How a different look at latency can help to develop novel diagnostics and vaccines against tuberculosis

Expert Opinion on Biological Therapy

Volumn 7, Issue 11, 2007, Pages 1665-1677

  Locht, Camille ^a,b   Rouanet, Carine ^a,b   Hougardy, Jean Michel ^c   Mascart, Françoise ^c,d  

^a INSTITUT PASTEUR DE LILLE   (France)

^b INSERM   (France)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d ERASME HOSPITAL   (Belgium)

Author keywords

Bacille Calmette Gu rin; BCG; Extrapulmonary dissemination; Granuloma; Heparin binding haemagglutinin; Mycobacterium tuberculosis; Reactivation; Tuberculin skin test

Indexed keywords

BCG VACCINE; HEMAGGLUTININ; HEPARIN BINDING HEMAGGLUTININ; ISONIAZID; RIFAMPICIN; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN;

BCG VACCINATION; DIAGNOSTIC TEST; GRANULOMA; HUMAN; IMMUNITY; INFECTION CONTROL; LUNG TUBERCULOSIS; MULTIDRUG RESISTANCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; REVIEW; VIRUS LATENCY; VIRUS REPLICATION; IMMUNOLOGY; PHYSIOLOGY;

CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS;

ANTIGENS, BACTERIAL; HUMANS; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS VACCINES; TUBERCULOSIS, PULMONARY;

EID: 36049040557     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.7.11.1665     Document Type: Review

References (100)

1. WORLD HEALTH ORGANIZATION: TB deaths reach historic levels. WHO Press, 21 March (1996):1-3.
2. WORLD HEALTH ORGANIZATION: WHO Report (1994) WHO/TB/94.177.
3. WORLD HEALTH ORGANIZATION: Global tuberculosis control: surveillance, planning, financing. WHO Report. Geneva, Switzerland (2007) WHO/HTM/TB/2007.376.
4. DYE C, WATT CJ, BLEED DM, HOSSEINI SM, RAVIGLIONE MC: Evolution of tuberculosis control and prospects for tuberculosis incidence, prevalence, and death globally. JAMA (2005) 293:2767-2775.
5. DYE C, SCHEEL S, DOLIN R, PATHANIA G, RAVIGLIONE MC: Global burden of tuberculosis. Estimated incidence, prevalence, and mortality by country. JAMA (1999) 182:677-686.
6. HOLMES CB, LOSINA E, WALENSKY RP, YAZDANPANAH Y, FREEBERG KA: Review on human immunodeficiency virus type 1-related opportunistic infections in sub-Saharan countries. Clin. Infect. Dis. (2003) 36:652-662.
7. SELWYN PA, HARTEL D, LEWIS VA et al.: A prospective study on the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. N. Engl. J. Med (1989) 320:545-550.
8. STEINGART KR, NG V, HENRY M et al.: Sputum processing methods to improve the sensitivity of smear microscopy for tuberculosis. A systematic review. Lancet Infect. Dis. (2006) 6:664-674.
9. URBANCZIK R: Present position of microscopy and of culture in diagnostic mycobacteriology. Zentralbl. Bakteriol. Mikrobiol. Hyg [A] (1985) 260:81-87.
10. SBARBARO JA: Skin testing in the diagnosis of tuberculosis. Semin. Respir. Infect. (1986) 1:234-248.
11. MENZIES D: Interpretation of repeated tuberculin tests: boosting, conversion and reversion. Am. J. Respir. Crit. Care Med. (1999) 159:15-21. • An important paper on the proper use of the TST.
12. PAI M, DHEDA K, CUNNINGHAM J, SCANO F, O'BRIEN R: T-cell assays foi the diagnosis of latent tuberculosis infection: moving the research agenda forward. Lancet Infect. Dis. (2007) 7:428-438.
13. KHATRI GR, FRIEDEN TR: Controlling tuberculosis in India. N Engl J. Med. (2002) 347:1420-1425.
14. RAVIGLIONE MC, PIO A: Evolution of WHO policies for tuberculosis control, 1948 - 2001. Lancet (2002) 350:624-629.
15. ZIGNOL M, HOSSEINI MS, WRIGHT A et al.: Global incidence of multidrug-resistant tuberculosis. J. Infect. Dis. (2006) 194:479-485.
16. ISEMAN MD: Treatment of multidrug-resistant tuberculosis. N. Engl. J Med. (1993) 329:784-791.
17. SHAH NS, WRIGHT A, BAI GH et al.: Worldwide emergence of extensively drug-resistant tuberculosis. Em. Infect. Dis. (2007) 13:380-387.
18. FINE PE: Variation in protection by BCG: implications of and for heterologous immunity. Lancet (1995) 346:1339-1345.
19. MARTIN C: Tuberculosis vaccines: past, present and future. Curr. Opin. Pulm. Med. (2006) 12:186-191.
20. RODRIGUES LC, DIWAN VK, WHEELER LG: Protective effect of BCG against tuberculosis meningitis and miliary tuberculosis: a meta-analysis. Int. J. Epidemiol. (1993) 22:1154-1158.
21. TRUNZ B, FINE P, DYE C: Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a meta-analysis and assessment of cost-effectiveness. Lancet (2006) 367:1173-1180.
22. COLDITZ GA, BREWER TF, BERKEY CS et al.: Efficacy of BCG vaccine in the prevention of tuberculosis - meta-analysis of the published literature. JAMA (1994) 271:698-702. • An important review on the protective efficacy of BCG vaccines against adult pulmonary TB.
23. BROSCH R, GORDON SV, GARNIER T et al.: Genome plasticity of BCG and the impact on vaccine efficacy. Proc. Natl. Acad. Sci. USA (2007) 104:5596-5601.
24. RODRIGUES LC, PEREIRA SM, CUNHA SS et al.: Effect of BCG revaccination on incidence of tuberculosis in school-aged children in Brazil; the BCG-REVAC cluster-randomised trial. Lancet (2005) 366:1290-1295. • Important study showing that re-vaccinating adolescents with BCG does not improve BCG efficacy.
25. WELLS WF, RADCLIFFE HL, CRUMB C: On the mechanism of droplet nuclei infection. Am. J. Hyg. (1948) 47:11-28.
26. RUSSELL DG: Mycobacterium tuberculosis: here today, and here tomorrow. Nat. Rev. Mol. Cell Biol. (2001) 2:569-577.
27. RUSSELL DG: Who puts the tubercle in tuberculosis? Nat. Rev. Microbiol. (2007) 5:39-47. • Interesting review on the formation of tuberculosis granulomas.
28. MEDLAR EM: The pathogenesis of minimal pulmonary tuberculosis: a study of 1225 necropsies in cases of sudden and unexpected death. Am. Rev. Tuberc. (1948) 58:583-611.
29. SWEANY HC, COOK CE, KEGERREIS RA: A study of the position of primary cavities in pulmonary tuberculosis. Am. Rev. Tuberc. (1931) 24:558-582.
30. LINCOLN EM, GILBERT LA, MORALES SM: Chronic pulmonary tuberculosis in individuals with known previous primary tuberculosis. Dis. Chest (1960) 38:473-482.
31. STEAD WW: The pathogenesis of pulmonary tuberculosis among older persons. Am. Rev. Respir. Dis. (1965) 91:811-822.
32. NEYROLLES O, HERNANDEZ-PANDO R, PIETRI-ROUXEL F et al.: Is adipose tissue a place for Mycobacterium tuberculosis persistence? PLoS One (2006) 1:E43. •• A key paper suggesting that during latency M. tuberculosis can reside outside the lungs in essentially any organ, imprisoned within adipocytes.
33. COMSTOCK GW: The epidemiology of tuberculosis. Am. Rev. Respir. Dis. (1982) 125(Suppl.):8-16.
34. AMERICAN THORACIC SOCIETY AND THE CENTERS FOR DISEASE CONTROLAND PREVENTION: Targeted tuberculin testing and treatment of latent tuberculosis infection. Am. J. Respir. Crit. Care Med. (2000) 161:S221-S247. • Important paper setting a number of standards for latent M. tuberculosis infection.
35. GRZYBOWSKI S, ALLEN EA: The challenge of tuberculosis in decline. A study based on the epidemiology of tuberculosis in Ontario, Canada. Am. Rev. Respir. Dis. (1964) 90:707-720.
36. STEAD NV, LOFGREN JP: Does the risk of tuberculosis increase with old age? J. Infect. Dis. (1983) 147:951-955.
37. DANNENBERG AM Jr, ROOK GAW: Pathogenesis of pulmonary tuberculosis: an interplay of tissue-damaging and macrophage-activating immune responses - dual mechanisms that control bacillary multiplication. In: Tuberculosis, Pathogenesis, Protection, and Control. Bloom BR (Ed.), ASM Press, Washington DC, USA (1994):459-483.
38. CANETTI G: Present aspects of bacterial resistance in tuberculosis. Am. Rev. Respir. Dis. (1965) 92:687-703.
39. KEANE J, GERSHON S, WISE RP et al.: Tuberculosis associated with infliximab, a TNF-α-neutralizing agent. N. Engl. J. Med (2001) 345:1098-1104.
40. + T cells in tuberculosis. Am. J. Respir. Crit. Care Med. (2002) 166:1116-1121.
41. + T cells. Eur. J. Immunol. (2000) 30:3689-3698.
42. MITTRUCKER HW, STEINHOFF U, KOHLER A et al.: Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. Proc. Natl. Acad. Sci. USA (2007) 104:12434-12439.
43. MCMURRAY DN: Guinea pig model of tuberculosis. In: Tuberculosis, Pathogenesis, Protection, and Control Bloom BR (Ed.), ASM Press, Washington DC, USA (1994):135-147.
44. REES RJW, HART D'A: Analysis of the host-parasite equilibrium in chronic murine tuberculosis by total and viable bacillary counts. Br. J. Exp. Pathol. (1961) 42:83-88.
45. MCCUNE RM, TOMPSETT R: Fate of Mycobacterium tuberculosis in mouse tissues as determined by the microbial enumeration technique. I. The persistence of drug-susceptible tubercle bacilli in tissues despite prolonged antimicrobial therapy. J. Exp. Med. (1956) 104:737-762.
46. MCCUNE RM, MCDERMOTT W. TOMPSETT R: The fate of Mycobacterium tuberculosis in mouse tissues as determined by the microbial enumeration technique. II. The conversion of tuberculous infection to the latent state by administration of pyrazinamide and a companion drug. J. Exp. Med. (1956) 104:763-802.
47. WAYNE LG, SRAMEK HA: Metronidazol is bactericidal to dormant cells of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. (1994) 38:2054-2058.
48. FLYNN JL: Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect. (2006) 8:1179-1188.
49. WAYNE LG: Dormancy of Mycobacterium tuberculosis and latency of disease. Eur. J. Clin. Microbiol. Infect. Dis. (1994) 13:908-914.
50. CARDONA PJ, RUIZ-MANZANO J: On the nature of Mycobacterium tuberculosis-latent bacilli. Eur. Respir. J. (2004) 24:1044-1051.
51. WAYNE LG, SOHASKEY CD: Nonreplicating persistence of Mycobacterium tuberculosis. Annu. Rev. Microbiol. (2001) 55:139-163. • Thorough review on the hypoxy hypothesis of dormancy.
52. SHERMAN DR, VOSKUIL M, SCHNAPPINGER D, LIAO R, HARRELL MI, SCHOOLNIK GK: Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding α-crystallin. Proc. Natl. Acad. Sci. USA (2001) 98:7534-7539.
53. RAJA A, UMA DEVI KR, RAMALINGAM B, BRENNAN PJ: 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.
54. WILKINSON RJ, WILKINSON KA, DE SMET KA et al.: Human T- and B-cell reactivity to the 16 kDa α-crystallin protein of Mycobacterium tuberculosis. Scand. J. Immunol. (1998) 48:403-409.
55. VOSKUIL MI, SCHNAPPINGER D, VISCONTI KC et al.: Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. (2003) 198:705-713.
56. LEYTEN EM, LIN MY, FRANKEN KL 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.
57. DEJERINE J: Recherche du bacille de Koch dans la tuberculose calcifiée. Compt. Rend. Soc. Biol. (1884) 36:500-505.
58. OPIE EL, ARONSON JD: Tubercle bacilli in latent tuberculosis lesions and in lung tissue without tuberculous lesions. Arch. Pathol Lab. Med. (1927) 4:1-21.
59. FELDMAN WH, BAGGENSTOSS AH: The residual infectivity of the primary complex of tuberculosis. Am. J. Pathol. (1938) 14:473-493.
60. MEDLAR EM, BERNSTEIN S, STEWARD DM: A bacteriologic study of resected tuberculous lesions. Am. Rev. Tuberc. (1952) 66:36-43.
61. HERNANDEZ-PANDO R, JEYANATHAN M, MENGISTU G et al.: Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet (2000) 356:2133-2137. •• A key paper showing evidence of the presence of M. tuberculosis DNA in cells other than macrophages of latendy infected individuals.
62. SHEPARD CC: Growth characteristics of tubercule bacilli and certain other mycobacteria in HeLa cells. J. Exp. Med. (1957) 105:39-48. •• One of the first thorough reports on the ability of M. tuberculosis to grow within cells other than macrophages, and its relation to virulence.
63. BERMUDEZ LE, GOODMAN J: Mycobacterium tuberculosis invades and replicates within type II alveolar cells. Infect. Immun. (1996) 64:1400-1406.
64. MCDONOUGH KA, KRESS Y: Cytotoxicity of lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis. Infect. Immun. (1995) 63:4802-4811.
65. METHA PK, KING CH, WHITE EH, MURTAGH JJJR, QUINN FD: Comparison of in vitro models for the study of Mycobacterium tuberculosis invasion and intracellular replication. Infect. Immun. (1996) 64:2673-2679.
66. BERMUDEZ LE, SANGARI FJ, KOLONOSKI P, PETROFSKY M, GOODMAN J: The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model for the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells. Infect. Immun. (2002) 70:140-146.
67. MENOZZI FD, ROUSE JH, ALAVI M et al.: Identification of a heparin-binding hemagglutinin present in mycobacteria. J. Exp. Med. (1996) 184:993-1001. • The first description of HBHA of M. tuberculosis.
68. PETHE K, ALONSO S, BIET F et al.: The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature (2001) 412:190-194. •• First demonstration of the role of HBHA in extrapulmonary dissemination of M. tuberculosis.
69. LOCHT C, RAZE D, ROUANET C, GENISSET C, SEGERS J, MASCART F: The mycobacterial heparin-binding hemagglutinin, virulence factor and antigen useful for diagnostics and vaccine development. In: The Mycobacterial Cell Wall. Daffé M, Reyrat JM (Eds), ASM Press, Washington DC, USA (2007) (In Press).
70. MENOZZI FD, BISCHOFF R, FORT E, BRENNAN MJ, LOCHT C: Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin. Proc. Natl. Acad. Sci. USA (1998) 95:12625-12630.
71. DELOGU G, BRENNAN MJ: Functional domains present in the mycobacterial hemagglutinin HBHA. J. Bacteriol. (1999) 181:7464-7469.
72. PETHE K, AUMERCIER M, FORT E, GATOT C, LOCHT C, MENOZZI FD: Characterization of the heparin-binding site of the mycobacterial heparin-binding hemagglutinin adhesin. J. Biol. Chem. (2000) 275:14273-14280.
73. DUPRES V, MENOZZI FD, LOCHT C et al.: Nanoscale mapping and functional analysis of individual adhesions on living bacteria. Nat. Methods (2005) 2:515-520.
74. PETHE K, BIFANI P, DROBECQ H et al.: Mycobacterial heparin-binding hemagglutinin and laminin-binding protein share antigenic methyllysines that confer resistance to proteolysis. Proc. Natl. Acad. Sci. USA (2002) 99:10759-10764. • Important paper showing that HBHA is methylated on the lysine residues within the C-terminal, functional domain of the protein.
75. HOST H, DROBECQ H, LOCHT C, MENOZZI FD: Enzymatic methylation of the Mycobacterium tuberculosis heparin-binding haemagglutinin. FEMS Microbiol Lett. (2007) 268:144-150.
76. MUELLER-ORITZ SL, SEPULVEDA E, OLSEN MR, JAGANNATH C, WANGER AR, NORRIS SJ: Decreased infectivity despite unaltered C3 binding by a ΔhbhA mutant of Mycobacterium tuberculosis. Infect. Immun. (2002) 70:6751-6760.
77. CHACKERIAN AA, ALT JM, PERERA TV, DASCHER CC, BEHAR SM: Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect. Immun. (2002) 70:4501-4509.
78. MENOZZI FD, REDDY VM, CAYET D et al.: Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions. Microbes Infect. (2006) 8:1-9.
79. BALASUBRAMANIAN V, WIEGESHAUS EH, TAYLOR T, SMITH DW: Pathogenesis of tuberculosis: pathway to apical localization. Tuber. Lung Dis. (1994) 75:168-178.
80. DELOGU G, SANGUINETTI M, POSTERARO B, ROCCA S, ZANETTI S, FADDA G: The hbhA gene of Mycobacterium tuberculosis is specifically upregulated in the lungs but not in the spleens of aerogenically infected mice. Infect. Immun. (2006) 74:3006-3011. •• An important paper showing that the hbhA gene is strongly upregulated during M. tuberculosis infection of epithelial cells.
81. CUNNINGHAM AC, MILNE DS, WILKES J, DARK JH, TETLEY TD, KIRBY JA: Constitutive expression of MHC and adhesion molecules by alveolar epithelial cells (type II pneumocytes) isolated from human lung and comparison with immunocytochemical findings. J. Cell Sci. (1994) 107:443-449.
82. + T cells. Am. J. Physiol. Lung. Mol. Physiol. (2005) 289:L274-L279. •• An important paper showing evidence that alveolar epithelial cells can actually present mycobacterial antigens to T cells.
83. MASUNGI C, TEMMERMAN S, VAN VOOREN JP et al.: Differential T and B cell responses against Mycobacterium tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis. J. Infect. Dis. (2002) 185:513-520.
84. TEMMERMAN S, PETHE K, PARRA M et al.: Methylation-dependent T cell immunity to Mycobacterium tuberculosis heparin-binding hemagglutinin. Nat. Med. (2004) 10:935-941. •• First report showing that HBHA is protective in mouse models and that the methylation of the protein plays a crucial role in its protective immunogenicity.
85. HOUGARDY JM, SCHEPERS K, PLACE S et al.: Heparin-binding hemagglutinin-induced IFN-γ release as a diagnostic tool for latent tuberculosis. PLoS One (2007):(In Press). • A study showing a good sensitivity and specificity of HBHA for the diagnosis of latent infection, especially as a result of a remote exposure. The study also shows that the HBHA-based diagnosis was not confounded by previous BCG vaccination.
86. HORSBURGH CR: Priorities for the treatment of latent tuberculosis infection in the United States. N. Engl. J. Med. (2004) 350:2060-2067.
87. JASMER RM, NAHID P, HOPEWELL PC: Clinical practice: latent tuberculosis infection. N. Engl. J. Med. (2002) 347:1860-1866.
88. RICHELDI L: An update on the diagnosis of tuberculosis infection. Am. J. Respir. Crit. Care Med. (2006) 174:736-742.
89. FERRARA G, LOSI M, D'AMICO R et al.: Use in routine clinical practice of two commercial blood tests for diagnosis of infection with Mycobacterium tuberculosis: a prospective study. Lancet (2006) 367:1328-1334.
90. KANG YA, LE HW, YOON HI et al.: Discrepancy between the tuberculin skin test and the whole-blood interferon γ assay for the diagnosis of latent tuberculosis infection in an intermediate tuberculosis-burden country. JAMA (2005) 293:2756-2761. • One of the first studies describing the relatively poor performance of whole-blood IFN-γ assays for the diagnosis of latent infection in low-incidence countries.
91. PHADKE MA, KSHIRSAGAR NA: Blood tests for diagnosis of tuberculosis. Lancet (2006) 368:282-283. • Excellent review on the new IFN-γ release assays for the detection of latent M. tuberculosis infection.
92. HOUGARDY JM, PLACE S, HILDEBRAND M et al.: Regulatory T cells depress immune responses to protective antigens in active tuberculosis. Am. J. Respir. Crit. Care Med. (2007) 176:409-416.
93. low/- regulatory T cells from peripheral blood lymphocytes of healthy Mycobacterium tuberculosis-infected humans. Microbes Infect. (2007) (In Press).
94. FLORES L, NAF S, HERNAEZ R, CONGET I, GOMIS R, ESMATJES E: Transforming growth factor-β at clinical onset of Type 1 diabetes mellitus. A pilot study. Diabet. Med. (2004) 21:818-822.
95. JAGIRDAR J, BEGIN R, DUFRESNE A, GOSWAMIS, LEE TC, ROM WN: Transforming growth factor-β (TGF-β) in silicosis. Am. J. Respir. Crit. Care Med. (1996) 154:1076-1081.
96. YAMAMOTO T, NOBLE NA, COHEN AH et al.: Expression of transforming growth factor-β isoforms in human glomerular diseases. Kidney Int. (1996) 49:461-469.
97. + T lymphocytes in latent human tuberculosis. J. Infect. Dis. (2005) 192:226-232.
98. LOCHT C, HOUGARDY JM, ROUANET C, PLACE S, MASCART F: Heparin-binding hemagglutinin, from an extrapulmonary dissemination factor to a powerful diagnostic and protective antigen against tuberculosis. Tuberculosis (2006) 86:303-309.
99. PARRA M, PICKETT T, DELOGU G et al.: The mycobacterial heparin-binding hemagglutinin is a protective antigen in the mouse aerosol challenge model of tuberculosis. Infect. Immun. (2004) 72:6799-6805.
100. LI Z, HOWARD A, KELLEY C, DELOGU G, COLLINS F, MORRIS S: Immunogenicity of DNA vaccines expressing tuberculosis proteins fused to tissue plasminogen activator signal sequences. Infect. Immun. (1999) 67:4780-4786.