Reactive Nitrogen Intermediates production by macrophages of Mycobacterium bovis-infected goats and supplemented with dyhidroxyvitamin d3 in vivo

American Journal of Animal and Veterinary Sciences

Volumn 4, Issue 1, 2009, Pages 6-13

  Martinez Romero, Aurora ^a   Ortega Sanchez, Jose Luis ^b   Hernandez Salgado, Jose Ramon ^b   Mendoza Ramos, Margarita Yolanda ^c   Rodriguez Martinez, Rafael ^c   Cervantes Flores, Maribel ^a   Lopez Perez, Joel ^e   Urtiz Estrada, Norma ^a   Arenas Vargas, Miguel ^d   Villegas Viscaino, Raul ^c  

^a UNIVERSIDAD JUÁREZ DEL ESTADO DE DURANGO   (Mexico)

^b Regional Unit University of Arid Zones   (Mexico)

^c UNIVERSIDAD AUTÓNOMA AGRARIA ANTONIO NARRO   (Mexico)

^d DEPARTAMENTO DE SISTEMAS BIOLÓGICOS   (Mexico)

^e Center of Innovation and Educational Development   (Mexico)

Author keywords

1,25 dihydroxyvitamin D3; Goats; M. bovis BCG vaccine; Nitrates; Nitrites

Indexed keywords

ANIMALIA; BOS; CAPRA HIRCUS; MYCOBACTERIUM BOVIS; MYCOBACTERIUM BOVIS BCG;

EID: 63849227356     PISSN: 15574555     EISSN: 15574563     Source Type: Journal    
DOI: 10.3844/ajavsp.2009.6.13     Document Type: Article

References (43)

1. Harth, G. and M.A. Horwitz, 2003. Inhibition of mycobacterium tuberculosis glutamine synthetase as a novel antibiotic strategy against tuberculosis: Demonstration of efficacy in vivo. Infect. Immunol., 71: 456-464. DOI: 10.1128/IAI.71.1.456-464.2003
2. Tazi, L., J. El Baghdadi, S. Lesjean, C. Locht, P. Supply and M. Tibayrenc et al., 2004. Genetic diversity and population structure of mycobacterium tuberculosis in Casablanca, a Moroccan city with high incidence of tuberculosis. J. Clin. Microbiol., 42: 461-466. DOI: 10.1128/JCM.42.1.461-466.2004
3. Giordano, T.P., H. Soini, L.D. Teeter, G.J. Adams, J.M. Musser and E.A. Graviss, 2004. Relating the size of molecularly defined clusters of tuberculosis to the duration of symptoms. Clin. Infect. Dis., 38: 10-16. DOI: 10.1086/380454
4. Choi, H.S., P.R. Rai, H.W. Chu, C. Cool and E.D. Chan, 2002. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am. J. Respir. Crit. Care Med., 166: 178-186. http://ajrccm.atsjournals.org/cgi/content/abstract/166/2/178
5. Firmani, M.A. and L.W. Riley, 2002. Reactive nitrogen intermediates have a bacteriostatic effect on mycobacterium tuberculosis in vitro. J. Clin. Microbiol., 40: 3162-3166. DOI: 10.1128/JCM.40.9.3162-3166.2002
6. MacMicking, J.D., R.J. North, R. LaCourse, J.S. Mudgett, S.K. Shah and C.F. Nathan, 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA., 94: 5243-5248. http://www.pnas.org/content/94/10/5243.abstract
7. Morris, K.R., R.D. Lutz, H.S. Choi, T. Kamitani, K. Chmura and E.D. Chan, 2003. Role of the NF-kappaB signaling pathway and kappaB cis-regulatory elements on the IRF-1 and iNOS promoter regions in mycobacterial lipoarabinomannan induction of nitric oxide. Infect. Immunol., 71: 1442-1452. DOI: 10.1128/IAI.71.3.1442-1452.2003
8. Chan, E.D., J. Chan and N.W. Schluger, 2001. What is the role of nitric oxide in murine and human host defense against tuberculosis?Current knowledge. Am. J. Respir. Cell. Mol. Biol., 25: 606-612. http://ajrcmb.atsjournals.org/cgi/content/abstract/25/5/606
9. Long, R., R. Jones, J. Talbot, I. Mayers, J. Barrie and M. Hoskinson et al., 2005. Inhaled nitric oxide treatment of patients with pulmonary tuberculosis evidenced by positive sputum smears. Antimicrob. Agents Chemother., 49:1209-1212. DOI: 10.1128/AAC.49.3.1209-1212.2005
10. Jung, Y.J., L. Ryan, R. LaCourse and R.J. North, 2003. Increased interleukin-10 expression is not responsible for failure of T helper 1 immunity to resolve airborne mycobacterium tuberculosis infection in mice. Immunology, 109: 295-299. http://www.ncbi.nlm.nih.gov/pubmed/12757625
11. Schon, T., R. Hernandez-Pando, J. Baquera-Heredia, Y. Negesse, L.E. Becerril-Villanueva and J.C. Eon-Contreras et al., 2004. Nitrotyrosine localization to dermal nerves in borderline leprosy. Br. J. Dermatol., 150: 570-574. http://cat.inist.fr/?aModele=afficheN&cpsidt=15587043
12. Waters, W.R., M.V. Palmer, D.L. Whipple, M.P. Carlson and B.J. Nonnecke, 2003. Diagnostic implications of antigen-induced gamma interferon, nitric oxide and tumor necrosis factor alpha production by peripheral blood mononuclear cells from mycobacterium bovis-infected cattle. Clin. Diagn. Lab. Immunol., 10: 960-966. DOI: 10.1128/CDLI.10.5.960-966.2003
13. Rook, G.A., 1988. The role of vitamin D in tuberculosis. Am. Rev. Respir. Dis., 138: 768-770. http://www.ncbi.nlm.nih.gov/pubmed/2849343
14. Rockett, K.A., R. Brookes, I. Udalova, V. Vidal, A.V. Hill and D. Kwiatkowski, 1998. 1,25-Dihydroxyvitamin D3 induces nitric oxide synthase and suppresses growth of mycobacterium tuberculosis in a human macrophage-like cell line. Infect. Immunol., 11: 5314-5321. http://iai.asm.org/cgi/content/abstract/66/11/5314
15. Koeffler, H.P., H. Reichel, J.E. Bishop and A.W. Norman, 1985. Gamma-interferon stimulates production of 1,25-dihydroxyvitamin D3 by normal human macrophages. Biochem. Biophys. Res. Commun., 127: 596-603. http://www.ncbi.nlm.nih.gov/pubmed/3919734
16. Rook, G.A., J. Steele, L. Fraher, S. Barker, R. Karmali and J. O'Riordan et al., 1986. Vitamin D3, gamma interferon and control of proliferation of mycobacterium tuberculosis by human monocytes. Immunology, 57: 159-163. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1453883
17. Waters, W.R., B.J. Nonnecke, M.V. Palmer, S. Robbe-Austermann, J.P. Bannantine and J.R. Stabel et al., 2004. Use of recombinant ESAT-6: CFP-10 fusion protein for differentiation of infections of cattle by mycobacterium bovis and by M. avium subsp avium and M. avium subsp paratuberculosis. Clin. Diagn. Lab. Immunol., 11: 729-735. DOI: 10.1128/CDLI.11.4.729-735.2004
18. Waters, W.R., M.V. Palmer, B.J. Nonnecke, D.L. Whipple and R.L. Horst, 2004. mycobacterium bovis infection of vitamin D-deficient NOS2-/-mice. Microb. Pathog., 36: 11-17. DOI: 10.1016/j.micpath.2003.08.008
19. Buddle, B.M., D.N. Wedlock, N.A. Parlane, L.A. Corner, G.W. De Lisle and M.A. Skinner, 2003. Revaccination of neonatal calves with mycobacterium bovis BCG reduces the level of protection against bovine tuberculosis induced by a single vaccination. Infect. Immunol., 71: 6411-6419. DOI: 10.1128/IAI.71.11.6411-6419.2003
20. Shi, L., Y.J. Jung, S. Tyagi, M.L. Gennaro and R.J. North, 2003. Expression of Th1-mediated immunity in mouse lungs induces a mycobacterium tuberculosis transcription pattern characteristic of nonreplicating persistence. Proc. Natl. Acad. Sci. USA., 100: 241-246. DOI: 10.1073/pnas.0136863100
21. Weatherby, K.E., B.S. Zwilling and W.P. Lafuse, 2003. Resistance of macrophages to mycobacterium avium is induced by alpha2-adrenergic stimulation. Infect. Immunol., 71: 22-29. DOI: 10.1128/IAI.71.1.22-29.2003
22. Bafica, A., C.A. Scanga, C. Serhan, F. Machado, S. White and A. Sher et al., 2005. Host control of mycobacterium tuberculosis is regulated by 5-lipoxygenase-dependent lipoxin production. J. Clin. Invest., 115: 1601-1606. DOI: 10.1172/JCI23949
23. Hibbs, Jr. J.B., 1991. Synthesis of nitric oxide from L-arginine: A recently discovered pathway induced by cytokines with antitumour and antimicrobial activity. Res. Immunol., 142: 565-569. http://cat.inist.fr/?aModele=afficheN&cpsidt=5083709
24. Adams, L.B., S.G. Franzblau, Z. Vavrin, J.B. Hibbs, Jr. and J.L. Krahenbuhl, 1991. L-arginine-dependent macrophage effector functions inhibit metabolic activity of mycobacterium leprae. J. Immunol., 147: 1642-1646. http://www.jimmunol.org/cgi/content/abstract/147/5/1642
25. Kroncke, K.D., K. Fehsel and V. Kolb-Bachofen, 1998. Inducible nitric oxide synthase in human diseases. Clin. Exp. Immunol., 113: 147-156. DOI: 10.1046/j.1365-2249.1998.00648.x
26. Brown, N., M. Jacobs, S.K. Parida, T. Botha, A. Santos and L. Fick et al., 2005. Reduced local growth and spread but preserved pathogenicity of a deltapurC mycobacterium tuberculosis auxotrophic mutant in gamma interferon receptor-deficient mice after aerosol infection. Infect. Immun., 73: 666-670. http://www.ncbi.nlm.nih.gov/pubmed/15618214
27. Rhee, K.Y., H. Erdjument-Bromage, P. Tempst and C.F. Nathan, 2005. S-nitroso proteome of mycobacterium tuberculosis: Enzymes of intermediary metabolism and antioxidant defense. Proc. Natl. Acad. Sci. USA., 102: 467-472. DOI: 10.1073/pnas.0406133102
28. Flynn, J.L. and J. Chan, 2003. Immune evasion by Mycobacterium tuberculosis: Living with the enemy. Curr. Opin. Immunol., 15: 450-455. DOI: 10.1016/S0952-7915(03)00075-X
29. Waters, W.R., B.J. Nonnecke, T.E. Rahner, M.V. Palmer, D.L. Whipple and R.L. Horst, 2001. Modulation of mycobacterium bovis-specific responses of bovine peripheral blood mononuclear cells by 1, 25-dihydroxyvitamin D(3). Clin. Diagn. Lab. Immunol., 8: 1204-1212. DOI: 10.1128/CDLI.8.6.1204-1212.2001
30. Huttunen, K., J. Pelkonen, K.F. Nielsen, U. Nuutinen, J. Jussila and M.R. Hirvonen, 2004. Synergistic interaction in simultaneous exposure to streptomyces californicus and stachybotrys chartarum. Environ. Health Perspect., 112: 659-665. http://www.ehponline.org/members/2004/6701/6701.html
31. Gretzer, C., P. Thomsen, 2000. Secretion of IL-1 and H2O2 by human mononuclear cells in vitro. Biomaterials, 21: 1047-1055. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=10768757
32. Rhoades, E.R., I.M. Orme, 1997. Susceptibility of a panel of virulent strains of mycobacterium tuberculosis to reactive nitrogen intermediates. Infect. Immunol., 65: 1189-1195. http://iai.asm.org/cgi/content/abstract/65/4/1189
33. Steel, R.G.D. and J.H. Torrie, 1980. Principles and Procedures of Statistics: A Biometrics Approach. 2nd Edn., McGraw-Hill, New York, pp: 633.
34. Cantorna, M.T., C.E. Hayes and H.F. DeLuca, 1996. 1,25-Dihydroxyvitamin D3 reversibly blocks the progression of relapsing encephalomyelitis, a model of multiple sclerosis. Proc. Natl. Acad. Sci. USA., 93: 7861-7864. http://www.pnas.org/content/93/15/7861.abstract
35. Provvedini, D.M., C.D. Tsoukas, L.J. Deftos and S.C. Manolagas, 1983. 1, 25-dihydroxyvitamin D3 receptors in human leukocytes. Science, 221: 1181-1183. DOI: 10.1126/science.6310748
36. Brennan, A., D.R. Katz, J.D. Nunn, S. Barker, M. Hewison and L.J. Fraher et al., 1987. Dendritic cells from human tissues express receptors for the immunoregulatory vitamin D3 metabolite, dihydroxycholecalciferol. Immunology, 61: 457-461. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1453440
37. Topilski, I., L. Flaishon, Y. Naveh, A. Harmelin, Y. Levo and I. Shachar, 2004. The anti-inflammatory effects of 1,25-dihydroxyvitamin D3 on Th2 cells in vivo are due in part to the control of integrin-mediated T lymphocyte homing. Eur. J. Immunol., 34: 1068-1076. DOI: 10.1002/eji.200324532
38. Wittke, A., V. Weaver, B.D. Mahon, A. August and M.T. Cantorna, 2004. Vitamin D receptor-deficient mice fail to develop experimental allergic asthma. J. Immunol., 173: 3432-3436. http://www.jimmunol.org/cgi/content/abstract/173/5/3432
39. Firmani, M.A. and L.W. Riley, 2002. mycobacterium tuberculosis CDC1551 is resistant to reactive nitrogen and oxygen intermediates in vitro. Infect. Immunol., 70: 3965-3968. DOI: 10.1128/IAI.70.7.3965-3968.2002
40. Flynn, J.L. and J. Chan, 2001. Tuberculosis: Latency and reactivation. Infect. Immun., 69: 4195-201. DOI: 10.1128/IAI.69.7.4195-4201.2001
41. Jagannath, C., J.K. Actor and Hunter R.L. Jr., 1998. Induction of nitric oxide in human monocytes and monocyte cell lines by mycobacterium tuberculosis. Nitric Oxide, 2: 174-186. DOI: 10.1006/niox.1998.9999
42. Stuehr, D.J., C.C. Wei, Z. Wang and R. Hille, 2005. Exploring the redox reactions between heme and tetrahydrobiopterin in the nitric oxide synthases. Dalton Trans., 21: 3427-3435. DOI: 10.1039/b506355h
43. Roy, S., S. Sharma, M. Sharma, R. Aggarwal and M. Bose, 2004. Induction of nitric oxide release from the human alveolar epithelial cell line A549: An in vitro correlate of innate immune response to mycobacterium tuberculosis. Immunology, 112: 471-480. http://www.ncbi.nlm.nih.gov/pubmed/15196216