Conservation of Babesia bovis Small Heat Shock Protein (Hsp20) among Strains and Definition of T Helper Cell Epitopes Recognized by Cattle with Diverse Major Histocompatibility Complex Class II Haplotypes

Infection and Immunity

Volumn 72, Issue 2, 2004, Pages 1096-1106

  Norimine, Junzo ^a   Mosqueda, Juan ^a,c   Palmer, Guy H ^a   Lewin, Harris A ^b   Brown, Wendy C ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c INSTITUTO NACIONAL DE INVESTIGACIONES FORESTALES   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; EPITOPE; HEAT SHOCK PROTEIN 20; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ANIMAL CELL; ANIMAL MODEL; ANTIGEN RECOGNITION; ARTICLE; BABESIA; BABESIA BOVIS; BABESIOSIS; CATTLE DISEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; HAPLOTYPE; IMMUNOBLOTTING; LYMPHOCYTE CLONE; MAJOR HISTOCOMPATIBILITY COMPLEX; MEROZOITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPOROZOITE; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; BABESIA BOVIS; CATTLE; CD4-POSITIVE T-LYMPHOCYTES; CONSERVED SEQUENCE; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; FEMALE; GENES, MHC CLASS II; HAPLOTYPES; HEAT-SHOCK PROTEINS; HSP20 HEAT-SHOCK PROTEINS; IMMUNIZATION; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; TICKS;

EID: 0842283047     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.2.1096-1106.2003     Document Type: Article

References (61)

1. Amills, M., V. Ramiya, J. Norimine, and H. A. Lewin. 1998. The major histocompatibility complex of ruminants. Rev. Sci. Tech. Off. Int. Epizoot. 1:108-120.
2. Arden, B., S. P. Clark, D. Kabelitz, and T. W. Mak. 1995. Human T-cell receptor variable gene segment families. Immunogenetics 42:455-500.
3. Bannister, L. H., J. M. Hopkins, R. E. Fowler, S. Krishna, and G. H. Mitchell. 2000. A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Immunol. Today 16:427-433.
4. Beyer, J. C., R. W. Stich, W. C. Brown, and W. P. Cheevers. 1998. Cloning and expression of caprine interferon-gamma. Gene 210:103-108.
5. Bohne, W., U. Gross, D. J. P. Ferguson, and J. Heesemann. 1995. Cloning and characterization of a bradyzoite-specifically expressed gene (hsp30/bag1) of Toxoplasma gondii, related to genes encoding small heat-shock proteins of plants. Mol. Microbiol. 16:1221-1230.
6. Brown, W. C., K. S. Logan, G. G. Wagner, and C. L. Tetzlaff. 1991. Cell-mediated immune responses to Babesia bovis antigens in cattle following infection with tick-derived or cultured parasites. Infect. Immun. 59:2418-2426.
7. Brown, W. C., K. S. Logan, S. Zhao, D. K. Bergman, and A. C. Rice-Ficht. 1995. Identification of Babesia bovis merozoite antigens separated by continuous-flow electrophoresis that stimulate proliferation of helper T cell clones derived from B. bovis-immune cattle. Infect. Immun. 63:106-116.
8. + T-lymphocyte clones specific for rhoptry-associated protein-1 (RAP-1) of Babesia bigemina stimulate enhanced immunoglobulin G1 (IgG1) and IgG2 synthesis. Infect. Immun. 67:155-164.
9. Brown, W. C., T. F. McElwain, B. J. Ruef, C. E. Suarez, V. Shkap, C. G. Chitko-McKown, A. C. Rice-Ficht, and G. H. Palmer. 1996. Babesia bovis rhoptry-associated protein-1 is immunodominant for T helper cells of immune cattle and contains T cell epitopes conserved among geographically distant B. bovis strains. Infect. Immun. 64:3341-3350.
10. + T lymphocytes recognize conserved immunodominant epitopes of Anaplasma marginale major surface protein la. Infect. Immun. 70:5521-5532.
11. - T lymphocyte epitopes that elicit strong recall responses. J. Immunol. 166:1114-1124.
12. Brown, W. C., and G. H. Palmer. 1999. Designing blood stage-stage-vaccines against Babesia bovis and B. bigemina. Parasitol. Today 15:275-281.
13. + T lymphocyte responses in B. bovis-immune cattle. Mol. Biochem. Parasitol. 119:97-109.
14. Brown, W. C., S. Zhao, V. M. Woods, C. A. Tripp, C. L. Tetzlaff, V. T. Heussler, D. A. Dobbelaere, and A. C. Rice-Ficht. 1993. Identification of two Th1 cell epitopes on the Babesia bovis-encoded 77-kilodalton merozoite protein (Bb-1) by use of truncated recombinant fusion proteins. Infect. Immun. 61:236-244.
15. Carson, R. T., K. M. Vignali, D. L. Woodland, and D. A. A. Vignali. 1997. T cell receptor recognition of MHC class II-bound peptide flanking residues enchances immunogenicity and results in altered TCR V region usage. Immunity 7:387-399.
16. Court, R. A. K. Sitte, J. P. Opdebeeck, and I. A. East. 1998. Mapping T cell epitopes of Babesia bovis antigen 12D3: implications for vaccine design. Parasite Immunol. 10:1-8.
17. Dagliesh, R. J., and N. P. Stewart. 1982. Some effects of time, temperature and feeding on infection rates with Babesia bovis and Babesia bigemina in Boophilus microplus larvae. Int. J. Parasitol. 12:323-326.
18. Davies, C. J., I. Joosten, D. L. Andersson, M. A. Arriens, D. Bernoco, B. Bissumbhar, G. Byrns, M. J. T. van Eijk, B. Kristensen, H. A. Lewin, S. Mikko, A. L. G. Morgan, N. E. Muggli-Cockett, P. R. Nilsson, R. A. Oliver, C. A. Park, J. J. van der Poel, M. Polli, R. L. Spooner, and J. A. Stewart. 1994. Polymorphism of bovine MHC class II genes. Joint report of the Fifth International Bovine Lymphocyte Antigen (BOLA) Workshop. Eur. J. Immunogenet. 21:259-289.
19. Davis, M. M., and M. G. McHeyzer-Williams. 1995. Antigen-specific development of primary and memory T cells in vivo. Science 268:106-111.
20. Dutia, B. M., L. MacCarthy-Morrough, E. J. Glass, R. L. Spooner, and J. Hopkins. 1995. Discrimination between major histocompatibility complex class II DQ and DR locus products in cattle. Anim. Genet. 26:111-114.
21. Doolan, D. L., S. L. Hoffman, S. Southwood, P. A. Wentworth, J. Sidney, R. W. Chesnut, E. Keough, E. Appella, T. B. Nutman, A. A. Lal, D. M. Gordon, A. Oloo, and A. Sette. 1997. Degenerate cytotoxic T cell epitopes from P. falciparum restricted by multiple HLA-A and HLB-B supertype alleles. Immunity 7:97-112.
22. Elwyn, Y. L., J. F. Elliott, S. Cwirla, L. L. Lanier, and M. M. Davis. 1989. Polymerase chain reaction with single-sided specificity: analysis of T cell receptor δ chain. Science 24:217-220.
23. Enders, B., E. Hundt, and B. Knapp. 1992. Strategies for the development of an antimalarial vaccine. Vaccine 10:920-927.
24. Glass, E. J., R. A. Oliver, and G. C. Russell. 2000. Duplicated DQ haplotypes increase the complexity of restriction element usage in cattle. J. Immunol. 165:134-138.
25. Goff, W. L., W. C. Johnson, S. M. Parish, G. M. Barrington, W. Tuo, and R. A. Valdez. 2001. The age-related immunity in cattle to Babesia bovis infection involves the rapid induction of interleukin-12, interferon-γ, and inducible nitric oxide synthase mRNA expression in the spleen. Parasite Immunol. 23:463-471.
26. Good, M. F. 2001. Towards a blood-stage vaccine for malaria: are we following all the leads? Nat. Rev. Immunol. 1:117-125.
27. Hines, S. A., G. H. Palmer, W. C. Brown, C. E. Suarez, O. Vidotto, T. F. McElwain, and A. C. Rice-Ficht. 1995. Genetic and antigenic characterization of Babesia bovis merozoite spherical body protein Bb-1. Mol. Biochem. Parasitol. 69:149-159.
28. Hines, S. A., G. H. Palmer, D. P. Jasmer, W. L. Goff, and T. F. McElwain. 1995. Immunization of cattle with recombinant Babesia bovis merozoite surface antigen-1. Infect. Immun. 63:349-352.
29. Horwitz, J. 1992. Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89:10449-10453.
30. Ishiguro, N., A. Tanaka, and M. Shinagawa. 1990. Sequence analysis of bovine T-cell receptor α chain. Immunogenetics 31:57-60.
31. Jakob, U., M. Gaestel, K. Engel, and J. Buchner. 1993. Small heat-shock proteins are molecular chaperones. J. Biol. Chem. 268:1517-1520.
32. Khusmith, S., Y. Charoenvit, S. Kumar, M. Sedegah, R. L. Beaudoin, and S. L. Hoffman. 1991. Protection against malaria by vaccination with sporozoite surface protein 2 plus CS protein. Science 252:715-718.
33. Knapp, B, E. Hundt, B. Enders, and H. A. Kupper. 1992. Protection of Aotus monkeys from malaria infection by immunization with recombinant hybrid proteins. Infect. Immun. 60:2397-2401.
34. Lindquist, S., and E. A. Craig. 1998. The heat-shock proteins. Annu. Rev. Genet. 22:631-77.
35. Löhr, C. V., K. A. Brayton, V. Shkap, R. T. Molad, A. F. Barbet, W. C. Brown, and G. H. Palmer. 2002. Expression of Anaplasma marginale major surface protein 2 operon-associated proteins during mammalian and arthropod infection. Infect. Immun. 70:6005-6012.
36. Mahoney, D. F. 1986. Studies on the protection of cattle against babesia bovis infection, p. 539-541. In W. I. Morrison (ed.), The ruminant immune system in health and disease. Cambridge University Press, Cambridge, United Kingdom.
37. McHeyzer-Williams, M. G., J. D. Altman, and M. M. Davis. 1996. Enumeration and characterization of memory cells in the TH compartment. Immunol. Rev. 150:5-21.
38. Mohamed, R. M., F. Aosai, M. Chen, H.-S. Mun, K. Norose, U. S. Belal, L.-X. Piao, and A. Yano. 2003. Induction of protective immunity by DNA vaccination with Toxoplasma gondii HSP70, HSP30, and SAG1 genes. Vaccine 21:2852-2861.
39. Mosqueda, J., T. F. McElwain, and G. H. Palmer. 2002. Babesia bovis surface antigen 2 proteins are expressed on the merozoite and sporozoite surface, and specific antibodies inhibit attachment and invasion of erythrocytes. Infect. Immun. 70:6448-6455.
40. Mosqueda, J., T. F. McElwain, D. Stiller, and G. H. Palmer. 2002. Babesia bovis merozoite surface antigen 1 and rhoptry-associated protein 1 are expressed in sporozoites and specific antibodies inhibit sporozoite attachment to erythrocytes. Infect. Immun. 70:1599-1603.
41. Moudgil, K. D., E. E. Sercarz, and I. S. Grewal. 1998. Modulation of the immunogenicity of antigenic determinants by their flanking residues. Immunol. Today 19:217-220.
42. Mun, H.-S., F. Aosai, and A. Yano. 1999. Role of Toxoplasma gondii Hsp70 and Toxoplasma godii Hsp30/bag1 in antibody formation and prophylactic immunity in mice experimentally infected with Toxocoplasma gondii. Microbiol. Immunol. 43:471-479.
43. + T lymphocyte responses in B. bovis-immune individuals are located in the amino-terminal domain. Infect. Immun. 70:2039-2048.
44. Norimine, J., J. Mosqueda, C. Suarez, G. H. Palmer, T. F. McElwain, G. Mbassa, and W. C. Brown. 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. Infect. Immun. 71:5021-5032.
45. Palmer, G. H., T. F. McElwain, L. E. Perryman, W. C. Davis, D. R. Reduker, D. P. Jasmer, V. Shkap, E. Pipano, W. L. Goff, and T. C. McGuire. 1991. Strain variation of Babesia bovis merozoite surface-exposed epitopes. Infect. Immun. 59:3340-3342.
46. Patarroyo, M. E., P. Romero, M. L. Torres, P. Clavijo, A. Moreno, A. Maritines, R. Rodriguez, F. Buzman, and E. Cabezas. 1987. Induction of protective immunity against experimental infection with malaria using synthetic peptides. Nature 328:629-632.
47. Rand, K. N., T. Moore, A. Sriskantha, K. Spring, R. Tellam, P. Willadsen, and G. S. Cobon. 1989. Cloning and expression of a protective antigen from the cattle tick Boophilus microplus. Proc. Natl. Acad. Sci. USA 86:9657-9661.
48. Reduker, D. W., D. P. Jasmer, W. L. Goff, L. E. Perryman, W. C. Davis, and T. C. McGuire. 1989. A recombinant surface protein in Babesia bovis elicits bovine antibodies that react with live merozoites. Mol. Biochem. Parasitol. 35:239-247.
49. Reinherz, E. L., K. Tan, L. Tang, P. Kern, J.-H. Liu, Y. Xiong, R. E. Hussey, A. Smolyar, B. Hare, R. Zhang, A. Joachimiak, H.-C. Chang, G. Wagner, and J.-H. Wang. 1999. The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286:1913-1921.
50. Sharif, S., B. A. Mallard, B. N. Wilkie, J. M. Sargeant, H. M. Scott, J. C. M. Dekkers, and K. E. Leslie. 1998. Associations of the bovine major histocompatibility complex DRB3 (BoLA-DRB3) alleles with occurrence of disease and milk somatic cell score in Canadian dairy cattle. Anim. Genet. 29:185-193.
51. Shoda, L. K. M., J. Florin-Christensen, M. Florin-Christensen, G. H. Palmer, and W. C. Brown. 2000. Babesia bovis-stimulated macrophages express interleukin-1β0, interleukin-12, tumor necrosis factor-alpha, and nitric oxide, and inhibit parasite replication in vitro. Infect. Immun. 68:5139-5145.
52. Stich, R. W., L. K. M. Shoda, M. Dreewes, B. Adler, T. W. Jungi, and W. C. Brown. 1998. Stimulation of nitric oxide production in macrophages by Babesia bovis. Infect. Immun. 66:4130-4136.
53. + T cell lines from genetically diverse cattle. Exp. Parasitol. 91:40-51.
54. Suarez, C. E., T. F. McElwain, E. B. Stephens, V. S. Misha, and G. H. Palmer. 1991. Sequence conservation among merozoite apical complex proteins of Babesia bovis, Babesia bigemina and other apicomplexa. Mol. Biochem. Parasitol. 49:329-332.
55. Tanaka, A., N. Ishiguro, and M. Shinagawa. 1990. Sequence and diversity of bovine T-cell receptor β-chain genes. Immunogenetics 32:263-271.
56. Tetzlaff, C. L., A. C. Rice-Ficht, V. M. Woods, and W. C. Brown. 1992. Induction of proliferative responses of T cells from Babesia bovis-immune cattle with a recombinant 77-kilodalton merozoite protein (Bb-1). Infect. Immun. 60:644-652.
57. Tuo, W., G. H. Palmer, T. C. McGuire, D. Zhu, and W. C. Brown. 2000. Interleukin-12 as an adjuvant promotes immunoglobulin G and type 1 cytokine recall responses to major surface protein 2 of the ehrlichial pathogen Anaplasma marginale. Infect. Immun. 68:270-80.
58. van Eijk, M. J. T., J. A. Stewart-Haynes, and H. A. Lewin. 1992. Extensive polymorphism of the BoLA-DRB3 gene distinguished by PCR-RFLP. Anim. Genet. 23:483-496.
59. Wright, I. G., R. Casu, M. A. Commins, B. P. Dalrymple, K. R. Gale, B. V. Goodger, P. W. Riddles, D. J. Waltisbuhl, I. Abetz, D. A. Berrie, Y. Bowles, C. Dimmock, T. Hayes, H. Kalnins, G. Leatch, R. McCrae, P. E. Montague, I. T. Nisbet, F. Parrodi, J. M. Peters, P. C. Scheiwe, W. Smith, K. Rode-Bramanis, and M. A. White. 1992. The development of a recombinant Babesia vaccine. Vet. Parasitol. 44:3-13.
60. Wright, I. G., B. V. Goodger, and I. A. Clark. 1988. Immunopathophysiology of Babesia bovis and Plasmodium falciparum infections. Parasitol. Today 4:214-218.
61. Zhang, Y., G. H. Palmer, J. R. Abbott, C. J. Howard, J. C. Hope, and W. C. Brown. 2003. CpG ODN 2006 and IL-12 are comparable for priming Thl lymphocyte and IgG responses in cattle immunized with a rickettsial outer membrane protein in alum. Vaccine 21:3307-3318.