Rv1675c (cmr) regulates intramacrophage and cyclic AMP-induced gene expression in Mycobacterium tuberculosis-complex mycobacteria

Molecular Microbiology

Volumn 71, Issue 2, 2009, Pages 434-448

  Gazdik, Michaela A ^a   Bai, Guangchun ^b   Wu, Yan ^a   McDonough, Kathleen A ^a,b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; HISTIDINE; PROTEIN; RV1675C PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DNA SEQUENCE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; REGULON; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CYCLIC AMP; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKDOWN TECHNIQUES; HYDROGEN-ION CONCENTRATION; MACROPHAGES; MICE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; PROMOTER REGIONS, GENETIC; REGULON; RNA, BACTERIAL; TRANSCRIPTION FACTORS;

CORYNEBACTERINEAE; MYCOBACTERIUM BOVIS BCG; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS COMPLEX;

EID: 58149287886     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06541.x     Document Type: Article

References (50)

1. Abdel Motaal, A., Tews, I., Schultz, J.E. Linder, J.U. (2006) Fatty acid regulation of adenylyl cyclase Rv2212 from Mycobacterium tuberculosis H37Rv. FEBS J 273 : 4219 4228.
2. Agarwal, N., Raghunand, T.R. Bishai, W.R. (2006) Regulation of the expression of whiB1 in Mycobacterium tuberculosis: role of cAMP receptor protein. Microbiology 152 : 2749 2756.
3. Alspaugh, J.A., Perfect, J.R. Heitman, J. (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev 11 : 3206 3217.
4. Alspaugh, J.A., Pukkila-Worley, R., Harashima, T., Cavallo, L.M., Funnell, D., Cox, G.M., et al. (2002) Adenylyl cyclase functions downstream of the Galpha protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot Cell 1 : 75 84.
5. Mt), a cyclic AMP receptor protein-like DNA binding protein. J Bacteriol 187 : 7795 7804.
6. Bai, G., Gazdik, M.A., Schaak, D.D. McDonough, K.A. (2007) The Mycobacterium bovis BCG cyclic AMP receptor-like protein is a functional DNA binding protein in vitro and in vivo, but its activity differs from that of its M. tuberculosis ortholog, Rv3676. Infect Immun 75 : 5509 5517.
7. Bai, G., Schaak, D.D. McDonough, K.A. (2009) cAMP levels within Mycobacterium tuberculosis and M. bovis BCG increase upon infection of macrophages. FEMS Immunol Med Microbiol (in press).
8. Banu, S., Honore, N., Saint-Joanis, B., Philpott, D., Prevost, M.C. Cole, S.T. (2002) Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens? Mol Microbiol 44 : 9 19.
9. Barzu, O. Danchin, A. (1994) Adenylyl cyclases: a heterogenous class of ATP-utilizing enzymes. Prog Nucleic Acid Res Mol Biol 49 : 241 283.
10. Botsford, J.L. Harman, J.G. (1992) Cyclic AMP in prokaryotes. Microbiol Rev 56 : 100 122.
11. Brennan, M.J., Delogu, G., Chen, Y., Bardarov, S., Kriakov, J., Alavi, M. Jacobs, W.R.J. (2001) Evidence that mycobacterial PE_PGRS proteins are cell surface constituents that influence interactions with other cells. Infect Immun 69 : 7326 7333.
12. Cappelli, G., Volpe, E., Grassi, M., Liseo, B., Colizzi, V. Mariani, F. (2006) Profiling of Mycobacterium tuberculosis gene expression during human macrophage infection: upregulation of alternative sigma factor G, a group of transcriptional regulators, and proteins with unknown function. Res Microbiol 157 : 445 455.
13. Castro, L.I., Hermsen, C., Schultz, J.E. Linder, J.U. (2005) Adenylyl cyclase Rv0386 from Mycobacterium tuberculosis H37Rv uses a novel mode for substrate selection. FEBS 272 : 3085 3092.
14. Cole, S.T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393 : 537 544.
15. Delogu, G. Brennan, M.J. (2001) Comparative immune response to PE and PE_PGRS antigens of Mycobacterium tuberculosis. Infect Immun 69 : 5606 5611.
16. Fisher, M.A., Plikaytis, B.B. Shinnick, T.M. (2002) Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in the phagosomes. J Bacteriol 184 : 4025 4032.
17. Florczyk, M.A., McCue, L.A., Stack, R.F., Hauer, C.R. McDonough, K.A. (2001) Identification and characterization of mycobacterial proteins differentially expressed under standing and shaking culture conditions, including Rv2623 from a novel class of putative ATP-binding proteins. Infect Immun 69 : 5777 5785.
18. Gazdik, M.A. McDonough, K.A. (2005) Identification of cyclic AMP-regulated genes in Mycobacterium tuberculosis complex bacteria under low-oxygen conditions. J Bacteriol 187 : 2681 2692.
19. Gross, A., Bouaboula, M., Casellas, P., Liautard, J.-P. Dornand, J. (2003) Subversion and utilization of the host cell cyclic adenosine 5′-monophosphate/protein kinase A pathway by Brucella during macrophage infection. J Immun 170 : 5607 5614.
20. Guo, Y.L., Seebacher, T., Kurz, U., Linder, J.U. Schultz, J.E. (2001) Adenylyl cyclase Rv1625c of Mycobacterium tuberculosis: a progenitor of mammalian adenylyl cyclases. EMBO J 20 : 3667 3675.
21. Hobson, R.J., McBride, A.J., Kempsell, K.E. Dale, J.W. (2002) Use of an arrayed promoter-probe library for the identification of macrophage-regulated genes in Mycobacterium tuberculosis. Microbiology 148 : 1571 1579.
22. Hunt, D.M., Saldanha, J.W., Brennan, J.F., Benjamin, P., Strom, M., Cole, J.A., et al. (2008) Single nucleotide polymorphisms that cause structural changes in the cyclic AMP receptor protein transcriptional regulator of the tuberculosis vaccine strain Mycobacterium bovis BCG alter global gene expression without attenuating growth. Infect Immun 76 : 2227 2234.
23. Kim, T.J., Chauhan, S., Motin, V.L., Goh, E.B., Igo, M.M. Young, G.M. (2007) Direct transcriptional control of the plasminogen activator gene of Yersinia pestis by the cyclic AMP receptor protein. J Bacteriol 189 : 8890 8900.
24. Liebmann, B., Gattung, S., Jahn, B. Brakhage, A.A. (2003) cAMP signaling in Aspergillus fumigatus is involved in the regulation of the virulence gene pksP and in defense against killing by macrophages. Mol Genet Genomics 269 : 420 435.
25. Linder, J.U., Schultz, A. Schultz, J.E. (2002) Adenylyl cyclase Rv1264 from Mycobacterium tuberculosis has an autoinhibitory N-terminal domain. J Biol Chem 277 : 15271 15276.
26. Lowrie, D.B., Jackett, P.S. Ratcliffe, N.A. (1975) Mycobacterium microti may protect itself from intracellular destruction by releasing cyclic AMP into phagosomes. Nature 254 : 600 602.
27. Lowrie, D.B., Aber, V.R. Jackett, P.S. (1979) Phagosome-lysosome fusion and cyclic adenosine 3′: 5′-monophosphate in macrophages infected with Mycobacterium microti, Mycobacterium bovis BCG or Mycobacterium lepraemurium. J Gen Microbiol 110 : 431 441.
28. McCue, L.A., McDonough, K.A. Lawrence, C.E. (2000) Functional classification of cNMP-binding proteins and nucleotide cyclases with implications for novel regulatory pathways in Mycobacterium tuberculosis. Genome Res 10 : 204 219.
29. McDonough, K.A., Kress, Y. Bloom, B.R. (1993) Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 61 : 2763 2773.
30. Manganelli, R., Dubnau, E., Tyagi, S., Kramer, F.R. Smith, I. (1999) Differential expression of 10 sigma factor genes in Mycobacterium tuberculosis. Mol Microbiol 31 : 715 724.
31. Monohan, I.M., Bettes, J., Banerjee, D.K. Butcher, P.D. (2001) Differential expression of mycobacterial proteins following phagocytosis by macrophages. Microbiology 147 : 459 471.
32. Nunn, P., Williams, B., Floyd, K., Dye, C., Elzinga, G. Raviglione, M. (2005) Tuberculosis control in the era of HIV. Nat Rev Immunol 5 : 819 826.
33. Olson, E.R. (1993) Influence of pH on bacterial gene expression. Mol Microbiol 8 : 5 14.
34. Peterkofsky, A., Reizer, A., Reizer, J., Gollop, N., Zhu, P.P. Amin, N. (1993) Bacterial adenylyl cyclases. Prog Nucleic Acid Res Mol Biol 44 : 31 65.
35. Petersen, S. Young, G.M. (2002) Essential role for cyclic AMP and its receptor protein in Yersinia enterocolitica virulence. Infect Immun 70 : 3665 3672.
36. Purkayastha, A., McCue, L.A. McDonough, K.A. (2002) Identification of a Mycobacterium tuberculosis putative classical nitroreductase gene whose expression is coregulated with that of the acr gene within macrophages, in standing versus shaking cultures, and under low oxygen conditions. Infect Immun 70 : 1518 1529.
37. Reddy, S.K., Kamireddi, M., Dhanireddy, K., Young, L., Davis, A. Reddy, P.T. (2001) Eukaryotic-like adenylyl cyclases in Mycobacterium tuberculosis H37Rv: cloning and characterization. J Biol Chem 14 (276 35141 35149.
38. Rickman, L., Scott, C., Hunt, D.M., Hutchinson, T., Menendez, M.C., Whalan, R., et al. (2005) A member of the cAMP receptor protein family of transcription regulators in Mycobacterium tuberculosis is required for virulence in mice and controls transcription of the rpfA gene coding for a resuscitation promoting factor. Mol Microbiol 56 : 1274 1286.
39. Rowland, B., Purkayastha, A., Monserrat, C., Casart, Y., Takiff, H. McDonough, K.A. (1999) Fluorescence-based detection of lacZ reporter gene expression in intact and viable bacteria including Mycobacterium species. FEMS Microbiol Lett 179 : 317 325.
40. Senaratne, R.H., Mobasheri, H., Papavinasasundaram, K.G., Jenner, P., Lea, E.J. Draper, P. (1998) Expression of a gene for a porin-line protein of the OmpA family from Mycobacterium tuberculosis H37Rv. J Bacteriol 180 : 3541 3547.
41. Shenoy, A.R. Visweswariah, S.S. (2006) New messages from old messengers: cAMP and mycobacteria. Trends Microbiol 14 : 543 550.
42. Shenoy, A.R., Sivakumar, K., Krupa, A., Srinivasan, N. Visweswariah, S.S. (2004) 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.
43. Sinha, S.C., Wetterer, M., Sprang, S.R., Schultz, J.E. Linder, J.U. (2005) Origin of asymmetry in adenylyl cyclases: structures of Mycobacterium tuberculosis Rv1900c. EMBO J 24 : 663 673.
44. Smith, I. (2003) Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev 16 : 463 496.
45. Smith, R.S., Wolfgang, M.C. Lory, S. (2004) An adenylate cyclase-controlled signaling network regulates Pseudomonas aeruginosa virulence in a mouse model of acute pneumonia. Infect Immun 72 : 1677 1684.
46. Steiner, A.L., Wehmann, R.E., Parker, C.W. Kipnis, D.M. (1972) Radioimmunoassay for the measurement of cyclic nucleotides. Adv Cyclic Nucleotide Res 2 : 51 61.
47. Sturgill-Koszycki, S., Schlesinger, P.H., Chakraborty, P., Haddix, P.L., Collins, H.L., Fok, A.K., et al. (1994) Lack of acidfication in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263 : 678 681.
48. Swift, T.A. Dias, J.A. (1987) Stimulation of polyamine biosynthesis by follicle-stimulating hormone in serum-free cultures of rat Sertoli cells. Endocrinology 120 : 394 400.
49. Tang, W.J. Hurley, J.H. (1998) Catalytic mechanism and regulation of mammalian adenylyl cyclases. Mol Pharm 54 : 231 240.
50. Tews, I., Findeisen, F., Sinning, I., Schultz, A., Schultz, J.E. Linder, J.U. (2005) The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science 308 : 1020 1023.