Lymphocyte hyporesponsiveness during filarial nematode infection

Parasite Immunology

Volumn 30, Issue 9, 2008, Pages 447-453

  Harnett, W ^a   Harnett, M M ^b  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Excretory secretory products; Filariasis; Hyporesponsiveness; Immunomodulation; Lymphocyte; Microfilaria; Signal transduction

Indexed keywords

CD28 ANTIGEN; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4;

CELL FUNCTION; CELL INTERACTION; CELL PROLIFERATION; ENZYME ACTIVATION; FILARIASIS; HUMAN; LYMPHOCYTE; MICROFILARIA (NEMATODE LARVA); NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; FILARIOIDEA; HUMANS; IMMUNE TOLERANCE; LYMPHOCYTES; NEMATODE INFECTIONS;

MICROFILARIA (NEMATODE GENUS); NEMATODA;

EID: 49249083902     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2008.01045.x     Document Type: Review

References (68)

1. June CH, Bluestone JA, Nadler LM Thompson CB. The B7 and CD28 receptor families. Immunol Today 1994 15: 321 331.
2. Dal Porto JM, Gauld SB, Merrell KT, Mills D, Pugh-Bernard AE Cambier J. B cell antigen receptor signaling 101. Mol Immunol 2004 41: 599 613.
3. Harnett MM, Katz E Ford CA. Differential signalling during B-cell maturation. Immunol Lett 2005 98: 33 44.
4. McHeyzer-Williams MG, McHeyzer-Williams LJ, Fanelli Panus J, et al. Antigen-specific immunity. Th cell-dependent B cell responses. Immunol Res 2001 22: 223 236.
5. Balazs M, Martin F, Zhou T Kearney J. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 2002 17: 341 352.
6. Qi H, Egen JG, Huang AY Germain RN. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 2006 312: 1672 1676.
7. Greenwald RJ, Freeman GJ Sharpe AH. The B7 family revisited. Annu Rev Immunol 2005 23: 515 548.
8. Young S, Parker PJ, Ullrich A Stabel S. Downregulation of protein kinase C is due to an increased rate of degradation. Biochem J 1987 244: 775 779.
9. Subramanian S, Stolk WA, Ramaiah KD, et al. The dynamics of Wuchereria bancrofti infection: a model-based analysis of longitudinal data from Pondicherry, India. Parasitology 2004 128: 467 482.
10. Ottesen EA, Weller PF Heck L. Specific cellular immune unresponsiveness in human filariasis. Immunology 1977 33: 413 421.
11. Weiss N. Dipetalonema viteae: in vitro blastogenesis of hamster spleen and lymph node cells to phytohemagglutinin and filarial antigens. Exp Parasitol 1978 46: 283 299.
12. Dalesandro DA. Evidence for immunodepression of syrian hamsters and mongolian jirds by Dipetalonema viteae infections. Transactions Royal Soc for Trop Med Hygiene 1976 70: 534 535.
13. Weller PF. Cell-mediated immunity in experimental filariasis: lymphocyte reactivity to filarial stage-specific antigens and to B- and T-cell mitogens during acute and chronic infection. Cellular Immunol 1978 37: 369 382.
14. Lammie PJ Katz SP. Immunoregulation in experimental filariasis. I. In vitro suppression of mitogen-induced blastogenesis by adherent cells from Jirds chronically infected with Brugia pahangi. J Immunol 1983 130: 1381 1385.
15. Lammie PJ Katz SP. Immunoregulation in experimental filariasis. II. Responses to parasite and nonparasite antigens in jirds with Brugia pahangi. J Immunol 1983 130: 1386 1389.
16. O'Connor RA, Jenson JS, Osborne J Devaney E. An enduring association? Microfilariae and immunosuppression [correction of immunosupression] in lymphatic filariasis. Trends Parasitol 2003 19: 565 570.
17. O'Connor RA, Jenson JS Devaney E. NO contributes to proliferative suppression in a murine model of filariasis. Infect Immun 2000 68: 6101 6107.
18. Wadee AA, Vickery AC Piessens WF. Characterization of immunosuppressive proteins of Brugia malayi microfilariae. Acta Trop 1987 44: 343 352.
19. Soboslay PT, Dreweck CM, Taylor HR, Brotman B, Wenk P Greene BM. Experimental onchocerciasis in chimpanzees. Cell-mediated immune responses, and production and effects of IL-1 and IL-2 with Onchocerca volvulus infection. J Immunol 1991 147: 346 353.
20. Ghosh RP, Murthy PK, Tyagi K, Murthy PS Chatterjee RK. Longitudinal cellular immune responses in asymptomatic and symptomatic Brugia malayi-infected Indian leaf monkey Presbytis entellus. J Parasitol 1999 85: 861 866.
21. Graham SP, Trees AJ, Collins RA, et al. Down-regulated lymphoproliferation coincides with parasite maturation and with the collapse of both gamma interferon and interleukin-4 responses in a bovine model of onchocerciasis. Infect Immun 2001 69: 4313 4319.
22. Mahanty S Nutman TB. Immunoregulation in human lymphatic filariasis. the role of interleukin 10. Parasite Immunol 1995 17: 385 392.
23. Gopinath R, Hanna LE, Kumaraswami V, et al. Long-term persistence of cellular hyporesponsiveness to filarial antigens after clearance of microfilaremia. Am J Trop Med Hyg 1999 60: 848 853.
24. Semnani RT, Law M, Kubofcik J Nutman TB. Filaria-induced immune evasion: suppression by the infective stage of Brugia malayi at the earliest host-parasite interface. J Immunol 2004 172: 6229 6238.
25. Babu S, Blauvelt CP, Kumaraswami V Nutman TB. Regulatory networks induced by live parasites impair both Th1 and Th2 pathways in patent lymphatic filariasis: implications for parasite persistence. J Immunol 2006 176: 3248 3256.
26. King CL. Transmission intensity and human immune responses to lymphatic filariasis. Parasite Immunol 2001 23: 363 371.
27. Harnett W Parkhouse RME, eds. Structure and Function of Nematode Surface and Excretory-Secretory Products. New Delhi: M/S Narendra Publication House, 1995.
28. Weil GJ. Parasite antigenemia in lymphatic filariasis. Exp Parasitol 1990 71: 353.
29. Harnett W, Worms MJ, Grainger M, Pyke SD Parkhouse RM. Association between circulating antigen and parasite load in a model filarial system, Acanthocheilonema viteae in jirds. Parasitology 1990 101 Part 3: 435 444.
30. Dimock KA, Eberhard ML Lammie PJ. Th1-Like Antifilarial Immune-Responses Predominate In Antigen-Negative Persons. Infect Immun 1996 64: 2962 2967.
31. Piessens WF, Ratiwayanto S, Tuti S, et al. Antigen-specific suppressor cells and suppressor factors in human filariasis with Brugia malayi. N Engl J Med 1980 302: 833 837.
32. Dasgupta A, Bala S Dutta SN. Cellular unresponsiveness in patients with soluble circulating antigens in bancroftian filariasis. Indian J Med Res 1987 85: 136 139.
33. Nicolas L, Plichart C, Nguyen LN Moulia-Pelat JP. Reduction of Wuchereria bancrofti adult worm circulating antigen after annual treatments of diethylcarbamazine combined with ivermectin in French Polynesia. J Infect Dis 1997 175: 489 492.
34. Elkhalifa MY, Ghalib HW, Dafa'Alla T Williams JF. Suppression of human lymphocyte responses to specific and non-specific stimuli in human onchocerciasis. Clin Exp Immunol 1991 86: 433 439.
35. Hartmann S, Kyewski B, Sonnenburg B Lucius R. A filarial cysteine protease inhibitor downregulates T cell proliferation and enhances interleukin-10 production. European J Immunol 1997 27: 2253 2260.
36. Harnett W Harnett MM. Inhibition of murine B cell proliferation and down-regulation of protein kinase C levels by a phosphorylcholine-containing filarial excretory-secretory product. J Immunol 1993 151: 4829 4837.
37. King CL, Kumaraswami V, Poindexter RW, et al. Immunologic tolerance in lymphatic filariasis. Diminished parasite-specific T and B lymphocyte precursor frequency in the microfilaremic state. J Clin Invest 1992 89: 1403 1410.
38. Steel C, Guinea A, McCarthy JS Ottesen EA. Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigens. Lancet 1994 343: 890 893.
39. Piessens WF, Ratiwayanto S, Piessens PW, et al. Effect of treatment with diethylcarbamazine on immune responses to filarial antigens in patients infected with Brugia malayi. Acta Trop 1981 38: 227 234.
40. Steel C Nutman TB. CTLA-4 in filarial infections: implications for a role in diminished T cell reactivity. J Immunol 2003 170: 1930 1938.
41. Taylor MD, LeGoff L, Harris A, Malone E, Allen JE Maizels RM. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol 2005 174: 4924 4933.
42. Babu S, Blauvelt CP, Kumaraswami V Nutman TB. Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J Immunol 2005 175: 1170 1176.
43. Babu S, Blauvelt CP, Kumaraswami V Nutman TB. Cutting edge: diminished T cell TLR expression and function modulates the immune response in human filarial infection. J Immunol 2006 176: 3885 3889.
44. Komai-Koma M, Jones L, Ogg GS, Xu D Liew FY. TLR2 is expressed on activated T cells as a costimulatory receptor. Proc Natl Acad Sci USA 2004 101: 3029 3034.
45. Xu D, Komai-Koma M Liew FY. Expression and function of Toll-like receptor on T cells. Cell Immunol 2005 233: 85 89.
46. + regulatory T cells. Proc Natl Acad Sci USA 2006 103: 7048 7053.
47. King CL, Mahanty S, Kumaraswami V, et al. Cytokine control of parasite-specific anergy in human lymphatic filariasis. Preferential induction of a regulatory T helper type 2 lymphocyte subset. J Clin Invest 1993 92: 1667 1673.
48. Sartono E, Kruize YCM, Partono F, Kurniawan A, Maizels RM Yazdanbakhsh M. Specific T cell unresponsiveness in human filariasis: diversity in underlying mechanisms. Parasite Immunol 1995 17: 587 594.
49. Doetze A, Satoguina J, Burchard G, et al. Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T (h) 3/T (r) 1-type cytokines IL-10 and transforming growth factor-beta but not by a T (h) 1 to T (h) 2 shift. Int Immunol 2000 12: 623 630.
50. + T cell hyporesponsiveness at sites peripheral to filarial infection. J Immunol 2006 176: 6918 6927.
51. Mahanty S Nutman TB. Immunoregulation In Human Lymphatic Filariasis - the Role of Interleukin-10. Parasite Immunol 1995 17: 385 392.
52. Soboslay PT, Luder CG, Riesch S, et al. Regulatory effects of Th1-type (IFN-gamma, IL-12) and Th2-type cytokines (IL-10, IL-13) on parasite-specific cellular responsiveness in Onchocerca volvulus-infected humans and exposed endemic controls. Immunology 1999 97: 219 225.
53. Osborne J Devaney E. Interleukin-10 and antigen-presenting cells actively suppress Th1 cells in BALB/c mice infected with the filarial parasite Brugia pahangi. Infect Immun 1999 67: 1599 1605.
54. Allen JE, Lawrence RA Maizels RM. APC from mice harbouring the filarial nematode, Brugia malayi, prevent cellular proliferation but not cytokine production. Int Immunol 1996 8: 143 151.
55. Loke P, MacDonald AS, Robb A, Maizels RM Allen JE. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur J Immunol 2000 30: 2669 2678.
56. Allen JE MacDonald AS. Profound suppression of cellular proliferation mediated by the secretions of nematodes. Parasite Immunol 1998 20: 241 247.
57. Harnett W, Grainger M, Kapil A, Worms MJ Parkhouse RME. Origin, kinetics of circulation and fate in vivo of the major excretory-secretory product of Acanthocheilonema viteae. Parasitol Today 1989 99: 229 239.
58. Weil GJ Liftis F. Identification and partial characterization of a parasite antigen in sera from humans infected with Wuchereria bancrofti. J Immunol 1987 138: 3035 3041.
59. Stepek G, Houston KM, Goodridge HS, Devaney E Harnett W. Stage-specific and species-specific differences in the production of the mRNA and protein for the filarial nematode secreted product, ES-62. Parasitol Today 2004 128: 91 98.
60. Wilson EH, Deehan MR, Katz E, et al. Hyporesponsiveness of murine B lymphocytes exposed to the filarial nematode secreted product ES-62 in vivo. Immunology 2003 109: 238 245.
61. Harnett W, Deehan MD, Houston KM Harnett MM. Immunomodulatory properties of a phosphorylcholine-containing secreted filarial glycoprotein. Parasite Immunol 1999 21: 601 608.
62. Lal RB, Kumaraswami V, Steel C Nutman TB. Phosphorylcholine-containing antigens of Brugia malayi non-specifically suppress lymphocyte function. Am J Trop Med Hygiene 1990 42: 56 64.
63. Deehan M, Harnett M Harnett W. A filarial nematode secreted product differentially modulates expression and activation of protein kinase C isoforms in B lymphocytes. J Immunol 1997 159: 6105 6111.
64. Deehan MR, Frame MJ, Parkhouse RM, et al. A phosphorylcholine-containing filarial nematode-secreted product disrupts B lymphocyte activation by targeting key proliferative signaling pathways. J Immunol 1998 160: 2692 2699.
65. Harnett MM, Deehan MR, Williams DM Harnett W. Induction of signalling anergy via the T-cell receptor in cultured Jurkat T cells by pre-exposure to a filarial nematode secreted product. Parasite Immunol 1998 20: 551 563.
66. Deehan MR, Harnett W Harnett MM. 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. J Immunol 2001 166: 7462 7468.
67. Wilson EH, Katz E, Goodridge HS, Harnett M Harnett W. In vivo activation of murine peritoneal B1 cells by the filarial nematode phosphorylcholine- containing glycoprotein ES-62. Parasite Immunol 2003 25: 463 466.
68. Goodridge HS, Marshall FA, Else KJ, et al. Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. J Immunol 2005 174: 284 293.