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Veterans Affairs Medical Center, 508 Fulton Street, Building 4, Durham, NC 27705, USA
Department of Medicine, Duke University Medical Center, Box 31080, Durham, NC 27710, USA
ABSTRACT
Genetic loci containing variable numbers of tandem repeats (VNTR loci) form the basis for human gene mapping and identification, forensic analysis and paternity testing. The variability of bacterial tandem repeats has not been systematically studied. Eleven tandem repeat loci in the M. tuberculosis genome were analysed. Five major polymorphic tandem repeat (MPTR) loci contained 15-bp repeats with substantial sequence variation in adjacent copies. Six exact tandem repeat (ETR) loci contained large DNA repeats with identical sequences in adjacent repeats. These 11 loci were amplified in 48 strains to determine the number of tandem repeats at each locus. The strains analysed included 25 wild-type strains of M. tuberculosis, M. bovis, M. africanum and M. microti and 23 substrains of the attenuated M. bovis BCG vaccine. One of the five MPTR loci and all six ETR loci had length polymorphisms corresponding to insertions or deletions of tandem repeats. Most ETR loci were located in intergenic regions where copy number may influence expression of downstream genes. Each ETR locus had multiple alleles in the panel. Combined analysis identified 22 distinct allele profiles in 25 wild-type strains of the M. tuberculosis complex and five allele profiles in 23 M. bovis BCG substrains. Allele profiles were reproducible and stable, as demonstrated by analyses of multiple isolates of particular reference strains obtained from different laboratories. VNTR typing may be generally useful for strain differentiation and evolutionary studies in bacteria.
*Author for correspondence: Richard Frothingham. Tel: +1919 286 0411 ext. 6566. Fax: +1 919 286 0264. e-mail: richard.frothingham@duke.edu
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P. J. Easterbrook, A. Gibson, S. Murad, D. Lamprecht, N. Ives, A. Ferguson, O. Lowe, P. Mason, A. Ndudzo, A. Taziwa, et al. High Rates of Clustering of Strains Causing Tuberculosis in Harare, Zimbabwe: a Molecular Epidemiological Study J. Clin. Microbiol., October 1, 2004; 42(10): 4536 - 4544. [Abstract] [Full Text] [PDF]
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J. T. Evans, P. M. Hawkey, E. G. Smith, K. A. Boese, R. E. Warren, and G. Hong Automated High-Throughput Mycobacterial Interspersed Repetitive Unit Typing of Mycobacterium tuberculosis Strains by a Combination of PCR and Nondenaturing High-Performance Liquid Chromatography J. Clin. Microbiol., September 1, 2004; 42(9): 4175 - 4180. [Abstract] [Full Text] [PDF]
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L. M. Schouls, H. G. J. van der Heide, L. Vauterin, P. Vauterin, and F. R. Mooi Multiple-Locus Variable-Number Tandem Repeat Analysis of Dutch Bordetella pertussis Strains Reveals Rapid Genetic Changes with Clonal Expansion during the Late 1990s J. Bacteriol., August 15, 2004; 186(16): 5496 - 5505. [Abstract] [Full Text] [PDF]
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K. Brudey, M. Gordon, P. Mostrom, L. Svensson, B. Jonsson, C. Sola, M. Ridell, and N. Rastogi Molecular Epidemiology of Mycobacterium tuberculosis in Western Sweden J. Clin. Microbiol., July 1, 2004; 42(7): 3046 - 3051. [Abstract] [Full Text] [PDF]
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M. Fabre, J.-L. Koeck, P. Le Fleche, F. Simon, V. Herve, G. Vergnaud, and C. Pourcel High Genetic Diversity Revealed by Variable-Number Tandem Repeat Genotyping and Analysis of hsp65 Gene Polymorphism in a Large Collection of "Mycobacterium canettii" Strains Indicates that the M. tuberculosis Complex Is a Recently Emerged Clone of "M. canettii" J. Clin. Microbiol., July 1, 2004; 42(7): 3248 - 3255. [Abstract] [Full Text] [PDF]
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A. L. Gibson, G. Hewinson, T. Goodchild, B. Watt, A. Story, J. Inwald, and F. A. Drobniewski Molecular Epidemiology of Disease Due to Mycobacterium bovis in Humans in the United Kingdom J. Clin. Microbiol., January 1, 2004; 42(1): 431 - 434. [Abstract] [Full Text] [PDF]
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L. Tazi, J. El Baghdadi, S. Lesjean, C. Locht, P. Supply, M. Tibayrenc, and A.-L. Banuls Genetic Diversity and Population Structure of Mycobacterium tuberculosis in Casablanca, a Moroccan City with High Incidence of Tuberculosis J. Clin. Microbiol., January 1, 2004; 42(1): 461 - 466. [Abstract] [Full Text] [PDF]
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I. de Benito, M. E. Cano, J. Aguero, and J. M. G. Lobo A polymorphic tandem repeat potentially useful for typing in the chromosome of Yersinia enterocolitica Microbiology, January 1, 2004; 150(1): 199 - 204. [Abstract] [Full Text] [PDF]
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 N. H. Smith, J. Dale, J. Inwald, S. Palmer, S. V. Gordon, R. G. Hewinson, and J. M. Smith The population structure of Mycobacterium bovis in Great Britain: Clonal expansion PNAS, December 9, 2003; 100(25): 15271 - 15275. [Abstract] [Full Text] [PDF]
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A. C. Noller, M. C. McEllistrem, A. G. F. Pacheco, D. J. Boxrud, and L. H. Harrison Multilocus Variable-Number Tandem Repeat Analysis Distinguishes Outbreak and Sporadic Escherichia coli O157:H7 Isolates J. Clin. Microbiol., December 1, 2003; 41(12): 5389 - 5397. [Abstract] [Full Text] [PDF]
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T. Stefanova, M. Chouchkova, J. Hinds, P. D. Butcher, J. Inwald, J. Dale, S. Palmer, R. G. Hewinson, and S. V. Gordon Genetic Composition of Mycobacterium bovis BCG Substrain Sofia J. Clin. Microbiol., November 1, 2003; 41(11): 5349 - 5349. [Full Text] [PDF]
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 P. F. Barnes and M. D. Cave Molecular Epidemiology of Tuberculosis N. Engl. J. Med., September 18, 2003; 349(12): 1149 - 1156. [Full Text] [PDF]
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R. S. Spurgiesz, T. N. Quitugua, K. L. Smith, J. Schupp, E. G. Palmer, R. A. Cox, and P. Keim Molecular Typing of Mycobacterium tuberculosis by Using Nine Novel Variable-Number Tandem Repeats across the Beijing Family and Low-Copy-Number IS6110 Isolates J. Clin. Microbiol., September 1, 2003; 41(9): 4224 - 4230. [Abstract] [Full Text] [PDF]
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P. M. Hawkey, E. G. Smith, J. T. Evans, P. Monk, G. Bryan, H. H. Mohamed, M. Bardhan, and R. N. Pugh Mycobacterial Interspersed Repetitive Unit Typing of Mycobacterium tuberculosis Compared to IS6110-Based Restriction Fragment Length Polymorphism Analysis for Investigation of Apparently Clustered Cases of Tuberculosis J. Clin. Microbiol., August 1, 2003; 41(8): 3514 - 3520. [Abstract] [Full Text] [PDF]
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J. Inwald, J. Hinds, S. Palmer, J. Dale, P. D. Butcher, R. G. Hewinson, and S. V. Gordon Genomic Analysis of Mycobacterium tuberculosis Complex Strains Used for Production of Purified Protein Derivative J. Clin. Microbiol., August 1, 2003; 41(8): 3929 - 3932. [Abstract] [Full Text] [PDF]
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J. T. Douglas, L. Qian, J. C. Montoya, J. M. Musser, J. D. A. Van Embden, D. Van Soolingen, and K. Kremer Characterization of the Manila Family of Mycobacterium tuberculosis J. Clin. Microbiol., June 1, 2003; 41(6): 2723 - 2726. [Abstract] [Full Text] [PDF]
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A. Sabat, J. Krzyszton-Russjan, W. Strzalka, R. Filipek, K. Kosowska, W. Hryniewicz, J. Travis, and J. Potempa New Method for Typing Staphylococcus aureus Strains: Multiple-Locus Variable-Number Tandem Repeat Analysis of Polymorphism and Genetic Relationships of Clinical Isolates J. Clin. Microbiol., April 1, 2003; 41(4): 1801 - 1804. [Abstract] [Full Text] [PDF]
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S. Ferdinand, C. Sola, B. Verdol, E. Legrand, K. S. Goh, M. Berchel, A. Aubery, M. Timothee, P. Joseph, J. W. Pape, et al. Molecular Characterization and Drug Resistance Patterns of Strains of Mycobacterium tuberculosis Isolated from Patients in an AIDS Counseling Center in Port-au-Prince, Haiti: a 1-Year Study J. Clin. Microbiol., February 1, 2003; 41(2): 694 - 702. [Abstract] [Full Text] [PDF]
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E. Savine, R. M. Warren, G. D. van der Spuy, N. Beyers, P. D. van Helden, C. Locht, and P. Supply Stability of Variable-Number Tandem Repeats of Mycobacterial Interspersed Repetitive Units from 12 Loci in Serial Isolates of Mycobacterium tuberculosis J. Clin. Microbiol., December 1, 2002; 40(12): 4561 - 4566. [Abstract] [Full Text] [PDF]
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A. G. M. van der Zanden, K. Kremer, L. M. Schouls, K. Caimi, A. Cataldi, A. Hulleman, N. J. D. Nagelkerke, and D. van Soolingen Improvement of Differentiation and Interpretability of Spoligotyping for Mycobacterium tuberculosis Complex Isolates by Introduction of New Spacer Oligonucleotides J. Clin. Microbiol., December 1, 2002; 40(12): 4628 - 4639. [Abstract] [Full Text] [PDF]
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 M. M. Gutacker, J. C. Smoot, C. A. L. Migliaccio, S. M. Ricklefs, S. Hua, D. V. Cousins, E. A. Graviss, E. Shashkina, B. N. Kreiswirth, and J. M. Musser Genome-Wide Analysis of Synonymous Single Nucleotide Polymorphisms in Mycobacterium tuberculosis Complex Organisms: Resolution of Genetic Relationships Among Closely Related Microbial Strains Genetics, December 1, 2002; 162(4): 1533 - 1543. [Abstract] [Full Text] [PDF]
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N. F. Mistry, A. M. Iyer, D. T. B. D'souza, G. M. Taylor, D. B. Young, and N. H. Antia Spoligotyping of Mycobacterium tuberculosis Isolates from Multiple-Drug-Resistant Tuberculosis Patients from Bombay, India J. Clin. Microbiol., July 1, 2002; 40(7): 2677 - 2680. [Abstract] [Full Text] [PDF]
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S. Roring, A. Scott, D. Brittain, I. Walker, G. Hewinson, S. Neill, and R. Skuce Development of Variable-Number Tandem Repeat Typing of Mycobacterium bovis: Comparison of Results with Those Obtained by Using Existing Exact Tandem Repeats and Spoligotyping J. Clin. Microbiol., June 1, 2002; 40(6): 2126 - 2133. [Abstract] [Full Text] [PDF]
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C. M. Gilpin, D. J. Dawson, G. O'Kane, J. G. Armstrong, and C. Coulter Failure of Commercial Ligase Chain Reaction To Detect Mycobacterium tuberculosis DNA in Sputum Samples from a Patient with Smear-Positive Pulmonary Tuberculosis Due to a Deletion of the Target Region J. Clin. Microbiol., June 1, 2002; 40(6): 2305 - 2307. [Abstract] [Full Text] [PDF]
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L. S. Cowan, L. Mosher, L. Diem, J. P. Massey, and J. T. Crawford Variable-Number Tandem Repeat Typing of Mycobacterium tuberculosis Isolates with Low Copy Numbers of IS6110 by Using Mycobacterial Interspersed Repetitive Units J. Clin. Microbiol., May 1, 2002; 40(5): 1592 - 1602. [Abstract] [Full Text] [PDF]
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R. A. Skuce, T. P. McCorry, J. F. McCarroll, S. M. M. Roring, A. N. Scott, D. Brittain, S. L. Hughes, R. G. Hewinson, and S. D. Neill Discrimination of Mycobacterium tuberculosis complex bacteria using novel VNTR-PCR targets Microbiology, February 1, 2002; 148(2): 519 - 528. [Abstract] [Full Text] [PDF]
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H. Cameron, R. O'Brien, A. Murray, B. Cryan, R. Hone, and M. Rogers Evaluation of the Mycobacterium bovis Restriction Fragment Length Polymorphism Probe pUCD, in Combination with the Direct Repeat Probe, for Molecular Typing of Mycobacterium tuberculosis Strains in Ireland J. Clin. Microbiol., December 1, 2001; 39(12): 4404 - 4406. [Abstract] [Full Text] [PDF]
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K. G. Dobbs, K. H. Lok, F. Bruce, D. Mulcahy, W. H. Benjamin, and N. E. Dunlap Value of Mycobacterium tuberculosis Fingerprinting as a Tool in a Rural State Surveillance Program Chest, December 1, 2001; 120(6): 1877 - 1882. [Abstract] [Full Text] [PDF]
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P. Supply, S. Lesjean, E. Savine, K. Kremer, D. van Soolingen, and C. Locht Automated High-Throughput Genotyping for Study of Global Epidemiology of Mycobacterium tuberculosis Based on Mycobacterial Interspersed Repetitive Units J. Clin. Microbiol., October 1, 2001; 39(10): 3563 - 3571. [Abstract] [Full Text] [PDF]
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N. Haddad, A. Ostyn, C. Karoui, M. Masselot, M. F. Thorel, S. L. Hughes, J. Inwald, R. G. Hewinson, and B. Durand Spoligotype Diversity of Mycobacterium bovis Strains Isolated in France from 1979 to 2000 J. Clin. Microbiol., October 1, 2001; 39(10): 3623 - 3632. [Abstract] [Full Text] [PDF]
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A. Johansson, I. Goransson, P. Larsson, and A. Sjostedt Extensive Allelic Variation among Francisella tularensis Strains in a Short-Sequence Tandem Repeat Region J. Clin. Microbiol., September 1, 2001; 39(9): 3140 - 3146. [Abstract] [Full Text] [PDF]
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R. E. L. Barlow, D. M. Gascoyne-Binzi, S. H. Gillespie, A. Dickens, S. Qamer, and P. M. Hawkey Comparison of Variable Number Tandem Repeat and IS6110-Restriction Fragment Length Polymorphism Analyses for Discrimination of High- and Low-Copy-Number IS6110 Mycobacterium tuberculosis Isolates J. Clin. Microbiol., July 1, 2001; 39(7): 2453 - 2457. [Abstract] [Full Text] [PDF]
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C. Sola, S. Ferdinand, C. Mammina, A. Nastasi, and N. Rastogi Genetic Diversity of Mycobacterium tuberculosis in Sicily Based on Spoligotyping and Variable Number of Tandem DNA Repeats and Comparison with a Spoligotyping Database for Population-Based Analysis J. Clin. Microbiol., April 1, 2001; 39(4): 1559 - 1565. [Abstract] [Full Text]
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W. H. Benjamin Jr., K. H. Lok, R. Harris, N. Brook, L. Bond, D. Mulcahy, N. Robinson, V. Pruitt, d. P. Kirkpatrick, M. E. Kimerling, et al. Identification of a Contaminating Mycobacterium tuberculosis Strain with a Transposition of an IS6110 Insertion Element Resulting in an Altered Spoligotype J. Clin. Microbiol., March 1, 2001; 39(3): 1092 - 1096. [Abstract] [Full Text]
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E. Mazars, S. Lesjean, A.-L. Banuls, M. Gilbert, V. Vincent, B. Gicquel, M. Tibayrenc, C. Locht, and P. Supply High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology PNAS, February 13, 2001; 98(4): 1901 - 1906. [Abstract] [Full Text] [PDF]
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C. Viana-Niero, C. Gutierrez, C. Sola, I. Filliol, F. Boulahbal, V. Vincent, and N. Rastogi Genetic Diversity of Mycobacterium africanum Clinical Isolates Based on IS6110-Restriction Fragment Length Polymorphism Analysis, Spoligotyping, and Variable Number of Tandem DNA Repeats J. Clin. Microbiol., January 1, 2001; 39(1): 57 - 65. [Abstract] [Full Text]
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D. M. Gascoyne-Binzi, R. E. L. Barlow, R. Frothingham, G. Robinson, T. A. Collyns, R. Gelletlie, and P. M. Hawkey Rapid Identification of Laboratory Contamination with Mycobacterium tuberculosis Using Variable Number Tandem Repeat Analysis J. Clin. Microbiol., January 1, 2001; 39(1): 69 - 74. [Abstract] [Full Text]
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Y.-C. Shin, H. Lee, H. Lee, G. P. Walsh, J.-D. Kim, and S.-N. Cho Variable Numbers of TTC Repeats in Mycobacterium leprae DNA from Leprosy Patients and Use in Strain Differentiation J. Clin. Microbiol., December 1, 2000; 38(12): 4535 - 4538. [Abstract] [Full Text]
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