METHODOLOGICAL APPROACHES TO MYCOBACTERIUM TUBERCULOSIS GENOTYPING FOR EVOLUTIONARY AND EPIDEMIOLOGICAL RESEARCH

Cover Page

Cite item

Abstract

Abstract. Current genome evolution of Mycobacterium tuberculosis is marked by virtual absence of the lateral gene transfer leading to the clonal population of this species consisting of separate genetic families. Standard typing method of M. tuberculosis (IS6110-RFLP, spoligo- and VNTR-typing) are based on variation of mobile and repetitive elements and provide sufficient strain discrimination for epidemiological purposes such as, estimation of recent transmission versus reactivation of latent tuberculosis, laboratory contamination, mixed infection. At the same time, rapid evolution of some markers may lead to emergence of identical profiles in the non-related strains (homoplasy) due to convergent evolution. Use of different independent markers may help solve this problem. Regularly updated databases are available for global and local analysis and are also important for standardised terminology and designation of the genotypes. Some of the M. tuberculosis genetic families continue to circulate in the limited areas while other families have become omnipresent due to their likely increased transmissibility and pathogeneicity (e.g., Beijing and LAM). The most frequently isolated Russian subvariant Beijing B0/W148 is marked by significantly higher population growth compared to the Russian Beijing population as a whole and hence may be defined as a successful clone in Russia. Recent years revealed higher than previously thought level of genome variation in M. tuberculosis even between related isolates. The whole-genome sequencing may become a useful typing method if its cost is reduced to be similar to that of the traditional typing methods. Accumulation of the data on old and new markers, development and use of new algorithms of their analysis will help to refine our knowledge about evolution of M. tuberculosis and its families, will provide better tools for epidemiological monitoring of the circulating strains on local and global scale.

About the authors

I. V. Mokrousov

ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург

Author for correspondence.
Email: imokrousov@mail.ru

д.б.н., ведущий научный сотрудник лаборатории молекулярной микробиологии

197101, Санкт-Петербург, ул. Мира, 14

Russian Federation

References

  1. Андреевская С.Н., Черноусова Л.Н., Смирнова Т.Г., Ларионова Е.Е., Кузьмин А.В. Влияние генотипа M. tuberculosis на выживаемость мышей при экспериментальном туберкулезе // Проблемы туберкулеза и болезней легких. — 2007. — № 7. — С. 45–50.
  2. Вишневский Б.И., Нарвская О.В., Васильева С.Н., Сапожникова Н.В., Мокроусов И.В., Оттен Т.Ф. Вирулентность микобактерий туберкулеза // Проблемы туберкулеза. — 2002. — № 10. — С. 33–36.
  3. Дмитриев А.В., Шен А.Д., Тотолян А.А. TR Прямые повторы и спейсеры гена sak0l92 Streptococcus agalactiae — генетические маркеры для характеристики штаммов // Молекулярная генетика, микробиология и вирусология. — 2007. — № 4. — С. 37–41.
  4. Мокроусов И.В. Генетическое разнообразие и эволюция Mycobacterium tuberculosis: Автореф. дис. … д-ра биол. наук. — СПб., 2009. — 40 с.
  5. Нарвская О.В. Геномный полиморфизм Mycobacterium tuberculosis и его роль в эпидемическом процессе: Дис. … д-ра мед. наук. — СПб., 2003. — 173 с.
  6. Нарвская О.В., Вишневский Б.И., Елькин А.В., Мокроусов И.В., Лимещенко Е.В., Оттен Т.Ф., Осташко О.М., Ариэль Б.М. Молекулярно-генетическая характеристика штаммов Mycobacte rium tuberculosis, выделенных от больных, оперированных по поводу туберкулеза легких // Проблемы туберкулеза. — 2002. — № 3. — С. 50–53.
  7. Нарвская О.В., Мокроусов И.В., Оттен Т.Ф., Вишневский Б.И. Генетическое маркирование полирезистентных штаммов Mycobacterium tuberculosis, выделенных на Северо-Западе России // Проблемы туберкулеза. — 1999. — № 3. — С. 39–41.
  8. Черноусова Л.Н., Андреевская С.Н., Смирнова Т.Г., Земскова З.С., Ларионова Е.Е. Биологические свойства штаммов M. tuberculosis кластера W // Проблемы туберкулеза и болезней легких. — 2008. — № 10. — С. 45–50.
  9. Шемякин И.Г., Степаншина В.Н., Иванов И.Ю., Липин М.Ю., Коpобова О.В., Анисимова В.А. Хаpактеpистика клинических изолятов Mycobacterium tuberculosis с использованием молекуляpно-биологических методов // Молекулярная генетика микробиология и вирусология. — 2003. — № 1. — С. 32–40.
  10. Abadia E., Zhang J., Vultos T. dos, Ritacco V., Kremer K., Aktas E., Matsumoto T., Refregier G., Soolingen D. van, Gicquel B., Sola C. Resolving lineage assignation on Mycobacterium tuberculosis clinical isolates classified by spoligotyping with a new high-throughput 3R SNPs based method // Infect. Genet. Evol. — 2010. — Vol. 10. — P. 1066–1074.
  11. Allix-Beguec C., Harmsen D., Weniger T., Supply P., Niemann S. Evaluation and strategy for use of MIRU-VNTRplus, a multifunctional database for online analysis of genotyping data and phylogenetic identification of Mycobacterium tuberculosis complex isolates // J. Clin. Microbiol. — 2008. — Vol. 46. — P. 2692–2699.
  12. Ashiru O.T., Pillay M., Sturm A.W. Adhesion to and invasion of pulmonary epithelial cells by the F15/LAM4/KZN and Beijing strains of Mycobacterium tuberculosis // J. Med. Microbiol. — 2010. — Vol. 59. — P. 528–533.
  13. Banu S., Gordon S.V., Palmer S., Islam M.R., Ahmed S., Alam K.M., Cole S.T., Brosch R. Genotypic analysis of Mycobacterium tuberculosis in Bangladesh and prevalence of the Beijing strain // J. Clin. Microbiol. — 2004. — Vol. 42. — P. 674–682.
  14. Barnes P.F., Cave M.D. Molecular epidemiology of tuberculosis // N. Engl. J. Med. — 2003. — Vol. 349. — P. 1149 –1156.
  15. Bifani J., Mathema B., Kurepina N.E., Kreiswirth B.N. Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains // Trends Microbiol. — 2002. — Vol. 10. — P. 45–52.
  16. Bolotin A., Quinquis B., Sorokin A., Ehrlich S.D. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin // Microbiology. — 2005. — Vol. 151. — P. 2551–2561.
  17. Brudey K., Driscoll J.R., Rigouts L., Prodinger W.M., Gori A., Al-Hajoj S.A., Allix C., Aristimuno L., Arora J., Baumanis V., Binder L., Cafrune P., Cataldi A., Cheong S., Diel R., Ellermeier C., Evans J.T., Fauville-Dufaux M., Ferdinand S., Garcia de Viedma D., Garzelli C., Gazzola L., Gomes H.M., Gutierrez M.C., Hawkey P.M., Helden P.D. van, Kadival G.V., Kreiswirth B.N., Kremer K., Kubin M., Kulkarni S.P., Liens B., Lillebaek T., Ly H.M., Martin C., Mokrousov I., Narvskaya O., Ngeow Y.F., Naumann L., Niemann S., Parwati I., Rahim M.Z., Rasolofo-Razanamparany V., Rasolonavalona T., Rossetti M.L., Rusch-Gerdes S., Sajduda A., Samper S., Shemyakin I., Singh U.B., Somoskovi A., Skuce R., Soolingen D. van, Streicher E.M., Suffys P.N., Tortoli E., Tracevska T., Vincent V., Victor T.C., Warren R., Yap S.F., Zaman K., Portaels F., Rastogi N., Sola C. Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology // BMC Microbiol. — 2006. — Vol. 6. — P. 23.
  18. Caminero J.A., Pena M.J., Campos-Herrero M.I., Rodriguez J.C., Garcia I., Cabrera P., Lafoz C., Samper S., Takiff H., Afonso O., Pavon J.M., Torres M.J., Soolingen D. van, Enarson D.A., Martin C. Epidemiological evidence of the spread of a Mycobacterium tuberculosis strain of the Beijing genotype on Gran Canaria Island // Am. J. Respir. Crit. Care Med. — 2001. — Vol. 164. — P. 1165–1170.
  19. Caws M., Thwaites G., Dunstan S., Hawn T.R., Lan N.T., Thuong N.T., Stepniewska K., Huyen M.N., Bang N.D., Loc T.H., Gagneux S., Soolingen D. van, Kremer K., Sande M. van der, Small P., Anh P.T., Chinh N.T., Quy H.T., Duyen N.T., Tho D.Q., Hieu N.T., Torok E., Hien T.T., Dung N.H., Nhu N.T., Duy P.M., Vinh Chau N. van, Farrar J. The influence of host and bacterial genotype on the development of disseminated disease with M. tuberculosis // PLoS Pathog. — 2008. — Vol. 4. — P. e1000034.
  20. Cox H.S., Kubica T., Doshetov D., Kebede Y., Rьsch-Gerdess S., Niemann S.. The Beijing genotype and drug resistant tuberculosis in the Aral Sea region of Central Asia // Respir. Res. — 2005. — Vol. 6. — P. 134.
  21. Daley C.L. Molecular epidemiology: a tool for understanding control of tuberculosis transmission // Clin. Chest Med. — 2005. — Vol. 26. — P. 217–231.
  22. Drobniewski F., Balabanova Y., Nikolayevsky V., Ruddy M., Kuznetzov S., Zakharova S., Melentyev A., Fedorin I. Drug-resistant tuberculosis, clinical virulence, and the dominance of the Beijing strain family in Russia // JAMA. — 2005. — Vol. 293. — P. 2726–2731.
  23. Dubiley S., Ignatova A., Mukhina T., Nizova A., Blagodatskikh S., Stepanshina V., Shemyakin I. Molecular epidemiology of tuberculosis in Tula area, central Russia, before Directly Observed Therapy Strategy // Clin. Microbiol. Infect. — 2010. — Vol. 16, N 9. — P. 1421–1426.
  24. Dymova M.A., Liashenko O.O., Poteiko P.I., Krutko V.S., Khrapov E.A., Filipenko M.L. Genetic variation of Mycobacterium tuberculosis circulating in Kharkiv Oblast, Ukraine // BMC Infect. Dis. — 2011. — Vol. 11. — P. 77.
  25. El Sahly H.M., Wright J.A., Soini H., Bui T.T., Williams-Bouyer N., Escalante P., Musser J.M., Graviss E.A. Recurrent tuberculosis in Houston, Texas: a population-based study // Int. J. Tuberc. Lung Dis. — 2004. — Vol. 8. — P. 333–340.
  26. Embden J. van, Cave M., Crawford J., Dale J., Eise nach K., Gicquel B., Hermans P., Martin C., McAdam R., Shinnick T., Small P. Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: Recommendation for a standardized method ology // J. Clin. Microbiol. — 1993. — Vol. 31. — P. 406–409.
  27. Embden J.D.A. van, Gorkom T. van, Kremer K., Jansen T., Zeijst B.A.M. van der, Schouls L.M. Genetic variation and evolutionary origin of the direct repeat locus of Mycobacterium tuberculosis complex bacteria // J. Bacteriol. — 2000. — Vol. 182. — P. 2393–2401.
  28. Ferdinand S., Valetudie G., Sola C., Rastogi N. Data mining of Mycobacterium tuberculosis complex genotyping results using mycobacterial interspersed repetitive units validates the clonal structure of spoligotyping-defined families // Res. Microbiol. — 2004. — Vol. 155, N 8. — P. 647–654.
  29. Filliol I., Driscoll J.R., Soolingen D. van, Kreiswirth B.N., Kremer K., Valetudie G., Anh D.D., Barlow R., Banerjee D., Bifani P.J., Brudey K., Cataldi A., Cooksey R.C., Cousins D.V., Dale J.W., Dellagostin O.A., Drobniewski F., Engelmann G., Ferdinand S., Gascoyne-Binzi D., Gordon M., Gutierrez M.C., Haas W.H., Heersma H., Kallenius G., Kassa-Kelembho E., Koivula T., Ly H.M., Makristathis A., Mammina C., Martin G., Mostrom P., Mokrousov I., Narbonne V., Narvskaya O., Nastasi A., Niobe S.-Eyangoh N., Pape J.W., Rasolofo-Razanamparany V., Ridell M., Rossetti M.L., Stauffer F., Suffys P.N., Takiff H., Texier-Maugein J., Vincent V., Waard J.H. de, Sola C., Rastogi N. Global distribution of Mycobacterium tuberculosis spoligotypes // Emerg. Infect. Dis. — 2002. — Vol. 8. — P. 1347–1349.
  30. Filliol I., Driscoll J.R., Soolingen D. van, Kreiswirth B.N., Kremer K., Valetudie G., Dang D.A., Barlow R., Banerjee D., Bifani P.J., Brudey K., Cataldi A., Cooksey R.C., Cousins D.V., Dale J.W., Dellagostin O.A., Drobniewski F., Engelmann G., Ferdinand S., Gascoyne-Binzi D., Gordon M., Gutierrez M.C., Haas W.H., Heersma H., Kassa-Kelembho E., Ho M.L., Makristathis A., Mammina C., Martin G., Mostrцm P., Mokrousov I., Narbonne V., Narvskaya O., Nastasi A., Niobe-Eyangoh S.N., Pape J.W., Rasolofo-Razanamparany V., Ridell M., Rossetti M.L., Stauffer F., Suffys P.N., Takiff H., Texier-Maugein J., Vincent V., Waard J.H. de, Sola C., Rastogi N. Snapshot of moving and expanding clones of Mycobacterium tuberculosis and their global distribution assessed by spoligotyping in an international study // J. Clin. Microbiol. — 2003. — Vol. 41. — P. 1963-1970.
  31. Filliol I., Motiwala A.S., Cavatore M., Qi W., Hazbуn M.H., Bobadilla del Valle M., Fyfe J., Garcнa-Garcнa L., Rastogi N., Sola C., Zozio T., Guerrero M.I., Leуn C.I., Crabtree J., Angiuoli S., Eisenach K.D., Durmaz R., Joloba M.L., Rendуn A., Sifuentes-Osornio J., Ponce de Leуn A., Cave M.D., Fleischmann R., Whittam T.S., Alland D. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: Insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set // J. Bacteriol. — 2006. — Vol. 188. — P. 759–772.
  32. Frothingham R., Meeker-O’Connell W.A. Genetic diversity in the Mycobacterium tuberculosis complex based on variable numbers of tandem DNA repeats // Microbiology. — 1998. — Vol. 144. — P. 1189–1196.
  33. Gagneux S. Small P.M. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development // Lancet Infect. Dis. — 2007. — Vol. 7. — P. 328–337.
  34. Gagneux S., DeRiemer K., Van T., Kato-Maeda M., Jong B.C. de, Narayanan S., Nicol M., Niemann S., Kremer K., Gutierrez M.C., Hilty M., Hopewell P.C., Small P.M. Variable host-pathogen compatibility in Mycobacterium tuberculosis // Proc. Natl. Acad. Sci. USA. — 2006. — Vol. 103. — P. 2869–2873.
  35. Garcia de Viedma D., Chaves F., Inigo J., for the Tuberculosis molecular epidemiology study group. New route of importation of Mycobacterium tuberculosis Beijing genotype // Emerg. Infect. Dis. — 2006. — Vol. 12. — P. 169–170.
  36. Gillespie S.H. Tuberculosis: evolution in millennia and minutes // Biochem. Soc. Trans. — 2007. — Vol. 35. — P. 1317–1320.
  37. Glynn J.R., Crampin A.C., Traore H., Yates M.D., Mwaungulu F.D., Ngwira B. M., Chaguluka S.D., Mwafulirwa D.T., Floyd S., Murphy C., Drobniewski F. A., Fine P.E. Mycobacterium tuberculosis Beijing genotype, northern Malawi // Emerg. Infect. Dis. — 2005. — Vol. 11. — P. 150–153.
  38. Glynn J.R., Whiteley J., Bifani P.J., Kremer K., Soolingen D. van. Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review // Emerg. Infect. Dis. — 2002. — Vol. 8. — P. 843–849.
  39. Godreuil S., Torrea G., Terru D Chevenet F., Diagbouga S., Supply P., Perre P. van de, Carriere C., Baсuls A.L. First molecular epidemiology study of Mycobacterium tuberculosis in Burkina Faso // J. Clin. Microbiol. — 2007. — Vol. 45. — P. 921–927.
  40. Groenen P.M., Bunschoten A.E., Soolingen D. van, Embden J.D. van. Nature of DNA polymorphism in the direct repeat cluster of Mycobacterium tuberculosis; application for strain differentiation by a novel typing method // Mol. Microbiol. — 1993. — Vol. 10, N 5. — P. 1057–1065.
  41. Gutacker M.M., Mathema B., Soini H., Shashkina E., Kreiswirth B.N., Graviss E.A., Musser J.M. Single-nucleotide polymorphism-based population genetic analysis of Mycobacterium tuberculosis strains from 4 geographic sites // J. Infect. Dis. — 2006. — Vol. 193. — P. 121–128.
  42. Hanekom M., Spuy G.D. van der, Gey van Pittius N.C., McEvoy C.R., Ndabambi S.L., Victor T.C., Hoal E.G., Helden P.D. van, Warren R.M. Evidence that the spread of Mycobacterium tuberculosis strains with the Beijing genotype is human population dependent // J. Clin. Microbiol. — 2007. — Vol. 45. — P. 2263–2256.
  43. Helden P.D. van, Warren R.M., Victor T.C., Spuy G. van der, Richardson M., Hoal van Helden E. Strain families of Mycobacterium tuberculosis // Trends Mic robiol. — 2002. — Vol. 10. — P. 167–168.
  44. Hermans P.W.M., Soolingen D. van, Bik E.M., Haas P.E.W. de, Dale J.W., Embden J.D.A. van. The insertion element IS987 from Mycobacterium bovis BCG is located in a hot spot integration region for insertion elements in Mycobacterium tuberculosis complex strains // Infect. Immun. — 1991. — Vol. 59. — P. 2695–2705.
  45. Ignatova A., Dubiley S., Stepanshina V., Shemyakin I. Predominance of multi-drug-resistant LAM and Beijing family strains among Mycobacterium tuberculosis isolates recovered from prison inmates in Tula Region, Russia // J. Med. Microbiol. — 2006. — Vol. 55, N 10. — P. 1413–1418.
  46. Iwamoto T., Fujiyama R., Yoshida S., Wada T., Shirai C., Kawakami Y. Population structure dynamics of Mycobacterium tuberculosis Beijing strains during past decades in Japan // J. Clin. Microbiol. — 2009. — Vol. 47. — P. 3340–3343.
  47. Iwamoto T., Yoshida S., Suzuki K., Tomita M., Fujiyama R., Tanaka N., Kawakami Y., Ito M. Hypervariable loci that enhance the discriminatory ability of newly proposed 15-loci and 24-loci variable-number tandem repeat typing method on Mycobacterium tuberculosis strains predominated by the Beijing family // FEMS Microbiol. Lett. — 2007. — Vol. 272. — P. 282–283.
  48. Jansen R., Embden J.D.A. van, Gaastra W., Schouls L.M. Identification of genes that are associated with DNA repeats in prokaryotes // Mol. Microbiol. — 2002. — Vol. 43. — P. 1565–1575.
  49. Kamerbeek J., Schouls L., Kolk A., Agterveld M. van, Soolingen D. van, Kuijper S., Bunschoten A., Molhuizen H., Shaw R., Goyal M., Embden J. van. Rapid detection and simultaneous strain differentiation of Mycobacterium tuberculosis for diagnosis and tuberculosis control // J. Clin. Microbiol. — 1997. — Vol. 35. — P. 907–914.
  50. Kremer K., Glynn J.R., Lillebaek T., Niemann S., Kurepina N.E., Kreiswirth B.N., Bifani P.J., Soolingen D. van, Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers // J. Clin. Microbiol. — 2004. — Vol. 42. — P. 4040–4049.
  51. Kremer K., Werf M.J. van der, Au B.K., Anh D.D., Kam K.M., Doorn H.R. van, Borgdorff M.W., Soolingen D. van. Vaccine-induced immunity circumvented by typical Mycobacterium tuberculosis Beijing strains // Emerg. Infect. Dis. — 2009. — Vol. 15. — P. 335–339.
  52. Krüüner A., Hoffner S.E., Sillastu H., Danilovits M., Levina K., Svenson S.B., Ghebremichael S., Koivula T., Källenius G. Spread of drug-resistant pulmonary tuberculosis in Estonia // J. Clin. Microbiol. — 2001. — Vol. 39. — P. 3339–3345.
  53. Kubica T., Rusch-Gerdes S., Niemann S. The Beijing genotype is emerging among multidrug-resistant Mycobacterium tuberculosis strains from Germany // Int. J. Tuberc. Lung Dis. — 2004. — Vol. 8. — P. 1107–1113.
  54. Kwara A., Schiro R., Cowan L.S., Hyslop N.E., Wiser M.F., Harrison S.R., Kissinger P., Diem L., Crawford J.T. Evaluation of the epidemiologic utility of secondary typing methods for differentiation of Mycobacterium tuberculosis isolates // J. Clin. Microbiol. — 2003. — Vol. 41. — P. 2683–2685.
  55. Lavender C., Globan M., Sievers A., Billman-Jacobe H., Fyfe J. Molecular characterization of isoniazid-resistant Mycobacterium tuberculosis isolates collected in Australia // Antimicrob. Agents Chemother. — 2005. — Vol. 49. — P. 4068–4074.
  56. Lazzarini L.C., Spindola S.M., Bang H., Gibson A.L., Weisenberg S., Silva Carvalho W. da, Augusto C.J., Huard R.C., Kritski A.L., Ho J.L. RDRio Mycobacterium tuberculosis infection is associated with a higher frequency of cavitary pulmonary disease // J. Clin. Microbiol. — 2008. — Vol. 46. — P. 2175–2183.
  57. Lopez B., Aguilar D., Orozco H., Burger M., Espitia C., Ritacco V., Barrera L., Kremer K., Hernandez-Pando R., Huygen K., Soolingen D. van. A marked difference in pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes // Clin. Exp. Immunol. — 2003. — Vol. 133. — P. 30 –37.
  58. Marais B.J., Victor T.C., Hesseling A.C., Barnard M., Jordaan A., Brittle W., Reuter H., Beyers N., Helden P.D. van, Warren R.M., Schaaf H.S. Beijing and Haarlem genotypes are overrepresented among children with drug-resistant tuberculosis in the Western Cape Province of South Africa // J. Clin. Microbiol. — 2006. — Vol. 44. — P. 3539–3543.
  59. Millet J., Baboolal S., Akpaka P.E., Ramoutar D., Rastogi N. Phylogeographical and molecular characterization of an emerging Mycobacterium tuberculosis clone in Trinidad and Tobago // Infect. Genet. Evol. — 2009. — Vol. 9. — P. 1336–1344.
  60. Millet J., Miyagi-Shiohira C., Yamane N., Sola C., Rastogi N. Assessment of mycobacterial interspersed repetitive unit-QUB markers to further discriminate the Beijing genotype in a population-based study of the genetic diversity of Mycobacterium tuberculosis clinical isolates from Okinawa, Ryukyu Islands, Japan // J. Clin. Microbiol. — 2007. — Vol. 45. — P. 3606 –3615.
  61. Mojica F.J., Diez-Villasenor C., Garcia-Martinez J., Soria E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements // J. Mol. Evol. — 2005. — Vol. 60. — P. 174–182.
  62. Mokrousov I. Corynebacterium diphtheriae: genome diversity, population structure and genotyping perspectives // Infect. Genet. Evol. — 2009. — Vol. 9. — P. 1–15.
  63. Mokrousov I. Genetic geography of Mycobacterium tuberculosis Beijing genotype: a multifacet mirror of human history? // Infection, Genetics and Evolution. — 2008. — Vol. 8. — P. 777–785.
  64. Mokrousov I., Ly H.M., Otten T., Lan N.N., Vyshnevskyi B., Hoffner S., Narvskaya O. Origin and primary dispersal of the Mycobacterium tuberculosis Beijing genotype: clues from human phylogeography // Genome Res. — 2005. — Vol. 15. — P. 1357–1364.
  65. Mokrousov I., Narvskaya O., Limeschenko E., Vyazovaya A., Otten T., Vyshnevskiy B. Analysis of the allelic diversity of the mycobacterial interspersed repetitive units in Mycobacterium tuberculosis strains of the Beijing family: practical implications and evolutionary considerations // J. Clin. Microbiol. — 2004. — Vol. 42. — P. 2438–2444.
  66. Mokrousov I., Narvskaya O., Otten T., Vyazovaya A., Limeschenko E., Steklova L., Vyshnevskyi B. Phylogenetic reconstruction within Mycobacterium tuberculosis Beijing genotype in northwest Russia // Res. Microbiol. — 2002. — Vol. 153. — P. 629–637.
  67. Mokrousov I., Narvskaya O., Vyazovaya A., Millet J., Otten T., Vishnevsky B., Rastogi N. Mycobacterium tuberculosis Beijing genotype in Russia: in search of informative VNTR loci // J. Clin. Microbiol. — 2008. — Vol. 46. — P. 3576–3584.
  68. Mokrousov I., Valcheva V., Sovhozova N., Aldashev A., Rastogi N., Isakova J. Penitentiary population of Mycobacterium tuberculosis in Kyrgyzstan: Exceptionally high prevalence of the Beijing genotype and its Russia-specific subtype // Infect. Genet. Evol. — 2009. — Vol. 9. — P. 1400–1405.
  69. Morcillo N., Di Giulio B., Chirico C., Kuriger A., Dolmann A., Alito A., Zumarraga M., Soolingen D. van, Kremer K., Cataldi A. First description of Mycobacterium tuberculosis Beijing genotype in Argentina // Rev. Argent. Microbiol. — 2005. — Vol. 37. — P. 92–95.
  70. Musser J.M., Amin A., Ramaswamy S. Negligible genetic diversity of Mycobacterium tuberculosis host immune system protein targets: evidence of limited selective pressure // Genetics. — 2000. — Vol. 155. — P. 7–16.
  71. Namouchi A., Karboul A., Mhenni B., Khabouchi N., Haltiti R., Ben Hassine R., Louzir B., Chabbou A., Mardassi H. Genetic profiling of Mycobacterium tuberculosis in Tunisia: predominance and evidence for the establishment of a few genotypes // J. Med. Microbiol. — 2008. — Vol. 57. — P. 864–872.
  72. Narvskaya O., Otten T., Limeschenko E., Sapozhnikova N., Graschenkova O., Steklova L., Nikonova I., Filipenko M.L., Mokrousov I., Vyshnevskiy B. Nosocomial outbreak of multidrug resistant tuberculosis caused by Mycobacterium tuberculosis W-Beijing family strain in St. Petersburg, Russia // Eur. J. Clin. Microbiol. Infect. Dis. — 2002. — Vol. 21. — P. 596–602.
  73. Nicol M.P., Wilkinson R.J. The clinical consequences of strain diversity in Mycobacterium tuberculosis // Trans. R. Soc. Trop. Med. Hyg. — 2008. — Vol. 102. — P. 955 –965.
  74. Niemann, S., Diel R., Khechinashvili G., Gegia M., Mdivani N., Tang Y.W. Mycobacterium tuberculosis Beijing lineage favors the spread of multidrug-resistant tuberculosis in the Republic of Georgia // J. Clin. Microbiol. — 2010. — Vol. 48. — P. 3544–3550.
  75. Niobe-Eyangoh S.N., Kuaban C., Sorlin P., Cunin P., Thonnon J., Sola C., Rastogi N., Vincent V., Gutierrez M.C. Genetic biodiversity of Mycobacterium tuberculosis complex strains from patients with pulmonary tuberculosis in Cameroon // J. Clin. Microbiol. — 2003. — Vol. 41. — P. 2547–2553.
  76. Oelemann M.C., Diel R., Vatin V., Haas W., Rusch-Gerdes S., Locht C., Niemann S., Supply P. Assessment of an optimized mycobacterial interspersed repetitive-unit-variable-number tandem-repeat typing system combined with spoligotyping for population-based molecular epidemiology studies of tuberculosis // J. Clin. Microbiol. — 2007. — Vol. 45. — P. 691–697.
  77. Ogarkov O.B., Medvedeva T.V., Nekipelov O.M., Antipina S.L., Men’shikov M.L. Study of DC-SIGN gene polymorphism in patients infected with Mycobacterium tuberculosis strains of different genotypes in the Irkutsk Region // Probl. Tuberk. Bolezn. Legk. — 2007. — N 11. — Р. 37–42.
  78. Pourcel C., Salvignol G., Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies // Microbiology. — 2005. — Vol. 151. — P. 653–663.
  79. Rad M.E., Bifani P., Martin C., Kremer K., Samper S., Rauzier J., Kreiswirth B., Blazquez J., Jouan M., Soolingen D. van, Gicquel B. Mutations in putative mutator genes of Mycobacterium tuberculosis strains of the W-Beijing family // Emerg. Infect. Dis. — 2003. — Vol. 9. — P. 838–845.
  80. Sampson S., Warren R., Richardson M., Spuy G. van der, Helden P. van. IS6110 insertions in Mycobacterium tuberculosis: predominantly into coding regions // J. Clin. Microbiol. — 2001. — Vol. 39, N 9. — P. 3423–3424.
  81. Sebban M., Mokrousov I., Rastogi N., Sola C. A data-mining approach to spacer oligonucleotide typing of Mycobacterium tuberculosis // Bioinformatics. — 2002. — Vol. 18, N 2. — P. 235–243.
  82. Sola C., Filliol I., Legrand E., Mokrousov I., Rastogi N. Mycobacterium tuberculosis phylogeny reconstruction based on combined numerical analysis with IS1081, IS6110, VNTR, and DR-based spoligotyping suggests the existence of two new phylogeographical clades // J. Mol. Evol. — 2001. — Vol. 53. — P. 680–689.
  83. Soolingen D. van, Qian L., Haas P.E.W. de, Douglas J.T., Traore H., Portaels F., Quing Z., Enkhasaikan D., Nymadawa P., Embden J.D.A. van. Predominance of a single genotype of Mycobacterium tuberculosis in countries of East Asia // J. Clin. Microbiol. — 1995. — Vol. 33. — P. 3234–3238.
  84. Sorek R., Kunin V., Hugenholtz P. CRISPR — a widespread system that provides acquired resistance against phages in bacteria and archaea // Nat. Rev. Microbiol. — 2008. — Vol. 6. — P. 181–186.
  85. Sreevatsan S., Pan X., Stockbauer K., Connell N., Kreiswirth B., Whittam T., Musser J.M. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionary recent global dissemination // Proc. Natl. Acad. Sci. USA. — 1997. — Vol. 97. — P. 9869–9874.
  86. Supply P., Allix C., Lesjean S., Cardoso-Oelemann M., Rusch-Gerdes S., Willery E., Savine E., Haas P. de, Deutekom H. van, Roring S., Bifani P., Kurepina N., Kreiswirth B., Sola C., Rastogi N., Vatin V., Gutierrez C.M., Fauville M., Niemann S., Skuce R., Kremer K., Locht C., Soolingen D. van. Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Myco bacterium tuberculosis // J. Clin. Micro biol. — 2006. — Vol. 44. — P. 4498–4510.
  87. Supply P., Lesjean S., Savine E., Kremer K., Soolingen D. van, Locht C. Automated high-throughput genotyping for study of global epidemiology of Mycobacterium tuberculosis based on mycobacterial interspersed repetitive units // J. Clin. Microbiol. — 2001. — Vol. 39. — P. 3563–3571.
  88. Surikova O.V., Voitech D.S., Kuzmicheva G., Tatkov S.I., Mokrousov I.V., Narvskaya O.V., Rot M.A., Soolingen D. van, Filipenko M.L. Efficient differentiation of Mycobacterium tuberculosis strains of the W-Beijing family from Russia using highly polymorphic VNTR loci // Eur. J. Epidemiol. — 2005. — Vol. 20, N 11. — P. 963–974.
  89. Suzuki T., Inoue T. Earliest Evidence of spinal tuberculosis from the Aneolithic Yayoi period in Japan // Int. J. Osteoarchaeol. — 2007. — Vol. 17. — P. 392–402.
  90. Taype Perez C. Host and pathogen genetics in tuberculosis and leishmaniasis. PhD thesis. — Leeds, UK: University of Leeds, 2007.
  91. Toungoussova O., Sandven P., Mariandyshev A., Nizovtseva N., Bjune G., Caugant D.A. Spread of drug-resistant Mycobacterium tuberculosis strains of the Beijing genotype in the Archangel Oblast, Russia // J. Clin. Microbiol. — 2002. — Vol. 40. — P. 1930–1937.
  92. Valcheva V., Mokrousov I., Narvskaya O., Rastogi N., Markova N. Molecular snapshot of drug-resistant and drug-susceptible Mycobacterium tuberculosis strains circulating in Bulgaria // Infect. Genet. Evol. — 2008. — Vol. 8. — P. 657–663.
  93. Valcheva V., Mokrousov I., Panaiotov S., Bachiiska E., Zozio T., Sola C., Markova N., Rastogi N. Bulgarian specificity and controversial phylogeography of Mycobacterium tuberculosis spoligotype ST125_BGR // FEMS Immunol. Clin. Microbiol. — 2010. — Vol. 59. — P. 90–99.
  94. Vultos T. dos, Mestre O., Rauzier J., Golec M., Rastogi N., Rasolofo V., Tonjum T., Sola C., Matic I., Gicquel B. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis // PLoS One. — 2008. — Vol. 3. — P. e1538.
  95. Warren R.M., Streicher E.M., Sampson S.L., Spuy G.D. van der, Richardson M., Nguyen D., Behr M.A., Victor T.C., Helden P.D. van. Microevolution of the direct repeat region of Mycobacterium tuberculosis: implications for interpretation of spoligotyping data // J. Clin. Microbiol. — 2002. — Vol. 40. — P. 4457–4465.
  96. Zhang M., Cong J., Yang Z., Samten B., Barnes P.F. Enhanced capacity of a widespread strain of Mycobacterium tuberculosis to grow in human macrophages // J. Infect. Dis. — 1999. — Vol. 179. — P. 1213–1217.

Copyright (c) 2014 Mokrousov I.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies