Understanding the biology of 16 kDa antigen of Mycobacterium tuberculosis: Scope in diagnosis, vaccine design and therapy

References

• Agrewala JN, Deacock S, Jurcevic S, Wilkinson R. (1997). Peptide recognition by T-cell clones of an HLA-DRB1*1501/*0901 heterozygous donor is promiscuous only between parental alleles. Hum Immunol, 55, 34–38.
   PubMed Web of Science ®Google Scholar
• Agrewala JN, Wilkinson RJ. (1998). Differential regulation of Th1 and Th2 cells by p91-110 and p21-40 peptides of the 16-kD α-crystallin antigen of Mycobacterium tuberculosis. Clin Exp Immunol, 114, 392–397.
   PubMed Web of Science ®Google Scholar
• Agrewala JN, Wilkinson RJ. (1999). Influence of HLA-DR on the phenotype of CD4+ T lymphocytes specific for an epitope of the 16-kDa α-crystallin antigen of Mycobacterium tuberculosis. Eur J Immunol, 29, 1753–1761.
   PubMed Web of Science ®Google Scholar
• Bagchi G, Mayuri, Tyagi JS. (2003). Hypoxia-responsive expression of Mycobacterium tuberculosis Rv3134c and devR promoters in Mycobacterium smegmatis. Microbiology (Reading, Engl), 149, 2303–2305.
   Google Scholar
• Balázsi G, Heath AP, Shi L, Gennaro ML. (2008). The temporal response of the Mycobacterium tuberculosis gene regulatory network during growth arrest. Mol Syst Biol, 4, 225.
   PubMed Web of Science ®Google Scholar
• Beck ST, Leite OM, Arruda RS, Ferreira AW. (2005). Humoral response to low molecular weight antigens of Mycobacterium tuberculosis by tuberculosis patients and contacts. Braz J Med Biol Res, 38, 587–596.
   Google Scholar
• Bienz M. (1984). Developmental control of the heat shock response in Xenopus. Proc Natl Acad Sci USA, 81, 3138–3142.
   PubMed Web of Science ®Google Scholar
• Boon C, Dick T. (2002). Mycobacterium bovis BCG response regulator essential for hypoxic dormancy. J Bacteriol, 184, 6760–6767.
   PubMed Web of Science ®Google Scholar
• Burdon RH. (1986). Heat shock and the heat shock proteins. Biochem J, 240, 313–324.
   PubMed Web of Science ®Google Scholar
• Caccamo N, Guggino G, Meraviglia S, Gelsomino G, Di Carlo P, Titone L, Bocchino M, Galati D, Matarese A, Nouta J, Klein MR, Salerno A, Sanduzzi A, Dieli F, Ottenhoff TH. (2009). Analysis of Mycobacterium tuberculosis-specific CD8 T-cells in patients with active tuberculosis and in individuals with latent infection. PLoS ONE, 4, e5528.
   PubMed Web of Science ®Google Scholar
• Caccamo N, Meraviglia S, Dieli F, Romano A, Titone L, Salerno A. (2005). Th0 to Th1 switch of CD4 T cell clones specific from the 16-kDa antigen of Mycobacterium tuberculosis after successful therapy: lack of involvement of epitope repertoire and HLA-DR. Immunol Lett, 98, 253–258.
   Google Scholar
• Chang Z, Primm TP, Jakana J, Lee IH, Serysheva I, Chiu W, Gilbert HF, Quiocho FA. (1996). Mycobacterium tuberculosis 16-kDa antigen (Hsp16.3) functions as an oligomeric structure in vitro to suppress thermal aggregation. J Biol Chem, 271, 7218–7223.
   PubMed Web of Science ®Google Scholar
• Chen L, Xu M, Wang ZY, Chen BW, Du WX, Su C, Shen XB, Zhao AH, Dong N, Wang YJ, Wang GZ. (2010). The development and preliminary evaluation of a new Mycobacterium tuberculosis vaccine comprising Ag85b, HspX and CFP-10:ESAT-6 fusion protein with CpG DNA and aluminum hydroxide adjuvants. FEMS Immunol Med Microbiol, 59, 42–52.
   PubMedGoogle Scholar
• Cho HY, Cho HJ, Kim YM, Oh JI, Kang BS. (2009). Structural insight into the heme-based redox sensing by DosS from Mycobacterium tuberculosis. J Biol Chem, 284, 13057–13067.
   PubMed Web of Science ®Google Scholar
• Comstock GW, Livesay VT, Woolpert SF. (1974). The prognosis of a positive tuberculin reaction in childhood and adolescence. Am J Epidemiol, 99, 131–138.
   PubMed Web of Science ®Google Scholar
• Cunningham AF, Spreadbury CL. (1998). Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton α-crystallin homolog. J Bacteriol, 180, 801–808.
   PubMed Web of Science ®Google Scholar
• Dasgupta N, Kapur V, Singh KK, Das TK, Sachdeva S, Jyothisri K, Tyagi JS. (2000). Characterization of a two-component system, devR-devS, of Mycobacterium tuberculosis. Tuber Lung Dis, 80, 141–159.
   PubMedGoogle Scholar
• Davidow A, Kanaujia GV, Shi L, Kaviar J, Guo X, Sung N, Kaplan G, Menzies D, Gennaro ML. (2005). Antibody profiles characteristic of Mycobacterium tuberculosis infection state. Infect Immun, 73, 6846–6851.
   PubMed Web of Science ®Google Scholar
• Demissie A, Leyten EM, Abebe M, Wassie L, Aseffa A, Abate G, Fletcher H, Owiafe P, Hill PC, Brookes R, Rook G, Zumla A, Arend SM, Klein M, Ottenhoff TH, Andersen P, Doherty TM; VACSEL Study Group. (2006). Recognition of stage-specific mycobacterial antigens differentiates between acute and latent infections with Mycobacterium tuberculosis. Clin Vaccine Immunol, 13, 179–186.
   PubMed Web of Science ®Google Scholar
• Demkow U, Zielonka TM, Nowak-Misiak M, Filewska M, Bialas B, Strzalkowski J, Rapala K, Zwolska Z, Skopinska-Rozewska E. (2002). Humoral immune response against 38-kDa and 16-kDa mycobacterial antigens in bone and joint tuberculosis. Int J Tuberc Lung Dis, 6, 1023–1028.
   Google Scholar
• Demkow U, Ziólkowski J, Filewska M, Bialas-Chromiec B, Zielonka T, Michalowska-Mitczuk D, Kus J, Augustynowicz E, Zwolska Z, Skopinska-Rózewska E, Rowinska-Zakrzewska E. (2004). Diagnostic value of different serological tests for tuberculosis in Poland. J Physiol Pharmacol, 55 Suppl 3, 57–66.
   Google Scholar
• Geluk A, Lin MY, van Meijgaarden KE, Leyten EM, Franken KL, Ottenhoff TH, Klein MR. (2007). T-cell recognition of the HspX protein of Mycobacterium tuberculosis correlates with latent M. tuberculosis infection but not with M. bovis BCG vaccination. Infect Immun, 75, 2914–2921.
   PubMed Web of Science ®Google Scholar
• Groenen PJ, Merck KB, de Jong WW, Bloemendal H. (1994). Structure and modifications of the junior chaperone α-crystallin. From lens transparency to molecular pathology. Eur J Biochem, 225, 1–19.
   PubMedGoogle Scholar
• Honaker RW, Leistikow RL, Bartek IL, Voskuil MI. (2009). Unique roles of DosT and DosS in DosR regulon induction and Mycobacterium tuberculosis dormancy. Infect Immun, 77, 3258–3263.
   PubMed Web of Science ®Google Scholar
• Hu Y, Movahedzadeh F, Stoker NG, Coates AR. (2006). Deletion of the Mycobacterium tuberculosis α-crystallin-like hspX gene causes increased bacterial growth in vivo. Infect Immun, 74, 861–868.
   PubMed Web of Science ®Google Scholar
• Huygen K, Van Vooren JP, Turneer M, Bosmans R, Dierckx P, De Bruyn J. (1988). Specific lymphoproliferation, γ interferon production, and serum immunoglobulin G directed against a purified 32 kDa mycobacterial protein antigen (P32) in patients with active tuberculosis. Scand J Immunol, 27, 187–194.
   Google Scholar
• Imaz MS, Comini MA, Zerbini E, Sequeira MD, Latini O, Claus JD, Singh M. (2004). Evaluation of commercial enzyme-linked immunosorbent assay kits for detection of tuberculosis in Argentinean population. J Clin Microbiol, 42, 884–887.
   PubMed Web of Science ®Google Scholar
• Imaz MS, Comini MA, Zerbini E, Sequeira MD, Spoletti MJ, Etchart AA, Pagano HJ, Bonifasich E, Diaz N, Claus JD, Singh M. (2001). Evaluation of the diagnostic value of measuring IgG, IgM and IgA antibodies to the recombinant 16-kilodalton antigen of mycobacterium tuberculosis in childhood tuberculosis. Int J Tuberc Lung Dis, 5, 1036–1043.
   Google Scholar
• Jackett PS, Bothamley GH, Batra HV, Mistry A, Young DB, Ivanyi J. (1988). Specificity of antibodies to immunodominant mycobacterial antigens in pulmonary tuberculosis. J Clin Microbiol, 26, 2313–2318.
   PubMed Web of Science ®Google Scholar
• Kennaway CK, Benesch JL, Gohlke U, Wang L, Robinson CV, Orlova EV, Saibil HR, Saibi HR, Keep NH. (2005). Dodecameric structure of the small heat shock protein Acr1 from Mycobacterium tuberculosis. J Biol Chem, 280, 33419–33425.
   PubMedGoogle Scholar
• Khan IH, Ravindran R, Yee J, Ziman M, Lewinsohn DM, Gennaro ML, Flynn JL, Goulding CW, DeRiemer K, Lerche NW, Luciw PA. (2008). Profiling antibodies to Mycobacterium tuberculosis by multiplex microbead suspension arrays for serodiagnosis of tuberculosis. Clin Vaccine Immunol, 15, 433–438.
   Google Scholar
• Kimerling ME, Kluge H, Vezhnina N, Iacovazzi T, Demeulenaere T, Portaels F, Matthys F. (1999). Inadequacy of the current WHO re-treatment regimen in a central Siberian prison: treatment failure and MDR-TB. Int J Tuberc Lung Dis, 3, 451–453.
   PubMed Web of Science ®Google Scholar
• Kong CU, Ng LG, Nambiar JK, Spratt JM, Weninger W, Triccas JA. (2011). Targeted induction of antigen expression within dendritic cells modulates antigen-specific immunity afforded by recombinant BCG. Vaccine, 29, 1374–1381.
   Google Scholar
• Kumar A, Deshane JS, Crossman DK, Bolisetty S, Yan BS, Kramnik I, Agarwal A, Steyn AJ. (2008). Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem, 283, 18032–18039.
   PubMed Web of Science ®Google Scholar
• Kumar A, Toledo JC, Patel RP, Lancaster JR Jr, Steyn AJ. (2007). Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc Natl Acad Sci USA, 104, 11568–11573.
   PubMed Web of Science ®Google Scholar
• Lee BY, Hefta SA, Brennan PJ. (1992). Characterization of the major membrane protein of virulent Mycobacterium tuberculosis. Infect Immun, 60, 2066–2074.
   PubMed Web of Science ®Google Scholar
• Lee BY, Horwitz MA. (1999). T-cell epitope mapping of the three most abundant extracellular proteins of Mycobacterium tuberculosis in outbred guinea pigs. Infect Immun, 67, 2665–2670.
   Google Scholar
• Leyten EM, Lin MY, Franken KL, Friggen AH, Prins C, van Meijgaarden KE, Voskuil MI, Weldingh K, Andersen P, Schoolnik GK, Arend SM, Ottenhoff TH, Klein MR. (2006). Human T-cell responses to 25 novel antigens encoded by genes of the dormancy regulon of Mycobacterium tuberculosis. Microbes Infect, 8, 2052–2060.
   PubMed Web of Science ®Google Scholar
• Li Q, Yu H, Zhang Y, Wang B, Jiang W, et al. (2011). Immunogenicity and protective efficacy of a fusion protein vaccine consisting of antigen Ag85B and HspX against Mycobacterium tuberculosis infection in mice. Scand J Immunol, 73, 568–76.
   PubMed Web of Science ®Google Scholar
• Lyashchenko K, Colangeli R, Houde M, Al Jahdali H, Menzies D, Gennaro ML. (1998). Heterogeneous antibody responses in tuberculosis. Infect Immun, 66, 3936–3940.
   PubMed Web of Science ®Google Scholar
• Mayuri Bagchi, G, Das TK, Tyagi JS. (2002). Molecular analysis of the dormancy response in Mycobacterium smegmatis: expression analysis of genes encoding the DevR-DevS two-component system, Rv3134c and chaperone α-crystallin homologues. FEMS Microbiol Lett, 211, 231–237.
   Google Scholar
• Narberhaus F. (2002). α-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev, 66, 64–93. table of contents.
   PubMed Web of Science ®Google Scholar
• Oftung F, Borka E, Mustafa AS. (1998). Mycobacterium tuberculosis reactive T cell clones from naturally converted PPD-positive healthy subjects: recognition of the M. tuberculosis 16-kDa antigen. FEMS Immunol Med Microbiol, 20, 319–325.
   Google Scholar
• Okuda Y, Maekura R, Hirotani A, Kitada S, Yoshimura K, Hiraga T, Yamamoto Y, Itou M, Ogura T, Ogihara T. (2004). Rapid serodiagnosis of active pulmonary Mycobacterium tuberculosis by analysis of results from multiple antigen-specific tests. J Clin Microbiol, 42, 1136–1141.
   Google Scholar
• Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR. (2003). Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol, 48, 833–843.
   PubMed Web of Science ®Google Scholar
• Preneta R, Papavinasasundaram KG, Cozzone AJ, Duclos B. (2004). Autophosphorylation of the 16 kDa and 70 kDa antigens (Hsp 16.3 and Hsp 70) of Mycobacterium tuberculosis. Microbiology, 150, 2135–2141.
   Google Scholar
• Rabahi MF, Junqueira-Kipnis AP, Dos Reis MC, Oelemann W, Conde MB. (2007). Humoral response to HspX and GlcB to previous and recent infection by Mycobacterium tuberculosis. BMC Infect Dis, 7, 148.
   Google Scholar
• Raja A, Uma Devi KR, Ramalingam B, Brennan PJ. (2002). Immunoglobulin G, A, and M responses in serum and circulating immune complexes elicited by the 16-kilodalton antigen of Mycobacterium tuberculosis. Clin Diagn Lab Immunol, 9, 308–312.
   PubMedGoogle Scholar
• Roberts DM, Liao RP, Wisedchaisri G, Hol WG, Sherman DR. (2004). Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J Biol Chem, 279, 23082–23087.
   PubMed Web of Science ®Google Scholar
• Roupie V, Romano M, Zhang L, Korf H, Lin MY, Franken KL, Ottenhoff TH, Klein MR, Huygen K. (2007). Immunogenicity of eight dormancy regulon-encoded proteins of Mycobacterium tuberculosis in DNA-vaccinated and tuberculosis-infected mice. Infect Immun, 75, 941–949.
   PubMed Web of Science ®Google Scholar
• Russnak RH, Jones D, Candido EP. (1983). Cloning and analysis of cDNA sequences coding for two 16 kilodalton heat shock proteins (hsps) in Caenorhabditis elegans: homology with the small hsps of Drosophila. Nucleic Acids Res, 11, 3187–3205.
   PubMed Web of Science ®Google Scholar
• Senol G, Erer OF, Yalcin YA, Coskun M, Gündüz AT, Biçmen C, Ertas M, Ozkan SA. (2007). Humoral immune response against 38-kDa and 16-kDa mycobacterial antigens in tuberculosis. Eur Respir J, 29, 143–148.
   Google Scholar
• Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK. (2001). Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding α -crystallin. Proc Natl Acad Sci USA, 98, 7534–7539.
   PubMed Web of Science ®Google Scholar
• Shi C, Chen L, Chen Z, Zhang Y, Zhou Z, Lu J, Fu R, Wang C, Fang Z, Fan X. (2010). Enhanced protection against tuberculosis by vaccination with recombinant BCG over-expressing HspX protein. Vaccine, 28, 5237–5244.
   PubMed Web of Science ®Google Scholar
• Silva VM, Kanaujia G, Gennaro ML, Menzies D. (2003). Factors associated with humoral response to ESAT-6, 38 kDa and 14 kDa in patients with a spectrum of tuberculosis. Int J Tuberc Lung Dis, 7, 478–484.
   Google Scholar
• Singh V, Gowthaman U, Jain S, Parihar P, Banskar S, Gupta P, Gupta UD, Agrewala JN. (2010). Coadministration of interleukins 7 and 15 with bacille Calmette-Guérin mounts enduring T cell memory response against Mycobacterium tuberculosis. J Infect Dis, 202, 480–489.
   PubMed Web of Science ®Google Scholar
• Sireci G, Dieli F, Di Liberto D, Buccheri S, La Manna MP, 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. Clin Vaccine Immunol, 14, 1231–1234.
   Google Scholar
• Sousa AO, Salem JI, Lee FK, Verçosa MC, Cruaud P, Bloom BR, Lagrange PH, David HL. (1997). An epidemic of tuberculosis with a high rate of tuberculin anergy among a population previously unexposed to tuberculosis, the Yanomami Indians of the Brazilian Amazon. Proc Natl Acad Sci USA, 94, 13227–13232.
   PubMedGoogle Scholar
• Sousa EH, Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA. (2007). DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Sci, 16, 1708–1719.
   PubMed Web of Science ®Google Scholar
• Spratt JM, Britton WJ, Triccas JA. (2010). In vivo persistence and protective efficacy of the bacille Calmette Guerin vaccine overexpressing the HspX latency antigen. Bioeng Bugs, 1, 61–65.
   PubMedGoogle Scholar
• Stewart GR, Newton SM, Wilkinson KA, Humphreys IR, Murphy HN, Robertson BD, Wilkinson RJ, Young DB. (2005). The stress-responsive chaperone α-crystallin 2 is required for pathogenesis of Mycobacterium tuberculosis. Mol Microbiol, 55, 1127–1137.
   PubMedGoogle Scholar
• Tabira Y, Ohara N, Yamada T. (2000). Identification and characterization of the ribosome-associated protein, HrpA, of Bacillus Calmette-Guérin. Microb Pathog, 29, 213–222.
   Google Scholar
• Tissières A, Mitchell HK, Tracy UM. (1974). Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol, 84, 389–398.
   PubMed Web of Science ®Google Scholar
• Torres M, Mendez-Sampeiro P, Jimenez-Zamudio L, Teran L, Camarena A, Quezada R, Ramos E, Sada E. (1994). Comparison of the immune response against Mycobacterium tuberculosis antigens between a group of patients with active pulmonary tuberculosis and healthy household contacts. Clin Exp Immunol, 96, 75–78.
   Google Scholar
• Van Montfort R, Slingsby C, Vierling E. (2001). Structure and function of the small heat shock protein/α-crystallin family of molecular chaperones. Adv Protein Chem, 59, 105–156.
   PubMedGoogle Scholar
• Verbon A, Hartskeerl RA, Schuitema A, Kolk AH, Young DB, Lathigra R. (1992). The 14,000-molecular-weight antigen of Mycobacterium tuberculosis is related to the α-crystallin family of low-molecular-weight heat shock proteins. J Bacteriol, 174, 1352–1359.
   Google Scholar
• Verbon A, Weverling GJ, Kuijper S, Speelman P, Jansen HM, Kolk AH. (1993). Evaluation of different tests for the serodiagnosis of tuberculosis and the use of likelihood ratios in serology. Am Rev Respir Dis, 148, 378–384.
   PubMedGoogle Scholar
• Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, Sherman DR, Schoolnik GK. (2003). Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med, 198, 705–713.
   PubMed Web of Science ®Google Scholar
• Wayne LG, Lin KY. (1982). Glyoxylate metabolism and adaptation of Mycobacterium tuberculosis to survival under anaerobic conditions. Infect Immun, 37, 1042–1049.
   PubMed Web of Science ®Google Scholar
• Wayne LG, Sohaskey CD. (2001). Nonreplicating persistence of mycobacterium tuberculosis. Annu Rev Microbiol, 55, 139–163.
   PubMed Web of Science ®Google Scholar
• Wayne LG, Sramek HA. (1979). Antigenic differences between extracts of actively replicating and synchronized resting cells of Mycobacterium tuberculosis. Infect Immun, 24, 363–370.
   PubMed Web of Science ®Google Scholar
• Wayne LG. (1994). Dormancy of Mycobacterium tuberculosis and latency of disease. Eur J Clin Microbiol Infect Dis, 13, 908–914.
   PubMed Web of Science ®Google Scholar
• Wayne LG. (2001). In Vitro Model of Hypoxically Induced Nonreplicating Persistence of Mycobacterium tuberculosis. Methods Mol Med, 54, 247–269.
   PubMedGoogle Scholar
• Yamilé López, Daniel Yero, Gustavo Falero-Diaz, Nesty Olivares, María E. Sarmiento, Sergio Sifontes, Rosa L. Solis, Jorge A. Barrios, Diana Aguilar, Rogelio Hernández-Pando, and Armando Acosta. (2009). Induction of a protective response with an IgA monoclonal antibody against Mycobacterium tuberculosis 16 kDa protein in a model of progressive pulmonary infection. International Journal of Medical Microbiology, 299, 447–452.
   Google Scholar
• Wilkinson RJ, Hasløv K, Rappuoli R, Giovannoni F, Narayanan PR, Desai CR, Vordermeier HM, Paulsen J, Pasvol G, Ivanyi J, Singh M. (1997). Evaluation of the recombinant 38-kilodalton antigen of Mycobacterium tuberculosis as a potential immunodiagnostic reagent. J Clin Microbiol, 35, 553–557.
   PubMedGoogle Scholar
• Wilkinson RJ, Wilkinson KA, De Smet KA, Haslov K, Pasvol G, Singh M, Svarcova I, Ivanyi J. (1998). Human T- and B-cell reactivity to the 16kDa α-crystallin protein of Mycobacterium tuberculosis. Scand J Immunol, 48, 403–409.
   Google Scholar
• Yuan Y, Crane DD, Barry CE 3rd. (1996). Stationary phase-associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial α-crystallin homolog. J Bacteriol, 178, 4484–4492.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Crane DD, Simpson RM, Zhu YQ, Hickey MJ, Sherman DR, Barry CE 3rd. (1998). The 16-kDa α-crystallin (Acr) protein of Mycobacterium tuberculosis is required for growth in macrophages. Proc Natl Acad Sci USA, 95, 9578–9583.
   PubMed Web of Science ®Google Scholar