Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-22T18:55:10.608Z Has data issue: false hasContentIssue false
  • English
  • Français

Subversion of immune cell signal transduction pathways by the secreted filarial nematode product, ES-62

Published online by Cambridge University Press:  11 November 2005

W. HARNETT ,
H. S. GOODRIDGE  and
M. M. HARNETT
W. HARNETT
Affiliation:
Department of Immunology, University of Strathclyde, Glasgow G4 0NR, UK
H. S. GOODRIDGE
Affiliation:
Division of Immunology, Infection and Inflammation, University of Glasgow, G11 6NT, UK
M. M. HARNETT
Affiliation:
Division of Immunology, Infection and Inflammation, University of Glasgow, G11 6NT, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Filarial nematodes achieve longevity within the infected host by suppressing and modulating the host immune response. To do this, the worms actively secrete products that have been demonstrated to possess immunomodulatory properties. In this article we discuss the immunomodulatory effects of the phosphorylcholine-containing filarial nematode secreted glycoprotein ES-62. In particular we describe how it modulates intracellular signal transduction pathways in a number of different cells of the immune system, in particular B-lymphocytes, T-lymphocytes, macrophages and dendritic cells.

Keywords

ES-62filarial nematodeimmune system cellssignal transduction
Type
Research Article
Information
Parasitology , Volume 130 , Issue S1 , March 2005 , pp. S63 - S68
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ACKERMAN, C. J., HARNETT, M. M., HARNETT, W., KELLY, S. M., SVERGUN, D. I. & BYRON, O. ( 2003). 19 A solution structure of the filarial nematode immunomodulatory protein, ES-62. Biophysical Journal 84, 489–500.CrossRefGoogle Scholar
AKIRA, S. & TAKEDA, K. ( 2004). Toll-like receptor signalling. Nature Reviews Immunology 4, 499–511.CrossRefGoogle Scholar
BAGRODIA, S., DERIJARD, B., DAVIS, R. J. & CERIONE, R. A. ( 1995). Cdc42 and Pak-mediated signaling leads to Jun kinase and P38 mitogen-activated protein-kinase activation. Journal of Biological Chemistry 270, 27995–27998.Google Scholar
BERRA, E., DIAZ-MECO, M. T., LOZANO, J., FRUTOS, S., MUNICIO, M. M., SANCHEZ, P., SANZ, L. & MOSCAT, J. ( 1995). Evidence for a role of MEK and MAPK during signal transduction by protein kinase C ξ. EMBO Journal 14, 6157–6163.Google Scholar
BRATTIG, N. W. ( 2004). Pathogenesis and host responses in human onchocerciasis: impact of Onchocerca filariae and Wolbachia endobacteria. Microbes and Infection 6, 113–128.CrossRefGoogle Scholar
BRICKGHANNAM, C., ERICSON, M. L., SCHELLE, I. & CHARRON, D. ( 1994). Differential regulation of mRNAs encoding protein kinase C isoenzymes in activated human B cells. Human Immunology 41, 216–224.CrossRefGoogle Scholar
BUSCHER, D., HIPSKIND, R. A., KRAUTWALD, S., REIMANN, T. & BACCARINI, M. ( 1995). Ras-dependent and -independent pathways target the mitogen-activated protein kinase network in macrophages. Molecular Cell Biology 15, 466–475.CrossRefGoogle Scholar
CAMBIER, J. C., PLEIMAN, C. & CLARK, M. R. ( 1994). Signal transduction by the B cell antigen receptor and its coreceptors. Annual Review of Immunology 12, 457–486.CrossRefGoogle Scholar
CAMPBELL, K. S. ( 1999). Signal transduction from the B cell antigen receptor. Current Opinion in Immunology 11, 256–264.CrossRefGoogle Scholar
DEEHAN, M., HARNETT, M. & HARNETT, W. ( 1997). A filarial nematode secreted product differentially modulates expression and activation of protein kinase C isoforms in B lymphocytes. Journal of Immunology 159, 6105–6111.Google Scholar
DEEHAN, M. R., FRAME, M. J., PARKHOUSE, R. M., SEATTER, S. D., REID, S. D., HARNETT, M. M. & HARNETT, W. ( 1998). A phosphorylcholine-containing filarial nematode-secreted product disrupts B lymphocyte activation by targeting key proliferative signaling pathways. Journal of Immunology 160, 2692–2699.Google Scholar
DEEHAN, M. R., HARNETT, W. & HARNETT, M. M. ( 2001). A filarial nematode-secreted phosphorylcholine-containing glycoprotein uncouples the B cell antigen receptor from extracellular signal-regulated kinase-mitogen-activated protein kinase by promoting the surface Ig-mediated recruitment of Src homology 2 domain-containing tyrosine phosphatase-1 and Pac-1 mitogen-activated kinase-phosphatase. Journal of Immunology 166, 7462–7468.CrossRefGoogle Scholar
FRANCIS, D. A., KARRAS, J. G., KE, X. Y., SEN, R. & ROTHSTEIN, T. L. ( 1995). Induction of the transcription factors NF-kappaB, AP-1 and NF-AT during B cell stimulation through the CD40 receptor. International Immunology 7, 151–161.CrossRefGoogle Scholar
GOODRIDGE, H. S., DEEHAN, M. R., HARNETT, W. & HARNETT, M. M. ( 2005 a). Subversion of immunological signalling by a filarial nematode phosphorylcholine-containing secreted product. Cell Signalling, 17, 11–16.Google Scholar
GOODRIDGE, H. S., HARNETT, W., LIEW, F. Y. & HARNETT, M. M. ( 2003). Differential regulation of interleukin-12 p40 and p35 induction via Erk mitogen-activated protein kinase-dependent and -independent mechanisms and the implications for bioactive IL-12 and IL-23 responses. Immunology, 109, 415–425.CrossRefGoogle Scholar
GOODRIDGE, H. S., MARSHALL, F. A., ELSE, K. J., HOUSTON, K. M., EGAN, C., AL-RIYAMI, L., LIEW, F. Y., HARNETT, W. & HARNETT, M. M. ( 2005 b). Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. Journal of Immunology 174, 284–293.Google Scholar
GOODRIDGE, H. S., STEPEK, G., HARNETT, W. & HARNETT, M. M. ( 2005 c). Signalling mechanisms underlying subversion of the immune response by a filarial nematode secreted product. Immunology, In press.Google Scholar
GOODRIDGE, H. S., WILSON, E. H., HARNETT, W., CAMPBELL, C. C., HARNETT, M. M. & LIEW, F. Y. ( 2001). Modulation of macrophage cytokine production by ES-62, a secreted product of the filarial nematode Acanthocheilonema viteae. Journal of Immunology 167, 940–945.CrossRefGoogle Scholar
HARNETT, M. M., DEEHAN, M. R., WILLIAMS, D. M. & HARNETT, W. ( 1998). Induction of signalling anergy via the T-cell receptor in cultured Jurkat T cells by pre-exposure to a filarial nematode secreted product. Parasite Immunology, 20, 551–563.CrossRefGoogle Scholar
HARNETT, W., DEEHAN, M. D., HOUSTON, K. M. & HARNETT, M. M. ( 1999). Immunomodulatory properties of a phosphorylcholine-containing secreted filarial glycoprotein. Parasite Immunology 21, 601–608.CrossRefGoogle Scholar
HARNETT, W., GRAINGER, M., KAPIL, A., WORMS, M. J. & PARKHOUSE, R. M. E. ( 1989). Origin, kinetics of circulation and fate in vivo of the major excretory-secretory product of Acanthocheilonema viteae. Parasitology Today 99, 229–239.CrossRefGoogle Scholar
HARNETT, W. & HARNETT, M. M. ( 1993). Inhibition of murine B cell proliferation and down-regulation of protein kinase C levels by a phosphorylcholine-containing filarial excretory-secretory product. Journal of Immunology 151, 4829–4837.Google Scholar
HARNETT, W. & HARNETT, M. M. ( 1999). Phosphorylcholine: Friend or foe of the immune system? Immunology Today 20, 125–129.Google Scholar
HARNETT, W., HARNETT, M. M. & BYRON, O. ( 2003). Structural/functional aspects of ES-62 – a secreted immunomodulatory phosphorylcholine-containing filarial nematode glycoprotein. Current Protein and Peptide Science 4, 59–72.CrossRefGoogle Scholar
HARNETT, W., HOUSTON, K. M., AMESS, R. & WORMS, M. J. ( 1993). Acanthocheilonema viteae: phosphorylcholine is attached to the major excretory-secretory product via an N-linked glycan. Experimental Parasitology 77, 498–502.CrossRefGoogle Scholar
HARNETT, W. & PARKHOUSE, R. M. E. (Eds.) ( 1995). Structure and Function of Nematode Surface and Excretory-Secretory Products, M/S Narendra Publication House, New Delhi.
HORNBECK, P., HUANG, K. P. & PAUL, W. E. ( 1988). Lamin B is rapidly phosphorylated in lymphocytes after activation of protein kinase C. Proceedings of the National Academy of Sciences, USA 85, 2279–2283.CrossRefGoogle Scholar
HOUSTON, K., WILSON, E. H., EYRES, L., BROMBACHER, F., HARNETT, M. M., ALEXANDER, J. & HARNETT, W. ( 2000). The presence of phosphorylcholine on a filarial nematode protein influences the IgG subclass response to a molecule and by a mechanism dependent on IL-10. Infection and Immunity 68, 5466–5468.CrossRefGoogle Scholar
KING, C. L. ( 2001). Transmission intensity and human immune responses to lymphatic filariasis. Parasite Immunology 23, 363–371.CrossRefGoogle Scholar
KLEMSZ, M. J., JUSTEMENT, L. B., PALMER, E. & CAMBIER, J. C. ( 1989). Induction of c-fos and c-myc expression during B cell activation by IL-4 and immunoglobulin binding ligands. Journal of Immunology 143, 1032–1039.Google Scholar
LAL, R. B., KUMARASWAMI, V., STEEL, C. & NUTMAN, T. B. ( 1990). Phosphorylcholine-containing antigens of Brugia malayi non-specifically suppress lymphocyte function. American Journal of Tropical Medicine and Hygiene 42, 56–64.CrossRefGoogle Scholar
MAIZELS, R. M., BLAXTER, M. L. & SCOTT, A. L. ( 2001). Immunological genomics of Brugia malayi: filarial genes implicated in immune evasion and protective immunity. Parasite Immunology 23, 327–344.CrossRefGoogle Scholar
MILLER, Y. I., VIRIYAKOSOL, S., BINDER, C. J., FERAMISCO, J. R., KIRKLAND, T. N. & WITZTUM, J. L. ( 2003). Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. Journal of Biological Chemistry 278, 1561–1568.CrossRefGoogle Scholar
MITTELSTADT, P. R. & DEFRANCO, A. L. ( 1993). Induction of early response genes by crosslinking membrane Ig on B lymphocytes. Journal of Immunology 150, 4822–4832.Google Scholar
NOR, Z. M., HOUSTON, K. M., DEVANEY, E. & HARNETT, W. ( 1997). Variation in the nature of attachment of phosphorylcholine to excretory-secretory products of adult Brugia pahangi. Parasitology Today 114, 257–262.CrossRefGoogle Scholar
O'NEILL, L. A., FITZGERALD, K. A. & BOWIE, A. G. ( 2003). The Toll-IL-1 receptor adaptor family grows to five members. Trends in Immunology 24, 286–290.CrossRefGoogle Scholar
PELECH, S. L. ( 1996). Kinase connections on the cellular internet. Current Biology 6, 551–554.CrossRefGoogle Scholar
PLEIMAN, C. M., D'AMBROSIA, D. & CAMBIER, J. C. ( 1994). The B-cell antigen receptor complex: Structure and signal transduction. Immunology Today 15, 393–398.CrossRefGoogle Scholar
SEYFERT, V. L., McMAHON, S., GLENN, W., CAO, X., SUKHATME, V. P. & MONROE, J. G. ( 1990). Egr-1 expression in surface Ig-mediated B cell activation. Journal of Immunology 145, 3647–3653.Google Scholar
STEPEK, G., AUCHIE, M., TATE, R., WATSON, K., RUSSELL, D. G., DEVANEY, E. & HARNETT, W. ( 2002). Expression of the filarial nematode phosphorylcholine-containing glycoprotein, ES-62, is stage-specific. Parasitology Today 125, 155–164.Google Scholar
STEPEK, G., HOUSTON, K. M., GOODRIDGE, H. S., DEVANEY, E. & HARNETT, W. ( 2004). Stage-specific and species-specific differences in the production of the mRNA and protein for the filarial nematode secreted product, ES-62. Parasitology Today 128, 91–98.CrossRefGoogle Scholar
SUBRAMANIAN, S., STOLK, W. A., RAMAIAH, K. D., PLAISIER, A. P., KRISHNAMOORTHY, K., VAN OORTMARSSEN, G. J., DOMINIC AMALRAJ, D., HABBEMA, J. D. & DAS, P. K. ( 2004). The dynamics of Wuchereria bancrofti infection: a model-based analysis of longitudinal data from Pondicherry, India. Parasitology 128, 467–482.CrossRefGoogle Scholar
TAKEDA, K., KAISHO, T. & AKIRA, S. ( 2003). Toll-like receptors. Annual Review of Immunology 21, 335–376.CrossRefGoogle Scholar
WALTON, K. A., COLE, A. L., YEH, M., SUBBANAGOUNDER, G., KRUTZIK, S. R., MODLIN, R. L., LUCAS, R. M., NAKAI, J., SMART, E. J., VORA, D. K. & BERLINER, J. A. ( 2003 a). Specific phospholipid oxidation products inhibit ligand activation of toll-like receptors 4 and 2. Arteriosclerosis, Thrombosis and Vascular Biology 23, 1197–1203.Google Scholar
WALTON, K. A., HSIEH, X., GHARAVI, N., WANG, S., WANG, G., YEH, M., COLE, A. L. & BERLINER, J. A. ( 2003 b). Receptors involved in the oxidized 1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphorylcholine-mediated synthesis of interleukin-8. A role for Toll-like receptor 4 and a glycosylphosphatidylinositol-anchored protein. Journal of Biological Chemistry 278, 29661–29666.Google Scholar
WHELAN, M., HARNETT, M. M., HOUSTON, K. M., PATEL, V., HARNETT, W. & RIGLEY, K. P. ( 2000). A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 Cells. Journal of Immunology 164, 6453–6460.CrossRefGoogle Scholar
WHO ( 2000). Filariasis. World Health Organisation, Geneva.
WILSON, E. H., DEEHAN, M. R., KATZ, E., BROWN, K. S., HOUSTON, K. M., O'GRADY, J., HARNETT, M. M. & HARNETT, W. ( 2003 a). Hyporesponsiveness of murine B lymphocytes exposed to the filarial nematode secreted product ES-62 in vivo. Immunology 109, 238–245.Google Scholar
WILSON, E. H., KATZ, E., GOODRIDGE, H. S., HARNETT, M. & HARNETT, W. ( 2003 b). In vivo activation of murine peritoneal B1 cells by the filarial nematode phosphorylcholine-containing glycoprotein ES-62. Parasite Immunology 25, 463–466.Google Scholar