In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults

Journal of Clinical Investigation

Volumn 99, Issue 7, 1997, Pages 1759-1766

  Malhotra, Indu ^a   Ouma, John ^b   Wamachi, Alex ^c   Kioko, John ^b   Mungai, Peter ^b   Omollo, Adams ^b   Elson, Lynne ^a   Koech, Davy ^c   Kazura, James W ^a   King, Christopher L ^a,d  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b Division of Vector Borne Diseases   (Kenya)

^c KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cytokines; filariasis; neonates; schistosomiasis; tuberculosis

Indexed keywords

CYTOKINE; PARASITE ANTIGEN;

ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN SPECIFICITY; ARTICLE; ENDEMIC DISEASE; FILARIASIS; HELMINTHIASIS; HUMAN; HUMAN CELL; KENYA; PRIORITY JOURNAL; SCHISTOSOMIASIS; SENSITIZATION; TUBERCULOSIS; UMBILICAL CORD BLOOD;

EID: 0030974934     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119340     Document Type: Article

References (55)

1. Lewert, R.M., and S. Mandlowitz. 1969. Schistosomiasis: Prenatal induction of tolerance to antigens. Nature (Lond.). 224:1029-1030.
2. Klei, T.R., D.P. Blanchard, and S.U. Coleman. 1986. Development of Brugia pahangi infections and lymphatic lesions in male offspring of female jirds with homologous infections. Trans. R. Soc. Trop. Med. Hyg. 80:214-216.
3. Billingham, R., L. Brent, and P.B. Medawar. 1953. Actively acquired tolerance of foreign cells. Nature (Lond.). 172:603-605.
4. Burnet, F., and F. Fenner. 1949. The Production of Antibodies. MacMillan, Melbourne. 102-105 pp.
5. Weil, G.J., R. Hussain, V. Kumaraswami, S.P. Tripathy, K.S. Phillips, and E.A. Ottesen. 1983. Prenatal allergic sensitization to helminth antigens in offspring of parasite-infected mothers. J. Clin. Invest. 71:1124-1129.
6. Steel, C., A. Guinea, J.S. McCarthy, and E.A. Ottesen. 1994. Long-term effect of prenatal exposure to maternal microfilaremia on immune responsiveness to filarial parasite antigens. Lancet. 343:890-893.
7. King, C.L., and T.B. Nutman. 1991. Regulation of the immune response in lymphatic filariasis and onchocerciasis. Immunol. Today. 12:A54-A58.
8. Newport, G.R., and D.G. Colley. 1993. Schistosomiasis. In Immunology and Molecular Biology of Parasitic Infections. K.S. Warren, editor. Blackwell Scientific Publications, Oxford.
9. Lambert, A.C. 1911. Fevers with urticaria and esosinophila and their relation to infection with Schistosoma japonicum. Trans. R. Soc. Trop. Med. Hyg. 5:38-45.
10. Gelfand, M. 1964. The hypersensitive response of the European to schistosomiasis. J. Trop. Med. Hyg. 67:255-256.
11. Partono, F., W. Purnomo, A. Pribadi, and A. Soewarta. 1978. Epidemiological and clinical features of Brugia timori in a newly established village, Karakuak, West Flores, Indonesia. Am. J. Trop. Med. Hyg. 27:910-915.
12. Prost, A., and E.G. Ponsay. 1979. Importance epidemiologique du parasitisme neo-natal par microfilaries donchocerca volvulus. Tropenmed. Parasitol. 30:477-481.
13. Wartman, W.B. 1947. Filariasis in American armed forces in World War II. Medicine. 26:333-394.
14. Lammie, P., W. Hitch, A. Walker, W. Hightower, and M. Eberhard. 1991. Maternal filarial infection as risk factor for infection in children. Lancet. 337:1005-1006.
15. Haque, A., W. Cuna, J. Pestel, A. Capron, and B. Bonnel. 1988. Tolerance in rats by transplacental transfer of Dipetalonema viteae microfilariae: recognition of putative toleragen(s) by antibodies that inhibit antigen-specific lymphocyte proliferation. Eur. J. Immunol. 18:1167-1172.
16. Haque, A., and A. Capron. 1982. Transplacental transfer of roden microfilariae induces antigen-specific tolerance in rats. Nature (Lond.). 299:361-363.
17. Schrater, A., A. Spielman, and W. Piessens. 1983. Predisposition to Brugia malayi microfilaremia in progeny of infected gerbils. Am. J. Trop. Med. Hyg. 32:1302-1308.
18. Hang, L., D. Boros, and K. Warren. 1974. Induction of immunological hyporesponsiveness to granulomatous hypersensitivity in Schistosoma mansoni infection. J. Infect. Dis. 130:515-522.
19. Aase, J.M., G.R. Noren, D.V. Reddy, and J.W. St. Geme, Jr. 1972. Mumps-virus infection in pregnant women and the immunologic response of their offspring. N. Eng. J. Med. 286:1379-1382.
20. Hara, T., S. Ohashi, Y. Yamashita, T. Abe, H. Hisaeda, K. Himeno, R.A. Good, and K. Takeshita. 1996. Human Vδ2+ γδ T-cell tolerance to foreign antigens of Toxoplasma gondii. Proc. Natl. Acad. Sci. USA. 93:5136-5140.
21. Gill, T.J.I., C.F. Repetti, E.A. Metlay, B.S. Rabin, F.H. Taylor, D.S. Thompson, and A.E. Cortese. 1983. Transplacental immunization of the human fetus to tetanus by immunization of the mother. J. Clin. Invest. 72:987-996.
22. Baker, C.J., M.A. Rench, M.S. Edwards, R.J. Carpenter, B.M. Hays, and D.L. Kasper. 1988. Immunization of pregnant women with a polysaccharide vaccine of group B streptococcus. N. Engl. J. Med. 319:1180-1185.
23. McCormick, J.B., H.H. Gusmao, S. Nakamura, J.B. Freire, J. Veras, G. Gorman, J.C. Felley, and P. Wingo. 1980. Antibody response to serogroup A and C meningococcal polysaccharide vaccines in infants born of mothers vaccinated during pregnancy. J. Clin. Invest. 65:1141-1144.
24. Camus, D., Y. Carliere, J.C. Bina, R. Borojevic, A. Prata, and A. Capron. 1976. Sensitization to Schistosoma mansoni antigen in uninfected children born to infected mothers. J. Infect. Dis. 134:405-108.
25. Tachon, P., and R. Borojevic. 1978. Mother-child relation in human schistosomiasis mansoni: skin test and cord blood reactivity to schistosomal antigens. Trans. R. Soc. Trop. Med. Hyg. 72:605-609.
26. Agarwal, M., G. Prasad, B. Harinath, and B. Bhatia. 1986. Transplacental transfer of filarial infection. Indian Pediatr. 23:169-174.
27. Eloi-Santos, S.M., E. Novata-Silva, V.M. Maselli, G. Gazzinelli, D.G. Colley, and R. Correa-Oliveira. 1989. Idiotypic sensitization in utero of children born to mothers with schistosomiasis or Changas' disease. J. Clin. Invest. 84: 1028-1031.
28. Novato-Silva, E., G. Gazzinelli, and D.G. Colley. 1992. Immune responses during human schistosomiasis mansoni. XVIII. Immunologic status of pregnant women and their neonates. Scand. J. Immunol. 35:429-437.
29. Barrios, C., P. Brawand, M. Berney, C. Brandt, P.-H. Lambert, and C.-A. Siegrist. 1996. Neonatal and early life immune responses to various forms of vaccine antigens qualitatively differ from adult responses: predominance of a Th2-biased pattern which persists alter adult boosting. Eur. J. Immunol. 26: 1489-1496.
30. Boros, D.V., and K.S. Warren. 1970. Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from schistosoma mansoni eggs. J. Exp. Med. 132:488-507.
31. Hussain, R., R.G. Hamilton, V. Kumaraswami, N.F. Adkinson, and E.A. Ottesen. 1981. IgE response in human filariasis. I. Quantitation of filaria-specific IgE. J. Immunol. 127:1623-1629.
32. de Waal Malefyt, R., J. Haanen, H. Spits, M. Roncarolo, A. te Velde, C. Figdor, K. Johnson, R. Kastelein, H. Yssel, and J. de Vries. 1991. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 174:915-924.
33. Mahanty, S., J.S. Abrams, C.L. King, A.P. Limaye, and T.B. Nutman. 1992. Parallel regulation of IL-4 and IL-5 in human helminth infections. J. Immunol. 148:3567-3571.
34. Li, Z., C.L. King, J.O. Ogundipe, L.S. Licate, and R.E. Blanton. 1995. Preferential recognition by human IgE and IgG4 of a species-specific Schistosoma haematobium serine protease inhibitor. J. Infect. Dis. 171:416-422.
35. King, C.L., S. Mahanty, V. Kumaraswami, J.S. Abrams, J. Regunathan, K. Jayaraman, E. A. Ottesen, and T.B. Nutman. 1993. Cytokine control of parasite-specific anergy in human lymphatic filariasis. J. Clin. Invest. 92:1667-1673.
36. Roncarolo, M.-G., M. Bigler, E. Ciuti, S. Martino, and P.-A. Tovo. 1994. Immune responses by cord blood cells. Blood Cells (Berlin). 20:573-586.
37. King, C.L., R.J. Stupi, N. Craighead, C.H. June, and G. Thyphronitis. 1995. CD28 activation promotes Th2 subset differentiation by human CD4+ cells. Eur. J. Immunol. 25:587-595.
38. Wilson, C.B., D.B. Lewis, and B.K. English. 1991. T cell development of the fetus and neonate. In Immunology of Milk and the Neonate. J. Mestecky, C. Blair, and P.L. Ogra, editors. Plenum Press, New York. 17-29.
39. King, C.L., A. Medhat, I. Malhotra, M. Nafeh, A. Helmy, J. Khaudary, S. Ibrahim, M. El-Sherbiny, S. Zaky, R. Stupi, et al. 1996. Cytokine control of parasite parasite-specific anergy in human urinary schistosomiasis: TL-10 modulates lymphocyte reactivity. J. Immunol. 156:4715-4721.
40. King, C.L., J. Hakimi, M.T. Shata, and A. Medhat. 1995. IL-12 regulation of parasite antigen-driven IgE production in human helminth infections. J. Immunol. 155:454-461.
41. Lal, R.B., and E.A. Ottesen. 1988. Enhanced diagnostic specificity in human filariasis by IgG4 antibody assessment. J. Infect. Dis. 158:1034-1039.
42. Iskander, R., P.K. Das, and R.C. Aalberse. 1981. IgG4 antibodies in Egyptian patients with schistosomiasis. Int. Archs. Allergy Appl. Immunol. 66: 200-218.
43. Ottesen, E.A. 1984. Immunological aspects of lymphatic filariasis and onchocerciasis in man. Trans. R. Soc. Trop. Med. Hyg. 78(Suppl.):9-18.
44. Nutman, T.B., V. Kumaraswami, and E.A. Ottesen. 1987. Parasite-specific anergy in human filariasis. Insights after analysis of parasite antigen-driven lymphokine production. J. Clin. Invest. 79:1516-1523.
45. Ridge, J.P., E.J. Fuchs, and P. Matzinger. 1996. Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science (Wash. DC). 271:1723-1726.
46. Forsthuber, T., and H.C. Yip. 1996. Induction of Th1 and Th2 immunity in neonatal mice. Science (Wash. DC). 271:1728-1730.
47. Pennisi, E. 1996. Teetering on the brink of danger. Science (Wash. DC). 271:1665-1667.
48. Schroder, J. 1974. Passage of leukocytes from mother to fetus. Scan. J. Immunol. 3:369-373.
49. Grogan, T., D. Broughton, and W. Doyle. 1975. Graft-versus-host reaction (GVHR): a case report suggesting GVHR occurred as a result of maternofetal cell transfer. Arch. Pathol. 99:330-334.
50. Fried, M., and P.E. Duffy. 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science (Wash. DC). 272:1502-1504.
51. Raghavan, N.G.S. 1958. Congenital filariasis. Bull. Nat. Soc. Indian Mal. Mosz. Dis. 6:147-154.
52. Carlier, Y., H. Nzeyimana, D. Bout, and A. Capron. 1980. Evaluation of circulating antigens by a sandwich radioimmunoassay, and of antibodies and immune complexes, in Schistosoma mansoni-infected African parturients and their newborn children. Am. J. Trop. Med. Hyg. 29:74-81.
53. Carlier, Y., D. Bout, J. Bina, D. Camus, J. Figueiredo, and A. Capron. 1975. Immunological studies in human schistosomiasis. I. Parasitic antigen in urine. Am. J. Trop. Med. Hyg. 24:949-954.
54. Santoro, F., Y. Carlier, R. Borojevic, D. Bout, P. Tachon, and A. Capron. 1976. Parasite "M" antigen in milk from mothers infected with Schistosoma mansoni (preliminary report). Ann. Trop. Med. Parasitol. 71:121-123.
55. Deelder, A., and T. Nash. 1985. Comparison of four schistosome excretory-secretory antigens: Phenol sulfuric lest active peak, cathodic circulating antigen, gut-associated proteoglycan, and circulating anodic antigen. Am. J. Trop. Med. Hyg. 34:236-241.