexico.
Rosas Lucia E
David John R
Bojalil Rafael
Satoskar Abhay R
Terrazas Luis I
References (46)
46 references, click to expand
  1. Protection from septic shock by neutralization of macrophage migration inhibitory factor.
    Nat Med. 2000 Feb;6(2):164-70 PMID: 10655104
  2. Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis.
    J Steroid Biochem Mol Biol. 1995 Jun;52(6):575-80 PMID: 7779761
  3. Macrophage migration inhibitory factor release by macrophages after ingestion of Plasmodium chabaudi-infected erythrocytes: possible role in the pathogenesis of malarial anemia.
    Infect Immun. 2000 Apr;68(4):2259-67 PMID: 10722628
  4. Regulation of macrophage migration inhibitory factor by endogenous glucocorticoids in rat adjuvant-induced arthritis.
    Arthritis Rheum. 2000 Apr;43(4):827-33 PMID: 10765927
  5. Mechanisms of resistance to S. mansoni infection: the rat model.
    Parasitol Int. 2000 Dec;49(4):339-45 PMID: 11077269
  6. Migration-inhibitory factor gene-deficient mice are susceptible to cutaneous Leishmania major infection.
    Infect Immun. 2001 Feb;69(2):906-11 PMID: 11159984
  7. Taenia solium disease in humans and pigs: an ancient parasitosis disease rooted in developing countries and emerging as a major health problem of global dimensions.
    Microbes Infect. 2000 Dec;2(15):1875-90 PMID: 11165932
  8. Role of macrophage migration inhibitory factor (MIF) in murine antigen-induced arthritis: interaction with glucocorticoids.
    Clin Exp Immunol. 2001 Feb;123(2):309-14 PMID: 11207663
  9. De Novo expression of macrophage migration inhibitory factor in atherogenesis.
    Circ Res. 2001 Mar 2;88(4):E31 PMID: 11230114
  10. Kinetics and characterization of cellular responses in the peritoneal cavity of mice infected with Taenia crassiceps.
    J Parasitol. 2001 Jun;87(3):591-9 PMID: 11426723
  11. Macrophage migration inhibitory factor and innate immune responses to bacterial infections.
    Crit Care Med. 2001 Jul;29(7 Suppl):S13-5 PMID: 11445727
  12. Immunoendocrine interactions during chronic cysticercosis determine male mouse feminization: role of IL-6.
    J Immunol. 2001 Oct 15;167(8):4527-33 PMID: 11591780
  13. A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection.
    J Immunol. 2001 Nov 1;167(9):5348-54 PMID: 11673551
  14. Development of chronic colitis is dependent on the cytokine MIF.
    Nat Immunol. 2001 Nov;2(11):1061-6 PMID: 11668338
  15. CD4+ TCRalphabeta T cells are critically involved in the control of experimental murine cysticercosis in C57BL/6J mice.
    Parasitol Res. 2001 Oct;87(10):826-32 PMID: 11688888
  16. Analysis of the peripheral immune response in patients with neurocysticercosis: evidence for T cell reactivity to parasite glycoprotein and vesicular fluid antigens.
    Am J Trop Med Hyg. 2001 Oct;65(4):366-70 PMID: 11693886
  17. MIF regulates innate immune responses through modulation of Toll-like receptor 4.
    Nature. 2001 Dec 20-27;414(6866):920-4 PMID: 11780066
  18. Macrophage migration inhibitory factor.
    Crit Care Med. 2002 Jan;30(1 Suppl):S27-35 PMID: 11782558
  19. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):345-50 PMID: 11756671
  20. Cutting edge: susceptibility to the larval stage of the helminth parasite Taenia crassiceps is mediated by Th2 response induced via STAT6 signaling.
    J Immunol. 2002 Apr 1;168(7):3135-9 PMID: 11907063
  21. Genetic control of susceptibility to Taenia crassiceps cysticercosis.
    Parasitology. 1996 Jan;112 ( Pt 1):119-24 PMID: 8587794
  22. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7849-54 PMID: 8755565
  23. Developmental differences determine larval susceptibility to nitric oxide-mediated killing in a murine model of vaccination against Schistosoma mansoni.
    Infect Immun. 1997 Jan;65(1):219-26 PMID: 8975915
  24. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models.
    Annu Rev Immunol. 1997;15:505-33 PMID: 9143698
  25. Mechanism of suppression of macrophage nitric oxide release by IL-13: influence of the macrophage population.
    J Immunol. 1997 Nov 1;159(9):4506-13 PMID: 9379051
  26. Increased resistance to Taenia crassiceps murine cysticercosis in Qa-2 transgenic mice.
    Infect Immun. 1998 Feb;66(2):760-4 PMID: 9453638
  27. Shift from an early protective Th1-type immune response to a late permissive Th2-type response in murine cysticercosis (Taenia crassiceps).
    J Parasitol. 1998 Feb;84(1):74-81 PMID: 9488341
  28. IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis.
    Immunity. 1998 Feb;8(2):255-64 PMID: 9492006
  29. Taenia crassiceps invasive cysticercosis: a new human pathogen in acquired immunodeficiency syndrome?
    Am J Surg Pathol. 1998 Apr;22(4):488-92 PMID: 9537478
  30. Analysis of immune lesions in neurocysticercosis patients: central nervous system response to helminth appears Th1-like instead of Th2.
    J Neuroimmunol. 1998 Aug 14;89(1-2):64-72 PMID: 9726827
  31. Taenia crassiceps cysticercosis and AIDS.
    AIDS. 1998 Aug 20;12(12):1551-2 PMID: 9727578
  32. Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11383-8 PMID: 9736745
  33. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis.
    J Exp Med. 1999 Jan 18;189(2):341-6 PMID: 9892616
  34. Th1-type cytokines improve resistance to murine cysticercosis caused by Taenia crassiceps.
    Parasitol Res. 1999 Feb;85(2):135-41 PMID: 9934963
  35. The systemic immune response of BALB/c mice infected with larval Taenia crassiceps is a mixed Th1/Th2-type response.
    Parasitology. 1999 Jun;118 ( Pt 6):623-33 PMID: 10406041
  36. Phage-displayed T-cell epitope grafted into immunoglobulin heavy-chain complementarity-determining regions: an effective vaccine design tested in murine cysticercosis.
    Infect Immun. 1999 Sep;67(9):4764-70 PMID: 10456929
  37. Castration and pregnancy of rural pigs significantly increase the prevalence of naturally acquired Taenia solium cysticercosis.
    Vet Parasitol. 2002 Aug 30;108(1):41-8 PMID: 12191898
  38. Intraperitoneal passage of Taenia crassiceps in rats.
    J Parasitol. 1976 Oct;62(5):837-9 PMID: 978374
  39. Macrophage NO2- production as a sensitive and rapid assay for the quantitation of murine IFN-gamma.
    J Immunol Methods. 1991 May 17;139(1):107-14 PMID: 1904084
  40. Immunological mediation of gonadal effects on experimental murine cysticercosis caused by Taenia crassiceps metacestodes.
    J Parasitol. 1992 Jun;78(3):471-6 PMID: 1597791
  41. IL-6 down-modulates the cytokine-enhanced antileishmanial activity in human macrophages.
    J Immunol. 1993 Oct 1;151(7):3682-92 PMID: 8397259
  42. High-affinity IgE receptor on eosinophils is involved in defence against parasites.
    Nature. 1994 Jan 13;367(6459):183-6 PMID: 8114916
  43. Immunoglobulin E and effector cells in schistosomiasis.
    Science. 1994 Jun 24;264(5167):1876-7 PMID: 8009216
  44. A role for 17-beta-estradiol in immunoendocrine regulation of murine cysticercosis (Taenia crassiceps).
    J Parasitol. 1994 Aug;80(4):563-8 PMID: 8064524
  45. IL-4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice.
    J Immunol. 1995 May 1;154(9):4675-84 PMID: 7722320
  46. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity.
    Curr Opin Immunol. 2000 Feb;12(1):64-76 PMID: 10679404
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
DOI
10.1128/IAI.71.3.1247-1254.2003
Published
2003-03-00
Pages
1247-54
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC148860
Subset
IM
Grants
NIAID NIH HHS · R01 AI051823 · United States
NIAID NIH HHS · AI51823 · United States
External Links
PubMed source DOI: 10.1128/IAI.71.3.1247-1254.2003 PMC Full Text View journal details
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