Mobility and temperature resistance of trehalose mycolates as key characteristics of the outer membrane of Mycobacterium tuberculosis

Journal of Biomolecular Structure and Dynamics

Volumn 33, Issue 2, 2015, Pages 447-459

  Migliardo, Federica ^a   Salmeron, Christophe ^b   Bayan, Nicolas ^b  

^a UNIVERSITY OF MESSINA   (Italy)

^b INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

Author keywords

diffusion; Mycobacterium tuberculosis; quasi elastic neutron scattering; stability; trehalose mycolates

Indexed keywords

LIPID; PHOSPHATIDYLCHOLINE; TREHALOSE MYCOLATE; UNCLASSIFIED DRUG; MYCOLIC ACID; TREHALOSE; WATER;

ARTICLE; BACTERIAL OUTER MEMBRANE; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DYNAMICS; ELASTIC INCOHERENT STRUCTURE FACTOR; ELASTICITY; ENERGY; EXCHANGED WAVEVECTOR Q; HYDRATION; MYCOBACTERIUM TUBERCULOSIS; NEUTRON SCATTERING; NONHUMAN; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; QUASI ELASTIC NEUTRON SCATTERING; TEMPERATURE DEPENDENCE; CELL MEMBRANE; CELL WALL; CHEMICAL MODEL; CHEMISTRY;

MYCOBACTERIUM TUBERCULOSIS;

CELL MEMBRANE; CELL WALL; LECITHINS; MODELS, CHEMICAL; MYCOBACTERIUM TUBERCULOSIS; MYCOLIC ACIDS; TREHALOSE; WATER;

EID: 84914147626     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2014.887032     Document Type: Article

References (60)

1. Adams, M. A., Howells, W. S., & Telling, M. T. F. (2001). The IRIS user guide (2nd ed.). Didcot: ISIS Facility.
2. Affouard, F., Bordat, P., Descamps, M., Magazù, S., Migliardo, F., Ramirez-Cuesta, A. J., & Telling, M. T. F. (2005). A combined neutron scattering and simulation study on bioprotectant systems. Chemical Physics, 317, 258-266.
3. Bànky, D., Ivàn, G., & Grolmusz, V. (2013). Equal opportunity for low-degree network nodes: A PageRank based method for protein target identification in metabolic graphs. PLoS ONE, 8, e54204-1-e54204-7.
4. Barry, C. E. (2001). Interpreting cell wall "virulence factors" of Mycobacterium tuberculosis. Trends in Microbiology, 9, 237-241.
5. Barry, C. E., Lee, R. E., Mdluli, K., Sampson, A. E., Schroeder, B. G., Slayden, R. A., & Yuan, Y. (1998). Mycolic acids: Structure, biosynthesis and physiological functions. Progress in Lipid Research, 37, 143-179.
6. Bayan, N., Houssin, C., Chami, M., & Leblon, G. (2003). Mycomembrane and S-layer: Two important structures of Corynebacterium glutamicum cell envelope with promising biotechnology applications. Journal of Biotechnology, 104, 55-67.
7. Bee, M. (1988). Quasielastic neutron scattering. Bristol: A. Hilger.
8. Bou Raad, R., Meniche, X., de Sousa-d'Auria, C., Chami, M., Salmeron, C., Tropis, M., ⋯ Bayan, N. (2010). A deficiency in arabinogalactan biosynthesis affects Corynebacterium glutamicum mycolate outer membrane stability. Journal of Bacteriology, 192, 2691-2700.
9. Brennan, P. J., & Nikaido, H. (1995). The envelope of mycobacteria. Annual Review of Biochemistry, 64, 29-63.
10. Chatterjee, D. (1997). The mycobacterial cell wall: Structure, biosynthesis and sites of drug action. Current Opinion in Chemical Biology, 1, 579-588.
11. Crowe, J. H., Clegg, J. S., & Crowe, L. M. (1998). Anhydrobiosis: The water replacement hypothesis. In D. S. Reid (Ed.), The roles of water in foods (pp. 440-455). New York, NY: Chapman & Hall.
12. Crowe, J. H., & Crowe, L. M. (1984). Preservation of membranes in anhydrobiotic organisms: The role of trehalose. Science, 223, 701-703.
13. Crowe, L. M., Spargo, B. J., Ioneda, T., Beaman, B. L., & Crowe, J. H. (1994). Interaction of cord factor (α,α′-trehalose-6,6′-dimycolate) with phospholipids. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1194, 53-60.
14. Daffé, M., & Draper, P. (1998). The envelope layers of mycobacteria with reference to their pathogenicity. Advances in Microbial Physiology, 39, 131-203.
15. Dover, L. G., Cerdeno-Tarraga, A. M., Pallen, M. J., Parkhill, J., & Besra, G. S. (2004). Comparative cell wall core biosynthesis in the mycolated pathogens, Mycobacterium tuberculosis and Corynebacterium diphtheria. FEMS Microbiology Reviews, 28, 225-250.
16. Draper, P. (1998). The outer parts of the mycobacterial envelope as permeability barriers. Frontiers in Bioscience, 3, d1253-d1261.
17. Dubnau, E., Chan, J., Raynaud, C., Mohan, V. P., Laneelle, M.-A., Yu, K., ⋯ Daffé, M. (2000). Oxygenated mycolic acids are necessary for virulence of M. tuberculosis in mice. Molecular Microbiology, 36, 630-637.
18. Fisher, M. A., Plikaytis, B. B., & Shinnick, T. M. (2002). Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes. Journal of Bacteriology, 184, 4025-4032.
19. Fitter, J., Verclas, S. A. W., Lechner, R. E., Seelert, H., & Dencher, N. A. (1998). Function and picosecond dynamics of bacteriorhodopsin in purple membrane at different lipidation and hydration. FEBS Letters, 433, 321-325.
20. Garcia-Manyes, S., Oncins, G., & Sanz, F. (2005). Effect of temperature on the nanomechanics of lipid bilayers studied by force spectroscopy. Biophysical Journal, 89, 4261-4274.
21. Gebhardt, H., Meniche, X., Tropis, M., Kramer, R., Daffe, M., & Morbach, S. (2007). The key role of the mycolic acid content in the functionality of the cell wall permeability barrier in Corynebacterineae. Microbiology, 153, 1424-1434.
22. George, K. M., Yuan, Y., Sherman, D. R., & Barry, C. E., III (1995). The biosynthesis of cyclopropanated mycolic acids in Mycobacterium tuberculosis. Identification and functional analysis of cmas-2. Journal of Biological Chemistry, 270, 27292-27298.
23. Gliss, C., Randel, O., Casalta, H., Sackmann, E., Zorn, E., & Bayerl, T. (1999). Anisotropic motion of cholesterol in oriented DPPC bilayers studied by quasielastic neutron scattering: The liquid-ordered phase. Biophysical Journal, 77, 331-340.
24. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M., & Engelhardt, H. (2008). Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proceedings of the National Academy of Sciences, 105, 3963-3967.
25. Hong, X., & Hopfinger, A. J. (2004). Construction, molecular modeling, and simulation of Mycobacterium tuberculosis cell walls. Biomacromolecules, 5, 1052-1065.
26. Horváti, K., Bacsa, B., Szabó, N., Dávid, S., Mezo{double acute}, G., Grolmusz, V., ⋯ Bo{double acute}sze, S. (2012). Enhanced cellular uptake of a new, in silico identified antitubercular candidate by peptide conjugation. Bioconjugate Chemistry, 23, 900-907.
27. Konig, S., Bayerl, T. M., Coddens, G., Richter, D., & Sackmann, E. (1995). Hydration dependence of chain dynamics and local diffusion in L-alpha-dipalmitoylphosphtidylcholine multilayers studied by incoherent quasi-elastic neutron scattering. Biophysical Journal, 68, 1871-1880.
28. Liu, J., Barry, C. E., III, Besra, G. S., & Nikaido, H. (1996). Mycolic acid structure determines the fluidity of the mycobacterial cell wall. Journal of Biological Chemistry, 271, 29545-29551.
29. Magazù, S., Migliardo, F., Mondelli, C., & Vadalà, M. (2005). Correlation between bioprotective effectiveness and dynamic properties of trehalose-water, maltose-water and sucrose-water mixtures. Carbohydrate Research, 340, 2796-2801.
30. Magazù, S., Migliardo, F., & Ramirez-Cuesta, A. J. (2005). Inelastic neutron scattering study on bioprotectant systems. Journal of The Royal Society Interface, 2, 527-532.
31. Magazù, S., Migliardo, F., & Telling, M. T. F. (2006). α, α-Trehalose-water solutions. VIII. Study of the Diffusive dynamics of water by high-resolution quasi elastic neutron scattering. The Journal of Physical Chemistry B, 110, 1020-1025.
32. Magazù, S., Migliardo, F., & Telling, M. T. F. (2007). Study of the dynamical properties of water in disaccharide solutions. European Biophysics Journal, 36, 163-171.
33. Magazù, S., Migliardo, F., & Telling, M. T. F. (2008). Structural and dynamical properties of water in sugar mixtures. Food Chemistry, 106, 1460-1466.
34. Marchand, C. H., Salmeron, C., Bou Raad, R., Meniche, X., Chami, M., Masi, M., ⋯ Bayan, N. (2012). Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum. Journal of Bacteriology, 194, 587-597.
35. Mészáros, B., Tóth, J., Vértessy, B. G., Dosztányi, Z., & Simon, I. (2011). Proteins with complex architecture as potential targets for drug design: A case study of Mycobacterium tuberculosis. PLOS Computational Biology, 7, e1002118-1-e1002118-14.
36. Migliardo, F., Salmeron, C., & Bayan, N. (2013). A neutron scattering study on the stability of trehalose mycolates under thermal stress. Chemical Physics, 424, 70-74.
37. Minnikin, D. E. (1982). Lipids: Complex lipids, their chemistry, biosynthesis and roles. In C. Ratledge & J. Stanford (Eds.), The biology of the mycobacteria: Physiology, identification and classification (pp. 95-184). Parow: Academic Press.
38. Nikaido, H., Kim, S.-H., & Rosenberg, E. Y. (1993). Physical organization of lipids in the cell wall of Mycobacterium chelonae. Molecular Microbiology, 8, 1025-1030.
39. Oliver, A. E., Crowe, L. M., & Crowe, J. H. (1998). Methods for dehydration-tolerance: Depression of the phase transition temperature in dry membranes and carbohydrate vitrification. Seed Science Research, 8, 211-221.
40. Pecsi, I., Hirmondo, R., Brown, A. C., Lopata, A., Parish, T., Vertessy, B. G., & Tóth, J. (2012). The dUTPase enzyme is essential in Mycobacterium smegmatis. PLoS ONE, 7, e37461-1-e37461-11.
41. Puech, V., Chami, M., Lemassu, A., Laneelle, M. A., Schiffler, B., Gounon, P., ⋯ Daffè, M. (2001). Structure of the cell envelope of corynebacteria: Importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology, 147, 1365-1382.
42. Rastogi, N. (1991). Recent observations concerning structure and function relationships in the mycobacterial cell envelope: Elaboration of a model in terms of mycobacterial pathogenicity, virulence and drug-resistance. Research in Microbiology, 142, 464-476.
43. Rohde, K. H., Abramovitch, R. B., & Russell, D. G. (2007). Mycobacterium tuberculosis invasion of macrophages: Linking bacterial gene expression to environmental cues. Cell Host & Microbe, 2, 352-364.
44. Scheich, C., Szabadka, Z., Vértessy, B., Pütter, V., Grolmusz, V., & Schade, M. (2011). Discovery of novel MDR-Mycobacterium tuberculosis inhibitor by new FRIGATE computational screen. PLoS ONE, 6, e28428-1-e28428-9.
45. Swenson, J., Kargl, F., Berntsen, P., & Svanberg, C. (2008). Solvent and lipid dynamics of hydrated lipid bilayers by incoherent quasielastic neutron scattering. Journal of Chemical Physics, 29, 045101-1-045101-7.
46. Telling, M. T. F., & Andersen, K. H. (2005a). The OSIRIS user guide (2nd ed.). Didcot: ISIS Facility.
47. Telling, M. T. F., & Andersen, K. H. (2005b). Spectroscopic characteristics of the OSIRIS near-backscattering crystal analyser spectrometer on the ISIS pulsed neutron source. Physical Chemistry Chemical Physics, 7, 1255-1261.
48. Telling, M. T. F., & Howells, W. S. (2003). MODES - IRIS data analysis (1st ed.). Didcot: ISIS Facility.
49. Tews, I., Findeisen, F., Sinning, I., Schultz, A., Schultz, J. E., & Linder, J. U. (2005). The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science, 308, 1020-1023.
50. Tran, S. L., Rao, M., Simmers, C., Gebhard, S., Olsson, K., & Cook, G. M. (2005). Mutants of Mycobacterium smegmatis unable to grow at acidic pH in the presence of the protonophore carbonyl cyanide m-Chlorophenylhydrazone. Microbiology, 151, 665-672.
51. Trias, J., & Benz, R. (1994). Permeability of the cell wall of Mycobacterium smegmatis. Molecular Microbiology, 14, 283-290.
52. Vandal, O. H., Nathan, C. F., & Ehrt, S. (2009). Acid Resistance in Mycobacterium tuberculosis. Journal of Bacteriology, 191, 4714-4721.
53. Vandal, O. H., Roberts, J. A., Odaira, T., Schnappinger, D., Nathan, C. F., & Ehrt, S. (2009). Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. Journal of Bacteriology, 191, 625-631.
54. Varga, B., Barabás, O., Takács, E., Nagy, N., Nagy, P., & Vértessy, B. G. (2008). Active site of mycobacterial dUTPase: Structural characteristics and a built-in sensor. Biochemical and Biophysical Research Communications, 373, 8-13.
55. Vergne, I., Chua, J., Singh, S. B., & Deretic, V. (2004). Cell biology of Mycobacterium tuberculosis phagosome. Annual Review of Cell and Developmental Biology, 20, 367-394.
56. Vértessy, B. G., & Tóth, J. (2009). Keeping uracil out of DNA: Physiological role, structure and catalytic mechanism of dUTPases. Accounts of Chemical Research, 42, 97-106.
57. Volino, F. (1978). Microscopic structure and dynamics of liquids, NATO ASI series: Ser B, 71. New York, NY: Wiley.
58. Volino, F., & Dianoux, A. J. (1978). Organic liquids; structures dynamics and chemical properties, NATO ASI series: Ser B, 33. New York, NY: John.
59. WHO Global Tuberculosis Control Report. (2011). WHO library cataloguing-in-publication data. ISBN-9789241564380.
60. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., & Daffe, M. (2008). Direct visualization of the outer membrane of Mycobacteria and Corynebacteria in their native state. Journal of Bacteriology, 190, 5672-5680.