Dissecting the mycobacterial cell envelope and defining the composition of the native mycomembrane

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Chiaradia, Laura ^a   Lefebvre, Cyril ^a   Parra, Julien ^a   Marcoux, Julien ^a   Burlet Schiltz, Odile ^a   Etienne, Gilles ^a   Tropis, Maryelle ^a   Daffé, Mamadou ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BIOLOGICAL MARKER; LIPOPOLYSACCHARIDE; MEMBRANE LIPID; MEMBRANE PROTEIN; MULTIENZYME COMPLEX; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE;

BIOLOGICAL MODEL; CELL MEMBRANE; CELL WALL; METABOLISM; MYCOBACTERIUM; PROTEOMICS; ULTRASTRUCTURE;

BACTERIAL PROTEINS; BIOMARKERS; CELL MEMBRANE; CELL WALL; LIPOPOLYSACCHARIDES; MEMBRANE LIPIDS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MULTIENZYME COMPLEXES; MYCOBACTERIUM; NADH, NADPH OXIDOREDUCTASES; PROTEOMICS;

EID: 85030978389     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-12718-4     Document Type: Article

References (45)

1. Han, X. Y. et al. A new Mycobacterium species causing diffuse lepromatous leprosy. Am J Clin Pathol 130, 856-864 (2008).
2. Wayne, L. G. & Kubica, G. P. The Mycobacteria. The Bergey's manual of systematic bacteriology 2, 1435-1457 (1986).
3. Daffe, M. & Draper, P. The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39, 131-203 (1998).
4. Brennan, P. J. & Goren, M. B. Structural studies on the type-specific antigens and lipids of the mycobacterium avium. Mycobacterium intracellulare. Mycobacterium scrofulaceum serocomplex. Mycobacterium intracellulare serotype 9. J Biol Chem 254, 4205-4211 (1979).
5. Jarlier, V. & Nikaido, H. Permeability Barrier to Hydrophilic Solutes in Mycobacterium-Chelonei. J Bacteriol 172, 1418-1423 (1990).
6. Zuber, B. et al. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol 190, 5672-5680 (2008).
7. Sani, M. et al. Direct Visualization by Cryo-EM of the Mycobacterial Capsular Layer: A Labile Structure Containing ESX-1-Secreted Proteins. Plos Pathog 6 (2010).
8. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M. & Engelhardt, H. Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. P Natl Acad Sci USA 105, 3963-3967 (2008).
9. Marrakchi, H., Laneelle, M. A. & Daffe, M. Mycolic Acids: Structures, Biosynthesis, and Beyond. Chem Biol 21, 67-85 (2014).
10. Bansal-Mutalik, R. & Nikaido, H. Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc Natl Acad Sci USA 111, 4958-4963 (2014).
11. Daffé, M., Quémard, A. & Marrakchi, H. Mycolic Acids: From Chemistry to Biology. Biogenesis of Fatty Acids, Lipids and Membranes, 1-36, doi: https://doi.org/10.1007/978-3-319-43676-0-18-1 (2017).
12. Daffé, M. & Etienne, G. The capsule of of Mycobacterium tuberculosis and its implication for pathogenicity. Tubercle and Lung Disease 79, 153-169 (1999).
13. Lemassu, A. et al. Extracellular and surface-exposed polysaccharides of non-tuberculous mycobacteria. Microbiology-Uk 142, 1513-1520 (1996).
14. Ortalomagne, A. et al. Molecular Composition of the Outermost Capsular Material of the Tubercle Bacillus. Microbiol-Uk 141, 1609-1620 (1995).
15. OrtaloMagne, A. et al. Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species. J Bacteriol 178, 456-461 (1996).
16. Stahl, C. et al. MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis. Mol Microbiol 40, 451-464 (2001).
17. Harboe, M., Oettinger, T., Wiker, H. G., Rosenkrands, I. & Andersen, P. Evidence for occurrence of the ESAT-6 protein in Mycobacterium tuberculosis and virulent Mycobacterium bovis and for its absence in Mycobacterium bovis BCG. Infect Immun 64, 16-22 (1996).
18. Buddle, B. M. et al. Differentiation between Mycobacterium bovis BCG-vaccinated and M. bovis-infected cattle by using recombinant mycobacterial antigens. Clinical and diagnostic laboratory immunology 6, 1-5 (1999).
19. Moradi, J., Mosavari, N., Ebrahimi, M., Arefpajohi, R. & Tebianian, M. Evaluation of Mycobacterium tuberculosis Early Secreted Antigenic Target 6 Recombinant Protein as a Diagnostic Marker in SkinTest. Osong public health and research perspectives 6, 34-38 (2015).
20. Rezwan, M., Laneelle, M. A., Sander, P. & Daffe, M. Breaking down the wall: Fractionation of mycobacteria. J Microbiol Meth 68, 32-39 (2007).
21. Marchand, C. H. et al. Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum. J Bacteriol 194, 587-597 (2012).
22. Kim, M. S. & Kim, Y. J. Enzymatic properties of the membrane-bound NADH oxidase system in the aerobic respiratory chain of Bacillus cereus. Journal of biochemistry and molecular biology 37, 753-756 (2004).
23. Wiker, H. G. & Harboe, M. The antigen 85 complex: a major secretion product of Mycobacterium tuberculosis. Microbiol Rev 56, 648-661 (1992).
24. Belisle, J. T. et al. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276, 1420-1422 (1997).
25. Dautin, N. et al. Mycoloyltransferases: A large and major family of enzymes shaping the cell envelope of Corynebacteriales. Biochim Biophys Acta 1861, 3581-3592 (2017).
26. Jackson, M. et al. Inactivation of the antigen 85C gene profoundly affects the mycolate content and alters the permeability of the Mycobacterium tuberculosis cell envelope. Mol Microbiol 31, 1573-1587 (1999).
27. Daffe, M. The mycobacterial antigens 85 complex-from structure to function and beyond. Trends Microbiol 8, 438-440 (2000).
28. De Bruyn, J. et al. Purification, characterization and identification of a 32 kDa protein antigen of Mycobacterium bovis BCG. Microb Pathogenesis 2, 351-366 (1987).
29. Niederweis, M. Nutrient acquisition by mycobacteria. Microbiology 154, 679-692 (2008).
30. Niederweis, M. et al. Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Mol Microbiol 33, 933-945 (1999).
31. Kaur, D., Guerin, M. E., Skovierova, H., Brennan, P. J. & Jackson, M. Biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Advances in applied microbiology 69, 23-78, https://doi.org/10.1016/S0065-2164(09)69002-X (2009).
32. Abrahams, K. A. & Besra, G. S. Mycobacterial cell wall biosynthesis: a multifaceted antibiotic target. Parasitology, 1-18, doi: https://doi.org/10.1017/S0031182016002377 (2016).
33. Etienne, G. et al. The impact of the absence of glycopeptidolipids on the ultrastructure, cell surface and cell wall properties, and phagocytosis of Mycobacterium smegmatis. Microbiology 148, 3089-3100 (2002).
34. Dhiman, R. K. et al. Lipoarabinomannan Localization and Abundance during Growth of Mycobacterium smegmatis. J Bacteriol 193, 5802-5809 (2011).
35. Frehel, C., de Chastellier, C., Lang, T. & Rastogi, N. Evidence for inhibition of fusion of lysosomal and prelysosomal compartments with phagosomes in macrophages infected with pathogenic Mycobacterium avium. Infect Immun 52, 252-262 (1986).
36. Quemard, A., Mazeres, S., Sut, A., Laneelle, G. & Lacave, C. Certain properties of isoniazid inhibition of mycolic acid synthesis in cell-free systems of M. aurum and M. avium. Biochim Biophys Acta 1254, 98-104 (1995).
37. Quemard, A. et al. Structure of a hydroxymycolic acid potentially involved in the synthesis of oxygenated mycolic acids of the Mycobacterium tuberculosis complex. Eur J Biochem 250, 758-763 (1997).
38. Quemard, A., Lacave, C. & Laneelle, G. Isoniazid inhibition of mycolic acid synthesis by cell extracts of sensitive and resistant strains of Mycobacterium aurum. Antimicrob Agents Chemother 35, 1035-1039 (1991).
39. Portevin, D. et al. The acyl-AMP ligase FadD32 and AccD4-containing acyl-CoA carboxylase are required for the synthesis of mycolic acids and essential for mycobacterial growth: identification of the carboxylation product and determination of the acyl-CoA carboxylase components. J Biol Chem 280, 8862-8874, https://doi.org/10.1074/jbc.M408578200 (2005).
40. Portevin, D. et al. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci USA 101, 314-319, https://doi.org/10.1073/pnas.0305439101 (2004).
41. Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Canadian journal of biochemistry and physiology 37, 911-917 (1959).
42. Daffé, M., Lanéelle, M. A., Asselineau, C., Lévy-Frébault, V. & David, H. L. Intérêt taxonomique des acides gras des Mycobactéries: proposition d'une méthode d'analyse. Ann. Microbiol. (Inst. Pasteur) 134, 241-256 (1983).
43. Tsai, C. M. & Frasch, C. E. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119, 115-119 (1982).
44. Prinzis, S., Chatterjee, D. & Brennan, P. J. Structure and antigenicity of lipoarabinomannan from Mycobacterium bovis BCG. J Gen Microbiol 139, 2649-2658 (1993).
45. Schieber, A., Bruckner, H. & Ling, J. R. GC-MS analysis of diaminopimelic acid stereoisomers and amino acid enantiomers in rumen bacteria. Biomedical chromatography: BMC 13, 46-50, https://doi.org/10.1002/(SICI)1099-0801(199902)13:1 < 46:AID-BMC808 > 3.0.CO;2-4 (1999).