A review of murine models of latent tuberculosis infection

References

• World Health Organization. Global tuberculosis control: epidemiology, strategy, financing: WHO report 2009. WHO/HTM/TB/2009.411 Geneva: WHO; 2009. Available at: http://www.who.int/tb/publications/global_report/2009/update/a-1_full.pdf (accessed March 2009).
   Google Scholar
• Wright A, Zignol M, Van Deun A, Falzon D, Gerdes SR, Feldman K, . Global project on anti-tuberculosis drug resistance surveillance. Epidemiology of antituberculosis drug resistance 2002–07: an updated analysis of the Global Project on Anti-Tuberculosis Drug Resistance Surveillance. Lancet 2009;373:1861–73.
   PubMed Web of Science ®Google Scholar
• Parrish NM, Dick JD, Bishai WR. Mechanisms of latency in Mycobacterium tuberculosis. Trends Microbiol 1998;6: 107–12.
   PubMed Web of Science ®Google Scholar
• Wiker HG, Mustafa T, Bjune GA, Harboe M. Evidence for waning of latency in a cohort study of tuberculosis. BMC Infect Dis 2010;10:37.
   PubMed Web of Science ®Google Scholar
• Wayne LG. Dormancy of Mycobacterium tuberculosis and latency of disease. Eur J Clin Microbiol Infect Dis 1994;13: 908–14.
   PubMed Web of Science ®Google Scholar
• Kobashi Y, Shimizu H, Ohue Y, Mouri K, Obase Y, Miyashita N, . Comparison of T-cell interferon-gamma release assays for Mycobacterium tuberculosis-specific antigens in patients with active and latent tuberculosis. Lung 2010;188:283–7.
   PubMed Web of Science ®Google Scholar
• Chang-hong S, Xiao-wu W, Hai Z, Ting-fen Z, Li-Mei W, Zhi-kai X. Immune responses and protective efficacy of the gene vaccine expressing Ag85B and ESAT6 fusion protein from Mycobacterium tuberculosis. DNA Cell Biol 2008;27: 199–207.
   PubMed Web of Science ®Google Scholar
• Seah GT, Scott GM, Rook GA. Type 2 cytokine gene activation and its relationship to extent of disease in patients with tuberculosis. J Infect Dis 2000;181:385–9.
   PubMed Web of Science ®Google Scholar
• North RJ. Mice incapable of making IL-4 or IL-10 display normal resistance to infection with Mycobacterium tuberculosis. Clin Exp Immunol 1998;113:55–8.
   PubMed Web of Science ®Google Scholar
• Biketov S, Potapov V, Ganina E, Downing K, Kana BD, Kaprelyants A. The role of resuscitation promoting factors in pathogenesis and reactivation of Mycobacterium tuberculosis during intra-peritoneal infection in mice. BMC Infect Dis 2007;7:146.
   PubMed Web of Science ®Google Scholar
• Flynn JL, Scanga CA, Tanaka KE, Chan J. Effects of aminoguanidine on latent murine tuberculosis. J Immunol 1998; 160:1796–803.
   PubMed Web of Science ®Google Scholar
• Dahl JL, Kraus CN, Boshoff HI, Doan B, Foley K, Avarbock D, . The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc Natl Acad Sci U S A 2003;100: 10026–31.
   PubMed Web of Science ®Google Scholar
• Karakousis PC, Yoshimatsu T, Lamichhane G, Woolwine SC, Nuermberger EL, Grosset J, . Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J Exp Med 2004;200:647–57.
   PubMed Web of Science ®Google Scholar
• Xu ZQ, Hollingshead MG, Borgel S, Elder C, Khilevich A, Flavin MT. In vivo anti-HIV activity of (+)-calanolide A in the hollow fiber mouse model. Bioorg Med Chem Lett 1999;9:133–8.
   PubMed Web of Science ®Google Scholar
• Lecoeur HF, Truffot-Pernot C, Grosset JH. Experimental short-course preventive therapy of tuberculosis with rifampin and pyrazinamide. Am Rev Respir Dis 1989;140:1189–93.
   PubMed Web of Science ®Google Scholar
• Jasmer RM, Nahid P, Hopewell PC. Clinical practice. Latent tuberculosis infection. N Engl J Med 2002;347:1860–6.
   PubMed Web of Science ®Google Scholar
• Nuermberger EL, Yoshimatsu T, Tyagi S, Bishai WR, Grosset JH. Paucibacillary tuberculosis in mice after prior aerosol immunization with Mycobacterium bovis BCG. Infect Immun 2004;72:1065–71.
   PubMed Web of Science ®Google Scholar
• Rhoades ER, Frank AA, Orme IM. Progression of chronic pulmonary tuberculosis in mice aerogenically infected with virulent Mycobacterium tuberculosis. Tuber Lung Dis 1997; 78:57–66.
   PubMedGoogle Scholar
• Zhang T, Zhang M, Rosenthal IM, Grosset JH, Nuermberger EL. Short-course therapy with daily rifapentine in a murine model of latent tuberculosis infection. Am J Respir Crit Care Med 2009;180:1151–7.
   PubMed Web of Science ®Google Scholar
• McCune RM Jr, 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 the administration of pyrazinamide and a companion drug. J Exp Med 1956;104:763–802.
   PubMed Web of Science ®Google Scholar
• Paramasivan CN, Kubendiran G, Herbert D. Action of metronidazole in combination with isoniazid and rifampicin on persisting organisms in experimental murine tuberculosis. Indian J Med Res 1998;108:115–9.
   PubMed Web of Science ®Google Scholar
• Repique CJ, Li A, Collins FM, Morris SL. DNA immunization in a mouse model of latent tuberculosis: effect of DNA vaccination on reactivation of disease and on reinfection with a secondary challenge. Infect Immun 2002;70:3318–23.
   PubMed Web of Science ®Google Scholar
• Ha SJ, Jeon BY, Kim SC, Kim DJ, Song MK, Sung YC, . Therapeutic effect of DNA vaccines combined with chemotherapy in a latent infection model after aerosol infection of mice with Mycobacterium tuberculosis. Gene Ther 2003;10: 1592–9.
   PubMed Web of Science ®Google Scholar
• Nikonenko BV, Averbakh JM, Lavebratt C, Schurr E, Apt AS. Comparative analysis of mycobacterial infections in susceptible I/St and resistant A/Sn inbred mice. Tuberc Lung Dis 2000;80:15–25.
   PubMedGoogle Scholar
• Medina E, North J. Genetically susceptible mice remain proportionally more susceptible to tuberculosis after vaccination. Immunology 1999;96:16–21.
   PubMed Web of Science ®Google Scholar
• Turner J, Gonzalez-Juarrero M, Saunders BM, Brooks JV, Marietta P, Ellis DL, . Immunological basis for reactivation of tuberculosis in mice. Infect Immun 2001;69:3264–70.
   PubMed Web of Science ®Google Scholar
• Scanga CA, Mohan VP, Joseph H, Yu K, Chan J, Flynn JL. Microbial persistence. I. The capacity of tubercle bacilli to survive sterilization in mouse tissues. J Exp Med 1966;123: 445–68.
   PubMed Web of Science ®Google Scholar
• Rees RJ, Hart PD. Analysis of the host–parasite equilibrium in chronic murine tuberculosis by total and viable bacillary counts. Br J Exp Pathol 1961;42:83–8.
   PubMed Web of Science ®Google Scholar
• Dhillon J, Mitchison DA. Effect of vaccines in a murine model of dormant tuberculosis. Tubercle Lung Dis 1994;75: 61–4.
   PubMedGoogle Scholar
• Sala C, Dhar N, Hartkoorn RC, Zhang M, Ha YH, Schneider P, . Simple model for testing drugs against nonreplicating Mycobacterium tuberculosis. Antimicrob Agents Chemother 2010;54:4150–8.
   PubMed Web of Science ®Google Scholar
• Arriaga AK, Orozco EH, Aguilar LD, Rook GA, Hernández Pando R. Immunological and pathological comparative analysis between experimental latent tuberculous infection and progressive pulmonary tuberculosis. Clin Exp Immunol 2002;128:229–37.
   PubMed Web of Science ®Google Scholar
• Campuzano J, Aguilar D, Arriaga K, León JC, Salas-Rangel LP, González-y-Merchand J, . The PGRS domain of Mycobacterium tuberculosis PE_PGRS Rv1759c antigen is an efficient subunit vaccine to prevent reactivation in a murine model of chronic tuberculosis. Vaccine 2007;25:3722–9.
   PubMed Web of Science ®Google Scholar
• Rivas-Santiago B, Contreras JC, Sada E, Hernández-Pando R. The potential role of lung epithelial cells and beta-defensins in experimental latent tuberculosis. Scand J Immunol 2008;67:448–52.
   PubMed Web of Science ®Google Scholar
• Mohan VP, Scanga CA, Yu K, Scott HM, Tanaka KE, Tsang E, . Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect Immun 2001;69:1847–55.
   PubMed Web of Science ®Google Scholar
• Scanga CA, Mohan VP, Joseph H, Yu K, Chan J, Flynn JL. Reactivation of latent tuberculosis: variations on the Cornell murine model. Infect Immun 1999;67:4531–8.
   PubMed Web of Science ®Google Scholar
• Wangoo A, Sparer T, Brown IN, Snewin VA, Janssen R, Thole J, . Contribution of Th1 and Th2 cells to protection and pathology in experimental models of granulomatous lung disease. J Immunol 2001;166:3432–9.
   PubMed Web of Science ®Google Scholar
• Martìnez Cordero E, Gonzàlez MM, Aguilar LD, Orozco EH, Hernàndez Pando R. Alpha-1-acid glycoprotein, its local production and immunopathological participation in experimental pulmonary tuberculosis. Tuberculosis (Edinb) 2008;88:203–11.
   PubMed Web of Science ®Google Scholar
• Kiwuwa MS, Charles K, Harriet MK. Patient and health service delay in pulmonary tuberculosis patients attending a referral hospital: a cross-sectional study. BMC Public Health 2005;24:122.
   Google Scholar
• Phyu S, Mustafa T, Hofstad T, Nilsen R, Fosse R, Bjune G. A mouse model for latent tuberculosis. Scand J Infect Dis 1998;30:59–68.
   PubMedGoogle Scholar
• Shi C, Yuan S, Zhang H, Zhang T, Wang L, Xu Z. Cell-mediated immune responses and protective efficacy against infection with Mycobacterium tuberculosis induced by Hsp65 and hIL-2 fusion protein in mice. Scand J Immunol 2009;69:140–9.
   PubMed Web of Science ®Google Scholar
• Miyazaki E, Chaisson RE, Bishai WR. Analysis of rifapentine for preventive therapy in the Cornell mouse model of latent tuberculosis. Antimicrob Agents Chemother 1999;43: 2126–30.
   PubMed Web of Science ®Google Scholar
• Hernández-Pando R, Jeyanathan M, Mengistu G, Aguilar D, Orozco H, Harboe M, . Persistence of DNA from M. tuberculosis in superficially normal lung tissue during latent infection. Lancet 2000;356:2133–8.
   PubMed Web of Science ®Google Scholar
• Howard AD, Zwilling BS. Cytokine production by CD4 and CD8 T cells during the growth of M. tuberculosis in mice. Clin Exp Immunol 1998;113:443–9.
   PubMed Web of Science ®Google Scholar
• Wigginton JE, Kirschner DA. Model to predict cell-mediated immune regulatory mechanisms during human infection with Mycobacterium tuberculosis. J Immunol 2001;166:1951–67.
   PubMed Web of Science ®Google Scholar
• Nemeth J, Winkler HM, Karlhofer F, Selenko-Gebauer N, Graninger W, Winkler S. Cells co-producing Mycobacterium tuberculosis-specific type 1 cytokines for the diagnosis of latent tuberculosis. Eur Cytokine Netw 2010;21:34–9.
   PubMed Web of Science ®Google Scholar
• Flynn JL, Chan J. Immunology of tuberculosis. Annu Rev Immunol 2001;19:93–129.
   PubMed Web of Science ®Google Scholar
• Keane MP, Strieter RM. The importance of balanced pro-inflammatory and anti-inflammatory mechanisms in diffuse lung disease. Respir Res 2002;3:5.
   PubMed Web of Science ®Google Scholar
• Carmona L, Gómez-Reino JJ, Rodríguez-Valverde V, Montero D, Pascual-Gómez E, Mola EM, . Effectiveness of recommendations to prevent reactivation of latent tuberculosis infection in patients treated with tumor necrosis factor antagonists. Arthritis Rheum 2005;52:1766–72.
   PubMed Web of Science ®Google Scholar
• Chakravarty SD, Zhu G, Tsai MC, Mohan VP, Marino S, Kirschner DE, . Tumor necrosis factor blockade in chronic murine tuberculosis enhances granulomatous inflammation and disorganizes granulomas in the lungs. Infect Immun 2008;76:916–26.
   PubMed Web of Science ®Google Scholar
• Bai X, Wilson SE, Chmura K, Feldman NE, Chan ED. Morphometric analysis of Th(1) and Th(2) cytokine expression in human pulmonary tuberculosis. Tuberculosis (Edinb) 2004;84:375–85.
   PubMed Web of Science ®Google Scholar
• Changhong S, Hai Z, Limei W, Jiaze A, Li X, Tingfen Z, . Therapeutic efficacy of a tuberculosis DNA vaccine encoding heat shock protein 65 of Mycobacterium tuberculosis and the human interleukin 2 fusion gene. Tuberculosis (Edinb) 2009;89:54–61.
   PubMed Web of Science ®Google Scholar
• Jain R, Dey B, Dhar N, Rao V, Singh R, Gupta UD, . Enhanced and enduring protection against tuberculosis by recombinant BCG-Ag85C and its association with modulation of cytokine profile in lung. PLoS One 2008;3:e3869.
   PubMed Web of Science ®Google Scholar
• Starck J, Kallenius G, Marklund BI, Andersson DI, Akerlund T. Comparative proteome analysis of Mycobacterium tuberculosis grown under aerobic and anaerobic conditions. Microbiology 2004;150:3821–9.
   PubMed Web of Science ®Google Scholar
• Rosenkrands I, Slayden RA, Crawford J, Aagaard C, Barry CE 3rd, Andersen P. Hypoxic response of Mycobacterium tuberculosis studied by metabolic labeling and proteome analysis of cellular and extracellular proteins. J Bacteriol 2002;184:3485–91.
   PubMed Web of Science ®Google Scholar
• Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc Natl Acad Sci U S A 2001;98:7534–9.
   PubMed Web of Science ®Google Scholar
• Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, . Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 2003;48:833–43.
   PubMed Web of Science ®Google Scholar
• Kinger AK, Tyagi JS. Identification and cloning of genes differentially expressed in the virulent strain of Mycobacterium tuberculosis. Gene 1993;131:113–7.
   PubMed Web of Science ®Google Scholar
• Rustad TR, Harrell MI, Liao R, Sherman DR. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 2008;3:e1502.
   PubMed Web of Science ®Google Scholar
• Shi C, Zhang H, Zhang T, Wang X, Bai B, Zhao Y, . New alternative vaccine component against Mycobacterium tuberculosis-heat shock protein 16.3 or its T-cell epitope. Scand J Immunol 2009;69:465–74.
   PubMedGoogle Scholar
• Florczyk MA, McCue LA, Purkayastha A, Currenti E, Wolin MJ, McDonough KA. A family of acr-coregulated Mycobacterium tuberculosis genes shares a common DNA motif and requires Rv3133c(dosR or devR) for expression. Infect Immun 2003;71:5332–43.
   PubMedGoogle Scholar
• Sriram D, Yogeeswari P, Senthilkumar P, Dewakar S, Rohit N, Debjani B, . Novel phthalazinyl derivatives: synthesis, antimycobacterial activities, and inhibition of Mycobacterium tuberculosis isocitrate lyase enzyme. Med Chem 2009;5: 422–33.
   PubMed Web of Science ®Google Scholar
• Girlanda S, Mantegani P, Baldissera E, Aiello P, Ratti M, Sabbadini MG, . ELISPOT-IFN-gamma assay instead of tuberculin skin test for detecting latent Mycobacterium tuberculosis infection in rheumatic patients candidate to anti-TNF-alpha treatment. Clin Rheumatol 2010;29:1135–41.
   PubMed Web of Science ®Google Scholar
• Hernandez-Pando R, Pavon L, Orozco EH, Rangel J, Rook GA. Interactions between hormone-mediated and vaccine-mediated immunotherapy for pulmonary tuberculosis in Balb/c mice. Immunology 2000;100:391–8.
   PubMed Web of Science ®Google Scholar
• Wanchu A, Kuttiatt VS, Sharma A, Singh S, Varma S. CD4 cell count recovery in HIV/TB co-infected patients versus TB uninfected HIV patients. Indian J Pathol Microbiol 2010;53:745–9.
   PubMed Web of Science ®Google Scholar
• Swaminathan S, Deivanayagam CN, Rajasekaran S, Venkatesan P, Padmapriyadarsini C, Menon PA, . Long term follow up of HIV-infected patients with tuberculosis treated with 6 month intermittent short course chemotherapy. Natl Med J India 2008;21:3–8.
   PubMed Web of Science ®Google Scholar
• Martin DJ, Sim JG, Sole GJ, Rymer L, Shalekoff S, van Niekerk AB, . CD4+ lymphocyte count in African patients co-infected with HIV and tuberculosis. J Acquir Immune Defic Syndr Hum Retrovirol 1995;8:386–91.
   PubMedGoogle Scholar
• Ahmad Z, Klinkenberg LG, Pinn ML, Fraig MM, Peloquin CA, Bishai WR, . Biphasic kill curve of isoniazid reveals the presence of drug-tolerant, not drug-resistant, Mycobacterium tuberculosis in the guinea pig. Infect Dis 2009;200:1136–43.
   Web of Science ®Google Scholar
• Jassal MS, Nedeltchev GG, Osborne J, Bishai WR. A modified scoring system to describe gross pathology in the rabbit model of tuberculosis. BMC Microbiol 2011;11:49.
   PubMed Web of Science ®Google Scholar
• Dutta NK, Mehra S, Didier PJ, Roy CJ, Doyle LA, Alvarez X, . Genetic requirements for the survival of tubercle bacilli in primates. J Infect Dis 2010;201:1743–52.
   PubMed Web of Science ®Google Scholar
• Aly S, Wagner K, Keller C, Malm S, Malzan A, Brandau S, . Oxygen status of lung granulomas in Mycobacterium tuberculosis-infected mice. J Pathol 2006;210:298–305.
   PubMed Web of Science ®Google Scholar
• Kaufmann SH, Cole ST, Mizrahi V, Rubin E, Nathan C. Mycobacterium tuberculosis and the host response. J Exp Med 2005;201:1693–7.
   PubMed Web of Science ®Google Scholar