Analysis of the immune response to Neospora caninum in a model of intragastric infection in mice

Parasite Immunology

Volumn 29, Issue 1, 2007, Pages 23-36

  Teixeira, L ^a   Botelho, A S ^a   Batista, A R ^a   Meireles, C S ^b   Ribeiro, A ^a   Domingues, H S ^b   Correia Da Costa, J M ^a,c   Castro, A G ^b   Faustino, A M R ^a   Vilanova, M ^a,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

^c NATIONAL INSTITUTE OF HEALTH   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

Author keywords

Foxp3; IFN ; IL 10; Intragastric infection; Neospora caninum

Indexed keywords

DNA; GAMMA INTERFERON; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; INTERLEUKIN 10; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL INFECTION; FEMALE; FLOW CYTOMETRY; GASTROINTESTINAL INFECTION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; NEOSPORA CANINUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE EXAMINATION; PEYER PATCH; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; STOMACH;

NEOSPORA CANINUM;

EID: 33845584829     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2006.00911.x     Document Type: Article

References (64)

1. Bjerkås I, Mohn SF & Presthus J. Unidentified cyst-forming sporozoan causing encephalomyelitis and myositis in dogs. Z Parasitenkd 1984; 70: 271-274.
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. Trees AJ, Davison HC, Innes EA & Wastling JM. Towards evaluating the economic impact of bovine neosporosis. Int J Parasitol 1999; 29: 1195-1200.
5. Davison HC, Otter A & Trees AJ. Estimation of vertical and horizontal transmission parameters of Neospora caninum infections in dairy cattle. Int J Parasitol 1999; 29: 1683-1689.
6. French NP, Clancy D, Davison HC & Tree AJ. Mathematical models of Neospora caninum infection in dairy cattle: transmission and options for control. Int J Parasitol 1999; 29: 1691-1704.
7. Marez TD, Liddell S, Dubey JP, Jenkins MC & Gasbarre L. Oral infection of calves with Neospora caninum oocysts from dogs: humoral and cellular immune responses. Int J Parasitol 1999; 29: 1647-1657.
8. McAlister MM, Dubey JP, Lindsay DS, Jolley WR, Wills RAW & McGuire AM. Dogs are the definitive hosts of. Neospora caninum. Int J Parasitol 1998; 28: 1473-1478.
9. Barr BC, Rowe JD, Sverlow KW et al. Experimental reproduction of bovine fetal Neospora infection and death with a bovine Neospora isolate. J Vet Diagn Invest 1994; 6: 207-215.
10. Dubey JP & Lindsay DS. Gerbils (Meriones unguiculatus) are highly susceptible to oral infection with Neospora caninum oocysts. Parasitol Res 2000; 86: 165-168.
11. Lindsay DS & Dubey JP. Neospora caninum (Protozoa: Apicomplexa) infections in mice. J Parasitol 1989; 75: 772-779.
12. Lindsay DS, Lenz SD, Cole RA, Dubey JP & Blagburn BL. Mouse model for central nervous system Neospora caninum infections. J Parasitol 1995; 81: 313-315.
13. 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: 1635-1646.
14. Eperon S, Bronnimann K, Hemphill A & Gottstein B. Susceptibility of B-cell deficient C57BL/6 (μMT) mice to Neospora caninum infection. Parasite Immunol 1999; 21: 225-236.
15. Khan IA, Schwartzman JD, Fonseka S & Kasper LH. Neospora caninum: role for immune cytokines in host immunity. Exp Parasitol 1997; 85: 24-34.
16. Long MT & Baszler TV. Neutralization of maternal IL-4 modulates congenital protozoal transmission: comparison of innate versus acquired immune responses. J Immunol 2000; 164: 4768-4774.
17. 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: 316-320.
18. Nishikawa Y, Inoue N, Makala L & Nagasawa H. A role for balance of interferon-γ and interleukin-4 production in protective immunity against Neospora caninum infection. Vet Parasitol 2003; 116: 175-184.
19. Nishikawa Y, Tragoolpua K, Inoue N et al. 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: 811-816.
20. Tanaka T, Hamada T, Inoue N et al. 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: 183-191.
21. Quinn HE, Miller CM & Ellis JT. The cell-mediated immune response to Neospora caninum during pregnancy in the mouse is associated with a bias towards production of interleukin-4. Int J Parasitol 2004; 34: 723-732.
22. Lindsay D & Dubey JP. Infections in mice with tachyzoites and bradyzoites of Neospora caninum (Protozoa: Apicomplexa). J Parasitol 1990; 76: 410-413.
23. 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: 893-898.
24. Ramamoorthy S, Sriranganathan N & Lindsay DS. Gerbil model of acute neosporosis. Vet Parasitol 2005; 127: 111-114.
25. O'Handley R, Liddell S, Parker C, Jenkins MC & Dubey JP. Experimental infection of sheep with Neospora caninum oocysts. J Parasitol 2002; 88: 1120-1123.
26. Dubey JP & Lindsay DS. Fatal Neospora caninum infection in kittens. J Parasitol 1989; 75: 148-151.
27. Hemphill A. Subcellular localization and functional characterization of Nc-p43, a major Neospora caninum tachyzoite surface protein. Infect Immun 1996; 64: 4279-4287.
28. Czuprynski CJ, Faith NG & Steinberg H. Ability of the Listeria monocytogenes strain Scott A to cause systemic infection in mice infected by the intragastric route. Appl Environ Microbiol 2002; 68: 2893-2900.
29. Grangette C, Muller-Alouf H, Geoffroy M, Goudercourt D, Turneer M & Mercenier A. Protection against tetanus toxin after intragastric administration of two recombinant lactic acid bacteria: impact of strain viability and in vivo persistence. Vaccine 2002; 20: 3304-3309.
30. 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: 816-821.
31. Lindsay DS & Dubey JP. Immunohistochemical diagnosis of Neospora caninum in tissue sections. Am J Vet Res 1989; 50: 1981-1983.
32. Nishikawa Y, Inoue N, Xuan X et al. Protective efficacy of vaccination by recombinant vaccinia virus against Neospora caninum infection. Vaccine 2001; 19: 1381-1390.
33. Muller N, Vonlaufen N, Gianinazzi C, Leib SL & Hemphill A. Application of real-time fluorescent PCR for quantitative assessment of Neospora caninum infections in organotypic slice cultures of rat central nervous system tissue. J Clin Microbiol 2002; 40: 252-255.
34. Poltorak A, Merlin T, Nielsen PJ et al. A point mutation in the IL-12R beta 2 gene underlies the IL-12 unresponsiveness of Lps-defective C57BL/10ScCr mice. J Immunol 2001; 167: 2106-2111.
35. Botelho AS, Teixeira L, Correia da Costa JM, Faustino AM, Castro AG & Vilanova M. Neospora caninum: high susceptibility to the parasite in C57BL/10 ScCr mice. Exp Parasitol 2006; in press.
36. Gottstein B, Eperon S, Dai WJ, Cannas A, Hemphill A & Greif G. Efficacy of toltrazuril and ponazuril against experimental Neospora caninum infection in mice. Parasitol Res 2001; 87: 43-48.
37. Denkers EY. From cells to signaling cascades: manipulation of innate immunity by Toxoplasma gondii. FEMS Immunol Med Microbiol 2003; 39: 193-203.
38. Wilson ME, Jeronimo SM & Pearson RD. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog 2005; 38: 147-160.
39. Langhorne J, Albano FR, Hensmann M et al. Dendritic cells, pro-inflammatory responses, and antigen presentation in a rodent malaria infection. Immunol Rev 2004; 201: 35-47.
40. Finkelman FD, Katona IM, Mosmann TR & Coffman RL. IFN-γ regulates the isotypes of Ig secreted during in vivo humoral immune responses. J Immunol 1988; 140: 1022-1027.
41. Bergstedt-Lindqvist S, Moon HB, Persson U, Moller G, Heusser C & Severinson E. Interleukin 4 instructs uncommitted B lymphocytes to switch to IgG1 and IgE. Eur J Immunol 1988; 18: 1073-1077.
42. Mathers AR & Cuff CF. Role of interleukin-4 (IL-4) and IL-10 in serum immunoglobulin G antibody responses following mucosal or systemic reovirus infection. J Virol 2004; 78: 3352-3360.
43. + regulatory T cells in immunological tolerance to self and nonself. Nat Immunol 2005; 6: 345-352.
44. Poltorak A, He X, Smirnova I et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998; 282: 2085-2088.
45. Kropf P, Freudenberg MA, Modolell M et al. Toll-like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infect Immun 2004; 72: 1920-1928.
46. Kropf P, Freudenberg N, Kalis C et al. Infection of C57BL/10ScCr and C57BL/10ScNCr mice with Leishmania major reveals a role for Toll-like receptor 4 in the control of parasite replication. J Leukoc Biol 2004; 76: 48-57.
47. Oliveira AC, Peixoto JR, de Arruda LB et al. Expression of functional TLR4 confers proinflammatory responsiveness to Trypanosoma cruzi glycoinositolphospholipids and higher resistance to infection with T. cruzi. J Immunol 2004; 173: 5688-5696.
48. Ammann P, Waldvogel A, Breyer I, Esposito M, Müller N & Gottstein B. The role of B- and T-cell immunity in Toltrazuril-treated C5BL/6 WT, μMT and nude mice experimentally infected with Neospora caninum. Parasitol Res 2004; 93: 178-187.
49. Teixeira L, Marques A, Meireles CS et al. Characterization of the B-cell immune response elicited in BALB/c mice challenged with Neospora caninum tachyzoites. Immunology 2005; 116: 38-52.
50. Butcher EC, Rouse RV, Coffman RL, Nottenburg CN, Hardy RR & Weissman IL. Surface phenotype of Peyer's patches germinal center cells: implications for the role of germinal centers in B cell differentiation. J Immunol 1982; 129: 2698-2707.
51. Elias RM, Sardinha LR, Bastos KR et al. Role of CD28 in polyclonal and specific T and B cell responses required for protection against blood stage malaria. J Immunol 2005; 174: 790-799.
52. Villegas EN, Elloso MM, Reichmann G, Peach R & Hunter CA. Role of CD28 in the generation of effector and memory responses required for resistance to Toxoplasma gondii. J Immunol 1999; 163: 3344-3353.
53. Hunter CA, Ellis-Neyer L, Gabriel KE et al. The role of the CD28/B7 interaction in the regulation of NK cell responses during infection with Toxoplasma gondii. J Immunol 1997; 158: 2285-2293.
54. Issazadeh S, Navikas V, Schaub M, Sayegh M & Khoury S. Kinetics of expression of costimulatory molecules and their ligands in murine relapsing experimental autoimmune encephalomyelitis in vivo. J Immunol 1998; 161: 1104-1112.
55. Karandikar NJ, Vanderlugt CL, Eagar T, Tan L, Bluestone JA & Miller SD. Tissue-specific up-regulation of B7-1 expression and function during the course of murine relapsing experimental autoimmune encephalomyelitis. J Immunol 1998; 161: 192-199.
56. Hussain S & Delovitch TL. Dysregulated B7-1 and B7-2 expression on nonobese diabetic mouse B cells is associated with increased T cell costimulation and the development of insulitis. J Immunol 2005; 174: 680-687.
57. Sharpe AH & Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol 2002; 2: 116-126.
58. Bonenfant C, Dimier-Poisson I, Velge-Roussel F et al. Intranasal immunization with SAG1 and nontoxic mutant heat-labile enterotoxins protects mice against Toxoplasma gondii. Infect Immun 2001; 69: 1605-1612.
59. Neyer LE, Grunig G, Fort M, Remington JS, Rennick D & Hunter CA. Role of interleukin-10 in regulation of T-cell-dependent and T-cell-independent mechanisms of resistance to Toxoplasma gondii. Infect Immun 1997; 65: 1675-1682.
60. + T cells and accompanied by overproduction of IL-12, IFN-γ and TNF-α. J Immunol 1996; 157: 798-805.
61. + T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur J Immunol 2002; 32: 1282-1291.
62. + regulatory T cells control the severity of viral immunoinflammatory lesions. J Immunol 2004; 172: 4123-4132.
63. + regulatory T cells suppress differentiation and functions of Th1 and Th2 cells, Leishmania major infection, and colitis in mice. J Immunol 2003; 170: 394-399.
64. + regulatory T cells control Leishmania major persistence and immunity. Nature 2002; 420: 502-507.