Characterization of the B-cell immune response elicited in BALB/c mice challenged with Neospora caninum tachyzoites

Immunology

Volumn 116, Issue 1, 2005, Pages 38-52

  Teixeira, Luzia ^a   Marques, Andreia ^a   Meireles, Carla Sofia ^a   Seabra, Ana Rita ^a   Rodrigues, Diana ^a   Madureira, Pedro ^a   Faustino, Augusto M R ^a   Silva, Carolina ^a   Ribeiro, Adília ^a   Ferreira, Paula ^a,b   Da Costa, José Manuel Correia ^a,c   Canada, Nuno ^a   Vilanova, Manuel ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c NATIONAL INSTITUTE OF HEALTH   (Portugal)

Author keywords

Antibodies; B cells; Neospora caninum

Indexed keywords

B7 ANTIGEN; CD69 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN M;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL LINEAGE; CELL MATURATION; CELL POPULATION; CELL SURFACE; CONTROLLED STUDY; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFECTION SENSITIVITY; LETHALITY; MALE; MOUSE; MOUSE STRAIN; NEOSPORA CANINUM; NONHUMAN; PERITONEUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL;

EID: 23944462617     PISSN: 00192805     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2005.02195.x     Document Type: Article

References (53)

1. Bjerkås I, Mohn SF, Presthus J. Unidentified cyst-forming sporozoan causing encephalomyelitis and myositis in dogs. Z Parasitenkd 1984; 70:271-4.
2. Dubey JP. Review of Neospora caninum and neosporosis in animals. Korean J Parasitol 2003; 41:1-16.
3. Hemphill A. The host-parasite relationship in neosporosis. Adv Parasitol 1999; 43:47-104.
4. Barr BC, Rowe JD, Sverlow KW, BonDurant RH, Ardans AA, Oliver MN, Conrad PA. Experimental reproduction of bovine fetal Neospora infection and death with a bovine Neospora isolate. J Vet Diagn Invest 1994; 6:207-15.
5. Dubey JP, Lindsay DS. Gerbils (Meriones unguiculatus) are highly susceptible to oral infection with Neospora caninum oocysts. Parasitol Res 2000; 86:165-8.
6. Lindsay DS, Dubey JP. Neospora caninum (Protozoa: apicomplexa) infections in mice. J Parasitol 1989; 75:772-9.
7. Lindsay DS, Lenz SD, Cole RA, Dubey JP, Blagburn BL. Mouse model for central nervous system Neospora caninum infections. J Parasitol 1995; 81:313-5.
8. Trees AJ, Davison HC, Innes EA, Wastling JM. Towards evaluating the economic impact of bovine neosporosis. Int J Parasitol 1999; 29:1195-200.
9. Baszler TV, Long MT, McElwain TF, Mathison BA. Interferon-γ and interleukin-12 mediate protection to acute Neospora caninum infection in BALB/c mice. Int J Parasitol 1999; 29:1635-46.
10. Eperon S, Bronnimann K, Hemphill A, Gottstein B. Susceptibility of B-cell deficient C57BL/6 (microMT) mice to Neospora caninum infection. Parasite Immunol 1999; 21:225-36.
11. Khan IA, Schwartzman JD, Fonseka S, Kasper LH. Neospora caninum: role for immune cytokines in host immunity. Exp Parasitol 1997; 85:24-34.
12. Long MT, Baszler TV. Neutralization of maternal IL-4 modulates congenital protozoal transmission: comparison of innate versus acquired immune responses. J Immunol 2000; 164:4768-74.
13. Long MT, Baszler TV, Mathison BA. Comparison of intracerebral parasite load, lesion development, and systemic cytokines in mouse strains infected with Neospora caninum. J Parasitol 1998; 84:316-20.
14. Nishikawa Y, Inoue N, Makala L, Nagasawa H. A role for balance of interferon-gamma and interleukin-4 production in protective immunity against Neospora caninum infection. Vet Parasitol 2003; 116:175-84.
15. Nishikawa Y, Tragoolpua K, Inoue N, Makala L, Nagasawa H, Otsuka H, Mikami T. In the absence of endogenous gamma interferon, mice acutely infected with Neospora caninum succumb to a lethal immune response characterized by inactivation of peritoneal macrophages. Clin Diagn Lab Immunol 2001; 8:811-6.
16. Ritter DM, Kerlin R, Sibert G, Brake D. Immune factors influencing the course of infection with Neospora caninum in the murine host. J Parasitol 2002; 88:271-80.
17. Tanaka T, Hamada T, Inoue N, Nagasawa H, Fujisaki K, Suzuki N, Mikami T. The role of CD4 (+) or CD8 (+) T cells in the protective immune response of BALB/c mice to Neospora caninum infection. Vet Parasitol 2000; 90:183-91.
18. + cytotoxic T lymphocytes. Infect Immun 2003; 71:3272-9.
19. Baszler TV, McElwain TF, Mathison BA. Immunization of BALB/c mice with killed Neospora caninum tachyzoite antigen induces a type 2 immune response and exacerbates encephalitis and neurological disease. Clin Diagn Lab Immunol 2000; 7: 893-8.
20. Kang H, Remington JS, Suzuki Y. Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-gamma, TNF-alpha, and inducible nitric oxide synthase. J Immunol 2000; 164:2629-34.
21. Sayles PC, Gibson GW, Johnson LL. B cells are essential for vaccination-induced resistance to virulent Toxoplasma gondii. Infect Immun 2000; 68:1026-33.
22. Minoprio P. Parasite polyclonal activators: new targets for vaccination approaches? Int J Parasitol 2001; 31:588-91.
23. Hsu SM, Raine L, Fanger H. The use of antividin antibody and avidin-biotin-peroxidase complex in immunoperoxidase techniques. Am J Clin Pathol 1981; 75:816-21.
24. Lindsay DS, Dubey JP. Immunohistochemical diagnosis of Neospora caninum in tissue sections. Am J Vet Res 1989; 50: 1981-3.
25. Czerkinsky CC, Nilsson LA, Nygren H, Ouchterlony O, Tarkowski A. A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J Immunol Meth 1983; 65:109-21.
26. Reina-San-Martin B, Cosson A, Minoprio P. Lymphocyte polyclonal activation: a pitfall for vaccine design against infectious agents. Parasitol Today 2000; 16:62-7.
27. Dubey JP, Jenkins MC, Thayer DW, Kwok OC, Shen SK. Killing of Toxoplasma gondii oocysts by irradiation and protective immunity induced by vaccination with irradiated oocysts. J Parasitol 1996; 82:724-7.
28. Hiramoto RM, Galisteo AJ, do Nascimento N, de Andrade HF Jr. 200 Gy sterilised Toxoplasma gondii tachyzoites maintain metabolic functions and mammalian cell invasion, eliciting cellular immunity and cytokine response similar to natural infection in mice. Vaccine 2002; 20:2072-81.
29. Colle JH, Truffa-Bachi P, Chedid L, Modabber F. Lack of general immunosuppression during visceral Leishmania tropica infection in BALB/c mice: augmented antibody response to thymus-independent antigens and polyclonal activation. J Immunol 1983; 131:1492-5.
30. Cordeiro-Da-Silva A, Borges MC, Guilvard E, Ouaissi A. Dual role of the Leishmania major ribosomal protein S3a homologue in regulation of T- and B-cell activation. Infect Immun 2001; 69:6588-96.
31. + T cells in experimental leishmaniasis. Infect Immun 1988; 56:2120-4.
32. Klinman DM. Cross-reactivity of IgM-secreting B cells from normal BALB/c mice. J Immunol 1992; 149:3569-73.
33. Vilanova M, Tavares D, Ferreira P, Oliveira L, Nóbrega A, Appelberg R, Arala-Chaves M. Role of monocytes in the up-regulation of the early activation marker CD69 on B and T murine lymphocytes induced by microbial mitogens. Scand J Immunol 1996; 43:155-63.
34. Lima M, Portnoi D, Bandeira A, Arala-Chaves M. Peripheral lymphoid hyperplasia and central lymphoid depletion in mice treated with a bacterial B-cell mitogen (F3′EP-Si/p90). Scand J Immunol 1993; 37:605-14.
35. Sundblad A, Coutinho A. B-lineage cell deficits in bone marrow of lpr/lpr mice. Int Immunol 1996; 8:247-54.
36. Sedger LM, Hou S, Osvath SR, Glaccum MB, Peschon JJ, van Rooijen N, Hyland L. Bone marrow B cell apoptosis during in vivo influenza virus infection requires TNF-alpha and lymphotoxin-alpha. J Immunol 2002; 169:6193-201.
37. Shibahara T, Kokuho T, Eto M, Haritani M, Hamaoka T, Shimura K, Nakamura K, Yokomizo Y, Yamane I. Pathological and immunological findings of athymic nude and congenic wild type BALB/c mice experimentally infected with Neospora caninum. Vet Pathol 1999; 36:321-7.
38. Bretscher PA, Wei G, Menon JN, Bielefeldt-Ohmann H. Establishment of stable, cell-mediated immunity that makes 'susceptible' mice resistant to Leishmania major. Science 1992; 257:539-42.
39. + T helper cell phenotype development in a T cell receptor-β-transgenic model. J Exp Med 1995; 182:1579-84.
40. Parish CR. The relationship between humoral and cell-mediated immunity. Transplant Rev 1972; 13:35-66.
41. Borriello F, Sethna MP, Boyd SD et al. B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 1997; 6:303-13.
42. Butcher EC, Rouse RV, Coffman RL, Nottenburg CN, Hardy RR, Weissman IL. Surface phenotype of Peyer's patch germinal center cells: implications for the role of germinal centers in B cell differentiation. J Immunol 1982; 129:2698-707.
43. Kosco-Vilbois MH, Gray D, Scheidegger D, Julius M. Follicular dendritic cells help resting B cells to become effective antigen-presenting cells, induction of B7/BB1 and upregulation of major histocompatibility complex class II molecules. J Exp Med 1993; 178:2055-66.
44. Lunden A, Wright S, Allen JE, Buxton D. Immunisation of mice against neosporosis. Int J Parasitol 2002; 32:867-76.
45. Cannas A, Naguleswaran A, Muller N, Gottstein B, Hemphill A. Reduced cerebral infection of Neospora caninum-infected mice after vaccination with recombinant microneme protein NcMIC3 and ribi adjuvant. J Parasitol 2003; 89:44-50.
46. Nishikawa Y, Xuan X, Nagasawa H, Igarashi I, Fujisaki K, Otsuka H, Mikami T. Prevention of vertical transmission of Neospora caninum in BALB/C mice by recombinant vaccinia virus carrying Ncsrs2 gene. Vaccine 2001; 19:1710-6.
47. Miyahira Y, Katae M, Kobayashi S, Takeuchi T, Fukuchi Y, Abe R, Okumura K, Yagita H, Aoki T. Critical contribution of CD28-CD80/CD86 costimulatory pathway to protection from Trypanosoma cruzi infection. Infect Immun 2003; 71: 3131-7.
48. Chen M, Mun HS, Piao LX et al. Induction of protective immunity by primed B-1 cells in Toxoplasma gondii-infected B cell-deficient mice. Microbiol Immunol 2003; 47:997-1003.
49. Yoder BJ, Goodrum KJ. Plasmodium chabaudi chabaudi B-1 cell expansion correlates with semiresistance in BALB/Cj mice. Exp Parasitol 2001; 98:71-82.
50. Casadevall A. Antibody immunity and invasive fungal infections. Infect Immun 1995; 63:4211-8.
51. Mahalingam S, Lidbury BA. Antibody-dependent enhancement of infection: bacteria do it too. Trends Immunol 2003; 24: 465-7.
52. Suhrbier A, La Linn M. Suppression of antiviral responses by antibody-dependent enhancement of macrophage infection. Trends Immunol 2003; 24:165-8.
53. Williams ME, Caspar P, Oswald I, Sharma HK, Pankewycz O, Sher A, James SL. Vaccination routes that fail to elicit protective immunity against Schistosoma mansoni induce the production of TGF-beta which down-regulates macrophage antiparasitic activity. J Immunol 1995; 154:4693-700.