Immunomodulation by filarial nematodes

Parasite Immunology

Volumn 27, Issue 10-11, 2005, Pages 417-429

  Hoerauf, Achim ^a   Satoguina, J ^a   Saeftel, M ^a   Specht, S ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Alternatively activated macrophages; Brugia; Confection; CTLA 4; Filariasis; GITR; IgG4; IL 10; Litomosoides; Malaria; Onchocerca; Regulatory T cells; TGF beta; Wuchereria

Indexed keywords

IMMUNOGLOBULIN G4; PARASITE ANTIGEN;

ALLERGY; B LYMPHOCYTE; DOWN REGULATION; FILARIA; FILARIASIS; GENETIC TRAIT; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCTION; IMMUNOMODULATION; INFECTION CONTROL; LARVA; MACROPHAGE ACTIVATION; MALARIA; NEMATODE; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TH1 CELL; TH2 CELL; VACCINATION;

ANIMALS; B-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FILARIASIS; FILARIOIDEA; HUMANS; IMMUNOGLOBULIN G; MACROPHAGES; MICE; T-LYMPHOCYTES, REGULATORY;

ANIMALIA; BRUGIA; LITOMOSOIDES; MURINAE; NEMATODA; ONCHOCERCA; WUCHERERIA;

EID: 26244438173     PISSN: 01419838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2005.00792.x     Document Type: Review

References (122)

1. WHO. WHO information fact sheets. Lymphatic filariasis [WWW document]. 2000. URL http://www.who.int/inf-fs/en/fact102.html.
2. WHO. WHO information fact sheets. Onchocerciasis [WWW document]. 2000. URL http://www.who.int/inf-fs/en/fact095.html.
3. Hoerauf A. Control of filarial infections: not the beginning of the end, but more research is needed. Curr Opin Infect Dis 2003; 16: 403-410.
4. Molyneux DH, Bradley M, Hoerauf A et al. Mass drug treatment for lymphatic filariasis and onchocerciasis. Trends Parasitol 2003; 19: 516-522.
5. Allen JE & Maizels RM. Th1-Th2: reliable paradigm or dangerous dogma? Immunol Today 1997; 18: 387-392.
6. Marechal P, Petit G, Diagne M et al. Use of the Litomosoides sigmodontis - mouse model in development of an Onchocerca vaccine. II - L. sigmodontis in the BALB/c mouse: vaccination experiments; preliminary immunological studies. Parasite 1994; 1: 31-32.
7. Marechal P, Goff L, Hoffmann W et al. Immune response to the filaria Litomosoides sigmodontis in susceptible and resistant mice. Parasite Immunol 1997; 19: 273-279.
8. Hoffmann W, Petit G, Schulz-Key H et al. Litomosoides sigmodontis in mice: reappraisal of an old model for filarial research. Parasitol Today 2000; 16: 387-389.
9. Trees AJ, Graham SP, Renz A et al. Onchocerca ochengi infections in cattle as a model for human onchocerciasis: recent developments. Parasitology 2000; 120: S133-S142.
10. Steel C, Guinea A, McCarthy JS et al. Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigens. Lancet 1994; 343: 890-893.
11. Elson LH, Days A, Calvopina M et al. In utero exposure to Onchocerca volvulus: relationship to subsequent infection intensity and cellular immune responsiveness. Infect Immun 1996; 64: 5061-5065.
12. Pit DS, Polderman AM, Schulz-Key H et al. Prenatal immune priming with helminth infections: parasite-specific cellular reactivity and Th1 and Th2 cytokine responses in neonates. Allergy 2000; 55: 732-739.
13. Malhotra I, Ouma JH, Wamachi A et al. Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infect Immun 2003; 71: 5231-5237.
14. Soboslay PT, Geiger SM, Drabner B et al. Prenatal immune priming in onchocerciasis-onchocerca volvulus-specific cellular responsiveness and cytokine production in newborns from infected mothers. Clin Exp Immunol 1999; 117: 130-137.
15. Terhell AJ, Wahyuni S, Pryce A et al. Antifilarial and total IgG4 and IgE antibody levels are correlated in mothers and their offspring. Trans R Soc Trop Med Hyg 2002; 96: 334-339.
16. McCarthy JS, Ottesen EA & Nutman TB. Onchocerciasis in endemic and nonendemic populations: differences in clinical presentation and immunologic findings. J Infect Dis 1994; 170: 736-741.
17. King CL, Connelly M, Alpers MP et al. Transmission intensity determines lymphocyte responsiveness and cytokine bias in human lymphatic filariasis. J Immunol 2001; 166: 7427-7436.
18. Duerr HP, Dietz K, Schulz-Key H et al. Density-dependent parasite establishment suggests infection-associated immunosuppression as an important mechanism for parasite density regulation in onchocerciasis. Trans R Soc Trop Med Hyg 2003; 97: 242-250.
19. Duerr HP, Dietz K, Schulz-Key H et al. The relationships between the burden of adult parasites, host age and the microfilarial density in human onchocerciasis. Int J Parasitol 2004; 34: 463-473.
20. Dreyer G, Noroes J, Figueredo-Silva J et al. Pathogenesis of lymphatic disease in bancroftian filariasis: a clinical perspective. Parasitol Today 2000; 16: 544-548.
21. Witt C & Ottesen EA. Lymphatic filariasis: an infection of childhood. Trop Med Int Health 2001; 6: 582-606.
22. Ottesen EA, Weil GJ, Lammie PJ et al. Towards a strategic plan for research to support the global program to eliminate lymphatic filariasis: Summary of iimmediate needs and opportunities for research on lymphatic filariasis. Am J Trop Med Hyg 2004; 71: 1-46.
23. Duke BOL. The population dynamics of Onchocerca volvulus in the human host. Trop Med Parasitol 1993; 44: 61-68.
24. Wildenburg G, Krömer M & Büttner DW. Dependence of eosinophil granulocyte infiltration into nodules on the presence of microfilariae producing Onchocerca volvulus. Parasitol Res 1996; 82: 117-124.
25. Korten S, Wildenburg G, Darge K et al. Mast cells in onchocercomas from patients with hyperreactive onchocerciasis (sowda). Acta Trop 1998; 70: 217-231.
26. Hoerauf A & Brattig N. Resistance and susceptibility in human onchocerciasis - beyond Th1 vs. Th2. Trends Parasitol 2002; 18: 25-31.
27. Greene BM, Fanning MM & Ellner JJ. Nonspecific suppression of antigen-induced lymphocyte blastogenesis in Onchocerca volvulus infection in man. Clin Exp Immunol 1983; 52: 259-265.
28. Elson LH, Calvopina HM, Paredes YW et al. Immunity to onchocerciasis: putative immune persons produce a Th1-like response to Onchocerca volvulus. J Infect Dis 1995; 171: 652-658.
29. + T cells from putatively immune individuals. Int Immunol 1997; 9: 721-729.
30. Sartono E, Kruize YC, Kurniawan A 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 1997; 175: 1276-1280.
31. Doetze A, Satoguina J, Burchard G et al. Antigen-specific cellular hyporesponsiveness in generalized onchocerciasis is mediated by Th3/Tr1-type cytokines IL-10 and TGF-beta but not by a Th1 to Th2 shift. Int Immunol 2000; 12: 623-630.
32. Brattig NW, Lepping B, Timmann C et al. Onchocerca volvulus-exposed persons fail to produce interferon-gamma in response to O. volvulus antigen but mount proliferative responses with interleukin 5 and IL-13 production that decrease with increasing microfilarial density. J Infect Dis 2002; 185: 1148-1154.
33. + T cells from microfilaraemic subjects compared with amicrofilaraemics. Clin Exp Immunol 1997; 108: 272-278.
34. Timmann C, Abraha RS, Hamelmann C et al. Cutaneous pathology in onchocerciasis associated with pronounced systemic T-helper 2-type responses to Onchocerca volvulus. Br J Dermatol 2003; 149: 782-787.
35. 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.
36. Mahanty S & Nutman TB. Immunoregulation in human lymphatic filariasis: the role of interleukin 10. Parasite Immunol 1995; 17: 385-392.
37. Cooper PJ, Mancero T, Espinel M et al. Early human infection with Onchocerca volvulus is associated with an enhanced parasite-specific cellular immune response. J Infect Dis 2001; 183: 1662-1668.
38. Henry NL, Law M, Nutman TB et al. Onchocerciasis in a non-endemic population: clinical and immunologic assessment before treatment and at the time of presumed cure. J Infect Dis 2001; 183: 512-516.
39. Yazdanbakhsh M, van den Biggelaar A & Maizels RM. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol 2001; 22: 372-377.
40. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997; 389: 737-742.
41. Satoguina J, Mempel M, Larbi J et al. Antigen-specific T-regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect 2002; 4: 1291-1300.
42. Steel C & Nutman TB. Ctla-4 in filarial infections: implications for a role in diminished T-cell reactivity. J Immunol 2003; 170: 1930-1938.
43. Satoguina J, Weyand E, Larbi J et al. T-regulatory-1 cells induce IgG4 production by B cells: role of IL-10. J Immunol 2005; 174: 4718-4726.
44. Atmadja AK, Atkinson R, Sartono E et al. Differential decline in filaria-specific IgG1, IgG4, and IgE antibodies in Brugia malayi-infected patients after diethylcarbamazine chemotherapy. J Infect Dis 1995; 172: 1567-1572.
45. Groux H. An overview of regulatory T cells. Microbes Infect 2001; 3: 883-889.
46. Bach JF. Regulatory T cells under scrutiny. Nat Rev Immunol 2003; 3: 189-198.
47. Bluestone JA & Abbas AK. Natural versus adaptive regulatory T cells. Nat Rev Immunol 2003; 3: 253-257.
48. Mittrücker HW & Kaufmann SH. Mini-review: regulatory T cells and infection: suppression revisited. Eur J Immunol 2004; 34: 306-312.
49. Maizels RM, Balic A, Gomez-Escobar N et al. Helminth parasites - masters of regulation. Immunol Rev 2004; 201: 89-116.
50. Taylor MD, LeGoff L, Harris A et al. Removal of regulatory T-cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol 2005; 174: 4924-4933.
51. Hoerauf A, Kruse S, Brattig NW et al. The variant Arg110Gln of human IL-13 is associated with an immunologically hyperreactive form of onchocerciasis (sowda). Microbes Infect 2002; 4: 37-42.
52. Timmann C, Fuchs S, Thoma C et al. Promoter haplotypes of the interleukin 10 gene influence proliferation of peripheral blood cells in response to helminth antigen. Genes Immun 2004; 5: 256-260.
53. Terhell AJ, Houwing-Duistermaat JJ, Ruiterman Y et al. Clustering of Brugia malayi infection in a community in South Sulawesi, Indonesia. Parasitology 2000; 120: 23-29.
54. Semnani RT, Law M, Kubofcik J et al. Filaria-induced immune evasion: suppression by the infective stage of Brugia malayi at the earliest host-parasite interface. J Immunol 2004; 172: 6229-6238.
55. + T cells. J Immunol 2003; 171: 1950-1960.
56. Brattig NW, Bazzocchi C, Kirschning CJ et al. The major surface protein of Wolbachia endosymbionts in filarial nematodes elicits immune responses through TLR2 and TLR4. J Immunol 2004; 173: 437-445.
57. Brattig NW, Rathjens U, Ernst M et al. Lipopolysaccharide-like molecules derived from Wolbachia endobacteria of the filaria Onchocerca volvulus are candidate mediators in the sequence of inflammatory and anti-inflammatory responses of human monocytes. Microbes Infect 2000; 2: 1147-1157.
58. Taylor MJ, Cross HF & Bilo K. Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. J Exp Med 2000; 191: 1429-1436.
59. Loke P, Nair MG, Parkinson J et al. IL-4-dependent alternatively- activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol 2002; 3: 7.
60. Hoerauf A, Kaifi J & Büttner DW. TGF-beta and suppression of Th2-mediated hyperreactivity in a chronic human helminth infection (onchocerciasis). Am J Trop Med Hyg 2003; 69 (Suppl): 566.
61. Hesse M, Modolell M, La Flamme AC et al. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of 1-arginine metabolism. J Immunol 2001; 167: 6533-6544.
62. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003; 3: 23-35.
63. Petit G, Diagne M, Marechal P et al. Maturation of the filaria Litomosoides sigmodontis in BALB/C Mice; Comparative Susceptibility of Nine Other Inbred Strains. Ann Parasitol Hum Comp 1992; 67: 144-150.
64. + T cells in controlling larval development. Infect Immun 1997; 65: 2457-2461.
65. Le Goff L, Martin C, Oswald IP et al. Parasitology and immunology of mice vaccinated with irradiated Litomosoides sigmodontis larvae. Parasitology 2000; 120: 271-280.
66. Martin C, Le Goff L, Ungeheuer MN et al. Drastic reduction of a filarial infection in eosinophilic IL-5 transgenic mice. Infect Immun 2000; 68: 3651-3656.
67. Al-Qaoud KM, Pearlman E, Klukowski J et al. A new mechanism for IL-5-dependent helminth control: neutrophil accumulation and neutrophil-mediated worm encapsulation in murine filariasis are abolished in the absence of IL-5. Int Immunol 2000; 12: 899-908.
68. Volkmann L, Bain O, Saeftel M et al. Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different worm developmental stages. Med Microbiol Immunol 2003; 192: 23-31.
69. Saeftel M, Volkmann L, Korten S et al. Lack of IFN-γ confers impaired neutrophil granulocyte function and imparts prolonged survival of adult filarial worms in murine filariasis. Microbes Infect 2001; 3: 203-213.
70. Le Goff L, Marechal P, Petit G et al. Early reduction of the challenge recovery rate following immunization with irradiated infective larvae in a filaria mouse system. Trop Med Int Health 1998; 2: 1170-1174.
71. Martin C, Al-Qaoud KM, Bain O et al. IL-5 is essential for protection after immunization against murine filariasis but not during primary infection. Med Microbiol Immunol 2000; 189: 67-74.
72. Martin C, Saeftel M, Vuong PN et al. B-cell deficiency suppresses vaccine-induced protection against murine filariasis but does not increase the recovery rate for primary infection. Infect Immun 2001; 69: 7067-7073.
73. Le Goff L, Lamb TJ, Graham AL et al. IL-4 is required to prevent filarial nematode development in resistant but not susceptible strains of mice. Int J Parasitol 2002; 32: 1277-1284.
74. Babu S, Ganley LM, Klei TR et al. Role of gamma interferon and interleukin 4 in host defense against the human filarial parasite Brugia malayi. Infect Immun 2000; 68: 3034-3035.
75. Saeftel M, Arndt M, Specht S et al. Synergism of gamma interferon and interleukin 5 in the control of murine filariasis. Infect Immun 2003; 71: 6978-6985.
76. Lawrence RA, Allen JE, Osborne J 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 1994; 153: 1216-1224.
77. Pearlman E, Hazlett FE, Boom WH et al. Induction of murine T-helper cell responses to the filarial nematode Brugia malayi. Infect Immun 1993; 61: 1105-1112.
78. Lawrence RA, Allen JE & Gray CA. Requirements for in vivo IFN-gamma induction by live microfilariae of the parasitic nematode, Brugia malayi. Parasitology 2000; 120: 631-640.
79. Taylor M & Hoerauf A. Wolbachia bacteria of filarial nematodes. Parasitol Today 1999; 15: 437-442.
80. Bandi C, Trees AJ & Brattig NW. Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol 2001; 98: 215-238.
81. Taylor GA, Collazo CM, Yap GS et al. Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc Natl Acad Sci USA 2000; 97: 751-755.
82. Gillian V, Lawrence RA & Devaney E. B cells play a regulatory role in mice infected with the L3 of Brugia pahangi. Int Immunol 2005; 17: 373-382.
83. Hoffmann WH, Pfaff AW, Schulz-Key H et al. Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis. Parasitology 2001; 122: 641-649.
84. Specht S, Volkmann L, Wynn T et al. Interleukin 10 (IL-10) counter-regulates IL-4-dependent effector mechanisms in murine filariasis. Infect Immun 2004; 72: 6287-6293.
85. Lang R, Rutschman RL, Greaves DR et al. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J Immunol 2002; 168: 3402-3411.
86. Hoerauf A, Kaifi J, Specht S et al. TGF-beta mediates suppression of Th2-dependent inflammation in chronic human helminth infection. Int J Med Microbiol 2004; 294S1: 195.
87. Beall MJ, McGonigle S & Pearce EJ. Functional conservation of Schistosoma mansoni smads in TGF-beta signaling. Mol Biochem Parasitol 2000; 111: 131-142.
88. Zang X, Taylor P, Wang JM et al. Homologues of human macrophage migration inhibitory factor from a parasitic nematode. Gene cloning, protein activity, and crystal structure. J Biol Chem 2002; 277: 44261-44267.
89. Falcone FH, Loke P, Zang X et al. A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection. J Immunol 2001; 167: 5348-5354.
90. Hartmann S & Lucius R. Modulation of host-immune responses by nematode cystatins. Int J Parasitol 2003; 33: 1291-1302.
91. Hartmann S, Kyewski B, Sonnenburg B et al. A filarial cysteine protease inhibitor down-regulates T-cell proliferation and enhances interleukin 10 production. Eur J Immunol 1997; 27: 2253-2260.
92. Zang X, Yazdanbakhsh M, Jiang H et al. A novel serpin expressed by blood-borne microfilariae of the parasitic nematode Brugia malayi inhibits human neutrophil serine proteinases. Blood 1999; 94: 1418-1428.
93. Zang X, Atmadja AK, Gray P 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 2000; 165: 5161-5169.
94. Tawill S, Le Goff L, Ali F et al. Both free-living and parasitic nematodes induce a characteristic Th2 response that is dependent on the presence of intact glycans. Infect Immun 2004; 72: 398-407.
95. Stepek G, Auchie M, Tate R et al. Expression of the filarial nematode phosphorylcholine-containing glycoprotein, ES62, is stage-specific. Parasitology 2002; 125: 155-164.
96. Goodridge HS, Wilson EH, Harnett W et al. Modulation of macrophage cytokine production by ES-62, a secreted product of the filarial nematode Acanthocheilonema viteae. J Immunol 2001; 167: 940-945.
97. Velupillai P, Posey C, Hoerauf AM et al. B-cell outgrowth and ligand-specific production of IL-10 correlate with Th2 dominance in certain parasitic diseases. Exp Parasitol 1996; 84: 168-177.
98. Hoerauf A, Volkmann L, Hamelmann C et al. Endosymbiotic bacteria in worms as targets for a novel chemotherapy in filariasis. Lancet 2000; 355: 1242-1243.
99. Hoerauf A, Mand S, Adjei O et al. Depletion of Wolbachia endobacteria in Onchocerca volvulus by doxycycline and microfilaridermia after ivermectin treatment. Lancet 2001; 357: 1415-1416.
100. Hoerauf A, Mand S, Volkmann L et al. Doxycycline in the treatment of human onchocerciasis: kinetics of Wolbachia endobacteria reduction and of inhibition of embryogenesis in female Onchocerca worms. Microbes Infect 2003; 5: 261-273.
101. Langworthy S, Renz A, Mackenstedt U et al. Macrofilaricidal activity of tetracycline against the filarial nematode, Onchocerca ochengi: elimination of Wolbachia preceeds worm death and suggests a dependent relationship. Proc R Soc Lond B Biol Sci 2000; 267: 1063-1069.
102. Taylor MJ, Makunde WH, McGarry HF et al. Macrofilaricidal activity following doxycycline treatment of Wuchereria bancrofti: a double-blind randomised controlled trial. Lancet 2005; 365: 2116-2121.
103. St. André A, Blackwell NM, Hall LR et al. A critical role for endosymbiotic Wolbachia bacteria and TLR4 signaling in the pathogenesis of river blindness. Science 2002; 295: 1892-1895.
104. Punkosdy GA, Addiss DG & Lammie PJ. Characterization of antibody responses to Wolbachia surface protein in humans with lymphatic filariasis. Infect Immun 2003; 71: 5104-5114.
105. Chirgwin SR, Coleman SU, Porthouse KH et al. Removal of Wolbachia from Brugia pahangi is closely linked to worm death and fecundity but does not result in altered lymphatic lesion formation in Mongolian gerbils (Meriones unguiculatus). Infect Immun 2003; 71: 6986-6994.
106. Foster J, Ganatra M, Kamal I et al. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 2005; 3: e121.
107. Gilette-Ferguson I, Hise A, Sun Y et al. Wolbachia and Onchocerca volvulus-induced keratitis (river blindness) is dependent on MyD88, TLR2 and TLR4, but not TLR9. Infect Immun 2005; in press.
108. Pfarr KM, Fischer K & Hoerauf A. Involvement of Toll-like receptor 4 in the embryogenesis of the rodent filaria Litomosoides sigmodontis. Med Microbiol Immunol 2003; 192: 53-56.
109. Brattig N, Büttner DW & Hoerauf A. Neutrophil accumulation around Onchocerca worms and chemotaxis of neutrophils are dependent on Wolbachia endobacteria. Microbes Infect 2001; 3: 439-446.
110. Cooper PJ, Espinel I, Paredes W et al. Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin 10. J Infect Dis 1998; 178: 1133-1138.
111. Nookala S, Srinivasan S, Kaliraj P et al. Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infect Immun 2004; 75: 2598-2604.
112. Yazdanbakhsh M, Kremsner PG & van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002; 296: 490-494.
113. van den Biggelaar AH, van Ree R, Rodrigues LC et al. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin 10. Lancet 2000; 356: 1723-1727.
114. van den Biggelaar AH, Rodrigues LC, van Ree R et al. Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. J Infect Dis 2004; 189: 892-900.
115. Pearlman E, Kazura JW, Hazlett FE et al. Modulation of murine cytokine responses to mycobacterial antigens by helminth-induced T-helper 2 cell responses. J Immunol 1993; 151: 4857-4864.
116. Stewart GR, Boussinesq M, Coulson T et al. Onchocerciasis modulates the immune response to mycobacterial antigens. Clin Exp Immunol 1999; 117: 517-523.
117. Nacher M, Gay F, Singhasivanon P et al. Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol 2000; 22: 107-113.
118. Nacher M, Singhasivanon P, Traore B et al. Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. Am J Trop Med Hyg 2002; 66: 304-309.
119. Nacher M, Singhasivanon P, Yimsamran S et al. Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J Parasitol 2002; 88: 55-58.
120. Spiegel A, Tall A, Raphenon G et al. Increased frequency of malaria attacks in subjects coinfected by intestinal worms and Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 2003; 97: 198-199.
121. Graham AL, Lamb TJ, Read AF et al. Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. J Infect Dis 2005; 191: 410-421.
122. Yan Y, Inuo G, Akao N et al. Down-regulation of murine susceptibility to cerebral malaria by inoculation with third-stage larvae of the filarial nematode Brugia pahangi. Parasitology 1997; 114: 333-338.