Identification of an essential gene of Listeria monocytogenes involved in teichoic acid biogenesis

Journal of Bacteriology

Volumn 188, Issue 18, 2006, Pages 6580-6591

  Dubail, Iharilalao ^a   Bigot, Armelle ^a   Lazarevic, Vladimir ^b   Soldo, Blazenka ^b   Euphrasie, Daniel ^a   Dupuis, Marion ^a   Charbit, Alain ^a,c  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c Faculte de Medecine Necker   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TEICHOIC ACID; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE 2 EPIMERASE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENOME; BACTERIAL STRAIN; ESSENTIAL GENE; GENE IDENTIFICATION; GRAM POSITIVE BACTERIUM; IMO2537 GENE; LISTERIA MONOCYTOGENES; NONHUMAN; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CARBOHYDRATE EPIMERASES; CELL LINE; COLONY COUNT, MICROBIAL; CYTOPLASM; DISEASE MODELS, ANIMAL; GENES, ESSENTIAL; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MACROPHAGES; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; SEQUENCE HOMOLOGY, AMINO ACID; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS; VIRULENCE FACTORS;

ANIMALIA; BACILLUS SUBTILIS; LISTERIA MONOCYTOGENES; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 33748783782     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00771-06     Document Type: Article

References (71)

1. Abachin, E., C. Poyart, E. Pellegrini, E. Milohanic, F. Fiedler, P. Berche, and P. Trieu-Cuot. 2002. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43:1-14.
2. Ames, B. N. 1966. Assay of inorganic phosphate, total phosphate, and phosphatases. Methods Enzymol. 8:115-118.
3. Appelberg, R. 2006. Macrophage nutriprive antimicrobial mechanisms. J. Leukoc. Biol.
4. Autret, N., and A. Charbit. 2005. Lessons from signature-tagged mutagenesis on the infectious mechanisms of pathogenic bacteria. FEMS Microbiol. Rev. 29:703-717.
5. Autret, N., I. Dubail, P. Trieu-Cuot, P. Berche, and A. Charbit. 2001. Identification of new genes involved in the virulence of Listeria monocytogenes by signature-tagged transposon mutagenesis. Infect. Immun. 69:2054-2065.
6. Autret, N., C. Raynaud, I. Dubail, P. Berche, and A. Charbit. 2003. Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect. Immun. 71:4463-4471.
7. Bhavsar, A. P., L. K. Erdman, J. W. Schertzer, and E. D. Brown. 2004. Teichoic acid is an essential polymer in Bacillus subtilis that is functionally distinct from teichuronic acid. J. Bacteriol. 186:7865-7873.
8. Biswas, I., A. Gruss, S. D. Ehrlich, and E. Maguin. 1993. High-efficiency gene inactivation and replacement system for gram-positive bacteria. J. Bacteriol. 175:3628-3635.
9. Bonnemain, C., C. Raynaud, H. Reglier-Poupet, I. Dubail, C. Frehel, M. A. Lety, P. Berche, and A. Charbit. 2004. Differential roles of multiple signal peptidases in the virulence of Listeria monocytogenes. Mol. Microbiol. 51:1251-1266.
10. Brehm, K., J. Kreft, M. T. Ripio, and J. A. Vazquez-Boland. 1996. Regulation of virulence gene expression in pathogenic Listeria. Microbiologia 12:219-236.
11. Bubert, A., Z. Sokolovic, S. K. Chun, L. Papatheodorou, A. Simm, and W. Goebel. 1999. Differential expression of Listeria monocytogenes virulence genes in mammalian host cells. Mol. Gen. Genet. 261:323-336.
12. Cabanes, D., P. Dehoux, O. Dussurget, L. Frangeul, and P. Cossart. 2002. Surface proteins and the pathogenic potential of Listeria monocytogenes. Trends Microbiol. 10:238-245.
13. Chen, P. S. 1956. Microdetermination of phosphorus. Anal. Chem. 18:1756-1758.
14. Collins, L. V., S. A. Kristian, C. Weidenmaier, M. Faigle, K. P. Van Kessel, J. A. Van Strijp, F. Gotz, B. Neumeister, and A. Peschel. 2002. Staphylococcus aureus strains lacking D-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J. Infect. Dis. 186:214-219.
15. Dancz, C. E., A. Haraga, D. A. Portnoy, and D. E. Higgins. 2002. Inducible control of virulence gene expression in Listeria monocytogenes: temporal requirement of listeriolysin O during intracellular infection. J. Bacteriol. 184:5935-5945.
16. Dubail, I., P. Berche, and A. Charbit. 2000. Listeriolysin O as a reporter to identify constitutive and in vivo-inducible promoters in the pathogen Listeria monocytogenes. Infect. Immun. 68:3242-3250.
17. Dussurget, O., J. Pizarro-Cerda, and P. Cossart. 2004. Molecular determinants of Listeria monocytogenes virulence. Annu. Rev. Microbiol. 58:587-610.
18. Ellwood, D. C., and D. W. Tempest. 1969. Control of teichoic acid and teichuronic acid biosyntheses in chemostat cultures of Bacillus subtilis var. niger. Biochem. J. 111:1-5.
19. Fiedler, F. 1988. Biochemistry of the cell surface of Listeria strains: a locating general view. Infection 16(Suppl. 2):S92-S97.
20. Fischer, W., T. Mannsfeld, and G. Hagen. 1990. On the basic structure of poly (glycerophosphate) lipoteichoic acids. Biochem. Cell. Biol. 68:33-43.
21. Forsyth, R. A., R. J. Haselbeck, K. L. Ohlsen, R. T. Yamamoto, H. Xu, J. D. Trawick, D. Wall, L. Wang, V. Brown-Driver, J. M. Froelich, G. C. Kedar, P. King, M. McCarthy, C. Malone, B. Misiner, D. Robbins, Z. Tan, Z. Y. Zhu Zy, G. Carr, D. A. Mosca, C. Zamudio, J. G. Foulkes, and J. W. Zyskind. 2002. A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Mol. Microbiol. 43:1387-1400.
22. Freitag, N. E., and K. E. Jacobs. 1999. Examination of Listeria monocytogenes intracellular gene expression by using the green fluorescent protein of Aequorea victoria. Infect. Immun. 67:1844-1852.
23. Freymond, P. P., V. Lazarevic, B. Soldo, and D. Xaramata. 2006. Poly(glucosyl-N-acetylgalactosamine 1-phosphate), a wall teichoic acid of Bacillus subtilis 168: its biosynthetic pathway and mode of attachment to peptidoglycan. Microbiology 152:1709-1718.
24. Fujii, H., K. Kamisango, M. Nagaoka, K. Uchikawa, I. Sekikawa, K. Yamamoto, and I. Azuma. 1985. Structural study on teichoic acids of Listeria monocytogenes types 4a and 4d. J. Biochem. 97:883-891.
25. Gahan, C. G., and C. Hill. 2000. The use of listeriolysin to identify in vivo induced genes in the gram-positive intracellular pathogen Listeria monocytogenes. Mol. Microbiol. 36:498-507.
26. Glaser, P., L. Frangeul, C. Buchrieser, A. Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couvé, A. de Daruvar, P. Dehoux, E. Domann, G. Domínguez-Bernal, E. Duchaud, L. Durand, O. Dussurget, K. D. Entian, H. Fsihi, F. Garcia-Del Portillo, P. Garrido, L. Gautier, W. Goebel, N. Gómez-López, T. Hain, J. Hauf, D. Jackson, L. M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueño, A. Maitournam, J. Mata Vicente, E. Ng, G. Nordsiek, S. Novella, B. de Pablos, J. C. Pérez-Diaz, R. Purcell, B. Remmel, M. Rose, C. Rusniok, T. Scblueter, N. Simoes, A. Tierrez, J. A. Vázquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294:849-852.
27. Glomski, I. J., M. M. Gedde, A. W. Tsang, J. A. Swanson, and D. A. Portnoy. 2002. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J. Cell Biol. 156:1029-1038.
28. Harder, A., R. Wildgruber, A. Nawrocki, S. J. Fey, P. M. Larsen, and A. Gorg. 1999. Comparison of yeast cell protein solubilization procedures for two-dimensional electrophoresis. Electrophoresis 20:826-829.
29. Jones, S., and D. A. Portnoy. 1994. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect. Immun. 61:5608-5613.
30. Kamisango, K., H. Fujii, H. Okumura, I. Saiki, Y. Araki, Y. Yamamura, and I. Azuma. 1983. Structural and immunochemical studies of teichoic acid of Listeria monocytogenes. J. Biochem. 93:1401-1409.
31. Kaya, S., Y. Araki, and E. Ito. 1985. Characterization of a novel linkage unit between ribitol teichoic acid and peptidoglycan in Listeria monocytogenes cell walls. Eur. J. Biochem. 146:517-522.
32. Kaya, S., K. Yokoyama, Y. Araki, and E. Ito. 1984. N- acetylmannosaminyl(1→4)N-acetylglucosamine, a linkage unit between glycerol teichoic acid and peptidoglycan in cell walls of several Bacillus strains. J. Bacteriol. 158:990-996.
33. Kiser, K. B., N. Bhasin, L. Deng, and J. C. Lee. 1999. Staphylococcus aureus cap5P encodes a UDP-N-acetylglucosamine 2-epimerase with functional redundancy. J. Bacteriol. 181:4818-4824.
34. Klarsfeld, A. D., P. L. Goossens, and P. Cossart. 1994. Five Listeria monocytogenes genes preferentially expressed in infected mammalian cells: plcA, purH, purD, pyrE and an arginine ABC transporter gene, arpJ. Mol. Microbiol. 13:585-597.
35. Knuth, K., H. Niesalla, C. J. Hueck, and T. M. Fuchs. 2004. Large-scale identification of essential Salmonella genes by trapping lethal insertions. Mol. Microbiol. 51:1729-1744.
36. Kobayashi, K., S. D. Ehrlich, A. Albertini, G. Amati, K. K. Andersen, M. Arnaud, K. Asai, S. Ashikaga, S. Aymerich, P. Bessieres, F. Boland, S. C. Brignell, S. Bron, K. Bunai, J. Chapuis, L. C. Christiansen, A. Danchin, M. Debarbouille, E. Dervyn, E. Deuerling, K. Devine, S. K. Devine, O. Dreesen, J. Errington, S. Fillinger, S. J. Foster, Y. Fujita, A. Galizzi, R. Gardan, C. Eschevins, T. Fukushima, K. Haga, C. R. Harwood, M. Hecker, D. Hosoya, M. F. Hullo, H. Kakeshita, D. Karamata, Y. Kasahara, F. Kawamura, K. Koga, P. Koski, R. Kuwana, D. Imamura, M. Ishimaru, S. Ishikawa, I. Ishio, D. Le Coq, A. Masson, C. Mauel, R. Meima, R. P. Mellado, A. Moir, S. Moriya, E. Nagakawa, H. Nanamiya, S. Nakai, P. Nygaard, M. Ogura, T. Ohanan, M. O'Reilly, M. O'Rourke, Z. Pragai, H. M. Pooley, G. Rapoport, J. P. Rawlins, L. A. Rivas, C. Rivolta, A. Sadaie, Y. Sadaie, M. Sarvas, T. Sato, H. H. Saxild, E. Scanlan, W. Schumann, J. F. Seegers, J. Sekiguchi, A. Sekowska, S. J. Seror, M. Simon, P. Stragier, R. Studer, H. Takamatsu, T. Tanaka, M. Takeuchi, H. B. Thomaides, V. Vagner, J. M. van Dijl, K. Watabe, A. Wipat, H. Yamamoto, M. Yamamoto, Y. Yamamoto, K. Yamane, K. Yata, K. Yoshida, H. Yoshikawa, U. Zuber, and N. Ogasawara. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100:4678-4683.
37. Lazarevic, V., F. X. Abellan, S. B. Moller, D. Karamata, and C. Mauel. 2002. Comparison of ribitol and glycerol teichoic acid genes in Bacillus subtilis W23 and 168: identical function, similar divergent organization, but different regulation. Microbiology 148:815-824.
38. Lazarevic, V., and D. Karamata. 1995. The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two wall teichoic acids. Mol. Microbiol. 16:345-355.
39. Lingnau, A., E. Domann, M. Hudel, M. Bock, T. Nichterlein, J. Wehland, and T. Chakraborty. 1995. Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and -independent mechanisms. Infect. Immun. 63:3896-3903.
40. Lucchini, S., H. Liu, Q. Jin, J. C. Hinton, and J. Yu. 2005. Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect. Immun. 73:88-102.
41. Mahan, M. J., J. W. Tobias, J. M. Slauch, P. C. Hanna, R. J. Collier, and J. J. Mekalanos. 1995. Antibiotic-based selection for bacterial genes that are specifically induced during infection of a host. Proc. Natl. Acad. Sci. USA 92:669-673.
42. Mauck, J., and L. Glaser. 1972. On the mode of in vivo assembly of the cell wall of Bacillus subtilis. J. Biol. Chem. 247:1180-1187.
43. Mauel, C., M. Young, and D. Karamata. 1991. Genes concerned with synthesis of poly(glycerol phosphate), the essential teichoic acid in Bacillus subtilis strain 168, are organized in two divergent transcription units. J. Gen. Microbiol. 137:929-941.
44. Miesel, L., J. Greene, and T. A. Black. 2003. Genetic strategies for antibacterial drug discovery. Nat. Rev. Genet. 4:442-456.
45. Moors, M. A., B. Levitt, P. Youngman, and D. A. Portnoy. 1999. Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect. Immun. 67:131-139.
46. Nair, S., C. Frehel, L. Nguyen, V. Escuyer, and P. Berche. 1999. ClpE, a novel member of the HSP100 family, is involved in cell division and virulence of Listeria monocytogenes. Mol. Microbiol. 31:185-196.
47. Neuhaus, F. C., and J. Baddiley. 2003. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67:686-723.
48. Newton, S. M., P. E. Klebba, C. Raynaud, Y. Shao, X. Jiang, I. Dubail, C. Archer, C. Frehel, and A. Charbit. 2005. The svpA-srtB locus of Listeria monocytogenes: fur-mediated iron regulation and effect on virulence. Mol. Microbiol. 55:927-940.
49. Peschel, A., M. Otto, R. W. Jack, H. Kalbacher, G. Jung, and F. Gotz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405-8410.
50. Piuri, M., C. Sanchez-Rivas, and S. M. Ruzal. 2005. Cell wall modifications during osmotic stress in Lactobacillus casei. J. Appl. Microbiol. 98:84-95.
51. Pooley, H. M., and D. Karamata. 2000. Incorporation of [2-3H]glycerol into cell surface components of Bacillus subtilis 168 and thermosensitive mutants affected in wall teichoic acid synthesis: effect of tunicamycin. Microbiology 146(Pt. 4):797-805.
52. Poyart, C., E. Pellegrini, M. Marceau, M. Baptista, F. Jaubert, M. C. Lamy, and P. Trieu-Cuot. 2003. Attenuated virulence of Streptococcus agalactiae deficient in D-alanyl-lipoteichoic acid is due to an increased susceptibility to defensins and phagocytic cells. Mol. Microbiol. 49:1615-1625.
53. Rediers, H., P. B. Rainey, J. Vanderleyden, and R. De Mot. 2005. Unraveling the secret lives of bacteria: use of in vivo expression technology and differential fluorescence induction promoter traps as tools for exploring niche-specific gene expression. Microbiol. Mol. Biol. Rev. 69:217-261.
54. Reglier-Poupet, H., C. Frehel, I. Dubail, J. L. Beretti, P. Berche, A. Charbit, and C. Raynaud. 2003. Maturation of lipoproteins by type II signal peptidase is required for phagosomal escape of Listeria monocytogenes. J. Biol. Chem. 278:49469-49477.
55. 50 and relative toxicity. Cesk. Fysiol. 10:408-422. (In Czech.)
56. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Expression of cloned genes in Escherichia coli, p. 17.37-17.41. In C. Nolan (ed.), Molecular cloning: a laboratory manual, vol. 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
57. Slutsker, L., and A. Schuchat. 1999. Subtyping Listeria monocytogenes. Marcel Dekker, Inc., New York, N.Y.
58. Soldo, B., V. Lazarevic, and D. Karamata. 2002. tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148:2079-2087.
59. Soldo, B., V. Lazarevic, P. Margot, and D. Karamata. 1993. Sequencing and analysis of the divergon comprising gtaB, the structural gene of UDP-glucose pyrophosphorylase of Bacillus subtilis 168. J. Gen. Microbiol. 139:3185-3195.
60. Soldo, B., V. Lazarevic, M. Pagni, and D. Karamata. 1999. Teichuronic acid operon of Bacillus subtilis 168. Mol. Microbiol. 31:795-805.
61. Soldo, B., V. Lazarevic, H. M. Pooley, and D. Karamata. 2002. Characterization of a Bacillus subtilis thermosensitive teichoic acid-deficient mutant: gene mnaA (yvyH) encodes the UDP-N-acetylglucosamine 2-epimerase. J. Bacteriol. 184:4316-4320.
62. Vadyvaloo, V., S. Arous, A. Gravesen, Y. Hechard, R. Chauhan-Haubrock, J. W. Hastings, and M. Rautenbach. 2004. Cell-surface alterations in class Ua bacteriocin-resistant Listeria monocytogenes strains. Microbiology 150:3025-3033.
63. Vazquez-Boland, J. A., M. Kuhn, P. Berche, T. Chakraborty, G. Dominguez-Bernal, W. Goebel, and B. Gonzalez-Zorn. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14:584-640.
64. Weidenmaier, C., J. F. Kokai-Kun, S. A. Kristian, T. Chanturiya, H. Kalbacher, M. Gross, G. Nicholson, B. Neumeister, J. J. Mond, and A. Peschel. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10:243-245.
65. Weidenmaier, C., A. Peschel, Y. Q. Xiong, S. A. Kristian, K. Dietz, M. R. Yeaman, and A. S. Bayer. 2005. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J. Infect. Dis. 191:1771-1777.
66. Wendlinger, G., M. J. Loessner, and S. Scherer. 1996. Bacteriophage receptors on Listeria monocytogenes cells are the N-acetylglucosamine and rhamnose substituents of teichoic acids or the peptidoglycan itself. Microbiology 142(Pt. 4):985-992.
67. Wilson, R. L., A. R. Tvinnereim, B. D. Jones, and J. T. Harty. 2001. Identification of Listeria monocytogenes in vivo-induced genes by fluorescence-activated cell sorting. Infect. Immun. 69:5016-5024.
68. Wu, J. D., H. C. Hsueh, W. T. Huang, H. S. Liu, H. W. Leung, Y. R. Ho, M. T. Lin, and M. D. Lai. 1997. The inducible lactose operator-repressor system is functional in the whole animal. DNA Cell Biol. 16:17-22.
69. Zalacain, M., S. Biswas, K. A. Ingraham, J. Ambrad, A. Bryant, A. F. Chalker, S. Iordanescu, J. Fan, F. Fan, R. D. Lunsford, K. O'Dwyer, L. M. Palmer, C. So, D. Sylvester, C. Volker, P. Warren, D. McDevitt, J. R. Brown, D. J. Holmes, and M. K. Burnham. 2003. A global approach to identify novel broad-spectrum antibacterial targets among proteins of unknown function. J. Mol. Microbiol. Biotechnol. 6:109-126.
70. Zhang, R., H. Y. Ou, and C. T. Zhang. 2004. DEG: a database of essential genes. Nucleic Acids Res. 32:271-272.
71. Zhao, X., Z. Li, B. Gu, and F. R. Frankel. 2005. Pathogenicity and immunogenicity of a vaccine strain of Listeria monocytogenes that relies on a suicide plasmid to supply an essential gene product. Infect. Immun. 73:5789-5798.