Modulation of the bovine trophoblastic innate immune response by Brucella abortus

Infection and Immunity

Volumn 76, Issue 5, 2008, Pages 1897-1907

  Carvalho Neta, Alcina V ^a   Stynen, Ana P R ^a   Paixão, Tatiane A ^a   Miranda, Karina L ^a   Silva, Fabiana L ^a   Roux, Christelle M ^b   Tsolis, Renée M ^b   Everts, Robin E ^c   Lewin, Harris A ^c   Adams, L Garry ^d   Carvalho, Alex F ^e   Lage, Andrey P ^a   Santos, Renato L ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF CALIFORNIA   (United States)

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

^d TEXAS A AND M UNIVERSITY   (United States)

^e LUDWIG INSTITUTE FOR CANCER RESEARCH   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CHEMOKINE; CHEMOKINE; CXCL11 CHEMOKINE; CYTOKINE; GRANULOCYTE CHEMOTACTIC PROTEIN 2; INTERLEUKIN 8;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BRUCELLA ABORTUS; BRUCELLOSIS; CHORIOALLANTOIS; CONTROLLED STUDY; COW; EXPLANT; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE REPRESSION; IMMUNOMODULATION; IN VITRO STUDY; INNATE IMMUNITY; INOCULATION; MEDIATOR; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STATISTICAL SIGNIFICANCE; TROPHOBLAST; UNINDEXED SEQUENCE; UPREGULATION; ANIMAL; BIOSYNTHESIS; CATTLE; DNA MICROARRAY; DOWN REGULATION; FEMALE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOLOGY; PLACENTA; TIME;

ANIMALS; BRUCELLA ABORTUS; CATTLE; CYTOKINES; DOWN-REGULATION; FEMALE; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLACENTA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; TROPHOBLASTS; UP-REGULATION;

EID: 42949114964     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01554-07     Document Type: Article

References (52)

1. Ackermann, M. R., N. F. Cheville, and B. L. Deyoe. 1988. Bovine ileal dome lymphoepithelial cell: endocytosis and transport of Brucella abortus strain 19. Vet. Pathol. 25:28-35.
2. Anderson, T. D., V. P. Meador, and N. F. Cheville. 1986. Pathogenesis of placentitis in the goat inoculated with Brucella abortus. I. Gross and histologic lesions. Vet. Pathol. 23:219-226.
3. Anderson, T. D., V. P. Meador, and N. F. Cheville. 1986. Pathogenesis of placentitis in the goat inoculated with Brucella abortus. II. Ultrastructural studies. Vet. Pathol. 23:227-239.
4. Barqueiro-Calvo, E., E. Chaves-Olarte, D. S. Weiss, C. Guzmán-Verri, C. Chacon-Diaz, A. Rucavado, I. Moriyon, and E. Moreno. 2007. Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS ONE 7:e631.
5. Bazer, F. W., T. E. Spencer, and T. L. Ott. 1997. Interferon tau: a novel pregnancy recognition signal. Am. J. Reprod. Immunol. 37:412-420.
6. Black, R. A., S. R. Kronheim, M. Cantrell, M. C. Deeley, C. J. March, K. S. Prickett, J. Wignall, P. J. Conlon, D. Cosman, T. P. Hopp, and D. Y. Mochizuki. 1988. Generation of biologically active interleukin-18 by proteolytic cleavage of the inactive precursor. J. Biol. Chem. 263:9437-9944.
7. Campos, M. A., G. M. S. Rosinha, I. C. Almeida, X. S. Salgueiro, B. W. Jarvis, G. A Splitter, N. Qureshi, O. Bruna-Romero, R. T. Gazinelli, and S. C. Oliveira. 2004. Role of Toll-like receptor 4 in induction of cell-mediated immunity and resistance to Brucella abortus infection in mice. Infect. Immun. 72:176-186.
8. Crawford, R. P., J. D. Huber, and B. S. Adams. 1990. Epidemiology and surveillance, pp. 131-151. In K. Nielsen and J. R. Duncan, Animal brucellosis. CRC Press, Boca Raton, FL.
9. Detilleux, P. G., B. L. Deyoe, and N. F. Cheville. 1990. Entry and intracellular localization of Brucella spp. in vero cells: fluorescence and electron microscopy. Vet. Pathol. 27:317-328.
10. Detilleux, P. G., B. L. Deyoe, and N. F. Cheville. 1990. Penetration and intracellular growth of Brucella abortus in nonphagocytic cells in vitro. Infect. Immun. 58:2320-2328.
11. Duenas, A. I., A. Orduna, M. S. Crespo, and C. Garcia-Rodriguez. 2004. Interaction of endotoxins with Toll-like receptor 4 correlates with their endotoxic potential and may explain the proinflammatory effect of Brucella spp. LPS. Int. Immunol. 16:1467-1475.
12. Eckmann, L., M. F. Kagnoff, and J. Fierer. 1993. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect. Immun. 61:4569-4574.
13. Enright, F. M., J. V. Walker, G. Jeffers, and B. L. Deyoe. 1984. Cellular and humoral responses of Brucella abortus-infected bovine fetuses. Am. J. Vet. Res. 45:424-430.
14. Eskra, L., A. Mathison, and G. Splitter. 2003. Microarray analysis of mRNA levels from raw264.7 macrophages infected with Brucella abortus. Infect. Immun. 71:1125-1133.
15. Essenberg, R. C., R. Seshadri, K. Nelson, and I. Paulsen. 2002. Sugar metabolism by Brucellae. Vet. Microbiol. 90:249-261.
16. Evans, H. E., and W. O. Sack. 1973. Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Anat. Histol. Embryol. 2:11-15.
17. Giambartolomei, G. H., A. Zwerdling, J. Cassataro, L. Bruno, C. A. Fossati, and M. T. Philipp. 2004. Lipoproteins, not lipopolysaccharide, are the key mediators of the proinflammatory response elicited by heat-killed Brucella abortus. J. Immunol. 173:4635-4642.
18. Godstein, J., T. Hoffman, C. Frasch, E. F. Lizzio, P. R. Beining, D. Hochstein, Y. L. Lee, R. D. Angus, and B. Golding. 1992. Lipopolysaccharide (LPS) from Brucella abortus is less toxic than that from Escherichia coli, suggesting the possible use of B. abortus or LPS from B. abortus as carrier in vaccines. Infect. Immun. 60:1385-1389.
19. Gorham, S. L., F. M. Enright, T. G. Snider III, and E. D. Roberts. 1986. Morphologic lesions in Brucella abortus infected ovine fetuses. Vet. Pathol. 23:331-332.
20. Hehlgans, T., and K. Pfeffer. 2005. The intriguing biology of tumor necrosis factor/tumor necrosis factor receptor superfamily: players, rules and the games. Immunology 115:1-20.
21. Huang, L. Y., J. Aliberti, C. A. Leifer, D. M. Segal, A. Sher, D. T. Golenbock, and B. Golding. 2003. Heat killed Brucella abortus induces TNF and IL-12p40 by distinct MyD88-dependent pathways: TNF, unlike IL-12p40 secretion, is toll-like receptor 2 dependent. J. Immunol. 171:1441-1446.
22. Jubier-Maurin, V., R. A. Boigegrain, A. Cloeckaert, A. Gross, M. T. Alvarez-Martinez, A. Terraza, J. Liautard, S. Köhler, B. Rouot, J. Dornand, and J. P. Liautard. 2001. Major outer membrane protein Omp25 of Brucella suis is involved in inhibition of tumor necrosis factor alpha production during infection of human macrophages. Infect. Immun. 69:4823-4830.
23. Jung, H. C., L. Eckmann, S. K. Yang, A. Panja, J. Fierer, E. Morzycka-Wroblewska, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Investig. 95:55-65.
24. Ko, J., and G. A. Splitter. 2003. Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and humans. Clin. Microbiol. Rev. 16:65-78.
25. Kostura, M. J., M. J. Tocci, G. Limjuco, J. Chin, P. Cameron, A. G. Hillman, N. A. Chartrain, and J. A. Schmidt. 1989. Identification of a monocyte specific pre-interleukin 1β convertase activity. Proc. Natl. Acad. Sci. USA 86:5227-5231.
26. Lapaque, N., O. Takeuchi, F. Corrales, S. Akira, I. Moriyon, J. C. Howard, and J. P. Gorvel. 2006. Differential inductions of TNF-alpha and IGTP, IIGP by structurally diverse classic and non-classic lipopolysaccharides. Cell. Microbiol. 8:401-413.
27. -ΔΔCT method. Methods 25:402-408.
28. Loor, J. J., R. E. Everts, M. Bionaz, H. M. Dann, D. Morin, R. Oliveira, S. L. Rodriguez-Zas, J. K. Drackley, and H. A. Lewin. 2007. Nutrition-induced ketosis alters metabolic and signaling gene networks in liver of periparturient dairy cows. Physiol. Genomics 32:105-116.
29. Meador, V. P., and B. L. Deyoe. 1989. Intracellular localization of Brucella abortus in bovine placenta. Vet. Pathol. 26:513-515.
30. Medzhitov, Jr., R., and C. A. Janeway. 1997. Innate immunity: the virtues of a monoclonal system of recognition. Cell 91:295-298.
31. Paixão, T. A., F. P. Poester, A. V. Carvalho Neta, A. M. Borges, A. P. Lage, and R. L. Santos. 2007. NRAMP1 3′ untranslated region polymorphisms are not associated with natural resistance to Brucella abortus in cattle. Infect. Immun. 75:2493-2499.
32. Pizarro-Cerdá, J., E. Moreno, V. Sanguedolce, J. L. Mege, and J. P. Gorvel. 1998. Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect. Immun. 66:2387-2392.
33. Pizarro-Cerdá, J., S. Méresse, R. G. Parton, G. Van Der Goot, A. Sola-Landa, I. Lopez-Goni, E. Moreno, and J. P. Gorvel. 1998. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 66:5711-5724.
34. Poester, F. P., V. S. P. Gonçalves, T. A. Paixão, R. L. Santos, S. O. Olsen, G. G. Schurig, and A. P. Lage. 2006. Efficacy of strain RB51 vaccine in heifers against experimental brucellosis. Vaccine 24:5327-5334.
35. Raffatellu, M., R. L. Santos, D. Chessa, R. P. Wilson, S. Winter, C. L. Bevins, L. G. Adams, and A. J. Bäumler. 2007. The capsule encoding the viaB locus reduces interleukin-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect. Immun. 75:4342-4350.
36. Roux, C. M., H. G. Rolán, R. L. Santos, P. D. Beremand, T. L. Thomas, L. G. Adams, and R. M. Tsolis. 2007. Brucella requires a functional type IV secretion system to elicit innate immune responses in mice. Cell. Microbiol. 9:1851-1869.
37. Samartino, L. E., and F. M. Enright. 1992. Interaction of bovine chorioallantoic membrane explants with three strains of Brucella abortus. Am. J. Vet. Res. 53:359-363.
38. Samartino, L. E., and F. M. Enright. 1993. Pathogenesis of abortion of bovine brucellosis. Comp. Immunol. Microbiol. Infect. Dis. 16:95-101.
39. Samartino, L. E., and F. M. Enright. 1996. Brucella abortus differs in the multiplication within bovine chorioallantoic membrane explants from early and late gestation. Comp. Immunol. Microbiol. Infect. Dis. 19:55-63.
40. Santos, R. L., M. T. D. Peixoto, R. Serakides, G. M. Costa, and N. E. Martins. 1998. Detección de Brucella abortus (muestra B19) por el complejo inmunoenzimático avidina-biotina-peroxidasa en el testículo y en el epidídimo de bovinos inoculados experimentalmente. Arch. Reprod. Anim. 6:34-41.
41. Santos, R. L., S. Zhang, R. M. Tsolis, A. J. Baumler, and L. G. Adams. 2002. Morphologic and molecular characterization of Salmonella typhimurium in neonatal calves. Vet. Pathol. 39:200-215.
42. Smith, H., A. E. Williams, J. H. Pearce, J. Keppie, P. W. Harris-Smith, R. B. Futzgeorge, and K. Witt. 1962. Foetal erythritol: a cause of the localization of Brucella abortus in bovine contagious abortion. Nature 193:47-49.
43. Smith, H., J. Keppie, J. H. Pearce, R. Fuller, and A. E. Williams. 1961. The chemical basis of the virulence of Brucella abortus. I. Isolation of Brucella abortus from bovine foetal tissue. Br. J. Exp. Pathol. 42:631.
44. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll like receptors. Annu. Rev. Immunol. 21:335-376.
45. Tumurkhuu, G., N. Koide, K. Takahashi, F. Hassan, H. Islam, I. Mori, T. Yoshida, and T. Yokochi. 2006. Characterization of biological activities of Brucella melitensis lipopolysaccharide. Microbiol. Immunol. 50:421-427.
46. Ushizawa, K., C. B. Herath, K. Kaneyama, S. Shiojima, A. Hirasawa. T. Takahashi, K. Imai, K. Ochiai, T. Tokunaga, Y. Tsunoda, G. Tsujimoto, and K. Hashizume. 2004. cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period. Reprod. Biol. Endocrinol. 2:77.
47. Ushizawa, K., T. Takahashi, K. Kaneyama, T. Tokunaga, Y. Tsunoda, and K. Hashizume. 2005. Gene expression profiles of bovine trophoblastic cell line (BT-1) analysed by a custom cDNA microarray. J. Reprod. Dev. 51:211-220.
48. Ushizawa, K., T. Takahashi, M. Hosoe, H. Ishiwata, K. Kaneyama, K. Kizaki, and K. Hashizume. 2007. Global gene expression analysis and regulation of the principal genes expressed in bovine placenta in relation to transcription factor AP-2 family. Reprod. Biol. Endocrinol. 5:17.
49. Weiss, D. S., K. Takeda, S. Akira, A. Zychlinsky, and E. Moreno. 2005. MyD88, but not Toll-like receptors 4 and 2, is required for efficient clearance of Brucella abortus. Infect. Immun. 73:5137-5143.
50. Whiteside, E. J., M. Kan, M. M. Jackson, J. G. Thompson, C. Mcnaughton, A. C. Herington, and M. B. Harvey. 2001. Urokinase-type plasminogen activator (uPA) and matrix metalloproteinase-9 (MMP-9) expression and activity during early embryo development in the cow. Anat. Embryol. 204:477-483.
51. Young, E. J. 1995. An overview of human brucellosis. Clin. Infect. Dis. 21:283-289.
52. Zhan, Y., Z. Liu, and C. Cheers. 1996. Tumor necrosis factor alpha and interleukin 12 contribute to resistance to the intracellular bacterium Brucella abortus by different mechanisms. Infect. Immun. 64:2782-2786.