This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Yuan, Y.
Right arrow Articles by Barry, C. E.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Yuan, Y.
Right arrow Articles by Barry, C. E., 3rd

 Previous Article  |  Next Article 

J. Bacteriol., 08 1996, 4484-4492, Vol 178, No. 15
Copyright © 1996, American Society for Microbiology

Stationary phase-associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial alpha-crystallin homolog

Y Yuan, DD Crane and CE Barry 3rd
Tuberculosis Research Unit, Laboratory of Intracellular Parasites, National Institutes for Allergy and Infectious Diseases, Rocky Mountain Laboratories, Hamilton, Montana 59840, USA.

The majority of active tuberculosis cases arise as a result of reactivation of latent organisms which are quiescent within the host. The ability of mycobacteria to survive extended periods without active replication is a complex process whose details await elucidation. We used two-dimensional gel electrophoresis to examine both steady-state protein composition and time-dependent protein synthetic profiles in aging cultures of virulent Mycobacterium tuberculosis. At least seven proteins were maximally synthesized 1 to 2 weeks following the end of log-phase growth. One of these proteins accumulated to become a predominant stationary-phase protein. N-terminal amino acid sequencing and immunoreactivity identified this protein as the 16-kDa alpha- crystallin-like small heat shock protein. The gene for this protein was shown to be limited to the slowly growing M. tuberculosis complex of organisms as assessed by Southern blotting. Overexpression of this protein in wild-type M. tuberculosis resulted in a slower decline in viability following the end of log-phase growth. Accumulation of this protein was observed in log-phase cultures following a shift to oxygen- limiting conditions but not by other external stimuli. The protein was purified to homogeneity from overexpressing M. smegmatis in two steps and shown to have a significant ability to suppress the thermal denaturation of alcohol dehydrogenase. Collectively, these results suggest that the mycobacterial alpha-crystallin protein may play a role in enhancing long-term protein stability and therefore long-term survival of M. tuberculosis.


This article has been cited by other articles:

  • Lin, M. Y., Reddy, T. B. K., Arend, S. M., Friggen, A. H., Franken, K. L. M. C., van Meijgaarden, K. E., Verduyn, M. J. C., Schoolnik, G. K., Klein, M. R., Ottenhoff, T. H. M. (2009). Cross-Reactive Immunity to Mycobacterium tuberculosis DosR Regulon-Encoded Antigens in Individuals Infected with Environmental, Nontuberculous Mycobacteria. Infect. Immun. 77: 5071-5079 [Abstract] [Full Text]  
  • Honaker, R. W., Leistikow, R. L., Bartek, I. L., Voskuil, M. I. (2009). Unique Roles of DosT and DosS in DosR Regulon Induction and Mycobacterium tuberculosis Dormancy. Infect. Immun. 77: 3258-3263 [Abstract] [Full Text]  
  • Black, G. F., Thiel, B. A., Ota, M. O., Parida, S. K., Adegbola, R., Boom, W. H., Dockrell, H. M., Franken, K. L. M. C., Friggen, A. H., Hill, P. C., Klein, M. R., Lalor, M. K., Mayanja, H., Schoolnik, G., Stanley, K., Weldingh, K., Kaufmann, S. H. E., Walzl, G., Ottenhoff, T. H. M., and the GCGH Biomarkers for TB Consortium, (2009). Immunogenicity of Novel DosR Regulon-Encoded Candidate Antigens of Mycobacterium tuberculosis in Three High-Burden Populations in Africa. CVI 16: 1203-1212 [Abstract] [Full Text]  
  • Vasudeva-Rao, H. M., McDonough, K. A. (2008). Expression of the Mycobacterium tuberculosis acr-Coregulated Genes from the DevR (DosR) Regulon Is Controlled by Multiple Levels of Regulation. Infect. Immun. 76: 2478-2489 [Abstract] [Full Text]  
  • Pang, X., Howard, S. T. (2007). Regulation of the {alpha}-Crystallin Gene acr2 by the MprAB Two-Component System of Mycobacterium tuberculosis. J. Bacteriol. 189: 6213-6221 [Abstract] [Full Text]  
  • Sireci, G., Dieli, F., Di Liberto, D., Buccheri, S., La Manna, M. P., Scarpa, F., Macaluso, P., Romano, A., Titone, L., Di Carlo, P., Singh, M., Ivanyi, J., Salerno, A. (2007). Anti-16-Kilodalton Mycobacterial Protein Immunoglobulin M Levels in Healthy but Purified Protein Derivative-Reactive Children Decrease after Chemoprophylaxis. CVI 14: 1231-1234 [Abstract] [Full Text]  
  • Beste, D. J. V., Laing, E., Bonde, B., Avignone-Rossa, C., Bushell, M. E., McFadden, J. J. (2007). Transcriptomic Analysis Identifies Growth Rate Modulation as a Component of the Adaptation of Mycobacteria to Survival inside the Macrophage. J. Bacteriol. 189: 3969-3976 [Abstract] [Full Text]  
  • Dubaniewicz, A., Dubaniewicz-Wybieralska, M., Sternau, A., Zwolska, Z., Izycka-Swieszewska, E., Augustynowicz-Kopec, E., Skokowski, J., Singh, M., Zimnoch, L. (2006). Mycobacterium tuberculosis Complex and Mycobacterial Heat Shock Proteins in Lymph Node Tissue from Patients with Pulmonary Sarcoidosis.. J. Clin. Microbiol. 44: 3448-3451 [Abstract] [Full Text]  
  • Kashino, S. S., Ovendale, P., Izzo, A., Campos-Neto, A. (2006). Unique model of dormant infection for tuberculosis vaccine development.. CVI 13: 1014-1021 [Abstract] [Full Text]  
  • Sharma, K., Gupta, M., Pathak, M., Gupta, N., Koul, A., Sarangi, S., Baweja, R., Singh, Y. (2006). Transcriptional Control of the Mycobacterial embCAB Operon by PknH through a Regulatory Protein, EmbR, In Vivo.. J. Bacteriol. 188: 2936-2944 [Abstract] [Full Text]  
  • Hu, Y., Movahedzadeh, F., Stoker, N. G., Coates, A. R. M. (2006). Deletion of the Mycobacterium tuberculosis {alpha}-Crystallin-Like hspX Gene Causes Increased Bacterial Growth In Vivo. Infect. Immun. 74: 861-868 [Abstract] [Full Text]  
  • Demissie, A., Leyten, E. M. S., Abebe, M., Wassie, L., Aseffa, A., Abate, G., Fletcher, H., Owiafe, P., Hill, P. C., Brookes, R., Rook, G., Zumla, A., Arend, S. M., Klein, M., Ottenhoff, T. H. M., Andersen, P., Doherty, T. M., the VACSEL Study Group, (2006). Recognition of Stage-Specific Mycobacterial Antigens Differentiates between Acute and Latent Infections with Mycobacterium tuberculosis. CVI 13: 179-186 [Abstract] [Full Text]  
  • Stewart, J. N., Rivera, H. N., Karls, R., Quinn, F. D., Roman, J., Rivera-Marrero, C. A. (2006). Increased pathology in lungs of mice after infection with an {alpha}-crystallin mutant of Mycobacterium tuberculosis: changes in cathepsin proteases and certain cytokines. Microbiology 152: 233-244 [Abstract] [Full Text]  
  • Saha, A., Sharma, A., Dhar, A., Bhattacharyya, B., Roy, S., Das Gupta, S. K. (2005). Antagonists of Hsp16.3, a Low-Molecular-Weight Mycobacterial Chaperone and Virulence Factor, Derived from Phage-Displayed Peptide Libraries. Appl. Environ. Microbiol. 71: 7334-7344 [Abstract] [Full Text]  
  • Doherty, T. M., Andersen, P. (2005). Vaccines for Tuberculosis: Novel Concepts and Recent Progress. Clin. Microbiol. Rev. 18: 687-702 [Abstract] [Full Text]  
  • Kennaway, C. K., Benesch, J. L. P., Gohlke, U., Wang, L., Robinson, C. V., Orlova, E. V., Saibi, H. R., Keep, N. H. (2005). Dodecameric Structure of the Small Heat Shock Protein Acr1 from Mycobacterium tuberculosis. J. Biol. Chem. 280: 33419-33425 [Abstract] [Full Text]  
  • Dahl, J. L., Arora, K., Boshoff, H. I., Whiteford, D. C., Pacheco, S. A., Walsh, O. J., Lau-Bonilla, D., Davis, W. B., Garza, A. G. (2005). The relA Homolog of Mycobacterium smegmatis Affects Cell Appearance, Viability, and Gene Expression. J. Bacteriol. 187: 2439-2447 [Abstract] [Full Text]  
  • Wilkinson, K. A., Stewart, G. R., Newton, S. M., Vordermeier, H. M., Wain, J. R., Murphy, H. N., Horner, K., Young, D. B., Wilkinson, R. J. (2005). Infection Biology of a Novel {alpha}-Crystallin of Mycobacterium tuberculosis: Acr2. J. Immunol. 174: 4237-4243 [Abstract] [Full Text]  
  • Starck, J., Kallenius, G., Marklund, B.-I., Andersson, D. I., Akerlund, T. (2004). Comparative proteome analysis of Mycobacterium tuberculosis grown under aerobic and anaerobic conditions. Microbiology 150: 3821-3829 [Abstract] [Full Text]  
  • Karakousis, P. C., Yoshimatsu, T., Lamichhane, G., Woolwine, S. C., Nuermberger, E. L., Grosset, J., Bishai, W. R. (2004). Dormancy Phenotype Displayed by Extracellular Mycobacterium tuberculosis within Artificial Granulomas in Mice. JEM 200: 647-657 [Abstract] [Full Text]  
  • Preneta, R., Papavinasasundaram, K. G., Cozzone, A. J., Duclos, B. (2004). Autophosphorylation of the 16 kDa and 70 kDa antigens (Hsp 16{middle dot}3 and Hsp 70) of Mycobacterium tuberculosis. Microbiology 150: 2135-2141 [Abstract] [Full Text]  
  • Roberts, D. M., Liao, R. P., Wisedchaisri, G., Hol, W. G. J., Sherman, D. R. (2004). Two Sensor Kinases Contribute to the Hypoxic Response of Mycobacterium tuberculosis. J. Biol. Chem. 279: 23082-23087 [Abstract] [Full Text]  
  • Whittington, R. J., Marshall, D. J., Nicholls, P. J., Marsh, I. B., Reddacliff, L. A. (2004). Survival and Dormancy of Mycobacterium avium subsp. paratuberculosis in the Environment. Appl. Environ. Microbiol. 70: 2989-3004 [Abstract] [Full Text]  
  • Timm, J., Post, F. A., Bekker, L.-G., Walther, G. B., Wainwright, H. C., Manganelli, R., Chan, W.-T., Tsenova, L., Gold, B., Smith, I., Kaplan, G., McKinney, J. D. (2003). Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proc. Natl. Acad. Sci. USA 100: 14321-14326 [Abstract] [Full Text]  
  • Kumar, A., Bose, M., Brahmachari, V. (2003). Analysis of Expression Profile of Mammalian Cell Entry (mce) Operons of Mycobacterium tuberculosis. Infect. Immun. 71: 6083-6087 [Abstract] [Full Text]  
  • Voskuil, M. I., Schnappinger, D., Visconti, K. C., Harrell, M. I., Dolganov, G. M., Sherman, D. R., Schoolnik, G. K. (2003). Inhibition of Respiration by Nitric Oxide Induces a Mycobacterium tuberculosis Dormancy Program. JEM 198: 705-713 [Abstract] [Full Text]  
  • Florczyk, M. A., McCue, L. A., Purkayastha, A., Currenti, E., Wolin, M. J., McDonough, K. A. (2003). A Family of acr-Coregulated Mycobacterium tuberculosis Genes Shares a Common DNA Motif and Requires Rv3133c (dosR or devR) for Expression. Infect. Immun. 71: 5332-5343 [Abstract] [Full Text]  
  • Smith, I. (2003). Mycobacterium tuberculosis Pathogenesis and Molecular Determinants of Virulence. Clin. Microbiol. Rev. 16: 463-496 [Abstract] [Full Text]  
  • Shi, L., Jung, Y.-J., Tyagi, S., Gennaro, M. L., North, R. J. (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 [Abstract] [Full Text]  
  • Boon, C., Dick, T. (2002). Mycobacterium bovis BCG Response Regulator Essential for Hypoxic Dormancy. J. Bacteriol. 184: 6760-6767 [Abstract] [Full Text]  
  • Haile, Y., Bjune, G., Wiker, H. G. (2002). Expression of the mceA, esat-6 and hspX genes in Mycobacterium tuberculosis and their responses to aerobic conditions and to restricted oxygen supply. Microbiology 148: 3881-3886 [Abstract] [Full Text]  
  • Stewart, G. R., Wernisch, L., Stabler, R., Mangan, J. A., Hinds, J., Laing, K. G., Young, D. B., Butcher, P. D. (2002). Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148: 3129-3138 [Abstract] [Full Text]  
  • Rosenkrands, I., Slayden, R. A., Crawford, J., Aagaard, C., Barry, C. E., I., Andersen, P. (2002). Hypoxic Response of Mycobacterium tuberculosis Studied by Metabolic Labeling and Proteome Analysis of Cellular and Extracellular Proteins. J. Bacteriol. 184: 3485-3491 [Abstract] [Full Text]  
  • Shleeva, M. O., Bagramyan, K., Telkov, M. V., Mukamolova, G. V., Young, M., Kell, D. B., Kaprelyants, A. S. (2002). Formation and resuscitation of 'non-culturable' cells of Rhodococcus rhodochrous and Mycobacterium tuberculosis in prolonged stationary phase. Microbiology 148: 1581-1591 [Abstract] [Full Text]  
  • Raja, A., Uma Devi, K. R., Ramalingam, B., Brennan, P. J. (2002). Immunoglobulin G, A, and M Responses in Serum and Circulating Immune Complexes Elicited by the 16-Kilodalton Antigen of Mycobacterium tuberculosis. CVI 9: 308-312 [Abstract] [Full Text]  
  • Narberhaus, F. (2002). {alpha}-Crystallin-Type Heat Shock Proteins: Socializing Minichaperones in the Context of a Multichaperone Network. Microbiol. Mol. Biol. Rev. 66: 64-93 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • DesJardin, L. E., Hayes, L. G., Sohaskey, C. D., Wayne, L. G., Eisenach, K. D. (2001). Microaerophilic Induction of the Alpha-Crystallin Chaperone Protein Homologue (hspX) mRNA of Mycobacterium tuberculosis. J. Bacteriol. 183: 5311-5316 [Abstract] [Full Text]  
  • Dahl, J. L., Wei, J., Moulder, J. W., Laal, S., Friedman, R. L. (2001). Subcellular Localization of the Intracellular Survival-Enhancing Eis Protein of Mycobacterium tuberculosis. Infect. Immun. 69: 4295-4302 [Abstract] [Full Text]  
  • Sherman, D. R., Voskuil, M., Schnappinger, D., Liao, R., Harrell, M. I., Schoolnik, G. K. (2001). Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha -crystallin. Proc. Natl. Acad. Sci. USA 98: 7534-7539 [Abstract] [Full Text]  
  • Boon, C., Li, R., Qi, R., Dick, T. (2001). Proteins of Mycobacterium bovis BCG Induced in the Wayne Dormancy Model. J. Bacteriol. 183: 2672-2676 [Abstract] [Full Text]  
  • Monahan, I. M., Betts, J., Banerjee, D. K., Butcher, P. D. (2001). Differential expression of mycobacterial proteins following phagocytosis by macrophages. Microbiology 147: 459-471 [Abstract] [Full Text]  
  • Keer, J., Smeulders, M. J., Williams, H. D. (2001). A purF mutant of Mycobacterium smegmatis has impaired survival during oxygen-starved stationary phase. Microbiology 147: 473-481 [Abstract] [Full Text]  
  • Betts, J. C., Dodson, P., Quan, S., Lewis, A. P., Thomas, P. J., Duncan, K., McAdam, R. A. (2000). Comparison of the proteome of Mycobacterium tuberculosis strain H37Rv with clinical isolate CDC 1551. Microbiology 146: 3205-3216 [Abstract] [Full Text]  
  • Hu, Y., Mangan, J. A., Dhillon, J., Sole, K. M., Mitchison, D. A., Butcher, P. D., Coates, A. R. M. (2000). Detection of mRNA Transcripts and Active Transcription in Persistent Mycobacterium tuberculosis Induced by Exposure to Rifampin or Pyrazinamide. J. Bacteriol. 182: 6358-6365 [Abstract] [Full Text]  
  • Primm, T. P., Andersen, S. J., Mizrahi, V., Avarbock, D., Rubin, H., Barry, C. E. III (2000). The Stringent Response of Mycobacterium tuberculosis Is Required for Long-Term Survival. J. Bacteriol. 182: 4889-4898 [Abstract] [Full Text]  
  • Keer, J., Smeulders, M. J., Gray, K. M., Williams, H. D. (2000). Mutants of Mycobacterium smegmatis impaired in stationary-phase survival. Microbiology 146: 2209-2217 [Abstract] [Full Text]  
  • Maeda, T., Yoshinaga, I., Shiba, T., Murakami, M., Wada, A., Ishida, Y. (2000). Cloning and Sequencing of the Gene Encoding an Aldehyde Dehydrogenase That Is Induced by Growing Alteromonas sp. Strain KE10 in a Low Concentration of Organic Nutrients. Appl. Environ. Microbiol. 66: 1883-1889 [Abstract] [Full Text]  
  • De Voss, J. J., Rutter, K., Schroeder, B. G., Su, H., Zhu, Y., Barry, C. E. III (2000). The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc. Natl. Acad. Sci. USA 97: 1252-1257 [Abstract] [Full Text]  
  • Manabe, Y. C., Chen, J. M., Ko, C. G., Chen, P., Bishai, W. R. (1999). Conditional Sigma Factor Expression, Using the Inducible Acetamidase Promoter, Reveals that the Mycobacterium tuberculosis sigF Gene Modulates Expression of the 16-Kilodalton Alpha-Crystallin Homologue. J. Bacteriol. 181: 7629-7633 [Abstract] [Full Text]  
  • Kartmann, B., Stengler, S., Niederweis, M. (1999). Porins in the Cell Wall of Mycobacterium tuberculosis. J. Bacteriol. 181: 6543-6546 [Abstract] [Full Text]  
  • Couture, M., Yeh, S.-R., Wittenberg, B. A., Wittenberg, J. B., Ouellet, Y., Rousseau, D. L., Guertin, M. (1999). A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 96: 11223-11228 [Abstract] [Full Text]  
  • Hu, Y., Butcher, P. D., Mangan, J. A., Rajandream, M.-A., Coates, A. R. M. (1999). Regulation of hmp Gene Transcription in Mycobacterium tuberculosis: Effects of Oxygen Limitation and Nitrosative and Oxidative Stress. J. Bacteriol. 181: 3486-3493 [Abstract] [Full Text]  
  • Lim, A., Eleuterio, M., Hutter, B., Murugasu-Oei, B., Dick, T. (1999). Oxygen Depletion-Induced Dormancy in Mycobacterium bovis BCG. J. Bacteriol. 181: 2252-2256 [Abstract] [Full Text]  
  • Berengian, A. R., Parfenova, M., Mchaourab, H. S. (1999). Site-directed Spin Labeling Study of Subunit Interactions in the alpha -Crystallin Domain of Small Heat-shock Proteins. COMPARISON OF THE OLIGOMER SYMMETRY IN alpha A-CRYSTALLIN, HSP 27, and HSP 16.3. J. Biol. Chem. 274: 6305-6314 [Abstract] [Full Text]  
  • Hu, Y., Coates, A. R. M. (1999). Transcription of the Stationary-Phase-Associated hspX Gene of Mycobacterium tuberculosis Is Inversely Related to Synthesis of the 16-Kilodalton Protein. J. Bacteriol. 181: 1380-1387 [Abstract] [Full Text]  
  • Münchbach, M., Nocker, A., Narberhaus, F. (1999). Multiple Small Heat Shock Proteins in Rhizobia. J. Bacteriol. 181: 83-90 [Abstract] [Full Text]  
  • Wong, D. K., Lee, B.-Y., Horwitz, M. A., Gibson, B. W. (1999). Identification of Fur, Aconitase, and Other Proteins Expressed by Mycobacterium tuberculosis under Conditions of Low and High Concentrations of Iron by Combined Two-Dimensional Gel Electrophoresis and Mass Spectrometry. Infect. Immun. 67: 327-336 [Abstract] [Full Text]  
  • Garbe, T. R., Hibler, N. S., Deretic, V. (1999). Response to Reactive Nitrogen Intermediates in Mycobacterium tuberculosis: Induction of the 16-Kilodalton alpha -Crystallin Homolog by Exposure to Nitric Oxide Donors. Infect. Immun. 67: 460-465 [Abstract] [Full Text]  
  • Smeulders, M. J., Keer, J., Speight, R. A., Williams, H. D. (1999). Adaptation of Mycobacterium smegmatis to Stationary Phase. J. Bacteriol. 181: 270-283 [Abstract] [Full Text]  
  • Yuan, Y., Crane, D. D., Simpson, R. M., Zhu, Y., Hickey, M. J., Sherman, D. R., Barry, C. E. III (1998). The 16-kDa alpha -crystallin (Acr) protein of Mycobacterium tuberculosis is required for growth in macrophages. Proc. Natl. Acad. Sci. USA 95: 9578-9583 [Abstract] [Full Text]  
  • Horvath, I., Glatz, A., Varvasovszki, V., Torok, Z., Pali, T., Balogh, G., Kovacs, E., Nadasdi, L., Benko, S., Joo, F., Vigh, L. (1998). Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: Identification of hsp17 as a "fluidity gene". Proc. Natl. Acad. Sci. USA 95: 3513-3518 [Abstract] [Full Text]  
  • Cunningham, A. F., Spreadbury, C. L. (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 [Abstract] [Full Text]