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Mutations in Streptomycin Resistance Genes and Their Relationship to Streptomycin Resistance and Lineage of Mycobacterium tuberculosis Thai Isolates

  • Hlaing, Yin Moe (Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University) ;
  • Tongtawe, Pongsri (Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University) ;
  • Tapchaisri, Pramuan (Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University) ;
  • Thanongsaksrikul, Jeeraphong (Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University) ;
  • Thawornwan, Unchana (Bamrasnaradura Infectious Diseases Institute) ;
  • Archanachan, Buppa (Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University) ;
  • Srimanote, Potjanee (Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University)
  • Received : 2016.12.04
  • Accepted : 2017.02.15
  • Published : 2017.04.30

Abstract

Background: Streptomycin (SM) is recommended by the World Health Organization (WHO) as a part of standard regimens for retreating multidrug-resistant tuberculosis (MDR-TB) cases. The incidence of MDR-TB in retreatment cases was 19% in Thailand. To date, information on SM resistance (SMR) gene mutations correlated to the SMR of Mycobacterium tuberculosis Thai isolates is limited. In this study, the mutations in rpsL, rrs, gidB, and whiB7 were investigated and their association to SMR and the lineage of M. tuberculosis were explored. Methods: The lineages of 287 M. tuberculosis collected from 2007 to 2011 were identified by spoligotyping. Drug susceptibility profiles were evaluated by the absolute concentration method. Mutations in SMR genes of 46 SM-resistant and 55 SM-susceptible isolates were examined by DNA sequencing. Results: Three rpsL (Lys43Arg, Lys88Arg, and Lys88Thr) and two gidB (Trp45Ter and Gly69Asp) mutations were present exclusively in the SM resistant M. tuberculosis. Lys43Arg rpsL was the most predominant SMR mutations (69.6%) and prevailed among Beijing isolates (p<0.001). No SMR-related mutation in was found rrs. The combination of rpsL and gidB mutations provided 76.1% sensitivity for detecting SMR in M. tuberculosis Thai isolates. whiB7 was not responsible for SMR in SM resistant isolates lacking rpsL and rrs mutations. The significance of the three gidB mutations, 276A>C, 615A>G, and 330G>T, as lineage signatures for Beijing and EAI were underscored. This study identified 423G>A gidB as a novel sub-lineage marker for EAI6-BGD1. Conclusion: Our study suggested that the majority of SMR in M. tuberculosis Thai isolates were responsible by rpsL and gidB polymorphisms constantly providing the novel lineage specific makers.

Keywords

References

  1. World Health Organization. Treatment of tuberculosis guidelines. 4th ed. WHO/HTM [Internet]. Geneva: World Health Organization; 2010 [cited 2015 Oct 12]. Available from: http://www.who.int/tb/publications/2010/9789241547833/en/.
  2. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 2000;407:340-8. https://doi.org/10.1038/35030019
  3. Meier A, Sander P, Schaper KJ, Scholz M, Bottger EC. Correlation of molecular resistance mechanisms and phenotypic resistance levels in streptomycin-resistant Mycobacterium tuberculosis. Antimicrob Agents Chemother 1996;40:2452-4.
  4. Zhang Y, Yew WW. Mechanisms of drug resistance in Mycobacterium tuberculosis . Int J Tuberc Lung Dis 2009;13:1320-30.
  5. Okamoto S, Tamaru A, Nakajima C, Nishimura K, Tanaka Y, Tokuyama S, et al. Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol Microbiol 2007;63:1096-106. https://doi.org/10.1111/j.1365-2958.2006.05585.x
  6. Spies FS, Ribeiro AW, Ramos DF, Ribeiro MO, Martin A, Palomino JC, et al. Streptomycin resistance and lineage-specific polymorphisms in Mycobacterium tuberculosis gidB gene. J Clin Microbiol 2011;49:2625-30. https://doi.org/10.1128/JCM.00168-11
  7. Zhao LL, Liu HC, Sun Q, Xiao TY, Zhao XQ, Li GL, et al. Identification of mutations conferring streptomycin resistance in multidrug-resistant tuberculosis of China. Diagn Microbiol Infect Dis 2015;83:150-3. https://doi.org/10.1016/j.diagmicrobio.2015.06.020
  8. Smittipat N, Juthayothin T, Billamas P, Jaitrong S, Rukseree K, Dokladda K, et al. Mutations in rrs, rpsL and gidB in streptomycin-resistant Mycobacterium tuberculosis isolates from Thailand. J Glob Antimicrob Resist 2016;4:5-10. https://doi.org/10.1016/j.jgar.2015.11.009
  9. Morris RP, Nguyen L, Gatfield J, Visconti K, Nguyen K, Schnappinger D, et al. Ancestral antibiotic resistance in Mycobacterium tuberculosis . Proc Natl Acad Sci U S A 2005;102:12200-5. https://doi.org/10.1073/pnas.0505446102
  10. Reeves AZ, Campbell PJ, Sultana R, Malik S, Murray M, Plikaytis BB, et al. Aminoglycoside cross-resistance in Mycobacterium tuberculosis due to mutations in the 5' untranslated region of whiB7. Antimicrob Agents Chemother 2013;57:1857-65. https://doi.org/10.1128/AAC.02191-12
  11. Villellas C, Aristimuno L, Vitoria MA, Prat C, Blanco S, Garcia de Viedma D, et al. Analysis of mutations in streptomycinresistant strains reveals a simple and reliable genetic marker for identification of the Mycobacterium tuberculosis Beijing genotype. J Clin Microbiol 2013;51:2124-30. https://doi.org/10.1128/JCM.01944-12
  12. World Health Organization. Global tuberculosis report 2015. WHO/HTM/TB/2015.22 [Internet]. Geneva: World Health Organization; 2015 [cited 2015 Nov 20]. Available from: http://www.who.int/tb/publications/global_report/en/.
  13. World Health Organization. Companion handbook to the WHO guidelines for the programmatic management of drugresistant tuberculosis. WHO/HTM/TB/2014.11 [Internet]. Geneva: World Health Organization; 2014 [cited 2014 Oct 12]. Available from: http://www.who.int/tb/publications/pmdt_companionhandbook/en/.
  14. Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 1997;35:907-14.
  15. TB-Insight. About TB-Lineage [Internet]. TB Insight; 2015 [cited 2015 Nov 28]. Available from: http://tbinsight.cs.rpi.edu/about_ tb_lineage.html.
  16. van Soolingen D, Hermans PW, de Haas PE, Soll DR, van Embden JD. Occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J Clin Microbiol 1991;29:2578-86.
  17. Meier A, Kirschner P, Bange FC, Vogel U, Bottger EC. Genetic alterations in streptomycin-resistant Mycobacterium tuberculosis : mapping of mutations conferring resistance. Antimicrob Agents Chemother 1994;38:228-33. https://doi.org/10.1128/AAC.38.2.228
  18. Springer B, Stockman L, Teschner K, Roberts GD, Bottger EC. Two-laboratory collaborative study on identification of mycobacteria: molecular versus phenotypic methods. J Clin Microbiol 1996;34:296-303.
  19. Via LE, Cho SN, Hwang S, Bang H, Park SK, Kang HS, et al. Polymorphisms associated with resistance and cross-resistance to aminoglycosides and capreomycin in Mycobacterium tuberculosis isolates from South Korean patients with drug-resistant tuberculosis. J Clin Microbiol 2010;48:402-11. https://doi.org/10.1128/JCM.01476-09
  20. Sowajassatakul A, Prammananan T, Chaiprasert A, Phunpruch S. Molecular characterization of amikacin, kanamycin and capreomycin resistance in M/XDR-TB strains isolated in Thailand. BMC Microbiol 2014;14:165. https://doi.org/10.1186/1471-2180-14-165
  21. Chen J, Tsolaki AG, Shen X, Jiang X, Mei J, Gao Q. Deletiontargeted multiplex PCR (DTM-PCR) for identification of Beijing/W genotypes of Mycobacterium tuberculosis. Tuberculosis (Edinb) 2007;87:446-9. https://doi.org/10.1016/j.tube.2007.05.014
  22. BLAST: Basic Local Alignment Search Tool [Internet]. Bethesda: National Center for Biotechnology Information; 2015 [cited 2015 Feb 4]. Available from: http://blast.ncbi.nlm.nih.gov/Blast.cgi.
  23. Lee AS, Ong DC, Wong JC, Siu GK, Yam WC. High-resolution melting analysis for the rapid detection of fluoroquinolone and streptomycin resistance in Mycobacterium tuberculosis. PLoS One 2012;7:e31934. https://doi.org/10.1371/journal.pone.0031934
  24. Morita M, Ohnishi M, Arakawa E, Bhuiyan NA, Nusrin S, Alam M, et al. Development and validation of a mismatch amplification mutation PCR assay to monitor the dissemination of an emerging variant of Vibrio cholerae O1 biotype El Tor. Microbiol Immunol 2008;52:314-7. https://doi.org/10.1111/j.1348-0421.2008.00041.x
  25. Wan X, Qian L, Hou S, Drees KP, Foster JT, Douglas JT. Complete genome sequences of Beijing and Manila family strains of Mycobacterium tuberculosis. Genome Announc 2014;2:e01135-14.
  26. Kornder JD. Streptomycin revisited: molecular action in the microbial cell. Med Hypotheses 2002;58:34-46. https://doi.org/10.1054/mehy.2001.1450
  27. Nhu NT, Lan NT, Phuong NT, Chau N, Farrar J, Caws M. Association of streptomycin resistance mutations with level of drug resistance and Mycobacterium tuberculosis genotypes. Int J Tuberc Lung Dis 2012;16:527-31. https://doi.org/10.5588/ijtld.11.0202
  28. Sun YJ, Luo JT, Wong SY, Lee AS. Analysis of rpsL and rrs mutations in Beijing and non-Beijing streptomycin-resistant Mycobacterium tuberculosis isolates from Singapore. Clin Microbiol Infect 2010;16:287-9. https://doi.org/10.1111/j.1469-0691.2009.02800.x
  29. Van Rie A, Warren R, Mshanga I, Jordaan AM, van der Spuy GD, Richardson M, et al. Analysis for a limited number of gene codons can predict drug resistance of Mycobacterium tuberculosis in a high-incidence community. J Clin Microbiol 2001;39:636-41. https://doi.org/10.1128/JCM.39.2.636-641.2001
  30. Siddiqi N, Shamim M, Hussain S, Choudhary RK, Ahmed N, Prachee, et al. Molecular characterization of multidrug-resistant isolates of Mycobacterium tuberculosis from patients in North India. Antimicrob Agents Chemother 2002;46:443-50. https://doi.org/10.1128/AAC.46.2.443-450.2002
  31. Feuerriegel S, Oberhauser B, George AG, Dafae F, Richter E, Rusch-Gerdes S, et al. Sequence analysis for detection of firstline drug resistance in Mycobacterium tuberculosis strains from a high-incidence setting. BMC Microbiol 2012;12:90. https://doi.org/10.1186/1471-2180-12-90
  32. Jnawali HN, Hwang SC, Park YK, Kim H, Lee YS, Chung GT, et al. Characterization of mutations in multi- and extensive drug resistance among strains of Mycobacterium tuberculosis clinical isolates in Republic of Korea. Diagn Microbiol Infect Dis 2013;76:187-96. https://doi.org/10.1016/j.diagmicrobio.2013.02.035
  33. Tudo G, Rey E, Borrell S, Alcaide F, Codina G, Coll P, et al. Characterization of mutations in streptomycin-resistant Mycobacterium tuberculosis clinical isolates in the area of Barcelona. J Antimicrob Chemother 2010;65:2341-6. https://doi.org/10.1093/jac/dkq322
  34. Ramaswamy SV, Dou SJ, Rendon A, Yang Z, Cave MD, Graviss EA. Genotypic analysis of multidrug-resistant Mycobacterium tuberculosis isolates from Monterrey, Mexico. J Med Microbiol 2004;53(Pt 2):107-13. https://doi.org/10.1099/jmm.0.05343-0
  35. Jagielski T, Ignatowska H, Bakula Z, Dziewit L, Napiorkowska A, Augustynowicz-Kopec E, et al. Screening for streptomycin resistance-conferring mutations in Mycobacterium tuberculosis clinical isolates from Poland. PLoS One 2014;9:e100078. https://doi.org/10.1371/journal.pone.0100078
  36. Comas I, Homolka S, Niemann S, Gagneux S. Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS One 2009;4:e7815. https://doi.org/10.1371/journal.pone.0007815

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