A phosphorylcholine-containing filarial nematode-secreted product disrupts B lymphocyte activation by targeting key proliferative signaling pathways

Journal of Immunology

Volumn 160, Issue 6, 1998, Pages 2692-2699

  Deehan, Maureen R ^a   Frame, Mhairi J ^a,c   Parkhouse, R Michael E ^b   Seatter, Sandra D ^c   Reid, Steven D ^c   Harnett, Margaret M ^c   Harnett, William ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHORYLCHOLINE;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL FUNCTION; CELL PROLIFERATION; ENZYME ACTIVATION; FILARIA; GENE DISRUPTION; GENE TARGETING; IMMUNE RESPONSE; NEMATODE; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WUCHERERIA BANCROFTI;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMINO ACID SEQUENCE; ANIMALS; B-LYMPHOCYTES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; DIPETALONEMA; HELMINTH PROTEINS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHORYLCHOLINE; PROTEIN-TYROSINE KINASES; RABBITS; RAS PROTEINS; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 0032521026     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. WHO 1987. Filariasis. World Health Organization, Geneva.
2. Vanamail, P., K. D. Ramaiah, S. P. Pani, P. K. Das, B. T. Grenfell, and D. A. P. Bundy. 1996. Estimation of the fecund life-span of Wuchereria bancrofti in an endemic area. Trans. R. Soc. Trop. Med. Hyg. 90:119.
3. Nutman, T. B., V. Kumaraswami, and E. A. Ottesen. 1987. Parasite-specific anergy in human filariasis: insights after analysis of parasite antigen-driven lymphokine production. J. Clin. Invest. 79:1516.
4. Nutman, T. B., V. Kumaraswami, L. Pao, P. R. Narayanan, and E. A. Ottesen. 1987. An analysis of in vitro B cell immune responsiveness in human lymphatic filariasis. J. Immunol. 138:3954.
5. Kazura, J. W., T. B. Nutman, and B. Greene. 1993. Filariasis. In In Immunology and Molecular Biology of Parasitic Infections. K. S. Warren, ed. Blackwell Scientific Publications, Oxford, pp. 473-495.
6. Ottesen, E. A. 1995. Immune responsiveness and the pathogenesis of human onchocerciasis. J. Infect. Dis. 171:659.
7. Piessens, W. F., S. Ratiwayanto, S. Tuti, J. H. Palmieri, P. W. Piessens, I. Koiman, and D. T. Dennis. 1980. Antigen-specific suppressor cells and suppressor factors in human filariasis with Brugia malayi. N. Engl. J. Med. 302:833.
8. Lammie, P. J., S. P. Katz, and W. H. K. Anderson. 1984. Serosuppression in experimental filariasis. Clin. Exp. Immunol. 55:602.
9. Weil, G. J. 1990. Parasite antigenaemia in lymphatic filariasis. Exp. Parasitol. 71:353.
10. Bradley, J. E., and T. R. Unnasch. 1996. Molecular approaches to the diagnosis of onchocerciasis. Adv. Parasitol. 37:57.
11. Harnett, W., and M. M. Harnett. 1993. Inhibition of murine B cell proliferation and down-regulation of protein kinase C levels by a phosphorylcholine-containing filarial excretory-secretory product. J. Immunol. 151:4829.
12. Elkhalifa, M. Y., H. W. Ghalib, T. Dafa'alla, and J. F. Williams. 1991. Suppression of human lymphocyte responses to specific and non-specific stimuli in human onchocerciasis. Clin. Exp. Immunol. 86:433.
13. 4 responsiveness in a subpopulation of microfilaremic persons. J. Infect. Dis. 172:1630.
14. Harnett, W., M. Grainger, A. Kapil, M. J. Worms, and R. M. E. Parkhouse. 1989. Origin, kinetics of circulation and fate in vivo of the major excretory-secretory product of Acanthocheilonema viteae. Parasitology 99:229.
15. Deehan, M. R., M. M. Harnett, and W. Harnett. 1997. A filarial nematode secreted product differentially modulates expression and activation of protein kinase C isoforms in B lymphocytes. J. Immunol. 159:6105.
16. Pleiman, C. M., D. D'Ambrosia, and J. C. Cambier. 1994. The B-cell antigen receptor complex: structure and signal transduction. Immunol. Today 15:393.
17. Gambier, J. C., C. Pleiman, and M. R. Clark. 1994. Signal transduction by the B cell antigen receptor and its coreceptors. Annu. Rev. Immunol. 12:457.
18. Satoh, T., M. Endo, M. Nakafuku, S. Nakamura, and Y. Kaziro. 1990. Platelet-derived growth factor stimulates formation of active p21(ras)GTP complex in Swiss mouse 3T3 cells. Proc. Natl. Acad. Sci. USA 87:5993.
19. Yamanashi, Y., Y. Fukui, W. Wongsasant, Y. Kinoshita, Y. Ichimori, K. Toyoshima, and T. Yamamoto. 1992. Activation of Src-like protein-tyrosine kinase Lyn and its association with phosphatidylinositol 3-kinase upon B-cell antigen receptor-mediated signaling. Proc. Natl. Acad. Sci. USA 89:1118.
20. Cook, S. J., and M. J. O. Wakelam. 1989. Analysis of the water soluble products of phosphatidylcholine breakdown by ion exchange chromatography: bombesin and C-kinase stimulated choline generation in Swiss 3T3 cells. Biochem. J. 263: 581.
21. Reid, P. A., S. D. Gardner, D. M. Williams, and M. M. Harnett. 1997. The antigen receptors on mature and immature T lymphocytes are coupled to phosphatidyl-choline-specific phospholipase D activation. Immunology 90:250.
22. Paterson, A., R. Plevin, and M. J. O. Wakelam. 1991. Accurate measurement of sn-1,2-diradylglycerol mass in cell lipid extracts. Biochem. J. 280:829.
23. Rodriguez-Viciana, P., P. H. Warne, R. Dhang, B. Vanhaesebroeck, I. Gout, M. J. Fry, M. D. Waterfield, and J. Downward. 1994. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370:527.
24. Tordai, A., R. A. Franklin, H. Patel, A. M. Gardner, G. L. Johnson, and E. W. Gelfand. 1994. Cross-linking of surface IgM stimulates the ras/raf-1/MEK/ MAPK cascade in human B lymphocytes. J. Biol. Chem. 269:7538.
25. Casillas, A., C. Hanekom, K. Williams, R. Katz, and A. E. Nel. 1991. Stimulation of B-cells via the membrane immunoglobulin receptor or with phorbol myristate 13-acetate induces tyrosine phosphorylation and activation of a 42-kDa microtubule-associated protein-2 kinase. J. Biol. Chem. 266:19088.
26. ras pathway couples antigen receptor stimulation to induction of the primary response gene egr-1 in B lymphocytes. J. Exp. Med. 181:417.
27. Buscher, D., R. A. Hipskind, S. Krautwald, T. Reimann, and M. Baccarini. 1995. Ras-dependent and -independent pathways target the mitogen-activated protein kinase network in macrophages. Mol. Cell. Biol. 15:466.
28. Denhardt, D. T. 1996. Signal transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: the potential for multiplex signalling. Biochem. J. 318:729.
29. Bjorkoy, G., M. Perander, A. Overvatn, and T. Johansen. 1997. Reversion of Ras and phosphatidyleholine-hydrolyzing phospholipase C-mediated transformation of NIH 3T3 cells by a dominant interfering mutant of protein kinase C lambda is accompanied by the loss of constitutive nuclear mitogen-activated protein kinase/ extracellular signal regulated kinase activity. J. Biol. Chem. 272:11557.
30. Pelech, S. L. 1996. Kinase connections on the cellular internet. Curr. Biol. 6:551.
31. Berra, E., M. T. Diaz-Meco, J. Lozano, S. Frutos, M. M. Municio, P. Sanchez, L. Sanz, and J. Moscat. 1995. Evidence for a role of MEK and MAPK during signal transduction by protein kinase C ξ. EMBO J. 14:6157.
32. Yao, B., Y. H. Zhang, S. Delikat, S. Mathias, S. Basu, and R. Kolesnick. 1995. Phosphorylation of Raf by ceramide-activated protein kinase. Nature 378:307.
33. Wakelam, M. J. O. 1996. Role and regulation of phospholipase-D. Immunology 89:Sn 42.
34. Nakanishi, H., K. A. Brewer, and J. H. Exton. 1993. Activation of the ζ isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268:13.
35. 3. J. Biol. Chem. 269:32358.
36. Mischak, H., W. Kolch, J. Goodnight, W. F. Cavidson, U. Rapp, S. Rose-John, and J. F. Mushinski. 1991. Expression of PKC genes in hematopoietic cells is cell-type differentiation and B cell differentiation stage specific. J. Immunol. 147: 3981.
37. Diaz-Meco, M. T., E. Berra, M. M. Municio, L. Sanz, J. Lozano, I. Domingue, V. Diazgolpe, M. T. L. Delera, J. Alcami, C. V. Paya, F. Arenzanaseisdedos, J. R. Virelizier, and J. Moscat. 1993. A dominant negative protein kinase C ζ subspecies blocks NF-κB activation. Mol. Cell. Biol. 13:4770.
38. Diaz-Meco, M. T., I. Dominguez, L. Sanz, P. Dent, J. Lozano, M. M. Municio, R. T. Hay, T. W. Sturgill, and J. Moscat. 1994. ζPKC induces phosphorylation and inactivation of IκB-α. EMBO J. 13:2842.
39. S6k activation mediated by phosphatidylinositol-3-OH kinase. Nature 370:71.
40. Weng, Q.-P., K. Andrabi, A. Klippel, M. T. Kozlowski, L. T. Williams, and J. Avruch. 1995. Phosphatidylinositol 3-kinase signals activation of p70 S6 kinase in situ through site-specific p70 phosphorylation. Proc. Natl. Acad. Sci. USA 92:5744.
41. Harnett, W., K. M. Houston, R. Amess, and M. J. Worms. 1983. Acanthocheilonema viteae: phosphorylcholine is attached to the major excretory-secretory product via an N-linked glycan. Exp. Parasitol. 77:498.
42. Mitchell, G. F., and H. M. Lewers. 1976. Studies on immune responses to parasite antigens in mice. IV. Inhibition of an anti-DNP antibody response with antigen, DNP-Ficoll containing phosphorylcholine. Int. Arch. Allergy Appl. Immunol. 52: 235.
43. Lal, R. B., V. Kumaraswami, C. Steel, and T. B. Nutman. 1990. Phosphorylcholine-containing antigens of Brugia malayi non-specifically suppress lymphocyte function. Am. J. Trop. Med. Hyg. 42:56.
44. Cuadrado, A., A. Carnero, F. Dolfi, B. Jimenez, and J. C. Lacal. 1993. Phosphorylcholine: a novel second messenger essential for mitogenic activity of growth factors. Oncogene 8:2959.
45. Jimenez, B., L. del Peso, S. Montaner, P. Esteve, and J. C. Lacal. 1995. Generation of phosphorylcholine as an essential event in the activation of Raf-1 and MAP-kinases in growth factors-induced mitogenic stimulation. J. Cell. Biochem. 57:141.
46. Mazer, B., J. Domenico, H. Sawami, and E. W. Gelfand. 1991. Platelet-activating factor induces an increase in intracellular calcium and expression of regulatory genes in human B lymphoblastoid cells. J. Immunol. 146:1914.
47. Cundell, D. R., N. P. Gerard, C. Gerard, I. Idanpaan-Heikkila, and E. I. Tuomanen. 1995. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 377:435.
48. Mazer, B., K. L. Clay, H. Renz, and E. W. Gelfand. 1990. Platelet-activating factor enhances Ig production in B lymphoblastoid cell lines. J. Immunol. 145: 2602.
49. Franklin, R. A., B. Mazer, H. Sawami, G. B. Mills, N. Terada, J. L. Lucas, and E. W. Gelfand. 1993. Platelet-activating factor triggers the phosphorylation and activation of MAP-2 kinase and S6 peptide kinase activity in human B cell lines. J. Immunol. 151:1802.
50. Ottesen, E. A., P. F. Weller, M. Lunde, and R. Hussain. 1982. Endemic filariasis on a Pacific island. II. Immunological aspects: immunoglobulin, complement and specific antifilarial IgG, IgM and IgE antibodies. Am. J. Trop. Med. Hyg. 31:953.