Mycobacterium tuberculosis modulates its cell surface via an oligopeptide permease (Opp) transport system

FASEB Journal

Volumn 23, Issue 12, 2009, Pages 4091-4104

  Flores Valdez, Mario Alberto ^a   Morris, Rowan P ^b   Laval, Françoise ^c,d   Daffé, Mamadou ^c,d   Schoolnik, Gary K ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Cell wall modulation; Chronic infection; Lipid virulence factors; Surface interaction

Indexed keywords

BACTERIAL ENZYME; LIPID; MYCOLIC ACID; OLIGOPEPTIDE PERMEASE; PERMEASE; PHTHIOCEROL DIMYCOCEROSATE; PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL SURFACE; CONTROLLED STUDY; DEATH; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENOME; GROWTH RETARDATION; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; REGULATORY MECHANISM; STRAIN DIFFERENCE; THIN LAYER CHROMATOGRAPHY; TUBERCULOSIS; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; CELL MEMBRANE; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; TRIGLYCERIDES;

ANIMALIA; BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA; STREPTOMYCES;

EID: 72749117648     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-132407     Document Type: Article

References (77)

1. Solomon, J. M., Lazazzera, B. A., and Grossman, A. D. (1996) Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. Genes Dev. 10, 2014-2024
2. Lazazzera, B. A., Solomon, J. M., and Grossman, A. D. (1997) An exported peptide functions intracellularly to contribute to cell density signaling in B. subtilis. Cell 89, 917-925
3. Lazazzera, B. A. (2001) The intracellular function of extracellular signaling peptides. Peptides 22, 1519-1527
4. Gominet, M., Slamti, L., Gilois, N., Rose, M., and Lereclus, D. (2001) Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence. Mol. Microbiol. 40, 963-975 (Pubitemid 32523193)
5. Slamti, L., and Lereclus, D. (2002) A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J. 21, 4550-4559 (Pubitemid 34984342)
6. Leonard, B. A., Podbielski, A., Hedberg, P. J., and Dunny, G. M. (1996) Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation. Proc. Natl. Acad. Sci. U. S. A. 93, 260-264 (Pubitemid 26038139)
7. Perego, M., and Hoch, J. A. (1996) Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 93, 1549-1553 (Pubitemid 26075162)
8. Green, R. M., Seth, A., and Connell, N. D. (2000) A peptide permease mutant of Mycobacterium bovis BCG resistant to the toxic peptides glutathione and S-nitrosoglutathione. Infect. Immun. 68, 429-436 (Pubitemid 30056490)
9. Stewart, G. R., Patel, J., Robertson, B. D., Rae, A., and Young, D. B. (2005) Mycobacterial mutants with defective control of phagosomal acidification. PLoS Pathog. 1, 269-278
10. Sassetti, C. M., and Rubin, E. J. (2003) Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. U. S. A. 100, 12989-12994
11. Steyn, A. J., Collins, D. M., Hondalus, M. K., Jacobs, W. R., Jr., Kawakami, R. P., and Bloom, B. R. (2002) Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host survival but is dispensable for in vivo growth. Proc. Natl. Acad. Sci. U. S. A. 99, 3147-3152
12. Kaushal, D., Schroeder, B. G., Tyagi, S., Yoshimatsu, T., Scott, C., Ko, C., Carpenter, L., Mehrotra, J., Manabe, Y. C., Fleischmann, R. D., and Bishai, W. R. (2002) Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proc. Natl. Acad. Sci. U. S. A. 99, 8330-8335 (Pubitemid 34651052)
13. Bardarov, S., Bardarov, S., Jr., Pavelka, M. S., Jr., Sambandamurthy, V., Larsen, M., Tufariello, J., Chan, J., Hatfull, G., and Jacobs, W. R., Jr. (2002) Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148, 3007-3017
14. Sassetti, C. M., Boyd, D. H., and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84
15. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., 3rd, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J., Quail, M. A., Rajandream, M. A., Rogers, J., Rutter, S., Seeger, K., Skelton, J., Squares, R., Squares, S., Sulston, J. E., Taylor, K., Whitehead, S., and Barrell, B. G. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544
16. Fleischmann, R. D., Alland, D., Eisen, J. A., Carpenter, L., White, O., Peterson, J., DeBoy, R., Dodson, R., Gwinn, M., Haft, D., Hickey, E., Kolonay, J. F., Nelson, W. C., Umayam, L. A., Ermolaeva, M., Salzberg, S. L., Delcher, A., Utterback, T., Weidman, J., Khouri, H., Gill, J., Mikula, A., Bishai, W., Jacobs, W. R., Jr., Venter, J. C., and Fraser, C. M. (2002) Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J. Bacteriol. 184, 5479-5490 (Pubitemid 35024395)
17. Schwartz, D., Berger, S., Heinzelmann, E., Muschko, K., Welzel, K., and Wohlleben, W. (2004) Biosynthetic gene cluster of the herbicide phosphinothricin tripeptide from Streptomyces viridochromogenes Tu494. Appl. Environ. Microbiol. 70, 7093-7102 (Pubitemid 39643772)
18. Perego, M., Higgins, C. F., Pearce, S. R., Gallagher, M. P., and Hoch, J. A. (1991) The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol. Microbiol. 5, 173-185 (Pubitemid 21895953)
19. Nodwell, J. R., McGovern, K., and Losick, R. (1996) An oligopeptide permease responsible for the import of an extracel- lular signal governing aerial mycelium formation in Streptomyces coelicolor. Mol. Microbiol. 22, 881-893 (Pubitemid 26411333)
20. Lorenzana, L. M., Perez-Redondo, R., Santamarta, I., Martin, J. F., and Liras, P. (2004) Two oligopeptide-permease-encoding genes in the clavulanic acid cluster of Streptomyces clavuligerus are essential for production of the beta-lactamase inhibitor. J. Bacteriol. 186, 3431-3438 (Pubitemid 38661539)
21. Borezee, E., Pellegrini, E., and Berche, P. (2000) OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survival. Infect. Immun. 68, 7069-7077 (Pubitemid 32463421)
22. Marrakchi, H., Bardou, F., Lanéelle, M. A., and Daffé, M. (2008) A comprehensive overview of the mycolic acid biosynthesis. In The Mycobacterial Cell Envelope (Daffé, M., and Reyrat, J. M., eds) pp. 41-62, ASM Press, Washington, DC
23. Barry, C. E., Crick, D. C., and McNeil, M. R. (2007) Targeting the formation of the cell wall core of M. tuberculosis. Infect. Disord. Drug Targets 7, 182-202 (Pubitemid 47099127)
24. Trivedi, O. A., Arora, P., Vats, A., Ansari, M. Z., Tickoo, R., Sridharan, V., Mohanty, D., and Gokhale, R. S. (2005) Dissecting the mechanism and assembly of a complex virulence mycobacterial lipid. Mol. Cell 17, 631-643 (Pubitemid 40320914)
25. Cox, J. S., Chen, B., McNeil, M., and Jacobs, W. R., Jr. (1999) Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402, 79-83
26. Camacho, L. R., Ensergueix, D., Perez, E., Gicquel, B., and Guilhot, C. (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol. Microbiol. 34, 257-267 (Pubitemid 29486244)
27. Guilhot, C. A. D. M. (2008) Polyketides and polyketide-containing glycolipids of M. tuberculosis: structure, biosynthesis and biological activities. In Handbook of Tuberculosis: Molecular Biology and Biochemistry , Vol.1 (Kaufmann, S. H. E., and Rubin, E. J., eds) pp. 21-51, Wiley-VCH, Weinheim, Germany
28. Jackson, M., Stadthagen, G., and Gicquel, B. (2007) Long-chain multiple methyl-branched fatty acid-containing lipids of Mycobacterium tuberculosis: biosynthesis, transport, regulation and biological activities. Tuberculosis (Edinb.) 87, 78-86 (Pubitemid 46217257)
29. Dubey, V. S., Sirakova, T. D., and Kolattukudy, P. E. (2002) Disruption of msl3 abolishes the synthesis of mycolipanoic and mycolipenic acids required for polyacyltrehalose synthesis in Mycobacterium tuberculosis H37Rv and causes cell aggregation. Mol. Microbiol. 45, 1451-1459
30. Lamb, J. R., Rees, A. D., Bal, V., Ikeda, H., Wilkinson, D., De Vries, R. R., and Rothbard, J. B. (1988) Prediction and identification of an HLA-DR-restricted T cell determinant in the 19-kDa protein of Mycobacterium tuberculosis. Eur. J. Immunol. 18, 973-976 (Pubitemid 18166647)
31. Ashbridge, K. R., Prestidge, R. L., Booth, R. J., and Watson, J. D. (1990) The mapping of an antibody-binding region on the Mycobacterium tuberculosis 19 kilodalton antigen. J. Immunol. 144, 3137-3142
32. Sorensen, A. L., Nagai, S., Houen, G., Andersen, P., and Andersen, A. B. (1995) Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect. Immun. 63, 1710-1717
33. Berthet, F. X., Rasmussen, P. B., Rosenkrands, I., Andersen, P., and Gicquel, B. (1998) A Mycobacterium tuberculosis operon encoding ESAT-6 and a novel low-molecular-mass culture filtrate protein (CFP-10). Microbiology 144(Pt. 11), 3195-3203 (Pubitemid 28515598)
34. Pethe, K., Alonso, S., Biet, F., Delogu, G., Brennan, M. J., Locht, C., and Menozzi, F. D. (2001) The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 412, 190-194 (Pubitemid 32674716)
35. Zvi, A., Ariel, N., Fulkerson, J., Sadoff, J. C., and Shafferman, A. (2008) Whole genome identification of Mycobacterium tuberculosis vaccine candidates by comprehensive data mining and bioinformatic analyses. BMC Med. Genomics 1, 18
36. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D., Nathan, C., and Schoolnik, G. K. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198, 693-704 (Pubitemid 37087769)
37. Munoz-Elias, E. J., and McKinney, J. D. (2006) Carbon metabolism of intracellular bacteria. Cell. Microbiol. 8, 10-22
38. Ochi, K., Kandala, J. C., and Freese, E. (1981) Initiation of Bacillus subtilis sporulation by the stringent response to partial amino acid deprivation. J. Biol. Chem. 256, 6866-6875 (Pubitemid 11010849)
39. Ochi, K. (1987) Metabolic initiation of differentiation and secondary metabolism by Streptomyces griseus: significance of the stringent response (ppGpp) and GTP content in relation to A factor. J. Bacteriol. 169, 3608-3616
40. Englebrecht, H. L. (1972) Time course of purine nucleoside phosphorylase occurrence in sporulation of Bacillus cereus. J. Bacteriol. 111, 33-36
41. Laval, F., Laneelle, M. A., Deon, C., Monsarrat, B., and Daffe, M. (2001) Accurate molecular mass determination of mycolic acids by MALDI-TOF mass spectrometry. Anal. Chem. 73, 4537-4544 (Pubitemid 32868257)
42. Camacho, L. R., Constant, P., Raynaud, C., Laneelle, M. A., Triccas, J. A., Gicquel, B., Daffe, M., and Guilhot, C. (2001) Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis: evidence that this lipid is involved in the cell wall permeability barrier. J. Biol. Chem. 276, 19845-19854 (Pubitemid 37411046)
43. Brennan, P. J. (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis (Edinb.) 83, 91-97 (Pubitemid 36683556)
44. Bentley, S. D., Chater, K. F., Cerdeno-Tarraga, A. M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H., Harper, D., Bateman, A., Brown, S., Chandra, G., Chen, C. W., Collins, M., Cronin, A., Fraser, A., Goble, A., Hidalgo, J., Hornsby, T., Howarth, S., Huang, C. H., Kieser, T., Larke, L., Murphy, L., Oliver, K., O'Neil, S., Rabbinowitsch, E., Rajandream, M. A., Rutherford, K., Rutter, S., Seeger, K., Saunders, D., Sharp, S., Squares, R., Squares, S., Taylor, K., Warren, T., Wietzorrek, A., Woodward, J., Barrell, B. G., Parkhill, J., and Hopwood, D. A. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141-147 (Pubitemid 34506788)
45. Ventura, M., Canchaya, C., Tauch, A., Chandra, G., Fitzgerald, G. F., Chater, K. F., and van Sinderen, D. (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol. Mol. Biol. Rev. 71, 495-548 (Pubitemid 47429283)
46. Morris, R. P., Nguyen, L., Gatfield, J., Visconti, K., Nguyen, K., Schnappinger, D., Ehrt, S., Liu, Y., Heifets, L., Pieters, J., Schoolnik, G., and Thompson, C. J. (2005) Ancestral antibiotic resistance in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 102, 12200-12205 (Pubitemid 41291152)
47. Nodwell, J. R., and Losick, R. (1998) Purification of an extracellular signaling molecule involved in production of aerial mycelium by Streptomyces coelicolor. J. Bacteriol. 180, 1334-1337
48. Chater, K. F., and Horinouchi, S. (2003) Signalling early developmental events in two highly diverged Streptomyces species. Mol. Microbiol. 48, 9-15
49. Ghosh, J., Larsson, P., Singh, B., Pettersson, B. M., Islam, N. M., Sarkar, S. N., Dasgupta, S., and Kirsebom, L. A. (2009) Sporulation in mycobacteria. Proc. Natl. Acad. Sci. U. S. A. 106, 10781-10786
50. Smirnova, G. V., and Oktyabrsky, O. N. (2005) Glutathione in bacteria. Biochemistry (Mosc.) 70, 1199-1211
51. Garton, N. J., Waddell, S. J., Sherratt, A. L., Lee, S. M., Smith, R. J., Senner, C., Hinds, J., Rajakumar, K., Adegbola, R. A., Besra, G. S., Butcher, P. D., and Barer, M. R. (2008) Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med. 5, e75
52. Daniel, J., Deb, C., Dubey, V. S., Sirakova, T. D., Abomoelak, B., Morbidoni, H. R., and Kolattukudy, P. E. (2004) Induction of a novel class of diacylglycerol acyltransferases and triacylglycerol accumulation in Mycobacterium tuberculosis as it goes into a dormancy-like state in culture. J. Bacteriol. 186, 5017-5030 (Pubitemid 38970829)
53. Park, H. D., Guinn, K. M., Harrell, M. I., Liao, R., Voskuil, M. I., Tompa, M., Schoolnik, G. K., and Sherman, D. R. (2003) Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 48, 833-843 (Pubitemid 36819066)
54. Betts, J. C., Lukey, P. T., Robb, L. C., McAdam, R. A., and Duncan, K. (2002) Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 43, 717-731
55. McKinney, J. D., Honer zu Bentrup, K., Munoz-Elias, E. J., Miczak, A., Chen, B., Chan, W. T., Swenson, D., Sacchettini, J. C., Jacobs, W. R., Jr., and Russell, D. G. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406, 735-738
56. Cirillo, S. L., Subbian, S., Chen, B., Weisbrod, T. R., Jacobs, W. R., Jr., and Cirillo, J. D. (2009) Protection of Mycobacterium tuberculosis from reactive oxygen species conferred by the mel2 locus impacts persistence and dissemination. Infect. Immun. 77, 2557-2567
57. Pandey, A. K., and Sassetti, C. M. (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl. Acad. Sci. U. S. A. 105, 4376-4380
58. Cundell, D. R., Pearce, B. J., Sandros, J., Naughton, A. M., and Masure, H. R. (1995) Peptide permeases from Streptococcus pneumoniae affect adherence to eucaryotic cells. Infect. Immun. 63, 2493-2498
59. Kerr, A. R., Adrian, P. V., Estevao, S., de Groot, R., Alloing, G., Claverys, J. P., Mitchell, T. J., and Hermans, P. W. (2004) The Ami-AliA/AliB permease of Streptococcus pneumoniae is involved in nasopharyngeal colonization but not in invasive disease. Infect. Immun. 72, 3902-3906 (Pubitemid 38821904)
60. Samen, U., Gottschalk, B., Eikmanns, B. J., and Reinscheid, D. J. (2004) Relevance of peptide uptake systems to the physiology and virulence of Streptococcus agalactiae. J. Bacteriol. 186, 1398-1408 (Pubitemid 38248730)
61. Pope, M. K., Green, B. D., and Westpheling, J. (1996) The bld mutants of Streptomyces coelicolor are defective in the regulation of carbon utilization, morphogenesis and cell-cell signalling. Mol. Microbiol. 19, 747-756 (Pubitemid 126423799)
62. Piette, A., Derouaux, A., Gerkens, P., Noens, E. E., Mazzucchelli, G., Vion, S., Koerten, H. K., Titgemeyer, F., De Pauw, E., Leprince, P., van Wezel, G. P., Galleni, M., and Rigali, S. (2005) From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant. J. Proteome Res. 4, 1699-1708 (Pubitemid 41464797)
63. Wang, C. H., Lin, C. Y., Luo, Y. H., Tsai, P. J., Lin, Y. S., Lin, M. T., Chuang, W. J., Liu, C. C., and Wu, J. J. (2005) Effects of oligopeptide permease in group a streptococcal infection. Infect. Immun. 73, 2881-2890 (Pubitemid 40570357)
64. Rachman, H., Strong, M., Ulrichs, T., Grode, L., Schuchhardt, J., Mollenkopf, H., Kosmiadi, G. A., Eisenberg, D., and Kaufmann, S. H. (2006) Unique transcriptome signature of Mycobacterium tuberculosis in pulmonary tuberculosis. Infect. Immun. 74, 1233-1242 (Pubitemid 43185563)
65. 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., Snapper, S. B., Barletta, R. G., Jacobs, W. R., Jr., and Bloom, B. R. (1991) New use of BCG for recombinant vaccines. Nature 351, 456-460
66. Manca, C., Tsenova, L., Barry, C. E., 3rd, Bergtold, A., Freeman, S., Haslett, P. A., Musser, J. M., Freedman, V. H., and Kaplan, G. (1999) Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. J. Immunol. 162, 6740-6746
67. Calamita, H., Ko, C., Tyagi, S., Yoshimatsu, T., Morrison, N. E., and Bishai, W. R. (2005) The Mycobacterium tuberculosis SigD sigma factor controls the expression of ribosome-associated gene products in stationary phase and is required for full virulence. Cell. Microbiol. 7, 233-244 (Pubitemid 40259739)
68. Agarwal, N., Woolwine, S. C., Tyagi, S., and Bishai, W. R. (2007) Characterization of the Mycobacterium tuberculosis sigma factor SigM by assessment of virulence and identification of SigM-dependent genes. Infect. Immun. 75, 452-461 (Pubitemid 46047921)
69. Ando, M., Yoshimatsu, T., Ko, C., Converse, P. J., and Bishai, W. R. (2003) Deletion of Mycobacterium tuberculosis sigma factor E results in delayed time to death with bacterial persistence in the lungs of aerosol-infected mice. Infect. Immun. 71, 7170-7172 (Pubitemid 37475351)
70. Chen, P., Ruiz, R. E., Li, Q., Silver, R. F., and Bishai, W. R. (2000) Construction and characterization of a Mycobacterium tuberculosis mutant lacking the alternate sigma factor gene, sigF. Infect. Immun. 68, 5575-5580 (Pubitemid 30739336)
71. Sun, R., Converse, P. J., Ko, C., Tyagi, S., Morrison, N. E., and Bishai, W. R. (2004) Mycobacterium tuberculosis ECF sigma factor sigC is required for lethality in mice and for the conditional expression of a defined gene set. Mol. Microbiol. 52, 25-38 (Pubitemid 38519619)
72. Dainese, E., Rodrigue, S., Delogu, G., Provvedi, R., Laflamme, L., Brzezinski, R., Fadda, G., Smith, I., Gaudreau, L., Palu, G., and Manganelli, R. (2006) Posttranslational regulation of Mycobacterium tuberculosis extracytoplasmic-function sigma factor sigma L and roles in virulence and in global regulation of gene expression. Infect. Immun. 74, 2457-2461
73. Hahn, M. Y., Raman, S., Anaya, M., and Husson, R. N. (2005) The Mycobacterium tuberculosis extracytoplasmic-function sigma factor SigL regulates polyketide synthases and secreted or membrane proteins and is required for virulence. J. Bacteriol. 187, 7062-7071 (Pubitemid 41428883)
74. Raman, S., Hazra, R., Dascher, C. C., and Husson, R. N. (2004) Transcription regulation by the Mycobacterium tuberculosis alternative sigma factor SigD and its role in virulence. J. Bacteriol. 186, 6605-6616 (Pubitemid 39258143)
75. Dubnau, E., Chan, J., Raynaud, C., Mohan, V. P., Laneelle, M. A., Yu, K., Quemard, A., Smith, I., and Daffe, M. (2000) Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol. Microbiol. 36, 630-637 (Pubitemid 30258847)
76. Glickman, M. S., Cox, J. S., and Jacobs, W. R., Jr. (2000) A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol. Cell. 5, 717-727
77. Rao, V., Gao, F., Chen, B., Jacobs, W. R., Jr., and Glickman, M. S. (2006) Trans-cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis-induced inflammation and virulence. J. Clin. Invest. 116, 1660-1667 (Pubitemid 43911020)