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. 1996 Jan;178(1):78–84. doi: 10.1128/jb.178.1.78-84.1996

Host-mediated modification of PvuII restriction in Mycobacterium tuberculosis.

D van Soolingen 1, P E de Haas 1, R M Blumenthal 1, K Kremer 1, M Sluijter 1, J E Pijnenburg 1, L M Schouls 1, J E Thole 1, M W Dessens-Kroon 1, J D van Embden 1, P W Hermans 1
PMCID: PMC177623  PMID: 8550446

Abstract

Restriction endonuclease PvuII plays a central role in restriction fragment length polymorphism analysis of Mycobacterium tuberculosis complex isolates with IS6110 as a genetic marker. We have investigated the basis for an apparent dichotomy in PvuII restriction fragment pattersn observed among strains of the M. tuberculosis complex. The chromosomal regions of two modified PvuII restriction sites, located upstream of the katG gene and downstream of an IS1081 insertion sequence, were studied in more detail. An identical 10-bp DNA sequence (CAGCTGGAGC) containing a PvuII site was found in both regions, and site-directed mutagenesis analysis revealed that this sequence was a target for modification. Strain-specific modification of PvuII sites was identified in DNA from over 80% of the nearly 800 isolates examined. Furthermore, the proportion of modifying and nonmodifying strains differs significantly from country to country.

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Selected References

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  1. ARBER W., DUSSOIX D. Host specificity of DNA produced by Escherichia coli. I. Host controlled modification of bacteriophage lambda. J Mol Biol. 1962 Jul;5:18–36. doi: 10.1016/s0022-2836(62)80058-8. [DOI] [PubMed] [Google Scholar]
  2. Adams G. M., Blumenthal R. M. Gene pvuIIW: a possible modulator of PvuII endonuclease subunit association. Gene. 1995 May 19;157(1-2):193–199. doi: 10.1016/0378-1119(94)00704-v. [DOI] [PubMed] [Google Scholar]
  3. Alland D., Kalkut G. E., Moss A. R., McAdam R. A., Hahn J. A., Bosworth W., Drucker E., Bloom B. R. Transmission of tuberculosis in New York City. An analysis by DNA fingerprinting and conventional epidemiologic methods. N Engl J Med. 1994 Jun 16;330(24):1710–1716. doi: 10.1056/NEJM199406163302403. [DOI] [PubMed] [Google Scholar]
  4. BERTANI G., WEIGLE J. J. Host controlled variation in bacterial viruses. J Bacteriol. 1953 Feb;65(2):113–121. doi: 10.1128/jb.65.2.113-121.1953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beck-Sagué C., Dooley S. W., Hutton M. D., Otten J., Breeden A., Crawford J. T., Pitchenik A. E., Woodley C., Cauthen G., Jarvis W. R. Hospital outbreak of multidrug-resistant Mycobacterium tuberculosis infections. Factors in transmission to staff and HIV-infected patients. JAMA. 1992 Sep 9;268(10):1280–1286. doi: 10.1001/jama.1992.03490100078031. [DOI] [PubMed] [Google Scholar]
  6. Bergmans A. M., Groothedde J. W., Schellekens J. F., van Embden J. D., Ossewaarde J. M., Schouls L. M. Etiology of cat scratch disease: comparison of polymerase chain reaction detection of Bartonella (formerly Rochalimaea) and Afipia felis DNA with serology and skin tests. J Infect Dis. 1995 Apr;171(4):916–923. doi: 10.1093/infdis/171.4.916. [DOI] [PubMed] [Google Scholar]
  7. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blumenthal R. M., Gregory S. A., Cooperider J. S. Cloning of a restriction-modification system from Proteus vulgaris and its use in analyzing a methylase-sensitive phenotype in Escherichia coli. J Bacteriol. 1985 Nov;164(2):501–509. doi: 10.1128/jb.164.2.501-509.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brooks J. E., Nathan P. D., Landry D., Sznyter L. A., Waite-Rees P., Ives C. L., Moran L. S., Slatko B. E., Benner J. S. Characterization of the cloned BamHI restriction modification system: its nucleotide sequence, properties of the methylase, and expression in heterologous hosts. Nucleic Acids Res. 1991 Feb 25;19(4):841–850. doi: 10.1093/nar/19.4.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Butkus V., Klimasauskas S., Petrauskiene L., Maneliene Z., Lebionka A., Janulaitis A. Interaction of AluI, Cfr6I and PvuII restriction-modification enzymes with substrates containing either N4-methylcytosine or 5-methylcytosine. Biochim Biophys Acta. 1987 Aug 25;909(3):201–207. doi: 10.1016/0167-4781(87)90078-9. [DOI] [PubMed] [Google Scholar]
  11. Chen D. F., Liu Q. A., Chen X. W., Zhao X. L., Chen Y. W. The inhibition of restriction endonuclease PvuII cleavage activity by methylation outside its recognition sequence. Nucleic Acids Res. 1991 Oct 25;19(20):5703–5705. doi: 10.1093/nar/19.20.5703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Collins D. M., Stephens D. M. Identification of an insertion sequence, IS1081, in Mycobacterium bovis. FEMS Microbiol Lett. 1991 Sep 15;67(1):11–15. doi: 10.1016/0378-1097(91)90435-d. [DOI] [PubMed] [Google Scholar]
  13. Craig N. L. Tn7: a target site-specific transposon. Mol Microbiol. 1991 Nov;5(11):2569–2573. doi: 10.1111/j.1365-2958.1991.tb01964.x. [DOI] [PubMed] [Google Scholar]
  14. Crawford J. T., Cave M. D., Bates J. H. Evidence for plasmid-mediated restriction-modification in Mycobacterium avium intracellulare. J Gen Microbiol. 1981 Dec;127(2):333–338. doi: 10.1099/00221287-127-2-333. [DOI] [PubMed] [Google Scholar]
  15. Edlin B. R., Tokars J. I., Grieco M. H., Crawford J. T., Williams J., Sordillo E. M., Ong K. R., Kilburn J. O., Dooley S. W., Castro K. G. An outbreak of multidrug-resistant tuberculosis among hospitalized patients with the acquired immunodeficiency syndrome. N Engl J Med. 1992 Jun 4;326(23):1514–1521. doi: 10.1056/NEJM199206043262302. [DOI] [PubMed] [Google Scholar]
  16. Gingeras T. R., Greenough L., Schildkraut I., Roberts R. J. Two new restriction endonucleases from Proteus vulgaris. Nucleic Acids Res. 1981 Sep 25;9(18):4525–4536. doi: 10.1093/nar/9.18.4525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hermans P. W., van Soolingen D., Dale J. W., Schuitema A. R., McAdam R. A., Catty D., van Embden J. D. Insertion element IS986 from Mycobacterium tuberculosis: a useful tool for diagnosis and epidemiology of tuberculosis. J Clin Microbiol. 1990 Sep;28(9):2051–2058. doi: 10.1128/jcm.28.9.2051-2058.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hermans P. W., van Soolingen D., van Embden J. D. Characterization of a major polymorphic tandem repeat in Mycobacterium tuberculosis and its potential use in the epidemiology of Mycobacterium kansasii and Mycobacterium gordonae. J Bacteriol. 1992 Jun;174(12):4157–4165. doi: 10.1128/jb.174.12.4157-4165.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jones W. D., Jr, Greenberg J. Host modification and restriction with a mycobacteriophage isolated from a pseudolysogenic Mycobacterium chelonei. J Gen Microbiol. 1977 Apr;99(2):389–395. doi: 10.1099/00221287-99-2-389. [DOI] [PubMed] [Google Scholar]
  20. Kelleher J. E., Raleigh E. A. Response to UV damage by four Escherichia coli K-12 restriction systems. J Bacteriol. 1994 Oct;176(19):5888–5896. doi: 10.1128/jb.176.19.5888-5896.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kramarov V. M., Smolianinov V. V. DNK-metilaza iz Arthrobacter luteus zashchishchaet DNK ot deistviia saitspetsificheskoi éndonukleazy Alu I. Biokhimiia. 1981 Aug;46(8):1526–1529. [PubMed] [Google Scholar]
  22. Liu Q., Chen X., Zhao X., Chen Y., Chen D. The effect of methylation outside the recognition sequence of restriction endonuclease PvuII on its cleavage efficiency. Gene. 1992 Apr 1;113(1):89–93. doi: 10.1016/0378-1119(92)90673-d. [DOI] [PubMed] [Google Scholar]
  23. McClelland M., Nelson M., Raschke E. Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Res. 1994 Sep;22(17):3640–3659. doi: 10.1093/nar/22.17.3640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nelson P. S., Papas T. S., Schweinfest C. W. Restriction endonuclease cleavage of 5-methyl-deoxycytosine hemimethylated DNA at high enzyme-to-substrate ratios. Nucleic Acids Res. 1993 Feb 11;21(3):681–686. doi: 10.1093/nar/21.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nikolskaya I. I., Lopatina N. G., Sharkova E. V., Suchkov S. V., Somodi P., Földes I., Debov S. S. Sequence specificity of isolated DNA-adenine methylases from Mycobacterium smegmatis (butyricum) and Shigella sonnei 47 cells. Biochem Int. 1985 Mar;10(3):405–413. [PubMed] [Google Scholar]
  26. Patel R., Kvach J. T., Mounts P. Isolation and restriction endonuclease analysis of mycobacterial DNA. J Gen Microbiol. 1986 Feb;132(2):541–551. doi: 10.1099/00221287-132-2-541. [DOI] [PubMed] [Google Scholar]
  27. Rado T. A., Bates J. H., Fitzhugh J. K. Evidence for host-dependent modification and restriction of bacteriophage DNA in Mycobacterium tuberculosis. J Gen Virol. 1976 Jan;30(1):91–97. doi: 10.1099/0022-1317-30-1-91. [DOI] [PubMed] [Google Scholar]
  28. Roberts R. J., Macelis D. REBASE--restriction enzymes and methylases. Nucleic Acids Res. 1994 Sep;22(17):3628–3639. doi: 10.1093/nar/22.17.3628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shankar S., Tyagi A. K. MchAI and MchAII, two class-II restriction endonucleases from Mycobacterium chelonei. Gene. 1993 Sep 30;132(1):119–123. doi: 10.1016/0378-1119(93)90523-6. [DOI] [PubMed] [Google Scholar]
  31. Shankar S., Tyagi A. K. MfoAI, a novel isoschizomer of HaeIII from Mycobacterium fortuitum recognizing 5'-GG/CC-3'. Nucleic Acids Res. 1992 Jun 11;20(11):2890–2890. doi: 10.1093/nar/20.11.2890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shankar S., Tyagi A. K. MhaAI, a novel isoschizomer of PstI from Mycobacterium habana recognizing 5'-CTGCA/G-3'. Nucleic Acids Res. 1992 Jun 11;20(11):2891–2891. doi: 10.1093/nar/20.11.2891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shankar S., Tyagi A. K. Purification and characterization of restriction endonuclease MgoI from Mycobacterium gordonae. Gene. 1993 Sep 6;131(1):153–154. doi: 10.1016/0378-1119(93)90686-w. [DOI] [PubMed] [Google Scholar]
  34. Sharkova E. V., Nikol'skaia I. I., Shomodi P., Fel'desh I., Debov S. S. Vydelenie i fraktsionirovanie DNK-metilaz Mycobacterium butyricum. Vopr Med Khim. 1984 Sep-Oct;30(5):72–76. [PubMed] [Google Scholar]
  35. Small P. M., Hopewell P. C., Singh S. P., Paz A., Parsonnet J., Ruston D. C., Schecter G. F., Daley C. L., Schoolnik G. K. The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N Engl J Med. 1994 Jun 16;330(24):1703–1709. doi: 10.1056/NEJM199406163302402. [DOI] [PubMed] [Google Scholar]
  36. Srivastava R., Gopinathan K. P., Ramakrishnan T. Deoxyribonucleic acid methylation in mycobacteria. J Bacteriol. 1981 Nov;148(2):716–719. doi: 10.1128/jb.148.2.716-719.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stover C. K., de la Cruz V. F., Fuerst T. R., Burlein J. E., Benson L. A., Bennett L. T., Bansal G. P., Young J. F., Lee M. H., Hatfull G. F. New use of BCG for recombinant vaccines. Nature. 1991 Jun 6;351(6326):456–460. doi: 10.1038/351456a0. [DOI] [PubMed] [Google Scholar]
  38. Tao T., Bourne J. C., Blumenthal R. M. A family of regulatory genes associated with type II restriction-modification systems. J Bacteriol. 1991 Feb;173(4):1367–1375. doi: 10.1128/jb.173.4.1367-1375.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tao T., Walter J., Brennan K. J., Cotterman M. M., Blumenthal R. M. Sequence, internal homology and high-level expression of the gene for a DNA-(cytosine N4)-methyltransferase, M.Pvu II. Nucleic Acids Res. 1989 Jun 12;17(11):4161–4175. doi: 10.1093/nar/17.11.4161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zhang Y., Heym B., Allen B., Young D., Cole S. The catalase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature. 1992 Aug 13;358(6387):591–593. doi: 10.1038/358591a0. [DOI] [PubMed] [Google Scholar]
  41. Zhang Y., Young D. Strain variation in the katG region of Mycobacterium tuberculosis. Mol Microbiol. 1994 Oct;14(2):301–308. doi: 10.1111/j.1365-2958.1994.tb01291.x. [DOI] [PubMed] [Google Scholar]
  42. van Embden J. D., Cave M. D., Crawford J. T., Dale J. W., Eisenach K. D., Gicquel B., Hermans P., Martin C., McAdam R., Shinnick T. M. Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol. 1993 Feb;31(2):406–409. doi: 10.1128/jcm.31.2.406-409.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. van Soolingen D., Hermans P. W., de Haas P. E., Soll D. R., van Embden J. D. 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 Nov;29(11):2578–2586. doi: 10.1128/jcm.29.11.2578-2586.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. van Soolingen D., Hermans P. W., de Haas P. E., van Embden J. D. Insertion element IS1081-associated restriction fragment length polymorphisms in Mycobacterium tuberculosis complex species: a reliable tool for recognizing Mycobacterium bovis BCG. J Clin Microbiol. 1992 Jul;30(7):1772–1777. doi: 10.1128/jcm.30.7.1772-1777.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. van Soolingen D., Qian L., de Haas P. E., Douglas J. T., Traore H., Portaels F., Qing H. Z., Enkhsaikan D., Nymadawa P., van Embden J. D. Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia. J Clin Microbiol. 1995 Dec;33(12):3234–3238. doi: 10.1128/jcm.33.12.3234-3238.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. van Soolingen D., de Haas P. E., Haagsma J., Eger T., Hermans P. W., Ritacco V., Alito A., van Embden J. D. Use of various genetic markers in differentiation of Mycobacterium bovis strains from animals and humans and for studying epidemiology of bovine tuberculosis. J Clin Microbiol. 1994 Oct;32(10):2425–2433. doi: 10.1128/jcm.32.10.2425-2433.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. van Soolingen D., de Haas P. E., Hermans P. W., Groenen P. M., van Embden J. D. Comparison of various repetitive DNA elements as genetic markers for strain differentiation and epidemiology of Mycobacterium tuberculosis. J Clin Microbiol. 1993 Aug;31(8):1987–1995. doi: 10.1128/jcm.31.8.1987-1995.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. van Soolingen D., de Haas P. E., Hermans P. W., van Embden J. D. DNA fingerprinting of Mycobacterium tuberculosis. Methods Enzymol. 1994;235:196–205. doi: 10.1016/0076-6879(94)35141-4. [DOI] [PubMed] [Google Scholar]

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