An enduring association? Microfilariae and immunosupression in lymphatic filariasis

Trends in Parasitology

Volumn 19, Issue 12, 2003, Pages 565-570

  O'Connor, Richard A ^a   Jenson, Jessica S ^b   Osborne, Julie ^b   Devaney, Eileen ^b  

^a TRUDEAU INSTITUTE   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CYTOKINE; FLICE INHIBITORY PROTEIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; NITRIC OXIDE SYNTHASE INHIBITOR; PARASITE ANTIGEN; PROTEIN BCL 2; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; APOPTOSIS; B CELL LEUKEMIA; B CELL LYMPHOMA; B LYMPHOCYTE; BRUGIA MALAYI; CELL DEATH; CELL PROLIFERATION; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; ELEPHANTIASIS; FILARIASIS; HOST CELL; HUMAN; IMMUNIZATION; IMMUNOBIOLOGY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; LARVAL STAGE; LOA LOA; MACROPHAGE; MICROFILARIA; NICK END LABELING; NONHUMAN; PARASITE SURVIVAL; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; REVIEW; SCHISTOSOMA MANSONI; T LYMPHOCYTE; TH2 CELL; WUCHERERIA;

ANIMALIA; BRUGIA; BRUGIA MALAYI; LOA LOA; MURINAE; NEMATODA; SCHISTOSOMA; SCHISTOSOMA MANSONI; WUCHERERIA;

EID: 0344430170     PISSN: 14714922     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pt.2003.09.017     Document Type: Article

References (55)

1. Maizels R.M., Lawrence R.A. Immunological tolerance: the key feature in human filariasis? Parasitol. Today. 7:1991;271-276.
2. Michael E., Bundy D.A. Global mapping of lymphatic filariasis. Parasitol. Today. 13:1997;472-477.
3. Vanamail P., et al. Estimation of the fecund life span of Wuchereria bancrofti in an endemic area. Trans. R. Soc. Trop. Med. Hyg. 90:1996;119-121.
4. Lawrence R.A., Devaney E. Lymphatic filariasis: parallels between the immunology of infection in humans and mice. Parasite Immunol. 23:2001;353-362.
5. Maizels R.M., et al. Immunological genomics of Brugia malayi: filarial genes implicated in immune evasion and protective immunity. Parasite Immunol. 23:2001;327-344.
6. Hawking F., et al. The periodicity of microfilariae. XI The effect of body temperature and other stimuli upon the cycles of Wuchereria bancrofti, Brugia malayi, B. ceylonensis and Dirofilaria repens. Trans. R. Soc. Trop. Med. Hyg. 60:1966;497-513.
7. Sartono E., et al. Reversal in microfilarial density and T cell responses in human lymphatic filariasis. Parasite Immunol. 21:1999;565-571.
8. Yazdanbakhsh M., et al. T cell responsiveness correlates differentially with antibody isotype levels in clinical and asymtomatic filariasis. J. Infect. Dis. 167:1993;925-931.
9. Sartono E., et al. Depression of antigen-specific interleukin-5 and interferon-gamma responses in human lymphatic filariasis as a function of clinical status and age. J. Infect. Dis. 175:1997;1276-1280.
10. Steel C., et al. Worm burden and host responsiveness in Wuchereria bancrofti infection: use of antigen detection to refine earlier assessments from the South Pacific. Am. J. Trop. Med. Hyg. 65:2001;498-503.
11. King C.L. Transmission intensity and human immune responses to lymphatic filariasis. Parasite Immunol. 23:2001;363-371.
12. Sartono E., et al. Specific T cell unresponsiveness in human filariasis: diversity in underlying mechanisms. Parasite Immunol. 17:1995;587-594.
13. Lammie P.J., et al. Alterations in filarial antigen-specific immunologic reactivity following treatment with ivermectin and diethylcarbamazine. Am. J. Trop. Med. Hyg. 46:1992;292-295.
14. Steel C., Ottesen E.A. Evolution of immunologic responsiveness of persons living in an area of endemic bancroftian filariasis: a 17-year follow-up. J. Infect. Dis. 184:2001;73-79.
15. Leiva L.E., Lammie P.J. Regulation of parasite antigen-induced T cell unresponsiveness in Brugia pahangi infected jirds. J. Immunol. 142:1989;1304-1309.
16. King C.L., 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. 92:1993;1667-1673.
17. Mahanty S., et al. Stage-specific induction of cytokines regulates the immune response in lymphatic filariasis. Exp. Parasitol. 84:1996;282-290.
18. Doetze A., 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. 12:2000;623-630.
19. King C.L., et al. Immunological tolerance in lymphatic filariasis. Diminished parasite specific T and B lymphocyte precursor frequency in the microfilaraemic state. J. Clin. Invest. 89:1992;1403-1410.
20. Steel C., et al. Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigens. Lancet. 343:1994;890-893.
21. Lammie P.J., et al. Maternal filarial infection as a risk factor for infection in children. Lancet. 337:1991;1005-1006.
22. Schrater A.F., et al. Predisposition to Brugia malayi microfilaraemia in progeny of infected gerbils. Am. J. Trop. Med. Hyg. 32:1983;1306-1308.
23. Sartono E., et al. Elevated cellular immune responses and interferon-γ release after long-term diethylcarbamizine treatment of patients with human lymphatic filariasis. J. Infect. Dis. 171:1995;1683-1687.
24. Whelan M., et al. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 164:2000;6453-6460.
25. Semnani R.T., et al. Filarial antigens impair the function of human dendritic cells during differentiation. Infect. Immun. 69:2001;5813-5822.
26. Goodridge H.S., et al. Modulation of macrophage cytokine production by ES-62, a secreted product of the filarial nematode Acanthocheilonema viteae. J. Immunol. 167:2001;940-945.
27. Allen J.E., Loke P. Divergent roles for macrophages in lymphatic filariasis. Parasite Immunol. 23:2001;345-352.
28. O'Connor R.A., et al. NO contributes to proliferative suppression in a mouse model of filariasis. Infect. Immun. 68:2000;6101-6107.
29. Lawrence R.A., et al. Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and Ig isotype responses in BALB/c mice. J. Immunol. 153:1994;1216-1224.
30. Lawrence R.A., et al. Requirements for in vivo IFN-γ induction by live microfilariae of the parasitic nematode, Brugia malayi. Parasitology. 120:2000;631-640.
31. Pearlman E., et al. Induction of murine T helper cell responses to the filarial parasite Brugia malayi. Infect. Immun. 61:1993;1105-1112.
32. + T lymphocytes: a mechanism of immune unresponsiveness in filariasis? Eur. J. Immunol. 32:2002;858-867.
33. Allen J.E., et al. APC from mice harbouring the filarial parasite, Brugia malayi, prevent cellular proliferation but not cytokine production. Int. Immunol. 8:1996;143-151.
34. Dalton D.K., et al. Interferon-γ eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J. Exp. Med. 192:2000;117-122.
35. Chu C.-Q., et al. Failure to suppress the expansion of the activated CD4 T cell population in interferon-γ-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J. Exp. Med. 192:2000;123-128.
36. Zhang X., et al. Unequal death in T helper cell (Th) 1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J. Exp. Med. 185:1997;1837-1849.
37. Zhang L., et al. Characterisation of apoptosis resistant antigen specific T cells in vivo. J. Exp. Med. 183:1996;2065-2073.
38. Stassi G., et al. Control of target cell survival in thyroid autoimmunity by T helper cytokines via regulation of apoptotic proteins. Nat. Immunol. 1:2000;483-488.
39. Cohen S.B., et al. Interleukin-10 rescues T cells from apoptotic cell death: association with an upregulation of Bcl-2. Immunology. 92:1997;1-5.
40. Refaeli Y., et al. Interferon-γ is required for activation-induced death of T lymphocytes. J. Exp. Med. 196:2002;999-1005.
41. Zang X., et al. The serpin secreted by Brugia malayi microfilariae, Bm-SPN-2, elicits strong, but short-lived, immune responses in mice and humans. J. Immunol. 165:2000;5161-5169.
42. Hartmann S., et al. Cystatins of filarial nematodes up-regulate the nitric oxide production of interferon-gamma-activated murine macrophages. Parasite Immunol. 24:2002;253-262.
43. Taylor M.J., et al. Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. J. Exp. Med. 191:2000;1429-1435.
44. Chen L., et al. Skin-stage schistosomula of Schistosoma mansoni produce an apoptosis-inducing factor that can cause apoptosis of T cells. J. Biol. Chem. 277:2002;34329-34335.
45. Hyoh Y., et al. Activation of caspases in intestinal villus epithelial cells of normal and nematode infected rats. Gut. 50:2002;71-77.
46. Krishnamoorthy B., et al. Apoptosis induced by filarial parasitic sheath protein in Hep2 cell lines blocked by ectopic expression of bcl-2. Cell Biol Int. 22:1998;483-492.
47. Semnani R.T., et al. Brugia malayi microfilariae induce cell death in human dendritic cells, inhibit their ability to make IL-12 and IL-10, and reduce their capacity to activate CD4(+) T cells. J. Immunol. 171:2003;1950-1960.
48. Allen J.E., Maizels R.M. Th1-Th2: reliable paradigm or dangerous dogma? Immunol. Today. 18:1997;387-392.
49. Brunet L.R., et al. Nitric oxide and the Th2 response combine to prevent severe hepatic damage during Schistosoma mansoni infection. J. Immunol. 163:1999;4976-4984.
50. Estaquier J., et al. Interleukin-10-mediated T cell apoptosis during the T helper type 2 cytokine response in murine Schistosoma mansoni parasite infection. Eur. Cytokine Netw. 8:1997;153-160.
51. Oliveira D.M., et al. Role of nitric oxide on human schistosomiasis mansoni: upregulation of in vitro granuloma formation by N omega-nitro-L- arginine methyl ester. Nitric Oxide. 2:1998;57-65.
52. Kalinkovich A., et al. Decreased CD4 and increased CD8 counts with T cell activation is associated with chronic helminth infection. Clin. Exp. Immunol. 114:1998;414-421.
53. McDonald P.P., et al. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-β in macrophages that have ingested apoptotic cells. J. Immunol. 163:1999;6164-6172.
54. Gao Y., et al. Anti-inflammatory effects of CD95 ligand (FasL)-induced apoptosis. J. Exp. Med. 188:1998;887-896.
55. Gavrieli Y., et al. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.