Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-25T11:11:47.126Z Has data issue: false hasContentIssue false

Recombinant protein Bd37 protected gerbils against heterologous challenges with isolates of Babesia divergens polymorphic for the bd37 gene

Published online by Cambridge University Press:  13 October 2006

K. HADJ-KADDOUR
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France
B. CARCY
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France
A. VALLET
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France
S. RANDAZZO
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France
S. DELBECQ
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France
J. KLEUSKENS
Affiliation:
Department of Parasitology, Intervet International B.V., Boxmeer, The Netherlands
T. SCHETTERS
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France Department of Parasitology, Intervet International B.V., Boxmeer, The Netherlands
A. GORENFLOT
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France
E. PRECIGOUT
Affiliation:
Laboratoire Biologie Cellulaire and Moléculaire, ERT 1038 ‘Vaccination anti-parasitaire’, UFR Pharmacie, Université Montpellier I, 15 Avenue Charles Flahault, B.P. 14491, 34093 Montpellier Cedex 5, France

Abstract

The Bd37gene encoding for a glycosyl-phosphatidyl-inositol anchored protein of Babesia divergens displays genetic polymorphisms among isolates. Five major polymorphic groups (clades) were shown by PCR-RFLP among different B. divergens isolates. Each group has been characterized according to a reference Bd37 gene (Rouen87, W8843, Y5, 6303E and 1705B). Recombinant (GST fusion) protein (Bd37r) expressed from the Bd37 gene, was used as antigen in a saponin-based formulation and was able to protect gerbils, after 2 injections at low dose vaccine concentration (1 μg per dose), against a virulent challenge with the B. divergens Rouen87 isolate. In spite of polymorphism of Bd37 gene, Bd37r induced complete immunoprotection against challenges with each of the 5 reference isolate groups defined by PCR-RFLP.

Type
Research Article
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Beattie, J. F., Michelson, M. L. and Holman, P. J. ( 2002). Acute babesiosis caused by Babesia divergens in a resident of Kentucky. New England Journal of Medicine 347, 697698.CrossRefGoogle Scholar
Ben Musa, N. and Dawoud, H. A. ( 2004). The protective activity of serum and fractionated serum from rats against Babesia divergens. Journal of the Egyptian Society of Parasitology 34, 407422.Google Scholar
Brown, W. C., Norimine, J., Goff, W. L., Suarez, C. E. and McElwain, T. F. ( 2006). Prospects for recombinant vaccines against Babesia bovis and related parasites. Parasite Immunology 28, 315327.CrossRefGoogle Scholar
Carcy, B., Precigout, E., Valentin, A., Gorenflot, A. and Schrevel, J. ( 1995). A 37-kilodalton glycoprotein of Babesia divergens is a major component of a protective fraction containing low-molecular-mass culture-derived exoantigens. Infection and Immunity 63, 811817.Google Scholar
Christensson, D. A. ( 1987). Clinical and serological response after experimental inoculation with Babesia divergens of newborn calves with and without maternal antibodies. Acta Veterinaria Scandinavica 28, 381392.Google Scholar
Christensson, D. A. ( 1989). Inverse age resistance to experimental Babesia divergens infection in cattle. Acta Veterinaria Scandinavica 30, 453464.Google Scholar
Daly, T. M. and Long, C. A. ( 1996). Influence of adjuvants on protection induced by a recombinant fusion protein against malarial infection. Infection and Immunity 64, 26022608.Google Scholar
Delbecq, S., Precigout, E., Vallet, A., Carcy, B., Schetters, T. P. and Gorenflot, A. ( 2002). Babesia divergens: cloning and biochemical characterization of Bd37. Parasitology 125, 305312.CrossRefGoogle Scholar
Goethert, H. K. and Telford, S. R. 3rd. ( 2003). Enzootic transmission of Babesia divergens among cottontail rabbits on Nantucket Island, Massachusetts. American Journal of Tropical Medicine and Hygiene 69, 455460.Google Scholar
Gorenflot, A., Brasseur, P., Precigout, E., L'Hostis, M., Marchand, A. and Schrevel, J. ( 1991). Cytological and immunological responses to Babesia divergens in different hosts: ox, gerbil, man. Parasitology Research 77, 312.CrossRefGoogle Scholar
Gorenflot, A., Moubri, K., Precigout, E., Carcy, B. and Schetters, T. P. ( 1998). Human babesiosis. Annals of Tropical Medicine and Parasitology 92, 489501.CrossRefGoogle Scholar
Gorenflot, A., Precigout, E., Bissuel, G., Lecointre, O., Brasseur, P., Vidor, E., L'Hostis, M. and Schrevel, J. ( 1990). Identification of major Babesia divergens polypeptides that induce protection against homologous challenge in gerbils. Infection and Immunity 58, 40764082.Google Scholar
Gorenflot, A., Precigout, E., Valentin, A., Bissuel, G., Carcy, B., Brasseur, P., Moreau, Y. and Schrevel, J. ( 1992). Babesia divergens vaccine. Memorias do Instituto Oswaldo Cruz 87 (Suppl. 3), 279281.CrossRefGoogle Scholar
Gray, J. S. and Harte, L. N. ( 1985). An estimation of the prevalence and economic importance of clinical babesiosis in the republic of Ireland. Ireland Veterinary Journal 69, 455460.Google Scholar
Herwaldt, B., Persing, D. H., Precigout, E., Goff, W. L., Mathiesen, D. A., Taylor, P. W., Eberhard, M. L. and Gorenflot, A. ( 1996). A fatal case of babesiosis in Missouri: identification of another piroplasm that infects humans. Annals of Internal Medicine 124, 643650.CrossRefGoogle Scholar
Herwaldt, B. L., de Bruyn, G., Pieniazek, N. J., Homer, M., Lofy, K. H., Slemenda, S. B., Fritsche, T. R., Persing, D. H. and Limaye, A. P. ( 2004). Babesia divergens-like infection, Washington State. Emerging Infectious Diseases 10, 622629.CrossRefGoogle Scholar
Holman, P. J., Spencer, A. M., Droleskey, R. E., Goethert, H. K. and Telford, S. R. 3rd. ( 2005). In vitro cultivation of a zoonotic Babesia sp. isolated from eastern cottontail rabbits (Sylvilagus floridanus) on Nantucket Island, Massachusetts. Journal of Clinical Microbiology 8, 39954001.Google Scholar
James, M. A. ( 1989). Application of exoantigens of Babesia and Plasmodium in vaccine development. Transactions of the Royal Society of Tropical Medicine and Hygiene 83 (Suppl.), 6772.CrossRefGoogle Scholar
Joyner, L. P. and Davies, S. F. ( 1967). Acquired resistance to Babesia divergens in experimental calves. Journal of Protozoology 14, 260262.CrossRefGoogle Scholar
Kumar, S., Collins, W., Egan, A., Yadava, A., Garraud, O., Blackman, M. J., Guevara Patino, J. A., Diggs, C. and Kaslow, D. C. ( 2000). Immunogenicity and efficacy in aotus monkeys of four recombinant Plasmodium falciparum vaccines in multiple adjuvant formulations based on the 19-kilodalton C terminus of merozoite surface protein 1. Infection and Immunity 68, 22152223.CrossRefGoogle Scholar
Kuttler, K. L. ( 1988). World-wide impact of babesiosis. In Babesiosis of Domestic Animals and Man (ed. Ristic, M.), pp. 122. CRC Press, Inc., Boca Raton, Florida.
Lewis, D. and Williams, H. ( 1979). Infection of the Mongolian gerbil with the cattle piroplasm Babesia divergens. Nature, London 278, 170171.CrossRefGoogle Scholar
L'Hostis, M., Chauvin, A., Valentin, A., Precigout, E. and Gorenflot, A. ( 1997). Survey of Babesia divergens antibody kinetics in cattle in western France. Veterinary Research 28, 481848.Google Scholar
Montenegro-James, S., Toro Benitez, M., Leon, E., Lopez, R. and Ristic, M. ( 1987). Bovine babesiosis: induction of protective immunity with culture-derived Babesia bovis and Babesia bigemina immunogens. Parasitology Research 74, 142150.CrossRefGoogle Scholar
Montenegro-James, S., Toro, M., Leon, E. and Guillen, A. T. ( 1992). Field evaluation of an exoantigen-containing Babesia vaccine in Venezuela. Memorias do Instituto Oswaldo Cruz 87 (Suppl.) 3, 283288.CrossRefGoogle Scholar
Norimine, J., Mosqueda, J., Suarez, C., Palmer, G. H., McElwain, T. F., Mbassa, G. and Brown, W. C. ( 2003). Stimulation of T-helper cell gamma interferon and immunoglobulin G responses specific for Babesia bovis rhoptry-associated protein 1 (RAP-1) or a RAP-1 protein lacking the carboxy-terminal repeat region is insufficient to provide protective immunity against virulent B. bovis challenge. Infection and Immunity 71, 50215032.CrossRefGoogle Scholar
Orinda, G. O., Gale, K. R., Wright, I. G. and Parrodi, F. ( 1992). Bovine babesiosis: failure to induce interferon gamma production in response to Babesia bovis antigens in cattle. International Journal for Parasitology 22, 395398.CrossRefGoogle Scholar
Precigout, E., Delbecq, S., Vallet, A., Carcy, B., Camillieri, S., Hadj-Kaddour, K., Kleuskens, J., Schetters, T. and Gorenflot, A. ( 2004). Association between sequence polymorphism in an epitope of Babesia divergens Bd37 exoantigen and protection induced by passive transfer. International Journal for Parasitology 34, 585593.CrossRefGoogle Scholar
Precigout, E., Gorenflot, A., Valentin, A., Bissuel, G., Carcy, B., Brasseur, P., Moreau, Y. and Schrevel, J. ( 1991). Analysis of immune responses of different hosts to Babesia divergens isolates from different geographic areas and capacity of culture-derived exoantigens to induce efficient cross-protection. Infection and Immunity 59, 27992805.Google Scholar
Schetters, T. ( 2005). Vaccination against canine babesiosis. Trends in Parasitology 21, 179184.CrossRefGoogle Scholar
Schetters, T. ( 1995). Vaccine development from a commercial point of view. Veterinary Parasitology 57, 267275.CrossRefGoogle Scholar
Schetters, T. P., Kleuskens, J. A., Scholtes, N. C., Gorenflot, A., Moubri, K. and Vermeulen, A. N. ( 2001). Vaccination of dogs against heterologous Babesia canis infection using antigens from culture supernatants. Veterinary Parasitology 100, 7586.CrossRefGoogle Scholar
Schetters, T. P., Kleuskens, J. A., Scholtes, N. C., Pasman, J. W. and Bos, H. J. ( 1994). Vaccination of dogs against Babesia canis infection using antigens from culture supernatants with emphasis on clinical babesiosis. Veterinary Parasitology 52, 219233.CrossRefGoogle Scholar
Schetters, T. P. and Montenero-James, S. ( 1995). Vaccines against babesiosis using soluble parasite antigens. Parasitology Today 11, 456462.CrossRefGoogle Scholar
Timms, P., Dalgliesh, R. J., Barry, D. N., Dimmock, C. K. and Rodwell, B. J. ( 1983). Babesia bovis: comparison of culture-derived parasites, non-living antigen and conventional vaccine in the protection of cattle against heterologous challenge. Australian Veterinary Journal 60, 7577.CrossRefGoogle Scholar
Valentin, A., Precigout, E., L'Hostis, M., Carcy, B., Gorenflot, A. and Schrevel, J. ( 1993). Cellular and humoral immune responses induced in cattle by vaccination with Babesia divergens culture-derived exoantigens correlate with protection. Infection and Immunity 61, 734741.Google Scholar
Yang, Y. S., Delbecq, S., Strub, M. P., Lohr, F., Schetters, T., Gorenflot, A., Precigout, E. and Roumestand, C. ( 2005). 1H, 15N and 13C Backbone resonance assignments of the 37 kDa surface antigen protein Bd37 from Babesia divergens. Journal of Biomolecular NMR 31, 6768.CrossRefGoogle Scholar