Signaling through Gαi2 protein is required for recruitment of neutrophils for antibody-mediated elimination of larval Strongyloides stercoralis in mice

Journal of Leukocyte Biology

Volumn 81, Issue 4, 2007, Pages 1120-1126

  Padigel, Udaikumar M ^a   Stein, Louis ^a   Redding, Kevin ^a   Lee, James J ^b   Nolan, Thomas J ^c   Schad, Gerhard A ^c   Birnbaumer, Lutz ^d   Abraham, David ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Antibody; Cytokine; G protein; Heterotrimeric; Parasite

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 4; INTERLEUKIN 5; MYELOPEROXIDASE; HELMINTH ANTIBODY; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNIZATION; LARVA; MALE; MICROENVIRONMENT; MOUSE; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; STRONGYLOIDES STERCORALIS; T LYMPHOCYTE; TH2 CELL; ANIMAL; CELL CULTURE; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; NEUTROPHIL; PHYSIOLOGY; SIGNAL TRANSDUCTION; STRONGYLOIDIASIS;

MUS; STRONGYLOIDES STERCORALIS;

ANIMALS; ANTIBODIES, HELMINTH; CELLS, CULTURED; GTP-BINDING PROTEIN ALPHA SUBUNIT, GI2; HOST-PARASITE RELATIONS; IMMUNITY, NATURAL; LARVA; MALE; MICE; NEUTROPHILS; SIGNAL TRANSDUCTION; STRONGYLOIDES STERCORALIS; STRONGYLOIDIASIS;

EID: 33947683313     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1106695     Document Type: Article

References (39)

1. He, J., Gurunathan, S., Iwasaki, A., Ash-Shaheed, B., Kelsall, B. L. (2000) Primary role for Gi protein signaling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses. J. Exp. Med. 191, 1605-1610.
2. Huang, T. T., Zong, Y., Dalwadi, H., Chung, C., Miceli, M. C., Spicher, K., Birnbaumer, L., Braun, J., Aranda, R. (2003) TCR-mediated hyper-responsiveness of autoimmune Gαi2(-/-) mice is an intrinsic naive CD4(+) T cell disorder selective for the Gαi2 subunit. Int. Immunol. 15, 1359-1367.
3. Murphy, P. M. (1994) The molecular biology of leukocyte chemoattractant receptors. Annu. Rev. Immunol. 12, 593-633.
4. Ryan, M., McCarthy, L., Rappuoli, R., Mahon, B. P., Mills, K. H. (1998) Pertussis toxin potentiates Th1 and Th2 responses to co-injected antigen: adjuvant action is associated with enhanced regulatory cytokine production and expression of the co-stimulatory molecules B7-1, B7-2 and CD28. Int. Immunol. 10, 651-662.
5. Birnbaumer, L., Birnbaumer, M. (1995) Signal transduction by G proteins: 1994 edition. J. Recept. Signal Transduct. Res. 15, 213-252.
6. Rudolph, U., Finegold, M. J., Rich, S. S., Harriman, G. R., Srinivasan, Y., Brabet, P., Bradley, A., Birnbaumer, L. (1995) Gi2 α protein deficiency: a model of inflammatory bowel disease. J. Clin. Immunol. 15, 101S-105S.
7. Hornquist, C. E., Lu, X., Rogers-Fani, P. M., Rudolph, U., Shappell, S., Birnbaumer, L., Harriman, G. R. (1997) G(α)i2-deficient mice with colitis exhibit a local increase in memory CD4+ T cells and proinflammatory Th1-type cytokines. J. Immunol. 158, 1068-1077.
8. Dalwadi, H., Wei, B., Schrage, M., Spicher, K., Su, T. T., Birnbaumer, L., Rawlings, D. J., Braun, J. (2003) B cell developmental requirement for the G α i2 gene. J. Immunol. 170, 1707-1715.
9. Hou, W., Wu, Y., Sun, S., Shi, M., Sun, Y., Yang, C., Pei, G., Gu, Y., Zhong, C., Sun, B. (2003) Pertussis toxin enhances Th1 responses by stimulation of dendritic cells. J. Immunol. 170, 1728-1736.
10. Ohman, L., Franzen, L., Rudolph, U., Birnbaumer, L., Hornquist, E. H. (2002) Regression of Peyer's patches in G α i2 deficient mice prior to colitis is associated with reduced expression of Bcl-2 and increased apoptosis. Gut 51, 392-397.
11. Ohman, L., Franzen, L., Rudolph, U., Harriman, G. R., Hultgren Hornquist, E. (2000) Immune activation in the intestinal mucosa before the onset of colitis in Gαi2-deficient mice. Scand. J. Immunol. 52, 80-90.
12. Mu, H. H., Sewell, W. A. (1993) Enhancement of interleukin-4 production by pertussis toxin. Infect. Immun. 61, 2834-2840.
13. Sewell, W. A., de Moerloose, P. A., McKimm-Breschkin, J. L., Vadas, M. A. (1986) Pertussigen enhances antigen-driven interferon-γ production by sensitized lymphoid cells. Cell. Immunol. 97, 238-247.
14. Brabb, T., Goldrath, A. W., von Dassow, P., Paez, A., Liggitt, H. D., Goverman, J. (1997) Triggers of autoimmune disease in a murine TCR-transgenic model for multiple sclerosis. J. Immunol. 159, 497-507.
15. McAllister, C. G., Vistica, B. P., Sekura, R., Kuwabara, T., Gery, I. (1986) The effects of pertussis toxin on the induction and transfer of experimental autoimmune uveoretinitis. Clin. Immunol. Immunopathol. 39, 329-336.
16. Herbert, D. R., Lee, J. J., Lee, N. A., Nolan, T. J., Schad, G. A., Abraham, D. (2000) Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J. Immunol. 165, 4544-4551.
17. Herbert, D. R., Nolan, T. J., Schad, G. A., Abraham, D. (2002) The role of B cells in immunity against larval Strongyloides stercoralis in mice. Parasite Immunol. 24, 95-101.
18. Brigandi, R. A., Rotman, H. L., Yutanawiboonchai, W., Leon, O., Nolan, T. J., Schad, G. A., Abraham, D. (1996) Strongyloides stercoralis: role of antibody and complement in immunity to the third stage of larvae in BALB/cByJ mice. Exp. Parasitol. 82, 279-289.
19. Rotman, H. L., Schnyder-Candrian, S., Scott, P., Nolan, T. J., Schad, G. A., Abraham, D. (1997) IL-12 eliminates the Th-2 dependent protective immune response of mice to larval Strongyloides stercoralis. Parasite Immunol. 19, 29-39.
20. Kerepesi, L. A., Hess, J. A., Nolan, T. J., Schad, G. A., Abraham, D. (2006) Complement component C3 is required for protective innate and adaptive immunity to larval Strongyloides stercoralis in mice. J. Immunol. 176, 4315-4322.
21. Galioto, A. M., Hess, J. A., Nolan, T. J., Schad, G. A., Lee, J. J., Abraham, D. (2006) Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval Strongyloides stercoralis in mice. Infect. Immun. 74, 5730-5738.
22. Lippert, E., Jacques, Y., Hermouet, S. (2000) Positive regulation of human T cell activation by Gi2 proteins and interleukin-8. J. Leukoc. Biol. 67, 742-748.
23. Fan, H., Peck, O. M., Tempel, G. E., Halushka, P. V., Cook, J. A. (2004) Toll-like receptor 4 coupled GI protein signaling pathways regulate extracellular signal-regulated kinase phosphorylation and AP-1 activation independent of NFκB activation. Shock 22, 57-62.
24. Kerepesi, L. A., Hess, J. A., Leon, O., Nolan, T. J., Schad, G. A., Abraham, D. (2007) Toll-like receptor 4 (TLR4) is required for protective immunity to larval Strongyloides stercoralis in mice. Microbes Infect., 9, 28-34.
25. Abraham, D., Rotman, H. L., Haberstroh, H. F., Yutanawiboonchai, W., Brigandi, R. A., Leon, O., Nolan, T. J., Schad, G. A. (1995) Strongyloides stercoralis: protective immunity to third-stage larvae inBALB/cByJ mice. Exp. Parasitol. 80, 297-307.
26. Herbert, D. R., Nolan, T. J., Schad, G. A., Lustigman, S., Abraham, D. (2002) Immunoaffinity-isolated antigens induce protective immunity against larval Strongyloides stercoralis in mice. Exp. Parasitol. 100, 112-120.
27. Lowell, C. A., Fumagalli, L., Berton, G. (1996) Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell Biol. 133, 895-910.
28. Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D., Allen, J. E. (2004) Helminth parasites - masters of regulation. Immunol. Rev. 201, 89-116.
29. Pearce, E. J., M. Kane, C., Sun, J., J. Taylor, J., McKee, A. S., Cervi, L. (2004) Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol. Rev. 201, 117-126.
30. Lawrence, R. A., Allen, J. E., Osborne, J., Maizels, R. M. (1994) Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and Ig isotype responses in BALB/c mice. J. Immunol. 153, 1216-1224.
31. Pearce, E. J., Caspar, P., Grzych, J. M., Lewis, F. A., Sher, A. (1991) Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J. Exp. Med. 173, 159-166.
32. Ligas, J. A., Kerepesi, L. A., Galioto, A. M., Lustigman, S., Nolan, T. J., Schad, G. A., Abraham, D. (2003) Specificity and mechanism of immunoglobulin M (IgM)- and IgG-dependent protective immunity to larval Strongyloides stercoralis in mice. Infect. Immun. 71, 6835-6843.
33. Rudolph, U., Finegold, M. J., Rich, S. S., Harriman, G. R., Srinivasan, Y., Brabet, P., Boulay, G., Bradley, A., Birnbaumer, L. (1995) Ulcerative colitis and adenocarcinoma of the colon in G α i2-deficient mice. Nat. Genet. 10, 143-150.
34. Falcone, F. H., Rossi, A. G., Sharkey, R., Brown, A. P., Pritchard, D. I., Maizels, R. M. (2001) Ascaris suum-derived products induce human neutrophil activation via a G protein-coupled receptor that interacts with the interleukin-8 receptor pathway. Infect. Immun. 69, 4007-4018.
35. Cyster, J. G., Goodnow, C. C. (1995) Pertussis toxin inhibits migration of B and T lymphocytes into splenic white pulp cords. J. Exp. Med. 182, 581-586.
36. Spangrude, G. J., Sacchi, F., Hill, H. R., Van Epps, D. E., Daynes, R. A. (1985) Inhibition of lymphocyte and neutrophil chemotaxis by pertussis toxin. J. Immunol. 135, 4135-4143.
37. Su, S. B., Silver, P. B., Zhang, M., Chan, C. C., Caspi, R. R. (2001) Pertussis toxin inhibits induction of tissue-specific autoimmune disease by disrupting G protein-coupled signals. J. Immunol. 167, 250-256.
38. Fan, H., Zingarelli, B., Peck, O. M., Teti, G., Tempel, G. E., Halushka, P. V., Spicher, K., Boulay, G., Birnbaumer, L., Cook, J. A. (2005) Lipopolysaccharide- and gram-positive bacteria-induced cellular inflammatory responses: role of heterotrimeric Gα(i) proteins. Am. J. Physiol. Cell Physiol. 289, C293-C301.
39. Pero, R. S., Borchers, M. T., Spicher, K., Ochkur, S. I., Sikora, L., Rao, S. P., Abdala-Valencia, H., O'Neill, K. R., Shen, H., Simon, M. I., McGarry, M. P., Lee, N. A., Cook-Mills, J. M., Sriramarao, P., Birnbaumer, L., Lee, J. J. (2006) Extravasation of leukocytes from circulation is controlled by Gαi2 signaling events in the endothelium. Proc. Natl. Acad. Sci. USA, in press.