Skip to main content
×
Home

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

  • W. HARNETT (a1), H. S. GOODRIDGE (a2) and M. M. HARNETT (a2)
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.

Copyright
Corresponding author
Department of Immunology, University of Strathclyde, Glasgow G4 0NR, UK. Tel: 0141-548-3725. Fax: 0141-548-3427. E-mail: w.harnett@strath.ac.uk
References
Hide All

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, 489500.
AKIRA, S. & TAKEDA, K. ( 2004). Toll-like receptor signalling. Nature Reviews Immunology 4, 499511.
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, 2799527998.
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, 61576163.
BRATTIG, N. W. ( 2004). Pathogenesis and host responses in human onchocerciasis: impact of Onchocerca filariae and Wolbachia endobacteria. Microbes and Infection 6, 113128.
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, 216224.
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, 466475.
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, 457486.
CAMPBELL, K. S. ( 1999). Signal transduction from the B cell antigen receptor. Current Opinion in Immunology 11, 256264.
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, 61056111.
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, 26922699.
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, 74627468.
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, 151161.
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, 1116.
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, 415425.
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, 284293.
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.
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, 940945.
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, 551563.
HARNETT, W., DEEHAN, M. D., HOUSTON, K. M. & HARNETT, M. M. ( 1999). Immunomodulatory properties of a phosphorylcholine-containing secreted filarial glycoprotein. Parasite Immunology 21, 601608.
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, 229239.
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, 48294837.
HARNETT, W. & HARNETT, M. M. ( 1999). Phosphorylcholine: Friend or foe of the immune system? Immunology Today 20, 125129.
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, 5972.
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, 498502.
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, 22792283.
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, 54665468.
KING, C. L. ( 2001). Transmission intensity and human immune responses to lymphatic filariasis. Parasite Immunology 23, 363371.
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, 10321039.
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, 5664.
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, 327344.
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, 15611568.
MITTELSTADT, P. R. & DEFRANCO, A. L. ( 1993). Induction of early response genes by crosslinking membrane Ig on B lymphocytes. Journal of Immunology 150, 48224832.
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, 257262.
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, 286290.
PELECH, S. L. ( 1996). Kinase connections on the cellular internet. Current Biology 6, 551554.
PLEIMAN, C. M., D'AMBROSIA, D. & CAMBIER, J. C. ( 1994). The B-cell antigen receptor complex: Structure and signal transduction. Immunology Today 15, 393398.
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, 36473653.
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, 155164.
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, 9198.
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, 467482.
TAKEDA, K., KAISHO, T. & AKIRA, S. ( 2003). Toll-like receptors. Annual Review of Immunology 21, 335376.
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, 11971203.
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, 2966129666.
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, 64536460.
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, 238245.
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, 463466.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 1
Total number of PDF views: 17 *
Loading metrics...

Abstract views

Total abstract views: 78 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 21st November 2017. This data will be updated every 24 hours.