Characterization of a Clp Protease Gene Regulator and the Reaeration Response in Mycobacterium tuberculosis

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Sherrid, Ashley M ^a,b   Rustad, Tige R ^a   Cangelosi, Gerard A ^a,b   Sherman, David R ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; ENDOPEPTIDASE CLP; ENDOPEPTIDASE CLP REGULATOR; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; CONTROLLED STUDY; DNA MODIFICATION; GENE IDENTIFICATION; GENE REPLICATION; GENE REPRESSION; GENETIC REGULATION; HYPOXIA; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN DEGRADATION; REOXYGENATION; RNA TRANSLATION; UPREGULATION; ANAEROBIC GROWTH; DNA MICROARRAY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS;

ANAEROBIOSIS; BACTERIAL PROTEINS; BLOTTING, WESTERN; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; MYCOBACTERIUM TUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

EID: 77955343540     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011622     Document Type: Article

References (57)

1. Gedde-Dahl T (1952) Tuberculous infection in the light of tuberculin matriculation. Am J Hyg 56: 139-214.
2. Marks GB, Bai J, Simpson SE, Sullivan EA, Stewart GJ (2000) Incidence of Tuberculosis among a Cohort of Tuberculin-Positive Refugees in Australia. Reappraising the Estimates of Risk. Am J Respir Crit Care Med 162: 1851-1854.
3. Comstock GW (1982) Epidemiology of Tuberculosis. Am Rev Respir Dis 125: 8-15.
4. Moss AR, Hahn JA, Tulsky JP, Daley CL, Small PM, et al. (2000) Tuberculosis in the Homeless. A Prospective Study. Am J Respir Crit Care Med 162: 460-464.
5. Selwyn PA, Hartell D, Lewis VA, Schoenbaum EE, Vermund SH, et al. (1989) A prospective study of the risk of tuberculosis among intravanous drug users with human immunodeficiency virus infection. N Engl J Med 320: 545-550.
6. World Health Organization (2009) Global tuberculosis control: epidemiology, strategy, financing. Geneva.
7. Rustad TR, Sherrid AM, Minch KJ, Sherman DR (2009) Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol 11: 1151-1159.
8. Novy FG, Soule MH (1925) Microbic Respiration. II. Repiration of the Tubercle Bacillus. J Infect Dis 36: 168.
9. Rich AR, Follis RH, Jr. (1942) The effect of low oxygen tension upon the development of experimental tuberculosis. Bull Johns Hopkins Hosp 71: 345-363.
10. Wayne LG (1977) Synchronized replication of Mycobacterium tuberculosis. Infect Immun 17: 528-530.
11. Tsai MC, Chakravarty S, Zhu G, Xu J, Tanaka K, et al. (2006) Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell Microbiol 8: 218-232.
12. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, et al. (2008) Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76: 2333-2340.
13. Haapanen JH, Kass I, Gensini G, Middlebrook G (1959) Studies on the gaseous content of tuberculous cavities. Am Rev Resp Dis 80: 1-5.
14. Wayne LG, Hayes LG (1996) An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64: 2062-2069.
15. Wayne LG, Hayes LG (1998) Nitrate reduction as a marker for hypoxic shiftdown of Mycobacterium tuberculosis. Tuber Lung Dis 79: 127-132.
16. Rao S, Alonso S, Rand L, Dick T, Pethe K (2008) The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 105: 11945- 11950.
17. Boshoff HI, Xu X, Tahlan K, Dowd CS, Pethe K, et al. (2008) Biosynthesis and recycling of nicotinamide cofactors in Mycobacterium tuberculosis. An essential role for NAD in nonreplicating bacilli. J Biol Chem 283: 19329- 19341.
18. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, et al. (2003) Rv3133c/ dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48: 833-843.
19. Dasgupta N, Kapur V, Singh KK, Das TK, Sachdeva S, et al. (2000) Characterization of a two-component system, devR-devS, of Mycobacterium tuberculosis. Tuber Lung Dis 80: 141-159.
20. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, et al. (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha -crystallin. Proc Natl Acad Sci U S A 98: 7534-7539.
21. Rustad TR, Harrell MI, Liao R, Sherman DR (2008) The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE 3: e1502.
22. Downing KJ, Mischenko VV, Shleeva MO, Young DI, Young M, et al. (2005) Mutants of Mycobacterium tuberculosis lacking three of the five rpf-like genes are defective for growth in vivo and for resuscitation in vitro. Infect Immun 73: 3038-3043.
23. Hegde P, Qi R, Abernathy K, Gay C, Dharap S, et al. (2000) A concise guide to cDNA microarray analysis. Biotechniques 29: 548-550, 552-544, 556 passim.
24. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
25. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
26. Wayne LG, Lin KY (1982) Glyoxylate metabolism and adaptation of Mycobacterium tuberculosis to survival under anaerobic conditions. Infect Immun 37: 1042-1049.
27. Cunningham AF, Spreadbury CL (1998) Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16- kilodalton alpha-crystallin homolog. J Bacteriol 180: 801-808.
28. Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
29. Rengarajan J, Bloom BR, Rubin EJ (2005) Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 102: 8237-8232.
30. Sassetti CM, Rubin EJ (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100: 12989-12994.
31. Dawes SS, Warner DF, Tsenova L, Timm J, McKinney JD, et al. (2003) Ribonucleotide reduction in Mycobacterium tuberculosis: function and expression of genes encoding class Ib and class II ribonucleotide reductases. Infect Immun 71: 6124-6131.
32. Barik S, Sureka K, Mukherjee P, Basu J, Kundu M (2010) RseA, the SigE specific anti-sigma factor of Mycobacterium tuberculosis, is inactivated by phosphorylation-dependent ClpC1P2 proteolysis. 75: 592-606.
33. Mehra S, Kaushal D (2009) Functional genomics reveals extended roles of the Mycobacterium tuberculosis stress response factor sigmaH. J Bacteriol 191: 3965-3980.
34. Engels S, Schweitzer JE, Ludwig C, Bott M, Schaffer S (2004) clpC and clpP1P2 gene expression in Corynebacterium glutamicum is controlled by a regulatory network involving the transcriptional regulators ClgR and HspR as well as the ECF sigma factor sH. Mol Microbiol 52: 285-302.
35. Bellier A, Gominet M, Mazodier P (2006) Post-translational control of the Streptomyces lividans ClgR regulon by Cl. Microbiology 152: 1021-1027.
36. Engels S, Ludwig C, Schweitzer JE, Mack C, Bott M, et al. (2005) The transcriptional activator ClgR controls transcription of genes involved in proteolysis and DNA repair in Corynebacterium glutamicum. Mol Microbiol 57: 576-591.
37. Bellier A, Mazodier P (2004) ClgR, a Novel Regulator of clp and lon Expression in Streptomyces. J Bacteriol 186: 3238-3248.
38. Russo S, Schweitzer J-E, Polen T, Bott M, Pohl E (2009) Crystal structure of the caseinolytic protease gene regulator, a transcriptional activator in actinomycetes. J Biol Chem 284: 5208-5216.
39. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385.
40. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
41. Low KL, Rao PSS, Shui G, Bendt AK, Pethe K, et al. (2009) Triacylglycerol utilization is required for regrowth of in vitro hypoxic nonreplicating Mycobacterium bovis bacillus Calmette-Guerin. J Bacteriol 191: 5037-5043.
42. Kana BD, Gordhan BG, Downing K, Sung N, Vostroktunova G, et al. (2008) The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol Microbiol 67: 672-684.
43. Mukamolova GV, Turapov OA, Young DI, Kaprelyants AS, Kell DB, et al. (2002) A family of autocrine growth factors in Mycobacterium tuberculosis. Mol Microbiol 46: 623-635.
44. Tufariello J, Kaixia M, Xu J, Manabe YC, Kesavan AK, et al. (2006) Deletion of the Mycobacterium tuberculosis resuscitation-promoting factor Rv1009 gene results in delayed reactivation from chronic tuberculosis. Infect Immun 74: 2985-2995.
45. Hett EC, Chao MC, Deng LL, Rubin EJ (2008) A Mycobacterial Enzyme Essential for Cell Division Synergizes with Resuscitation-Promoting Factor. PLoS Pathog 4: e1000001.
46. Beste DJ, Peters J, Hooper T, Avignone-Rossa C, Bushell ME, et al. (2005) Compiling a molecular inventory for Mycobacterium bovis BCG at two growth rates: evidence for growth rate-mediated regulation of ribosome biosynthesis and lipid metabolism. J Bacteriol 187: 1677-1684.
47. Gengenbacher M, Rao SPS, Pethe K, Dick T (2010) Nutrient-starved, nonreplicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability. Microbiology 156: 81-87.
48. Manganelli R, Voskuil MI, Schoolnik GK, Dubnau E, Gomez M, et al. (2002) Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression. Mol Microbiol 45: 365-374.
49. Stewart GR, Wernisch L, Stabler R, Mangan JA, Hinds J, et al. (2002) Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 128: 3129-3138.
50. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, et al. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198: 693-704.
51. Rohde KH, Abramovitch RB, Russell DG (2007) Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host & Microbe 2: 352-364.
52. Ventura M, Zhang Z, Cronin M, Canchaya C, Kenny JG, et al. (2005) The ClgR protein regulates transcription of the clpP operon in Bifidobacterium breve UCC 2003. J Bacteriol 187: 8411-8426.
53. Goley ED, Iniesta AA, Shapiro L (2007) Cell cycle regulation in Caulobacter: location, location, location. J Cell Science 120: 3501-3507.
54. Crécy-Lagard Vd, Servant-Moisson P, Viala J, Grandvalet C, Mazodier P (1999) Alteration of the synthesis of the Clp ATP-dependent protease affects morphological and physiological differentiation in Streptomyces. Mol Microbiol 32: 505-517.
55. Darwin KH, Ehrt S, Gutierrez-Ramos J-C, Weich N, Nathan CF (2003) The Proteasome of Mycobacterium tuberculosis Is Required for Resistance to Nitric Oxide. Science 302: 1963-1966.
56. Lin G, Li D, de Carvalho LPS, Deng H, Tao H, et al. (2009) Inhibitors selective for mycobacterial versus human proteasomes. Nature 461: 621-626.
57. Pai M, Minion J, Steingart K, Ramsay A (2010) New and improved tuberculosis diagnostics: evidence, policy, practice, and impact. Current Opinion in Pulmonary Medicine 16: 271-284.