A role for the class a penicillin-binding protein PonA2 in the survival of Mycobacterium smegmatis under conditions of nonreplication

Journal of Bacteriology

Volumn 192, Issue 12, 2010, Pages 3043-3054

  Patru, Maria Magdalena ^a   Pavelka Jr , Martin S ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PENICILLIN BINDING PROTEIN 2A; PROLINE; PROTEIN SERINE THREONINE KINASE; PENICILLIN BINDING PROTEIN;

ADAPTATION; AMINO TERMINAL SEQUENCE; ANAEROBIC GROWTH; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM CULTURE; CELL CYCLE; CELL SURFACE; CONVALESCENCE; CROSS LINKING; CULTURAL ANTHROPOLOGY; ENVIRONMENTAL STRESS; GENOME; GENUS; LABORATORY; MORPHOLOGY; MUTANT; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PARALOGY; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SOIL MICROFLORA; STARVATION; SURVIVAL; AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; OXYGEN CONSUMPTION; PHYSIOLOGY; TIME;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM; MYCOBACTERIUM SMEGMATIS;

AMINO ACID SEQUENCE; ANAEROBIOSIS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTATION; MYCOBACTERIUM SMEGMATIS; OXYGEN CONSUMPTION; PENICILLIN-BINDING PROTEINS; TIME FACTORS;

EID: 77954005502     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00025-10     Document Type: Article

References (69)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New York, NY.
2. Azuma, I., D. W. Thomas, A. Adam, J. M. Ghuysen, R. Bonaly, J. F. Petit, and E. Lederer. 1970. Occurrence of N-glycolylmuramic acid in bacterial cell walls. A preliminary survey. Biochim. Biophys. Acta 208:444-451.
3. Balasubramanian, V., M. S. Pavelka, Jr., S. S. Bardarov, J. Martin, T. R. Weisbrod, R. A. McAdam, B. R. Bloom, and W. R. Jacobs, Jr. 1996. Allelic exchange in Mycobacterium tuberculosis with long linear recombination substrates. J. Bacteriol. 178:273-279.
4. Basu, J., S. Mahapatra, M. Kundu, S. Mukhopadhyay, M. Nguyen-Disteche, P. Dubois, B. Joris, J. Van Beeumen, S. T. Cole, P. Chakrabarti, and J. M. Ghuysen. 1996. Identification and overexpression in Escherichia coli of a Mycobacterium leprae gene, pon1, encoding a high-molecular-mass class A penicillin-binding protein, PBP1. J. Bacteriol. 178:1707-1711.
5. Bhakta, S., and J. Basu. 2002. Overexpression, purification and biochemical characterization of a class A high-molecular-mass penicillin-binding protein (PBP), PBP1*, and its soluble derivative from Mycobacterium tuberculosis. Biochem. J. 361:635-639.
6. Billman-Jacobe, H., R. E. Haites, and R. L. Coppel. 1999. Characterization of a Mycobacterium smegmatis mutant lacking penicillin binding protein 1. Antimicrob. Agents Chemother. 43:3011-3013.
7. Brennan, P. J. 2003. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis (Edinb.) 83:91-97.
8. Brennan, P. J., and H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64:29-63.
9. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry III, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, B. G. Barrell, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
10. Coulombe, F., M. Divangahi, F. Veyrier, L. de Leseleuc, J. L. Gleason, Y. Yang, M. A. Kelliher, A. K. Pandey, C. M. Sassetti, M. B. Reed, and M. A. Behr. 2009. Increased NOD2-mediated recognition of N-glycolyl muramyl dipeptide. J. Exp. Med. 206:1709-1716.
11. Dasgupta, A., P. Datta, M. Kundu, and J. Basu. 2006. The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 152:493-504.
12. Deng, L. L., D. E. Humphries, R. D. Arbeit, L. E. Carlton, S. C. Smole, and J. D. Carroll. 2005. Identification of a novel peptidoglycan hydrolase CwlM in Mycobacterium tuberculosis. Biochim. Biophys. Acta 1747:57-66.
13. Draper, P. 1976. Cell walls of Mycobacterium leprae. Int. J. Lepr. Other Mycobact. Dis. 44:95-98.
14. Flores, A. R., L. M. Parsons, and M. S. Pavelka, Jr. 2005. Characterization of novel Mycobacterium tuberculosis and Mycobacterium smegmatis mutants hypersusceptible to beta-lactam antibiotics. J. Bacteriol. 187:1892-1900.
15. Flores, A. R., L. M. Parsons, and M. S. Pavelka, Jr. 2005. Genetic analysis of the beta-lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to beta-lactam antibiotics. Microbiology 151:521-532.
16. Ghuysen, J. M. 1968. Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol. Rev. 32:425-464.
17. Goffin, C., and J. M. Ghuysen. 2002. Biochemistry and comparative genomics of SxxK superfamily acyltransferases offer a clue to the mycobacterial paradox: presence of penicillin-susceptible target proteins versus lack of efficiency of penicillin as therapeutic agent. Microbiol. Mol. Biol. Rev. 66:702-738.
18. Goffin, C., and J. M. Ghuysen. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079-1093.
19. Gomez, J. E., and J. D. McKinney. 2004. M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinb.) 84:29-44.
20. Gordon, E., N. Mouz, E. Duee, and O. Dideberg. 2000. The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance. J. Mol. Biol. 299:477-485.
21. Hett, E. C., M. C. Chao, A. J. Steyn, S. M. Fortune, L. L. Deng, and E. J. Rubin. 2007. A partner for the resuscitation-promoting factors of Mycobacterium tuberculosis. Mol. Microbiol. 66:658-668.
22. Iacono, V. J., S. M. Zove, B. L. Grossbard, J. J. Pollock, D. H. Fine, and L. S. Greene. 1985. Lysozyme-mediated aggregation and lysis of the periodontal microorganism Capnocytophaga gingivalis 2010. Infect. Immun. 47:457-464.
23. Jones, G., and P. Dyson. 2006. Evolution of transmembrane protein kinases implicated in coordinating remodeling of gram-positive peptidoglycan: inside versus outside. J. Bacteriol. 188:7470-7476.
24. Kay, B. K., M. P. Williamson, and M. Sudol. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14:231-241.
25. Keer, J., M. J. Smeulders, K. M. Gray, and H. D. Williams. 2000. Mutants of Mycobacterium smegmatis impaired in stationary-phase survival. Microbiology 146:2209-2217.
26. Khan, A. A., S. J. Kim, D. D. Paine, and C. E. Cerniglia. 2002. Classification of a polycyclic aromatic hydrocarbon-metabolizing bacterium, Mycobacterium sp. strain PYR-1, as Mycobacterium vanbaalenii sp. nov. Int. J. Syst. Evol. Microbiol. 52:1997-2002.
27. Kim, Y. H., K. H. Engesser, and C. E. Cerniglia. 2005. Numerical and genetic analysis of polycyclic aromatic hydrocarbon-degrading mycobacteria. Microb. Ecol. 50:110-119.
28. Kotani, S., I. Yanagida, K. Kato, and T. Matsuda. 1970. Studies on peptides, glycopeptides and antigenic polysaccharide-glycopeptide complexes isolated from an L-11 enzyme lysate of the cell walls of Mycobacterium tuberculosis strain H37Rv. Biken J. 13:249-275.
29. Kremer, L., and G. S. Besra. 2005. A waxy tale, by Mycobacterium tuberculosis, p. 287-305. In S. T. Cole, K. D. Eisenbach, D. N. McMurray, and J. W. R. Jacobs (ed.), Tuberculosis and the tubercle bacillus. ASM Press, Washington, DC.
30. Lam, H., D. C. Oh, F. Cava, C. N. Takacs, J. Clardy, M. A. de Pedro, and M. K. Waldor. 2009. D-Amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552-1555.
31. Lavollay, M., M. Arthur, M. Fourgeaud, L. Dubost, A. Marie, N. Veziris, D. Blanot, L. Gutmann, and J. L. Mainardi. 2008. The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by LD-transpeptidation. J. Bacteriol. 190:4360-4366.
32. Lederer, E. 1971. The mycobacterial cell wall. Pure Appl. Chem. 25:135-165.
33. Lu, J. Z., T. Fujiwara, H. Komatsuzawa, M. Sugai, and J. Sakon. 2006. Cell wall-targeting domain of glycylglycine endopeptidase distinguishes among peptidoglycan cross-bridges. J. Biol. Chem. 281:549-558.
34. Magnet, S., A. Arbeloa, J. L. Mainardi, J. E. Hugonnet, M. Fourgeaud, L. Dubost, A. Marie, V. Delfosse, C. Mayer, L. B. Rice, and M. Arthur. 2007. Specificity of L,D-transpeptidases from Gram-positive bacteria producing different peptidoglycan chemotypes. J. Biol. Chem. 282:13151-13159.
35. Mahapatra, S., J. Basu, P. J. Brennan, and D. C. Crick. 2005. Structure, biosynthesis, and genetics of the mycolic acid-arabinogalactan-peptidoglycan complex, p. 275-277. In S. T. Cole, K. D. Eisenbach, D. N. McMurray, and J. W. R. Jacobs (ed.), Tuberculosis and the tubercle bacillus. ASM Press, Washington, DC.
36. Mahapatra, S., S. Bhakta, J. Ahamed, and J. Basu. 2000. Characterization of derivatives of the high-molecular-mass penicillin-binding protein (PBP) 1 of Mycobacterium leprae. Biochem. J. 350:75-80.
37. Mahapatra, S., H. Scherman, P. J. Brennan, and D. C. Crick. 2005. N-glycolylation of the nucleotide precursors of peptidoglycan biosynthesis of Mycobacterium spp. is altered by drug treatment. J. Bacteriol. 187:2341-2347.
38. Mahapatra, S., T. Yagi, J. T. Belisle, B. J. Espinosa, P. J. Hill, M. R. McNeil, P. J. Brennan, and D. C. Crick. 2005. Mycobacterial lipid II is composed of a complex mixture of modified muramyl and peptide moieties linked to decaprenyl phosphate. J. Bacteriol. 187:2747-2757. (Pubitemid 40490379)
39. Mainardi, J. L., M. Fourgeaud, J. E. Hugonnet, L. Dubost, J. P. Brouard, J. Ouazzani, L. B. Rice, L. Gutmann, and M. Arthur. 2005. A novel peptidoglycan cross-linking enzyme for a beta-lactam-resistant transpeptidation pathway. J. Biol. Chem. 280:38146-38152.
40. Mainardi, J. L., R. Legrand, M. Arthur, B. Schoot, J. van Heijenoort, and L. Gutmann. 2000. Novel mechanism of beta-lactam resistance due to bypass of DD-transpeptidation in Enterococcus faecium. J. Biol. Chem. 275:16490-16496.
41. Mainardi, J. L., V. Morel, M. Fourgeaud, J. Cremniter, D. Blanot, R. Legrand, C. Frehel, M. Arthur, J. Van Heijenoort, and L. Gutmann. 2002. Balance between two transpeptidation mechanisms determines the expression of beta-lactam resistance in Enterococcus faecium. J. Biol. Chem. 277:35801-35807.
42. Miesel, L., T. R. Weisbrod, J. A. Marcinkeviciene, R. Bittman, and W. R. Jacobs, Jr. 1998. NADH dehydrogenase defects confer isoniazid resistance and conditional lethality in Mycobacterium smegmatis. J. Bacteriol. 180:2459-2467.
43. Miller, C. D., K. Hall, Y. N. Liang, K. Nieman, D. Sorensen, B. Issa, A. J. Anderson, and R. C. Sims. 2004. Isolation and characterization of polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates from soil. Microb. Ecol. 48:230-238.
44. Mukamolova, G. V., O. A. Turapov, D. I. Young, A. S. Kaprelyants, D. B. Kell, and M. Young. 2002. A family of autocrine growth factors in Mycobacterium tuberculosis. Mol. Microbiol. 46:623-635.
45. Paul, T. R., and T. J. Beveridge. 1992. Reevaluation of envelope profiles and cytoplasmic ultrastructure of mycobacteria processed by conventional embedding and freeze-substitution protocols. J. Bacteriol. 174:6508-6517.
46. Pavelka, M. S., Jr., and W. R. Jacobs, Jr. 1996. Biosynthesis of diaminopimelate (DAP), the precursor of lysine and a component of the peptidoglycan, is an essential function of Mycobacterium smegmatis. J. Bacteriol. 178:6496-6507.
47. Pavelka, M. S., Jr., and W. R. Jacobs, Jr. 1999. Comparison of the construction of unmarked deletion mutations in Mycobacterium smegmatis, Mycobacterium bovis bacillus Calmette-Guerin, and Mycobacterium tuberculosis H37Rv by allelic exchange. J. Bacteriol. 181:4780-4789.
48. Petit, J. F., A. Adam, and J. Wietzerbin-Falszpan. 1970. Isolation of UDP-N-glycolylmuramyl-(Ala, Glu, DAP) from Mycobacterium phlei. FEBS Lett. 6:55-57.
49. Petit, J. F., J. Wietzerbin, B. C. Das, and E. Lederer. 1975. Chemical structure of the cell wall of Mycobacterium tuberculosis var. bovis, strain BCG. Z. Immunitaetsforsch. Exp. Klin. Immunol. 149:118-125.
50. Quintela, J. C., M. Caparros, and M. A. de Pedro. 1995. Variability of peptidoglycan structural parameters in gram-negative bacteria. FEMS Microbiol. Lett. 125:95-100.
51. Quintela, J. C., M. A. de Pedro, P. Zollner, G. Allmaier, and F. Garcia-del Portillo. 1997. Peptidoglycan structure of Salmonella typhimurium growing within cultured mammalian cells. Mol. Microbiol. 23:693-704.
52. Ravi Chandra, B., R. Gowthaman, R. Raj Akhouri, D. Gupta, and A. Sharma. 2004. Distribution of proline-rich (PxxP) motifs in distinct proteomes: functional and therapeutic implications for malaria and tuberculosis. Protein Eng. Des. Sel. 17:175-182.
53. Raymond, J. B., S. Mahapatra, D. C. Crick, and M. S. Pavelka, Jr. 2005. Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J. Biol. Chem. 280:326-333.
54. Schleifer, K. H., and O. Kandler. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36:407-477.
55. Signoretto, C., M. M. Lleo, and P. Canepari. 2002. Modification of the peptidoglycan of Escherichia coli in the viable but nonculturable state. Curr. Microbiol. 44:125-131.
56. Slayden, R. A., and J. T. Belisle. 2009. Morphological features and signature gene response elicited by inactivation of FtsI in Mycobacterium tuberculosis. J. Antimicrob. Chemother. 63:451-457.
57. Slayden, R. A., D. L. Knudson, and J. T. Belisle. 2006. Identification of cell cycle regulators in Mycobacterium tuberculosis by inhibition of septum formation and global transcriptional analysis. Microbiology 152:1789-1797.
58. Snapper, S. B., R. E. Melton, S. Mustafa, T. Kieser, and W. R. Jacobs, Jr. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4:1911-1919.
59. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. Benson, L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, et al. 1991. New use of BCG for recombinant vaccines. Nature 351:456-460.
60. Turner, M. S., L. M. Hafner, T. Walsh, and P. M. Giffard. 2004. Identification, characterisation and specificity of a cell wall lytic enzyme from Lactobacillus fermentum BR11. FEMS Microbiol. Lett. 238:9-15.
61. Vandal, O. H., L. M. Pierini, D. Schnappinger, C. F. Nathan, and S. Ehrt. 2008. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat. Med. 14:849-854.
62. Vandal, O. H., J. A. Roberts, T. Odaira, D. Schnappinger, C. F. Nathan, and S. Ehrt. 2009. Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J. Bacteriol. 191:625-631.
63. Wayne, L. G., and K. Y. Lin. 1982. Glyoxylate metabolism and adaptation of Mycobacterium tuberculosis to survival under anaerobic conditions. Infect. Immun. 37:1042-1049.
64. Whisstock, J. C., and A. M. Lesk. 1999. SH3 domains in prokaryotes. Trends Biochem. Sci. 24:132-133.
65. Wietzerbin, J., B. C. Das, J.-F. Petit, E. Lederer, M. Leyh-Bouille, and J.-M. Ghuysen. 1974. Occurence of D-alanyl-(D)-meso-diaminopimelic acid and meso-diaminopimelyl-meso-diaminopimelic acid interpeptide linkages in the peptidoglycan of mycobacteria. Biochemistry 13:3471-3476.
66. Williamson, M. P. 1994. The structure and function of proline-rich regions in proteins. Biochem. J. 297:249-260. (Pubitemid 24026414)
67. Yeats, C., R. D. Finn, and A. Bateman. 2002. The PASTA domain: a beta-lactam-binding domain. Trends Biochem. Sci. 27:438.
68. Zhao, G., T. I. Meier, S. D. Kahl, K. R. Gee, and L. C. Blaszczak. 1999. BOCILLIN FL, a sensitive and commercially available reagent for detection of penicillin-binding proteins. Antimicrob. Agents Chemother. 43:1124-1128.
69. Zhu, W., B. B. Plikaytis, and T. M. Shinnick. 2003. Resuscitation factors from mycobacteria: homologs of Micrococcus luteus proteins. Tuberculosis (Edinb.) 83:261-269.