Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase

Nature

Volumn 460, Issue 7251, 2009, Pages 98-102

  Agarwal, Nisheeth ^a   Lamichhane, Gyanu ^a   Gupta, Radhika ^a   Nolan, Scott ^a   Bishai, William R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

BACTERIUM; CYTOLOGY; ENZYME ACTIVITY; FUNGAL DISEASE; PROTEIN; SIGNALING; STERILIZATION; SURVIVAL; TUBERCULOSIS; VIRULENCE;

ADENYLATE CYCLASE GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; EMBRYO; GENE; HOST CELL; IMMUNOPATHOLOGY; INTOXICATION; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL;

ADENYLATE CYCLASE; ANIMALS; CELL LINE; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSOL; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORYLATION; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 67650074482     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08123     Document Type: Article

References (34)

1. Dye, C. Global epidemiology of tuberculosis. Lancet 367, 938-940 (2006).
2. Wright, A. et al. Epidemiology of antituberculosis drug resistance 2002-07: an updated analysis of the Global Project on Anti-Tuberculosis Drug Resistance Surveillance. Lancet doi:10.1016/S0140-6736(09)60331-7 (in the press).
3. Flannagan, R. S., Cosio, G. &Grinstein, S. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nature Rev. Microbiol. 7, 355-366 (2009).
4. Dannenberg, A. M. Jr. Immunopathogenesis of pulmonary tuberculosis. Hosp. Pract. (Off. Ed.) 28, 51-58 (1993).
5. Bai, G., Schaak, D. D. & McDonough, K. A. cAMP levels within Mycobacterium tuberculosis and Mycobacterium bovis BCG increase upon infection of macrophages. FEMS Immunol. Med. Microbiol. 55, 68-73 (2009).
6. Roach, S. K., Lee, S. B. & Schorey, J. S. Differential activation of the transcription factor cyclic AMP response element binding protein (CREB) in macrophages following infection with pathogenic and nonpathogenic my cobacteria and role for CREB in tumor necrosis factor a production. Infect. Immun. 73, 514-522 (2005).
7. Lowrie, D. B., Jackett, P. S. & Ratcliffe, N. A. Mycobacterium microti may protect itself from intracellular destruction by releasing cyclic AMP into phagosomes. Nature 254, 600-602 (1975).
8. Baker, D. A. &Kelly, J. M. Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol. Microbiol. 52, 1229-1242 (2004).
9. Sands, W. A. & Palmer, T. M. Regulating gene transcription in response to cyclic AMP elevation. Cell. Signal. 20, 460-466 (2008).
10. Serezani, C. H., Ballinger, M. N., Aronoff, D. M. & Peters-Golden, M. Cyclic AMP: master regulator of innate immune cell function. Am. J. Respir. Cell Mol. Biol. 39, 27-132 (2008).
11. Johannessen, M. & Moens, U. Multisite phosphorylation of the cAMP response element-binding protein (CREB) by a diversity of protein kinases. Front. Biosci. 12, 814-1832(2007).
12. Servillo, G., Della Fazia, M. A. & Sassone-Corsi, P. Coupling cAMP signaling to transcription in the liver: pivotal role of CREB and CREM. Exp. Cell Res. 275, 143-154(2002).
13. Pethe, K. et al. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc. Natl Acad. Sci. USA 101, 13642-13647 (2004).
14. Walburger, A. et al. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304, 1800-1804 (2004).
15. Fratti, R. A., Chua, J., Vergne, I. & Deretic, V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl Acad. Sci. USA 100, 5437-5442 (2003).
16. Axelrod, S. et al. Delay of phagosome maturation by a mycobacterial lipid is reversed by nitric oxide. Cell. Microbiol. 10, 1530-1545 (2008).
17. Hunter,R. L.,Jagannath,C.&Actor,J. K. Pathologyofpostprimarytuberculosisin humans and mice: contradiction of long-held beliefs. Tuberculosis (Edinb.) 87, 267-278 (2007).
18. Tsai, M. C. et al. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell. Microbiol. 8, 218-232 (2006).
19. Timm, J. et al. Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genesin thelungsofchronically infected miceand tuberculosis patients. Proc. Natl Acad. Sci. USA 100, 14321-14326 (2003).
20. Via, L. E. et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect. Immun. 76, 2333-2340 (2008).
21. Shenoy, A. R., Sivakumar, K., Krupa, A., Srinivasan, N. & Visweswariah, S. S. A survey of nucleotide cyclases in Actinobacteria: unique domain organization and expansion of the class III cyclase family in Mycobacterium tuberculosis. Comp. Funct. Genomics 5, 17-38 (2004).
22. Lamichhane, G. et al. A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 100, 7213-7218 (2003).
23. Ahuja, N., Kumar, P. & Bhatnagar, R. The adenylate cyclase toxins. Crit. Rev. Microbiol. 30, 187-196 (2004).
24. von Knethen, A. & Brune, B. Attenuation of macrophage apoptosis by the cAMP- signaling system. Mol. Cell. Biochem. 212, 35-43 (2000).
25. Keane, J. et al. Tuberculosis associated with infliximab, a tumor necrosis factor a-neutralizing agent. N. Engl. J. Med. 345, 1098-1104 (2001).
26. Chakravarty, S. D. et al. Tumor necrosis factor blockade in chronic murine tuberculosis enhances granulomatous inflammation and disorganizes granulomas in the lungs. Infect. Immun. 76, 916-926 (2008).
27. Bekker, L. G. et al. Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect. Immun. 68, 6954-6961 (2000).
28. Clay, H., Volkman, H. E. & Ramakrishnan, L. Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death. Immunity 29, 283-294 (2008).
29. Hanekom, W. A. et al. Mycobacterium tuberculosis inhibits maturation of human monocyte-derived dendritic cells in vitro. J. Infect. Dis. 188, 257-266 (2003).
30. Davis, J. M. & Ramakrishnan, L. The role of the granuloma in expansion and dissemination ofearly tuberculous infection. Cell 136, 37-49 (2009).
31. Agarwal, N., Woolwine, S. C., Tyagi, S. & Bishai, W. R. Characterization of the Mycobacterium tuberculosis sigma factor SigM by assessment ofvirulence and identification of SigM-dependent genes. Infect. Immun. 75, 452-461 (2007).
32. Shenoy, A.R., Sreenath, N., Podobnik, M., Kovacevic, M. & Visweswariah, S.S. The Rv0805 gene from Mycobacterium tuberculosis encodes a 3',5'-cyclic nucleotide phosphodiesterase: biochemical and mutational analysis. Biochemistry 44, 15695-15704 (2005).
33. Higashida, H., Hossain, K. Z., Takahagi, H. & Noda, M. Measurement of adenyly cyc ase by separating cyc ic AMP on si ica ge thin- ayer chromatography. Anal. Biochem. 308, 106-111 (2002).
34. Bohme, E. & Schultz, G. Separation of cyclic nucleotides by thin-layer chromatography on polyethyleneimine cellulose. Methods Enzymol. 38, 27-38 (1974).