Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites

Immunological Reviews

Volumn 201, Issue , 2004, Pages 139-155

  Finkelman, Fred D ^a,b,c   Shea Donohue, Terez ^d   Morris, Suzanne C ^b,c   Gildea, Lucy ^e   Strait, Richard ^c   Madden, Kathleen B ^f   Schopf, Lisa ^d   Urban Jr , Joseph F ^d  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

^e PROCTER AND GAMBLE COMPANY   (United States)

^f UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN E ANTIBODY; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; STAT6 PROTEIN;

ANAPHYLAXIS; B LYMPHOCYTE; CELL FUNCTION; COMPARATIVE STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EOSINOPHILIA; HOST PARASITE INTERACTION; IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; INTESTINE MUSCLE; MAST CELL; MASTOCYTOSIS; MUCUS SECRETION; NEMATODE; NEMATODIASIS; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTECTION; REVIEW; SHOCK; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTILITY; T LYMPHOCYTE; TH1 CELL; TH2 CELL; TRICHINELLA SPIRALIS; WORM EXPULSION; WORM INFECTION;

ANIMALS; INTERLEUKIN-13; INTERLEUKIN-4; INTESTINAL DISEASES, PARASITIC; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEMATODE INFECTIONS; STRONGYLIDA; TRICHINELLA SPIRALIS;

EID: 4844221210     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2004.00192.x     Document Type: Review

References (68)

1. Scott P, Natovitz P, Coffman RL, Pearce E, Sher A. Immunoregulation of cutaneous leishmaniasis. T cell lines that transfer protective immunity or exacerbation belong to different T helper subsets and respond to distinct parasite antigens. J Exp Med 1988;168:1675-1684.
2. Heinzel FP, Sadick MD, Holaday BJ, Coffman RL, Locksley RM. Reciprocal expression of interferon γ or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med 1989;169:59-72.
3. Suzuki Y, Conley FK, Remington JS. Importance of endogenous IFN-γ for prevention of toxoplasmic encephalitis in mice. J Immunol 1989;143:2045-2050.
4. Sedegah M, Finkelman F, Hoffman SL. Interleukin 12 induction of interferon γ-dependent protection against malaria. Proc Natl Acad Sci USA 1994:91:10700-10702.
5. Stevenson MM, Tam MF, Wolf SF, Sher A. IL-12-induced protection against bloodstage Plasmodium chabaudi as requires IFN-γ and TNF-α and occurs via a nitric oxide-dependent mechanism. J Immunol 1995;155:2545-2556.
6. + T lymphocytes in protective immunity. J Immunol 1991;147:1014-1022.
7. Urban JF Jr, Fayer R, Chen SJ, Gause WC, Gately MK, Finkelman FD. IL-12 protects immunocompetent and immunodeficient neonatal mice against infection with Cryptosporidium parvum. J Immunol 1996;156:263-268.
8. Buchmeier NA Jr, Schreiber RD. Requirement of endogenous interferon-α production for resolution of Listeria monocytogenes infection. Proc Natl Acad Sci USA 1985;82:7404-7408.
9. Orange JS, Wang B, Terhorst C, Biron CA. Requirement for natural killer cell-produced interferon γ in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J Exp Med 1995;182:1045-1056.
10. Kaufmann SH, Follows GA, Munk ME. Immunity to intracellular bacteria. Mem Inst Oswaldo Cruz 1992;87:91-94.
11. Finkelman FD, et al. Effects of interleukin 12 on immune responses and host protection in mice infected with intestinal nematode parasites. J Exp Med 1994;179:1563-1572.
12. Morris SC, et al. Effects of IL-12 on in vivo cytokine gene expression and Ig isotype selection. J Immunol 1994;152:1047-1056.
13. Gately MK, et al. The interleukin-12/interleukin-12-receptor system: Role in normal and pathologic immune responses. Annu Rev Immunol 1998;16:495-521.
14. Jacobson RH, Reed ND. The immune response of congenitally athymic (nude) mice to the intestinal nematode Nippostrongylus brasiliensis. Proc Soc Exp Biol Med 1974;147:667-670.
15. + T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J Immunol 1988;140:3206-3211.
16. Finkelman FD, et al. Anti-cytokine antibodies as carrier proteins. Prolongation of in vivo effects of exogenous cytokines by injection of cytokine-anti-cytokine antibody complexes. J Immunol 1993;151:1235-1244.
17. Else KJ, Finkelman FD, Maliszewski CR, Grencis RK. Cytokine-mediated regulation of chronic intestinal helminth infection. J Exp Med 1994;179:347-351.
18. Urban JF Jr, Maliszewski CR, Madden KB, Katona IM, Finkelman FD. IL-4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice. J Immunol 1995;154:4675-4684.
19. Urban JF Jr, et al. IL-13, IL-4Rα, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 1998;8:255-264.
20. Finkelman FD, Wynn TA, Donaldson DD, Urban JF. The role of IL-13 in helminth-induced inflammation and protective immunity against nematode infections. Curr Opin Immunol 1999;11:420-426.
21. Kaplan MH, Schindler U, Smiley ST, Grusby MJ. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 1996;4:313-319.
22. Shimoda K, et al. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 1996;380:630-633.
23. Takeda K, et al. Essential role of Stat6 in IL-4 signalling. Nature 1996;380:627-630.
24. McKenzie GJ, Bancroft A, Grencis RK, McKenzie AN. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr Biol 1998;8:339-342.
25. McKenzie GJ, Fallon PG, Emson CL, Grencis RK, McKenzie AN. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J Exp Med 1999;189:1565-1572.
26. Gurish MF, Ghildyal N, McNeil HP, Austen KF, Gillis S, Stevens RL. Differential expression of secretory granule proteases in mouse mast cells exposed to interleukin 3 and c-kit ligand. J Exp Med 1992;175:1003-1012.
27. Finkelman FD, Morris SC. Development of an assay to measure in vivo cytokine production in the mouse. Int Immunol 1999;11:1811-1818.
28. Finkelman FD, Morris SC, Orekhova T, Sehy D. The in vivo cytokine capture assay (IVCCA) for measurement of in vivo cytokine production in the mouse. Curr Protoc Immunol 2003:6.28.1-6.28.10.
29. Finkelman FD, et al. Stat6 regulation of in vivo IL-4 responses. J Immunol 2000;164:2303-2310.
30. Urban JF Jr, Noben-Trauth N, Schopf L, Madden KB, Finkelman FD. Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J Immunol 2001;167:6078-6081.
31. Shanta CS, Meerovitch E. The life cycle of Trichinella spiralis. II. The muscle phase of development and its possible evolution. Can J Zool 1967;45:1261-1267.
32. Shanta CS, Meerovitch E. The life cycle of Trichinella spiralis. I. The intestinal phase of development. Can J Zool 1967;45:1255-1260.
33. Grencis RK, Hultner 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.
34. V mice. Infect Immun 1983;41:445-447.
35. V mice reconstituted with haematopoietic and lymphopoietic cells and origin of mucosal mast cells. Immunology 1984;53:337-344.
36. V mice. J Helminthol 1985;59:233-239.
37. Itayama H, Oku Y, Kamiya M. Longevity and fecundity of Trichinella spiralis in mast cell-deficient Sl/Sld mice. Jpn J Vet Res 1987;35:195-207.
38. Grencis RK, Else KJ, Huntley JF, Nishikawa SI. The in vivo role of stem cell factor (c-kit ligand) on mastocytosis and host protective immunity to the intestinal nematode Trichinella spiralis in mice. Parasite Immunol 1993;15:55-59.
39. Coffman RL, Ohara J, Bond MW, Carty J, Zlotnik A, Paul WE. B cell stimulatory factor-1 enhances the IgE response of lipopolysaccharide-activated B cells. J Immunol 1986;136:4538-4541.
40. Finkelman FD, Katona IM, Urban JF Jr, Snapper CM, Ohara J, Paul WE. Suppression of in vivo polyclonal IgE responses by monoclonal antibody to the lymphokine B-cell stimulatory factor 1. Proc Natl Acad Sci USA 1986;83:9675-9678.
41. Urban JF Jr, et al. Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. J Immunol 2000;164:2046-2052.
42. Knight PA, Wright SH, Lawrence CE, Paterson YY, Miller HR. 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 2000;192:1849-1856.
43. Ishizaka T, Ishizaka K, Tomioka H. Release of histamine and slow reacting substance of anaphylaxis (SRS-A) by IgE-anti-IgE reactions on monkey mast cells. J Immunol 1972;108:513-520.
44. Kitamura D, Roes J, Kuhn R, Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature 1991;350:423-426.
45. Madden KB, Urban JF Jr, Ziltener HJ, Schrader JW, Finkelman FD, Katona IM. Antibodies to IL-3 and IL-4 suppress helminth-induced intestinal mastocytosis. J Immunol 1991;147:1387-1391.
46. Madden KB, et al. Role of stat6 and mast cells in IL-4- and IL-13-induced alterations in murine intestinal epithelial cell function. J Immunol 2002;169:4417-4422.
47. Shea-Donohue T, et al. The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine epithelial cell function. J Immunol 2001;167:2234-2239.
48. Zhao A, et al. Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J Immunol 2003;171:948-954.
49. Goldhill J, et al. Interleukin-4 modulates cholinergic neural control of mouse small intestinal longitudinal muscle. Am J Physiol 1997;272:G1135-G1140.
50. Madden KB, et al. Enteric nematodes induce stereotypic Stat6-dependent alterations in intestinal epithelial cell function. J Immunol 2004;172:5616-5621.
51. Khan WI, Abe T, Ishikawa N, Nawa Y, Yoshimura K. Reduced amount of intestinal mucus by treatment with anti-CD4 antibody interferes with the spontaneous cure of Nippostrongylus brasiliensis-infection in mice. Parasite Immunol 1995;17:485-491.
52. Bansemir AD, Sukhdeo MV. Intestinal distribution of worms and host ingesta in Nippostrongylus brasiliensis. J Parasitol 2001;87:1470-1472.
53. Ouellette AJ, Selsted ME. Paneth cell defensins: Endogenous peptide components of intestinal host defense. FASEB J 1996;10:1280-1289.
54. Love RJ. Nippostrongylus brasiliensis infections in mice: The immunological basis of worm expulsion. Parasitology 1975;70:11-18.
55. Iff ET, Vaz NM. Mechanisms of anaphylaxis in the mouse. Similarity of shock induced by anaphylaxis and by mixtures of histamine and serotonin. Int Arch Allergy Appl Immunol 1966;30:313-322.
56. Bochner BS, Lichtenstein LM. Anaphylaxis. N Engl J Med 1991;324:1785-1790.
57. Strait RT, Morris SC, Yang M, Qu XW, Finkelman FD. Pathways of anaphylaxis in the mouse. J Allergy Clin Immunol 2002;109:658-668.
58. Miyajima I, Dombrowicz D, Martin TR, Ravetch JV, Kinet JP, Galli SJ. Systemic anaphylaxis in the mouse can be mediated largely through IgG1 and FcγRIII. Assessment of the cardiopulmonary changes, mast cell degranulation, and death associated with active or IgE- or IgG1-dependent passive anaphylaxis. J Clin Invest 1997;99:901-914.
59. Strait RT, Morris SC, Smiley K, Urban JF Jr, Finkelman FD. IL-4 exacerbates anaphylaxis. J Immunol 2003;170:3835-3842.
60. Seder RA, et al. Mouse splenic and bone marrow cell populations that express high-affinity Fcε receptors and produce interleukin 4 are highly enriched in basophils. Proc Natl Acad Sci USA 1991;88:2835-2839.
61. Faulkner H, Renauld JC, Van Snick J, Grencis RK. Interleukin-9 enhances resistance to the intestinal nematode Trichuris muris. Infect Immun 1998;66:3832-3840.
62. Richard M, Grencis RK, Humphreys NE, Renauld JC, Van Snick J. Anti-IL-9 vaccination prevents worm expulsion and blood eosinophilia in Trichuris muris-infected mice. Proc Natl Acad Sci USA 2000;97:767-772.
63. Ovington KS, McKie K, Matthaei KI, Young IG, Behm CA. Regulation of primary Strongyloides ratti infections in mice: A role for interleukin-5. Immunology 1998;95:488-493.
64. Rotman HL, et al. Strongyloides stercoralis: Eosinophil-dependent immune-mediated killing of third stage larvae in BALB/cByJ mice. Exp Parasitol 1996;82:267-278.
65. Korenaga M, Hitoshi Y, Takatsu K, Tada I. Regulatory effect of anti-interleukin-5 monoclonal antibody on intestinal worm burden in a primary infection with Strongyloides venezuelensis in mice. Int J Parasitol 1994;24:951-957.
66. Sasaki O, Sugaya H, Ishida K, Yoshimura K. Ablation of eosinophils with anti-IL-5 antibody enhances the survival of intracranial worms of Angiostrongylus cantonensis in the mouse. Parasite Immunol 1993;15:349-354.
67. Sugaya H, Aoki M, Yoshida T, Takatsu K, Yoshimura K. Eosinophilia and intracranial worm recovery in interleukin-5 transgenic and interleukin-5 receptor α chain-knockout mice infected with Angiostrongylus cantonensis. Parasitol Res 1997;83:583-590.
68. Fallon PG, et al. IL-4 induces characteristic Th2 responses even in the combined absence of EL-5, IL-9, and IL-13. Immunity 2002;17:7-17.