МОДЕЛИ ПОКОЯЩЕГОСЯ СОСТОЯНИЯ MYCOBACTERIUM TUBERCULOSIS IN VITRO И ЛАТЕНТНОЙ ТУБЕРКУЛЕЗНОЙ ИНФЕКЦИИ IN VIVO
ISSN: 0869-2084 (Print) ISSN: 2412-1320 (Online)
Аннотация
Моделирование латентной туберкулезной инфекции (ЛТБИ) осуществляется в целях выяснения аспектов туберкулезного патогенеза, а также тестирования новых лекарственных противотуберкулезных препаратов. В настоящем обзоре дана характеристика in vitro-моделей (n=16) покоящегося состояния Mycobacterium tuberculosis и in vivo-моделей (n=14) получения латентной туберкулезной инфекции на разных видах животных, опубликованных в отечественной и зарубежной научной литературе к настоящему времени. Представлено краткое описание модели и полученные авторами основные результаты. Анализ литературных данных отображает спектр методических приемов, позволяющих исследователям изучать механизм перехода клеток M. tuberculosis в покоящееся состояние и выхода из него, а также процессы перехода активной туберкулезной инфекции в латентную форму и ее реактивации.
Об авторах
ФБУН «ГНЦ прикладной микробиологии и биотехнологии» Роспотребнадзора 142279, Оболенск, Московская обл., Россия науч. сотр. отдела подготовки и усовершенствования специалистов mikhail.fursov88@gmail.com
Список литературы
Global tuberculosis report 2017. Geneva: World Health Organization; 2017. Licence: CC BY-NCSA 3.0 IGO. ISBN 978-92-4-156551-6. URL: https://www.who.int/tb/publications/global_report/en/
Zwerling A., Pai M. The BCG World Atlas: a database of global BCG vaccination policies and practices. Expert Rev. Anti. Infect. Ther. 2011; 9(8): 559-61.
Rangaka M.X., Wilkinson K.A., Glynn J.R., Ling D., Menzies D., Mwansa-Kambafwile J., Fielding K., Wilkinson R.J., Pai M. Predictive value of interferon-γ release assays for incident active tuberculosis: a systematic review and meta-analysis. Lancet Infect. Dis. 2012; 12(1): 45-55.
Flynn J.L., Chan J. Tuberculosis: latency and reactivation. Infect. Immun. 2001; 69: 4195-4201.
Kaplan G., Post F.A., Moreira A.L., Wainwright H., Kreiswirth B.N., Tanverdi M., Mathema B., Ramaswamy S.V., Walther G., Steyn L.M., Barry C. E., Bekker L. G. Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity Infect. Immun. 2003; 71: 7099-7108.
Grosset J. Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrob. Agents Chemother. 2003; 47: 833-6.
Karakousis P.C., Yoshimatsu T., Lamichhane G., Woolwine S.C., Nuermberger E.L., Grosset J., Bishai W.R. Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J. Exp. Med. 2004; 200(5): 647-57.
Wayne L.G., Sohaskey C.D. Nonreplicating persistence of mycobacterium tuberculosis. Annu. Rev. Microbiol. 2001; 55: 139-63.
Wayne L.G., Sramek H.A. Metronidazole is bactericidal to dormant cells of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 1994; 38: 2054-8.
Murugasu-Oei B., Dick T. J. Bactericidal activity of nitrofurans against growing and dormant Mycobacterium bovis BCG. Antimicrob. Chemother. 2000; 46: 917-9.
Mayuri, Bagchi G., Das T.K., Tyagi J.S. Molecular analysis of the dormancy response in Mycobacterium smegmatis: expression analysis of genes encoding the DevRDevS two-component system, Rv3134c and chaperone alphacrystallin homologues. FEMS Microbiol. Lett. 2002; 211: 231-7.
Ignatov D.V., Salina E.G., Fursov M.V., Skvortsov T.A., Azhikina T.L., Kaprelyants A.S. Dormant non-culturable Mycobacterium tuberculosis retains stable low-abundant mRNA. BMC Genomics. 2015; 16: 954.
Zhang Y. Mechanisms of drug resistance in Mycobacterium tuberculosis. Front. Biosci. 2004; 1(9): 1136-56.
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; 6: 2062-9.
Hu Y., Mangan J.A., Dhillon J., Sole K.M., Mitchison D.A., Butcher P.D., Coates A.R. Detection of mRNA transcripts and active transcription in persistent Mycobacterium tuberculosis induced by exposure to rifampin or pyrazinamide. J. Bacteriol. 2000; 182: 6358-65.
Cho S.H., Warit S., Wan B., Hwang C.H., Pauli G.F., Franzblau S.G. Low-oxygen-recovery assay for high-throughput screening of compounds against nonreplicating Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 2007; 51: 1380-5.
Betts J.C., Lukey P.T., Robb L.C., McAdam R.A., Duncan K. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 2002; 3: 717-31.
James B.W., Bacon J., Hampshire T., Morley K., Marsh P.D. In vitro gene expression dissected: chemostat surgery for mycobacterium tuberculosis. Comp. Funct. Genomics. 2002; 3: 345-7.
Deb C., Lee C. M., Dubey V., Daniel J., Abomoelak B., Sirakova T., Pawar S., Rogers L., Kolattukudy P. E. A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One. 2009; 4: e6077.
Voskuil M.I., Schnappinger D., Visconti K.C., Harrell M.I., Dolganov G.M., Sherman D.R., Schoolnik G.K. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 2003; 198: 705-13.
Shleeva M.O., Kudykina Y.K., Vostroknutova G.N., Suzina N.E., Mulyukin A.L., Kaprelyants A.S. Dormant ovoid cells of Mycobacterium tuberculosis are formed in response to gradual external acidification. Tuberculosis (Edinb.). 2011; 91(2): 146-54.
Alnimr A.M. Dormancy models for Mycobacterium tuberculosis: A minireview. Braz. J. Microbiol. 2015; 46(3): 641-7.
Carlsson H.E., Schapiro S.J., Farah I., Hau J. Use of primates in research: a global overview. Am. J. Primatol. 2004; 63: 225-37.
Sugawara I., Udagawa T., Aoki T., Mizuno S. Establishment of a guinea pig model of latent tuberculosis with GFP-introduced Mycobacterium tuberculosis. Tohoku. J. Exp. Med. 2009; 3: 257-62.
Phyu S., Mustafa T., Hofstad T., Nilsen R., Fosse R., Bjune G. A mouse model for latent tuberculosis. Scand. J. Infect. Dis. 1998; 1(30): 59-68.
Kashino S.S., Ovendale P., Izzo A., Campos-Neto A. Unique model of dormant infection for tuberculosis vaccine development. Clin. Vaccine Immunol. 2006; 9: 1014-21.
Young M., Mukamolova G.V., Kaprelyants A.S. Mycobacterial dormancy and its relation to persistence. In: Mycobacterium: molecular microbiology. Ed. Parish T. London, United Kingdom: Horizon Bioscience: 2005; 265-320.
Lanoix J.P., Betoudji F., Nuermberger E. Novel regimens identified in mice for treatment of latent tuberculosis infection in contacts of patients with multidrug-resistant tuberculosis. Antimicrob. Agents Chemother. 2014; 58(4): 2316-21.
Corper H.J., Cohn M.L. The virulence of tubercle bacilli and the fallacy of assuming the grade of virulence from arbitrary designations. Am. Rev. Tuberc. 1933; 28: 856-74.
Biketov S., Mukamolova G.V., Potapov V., Gilenkov E., Vostroknutova G., Kell D.B., Young M., Kaprelyants A.S. Culturability of Mycobacterium tuberculosis cells isolated from murine macrophages: a bacterial growth factor promotes recovery. FEMS Immunol. Med. Microbiol. 2000; 29(4): 233-40.
Shleeva M.O., Bagramyan K., Telkov M.V., Mukamolova G.V., Young M., Kell D.B., Kaprelyants A.S. Formation and resuscitation of “non-culturable” cells of Rhodococcus rhodochrous and Mycobacterium tuberculosis in prolonged stationary phase. Microbiology. 2002; 148(5): 1581-91.
Gordillo S., Guirado E., Gil O., Díaz J., Amat I., Molinos S., Vilaplana C., Ausina V., Cardona P.J. Usefulness of acr expression for monitoring latent Mycobacterium tuberculosis bacilli in ‘in vitro’ and ‘in vivo’ experimental models. Scand. J. Immunol. 2006; 64(1): 30-9.
Salina E.G., Mollenkopf H.J., Kaufmann S.H., Kaprelyants A.S. M. tuberculosis Gene Expression during Transition to the “Non-Culturable” State. Acta Naturae. 2009; 1(2): 73-7.
Salina E., Ryabova O., Kaprelyants A., Makarov V. New 2-thiopyridines as potential candidates for killing both actively growing and dormant Mycobacterium tuberculosis cells. Antimicrob. Agents Chemother. 2014a; 58(1): 55-60.
Salina E.G., Waddell S.J., Hoffmann N., Rosenkrands I., Butcher P.D., Kaprelyants A.S. Potassium availability triggers Mycobacterium tuberculosis transition to, and resuscitation from, non-culturable (dormant) states. Open Biol. 2014b; 4(10) pii 140106.
Sala C., Dhar N., Hartkoorn R.C., Zhang M., Ha Y.H., Schneider P., Schneider P., Cole S.T. Simple model for testing drugs against nonreplicating Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 2010; 54(10): 4150-8.
Kapoor N., Pawar S., Sirakova T.D., Deb C., Warren W.L., Kolattukudy P.E. Human granuloma in vitro model, for TB dormancy and resuscitation. PLoS One. 2013; 8(1): e53657.
Soto-Ramirez M.D., Aguilar-Ayala D.A., Garcia-Morales L., Rodriguez-Peredo S.M., Badillo-Lopez C., Rios-Muñiz D.E., Meza-Segura M.A., Rivera-Morales G.Y., Leon-Solis L., Cerna-Cortes J.F., Rivera-Gutierrez S., Helguera-Repetto A.C., Gonzalez-Y-Merchand J.A. Cholesterol plays a larger role during Mycobacterium tuberculosis in vitro dormancy and reactivation than previously suspected. Tuberculosis (Edinb.). 2017; 103: 1-9.
Aguilar-Ayala D.A., Cnockaert M., Vandamme P., Palomino J.C., Martin A., Gonzalez-Y-Merchand J. Antimicrobial activity against Mycobacterium tuberculosis under in vitro lipid-rich dormancy conditions. J. Med. Microbiol. 2018; 67(3): 282-285.
McCune R. M., 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 the tissues despite prolonged antimicrobial therapy. J. Exp. Med. 1956a; 104: 737.
McCune R.M., Tompsett R., McDermott W. Fate of Mycobacterium tuberculosis in mouse tissues as determined by the microbial enumeration technique. II. The conversion of tuberculosis infection to the latent state by the administration of pyrazinamide and a companion drug. J. Exp. Med. 1956b; 104: 763.
McCune R.M., Feldmann F.M., Lambert H.P., McDermott W. Microbial persistance. The capacity of tubercle bacilli to survive sterilization in mouse tissues. J. Exp. Med. 1966; 123: 445-68.
Mustafa T., Phyu S., Nilsen R., Jonsson R., Bjune G. In situ expression of cytokines and cellular phenotypes in the lungs of mice with slowly progressive primary tuberculosis. Scand. J. Immunol. 1999; 2: 127-36.
Capuano S.V., Croix D.A., Pawar S., Zinovik A., Myers A., Lin P.L., Bissel S., Fuhrman C., Klein E., Flynn J.L. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect. Immun. 2003; 10: 5831-44.
Lin P.L., Rodgers M., Smith L., Bigbee M., Myers A., Bigbee C., Chiosea I., Capuano S.V., Fuhrman C., Klein E., Flynn J. L. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect. Immun. 2009; 10: 4631-42.
Radaeva T.V., Nikonenko B.V., Mischenko V.V., Averbakh M.M. Direct comparison of low-dose and Cornell-like models of chronic and reactivation tuberculosis in genetically susceptible I/St and resistant B6 mice. Jr, Apt A.S. Tuberculosis (Edinb.). 2005; 1-2: 65-72.
Biketov S., Potapov V., Ganina E., Downing K., Kana B.D., 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.
Шрамко П.А. Грищенко Н.С., Рудницкая Т.И., Потапов В.Д., Капрельянц А.С., Бикетов С.Ф. Моделирование хронической туберкулезной инфекции у мышей методом внутрибрюшинного заражения и анализ активации аминогуанидином мутантов штамма Mycobacterium tuberculosis H37RV с делециями по генам rpf. Туберкулез и болезни легких. 2010; 4: 47-50.
Потапов В.Д. Разработка и применение биологических моделей для изучения хронической туберкулезной инфекции. Оболенск: ФБУН ГНЦ ПМБ; 2013.
Manabe Y.C., Kesavan A.K., Lopez-Molina J., Hatem C.L., Brooks M., Fujiwara R., Hochstein K., Pitt M.L., Tufariello J., Chan J., McMurray D. N., Bishai W. R., Dannenberg A. M. Jr, Mendez S. The aerosol rabbit model of TB latency, reactivation and immune reconstitution inflammatory syndrome. Tuberculosis (Edinb.). 2008; 3: 187-96.
Kashino S.S., Napolitano D.R., Skobe Z., Campos-Neto A. Guinea pig model of Mycobacterium tuberculosis latent/dormant infection. Microbes Infect. 2008; 10(14-15): 1469-76.
Radaeva T.V., Kondratieva E.V., Sosunov V.V., Majorov K.B., Apt A. A human-like TB in genetically susceptible mice followed by the true dormancy in a Cornell-like model. Tuberculosis (Edinb.). 2008; 88: 576-85.
Elwood R.L., Rajnik M., Wilson S., Yim K., Blanco J.C., Nikonenko B., Hemming V.G. Characterization of late tuberculosis infection in Sigmodon hispidus. Tuberculosis (Edinb.). 2009; 89(2): 183-8.
Mehra S., Golden N.A., Dutta N.K., Midkiff C.C., Alvarez X., Doyle L.A., Asher M., Russell-Lodrigue K., Monjure C., Roy C.J., Blanchard J.L., Didier P.J., Veazey R.S., Lackner A.A., Kaushal D. Reactivation of latent tuberculosis in rhesus macaques by coinfection with simian immunodeficiency virus. J. Med. Primatol. 2011; 40(4): 233-43.
Shleeva M., Kondratieva T., Rubakova E., Vostroknutova G., Kaprelyants A., Apt A. Reactivation of dormant “non-culturable” Mycobacterium tuberculosis developed in vitro after injection in mice: both the dormancy depth and host genetics influence the outcome. Microb. Pathog. 2015; 78: 63-6.