Cellular and immunological basis of the host-parasite relationship during infection with Neospora caninum

Parasitology

Volumn 133, Issue 3, 2006, Pages 261-278

  Hemphill, A ^a   Vonlaufen, N ^a   Naguleswaran, A ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Cell surface receptors; Host cell invasion; Host cell modulation; Murine model; Neospora caninum; Stage conversion; Vaccination

Indexed keywords

DNA VACCINE; METALLOPROTEINASE; NEOGUARD; PROTOZOAL PROTEIN; PROTOZOAL VACCINE; RECOMBINANT VACCINE; SERINE PROTEINASE;

CATTLE; CELL ADHESION; CELL MEMBRANE; CELL SURFACE; CELL VACUOLE; CELLULAR IMMUNITY; DRUG SENSITIVITY; HOST CELL; HOST PARASITE INTERACTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOCOMPETENCE; IN VITRO STUDY; NEOSPORA CANINUM; NONHUMAN; PARASITE TRANSMISSION; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTOZOAL INFECTION; PROTOZOON; REVIEW; TOXOPLASMA GONDII; VACCINATION; VERTICAL TRANSMISSION;

ANIMALS; CATTLE; CATTLE DISEASES; CELL COMMUNICATION; CELLS, CULTURED; COCCIDIOSIS; HOST-PARASITE RELATIONS; LIFE CYCLE STAGES; MICE; NEOSPORA; PEPTIDE HYDROLASES; PROTOZOAN PROTEINS; PROTOZOAN VACCINES; RECEPTORS, CELL SURFACE;

ANIMALIA; BOS TAURUS; MURINAE; NEOSPORA CANINUM; TOXOPLASMA GONDII;

EID: 33747074886     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182006000485     Document Type: Review

References (156)

1. Alaeddine, F., Keller, N., Leepin, A. and Hemphill, A. (2005). Reduced infection and protection from clinical signs of cerebral neosporosis in C57BL/6 mice vaccinated with the recombinant microneme antigen NcMIC1. Journal of Parasitology 91, 657-665.
2. Alexander, J., Scharton-Kersten, T. M., Yap, G., Roberts, C. W., Liew, F. Y. and Sher, A. (1997). Mechanisms of innate resistance to Toxoplasma gondii. Philososphical Transactions of the Royal Societey London 352, 1355-1359.
3. Andrianarivo, A. G., Choromonaski, L., McDonough, S. P., Packham, A. E. and Conrad, P. A. (1999). Immunogenicity of a killed whole Neospora caninum tachyzoite preparation formulated with different adjuvants. International Journal for Parasitology 29, 1613-1625.
4. Athanassakis, I. and Iconomidou, B. (1996). Cytokine production in the serum and spleen of mice from day 6 to 14 of gestation : cytokines/placenta/ spleen/serum. Developmental Immunology 4, 247-255.
5. Atkinson, R., Harper, P. A., Ryce, C., Morrison, D. A. and Ellis, J. T. (1999). Comparison of the biological characteristics of two isolates of Neospora caninum. Parasitology 118, 363-370.
6. Barber, J. S., Homdahl, O. J., Owen, M. R., Guy, F., Uggla, A. and Trees, A. J. (1995). Characterization of the first European isolate of Neospora caninum (Dubey, Carpenter, Speer, Topper and Uggla). Parasitology 111, 563-568.
7. Baszler, T. V., Adams, S., Vander-Schalie, J., Mathison, B. A. and Kostovic, M. (2001). Validation of a commercially available monoclonal antibody-based competitive-inhibition enzyme-linked immunosorbent assay for detection of serum antibodies to Neospora caninum in cattle. Journal of Clinical Microbiology 39, 3851-3857.
8. Baszler, T. V., Knowles, D. P., Dubey, J. P., Gay, J. M., Mathison, B. A. and McElwain, T. F. (1996). Serological diagnosis of bovine neosporosis by Neospora caninum monoclonal antibody-based competitive inhibition enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 34, 1423-1428.
9. Baszler, T. V., Long, M. T., Mcelwain, T. F. and Mathison, B. A. (1999). Interferon-gamma and interleukin-12 mediate protection to acute Neospora caninum infection in BALB/c mice. International Journal for Parasitology 29, 1635-1646.
10. Beckers, C. J., Dubremetz, J. F., Mercereau-Puijalon, O. and Joiner, K. A. (1999). The Toxoplasma gondii rhoptry protein ROP 2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm. Journal of Cell Biology 27, 947-961.
11. Binder, E. M. and Kim, K. (2004). Location, location, location: traficking and function of secreted proteases of Toxoplasma and Plasmodium. Trafic 5, 914-924.
12. Bjerkås, I., Mohn, S. F. and Presthus, J. (1984). Unidentified cyst-forming sporozoon causing encephalomyelitis and myositis in dogs. Zeitschrift für Parasitenkunde 70, 271-274.
13. Björkman, C., Johansson, O., Stenlund, S., Holmdahl, O. J. M. and Uggla, A. (1996). Neospora species infection in a herd of dairy cattle. Journal of the American Veterinary Medical Association 208, 1441-1444.
14. Bohne, W., Heesemann, J. and Gross, U. (1994). Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: a possible role for nitric oxide in triggering stage conversion. Infection and Immunity 62, 1761-1767.
15. Boysen, P., Klevar, S., Olsen, I., and Storset, A. K. (2006). The protozoan Neospora caninum directly triggers bovine NK cells to produce gamma interferon and to kill infected fibroblasts. Infection and Immunity 74, 953-960.
16. Butcher, B. A. and Denkers, E. Y. (2002). Mechanism of entry determines the ability of Toxoplasma gondii to inhibit macrophage proinflammatory cytokine production. Infection and Immunity 70, 5216-5224.
17. Buxton, D., McAllister, M. M. and Dubey, J. P. (2002). The comparative pathogenesis of neosporosis. Trends Parasitology 18, 546-552.
18. Cannas, A., Naguleswaran, A., Müller, N., Gottstein, B., Eperon, S. and Hemphill, A. (2003a). Vaccination of mice against experimental N. caninum infection using NcSAG1- and NcSRS2-based recombinant antigens and DNA-vaccines. Parasitology 126, 303-312.
19. Cannas, A., Naguleswaran, A., Müller, N., Gottstein, B. and Hemphill, A. (2003b). Protective effect of vaccination with recombinant microneme protein NcMIC3 in mice following challenge infection with Neospora caninum tachyzoites. Journal of Parasitology 89, 44-50.
20. Carruthers, V. B. (2002). Host cell invasion by the opportunistic pathogen Toxoplasma gondii. Acta Tropica 81, 111-122.
21. Carruthers, V. B. and Blackman, M. J. (2005). A new release on life : emerging concepts in proteolysis and parasite invasion. Molecular Microbiology 55, 1617-1630.
22. Cesbron-Delauw, M. F., Lecordier, L. and Mercier, C. (1996). Role of secretory dense granule organelles in the pathogenesis of toxoplasmosis. Current Topics in Microbiology and Immunology 219, 59-65.
23. Choromanski, L. J. (2002). Neospora caninum vaccine field safety evaluation. Intervet Bulletin 1-3.
24. Cole, R. A., Lindsay, D. S., Blagburn, B. L. and Dubey, J. P. (1995). Vertical transmission of Neospora caninum in mice. Journal of Parasitology 81, 730-732.
25. Cooper, C. E. (1999). Nitric oxide and iron proteins. Biochimica et Biophysica Acta 1411, 290-309.
26. Darcy, F. and Santoro, F. (1994). Toxoplasmosis. In Parasitic Infections and the Immune System (ed. Kierszenbaum, F.), pp. 163-190. Academic Press, New York.
27. Davison, H. C., Otter, A. and Trees, A. J. (1999). Estimation of vertical and horizontal transmission parameters of Neospora caninum infections in dairy cattle. International Journal for Parasitology 29, 1683-1689.
28. Denkers, E. Y., Butcher, B. A., Del Rio, L. and Kim, L. (2004). Manipulation of mitogen-activated protein kinase/nuclear factor-kappaB-signaling cascades during intracellular Toxoplasma gondii infection. Immunology Review 201, 191-205.
29. Dijkstra, T., Barkema, H. W., Eysker, M. and Wouda, W. (2001). Evidence of post-natal transmission of Neospora caninum in Dutch dairy herds. International Journal for Parasitology 31, 209-215.
30. Dowse, T. J., Pascall, J. C., Brown, K. D. and Soldati, D. (2005). Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion. International Journal for Parasitology 35, 747-756.
31. Dowse, T. J. and Soldati, D. (2004). Host cell invasion by the apicomplexans: the significance of microneme protein proteolysis. Current Opinion in Microbiology 7, 388-396.
32. Dubey, J. P. (2003). Review of Neospora caninum and neosporosis in animals. The Korean Journal of Parasitology 41, 1-16.
33. Dubey, J. P., Barr, B. C., Barta, J. R., Bjerkas, I., Bjorkman, C., Blagburn, B. L., Bowman, D. D., Buxton, D., Ellis, J. T., Gottstein, B., Hemphill, A., Hill, D. E., Howe, D. K., Jenkins, M. C., Kobayashi, Y., Koudela, B., Marsh, A. E., Mattsson, J. G., McAllister, M. M., Modry, D., Omata, Y., Sibley, L. D., Speer, C. A., Trees, A. J., Uggla, A., Upton, S. J., Williams, D. J. and Lindsay, D. S. (2002). Redescription of Neospora caninum and its differentiation from related coccidia. International Journal for Parasitology 32, 929-946.
34. Dubey, J. P., Carpenter, J. L., Speer, C. A., Topper, M. J. and Uggla, A. (1988a). Newly recognized fatal protozoan disease of dogs. Journal of the American Veterinary Medical Association 192, 1269-1285.
35. Dubey, J. P., Hattel, A. L., Lindsay, D. S. and Topper, M. J. (1988b). Neonatal Neospora caninum infection in dogs: isolation of the causative agent and experimental transmission. Journal of the American Veterinary Medical Association 193, 1259-1263.
36. Dubey, J. P. and Lindsay, D. S. (1996). A review of Neospora caninum and neosporosis. Veterinary Parasitology 67, 1-59.
37. Eperon, S., Broennimann, K., Hemphill, A. and Gottstein, B. (1999). Susceptibility of B-cell deficient C57BL/6 (μMT) mice to Neospora caninum infection. Parasite Immunology 21, 225-236.
38. Fernandez-Garcia, A., Risco-Castillo, V., Zaballos, A., Alvarez-Garcia, G. and Ortega-Mora, L. M. (2005). Identification and molecular cloning of the Neospora caninum SAG4 gene specifically expressed at bradyzoite stage. Molecular and Biochemical Parasitology [Epub ahead of print].
39. French, N. P., Clancy, D., Davison, H. C. and Trees, A. J. (1999). Mathematical models of Neospora caninum infection in dairy cattle : transmission and options for control. International Journal for Parasitology 29, 1691-1704.
40. Fuchs, N., Bütikofer, P., Sonda, S. and Hemphill, A. (1999). Detection of surface-associated and intracellular glycoconjugates and glycoproteins in Neospora caninum tachyzoites. International Journal for Parasitology 29, 1597-1611.
41. Gazzinelli, R. T., Amichay, D., Sharton-Kersten, T., Grunwald, E., Farber, J. M. and Sher, A. (1996). Role of macrophage-derived cytokines in the induction and regulation of cell-mediated immunity to Toxoplasma gondii. Current Topics in Microbiology and Immunology 219, 127-139.
42. Goebel, S., Gross, U. and Luder, C. G. (2001). Inhibition of host cell apoptosis by Toxoplasma gondii is accompanied by reduced activation of the caspase cascade and alterations of poly(ADP-ribose) polymerase expression. Journal of Cell Science 114, 3495-3505.
43. Gondim, M., McAllister, M. M., Anderson-Sprecher, R. C., Björkman, C., Locks, T. F., Firkins, L. D., Gao, L. and Fisxher, W. R. (2005). Transplacental transmission and abortion in cows administred Neospora caninum oocysts. Journal of Parasitology 90, 1394-1400.
44. Gondim, M., McAllister, M. M., Pitt, W. C. and Zemlicka, D. E. (2004). Coyotes (Canis latrans) are definitive hosts of Neospora caninum. International Journal for Parasitology 34, 159-161.
45. Graham, D. A., Calvert, V., Whyte, M. and Marks, J. (1999). Absence of serological evidence for human Neospora caninum infection. Veterinary Record 144, 672-673.
46. Guy, C. S., Williams, D. J. L., Kelley, D. F., McGarry, J. W., Guy, F., Bjorkman, C., Smith, R. F. and Trees, A. J. (2001). Neospora caninum in persitently infected, pregnant cows: spontaneous transplacental infection is associated with an acute increase in maternal antibody. Veterinary Record 149, 443-449.
47. Haldorson, G. J., Mathison, B. A., Wenberg, K., Conrad, P. A., Dubey, J. P., Trees, A. J., Yamane, I. and Baszler, T. V. (2005). Immunization with native surface protein NcSRS2 induces a Th2 immune response and reduces congenital Neospora caninum transmission in mice. International Journal for Parasitology 35, 1407-1415.
48. Hemphill, A. (1996). Subcellular localization and functional characterization of Nc-p43, a major Neospora caninum tachyzoite surface protein. Infection and Immunity 64, 4279-4287.
49. Hemphill, A. (1999). The host-parasite relationship in neosporosis. Advances in Parasitology 43, 47-104.
50. Hemphill, A., Gajendran, N., Sonda, S., Fuchs, N., Gottstein, B., Hentrich, B. and Jenkins, M. (1998). Identification and characterization of a dense granule-associated protein in Neospora caninum tachyzoites. International Journal for Parasitology 28, 429-438.
51. Hemphill, A. and Gottstein, B. (2000). A European perspective on Neospora caninum. International Journal for Parasitology 30, 877-924.
52. Hemphill, A., Gottstein, B. and Kaufmann, H. (1996). Adhesion and invasion of bovine endothelial cells by Neospora caninum. Parasitology 112, 183-197.
53. Hemphill, A., Fuchs, N., Sonda, S., Gottstein, B. and Hentrich, B. (1997). Identification and partial characterization of a 36 kD surface protein on Neospora caninum tachyzoites. Parasitology 115, 371-380.
54. Hemphill, A., Vonlaufen, N., Naguleswaran, A., Keller, N., Riesen, M., Guetg, N., Srinivasan, S. and Alaeddine, F. (2004). Tissue culture and explant approaches to studying and visualizing Neospora caninum and its interactions with the host cell. Microscopy and Microanalysis 10, 602-620.
55. Heussler, V., Küenzi, P. and Rottenberg, S. (2001). Inhibition of apoptosis by intracellular protozoan parasites. International Journal for Parasitology 31, 1166-1176.
56. Heydorn, A. O. and Mehlhorn, H. (2002). A re-evaluation of Neospora and Hammondia spp. Trends in Parasitology 18, 246.
57. Hisaeda, H., Sakai, T., Ishikawa, H., Maekawa, ,Y., Yasumoto, K., Good, R. A. and Himeno, K. (1997). Heat shock protein 65 induced by gamma delta T cells prevents apoptosis of macrophages and contributes to host defense in mice infected with Toxoplasma gondii. Journal of Immunology 159, 2375-2378.
58. Hisaeda, H., Sakai, T., Nagasawa, H., Ishikawa, H., Yasutomo, K., Maekawa, Y. and Himeno, K. (1996). Contribution of extrathymic interferon gamma delta T cells to the expression of heat shock protein and to protective immunity in mice infected with Toxoplasma gondii. Immunology 88, 551-557.
59. Howe, D. K. and Sibley, L. D. (1995). Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. Journal of Infectious Diseases 172, 1561-1566.
60. Howe, D. K., Crawford, A. C., Lindsay, D. and Sibley, L. D. (1998). The p29 and p35 immunodominant antigens of Neospora caninum tachyzoites are homologous to the family of surface antigens of Toxoplasma gondii. Infection and Immunity 66, 5322-5328.
61. Innes, E. A., Andrianarivo, A. G., Björkman, C., Williams, D. J. and Conrad, P. A. (2002). Immune responses to Neospora caninum and prospects for vaccination. Trends in Parasitology 18, 497-504.
62. Innes, E. A., Buxton, D., Eperon, S. and Gottstein, B. (2000). Immunology of Neospora caninum infection in cattle and mice. International Journal for Parasitology 30, 896-900.
63. Innes, E. A., Wright, S. E., Maley, S., Rae, A., Schock, A., Kirvar, E., Bartley, P., Hamilton, C., Carey, I. M. and Buxton, D. (2001). Protection against vertical transmission in bovine neosporosis. International Journal for Parasitology 31, 1523-1534.
64. Innes, E. A., Wright, S., Bartley, P., Maley, S., Macaldowie, C., Esteban Redondo, I. and Buxton, D. (2005). The host-parasite relationship in bovine neosporosis. Veterinary Immunology and Immunopathology 108, 29-36.
65. Jenkins, M., Parker, C., Tuo, W., Vinyard, B. and Dubey, J. P. (2004). Inclusion of Cpg adjuvant with plasmid DNA coding for NcGRA7 improves protection against congenital neosprosis. Infection and Immunity 72, 1817-1819.
66. Kano, R., Masukata, Y., Omata, Y., Kobayashi, Y., Maeda, R. and Saito, A. (2005). Relationship between type 1/type 2 immune responses and occurrence of vertical transmission in Balb/c mice infected with Neospora caninum. Veterinary Parasitology 129, 159-164.
67. + T-cells protect against lethal toxoplasmosis in mice infected with Neospora caninum. Infection and Immunity 66, 1554-1560.
68. Keeley, A. and Soldati, D. (2004). The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends in Cell Biology 14, 528-532.
69. Keller, N., Naguleswaran, A., Cannas, A., Vonlaufen, N., Bienz, M., Björkman, C., Bohne, W. and Hemphill, A. (2002). Identification of a Neospora caninum microneme protein (NcMIC1) which interacts with sulfated host cell surface glycosaminoglycans. Infection and Immunity 70, 3187-3198.
70. Keller, N., Riesen, M., Naguleswaran, A., Vonlaufen, N., Stettler, R., Leepin, A., Wastling, J. M. and Hemphill, A. (2004). Identification and characterization of a Neospora caninum microneme-associated protein (NcMIC4) that exhibits unique lactose-binding properties. Infection and Immunity 72, 4791-4800.
71. Khan, I. A., Schwartzman, J. D., Fonseka, S. and Kasper, L. H. (1997). Neospora caninum: role for immune cytokines in host immunity. Experimental Parasitology 85, 24-34.
72. Kim, K. (2004). Role of proteases in host cell invasion by Toxoplasma gondii and other apicomplexa. Acta Tropica 91, 69-81.
73. Kirkman, L. A., Weiss, L. M. and Kim, K. (2001). Cyclic nucleotide signaling in Toxoplasma gondii bradyzoite differentiation. Infection and Immunity 69, 148-153.
74. Lecordier, L., Mercier, C., Sibley, L. D. and Cesbron-Delauw, M. F. (1999). Transmembrane insertion of the Toxoplasma gondii GRA5 protein occurs after soluble secretion into the host cell. Molecular Biology of the Cell 10, 1277-1287.
75. Lei, Y., Davey, M. and Ellis, J. T. (2005a). Attachment and invasion of Toxoplasma gondii and Neospora caninum to epithelial and fibroblast cell lines in vitro. Parasitology 131, 583-590.
76. Lei, Y., Birch, D., Davey, M. and Ellis, J. T. (2005b). Subcellular fractionation and molecular characterization of the pellicle and plasmalemma of Neospora caninum. Parasitology 131, 467-475.
77. Liddell, S., Jenkins, M., Collica, C. M. and Dubey, J. P. (1999). Prevention of vertical transfer of Neospora caninum in BALB/c mice by vaccination. Journal of Parasitology 85, 1072-1075.
78. Liddell, S., Parker, C., Vinyard, B., Jenkins, M. and Dubey, J. P. (2003). Immunization of mice with plasmid DNA coding for NcGRA7 and NcHSP33 con fers partial protection against vertical transmission of Neospora caninum. Journal of Parasitology 89, 496-500.
79. Lindsay, D. S. and Dubey, J. P. (1989). Neospora caninum (Protozoa: apicomplexa) infections in mice. Journal of Parasitology 75, 772-779.
80. Lindsay, D. S., Dubey, J. P. and Duncan, R. B. (1999a). Confirmation that the dog is a definitive host for Neospora caninum. Veterinary Parasitology 82, 327-333.
81. Lindsay, S. D., Lenz, R., Blagburn, B. L. and Brake, D. A. (1999b). Characterization of temperature-sensitive strains of Neospora caninum in mice. Journal of Parasitology 85, 64-67.
82. Lindsay, S. D., Lenz, R., Cole, R. A. J., Dubey, J.P. and Blagburn, B. L. (1995). Mouse model for central nervous system Neospora caninum infections. Journal of Parasitology 81, 313-315.
83. Long, M. T. and Baszler, T. V. (1996). Fetal loss in BALB/c mice infected with Neospora caninum. Journal of Parasitology 82, 608-611.
84. Long, M. T., Baszler, T. V. and Mathison, B. A. (1998). Comparison of intracerebral parasite load, lesion development, and systemic cytokines in mouse strains infected with Neospora caninum. Journal of Parasitology 84, 316-320.
85. Long, M. T. and Baszler, T. V. (2000). Neutralization of maternal IL-4 modulates congenital protozoal transmission: comparison of innate versus acquired immune responses. Journal of Immunology 164, 4768-4774.
86. Louie, K. and Conrad, P. A. (1999). Characterization of a cDNA encoding a subtilisin-like serine protease (NC-p65) of Neospora caninum. Molecular and Biochemical Parasitology 107, 211-223.
87. Louie, K., Nordhausen, R., Robinson, T. W., Barr, B. C. and Conrad, P. A. (2002). Characterization of a Neospora caninum protease, NcSUB1 (NC-P65), with rabbit anti-N54. Journal of Parasitology 88, 1113-1119.
88. Lovett, J. L., Howe, D. K. and Sibley, L. D. (2000). Molecular characterization of a thrombospondin-related anonymous protein homologue in Neospora caninum. Molecular and Biochemical Parasitology 107, 33-43.
89. Luder, C. G., Algner, M., Lang, C., Bleicher, N. and Gross, U. (2003a). Reduced expression of the inducible nitric oxide synthase after infection with Toxoplasma gondii facilitates parasite replication in activated murine macrophages. International Journal for Parasitology 33, 833-844.
90. Luder, C. G., Lang, C., Giraldo-Velasquez, M., Algner, M., Gerdes, J. and Gross, U. (2003b). Toxoplasma gondii inhibits MHC class II expression in neural antigen-presenting cells by down-regulating the class II transactivator CIITA. Journal of Neuroimmunology 134, 12-24.
91. Luder, C. G., Walter, W., Beuerle, B., Maeurer, M. J. and Gross, U. (2001). Toxoplasma gondii down-regulates MHC class II gene expression and antigen presentation by murine macrophages via interference with nuclear translocation of STAT1alpha. European Journal of Immunology 31, 1475-1484.
92. Lunden, A., Marks, J., Maley, S. W. and Innes, E. A. (1998). Cellular immune responses in cattle experimentally infected with Neospora caninum. Parasite Immunology 20, 519-526.
93. Lunden, A., Wright, S., Allen, J. E. and Buxton, D. (2002). Immunisation of mice against neosporosis. International Journal for Parasitology 32, 867-876.
94. Lyons, R. E., McLeod, R. and Roberts, C. W. (2002). Toxoplasma gondii tachyzoite-bradyzoite interconversion. Trends in Parasitology 18, 198-201.
95. McAllister, M. M., Bjoerkman, C., Anderson-Sprecher, R. and Rogers, D. G. (2000). Evidence of point-source exposure to Neospora caninum and protective immunity in a herd of beef cows. Journal of the American Veterinary Medical Association 217, 881-887.
96. McAllister, M. M., Dubey, J. P., Lindsay, D. S., Jolley, W. R., Wills, R. A. and McGuire, A. M. (1998). Dogs are definitive hosts of Neospora caninum. International Journal for Parasitology 28, 1473-1478.
97. Mercier, C., Adjogble, K. D., Daubener, W. and Delauw, M. F. (2005). Dense granules: are they key organelles to help understand the parasitophorous vacuole of all apicomplexan parasites? International Journal for Parasitology 35, 8298-8249.
98. Miller, C. M., Quinn, H. E., Reichel, M. P. and Ellis, J. T. (2005). Reduction in transplacental transmission of Neospora caninum in outbred mice by vaccination. International Journal for Parasitology 35, 821-828.
99. Molestina, R. E., Payne, T. M., Coppens, I. and Sinai, A. P. (2003). Activation of NF-kappaB by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated IkappaB to the parasitophorous vacuole membrane. Journal of Cell Science 116, 4359-4371.
100. Molestina, R. E. and Sinai, A. P. (2005). Detection of a novel parasite kinase activity at the Toxoplasma gondii parasitophorous vacuole membrane capable of phophorylating host IkBa. Cellular Microbiology 7, 351-362.
101. Mordue, D. G., Desai, N., Dustin, M. and Sibley, L. D. (1999). Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. Journal of Experimental Medicine 190, 1783-1792.
102. Mordue, D. G. and Sibley, L. D. (1997). Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. Journal of Immunology 159, 4452-4459.
103. Naguleswaran, A., Alaeddine, F., Guionaud, C., Vonlaufen, N., Sonda, S., Jenoe, P., Mevissen, M. and Hemphill, A. (2005). Neospora caninum protein disulfide isomerase is involved in tachyzoite-host cell interaction. International Journal for Parasitology 35, 1459-1472.
104. Naguleswaran, A., Cannas, A., Keller, N., Vonlaufen, N., Björkman, C. and Hemphill, A. (2002). Vero cell surface proteoglycan interaction with the microneme protein NcMIC3 mediates adhesion of Neospora caninum tachyzoites to host cells unlike that in Toxoplasma gondii. International Journal for Parasitology 32, 695-704.
105. Naguleswaran, A., Cannas, A., Keller, N., Vonlaufen, N., Schares, G., Conraths, F. J., Björkman, C. and Hemphill, A. (2001). Neospora caninum microneme protein NcMIC3: Secretion, subcellular localization and functional involvement in host cell interaction. Infection and Immunity 69, 6483-6494.
106. Naguleswaran, A., Müller, N. and Hemphill, A. (2003). Neospora caninum and Toxoplasma gondii: a novel adhesion/invasion assay reveals distinct differences in tachyzoite-host cell interactions. Experimental Parasitology 104, 149-158.
107. Nishikawa, Y., Inoue, N., Xuan, X., Nagasawa, H., Igarasha, I., Fujisaka, K., Otsuka, H. and Mikami, T. (2001a). Protective vaccination by recombinant vaccinia virus against Neospora caninum infection. Vaccine 19, 1381-1390.
108. Nishikawa, Y., Xuan, X., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. (2001b). Prevention of vertical transmission of Neospora caninum in BALB/c mice by recombinant vaccinia virus carrying NcSRS2 gene. Vaccine 19, 1710-1716.
109. Nishikawa, Y., Mishima, M., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. (2001c). Interferon gamma induced apoptosis in host cells infected with Neospora caninum. Parasitology 123, 25-31.
110. Nishikawa, Y., Makala, L., Otsuka, H., Mikami, T. and Nagasawa, H. (2002). Mechanisms of apoptosis in murine fibroblasts by two intracellular protozoan parasites, Toxoplasma gondii and Neospora caninum. Parasite Immunology 24, 347-354.
111. Nishikawa, Y., Xuan, X., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. (2000). Monoclonal antibody inhibition of Neospora caninum tachyzoite invasion into host cells. International Journal for Parasitology 30, 51-58.
112. Omata, Y., Kano, R., Masukata, Y., Kobayashi, Y., Igarashi, M., Maeda, R. and Saito, R. (2005). Development of Neospora caninum cultured with human serum in vitro and in vivo. Journal of Parasitology 91, 222-225.
113. Opitz, C. and Soldati, D. (2002). 'The glideosome' : a dynamic complex powering gliding motion and host cell invasion by Toxoplasma gondii. Molecular Microbiology 45, 597-604.
114. Paré, J., Thurmond, M. C. and Hietala, S. K. (1996). Congenital Neospora caninum infection in dairy cattle and associated calfhood mortality. Canadian Journal of Veterinary Research 60, 133-139.
115. Peters, M., Lütkefels, E., Heckeroth, A. R. and Schares, G. (2001). Immunohistochemical and ultrastructural evidence for Neospora caninum tissue cysts in skeletal muscles of naturally infected dogs and cattle. International Journal for Parasitology 31, 1144-1148.
116. Petersen, E., Lebech, M., Jensen, L., Lind, P., Rask, M., Bagger, P., bjorkman, C. and Uggla, A. (1999). Neospora caninum infection and repeated abortions in humans. Emerging Infectious Diseases 5, 278-280.
117. Pinitkiatisakul, S., Mattsson, J. G., Wikman, M., Friedman, M., Bengtsson, K. L., Stahl, S. and Lunden, A. (2005). Immunization of mice against neosporosis with recombinant NcSRS2 iscoms. Veterinary Parasitology 129, 25-34.
118. Purner, M. B., Berens, P. B., Nash, P. B., van Linden, A., Ross, E., Kruse, C., Krug, E. C. and Cureil, T. J. (1996). CD4-mediated and CD8-mediated cytotoxic and proliferative immune responses to Toxoplasma gondii in seropositive humans. Infection and Immunity 64, 4330-4338.
119. Quinn, H. E., Ellis, J. T. and Smith, N. C. (2002). Neospora caninum: a cause of immune-mediated failure of pregnancy? Trends in Parasitology 18, 391-394.
120. Quinn, H. E., Miller, C. M. and Ellis, J. T. (2004). The cell-mediated immune response to Neospora caninum during pregnancy in the mouse is associated with a bias towards production of interleukin-4. International Journal for Parasitology 34, 723-732.
121. Rettigner, C., De Meerschman, F., Focant, C., Vanderplasschen, A. and Losson, B. (2004). The vertical transmission following the reactivation of a Neospora caninum chronic infection does not seem to be due to an alteration of the systemic immune response in pregnant CBA/Ca mice. Parasitology 128, 149-160.
122. Risco-Castillo, V., Fernandez-Garcia, A. and Ortega-Mora, L. M. (2004). Comparative analysis of stress agents in a simplified in vitro system of Neospora caninum bradyzoite production. Journal of Parasitology 90, 466-470.
123. Ritter, D. M., Kerlin, R., Sibert, G. and Brake, D. (2002). Immune factors influencing the course of infection with Neospora caninum in the murine host. Journal of Parasitology 88, 271-280.
124. Romero, J. J., Perez, E. and Frankena, K. (2004). Effect of a killed whole Neospora caninum tachyzoite vaccine on the crude abotion rate of Costa Rican dairy cows under field conditions. Veterinary Parasitology 123, 149-159.
125. Schares, G., Peters, M., Wurm, R., Barwald, A. and Conraths, F. J. (1998). The efficiency of vertical transmission of Neospora caninuim in dairy cattle analysed by serological techniques. Veterinary Parasitology 80, 87-98.
126. Schares, G., Zinecker, C. F., Schmidt, J., Azzouz, N., Conraths, F. J., Gerold, P. and Schwarz, R. T. (2000). Structural analysis of free and protein-bound glycosyl-phosphatidylinositols of Neospora caninum. Molecular and Biochemical Parasitology 105, 155-161.
127. Sher, A., Denkers, E. Y. and Gazzinelli, R. T. (1995). Induction and regulation of host cell mediated immunity by Toxoplasma gondii. Ciba Foundation Symposium 195, 95-104.
128. Shibahara, T., Kokuho, T., Eto, M., Haritani, M., Hamaoka, T., Shimura, K., Nakamura, K., Yokomizo, Y. and Yamane, I. (1999). Pathological and immunological findings of athymic nude and congenic wild type BALB/c mice experimentally infected with Neospora caninum. Veterinary Pathology 36, 321-327.
129. Sinai, A. P. and Joiner, K. (2001). The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. Journal of Cell Biology 154, 95-108.
130. Sinai, A. P., Payne, T. M., Carmen, J. C., Hardi, L., Watson, S. J. and Molestina, R. E. (2004). Mechanisms underlying the manipulation of host apoptotic pathways by Toxoplasma gondii. International Journal for Parasitology 34, 381-391.
131. Sinai, A. P., Webster, P. and Joiner, K. (1997). Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high afinity interaction. Journal of Cell Science 110, 2117-2128.
132. Soete, M., Camus, D. and Dubremetz, J. F. (1994). Experimental induction of bradyzoite-specific antigen expression and cyst formation by the RH strain of Toxoplasma gondii in vitro. Experimental Parasitology 78, 361-370.
133. Soldati, D., Dubremetz, J. F. and Lebrun, M. (2001). Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii. International Journal for Parasitology 31, 1293-1302.
134. Sonda, S., Fuchs, N., Connolly, B., Fernandez, P., Gottstein, B. and Hemphill, A. (1998). The major 36 kDa Neospora caninum tachyzoite surface protein is closely related to the major Toxoplasma gondii surface antigen 1. Molecular and Biochemical Parasitology 97, 97-108.
135. Sonda, S., Fuchs, N., Gottstein, B. and Hemphill, A. (2000). Molecular characterization of a novel microneme antigen in Neospora caninum. Molecular and Biochemical Parasitology 108, 39-51.
136. Speer, C. A., Dubey, J. P., McAllister, M. M. and Blixt, J. A. (1999). Comparative ultrastructure of tachyzoites, bradyzoites, and tissue cysts of Neospora caninum and Toxoplasma gondii. International Journal for Parasitology 29, 1509-1519.
137. Staska, L. M., Dvies, C., Brown, W. C., McGuire, T. C., Suarez, C. E., Park, J. Y., Mathison, B. A., Abbott, J. R. and Baszler, T. V. (2005). Identification of vaccine candidate peptides in the NcSRS2 surface protein of Neospora caninum by using CD4+ cytotoxic T lymphocytes and gamma interferon secreting T lymphocytes of infected Holstein cattle. Infection and Immunity 73, 1321-1329.
138. Staska, L. M., McGuire, T. C., Davies, C. J., Lewin, H. A. and Baszler, T. V. (2003). Neospora caninum infected cattle develop parasite specific CD4+ cytotoxic T lymphocytes. Infection and Immunity 71, 3272-3279.
139. Stenlund, S., Bjorkman, C., Holmdahl, O. J., Kindahl, H. and Uggla, A. (1997). Characterization of a Swedish bovine isolate of Neospora caninum. Parasitology Research 83, 214-219.
140. Tenter, A. M. and Johnson, A. M. (1997). Phylogeny of the tissue cyst-forming coccidian. Advances in Parasitology 39, 169-139.
141. Tomley, F. M. and Soldati, D. S. (2001). Mix and match modules: structure and function of microneme proteins in apicomplexan parasites. Trends in Parasitology 17, 81-88.
142. Tranas, J., Heinzen, R. A., Weiss, L. M. and McAllister, M. M. (1999). Serological evidence of human infection with the protozoan Neospora caninum. Clinical and Diagnostic Laboratory Immunology 6, 765-777.
143. Trees, A. J., McAllister, M. M., Guy, C. S., McGarry, J. W., Smith, R. F. and Williams, D. J. (2002). Neospora caninum: oocyst challenge of pregnant cows. Veterinary Parasitology 109, 147-154.
144. Tunev, S. S., McAllister, M. M., Anderson-Sprecher, R. C. and Weiss, L. M. (2002). Neospora caninum in vitro: evidence that the destiny of a parasitophorous vacuole depends on the phenotype of the progenitor zoite. Journal of Parasitology 88, 1095-1099.
145. Tuo, W., Davis, W. C., Fetterer, R., Jenkins, M., Boyd, P. C., Gasbarre, L. C. and Dubey, J. P. (2004). Establishment of Neospora antigen-specific T cell lines of primarily CD4 T cells. Parasite Immunology 26, 243-246.
146. Tuo, W., Fetterer, R. H., Davis, W. C., Jenkins, M. C. and Dubey, J. P. (2005). Neospora antigens defined by antigen-dependent bovine CD4+ T cells. Journal of Parasitology 91, 564-568.
147. Uchida, Y., Ike, K., Kurotaki, T., Ito, A. and Imai, S. (2004). Monoclonal antibodies preventing invasion of Neospora caninum tachyzoites into host cells. Journal of Veterinary Medical Science 66, 1355-1358.
148. Uggla, A., Stenlund, S., Holmdahl, O. J. M., Jakubek, E. B., Thebo, P., Kindahl, H. and Björkman, C. (1998). Oral Neospora caninum inoculation of neonatal calves. International Journal for Parasitology 28, 1467-1472.
149. Vonlaufen, N., Guetg, N., Naguleswaran, A., Müller, N., Bjorkman, C., Schares, G., von Blumroeder, D., Ellis, J. and Hemphill, A. (2004). In vitro induction of Neospora caninum bradyzoites in Vero cells reveals differential antigen expression, localization, and host-cell recognition of tachyzoites and
150. Vonlaufen, N., Müller, N., Keller, N., Naguleswaran, A., Bohne, W., McAllister, M., Björkman, C., Müller, E., Caldelari, R. and Hemphill, A. (2002). Exogenous nitric oxide triggers Neospora caninum tachyzoite-to- bradyzoite stage conversion in murine epidermal keratinocyte cell cultures. International Journal for Parasitology 32, 1253-1265.
151. Weiss, L. M., Ma, Y. F., Halonen, S., McAllister, M. M. and Zhang, Y. W. (1999). The in vitro development of Neospora caninum bradyzoites. International Journal for Parasitology 29, 1713-1723.
152. Williams, D. J., Guy, C. S., Smith, R. F., Guy, F., McGarry, J. W., McKay, J. S. and Trees, A. J. (2003). First demonstration of protective immunity against foetopathy in cattle with latent Neospora caninum infection. International Journal for Parasitology 33, 1059-1065.
153. Williams, D. J., Guy, C. S., McGarry, J. W., Guy, F., Tasker, L., Smith, R. F., MacEachern, K., Cripps, P. J., Kelly, D. F. and Trees, A. J. (2000). Neospora caninum-associated abortion in cattle : the time of experimentally-induced parasitaemia during gestation determines foetal survival. Parasitology 121, 347-358.
154. Williams, D. J. and Trees, A. J. (2006). Protecting babies: vaccine strategies to prevent foetopathy in Neospora-infected cattle. Parasite Immunology 28, 61-67.
155. Wouda, W., Bartels, C. J. M. and Moen, A. R. (1999). Characteristics of Neospora caninum associated abortion strorms in dairy herds in the Netherlands (1995-1997). Theriogenology 52, 233-245.
156. Yamage, M., Flechtner, O. and Gottstein, B. (1996). Neospora caninum: specific oligonucleotide primers for the detection of brain "cyst" DNA of experimentally infected nude mice by the polymerase chain reaction (PCR). Journal of Parasitology 82, 272-279.