1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Cyclic AMP Signaling in Mycobacteria

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
    124.81 Kb
  • HTML
    145.16 Kb
  • PDF
    433.00 Kb
  • Authors: Gwendowlyn S. Knapp1, Kathleen A. McDonough2
  • Editors: Graham F. Hatfull4, William R. Jacobs Jr.5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Wadsworth Center, New York State Department of Health, 120 New Scotland Avenue, PO Box 22002, Albany, NY 12222; 2: Wadsworth Center, New York State Department of Health, 120 New Scotland Avenue, PO Box 22002, Albany, NY 12222; 3: Department of Biomedical Sciences, University at Albany, Albany, NY 12222; 4: University of Pittsburgh, Pittsburgh, PA 15260; 5: Howard Hughes Medical Institute, Albert Einstein College of Medicine, Bronx, NY 10461
    • Source: microbiolspec April 2014 vol. 2 no. 2 doi:10.1128/microbiolspec.MGM2-0011-2013
  • Received 29 August 2013 Accepted 04 September 2013 Published 04 April 2014
  • K. A. McDonough, [email protected]
image of Cyclic AMP Signaling in Mycobacteria
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Cyclic AMP Signaling in Mycobacteria, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/2/2/MGM2-0011-2013-1.gif /docserver/preview/fulltext/microbiolspec/2/2/MGM2-0011-2013-2.gif

  • Abstract:

    All cells must adapt to changing conditions, and many use cyclic AMP (cAMP) as a second messenger to sense and respond to fluctuations in their environment. cAMP is made by adenylyl cyclases (ACs), and mycobacteria have an unusually large number of biochemically distinct ACs. cAMP is important for gene regulation in mycobacteria, and the ability to secrete cAMP into host macrophages during infection contributes to pathogenesis. This article discusses the many roles of cAMP in mycobacteria and reviews what is known about the factors that contribute to production, destruction, and utilization of this important signal molecule. Special emphasis is placed on cAMP signaling in complex bacteria and its importance to during host infection.

  • Citation: Knapp G, McDonough K. 2014. Cyclic AMP Signaling in Mycobacteria. Microbiol Spectrum 2(2):MGM2-0011-2013. doi:10.1128/microbiolspec.MGM2-0011-2013.

References

1. Altarejos JY, Montminy M. 2011. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12:141–151. [PubMed][CrossRef]
2. Kolb A, Busby S, Buc H, Garges S, Adhya S. 1993. Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 62:749–795. [PubMed][CrossRef]
3. Kamenetsky M, Middelhaufe S, Bank EM, Levin LR, Buck J, Steegborn C. 2006. Molecular details of cAMP generation in mammalian cells: a tale of two systems. J Mol Biol 362:623–639. [PubMed][CrossRef]
4. Gorke B, Stulke J. 2008. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624. [PubMed][CrossRef]
5. Botsford JL, Harman JG. 1992. Cyclic AMP in prokaryotes. Microbiol Rev 56:100–122. [PubMed]
6. Kresge N, Simoni RD, Hill RL. 2005. Earl W. Sutherland's discovery of cyclic adenine monophosphate and the second messenger system. J Biol Chem 280:e39–e40.
7. Serezani CH, Ballinger MN, Aronoff DM, Peters-Golden M. 2008. Cyclic AMP: master regulator of innate immune cell function. Am J Respir Cell Mol Biol 39:127–132. [PubMed][CrossRef]
8. Botsford JL. 1981. Cyclic nucleotides in procaryotes. Microbiol Rev 45:620–642. [PubMed]
9. McDonough KA, Rodriguez A. 2012. The myriad roles of cyclic AMP in microbial pathogens: from signal to sword. Nat Rev Microbiol 10:27–38. [PubMed][CrossRef]
10. Leppla SH. 1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci USA 79:3162–3166. [PubMed]
11. Weiss AA, Hewlett EL, Myers GA, Falkow S. 1984. Pertussis toxin and extracytoplasmic adenylate cyclase as virulence factors of Bordetella pertussis. J Infect Dis 150:219–222. [PubMed]
12. Yahr TL, Vallis AJ, Hancock MK, Barbieri JT, Frank DW. 1998. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci USA 95:13899–13904. [PubMed]
13. Gallagher DT, Kim SK, Robinson H, Reddy PT. 2011. Active-site structure of class IV adenylyl cyclase and transphyletic mechanism. J Mol Biol 405:787–803. [PubMed][CrossRef]
14. Smith N, Kim SK, Reddy PT, Gallagher DT. 2006. Crystallization of the class IV adenylyl cyclase from Yersinia pestis. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:200–204. [PubMed][CrossRef]
15. Sismeiro O, Trotot P, Biville F, Vivares C, Danchin A. 1998. Aeromonas hydrophila adenylyl cyclase 2: a new class of adenylyl cyclases with thermophilic properties and sequence similarities to proteins from hyperthermophilic archaebacteria. J Bacteriol 180:3339–3344. [PubMed]
16. Cotta MA, Whitehead TR, Wheeler MB. 1998. Identification of a novel adenylate cyclase in the ruminal anaerobe, Prevotella ruminicola D31d. FEMS Microbiol Lett 164:257–260. [PubMed]
17. Tellez-Sosa J, Soberon N, Vega-Segura A, Torres-Marquez ME, Cevallos MA. 2002. The Rhizobium etli cyaC product: characterization of a novel adenylate cyclase class. J Bacteriol 184:3560–3568. [PubMed]
18. Tang WJ, Yan S, Drum CL. 1998. Class III adenylyl cyclases: regulation and underlying mechanisms. Adv Second Messenger Phosphoprotein Res 32:137–151. [PubMed]
19. McCue LA, McDonough KA, Lawrence CE. 2000. Functional classification of cNMP-binding proteins and nucleotide cyclases with implications for novel regulatory pathways in Mycobacterium tuberculosis. Genome Res 10:204–219. [PubMed]
20. Cha PH, Park SY, Moon MW, Subhadra B, Oh TK, Kim E, Kim JF, Lee JK. 2010. Characterization of an adenylate cyclase gene ( cyaB) deletion mutant of Corynebacterium glutamicum ATCC 13032. Appl Microbiol Biotechnol 85:1061–1068. [PubMed][CrossRef]
21. Shenoy AR, Sivakumar K, Krupa A, Srinivasan N, Visweswariah SS. 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. [PubMed][CrossRef]
22. Klengel T, Liang WJ, Chaloupka J, Ruoff C, Schroppel K, Naglik JR, Eckert SE, Mogensen EG, Haynes K, Tuite MF, Levin LR, Buck J, Muhlschlegel FA. 2005. Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15:2021–2026. [PubMed][CrossRef]
23. Mallet L, Renault G, Jacquet M. 2000. Functional cloning of the adenylate cyclase gene of Candida albicans in Saccharomyces cerevisiae within a genomic fragment containing five other genes, including homologues of CHS6 and SAP185. Yeast 16:959–966. [PubMed][CrossRef]
24. Shenoy AR, Sreenath N, Podobnik M, Kovacevic M, Visweswariah SS. 2005. The Rv0805 gene from Mycobacterium tuberculosis encodes a 3′,5′-cyclic nucleotide phosphodiesterase: biochemical and mutational analysis. Biochemistry 44:15695–15704. [PubMed][CrossRef]
25. Shenoy AR, Capuder M, Draskovic P, Lamba D, Visweswariah SS, Podobnik M. 2007. Structural and biochemical analysis of the Rv0805 cyclic nucleotide phosphodiesterase from Mycobacterium tuberculosis. J Mol Biol 365:211–225. [PubMed][CrossRef]
26. Keppetipola N, Shuman S. 2008. A phosphate-binding histidine of binuclear metallophosphodiesterase enzymes is a determinant of 2′,3′-cyclic nucleotide phosphodiesterase activity. J Biol Chem 283:30942–30949. [PubMed][CrossRef]
27. Podobnik M, Tyagi R, Matange N, Dermol U, Gupta AK, Mattoo R, Seshadri K, Visweswariah SS. 2009. A mycobacterial cyclic AMP phosphodiesterase that moonlights as a modifier of cell wall permeability. J Biol Chem 284:32846–32857. [PubMed][CrossRef]
28. de Carvalho LP, Fischer SM, Marrero J, Nathan C, Ehrt S, Rhee KY. 2010. Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem Biol 17:1122–1131. [PubMed][CrossRef]
29. Buettner MJ, Spitz E, Rickenberg HV. 1973. Cyclic adenosine 3′,5′-monophosphate in Escherichia coli. J Bacteriol 114:1068–1073. [PubMed]
30. Epstein W, Rothman-Denes LB, Hesse J. 1975. Adenosine 3′:5′-cyclic monophosphate as mediator of catabolite repression in Escherichia coli. Proc Natl Acad Sci USA 72:2300–2304. [PubMed]
31. Bai G, Schaak DD, McDonough KA. 2009. cAMP levels within Mycobacterium tuberculosis and Mycobacterium bovis BCG increase upon infection of macrophages. FEMS Immunol Med Microbiol 55:68–73. [PubMed][CrossRef]
32. Dass BK, Sharma R, Shenoy AR, Mattoo R, Visweswariah SS. 2008. Cyclic AMP in mycobacteria: characterization and functional role of the Rv1647 ortholog in Mycobacterium smegmatis. J Bacteriol 190:3824–3834. [PubMed][CrossRef]
33. Padh H, Venkitasubramanian TA. 1976. Adenosine 3′,5′-monophosphate in Mycobacterium phlei and Mycobacterium tuberculosis H37Ra. Microbios 16:183–189. [PubMed]
34. Lee CH. 1979. Metabolism of cyclic AMP in non-pathogenic Mycobacterium smegmatis. Arch Microbiol 120:35–37. [PubMed]
35. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544. [PubMed][CrossRef]
36. Shenoy AR, Visweswariah SS. 2006. New messages from old messengers: cAMP and mycobacteria. Trends Microbiol 14:543–550. [PubMed][CrossRef]
37. Shenoy AR, Sreenath NP, Mahalingam M, Visweswariah SS. 2005. Characterization of phylogenetically distant members of the adenylate cyclase family from mycobacteria: Rv1647 from Mycobacterium tuberculosis and its orthologue ML1399 from M. leprae. Biochem J 387:541–551. [PubMed][CrossRef]
38. Guo YL, Seebacher T, Kurz U, Linder JU, Schultz JE. 2001. Adenylyl cyclase Rv1625c of Mycobacterium tuberculosis: a progenitor of mammalian adenylyl cyclases. EMBO J 20:3667–3675. [PubMed][CrossRef]
39. Reddy SK, Kamireddi M, Dhanireddy K, Young L, Davis A, Reddy PT. 2001. Eukaryotic-like adenylyl cyclases in Mycobacterium tuberculosis H37Rv: cloning and characterization. J Biol Chem 276:35141–35149. [PubMed][CrossRef]
40. Linder JU, Schultz A, Schultz JE. 2002. Adenylyl cyclase Rv1264 from Mycobacterium tuberculosis has an autoinhibitory N-terminal domain. J Biol Chem 277:15271–15276. [PubMed][CrossRef]
41. Tews I, Findeisen F, Sinning I, Schultz A, Schultz JE, Linder JU. 2005. The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science 308:1020–1023. [PubMed][CrossRef]
42. Linder JU, Hammer A, Schultz JE. 2004. The effect of HAMP domains on class IIIb adenylyl cyclases from Mycobacterium tuberculosis. Eur J Biochem 271:2446–2451. [PubMed][CrossRef]
43. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, Schultz A, Martin J, Schultz JE, Lupas AN, Coles M. 2006. The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929–940. [PubMed][CrossRef]
44. Agarwal N, Lamichhane G, Gupta R, Nolan S, Bishai WR. 2009. Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase. Nature 460:98–102. [PubMed][CrossRef]
45. Sinha SC, Wetterer M, Sprang SR, Schultz JE, Linder JU. 2005. Origin of asymmetry in adenylyl cyclases: structures of Mycobacterium tuberculosis Rv1900c. EMBO J 24:663–673. [PubMed][CrossRef]
46. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK. 2001. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc Natl Acad Sci USA 98:7534–7539. [PubMed][CrossRef]
47. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K. 2002. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43:717–731. [PubMed]
48. Abdel Motaal A, Tews I, Schultz JE, Linder JU. 2006. Fatty acid regulation of adenylyl cyclase Rv2212 from Mycobacterium tuberculosis H37Rv. FEBS J 273:4219–4228. [PubMed][CrossRef]
49. Cann MJ, Hammer A, Zhou J, Kanacher T. 2003. A defined subset of adenylyl cyclases is regulated by bicarbonate ion. J Biol Chem 278:35033–35038. [PubMed][CrossRef]
50. Townsend PD, Holliday PM, Fenyk S, Hess KC, Gray MA, Hodgson DR, Cann MJ. 2009. Stimulation of mammalian G-protein-responsive adenylyl cyclases by carbon dioxide. J Biol Chem 284:784–791. [PubMed][CrossRef]
51. Nambi S, Basu N, Visweswariah SS. 2010. cAMP-regulated protein lysine acetylases in mycobacteria. J Biol Chem 285:24313–24323. [PubMed][CrossRef]
52. Bai G, Gazdik MA, Schaak DD, McDonough KA. 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. [PubMed][CrossRef]
53. Bai G, McCue LA, McDonough KA. 2005. Characterization of Mycobacterium tuberculosis Rv3676 (CRPMt), a cyclic AMP receptor protein-like DNA binding protein. J Bacteriol 187:7795–7804. [PubMed][CrossRef]
54. Reddy MC, Palaninathan SK, Bruning JB, Thurman C, Smith D, Sacchettini JC. 2009. Structural insights into the mechanism of the allosteric transitions of Mycobacterium tuberculosis cAMP receptor protein. J Biol Chem 284:36581–36591. [PubMed][CrossRef]
55. Stapleton M, Haq I, Hunt DM, Arnvig KB, Artymiuk PJ, Buxton RS, Green J. 2010. Mycobacterium tuberculosis cAMP receptor protein (Rv3676) differs from the Escherichia coli paradigm in its cAMP binding and DNA binding properties and transcription activation properties. J Biol Chem 285:7016–7027. [PubMed][CrossRef]
56. Kumar M, Khan FG, Sharma S, Kumar R, Faujdar J, Sharma R, Chauhan DS, Singh R, Magotra SK, Khan IA. 2011. Identification of Mycobacterium tuberculosis genes preferentially expressed during human infection. Microb Pathog 50:31–38. [PubMed][CrossRef]
57. Stapleton MR, Smith LJ, Hunt DM, Buxton RS, Green J. 2012. Mycobacterium tuberculosis WhiB1 represses transcription of the essential chaperonin GroEL2. Tuberculosis (Edinb) 92:328–332. [PubMed][CrossRef]
58. Gazdik MA, Bai G, Wu Y, McDonough KA. 2009. Rv1675c ( cmr) regulates intramacrophage and cyclic AMP-induced gene expression in Mycobacterium tuberculosis-complex mycobacteria. Mol Microbiol 71:434–448. [PubMed][CrossRef]
59. Pelly S, Bishai WR, Lamichhane G. 2012. A screen for non-coding RNA in Mycobacterium tuberculosis reveals a cAMP-responsive RNA that is expressed during infection. Gene 500:85–92. [PubMed][CrossRef]
60. Gazdik MA, McDonough KA. 2005. Identification of cyclic AMP-regulated genes in Mycobacterium tuberculosis complex bacteria under low-oxygen conditions. J Bacteriol 187:2681–2692. [PubMed][CrossRef]
61. Rickman L, Scott C, Hunt DM, Hutchinson T, Menendez MC, Whalan R, Hinds J, Colston MJ, Green J, Buxton RS. 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. [PubMed][CrossRef]
62. Gottesman S, Storz G. 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3(12). [PubMed][CrossRef]
63. DiChiara JM, Contreras-Martinez LM, Livny J, Smith D, McDonough KA, Belfort M. 2010. Multiple small RNAs identified in Mycobacterium bovis BCG are also expressed in Mycobacterium tuberculosis and Mycobacterium smegmatis. Nucleic Acids Res 38:4067–4078. [PubMed][CrossRef]
64. Arnvig KB, Young DB. 2009. Identification of small RNAs in Mycobacterium tuberculosis. Mol Microbiol 73:397–408. [PubMed][CrossRef]
65. Arnvig KB, Comas I, Thomson NR, Houghton J, Boshoff HI, Croucher NJ, Rose G, Perkins TT, Parkhill J, Dougan G, Young DB. 2011. Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis. PLoS Pathog 7:e1002342. [PubMed][CrossRef]
66. Lamichhane G, Arnvig KB, McDonough KA. 2013. Definition and annotation of (myco)bacterial non-coding RNA. Tuberculosis (Edinb) 93:26–29. [PubMed][CrossRef]
67. Spreadbury CL, Pallen MJ, Overton T, Behr MA, Mostowy S, Spiro S, Busby SJ, Cole JA. 2005. Point mutations in the DNA- and cNMP-binding domains of the homologue of the cAMP receptor protein (CRP) in Mycobacterium bovis BCG: implications for the inactivation of a global regulator and strain attenuation. Microbiology 151:547–556. [PubMed][CrossRef]
68. Hunt DM, Saldanha JW, Brennan JF, Benjamin P, Strom M, Cole JA, Spreadbury CL, Buxton RS. 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. [PubMed][CrossRef]
69. Clarke SJ, Low B, Konigsberg WH. 1973. Close linkage of the genes serC (for phosphohydroxy pyruvate transaminase) and serS (for seryl-transfer ribonucleic acid synthetase) in Escherichia coli K-12. J Bacteriol 113:1091–1095. [PubMed]
70. Bai G, Schaak DD, Smith EA, McDonough KA. 2011. Dysregulation of serine biosynthesis contributes to the growth defect of a Mycobacterium tuberculosis crp mutant. Mol Microbiol 82:180–198. [PubMed][CrossRef]
71. Mukamolova GV, Turapov OA, Young DI, Kaprelyants AS, Kell DB, Young M. 2002. A family of autocrine growth factors in Mycobacterium tuberculosis. Mol Microbiol 46:623–635. [PubMed]
72. Akhter Y, Yellaboina S, Farhana A, Ranjan A, Ahmed N, Hasnain SE. 2008. Genome scale portrait of cAMP-receptor protein (CRP) regulons in mycobacteria points to their role in pathogenesis. Gene 407:148–158. [PubMed][CrossRef]
73. Krawczyk J, Kohl TA, Goesmann A, Kalinowski J, Baumbach J. 2009. From Corynebacterium glutamicum to Mycobacterium tuberculosis: towards transfers of gene regulatory networks and integrated data analyses with MycoRegNet. Nucleic Acids Res 37:e97. [PubMed][CrossRef]
74. Agarwal N, Raghunand TR, Bishai WR. 2006. Regulation of the expression of whiB1 in Mycobacterium tuberculosis: role of cAMP receptor protein. Microbiology 152:2749–2756. [PubMed][CrossRef]
75. Bai G, Knapp GS, McDonough KA. 2011. Cyclic AMP signalling in mycobacteria: redirecting the conversation with a common currency. Cell Microbiol 13:349–358. [PubMed][CrossRef]
76. Gallagher DT, Smith N, Kim SK, Robinson H, Reddy PT. 2009. Profound asymmetry in the structure of the cAMP-free cAMP receptor protein (CRP) from Mycobacterium tuberculosis. J Biol Chem 284:8228–8232. [PubMed][CrossRef]
77. Kumar P, Joshi DC, Akif M, Akhter Y, Hasnain SE, Mande SC. 2010. Mapping conformational transitions in cyclic AMP receptor protein: crystal structure and normal-mode analysis of Mycobacterium tuberculosis apo-cAMP receptor protein. Biophys J 98:305–314. [PubMed][CrossRef]
78. Aiba H, Nakamura T, Mitani H, Mori H. 1985. Mutations that alter the allosteric nature of cAMP receptor protein of Escherichia coli. EMBO J 4:3329–3332. [PubMed]
79. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834–840. [PubMed][CrossRef]
80. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y. 2006. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23:607–618. [PubMed][CrossRef]
81. Zhao JY, Lu N, Yan Z, Wang N. 2010. SAHA and curcumin combinations co-enhance histone acetylation in human cancer cells but operate antagonistically in exerting cytotoxic effects. J Asian Nat Prod Res 12:335–348. [PubMed][CrossRef]
82. Wang Q, Zhang Y, Yang C, Xiong H, Lin Y, Yao J, Li H, Xie L, Zhao W, Yao Y, Ning ZB, Zeng R, Xiong Y, Guan KL, Zhao S, Zhao GP. 2010. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. 327:1004–1007. [PubMed][CrossRef]
83. Thao S, Chen CS, Zhu H, Escalante-Semerena JC. 2010. Nepsilon-lysine acetylation of a bacterial transcription factor inhibits its DNA-binding activity. PLoS One 5:e15123. [PubMed][CrossRef]
84. Xu H, Hegde SS, Blanchard JS. 2011. Reversible acetylation and inactivation of Mycobacterium tuberculosis acetyl-CoA synthetase is dependent on cAMP. Biochemistry 50:5883–5892. [PubMed][CrossRef]
85. Lee HJ, Lang PT, Fortune SM, Sassetti CM, Alber T. 2012. Cyclic AMP regulation of protein lysine acetylation in Mycobacterium tuberculosis. Nat Struct Mol Biol 19:811–818. [PubMed][CrossRef]
86. Starai VJ, Escalante-Semerena JC. 2004. Acetyl-coenzyme A synthetase (AMP forming). Cell Mol Life Sci 61:2020–2030. [PubMed][CrossRef]
87. Zhao K, Chai X, Marmorstein R. 2004. Structure and substrate binding properties of cobB, a Sir2 homolog protein deacetylase from Escherichia coli. J Mol Biol 337:731–741. [PubMed][CrossRef]
88. Castano-Cerezo S, Bernal V, Blanco-Catala J, Iborra JL, Canovas M. 2011. cAMP-CRP co-ordinates the expression of the protein acetylation pathway with central metabolism in Escherichia coli. Mol Microbiol 82:1110–1128. [PubMed][CrossRef]
89. Richter W. 2002. 3′,5′ Cyclic nucleotide phosphodiesterases class III: members, structure, and catalytic mechanism. Proteins 46:278–286. [PubMed]
90. Imamura R, Yamanaka K, Ogura T, Hiraga S, Fujita N, Ishihama A, Niki H. 1996. Identification of the cpdA gene encoding cyclic 3′,5′-adenosine monophosphate phosphodiesterase in Escherichia coli. J Biol Chem 271:25423–25429. [PubMed]
91. Carte J, Wang R, Li H, Terns RM, Terns MP. 2008. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 22:3489–3496. [PubMed][CrossRef]
92. Zhang Y, Zhang J, Hara H, Kato I, Inouye M. 2005. Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase. J Biol Chem 280:3143–3150. [PubMed][CrossRef]
93. Zhang Y, Zhu L, Zhang J, Inouye M. 2005. Characterization of ChpBK, an mRNA interferase from Escherichia coli. J Biol Chem 280:26080–26088. [PubMed][CrossRef]
94. Barba J, Alvarez AH, Flores-Valdez MA. 2010. Modulation of cAMP metabolism in Mycobacterium tuberculosis and its effect on host infection. Tuberculosis (Edinb) 90:208–212. [PubMed][CrossRef]
95. Padh H, Venkitasubramanian TA. 1976. Cyclic adenosine 3′, 5′-monophosphate in mycobacteria. Indian J Biochem Biophys 13:413–414. [PubMed]
96. Ahuja N, Kumar P, Bhatnagar R. 2004. The adenylate cyclase toxins. Crit Rev Microbiol 30:187–196. [PubMed][CrossRef]
97. Krueger KM, Barbieri JT. 1995. The family of bacterial ADP-ribosylating exotoxins. Clin Microbiol Rev 8:34–47. [PubMed]
98. Lory S, Wolfgang M, Lee V, Smith R. 2004. The multi-talented bacterial adenylate cyclases. Int J Med Microbiol 293:479–482. [PubMed][CrossRef]
99. Lowrie DB, Aber VR, Jackett PS. 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. [PubMed]
100. Lowrie DB, Jackett PS, Ratcliffe NA. 1975. Mycobacterium microti may protect itself from intracellular destruction by releasing cyclic AMP into phagosomes. Nature 254:600–602. [PubMed]
101. Roach SK, Lee SB, Schorey JS. 2005. Differential activation of the transcription factor cyclic AMP response element binding protein (CREB) in macrophages following infection with pathogenic and nonpathogenic mycobacteria and role for CREB in tumor necrosis factor alpha production. Infect Immun 73:514–522. [PubMed][CrossRef]
102. Yadav M, Roach SK, Schorey JS. 2004. Increased mitogen-activated protein kinase activity and TNF-alpha production associated with Mycobacterium smegmatis- but not Mycobacterium avium-infected macrophages requires prolonged stimulation of the calmodulin/calmodulin kinase and cyclic AMP/protein kinase A pathways. J Immunol 172:5588–5597.
103. Kalamidas SA, Kuehnel MP, Peyron P, Rybin V, Rauch S, Kotoulas OB, Houslay M, Hemmings BA, Gutierrez MG, Anes E, Griffiths G. 2006. cAMP synthesis and degradation by phagosomes regulate actin assembly and fusion events: consequences for mycobacteria. J Cell Sci 119:3686–3694. [PubMed][CrossRef]
104. Ohno H, Zhu G, Mohan VP, Chu D, Kohno S, Jacobs WR, Jr, Chan J. 2003. The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell Microbiol 5:637–648. [PubMed]
105. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, Schoolnik GK. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198:693–704. [PubMed][CrossRef]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013
2014-04-04
2021-04-23

Abstract:

All cells must adapt to changing conditions, and many use cyclic AMP (cAMP) as a second messenger to sense and respond to fluctuations in their environment. cAMP is made by adenylyl cyclases (ACs), and mycobacteria have an unusually large number of biochemically distinct ACs. cAMP is important for gene regulation in mycobacteria, and the ability to secrete cAMP into host macrophages during infection contributes to pathogenesis. This article discusses the many roles of cAMP in mycobacteria and reviews what is known about the factors that contribute to production, destruction, and utilization of this important signal molecule. Special emphasis is placed on cAMP signaling in complex bacteria and its importance to during host infection.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/2/2/MGM2-0011-2013.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013&mimeType=html&fmt=ahah

Figures

Cyclic AMP Signaling in Mycobacteria
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-1,properties={foaf_givenname=Gwendowlyn S., foaf_name=Gwendowlyn S. Knapp, foaf_surname=Knapp, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-2,properties={foaf_givenname=Kathleen A., foaf_name=Kathleen A. McDonough, foaf_surname=McDonough, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-aff2]]}]]
Citation: Knapp G, McDonough K. 2014. Cyclic amp signaling in mycobacteria. microbiolspec 2(2): doi:10.1128/microbiolspec.MGM2-0011-2013
/content/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013.fig1
FIGURE 1
Environmental signals to regulatory outputs by cAMP. The conversion of ATP into cAMP and inorganic pyrophosphate and AMP is catalyzed by ACs. Degradation of cAMP is catalyzed by the phosphodiesterase. Activation of the AC can come from extracellular and intracellular signals that are relayed to the AC through membrane-bound or cytoplasmic receptors. The newly generated cAMP relays the activating signal to cAMP-binding proteins.
microbiolspec/2/2/MGM2-0011-2013-fig1_thmb.gif
microbiolspec/2/2/MGM2-0011-2013-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

Environmental signals to regulatory outputs by cAMP. The conversion of ATP into cAMP and inorganic pyrophosphate and AMP is catalyzed by ACs. Degradation of cAMP is catalyzed by the phosphodiesterase. Activation of the AC can come from extracellular and intracellular signals that are relayed to the AC through membrane-bound or cytoplasmic receptors. The newly generated cAMP relays the activating signal to cAMP-binding proteins.

Source: microbiolspec April 2014 vol. 2 no. 2 doi:10.1128/microbiolspec.MGM2-0011-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013.fig2
FIGURE 2
cAMP signaling pathways. ACs are shown with their known signals. Upon activation by the signal, the ACs generate cAMP and there are several fates of cAMP within . Most notable is cAMP binding to cNMP binding proteins to affect virulence, gene expression (including macrophage gene expression), and protein lysine acetylation. cAMP can be exported to the macrophage to affect TNFα production. Finally, Rv0805 can decrease cAMP levels by degrading the cAMP. Activating signals are shown in green, cAMP effector proteins are in yellow, and functional outcomes are designated in blue.
microbiolspec/2/2/MGM2-0011-2013-fig2_thmb.gif
microbiolspec/2/2/MGM2-0011-2013-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

cAMP signaling pathways. ACs are shown with their known signals. Upon activation by the signal, the ACs generate cAMP and there are several fates of cAMP within . Most notable is cAMP binding to cNMP binding proteins to affect virulence, gene expression (including macrophage gene expression), and protein lysine acetylation. cAMP can be exported to the macrophage to affect TNFα production. Finally, Rv0805 can decrease cAMP levels by degrading the cAMP. Activating signals are shown in green, cAMP effector proteins are in yellow, and functional outcomes are designated in blue.

Source: microbiolspec April 2014 vol. 2 no. 2 doi:10.1128/microbiolspec.MGM2-0011-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013.fig3
FIGURE 3
cAMP-dependent regulation of acetylation in and . In , cAMP's role in regulation is at the transcriptional level, whereas in cAMP binds to the acetyltransferase, PatA, directly. cAMP-CRP complexes regulate and Z at the transcriptional level in while the role of CRP in regulation of and A is unknown at this time. CobB is a NAD-dependent sirtuin, as is Rv1151c.
microbiolspec/2/2/MGM2-0011-2013-fig3_thmb.gif
microbiolspec/2/2/MGM2-0011-2013-fig3.gif
Image of FIGURE 3

Click to view

FIGURE 3

cAMP-dependent regulation of acetylation in and . In , cAMP's role in regulation is at the transcriptional level, whereas in cAMP binds to the acetyltransferase, PatA, directly. cAMP-CRP complexes regulate and Z at the transcriptional level in while the role of CRP in regulation of and A is unknown at this time. CobB is a NAD-dependent sirtuin, as is Rv1151c.

Source: microbiolspec April 2014 vol. 2 no. 2 doi:10.1128/microbiolspec.MGM2-0011-2013
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Cyclic AMP Signaling in Mycobacteria
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-1,properties={foaf_givenname=Gwendowlyn S., foaf_name=Gwendowlyn S. Knapp, foaf_surname=Knapp, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-2,properties={foaf_givenname=Kathleen A., foaf_name=Kathleen A. McDonough, foaf_surname=McDonough, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013-aff2]]}]]
Citation: Knapp G, McDonough K. 2014. Cyclic amp signaling in mycobacteria. microbiolspec 2(2): doi:10.1128/microbiolspec.MGM2-0011-2013
/content/microbiolspec/10.1128/microbiolspec.MGM2-0011-2013.T1
TABLE 1
ACs in
Generic image for table

Click to view

TABLE 1

ACs in

Source: microbiolspec April 2014 vol. 2 no. 2 doi:10.1128/microbiolspec.MGM2-0011-2013

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error