Challenging Mycobacterium tuberculosis dormancy mechanisms and their immunodiagnostic potential

Brazilian Journal of Infectious Diseases

Volumn 19, Issue 6, 2015, Pages 636-642

  Chaves, Alexandre Silva ^a   Rodrigues, Michele Fernandes ^a   Mattos, Ana Márcia Menezes ^a   Teixeira, Henrique Couto ^a  

^a FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

Author keywords

Diagnosis; DosR antigens; Latency; Tuberculosis

Indexed keywords

DORMANCY SURVIVAL REGULATOR ANTIGEN; MYCOBACTERIUM ANTIGEN; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; DOSR PROTEIN, MYCOBACTERIUM TUBERCULOSIS; DOST PROTEIN, MYCOBACTERIUM TUBERCULOSIS; PROTEIN KINASE;

BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRUCTURES; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; GOLD STANDARD; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPROMISED PATIENT; INTERFERON GAMMA RELEASE ASSAY; MOLECULAR BIOLOGY; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS TEST KIT; NONHUMAN; PRACTICE GUIDELINE; REGULON; SENSITIVITY AND SPECIFICITY; SERODIAGNOSIS; SHORT SURVEY; TUBERCULIN TEST; TUBERCULOSIS; GENETICS; HOST PATHOGEN INTERACTION; IMMUNE EVASION; IMMUNOLOGICAL PROCEDURES; IMMUNOLOGY; LATENT TUBERCULOSIS; MICROBIOLOGY; PHYSIOLOGY;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNOLOGIC TESTS; LATENT TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; PROTEIN KINASES;

EID: 84949092167     PISSN: 14138670     EISSN: 16784391     Source Type: Journal    
DOI: 10.1016/j.bjid.2015.08.004     Document Type: Short Survey

References (69)

1. World Health Organization, WHO Global Tuberculosis Report 2014 2014, WHO, Geneva, Switzerland, http://www.who.int/tb/publications/global_report/gtbr14_main_text.pdf [accessed 20.03.15].
2. Baena A., Porcelli S.A. Evasion and subversion of antigen presentation by Mycobacterium tuberculosis. Tissue Antigens 2009, 74:189-204.
3. Tufariello J.M., Chan J., Flynn J.L. Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect Dis 2003, 3:578-590.
4. Koul A., Arnoult E., Lounis N., Guillemont J., Andries K. The challenge of new drug discovery for tuberculosis. Nature 2011, 469:483-490.
5. Lin P.L., Flynn J.L. Understanding latent tuberculosis: a moving target. J Immunol 2010, 185:15-22.
6. Kizza F.N., List J., Nkwata A.K., et al. Prevalence of latent tuberculosis infection and associated risk factors in an urban African setting. BMC Infect Dis 2015, 15:165.
7. Fox G.J., Barry S.E., Britton W.J., Marks G.B. Contact investigation for tuberculosis: a systematic review and meta-analysis. Eur Respir J 2013, 41:140-156.
8. Dheda K., van Zyl Smit R., Badri M., Pai M. T-cell interferon-gamma release assays for the rapid immunodiagnosis of tuberculosis: clinical utility in high-burden vs. low-burden settings. Curr Opin Pulm Med 2009, 15:188-200.
9. Joshi R., Reingold A.L., Menzies D., Pai M. Tuberculosis among health-care workers in low- and middle-income countries: a systematic review. PLoS Med 2006, 3:e494.
10. Legesse M., Ameni G., Mamo G., Medhin G., Bjune G., Abebe F. Community-based cross-sectional survey of latent tuberculosis infection in Afar pastoralists, Ethiopia, using QuantiFERON-TB Gold In-Tube and tuberculin skin test. BMC Infect Dis 2011, 11:89.
11. Lalvani A., Millington K.A. T cell-based diagnosis of childhood tuberculosis infection. Curr Opin Infect Dis 2007, 20:264-271.
12. Brock I., Munk M.E., Kok-Jensen A., Andersen P. Performance of whole blood IFN-gamma test for tuberculosis diagnosis based on PPD or the specific antigens ESAT-6 and CFP-10. Int J Tuberc Lung Dis 2001, 5:462-467.
13. Lalvani A., Pareek M. Interferon gamma release assays: principles and practice. Enferm Infecc Microbiol Clin 2010, 28:245-252.
14. Redelman-Sidi G., Sepkowitz K.A. IFN-gamma release assays in the diagnosis of latent tuberculosis infection among immunocompromised adults. Am J Respir Crit Care Med 2013, 188:422-431.
15. Sester M., Sester U., Clauer P., et al. Tuberculin skin testing underestimates a high prevalence of latent tuberculosis infection in hemodialysis patients. Kidney Int 2004, 65:1826-1834.
16. Pai M., Zwerling A., Menzies D. Systematic review: T-cell-based assays for the diagnosis of latent tuberculosis infection: an update. Ann Intern Med 2008, 149:177-184.
17. Diel R., Goletti D., Ferrara G., et al. Interferon-gamma release assays for the diagnosis of latent Mycobacterium tuberculosis infection: a systematic review and meta-analysis. Eur Respir J 2011, 37:88-99.
18. Pai M., Banaei N. Occupational screening of health care workers for tuberculosis infection: tuberculin skin testing or interferon-gamma release assays?. Occup Med (Lond) 2013, 63:458-460.
19. Chao J.D., Papavinasasundaram K.G., Zheng X., et al. Convergence of Ser/Thr and two-component signaling to coordinate expression of the dormancy regulon in Mycobacterium tuberculosis. J Biol Chem 2010, 285:29239-29246.
20. Wayne L.G., Sohaskey C.D. Nonreplicating persistence of Mycobacterium tuberculosis. Annu Rev Microbiol 2001, 55:139-163.
21. Kumar A., Deshane J.S., Crossman D.K., et al. Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 2008, 283:18032-18039.
22. Taneja N.K., Dhingra S., Mittal A., Naresh M., Tyagi J.S. Mycobacterium tuberculosis transcriptional adaptation, growth arrest and dormancy phenotype development is triggered by vitamin C. PLoS ONE 2010, 5:e10860.
23. Bartek I.L., Rutherford R., Gruppo V., et al. The DosR regulon of M. tuberculosis and antibacterial tolerance. Tuberculosis (Edinb) 2009, 89:310-316.
24. Majumdar S.D., Vashist A., Dhingra S., et al. Appropriate DevR (DosR)-mediated signaling determines transcriptional response, hypoxic viability and virulence of Mycobacterium tuberculosis. PLoS ONE 2012, 7:e35847.
25. Chauhan S., Sharma D., Singh A., Surolia A., Tyagi J.S. Comprehensive insights into Mycobacterium tuberculosis DevR (DosR) regulon activation switch. Nucleic Acids Res 2011, 39:7400-7414.
26. Via L.E., Lin P.L., Ray S.M., et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 2008, 76:2333-2340.
27. Wayne L.G., Hayes L.G. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 1996, 64:2062-2069.
28. Sohaskey C.D. Nitrate enhances the survival of Mycobacterium tuberculosis during inhibition of respiration. J Bacteriol 2008, 190:2981-2986.
29. Cho H.Y., Cho H.J., Kim Y.M., Oh J.I., Kang B.S. Structural Insight into the Heme-based Redox Sensing by DosS from Mycobacterium tuberculosis. J Biol Chem 2009, 284:13057-13067.
30. Leistikow R.L., Morton R.A., Bartek I.L., Frimpong I., Wagner K., Voskuil M.I. The Mycobacterium tuberculosis DosR regulon assists in metabolic homeostasis and enables rapid recovery from nonrespiring dormancy. J Bacteriol 2010, 192:1662-1670.
31. Park H-D., Guinn K.M., Harrell M.I., et al. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 2003, 48:833-843.
32. Rustad T.R., Harrell M.I., Liao R., Sherman D.R. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE 2008, 3:e1502.
33. Bold T.D., Banaei N., Wolf A.J., Ernst J.D. Suboptimal activation of antigen-specific CD4+ effector cells enables persistence of M. tuberculosis in vivo. PLoS Pathog 2011, 7:e1002063.
34. Jung Y.J., LaCourse R., Ryan L., North R.J. Virulent but not avirulent Mycobacterium tuberculosis can evade the growth inhibitory action of a T helper 1-dependent, nitric oxide Synthase 2-independent defense in mice. J Exp Med 2002, 196:991-998.
35. Mehra S., Foreman T.W., Didier P.J., et al. The DosR regulon modulates adaptive immunity and is essential for Mycobacterium tuberculosis persistence. Am J Respir Crit Care Med 2015, 191:1185-1196.
36. Mariotti S., Pardini M., Gagliardi M.C., et al. Dormant Mycobacterium tuberculosis fails to block phagosome maturation and shows unexpected capacity to stimulate specific human T lymphocytes. J Immunol 2013, 191:274-282.
37. Venkatasubramanian S., Dhiman R., Paidipally P., et al. A rho GDP dissociation inhibitor produced by apoptotic T-cells inhibits growth of Mycobacterium tuberculosis. PLoS Pathog 2015, 11:e1004617.
38. Ryndak M.B., Singh K.K., Peng Z., Laal S. Transcriptional profile of Mycobacterium tuberculosis replicating in type II alveolar epithelial cells. PLoS ONE 2015, 10:e0123745.
39. Ehlers S. Lazy, dynamic or minimally recrudescent? On the elusive nature and location of the mycobacterium responsible for latent tuberculosis. Infection 2009, 37:87-95.
40. Gengenbacher M., Kaufmann S.H. Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev 2012, 36:514-532.
41. Gideon H.P., Flynn J.L. Latent tuberculosis: what the host sees?. Immunol Res 2011, 50:202-212.
42. Chegou N.N., Hoek K.G., Kriel M., Warren R.M., Victor T.C., Walzl G. Tuberculosis assays: past, present and future. Expert Rev Anti Infect Ther 2011, 9:457-469.
43. Trebucq A., Enarson D.A., Chiang C.Y., et al. Xpert(R) MTB/RIF for national tuberculosis programmes in low-income countries: when, where and how?. Int J Tuberc Lung Dis 2011, 15:1567-1572.
44. Hu Y., Coates A.R. Transcription of the stationary-phase-associated hspX gene of Mycobacterium tuberculosis is inversely related to synthesis of the 16-kilodalton protein. J Bacteriol 1999, 181:1380-1387.
45. Demissie A., Leyten E.M., Abebe M., et al. Recognition of stage-specific mycobacterial antigens differentiates between acute and latent infections with Mycobacterium tuberculosis. Clin Vaccine Immunol 2006, 13:179-186.
46. Goletti D., Butera O., Vanini V., et al. Response to Rv2628 latency antigen associates with cured tuberculosis and remote infection. Eur Respir J 2010, 36:135-142.
47. Leyten E.M., Lin M.Y., Franken K.L., et al. Human T-cell responses to 25 novel antigens encoded by genes of the dormancy regulon of Mycobacterium tuberculosis. Microbes Infect 2006, 8:2052-2060.
48. Lin M.Y., Geluk A., Smith S.G., et al. Lack of immune responses to Mycobacterium tuberculosis DosR regulon proteins following Mycobacterium bovis BCG vaccination. Infect Immun 2007, 75:3523-3530.
49. Schuck S.D., Mueller H., Kunitz F., et al. Identification of T-cell antigens specific for latent Mycobacterium tuberculosis infection. PLoS ONE 2009, 4:e5590.
50. Commandeur S., Lin M.Y., van Meijgaarden K.E., et al. Double- and monofunctional CD4(+) and CD8(+) T-cell responses to Mycobacterium tuberculosis DosR antigens and peptides in long-term latently infected individuals. Eur J Immunol 2011, 41:2925-2936.
51. Adekambi T., Ibegbu C.C., Kalokhe A.S., Yu T., Ray S.M., Rengarajan J. Distinct effector memory CD4+ T cell signatures in latent Mycobacterium tuberculosis infection, BCG vaccination and clinically resolved tuberculosis. PLoS ONE 2012, 7:e36046.
52. Caccamo N., Guggino G., Joosten S.A., et al. Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol 2010, 40:2211-2220.
53. Seder R.A., Darrah P.A., Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008, 8:247-258.
54. Chowdhury I.H., Ahmed A.M., Choudhuri S., et al. Alteration of serum inflammatory cytokines in active pulmonary tuberculosis following anti-tuberculosis drug therapy. Mol Immunol 2014, 62:159-168.
55. Raja A., Uma Devi K.R., Ramalingam B., Brennan P.J., 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 2002, 9:308-312.
56. Rabahi M.F., Junqueira-Kipnis A.P., Dos Reis M.C., Oelemann W., Conde M.B. Humoral response to HspX and GlcB to previous and recent infection by Mycobacterium tuberculosis. BMC Infect Dis 2007, 7:148.
57. Mattos A.M., Almeida C.deS., Franken K.L., et al. Increased IgG1, IFN-gamma, TNF-alpha and IL-6 responses to Mycobacterium tuberculosis antigens in patients with tuberculosis are lower after chemotherapy. Int Immunol 2010, 22:775-782.
58. de Souza F.M., do Prado T.N., Pinheiro J.dosS., et al. Comparison of interferon-gamma release assay to two cut-off points of tuberculin skin test to detect latent Mycobacterium tuberculosis infection in primary health care workers. PLoS ONE 2014, 9:e102773.
59. Belay M., Legesse M., Mihret A., et al. Pro- and anti-inflammatory cytokines against Rv2031 are elevated during latent tuberculosis: a study in cohorts of tuberculosis patients, household contacts and community controls in an endemic setting. PLoS ONE 2015, 10:e0124134.
60. Caws M., Thwaites G., Dunstan S., et al. The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog 2008, 4:e1000034.
61. Garton N.J., Waddell S.J., Sherratt A.L., et al. Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med 2008, 5:e75.
62. Lin P.L., Rodgers M., Smith L., et al. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect Immun 2009, 77:4631-4642.
63. Arlehamn C.S., Sidney J., Henderson R., et al. Dissecting mechanisms of immunodominance to the common tuberculosis antigens ESAT-6, CFP10, Rv2031c (hspX), Rv2654c (TB7.7), and Rv1038c (EsxJ). J Immunol 2012, 188:5020-5031.
64. Sallusto F., Geginat J., Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004, 22:745-763.
65. Chiacchio T., Petruccioli E., Vanini V., et al. Higher frequency of T-cell response to M. tuberculosis latency antigen Rv2628 at the site of active tuberculosis disease than in peripheral blood. PLoS ONE 2011, 6:e27539.
66. Arend S.M., van Soolingen D., Ottenhoff T.H. Diagnosis and treatment of lung infection with nontuberculous mycobacteria. Curr Opin Pulm Med 2009, 15:201-208.
67. Lin M.Y., Reddy T.B.K., Arend S.M., et al. Cross-reactive immunity to Mycobacterium tuberculosis DosR regulon-encoded antigens in individuals infecte with environmental, nontuberculous mycobacteria. Infect Immun 2009, 77:9.
68. Riano F., Arroyo L., Paris S., et al. T cell responses to DosR and Rpf proteins in actively and latently infected individuals from Colombia. Tuberculosis (Edinb) 2012, 92:148-159.
69. Black G.F., Thiel B.A., Ota M.O., et al. Immunogenicity of novel DosR regulon-encoded candidate antigens of Mycobacterium tuberculosis in three high-burden populations in Africa. Clin Vaccine Immunol 2009, 16:1203-1212.