Resistance to re-infection after exposure to normal and attenuated schistosome parasites in the baboon model

Parasite Immunology

Volumn 27, Issue 7-8, 2005, Pages 281-288

  Kariuki, T M ^a   Farah, Idle O ^a,b  

^a INSTITUTE OF PRIMATE RESEARCH   (Kenya)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Baboon; Chemotherapy; Infection; Schistosomiasis; Vaccination

Indexed keywords

FATTY ACID BINDING PROTEIN; GLUTATHIONE TRANSFERASE; MYOSIN HEAVY CHAIN; PARAMYOSIN; PRAZIQUANTEL; TRIOSEPHOSPHATE ISOMERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; BABOON; CONTROLLED STUDY; EXPOSURE; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFECTION RESISTANCE; INNATE IMMUNITY; LIFE CYCLE; NONHUMAN; PARASITE CONTROL; PARASITOSIS; PRIORITY JOURNAL; REINFECTION; RESEARCH; REVIEW; SCHISTOSOMIASIS; VACCINATION;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; PAPIO; PRAZIQUANTEL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SCHISTOSOMICIDES; VACCINATION; VACCINES, ATTENUATED;

ANIMALIA; PAPIO HAMADRYAS; SCHISTOSOMA;

EID: 25144507000     PISSN: 01419838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2005.00783.x     Document Type: Review

References (76)

1. Cheever AW, Lenzi JA, Lenzi HL & Andrade ZA. Experimental models of Schistosoma mansoni infection. Mem Inst Oswlado Cruz 2002; 97: 917-940.
2. Eberl M, Langermans JAM, Frost PA et al. Cellular and humoral immune responses and protection against schistosomes induced by a radiation-attenuated vaccine in chimpanzees. Infect Immun 2001; 69: 5352-5362.
3. Nyindo M & Farah IO. The baboon as a non-human primate model of human schistosome infection. Parasitol Today 1999; 15: 478-482.
4. Cheevers AW & Powers KG. Schistosoma mansoni infection in the rhesus monkeys: comparison of the course of heavy and light infections. Bull World Health Organization 1972; 46: 301-309.
5. Cioli D. Praziquantel: is there real resistance and are there alternatives? Curr Opin Infect Dis 2000; 13: 659-663.
6. Sturrock RF, Cottrell BJ & Kimani R. Observations on the ability of repeated, light exposures to Schistosoma mansoni cercariae to induce resistance to reinfection in Kenyan baboons (Papio anubis). Parasitology 1984; 88: 505-514.
7. Mola PW, Farah IO, Kariuki TM, Nyindo M, Blanton RE & King CL. Cytokine control of the granulomatous response in Schistosoma mansoni-infected baboons: role of exposure and treatment. Infect Immun 1999; 67: 6565-6571.
8. Farah IO, Mola PW, Kariuki TM, Nyindo M, Blanton RE & King CL. Repeated exposure induces periportal fibrosis in Schistosoma mansoni-infected baboons: role of TGF-β and IL-4. J Immunol 2000; 164: 5337-5343.
9. Damian RT, Greene ND, Suzuki T & Dean DA. Schistosomiasis mansoni in baboons. V. Antibodies and immediate hypersensitivity in multiply infected Papio cynocephalus. Am J Trop Med Hyg 1981; 30: 836-843.
10. Cottrell BJ & Sturrock RF. The modulation of specific and non-specific cell-mediated immunity in baboons (Papio anubis) infected with Schistosoma mansoni. Immunology 1982; 45: 341-348.
11. Sturrock RF, Butterworth AE, Houba V et al. Attempts to manipulate specific responses to induce resistance to Schistosoma mansoni in Kenyan baboons (Papio anubis). J Helminthol 1985; 59: 175-186.
12. Sturrock RF, Cottrell BJ, Mahmoud AA, Chedid L & Kimani R. Attempts to induce resistance to Schistosoma mansoni and S. haematobium in Kenyan Baboons (Papio anubis) using non-specific Immunostimulants. Parasitology 1985; 90: 101-10.
13. Mountford AP & Trottein F. Schistosomes in the skin: a balance between immune priming and regulation. Trends Parasitol 2004; 20: 221-226.
14. Pearce E, La Flamme A, Sabin E & Brunet L. The initiation and function of Th2 responses during infection with Schistosoma mansoni. Adv Exp Med Biol 1998; 452: 67-73.
15. Morales-Montor J, Mohamed F, Drake L, Baghdadi A, Baig S & Damian RT. Dynamics of the cytokine messenger RNA expression pattern in the liver of baboons infected with Schistosoma mansoni. J Parasitol 2004; 90: 547-556.
16. Kariuki TM, Farah IO, Yole DS et al. Parameters of the attenuated Schistosome vaccine evaluated in the olive baboon. Infection and Immunity 2004; 72: 5526-5529.
17. Chou TM, Stich RW, Marsala C et al. Development of a molecular probe to baboon interleukin-10 mRNA for in situ hybridization during experimental schistosomiasis. Ann N Y Acad Sci 2000; 916: 410-416.
18. Nyindo M, Kariuki TM, Mola WP et al. Role of adult worm antigen-specific immunoglobulin E in acquired immunity to S. mansoni infection in Baboons. Infection Immunity 1999; 67: 636-642.
19. Andrade ZA. Pathology of human schistosomiasis. Mem Ins t Oswaldo Cruz 1987; 82: 17-23.
20. Farah IO, Nyindo M, Suleman MA et al. Schistosoma mansoni: development and modulation of the granuloma after single or multiple exposures in the baboon (Papio cynocephalus anubis). Exp Parasitol 1997; 86: 93-101.
21. Bosshardt SC & Damian RT. Serum factors from infected baboons inhibit oviposition and cause unpairing of Schistosoma mansoni in vitro. J Parasitol 1986; 72: 583-587.
22. Yole DS, Pemberton R, Reid GD & Wilson RA. Protective immunity to Schistosoma mansoni induced in the olive baboon Papio anubis by the irradiated cercaria vaccine. Parasitology 1996; 112: 37-46.
23. Butterworth AE. Cell-mediated damage to helminths. Adv Parasitol 1984; 23: 143-235.
24. Siddiqi AA, Pinkston JR, Quinlin ML et al. Characterization of the immune response to DNA vaccination strategies for schistosomiasis candidate antigen, Sm-p80 in the baboon. Vaccine 2005; 23: 1451-1456.
25. Capron M, Torpier G & Capron A. In vitro killing of S. mansoni schistosomula by eosinophils from infected rats: role of cytophilic antibodies. J Immunol 1979; 123: 2220-2230.
26. Coulson PS & Wilson RA. Portal shunting and resistance to Schistosoma mansoni in 129 strain mice. Parasitology 1989; 99: 383-389.
27. Wilson RA, Coulson PS, Sturrock RF & Reid GD. Schistosome migration in primates: a study in the olive baboon (Papio anubis). Trans R Soc Trop Med Hyg 1990; 84: 80-83.
28. Richter D, Harn DA & Matuschka F-R. The irradiated cercariae vaccine model: looking on the bright side of radiation. Parasitol Today 1995; 8: 288-293.
29. Coulson PS. The radiation-attenuated vaccine against Schistosomiasis in animal models: paradigm for a human vaccine? Adv Parasitol 1997; 39: 271-336.
30. Wilson RA, Coulson PS & Mountford AP. Immune responses to the radiation-attenuated schistosome vaccine: what can we learn from knock-out mice? Immunol Lett 1999; 65: 117-123.
31. Stek MF, Minard P, Dean DA & Hall JE. Immunization of Baboons with Schistosoma mansoni cercariae attenuated by gamma irradiation. Science 1981; 212: 1518-1520.
32. Damian RT, Roberts ML, Powell MR, Clark JD, Lewis FA & Stirewalt MA. Schistosoma mansoni egg granuloma size reduction in challenged baboons after vaccination with irradiated cryopreserved schistosomula. Proc Natl Acad Sci USA 1984; 81: 3552-3556.
33. James ER, Otieno M, Harrison R, Dobinson AR, Monorei J & Else JG. Partial protection of baboons against Schistosoma mansoni using radiation attenuated cryopreserved schistosomula. Trans R Soc Trop Med Hyg 1986; 80: 378-384.
34. Harrison RA, Bickle QD, Kiarie S et al. Immunization of baboons with attenuated schistosomula of Schistosoma haematobium: levels of protection induced by immunization with larvae irradiated with 20 and 60 krad. Trans R Soc Trop Med Hyg 1990; 84: 89-99.
35. Byram JE, Harrison RA, Von Lichtenberg F, Webbe G & Sturrock RF. Pathology resulting from the administration of a live attenuated anti-Schistosoma haematobium vaccine in baboons. Am J Trop Med Hyg 1989; 40: 55-65.
36. Reid GD, Sturrock RF, Harrison RA & Tarara RP. Schistosoma haematobium in the baboon (Papio anubis): assessment of protection levels against either a single mass challenge or repeated trickle challenges after vaccination with irradiated schistosomula. J Helminthol 1995; 69: 139-147.
37. Farah IO & Nyindo M. Acute schistosomiasis mansoni in the baboon Papio anubis gives rise to goblet-cell hyperplasia and villus atrophy that are modulated by an irradiated cercarial vaccine. Parasitol Res 1996; 83: 281-284.
38. Yole DS, Reid GD & Wilson RA. Protection against Schistosoma mansoni and associated immune responses induced in the vervet monkey Cercopithecus aethiops by the irradiated cercaria vaccine. Am J Trap Med Hyg 1996; 54: 265-270.
39. Mumo JM & Kinoti GK. Vaccination of vervet monkeys (Cercopithecus aethiops) against infection with Schistosoma mansoni. Scand J Immunol 1992; 11: 23-28.
40. Cheever AW. Quantitative comparison of the intensity of Schistosoma mansoni infections in man and experimental animals. Trans R Soc Trop Med Hyg 1969; 63: 781-795.
41. Fallon FG, Gibbons J, Vervenne RA et al. Juvenile rhesus monkeys have lower type 2 cytokine responses than adults after primary infection with Schistosoma mansoni. J Infect Dis 2003; 187: 939-945.
42. Sturrock RF, Otieno FM, Tarara R, Kimani R, Harrison R & Else JG. Experimental Schistosoma mansoni in vervet monkeys (Cercopithecus aethiops) in Kenya: I. Susceptibility to a primary infection. J Helmithol 1984; 58: 79-92.
43. Bergquist NR, Leonardo LR & Mitchell GF. Vaccine-linked chemotherapy: can schistosomiasis control benefit from an integrated approach? Trends in Parasitol 2005; 21: 112-117.
44. Genton B, Betuela I, Felger I et al. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase l-2b trial in Papua New Guinea. J Infect Dis 2002; 185: 820-827.
45. Mutapi F. Heterogeneities in anti-schistosome humoral responses following chemotherapy. Trends Parasitol 2001; 17: 518-524.
46. Bergquist NR. Blueprint for Schistosomiasis vaccine development. Acta Trop 2002; 82: 183-192.
47. Boulanger D, Reid GD, Sturrock RF et al. Immunization of mice and baboons with the recombinant Sm28GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni. Parasite Immunol 1991; 13: 473-490.
48. Wolowczuk I, Auriault C, Bossus M et al. Antigenicity and immunogenicity of a multiple peptidic construction of the Schistosoma mansoni Sm-28 GST antigen in rat, mouse, and monkey. 1. Partial protection of Fischer rat after active immunization. J Immunol 1991; 146: 1987-1995.
49. Soisson LA, Reid GD, Farah IO, Nyindo M & Strand M. Protective immunity in baboons vaccinated with a recombinant antigen or radiation-attenuated cercariae of Schistosoma mansoni are antibody-dependent. J Immunol 1993; 151: 4782-4789.
50. Kanamura HY, Hancock K, Rodrigues V & Damian RT. Schistosoma mansoni heat shock protein 70 elicits an early humoral immune response in S. mansoni infected baboons. Mem Inst Oswaldo Cruz 2002; 97: 711-716.
51. Sturrock RF. A review of the use of primates in studying human schistosomiasis. J Med Primatol 1986; 15: 267-279.
52. Renquist DM, Johnson AJ, Lewis JC & Johnson DJ. A natural case of Schistosoma mansoni in the chimpanzee (Pan troglodytes). Lab Anim Sci 1975; 25: 763-768.
53. Duplantier JM & Sene M. Rodents as reservoir hosts in the transmission of Schistosoma mansoni in Richard-Toll, Senegal, West Africa. J Helminthol 2000; 74: 129-135.
54. James SL. Experimental models of immunization against schistosomes: lessons for vaccine development. Immunol Invest 1992; 21: 477-493.
55. Wilson RA & Coulson PS. The effect of softwood sawdust bed-ding on the maturation of an infection of Schistosoma mansoni in mice exposed to cercariae via the tail or abdominal skin. Trans R Soc Trop Med Hyg 1984; 78: 411-412.
56. Warren KS & Dewitt WB. Production of portal hypertension and oesophageal varices in the mouse. Proc Soc Exp Biol Med 1958; 98: 99-101.
57. Von Lichtenberg F & Sadun EH. Experimental production of bilharzial pipe-stem fibrosis in the chimpanzee. Exp Parasitol 1968; 22: 264-278.
58. Tsukamoto H, Matsuoka M & French SW. Experimental models of hepatic fibrosis: a review. Semin Liver Dis 1990; 10: 56-65.
59. Eberl M, Langermans JAM, Frost PA et al. Cellular and humoral immune responses and protection against schistosomes induced by a radiation-attenuated vaccine in chimpanzees. Infect Immun 2001; 69: 5352-5362.
60. Pearce EJ & MacDonald AS. The immunobiology of schistosomiasis. Nat Rev Immunol 2002; 2: 499-511.
61. Khalife J, Cetre C, Pierrot C & Capron M. Mechanisms of resistance to S. mansoni infection: the rat model. Parasitol Int 2000; 49: 339-345.
62. Wynn TA & Cheever AW. Cytokine regulation of granuloma formation in schistosomiasis. Curr Opin Immunol 1995; 7: 505-511.
63. Balloul JM, Grzych JM, Pierce RJ & Capron A. A purified 28 000 dalton protein from Schistosoma mansoni adult worms protects rats and mice against experimental schistosomiasis. J Immunol 1987; 138: 3448-3453.
64. Rao K, He Y & Kalyanasundaram R. Expression of a 28-kilodalton glutathione S-transferase antigen of Schistosoma mansoni on the surface of filamentous phages and evaluation of its vaccine potential. Clin Diagn Lab Immunol 2003; 10: 536-541.
65. Boulanger D, Warter A, Trottein F et al. Vaccination of patas monkeys experimentally infected with Schistosoma haematobium using a recombinant glutathione S-transferase cloned from S. mansoni. Parasite Immunol 1995; 17: 361-369.
66. Capron A, Riveau G, Capron M & Trottein F. Schistosomes: the road from host-parasite interactions to vaccines in clinical trials. Trends in Parasitol 2005; 21: 143-149.
67. Pearce EJ, James SL, Hieny S, Lanar DE & Sher A. Induction of protective immunity against Schistosoma mansoni by vaccination with schistosome paramyosin (Sm97), a nonsurface parasite antigen. Proc Natl Acad Sci USA 1988; 85: 5678-5682.
68. Sher A, Pearce E, Hieny S & James S. Induction of protective immunity against Schistosoma mansoni by a nonliving vaccine. IV. Fractionation and antigenic properties of a soluble adult worm immunoprophylactic activity. J Immunol 1986; 136: 3878-3883.
69. Fonseca C, Cunha-Neto E, Kalil J et al. Identification of immunodominant epitopes of Schistosoma mansoni vaccine candidate antigens using human T cells. Mem Inst Oswaldo Cruz 2004; 99: 63-66.
70. Al-Sherbiny M, Osman A, Barakat R, El Morshedy H, Bergquist R & Olds R. In vitro cellular and humoral responses to Schistosoma mansoni vaccine candidate antigens. Acta Trop 2003; 88: 117-130.
71. Soisson LM, Masterson CP, Tom TD, Mcnally MT, Lowell GH & Strand M. Induction of protective immunity in mice using a 62-kDa recombinant fragment of a Schistosoma mansoni surface antigen. J Immunol 1992; 149: 3612-3620.
72. Ribeiro De Jesus A, Araujo I, Bacellar O et al. Human immune responses to Schistosoma mansoni vaccine candidate antigens. Infect Immun 2000; 68: 2797-2803.
73. Harn DA, Gu W, Oligino LD, Mitsuyama M, Gebremichael A & Richter D. A protective monoclonal antibody specifically recognizes and alters the catalytic activity of schistosome triosephosphate isomerase. J Immunol 1992; 148: 562-567.
74. Tendler M, Brito CA, Vilar MM et al. A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine. Proc Natl Acad Sci USA 1996; 93: 269-273.
75. Abreu P, Miyasato P, Vilar M et al. Sm14 of Schistosoma mansoni in fusion with tetanus toxin fragment C induces immunoprotection against tetanus and schistosomiasis in mice. Infect Immun 2004; 72: 5931-5937.
76. Richter D & Harn DA. Candidate vaccine antigens identified by antibodies from mice vaccinated with 15- or 50-kilorad-irradiated cercariae of Schistosoma mansoni. Infect Immun 1993; 61: 146-154.