IS6110 functions as a mobile, monocyte-activated promoter in Mycobacterium tuberculosis

Molecular Microbiology

Volumn 52, Issue 4, 2004, Pages 999-1012

  Safi, Hassan ^a   Barnes, Peter F ^a,b   Lakey, David L ^a,b   Shams, Homayoun ^a   Samten, Buka ^a   Vankayalapati, Ramakrishna ^a   Howard, Susan T ^a  

^a UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

^b Health Science Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; CONTROLLED STUDY; GENE ACTIVATION; GENE CONTROL; GENE INSERTION SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STATISTICAL SIGNIFICANCE; UPREGULATION;

ARTIFICIAL GENE FUSION; CELL LINE; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, MESSENGER; TERMINAL REPEAT SEQUENCES; TRANSCRIPTION INITIATION SITE; UP-REGULATION;

ACTINOBACTERIA (CLASS); BACTERIA (MICROORGANISMS); INSERTION SEQUENCES; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTA; TRANSPOSONS; UNCULTURED ACTINOMYCETE; UNIDENTIFIED INSERTION SEQUENCE;

EID: 3142706519     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04037.x     Document Type: Article

References (72)

1. Alland, D., Whittam, T.S., Murray, M.B., Cave, M.D., Hazbon, M.H., Dix, K., et al. (2003) Modeling bacterial evolution with comparative-genome-based marker systems: application to Mycobacterium tuberculosis evolution and pathogenesis. J Bacteriol 185: 3392-3399.
2. Bannantine, J.P., Barletta, R.G., Thoen, C.O., and Andrews, R.E., Jr (1997) Identification of Mycobacterium paratuberculosis gene expression signals. Microbiology 143: 921-928.
3. Banu, S., Honore, N., Saint-Joanis, B., Philpott, D., Prevost, M.C., and Cole, S.T. (2002) Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens? Mol Microbiol 44: 9-19.
4. Barnes, P.F., Yang, Z., Preston-Martin, S., Pogoda, J.M., Jones, B.E., Otaya, M., et al. (1997) Patterns of tuberculosis transmission in Central Los Angeles. JAMA 278: 1159-1163.
5. Bashyam, M.D., Kaushal, D., Dasgupta, S.K., and Tyagi, A.K. (1996) A study of mycobacterial transcriptional apparatus: identification of novel features in promoter elements. J Bacteriol 178: 4847-4853.
6. F activity by distinct mechanisms. Mol Microbiol 45: 1527-1540.
7. Beggs, M.L., Eisenach, K.D., and Cave, M.D. (2000) Mapping of IS6110 insertion sites in two epidemic strains of Mycobacterium tuberculosis. J Clin Microbiol 38: 2923-2928.
8. Bifani, P.J., Mathema, B., Kurepina, N.E., and Kreiswirth, B.N. (2002) Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains. Trends Microbiol 10: 45-52.
9. Bjedov, I., Tenaillon, O., Gerard, B., Souza, V., Denamur, E., Radman, M., et al. (2003) Stress-induced mutagenesis in bacteria. Science 300: 1404-1409.
10. Brennan, M.J., Delogu, G., Chen, Y., Bardarov, S., Kriakov, J., Alavi, M., and Jacobs, W.R., Jr (2001) Evidence that mycobacterial PE_PGRS proteins are cell surface constituents that influence interactions with other cells. Infect Immun 69: 7326-7333.
11. Brosch, R., Philipp, W.J., Stavropoulos, E., Colston, M.J., Cole, S.T., and Gordon, S.V. (1999) Genomic analysis reveals variation between Mycobacterium tuberculosis H37Rv and the attenuated M. tuberculosis H37Ra strain. Infect Immun 67: 5768-5774.
12. Brosch, R., Gordon, S.V., Eiglmeier, K., Garnier, T., Tekaia, F., Yeramian, E., and Cole, S.T. (2000) Genomics, biology, and evolution of the Mycobacterium tuberculosis complex. In Molecular Genetics of Mycobacteria, Vol. 19-36. Hatfull, G.F., and Jacobs, W.R., Jr (eds). Washington, DC: American Society for Microbiology Press.
13. Charlier, D., Piette, J., and Glansdorff, N. (1982) IS3 can function as a mobile promoter in E. coli. Nucleic Acids Res 10: 5935-5948.
14. Cole, S.T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
15. Couto, I., Wu, S.W., Tomasz, A., and de Lencastre, H. (2003) Development of methicillin resistance in clinical isolates of Staphylococcus sciuri by transcriptional activation of the mecA homologue native to the species. J Bacteriol 185: 645-653.
16. Delogu, G., and Brennan, M.J. (2001) Comparative immune response to PE and PE-PGRS antigens of Mycobacterium tuberculosis. Infect Immun 69: 5606-5611.
17. DeShazer, D., Wood, G.E., and Friedman, R.L. (1994) Molecular characterization of catalase from Bordetella pertussis: identification of the katA promoter in an upstream insertion sequence. Mol Microbiol 14: 123-130.
18. Edwards, R., and Read, P.N. (2000) Expression of the carbapenemase gene (cfiA) in Bacteroides fragilis. J Antimicrob Chemother 46: 1009-1012.
19. van Embden, J.D., Cave, M.D., Crawford, J.T., Dale, J.W., Eisenach, K.D., Gicquel, B., et al. (1993) Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol 31: 406-409.
20. Espitia, C., Laclette, J.P., Mondragon-Palomino, M., Amador, A., Campuzano, J., Martens, A., et al. (1999) The PE-PGRS glycine-rich proteins of Mycobacterium tuberculosis: a new family of fibronectin-binding proteins? Microbiology 145: 3487-3495.
21. Fang, Z., and Forbes, K.J. (1997) A Mycobacterium tuberculosis IS6110 preferential locus (ipl) for insertion into the genome. J Clin Microbiol 35: 479-481.
22. Fang, Z., Morrison, N., Watt, B., Doig, C., and Forbes, K.J. (1998) IS6110 transposition and evolutionary scenario of the direct repeat locus in a group of closely related Mycobacterium tuberculosis strains. J Bacteriol 180: 2102-2109.
23. Fang, Z., Doig, C., Kenna, D.T., Smittipat, N., Palittapongarnpim, P., Watt, B., and Forbes, K.J. (1999) IS6110-mediated deletions of wild-type chromosomes of Mycobacterium tuberculosis. J Bacteriol 181: 1014-1020.
24. Fang, Z., Kenna, D.T., Doig, C., Smittipat, D.N., Palittapongarnpim, P., Watt, B., and Forbes, K.J. (2001) Molecular evidence for independent occurrence of IS6110 insertions at the same sites of the genome of Mycobacterium tuberculosis in different clinical isolates. J Bacteriol 183: 5279-5284.
25. Fraaije, M.W., van den Heuvel, R.H., van Berkel, W.J., and Mattevi, A. (1999) Covalent flavinylation is essential for efficient redox catalysis in vanillyl-alcohol oxidase. J Biol Chem 274: 35514-35520.
26. Ghanekar, K., McBride, A., Dellagostin, O., Thorne, S., Mooney, R., and McFadden, J. (1999) Stimulation of transposition of the Mycobacterium tuberculosis insertion sequence IS6110 by exposure to a microaerobic environment. Mol Microbiol 33: 982-993.
27. Gomez, M., and Smith, I. (2000) Determinants of mycobacterial gene expression. In Molecular Genetics of Mycobacteria. Hatfull, G.F., and Jacobs, W.R., Jr (eds). Washington, DC: American Society for Microbiology Press, pp. 111-129.
28. Goosen, N., and van de Putte, P. (1986) Role of ner protein in bacteriophage Mu transposition. J Bacteriol 167: 503-507.
29. Hall, B.G. (1999a) Transposable elements as activators of cryptic genes in E. coli. Genetica 107: 181-187.
30. Hall, B.G. (1999b) Spectra of spontaneous growth-dependent and adaptive mutations at ebgR. J Bacteriol 181: 1149-1155.
31. Ho, T.B.L., Robertson, B.D., Taylor, G.M., Shaw, R.J., and Young, D.B. (2000) Comparison of Mycobacterium tuberculosis genomes reveals frequent deletions in a 20 kb variable region in clinical isolates. Yeast 17: 272-282.
32. Hubner, A., and Hendrickson, W. (1997) A fusion promoter created by a new insertion sequence, IS1490, activates transcription of 2,4,5- trichlorophenoxyacetic acid catabolic genes in Burkholderia cepacia AC1100. J Bacteriol 179: 2717-2723.
33. Kallastu, A., Horak, R., and Kivisaar, M. (1998) Identification and characterization of IS1411, a new insertion sequence which causes transcriptional activation of the phenol degradation genes in Pseudomonas putida. J Bacteriol 180: 5306-5312.
34. Karunakaran, P., and Davies, J. (2000) Genetic antagonism and hypermutability in Mycobacterium smegmatis. J Bacteriol 182: 3331-3335.
35. Kurepina, N.E., Sreevatsan, S., Plikaytis, B.B., Bifani, P.J., Connell, N.D., Donnelly, R.J., et al. (1998) Characterization of the phylogenetic distribution and chromosomal insertion sites of five IS6110 elements in Mycobacterium tuberculosis: non-random integration in the dnaA-dnaN region. Tuber Lung Dis 79: 31-42.
36. Leelaporn, A., Firth, N., Byrne, M.E., Roper, E., and Skurray, R.A. (1994) Possible role of insertion sequence IS257 in dissemination and expression of high- and low-level trimethoprim resistance in staphylococci. Antimicrob Agents Chemother 38: 2238-2244.
37. Lopez de Felipe, F., Magni, C., de Mendoza, D., and Lopez, P. (1996) Transcriptional activation of the citrate permease P gene of Lactococcus lactis biovar diacetylactis by an insertion sequence-like element present in plasmid pCIT264. Mol Gen Genet 250: 428-436.
38. McAdam, R.A., Hermans, P.W., van Soolingen, D., Zainuddin, Z.F., Catty, D., van Embden, J.D., and Dale, J.W. (1990) Characterization of a Mycobacterium tuberculosis insertion sequence belonging to the IS3 family. Mol Microbiol 4: 1607-1613.
39. Manillon, J., and Chandler, M. (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
40. Maki, H., and Murakami, K. (1997) Formation of potent hybrid promoters of the mutant IIm gene by IS256 transposition in methicillin-resistant Staphylococcus aureus. J Bacteriol 179: 6944-6948.
41. E: role in global gene expression and survival in macrophages. Mol Microbiol 41: 423-437.
42. Marchler-Bauer, A., Panchenko, A.R., Shoemaker, B.A., Thiessen, P.A., Geer, L.Y., and Bryant, S.H. (2002) CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res 30: 281-283.
43. Mendiola, M.V., Martin, C., Otal, I., and Gicquel, B. (1992) Analysis of the regions responsible for IS6110 RFLP in a single Mycobacterium tuberculosis strain. Res Microbiol 143: 767-772.
44. Munsiff, S.S., Nivin, B., Sacajiu, G., Mathema, B., Bifani, P., and Kreiswirth, B.N. (2003) Persistence of a highly resistant strain of tuberculosis in New York City during 1990-99. J Infect Dis 188: 356-363.
45. Podglajen, I., Breuil, J., and Collatz, E. (1994) Insertion of a novel DNA sequence, 1S1186, upstream of the silent carbapenemase gene cfiA, promotes expression of carbapenem resistance in clinical isolates of Bacteroides fragilis. Mol Microbiol 12: 105-114.
46. Podglajen, I., Breuil, J., Rohaut, A., Monsempes, C., and Collatz, E. (2001) Multiple mobile promoter regions for the rare carbapenem resistance gene of Bacteroides fragilis. J Bacteriol 183: 3531-3535.
47. Ramakrishnan, L., Federspiel, N.A., and Falkow, S. (2000) Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288: 1436-1439.
48. Raman, S., Song, T., Puyang, X., Bardarov, S., Jacobs, W.R., Jr, and Husson, R.N. (2001) The alternative sigma factor SigH regulates major components of oxidative and heat stress responses in Mycobacterium tuberculosis. J Bacteriol 183: 6119-6125.
49. Reed, D.W., and Hartzell, P.L. (1999) The Archaeoglobus fulgidus D-lactate dehydrogenase is a Zn(2+) flavoprotein. J Bacteriol 181: 7580-7587.
50. Rosenberg, S.M., and Hastings, P.J. (2003) Modulating mutation rates in the wild (Commentary). Science 300: 1382-1383.
51. Russell, D.G. (1999) Mycobacterium and the seduction of the macrophage. In Mycobacteria: Molecular Biology and Virulence. Ratledge, C., and Dale, J. (eds). Oxford: Blackwell Science, pp. 371-388.
52. Safi, H., Aznar, J., and Palomares, J.C. (1997) Molecular epidemiology of Mycobacterium tuberculosis strains isolated during a 3-year period (1993-95) in Seville, Spain. J Clin Microbiol 35: 2472-2476.
53. Sampson, S.L., Warren, R.M., Richardson, M., van der Spuy, G.D., and van Helden, P.D. (1999) Disruption of coding regions by IS6110 insertion in Mycobacterium tuberculosis. Tuber Lung Dis 79: 349-359.
54. Sampson, S., Warren, R., Richardson, M., van der Spuy, G., and van Helden, P. (2001) IS6110 insertions in Mycobacterium tuberculosis: predominantly into coding regions. J Clin Microbiol 39: 3423-3424.
55. Sampson, S.L., Warren, R.M., Richardson, M., Victor, T.C., Jordaan, A.M., van der Spuy, G.D., and van Helden, P.D. (2003) IS6110-mediated deletion polymorphism in the direct repeat region of clinical isolates of Mycobacterium tuberculosis. J Bacteriol 185: 2856-2866.
56. Singh, K.K., Zhang, X., Patibandla, A.S., Chien, P., Jr, and Laal, S. (2001) Antigens of Mycobacterium tuberculosis expressed during preclinical tuberculosis: serological immunodominance of proteins with repetitive amino acid sequences. Infect Immun 69: 4185-4191.
57. Small, P.M., Hopewell, P.C., Singh, S.P., Paz, A., Parsonnet, J., Ruston, D.C., et al. (1994) The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N Engl J Med 330: 1703-1709.
58. van Soolingen, D., Hermans, P.W., de Haas, P.E., Soll, D.R., and van Embden, J.D. (1991) 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 29: 2578-2586.
59. Sreevatsan, S., Pan, X., Stockbauer, K.E., Connell, N.D., Kreiswirth, B.N., Whittam, T.S., and Musser, J.M. (1997) Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci USA 94: 9869-9874.
60. Stover, C.K., de la Cruz, V.F., Fuerst, T.R., Burlein, J.E., Benson, L.A., Bennett, L.T., et al. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
61. Talaat, A.M., Hunter, P., and Johnston, S.A. (2000) Genome-directed primers for selective labeling of bacterial transcripts for DNA microarray analysis. Nature Biotechnol 18: 679-682.
62. Tanaka, M.M., Small, P.M., Salamon, H., and Feldman, M.W. (2000) The dynamics of repeated elements: applications to the epidemiology of tuberculosis. Proc Natl Acad Sci USA 97: 3532-3537.
63. Thierry, D., Cave, M.D., Eisenach, K.D., Crawford, J.T., Bates, J.H., Gicquel, B., and Guesdon, J.L. (1990) IS6110, an IS-like element of Mycobacterium tuberculosis complex. Nucleic Acids Res 18: 188.
64. Vera-Cabrera, L., Howard, S.T., Laszlo, A., and Johnson, W.M. (1997) Analysis of genetic polymorphism in the phospholipase region of Mycobacterium tuberculosis. J Clin Microbiol 35: 1190-1195.
65. Vera-Cabrera, L., Hernandez-Vera, M.A., Welsh, O., Johnson, W.M., and Castro-Garza, J. (2001) Phospholipase region of Mycobacterium tuberculosis is a preferential locus for IS6110 transposition. J Clin Microbiol 39: 3499-3504.
66. Warren, R.M., Sampson, S.L., Richardson, M., van der Spuy, G.D., Lombard., C.J., Victor, T.C., and van Helden, P.D. (2000) Mapping of IS6110 flanking regions in clinical isolates of Mycobacterium tuberculosis demonstrates genome plasticity. Mol Microbiol 37: 1405-1416.
67. Warren, R.M., van der Spuy, G.D., Richardson, M., Beyers, N., Booysen, C., Behr, M.A., and van Helden, P.D. (2002) Evolution of the IS6110-based restriction fragment length polymorphism pattern during the transmission of Mycobacterium tuberculosis. J Clin Microbiol 40: 1277-1282.
68. Wery, J., Hidayat, B., Kieboom, J., and de Bont, J.A.M. (2001) An insertion sequence prepares Pseudomonas putida S12 for severe solvent stress. J Biol Chem 276: 5700-5706.
69. Yang, Z., Barnes, P.F., Chaves, F., Eisenach, K.D., Weis, S.E., Bates, J.H., and Cave, M.D. (1998) Diversity of DNA fingerprints of Mycobacterium tuberculosis isolates in the United States. J Clin Microbiol 36: 1003-1007.
70. Zafarullah, M., Charlier, D., and Glansdorff, N. (1981) Insertion of IS3 can 'turn-on' a silent gene in Escherichia coli. J Bacteriol 146: 415-417.
71. Zhang, M., Gong, J., Yang, Z., Samten, B., Cave, M.D., and Barnes, P.F. (1999) Enhanced capacity of a widespread strain of Mycobacterium tuberculosis to grow in human macrophages. J Infect Dis 179: 1213-1217.
72. Ziegler-Heitbrock, H.W., Thiel, E., Futterer, A., Herzog, V., Wirtz, A., and Riethmuller, G. (1988) Establishment of a human cell line (Mono Mac 6) with characteristics of mature monocytes. Int J Cancer 41: 456-461.