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21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules

Authors: Caroline Deshayes1, Dana Kocíncová2, Gilles Etienne3, Jean-Marc Reyrat4
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Affiliations: 1: Faculté de Médecine René Descartes, Université Paris Descartes, and Groupe Avenir, Unité de Pathogénie des Infections Systémiques—U570, INSERM, F-75730 Paris Cedex 15, France; 2: Faculté de Médecine René Descartes, Université Paris Descartes, and Groupe Avenir, Unité de Pathogénie des Infections Systémiques—U570, INSERM, F-75730 Paris Cedex 15, France; 3: Department of Molecular Mechanisms of Mycobacterial Infections, Institut de Pharmacologie et de Biologie Structurale du Centre National de la Recherche Scientifique (CNRS), and Université Paul Sabatier, 205 route de Narbonne, 31077 Toulouse Cedex 4, France; 4: Faculté de Médecine René Descartes, Université Paris Descartes, and Groupe Avenir, Unité de Pathogénie des Infections Systémiques—U570, INSERM, F-75730 Paris Cedex 15, France
Content Type: Monograph
Publication Year: 2008
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Abstract:

This chapter describes the major advances in the understanding of the biology and biosynthesis of glycopeptidolipids (GPLs). Strains from the complex contain surface species-specific lipids, allowing their precise identification. In bv. Peregrinum, two major GPLs were characterized by a combination of chemical analyses. The -- complex (MAC) is among the most common nontuberculous mycobacteria recovered from clinical specimens and is also a prevalent pathogen in AIDS patients. An immunogenic GPL, named GPL X-I, was isolated from , a nontuberculous mycobacterium responsible for pulmonary and disseminated infectious diseases mainly occurring in immunocompromised patients. subsp. paratuberculosis is closely related to subsp. and is responsible for cattle infections. The isolation of GPL-nonproducing mutants after a transposon mutagenesis of was greatly facilitated thanks to the characteristic morphotypes of these mutants. The lipopeptide core can be modified by glycosylation, O methylation, and O acetylation, and each of the genes responsible for these modifications has been characterized. Freeze-fracture electron microscopy has been used to study the structure of the envelope of cells growing inside mouse liver macrophages and has revealed an onion-like structure. A study investigated the consequence of drug treatment with a regimen of clarithromycin and ethambutol on the chemical alterations of GPLs in . Small metabolites such as sulfolipids, phenolglycolipids, or glycopeptidolipids use the same building blocks that are Pks, FadD, FadE, MmpL, and Gtf and that have evolved substrate specificity.

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
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21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules
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Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
/content/10.1128/9781555815783.ch21.ch21fig01
Figure 1.
General structures of mycobacterial GPLs. (Adapted from ; and .) Ac, acetyl.
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10.1128/9781555815783/f0346-01.gif
Image of Figure 1.
Figure 1.

General structures of mycobacterial GPLs. (Adapted from ; and .) Ac, acetyl.

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
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Figure 2.
(A) Structural aspect of the multilamellar coat (asterisk) that invests intraphagosomal bacilli in mouse liver cells after 3-month infections as revealed by freeze fracture electron microscopy (magnification, X62,000) ( ). (B) Transmission electron micrograph of strain mc155 and a non-GPL-producing mutant ( ).
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10.1128/9781555815783/f0349-01.gif
Image of Figure 2.
Figure 2.

(A) Structural aspect of the multilamellar coat (asterisk) that invests intraphagosomal bacilli in mouse liver cells after 3-month infections as revealed by freeze fracture electron microscopy (magnification, X62,000) ( ). (B) Transmission electron micrograph of strain mc155 and a non-GPL-producing mutant ( ).

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
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/content/10.1128/9781555815783.ch21.ch21fig03
Figure 3.
Genetic organization of the GPL locus in various mycobacterial species. The ORFs are depicted as arrows and have been drawn proportionally to their size ( ). Color code: light blue, family; black, unknown; purple, sugar biosynthesis, activation, transfer and modifications; red, lipid biosynthesis, activation, transfer and modifications; green, pseudopeptide biosynthesis; yellow, required for GPL transport to the surface; gray, regulation.
10.1128/9781555815783/f0351-01_thmb.gif
10.1128/9781555815783/f0351-01.gif
Image of Figure 3.
Figure 3.

Genetic organization of the GPL locus in various mycobacterial species. The ORFs are depicted as arrows and have been drawn proportionally to their size ( ). Color code: light blue, family; black, unknown; purple, sugar biosynthesis, activation, transfer and modifications; red, lipid biosynthesis, activation, transfer and modifications; green, pseudopeptide biosynthesis; yellow, required for GPL transport to the surface; gray, regulation.

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
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Figure 4.
(A) Transmission electron microscopy analysis of the wild-type strain mc155 and the gap mutant strain after ruthenium red staining ( ). (B) Topology of Gap protein predicted by Sosui program. (C) Amino acid alignment of various Gap orthologues found in sequenced mycobacterial genomes: (MSMEG), (Rv), subsp. (MAP) and (ML). Color code: red, high concensus (>90%); blue, low consensus (>50%). The central parts bordered in orange correspond to the predicted cytoplasmic portion and may be the region of selectivity of Gap proteins.
10.1128/9781555815783/f0354-01_thmb.gif
10.1128/9781555815783/f0354-01.gif
Image of Figure 4.
Figure 4.

(A) Transmission electron microscopy analysis of the wild-type strain mc155 and the gap mutant strain after ruthenium red staining ( ). (B) Topology of Gap protein predicted by Sosui program. (C) Amino acid alignment of various Gap orthologues found in sequenced mycobacterial genomes: (MSMEG), (Rv), subsp. (MAP) and (ML). Color code: red, high concensus (>90%); blue, low consensus (>50%). The central parts bordered in orange correspond to the predicted cytoplasmic portion and may be the region of selectivity of Gap proteins.

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
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Figure 5.
The mechanism arising in the upstream region of the operon in . In the ATCC607 strain, the operon is under the direct or indirect negative control of Lsr2, which leads to a low level of mRNA and a low level of GPLs (Kocincova et al., unpublished data). In the mutant, the operon is highly expressed because of the absence of the negative regulator Lsr2 that leads to high production of GPLs. In the mc155 strain, the Lsr2-dependent regulation is lost upon insertion of the mobile element, which leads to a major expression of the operon and consequently to a high level of GPL.
10.1128/9781555815783/f0355-01_thmb.gif
10.1128/9781555815783/f0355-01.gif
Image of Figure 5.
Figure 5.

The mechanism arising in the upstream region of the operon in . In the ATCC607 strain, the operon is under the direct or indirect negative control of Lsr2, which leads to a low level of mRNA and a low level of GPLs (Kocincova et al., unpublished data). In the mutant, the operon is highly expressed because of the absence of the negative regulator Lsr2 that leads to high production of GPLs. In the mc155 strain, the Lsr2-dependent regulation is lost upon insertion of the mobile element, which leads to a major expression of the operon and consequently to a high level of GPL.

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
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Figure 6.
Motility on Tween 80-containing plate of mc155 (A) and a GPL-nonproducing mutant (B). (Our unpublished data).
10.1128/9781555815783/f0358-01_thmb.gif
10.1128/9781555815783/f0358-01.gif
Image of Figure 6.
Figure 6.

Motility on Tween 80-containing plate of mc155 (A) and a GPL-nonproducing mutant (B). (Our unpublished data).

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
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References

/content/book/10.1128/9781555815783.ch21
1. Aspinall, G. O.,, D. Chatterjee, and, P. J. Brennan. 1995. The variable surface glycolipids of mycobacteria: structures, synthesis of epitopes, and biological properties. Adv. Carbohydr. Chem. Biochem. 51: 169– 242.
2. Barrow, W. W. 1997. Processing of mycobacterial lipids and effects on host responsiveness. Front. Biosci. 2: d387– d400.
3. Barrow, W. W.,, B. P. Ullom, and, P. J. Brennan. 1980. Peptidoglycolipid nature of the superficial cell wall sheath of smoothcolony-forming mycobacteria. J. Bacteriol. 144: 814– 822.
4. Barrow, W. W., and, P. J. Brennan. 1982. Isolation in high frequency of rough variants of Mycobacterium intracellulare lacking C-mycoside glycopeptidolipid antigens. J. Bacteriol. 150: 381– 384.
5. Barrow, W. W.,, J. P. de Sousa,, T. L. Davis,, E. L. Wright,, M. Bachelet, and, N. Rastogi. 1993. Immunomodulation of human peripheral blood mononuclear cell functions by defined lipid fractions of Mycobacterium avium. Infect. Immun. 61: 5286– 5293.
6. Barrow, W. W.,, T. L. Davis,, E. L. Wright,, V. Labrousse,, M. Bachelet, and, N. Rastogi. 1995. Immunomodulatory spectrum of lipids associated with Mycobacterium avium serovar 8. Infect. Immun. 63: 126– 133.
7. Beatty, W. L.,, E. R. Rhoades,, H. J. Ullrich,, D. Chatterjee,, J. E. Heuser, and, D. G. Russell. 2000. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1: 235– 247.
8. Belisle, J. T., and, P. J. Brennan. 1989. Chemical basis of rough and smooth variation in mycobacteria. J. Bacteriol. 171: 3465– 3470.
9. Belisle, J. T.,, L. Pascopella,, J. M. Inamine,, P. J. Brennan, and, W. R. Jacobs, Jr. 1991. Isolation and expression of a gene cluster responsible for biosynthesis of the glycopeptidolipid antigens of Mycobacterium avium. J. Bacteriol. 173: 6991– 6997.
10. Belisle, J. T.,, K. Klaczkiewicz,, P. J. Brennan,, W. R. Jacobs, Jr., and, J. M. Inamine. 1993. Rough morphological variants of Mycobacterium avium. Characterization of genomic deletions resulting in the loss of glycopeptidolipid expression. J. Biol. Chem. 268: 10517– 10523.
11. Besra, G. S.,, M. R. McNeil,, B. Rivoire,, K. H. Khoo,, H. R. Morris,, A. Dell, and, P. J. Brennan. 1993. Further structural definition of a new family of glycopeptidolipids from Mycobacterium xenopi. Biochemistry 32: 347– 355.
12. Biet, F.,, M. L. Boschiroli,, M. F. Thorel, and, L. A. Guilloteau. 2005. Zoonotic aspects of Mycobacterium bovis and Mycobacterium avium-intracellulare complex (MAC). Vet. Res. 36: 411– 436.
13. Billman-Jacobe, H.,, M. J. McConville,, R. E. Haites,, S. Kovacevic, and, R. L. Coppel. 1999. Identification of a peptide synthetase involved in the biosynthesis of glycopeptidolipids of Mycobacterium smegmatis. Mol. Microbiol. 33: 1244– 1253.
14. Brennan, P. J., and, M. B. Goren. 1979. 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.
15. Brennan, P. J.,, H. Mayer,, G. O. Aspinall, and, J. E. Nam Shin. 1981. Structures of the glycopeptidolipid antigens from serovars in the Mycobacterium avium/Mycobacterium intracellulare/Mycobacterium scrofulaceum serocomplex. Eur. J. Biochem. 115: 7– 15.
16. Brennan, P. J. 1988. Mycobacterium and other actinomycetes, p. 203–298. In C. Ratledge and, S. G. Wilkinson (ed.), Microbial Lipids. Academic Press, London, United Kingdom.
17. Brennan, P. J., and, H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64: 29– 63.
18. Brown-Elliott, B. A., and, R. J. Wallace, Jr. 2002. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin. Microbiol. Rev. 15: 716– 746.
19. Brownback, P. E., and, W. W. Barrow. 1988. Modified lymphocyte response to mitogens after intraperitoneal injection of glycopeptidolipid antigens from Mycobacterium avium complex. Infect. Immun. 56: 1044– 1050.
20. Buglino, J.,, K. C. Onwueme,, J. A. Ferreras,, L. E. Quadri, and, C. D. Lima. 2004. Crystal structure of PapA5, a phthiocerol dimycocerosyl transferase from Mycobacterium tuberculosis. J. Biol. Chem. 279: 30634– 30642.
21. Byrd, T. F., and, C. R. Lyons. 1999. Preliminary characterization of a Mycobacterium abscessus mutant in human and murine models of infection. Infect. Immun. 67: 4700– 4707.
22. Camacho, L. R.,, P. Constant,, C. Raynaud,, M. A. Laneelle,, J. A. Triccas,, B. Gicquel,, M. Daffe, and, C. Guilhot. 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.
23. Camphausen, R. T.,, R. L. Jones, and, P. J. Brennan. 1985. A glycolipid antigen specific to Mycobacterium paratuberculosis: structure and antigenicity. Proc. Natl. Acad. Sci. USA 82: 3068– 3072.
24. Cane, D. E.,, C. T. Walsh, and, C. Khosla. 1998. Harnessing the biosynthetic code: combinations, permutations, and mutations. Science 282: 63– 68.
25. Cangelosi, G. A.,, C. O. Palermo,, J. P. Laurent,, A. M. Hamlin, and, W. H. Brabant. 1999. Colony morphotypes on Congo red agar segregate along species and drug susceptibility lines in the Mycobacterium avium-intracellulare complex. Microbiology 145 (Pt. 6): 1317– 1324.
26. Catherinot, E.,, J. Clarissou,, G. Etienne,, F. Ripoll,, J. F. Emile,, M. Daffe,, C. Perronne,, C. Soudais,, J. L. Gaillard, and, M. Rottman. 2007. Hypervirulence of a rough variant of the Mycobacterium abscessus type strain. Infect. Immun. 75: 1055– 1058.
27. Chatterjee, D., and, K. H. Khoo. 2001. The surface glycopeptidolipids of mycobacteria: structures and biological properties. Cell Mol. Life Sci. 58: 2018– 2042.
28. Chen, J. M.,, G. J. German,, D. C. Alexander,, H. Ren,, T. Tan, and, J. Liu. 2006. Roles of Lsr2 in colony morphology and biofilm formation of Mycobacterium smegmatis. J. Bacteriol. 188: 633– 641.
29. Chiu, J.,, J. Nussbaum,, S. Bozzette,, J. G. Tilles,, L. S. Young,, J. Leedom,, P. N. Heseltine, and, J. A. McCutchan. 1990. Treatment of disseminated Mycobacterium avium complex infection in AIDS with amikacin, ethambutol, rifampin, and ciprofloxacin. Ann. Intern. Med. 113: 358– 361.
30. Cole, S. T.,, R. Brosch,, J. Parkhill,, T. Garnier,, C. Churcher,, D. Harris,, S. V. Gordon,, K. Eiglmeier,, S. Gas,, C. E. Barry,, 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,, A. Krogh,, J. McLean,, S. Moule,, L. Murphy,, K. Oliver,, J. Osborne,, M. A. Quail,, M. A. Rajandream,, J. Rogers,, S. Rutter,, K. Seeger,, J. Skelton,, R. Squares,, S. Squares,, J. E. Sulston,, K. Taylor,, S. Whitehead, and, B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537– 544.
31. Converse, S. E.,, J. D. Mougous,, M. D. Leavell,, J. A. Leary,, C. R. Bertozzi, and, J. S. Cox. 2003. MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence. Proc. Natl. Acad. Sci. USA 100: 6121– 6126.
32. Cox, J. S.,, B. Chen,, M. McNeil, and, W. R., Jacobs, Jr. 1999. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402: 79– 83.
33. Daffe, M.,, M. A. Laneelle, and, G. Puzo. 1983. Structural elucidation by field desorption and electron-impact mass spectrometry of the C-mycosides isolated from Mycobacterium smegmatis. Biochim. Biophys. Acta 751: 439– 443.
34. Daffe, M., and, P. Draper. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39: 131– 203.
35. Deshayes, C.,, F. Laval,, H. Montrozier,, M. Daffe,, G. Etienne, and, J. M. Reyrat. 2005. A glycosyltransferase involved in biosynthesis of triglycosylated glycopeptidolipids in Mycobacterium smegmatis: impact on surface properties. J. Bacteriol. 187: 7283– 7291.
36. de Souza Matos, D. C.,, R. Marcovistz,, T. Neway,, A. M. Vieira da Silva,, E. N. Alves, and, C. Pilet. 2000. Immunostimulatory effects of polar glycopeptidolipids of Mycobacterium chelonae for inactivated rabies vaccine. Vaccine 18: 2125– 2131.
37. Domenech, P.,, M. B. Reed,, C. S. Dowd,, C. Manca,, G. Kaplan, and, C. E. Barry, III. 2004. The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis. J. Biol. Chem. 279: 21257– 21265.
38. Draper, P. 1974. The mycoside capsule of Mycobacterium avium 357. J. Gen. Microbiol. 83: 431– 433.
39. Draper, P., and, R. J. Rees. 1970. Electron-transparent zone of mycobacteria may be a defence mechanism. Nature 228: 860– 861.
40. Draper, P., and, R. J. Rees. 1973. The nature of the electron-transparent zone that surrounds Mycobacterium lepraemurium inside host cells. J. Gen. Microbiol. 77: 79– 87.
41. Eckstein, T. M.,, F. S. Silbaq,, D. Chatterjee,, N. J. Kelly,, P. J. Brennan, and, J. T. Belisle. 1998. Identification and recombinant expression of a Mycobacterium avium rhamnosyltransferase gene (rtfA) involved in glycopeptidolipid biosynthesis. J. Bacteriol. 180: 5567– 5573.
42. Eckstein, T. M.,, J. T. Belisle, and, J. M. Inamine. 2003. Proposed pathway for the biosynthesis of serovar-specific glycopeptidolipids in Mycobacterium avium serovar 2. Microbiology 149: 2797– 2807.
43. Eckstein, T. M.,, S. Chandrasekaran,, S. Mahapatra,, M. R. McNeil,, D. Chatterjee,, C. D. Rithner,, P. W. Ryan,, J. T. Belisle, and, J. M. Inamine. 2006. A major cell wall lipopeptide of Mycobacterium avium subspecies paratuberculosis. J. Biol. Chem. 281: 5209– 5215.
44. Etienne, G.,, C. Villeneuve,, H. Billman-Jacobe,, C. Astarie-Dequeker,, M. A. Dupont, and, M. Daffe. 2002. 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.
45. Freeman, R.,, H. Geier,, K. M. Weigel,, J. Do,, T. E. Ford, and, G. A. Cangelosi. 2006. Roles for cell wall glycopeptidolipid in surface adherence and planktonic dispersal of Mycobacterium avium. Appl. Environ. Microbiol. 72: 7554– 7558.
46. Fregnan, G. B.,, D. W. Smith, and, H. M. Randall. 1961. Biological and chemical studies on mycobacteria. Relationship of colony morphology to mycoside content for Mycobacterium kansasii and Mycobacterium fortuitum. J. Bacteriol. 82: 517– 527.
47. Fregnan, G. B., and, D. W. Smith. 1962. Description of various colony forms of mycobacteria. J. Bacteriol. 83: 819– 827.
48. Frehel, C.,, A. Ryter,, N. Rastogi, and, H. David. 1986. The electron-transparent zone in phagocytized Mycobacterium avium and other mycobacteria: formation, persistence and role in bacterial survival. Ann. Inst. Pasteur Microbiol. 137B: 239– 257.
49. Fujiwara, N.,, N. Nakata,, S. Maeda,, T. Naka,, M. Doe,, I. Yano, and, K. Kobayashi. 2007. Structural characterization of a specific glycopeptidolipid containing a novel N-acyl-deoxy sugar from Mycobacterium intracellulare serotype 7 and genetic analysis of its glycosylation pathway. J. Bacteriol. 189: 1099– 1108.
50. Furuchi, A., and, T. Tokunaga. 1972. Nature of the receptor substance of Mycobacterium smegmatis for D4 bacteriophage adsorption. J. Bacteriol. 111: 404– 411.
51. Gjata, B.,, C. Hannoun,, H. J. Boulouis,, T. Neway, and, C. Pilet. 1994. Adjuvant activity of polar glycopeptidolipids of Mycobacterium chelonae (pGPL-Mc) on the immunogenic and protective effects of an inactivated influenza vaccine. C. R. Acad. Sci. III 317: 257– 263.
52. Goren, M. B.,, J. K. McClatchy,, B. Martens, and, O. Brokl. 1972. Mycosides C: behavior as receptor site substance for mycobacteriophage D4. J. Virol. 9: 999– 1003.
53. Helmann, J. D. 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46: 47– 110.
54. Hines, M. E., II,, J. M. Jaynes,, S. A. Barker,, J. C. Newton,, F. M. Enright, and, T. G. Snider, III. 1993. Isolation and partial characterization of glycolipid fractions from Mycobacterium avium serovar 2 ( Mycobacterium paratuberculosis 18) that inhibit activated macrophages. Infect. Immun. 61: 1– 7.
55. Hooper, L. C.,, M. M. Johnson,, V. R. Khera, and, W. W. Barrow. 1986. Macrophage uptake and retention of radiolabeled glycopeptidolipid antigens associated with the superficial L1 layer of Mycobacterium intracellulare serovar 20. Infect. Immun. 54: 133– 141.
56. Hooper, L. C., and, W. W. Barrow. 1988. Decreased mitogenic response of murine spleen cells following intraperitoneal injection of serovar-specific glycopeptidolipid antigens from the Mycobacterium avium complex. Adv. Exp. Med. Biol. 239: 309– 325.
57. Horgen, L.,, E. L. Barrow,, W. W. Barrow, and, N. Rastogi. 2000. Exposure of human peripheral blood mononuclear cells to total lipids and serovar-specific glycopeptidolipids from Mycobacterium avium serovars 4 and 8 results in inhibition of TH1-type responses. Microb. Pathog. 29: 9– 16.
58. Howard, S. T.,, E. Rhoades,, J. Recht,, X. Pang,, A. Alsup,, R. Kolter,, C. R. Lyons, and, T. F. Byrd. 2006. Spontaneous reversion of Mycobacterium abscessus from a smooth to a rough morphotype is associated with reduced expression of glycopeptidolipid and reacquisition of an invasive phenotype. Microbiology 152: 1581– 1590.
59. Jain, M., and, J. S. Cox. 2005. Interaction between polyketide synthase and transporter suggests coupled synthesis and export of virulence lipid in M. tuberculosis. PLoS Pathog. 1: e2.
60. Jeevarajah, D.,, J. H. Patterson,, M. J. McConville, and, H. Billman-Jacobe. 2002. Modification of glycopeptidolipids by an Omethyltransferase of Mycobacterium smegmatis. Microbiology 148: 3079– 3087.
61. Jeevarajah, D.,, J. H. Patterson,, E. Taig,, T. Sargeant,, M. J. McConville, and, H. Billman-Jacobe. 2004. Methylation of GPLs in Mycobacterium smegmatis and Mycobacterium avium. J. Bacteriol. 186: 6792– 6799.
62. Kano, H.,, T. Doi,, Y. Fujita,, H. Takimoto,, I. Yano, and, Y. Kumazawa. 2005. Serotype-specific modulation of human monocyte functions by glycopeptidolipid (GPL) isolated from Mycobacterium avium complex. Biol. Pharm. Bull. 28: 335– 339.
63. Khoo, K. H.,, D. Chatterjee,, A. Dell,, H. R. Morris,, P. J. Brennan, and, P. Draper. 1996. Novel O-methylated terminal glucuronic acid characterizes the polar glycopeptidolipids of Mycobacterium habana strain TMC 5135. J. Biol. Chem. 271: 12333– 12342.
64. Khoo, K. H.,, E. Jarboe,, A. Barker,, J. Torrelles,, C. W. Kuo, and, D. Chatterjee. 1999. Altered expression profile of the surface glycopeptidolipids in drug-resistant clinical isolates of Mycobacterium avium complex. J. Biol. Chem. 274: 9778– 9785.
65. Kim, K.-S.,, M. R. J. Salton, and, L. Barksdale. 1976. Ultrastructure of superficial mycosidic integuments of Mycobacterium sp. J. Bacteriol. 125: 739– 743.
66. Kolk, A. H.,, R. Evers,, D. G. Groothuis,, H. Gilis, and, S. Kuijper. 1989. Production and characterization of monoclonal antibodies against specific serotypes of Mycobacterium avium and the Mycobacterium avium-Mycobacterium intracellulare-Mycobacterium scrofulaceum complex. Infect. Immun. 57: 2514– 2521.
67. Krzywinska, E.,, J. Krzywinski, and, J. S. Schorey. 2004. Phylogeny of Mycobacterium avium strains inferred from glycopeptidolipid biosynthesis pathway genes. Microbiology 150: 1699– 1706.
68. Kumar, S.,, M. Bose, and, M. Isa. 2006. Genotype analysis of human Mycobacterium avium isolates from India. Indian J. Med. Res. 123: 139– 144.
69. Lagrange, P. H.,, M. Fourgeaud,, T. Neway, and, C. Pilet. 1994. Enhanced resistance against lethal disseminated Candida albicans infection in mice treated with polar glycopeptidolipids from Mycobacterium chelonae (pGPL-Mc). C. R. Acad. Sci. III 317: 1107– 1113.
70. Lagrange, P. H.,, M. Fourgeaud,, T. Neway, and, C. Pilet. 1995. Mycobacterial polar glycopeptidolipids enhance resistance to experimental murine candidiasis. C. R. Acad. Sci. III 318: 359– 365.
71. Laneelle, G., and, J. Asselineau. 1962. Isolation of peptide lipids from Mycobacterium paratuberculosis. Biochim. Biophys. Acta 59: 731– 732.
72. Laneelle, M. A.,, G. Laneelle,, P. Bennet, and, J. Asselineau. 1965. On the lipids from a non-photochromogenic strain of mycobacteria. Bull. Soc. Chim. Biol. (Paris) 47: 2047– 2067.
73. Laurent, J. P.,, K. Hauge,, K. Burnside, and, G. Cangelosi. 2003. Mutational analysis of cell wall biosynthesis in Mycobacterium avium. J. Bacteriol. 185: 5003– 5006.
74. Lautru, S., and, G. L. Challis. 2004. Substrate recognition by nonribosomal peptide synthetase multi-enzymes. Microbiology 150: 1629– 1636.
75. Lopez Marin, L. M.,, M. A. Laneelle,, D. Prome,, M. Daffe,, G. Laneelle, and, J. C. Prome. 1991. Glycopeptidolipids from Mycobacterium fortuitum: a variant in the structure of C-mycoside. Biochemistry 30: 10536– 10542.
76. Lopez Marin,, L. M.,, M. A. Laneelle,, D. Prome,, G. Laneelle,, J. C. Prome, and, M. Daffe. 1992. Structure of a novel sulfate-containing mycobacterial glycolipid. Biochemistry 31: 11106– 11111.
77. Lopez Marin,, L. M.,, M. A. Laneelle,, D. Prome, and, M. Daffe. 1993. Structures of the glycopeptidolipid antigens of two animal pathogens: Mycobacterium senegalense and Mycobacterium porcinum. Eur. J. Biochem. 215: 859– 866.
78. Lopez-Marin, L. M.,, N. Gautier,, M. A. Laneelle,, G. Silve, and, M. Daffe. 1994a. Structures of the glycopeptidolipid antigens of Mycobacterium abscessus and Mycobacterium chelonae and possible chemical basis of the serological cross-reactions in the Mycobacterium fortuitum complex. Microbiology 140( Pt. 5): 1109– 1118.
79. Lopez-Marin, L. M.,, D. Quesada,, F. Lakhdar-Ghazal,, J. F. Tocanne, and, G. Laneelle. 1994b. Interactions of mycobacterial glycopeptidolipids with membranes: influence of carbohydrate on induced alterations. Biochemistry 33: 7056– 7061.
80. Ma, Y.,, J. A. Mills,, J. T. Belisle,, V. Vissa,, M. Howell,, K. Bowlin,, M. S. Scherman, and, M. McNeil. 1997. Determination of the pathway for rhamnose biosynthesis in mycobacteria: cloning, sequencing and expression of the Mycobacterium tuberculosis gene encoding alpha-D-glucose-1-phosphate thymidylyltransferase. Microbiology 143( Pt. 3): 937– 945.
81. Martinez, A.,, S. Torello, and, R. Kolter. 1999. Sliding motility in mycobacteria. J. Bacteriol. 181: 7331– 7338.
82. Maslow, J. N.,, V. R. Irani,, S. H. Lee,, T. M. Eckstein,, J. M. Inamine, and, J. T. Belisle. 2003. Biosynthetic specificity of the rhamnosyltransferase gene of Mycobacterium avium serovar 2 as determined by allelic exchange mutagenesis. Microbiology 149: 3193– 3202.
83. McCarthy, C. 1970. Spontaneous and induced mutation in Mycobacterium avium. Infect. Immun. 2: 223– 228.
84. Mederos, L. M.,, J. A. Valdivia,, M. A. Sempere, and, P. L. Valero-Guillen. 1998. Analysis of lipids reveals differences between ‘ Mycobacterium habana’ and Mycobacterium simiae. Microbiology 144( Pt. 5): 1181– 1188.
85. Mederos, L. M.,, J. A. Valdivia, and, P. L. Valero-Guillen. 2006. Lipids of ‘ Mycobacterium habana’, a synonym of Mycobacterium simiae with vaccine potential. Tuberculosis (Edinburgh) 86: 324– 329.
86. Miyamoto, Y.,, T. Mukai,, N. Nakata,, Y. Maeda,, M. Kai,, T. Naka,, I. Yano, and, M. Makino. 2006. Identification and characterization of the genes involved in glycosylation pathways of mycobacterial glycopeptidolipid biosynthesis. J. Bacteriol. 188: 86– 95.
87. Motiwala, A. S.,, L. Li,, V. Kapur, and, S. Sreevatsan. 2006. Current understanding of the genetic diversity of Mycobacterium avium subsp. paratuberculosis. Microbes Infect. 8: 1406– 1418.
88. Mukherjee, R.,, M. Gomez,, N. Jayaraman,, I. Smith, and, D. Chatterji. 2005. Hyperglycosylation of glycopeptidolipid of Mycobacterium smegmatis under nutrient starvation: structural studies. Microbiology 151: 2385– 2392.
89. Ojha, A. K.,, S. Varma, and, D. Chatterji. 2002. Synthesis of an unusual polar glycopeptidolipid in glucose-limited culture of Mycobacterium smegmatis. Microbiology 148: 3039– 3048.
90. Onwueme, K. C.,, J. A. Ferreras,, J. Buglino,, C. D. Lima, and, L. E. Quadri. 2004. Mycobacterial polyketide-associated proteins are acyltransferases: proof of principle with Mycobacterium tuberculosis PapA5. Proc. Natl. Acad. Sci. USA 101: 4608– 4613.
91. Ortalo-Magne, A.,, A. Lemassu,, M. A. Laneelle,, F. Bardou,, G. Silve,, P. Gounon,, G. Marchal, and, M. Daffe. 1996. Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species. J. Bacteriol. 178: 456– 461.
92. Patterson, J. H.,, M. J. McConville,, R. E. Haites,, R. L. Coppel, and, H. Billman-Jacobe. 2000. Identification of a methyltransferase from Mycobacterium smegmatis involved in glycopeptidolipid synthesis. J. Biol. Chem. 275: 4900– 4906.
93. Pourshafie, M.,, Q. Ayub, and, W. W. Barrow. 1993. Comparative effects of Mycobacterium avium glycopeptidolipid and lipopeptide fragment on the function and ultrastructure of mononuclear cells. Clin. Exp. Immunol. 93: 72– 79.
94. Pourshafie, M. R.,, G. Sonnenfeld, and, W. W. Barrow. 1999. Immunological and ultrastructural disruptions of T lymphocytes following exposure to the glycopeptidolipid isolated from the Mycobacterium avium complex. Scand. J. Immunol. 49: 405– 410.
95. Quadri, L. E.,, J. Sello,, T. A. Keating,, P. H. Weinreb, and, C. T. Walsh. 1998. Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin. Chem. Biol. 5: 631– 645.
96. Rastogi, N.,, C. Frehel, and, H. L. David. 1984. Cell envelope architectures of leprosy-derived corynebacteria, Mycobacterium leprae, and related organisms: a comparative study. Curr. Microbiol. 11: 23– 30.
97. Rastogi, N., and, H. L. David. 1988. Mechanisms of pathogenicity in mycobacteria. Biochimie 70: 1101– 1120.
98. Recht, J.,, A. Martinez,, S. Torello, and, R. Kolter. 2000. Genetic analysis of sliding motility in Mycobacterium smegmatis. J. Bacteriol. 182: 4348– 4351.
99. Recht, J., and, R. Kolter. 2001. Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J. Bacteriol. 183: 5718– 5724.
100. Ren, H.,, L. G. Dover,, S. T. Islam,, D. C. Alexander,, J. M. Chen,, G. S. Besra, and, J. Liu. 2007. Identification of the lipooligosaccharide biosynthetic gene cluster from Mycobacterium marinum. Mol. Microbiol. 63: 1345– 1359.
101. Ripoll, F.,, C. Deshayes,, S. Pasek,, F. Laval,, J. L. Beretti,, F. Biet,, J. L. Risler,, M. Daffé,, G. Etienne,, J. L. Gaillard, and, J. M. Reyrat. 2007. Genomics of glycopeptidolipid biosynthesis in Mycobacterium abscessus and M. chelonae. BMC Genomics 8: 114.
102. Riviere, M., and, G. Puzo. 1991. A new type of serine-containing glycopeptidolipid from Mycobacterium xenopi. J. Biol. Chem. 266: 9057– 9063.
103. Riviere, M.,, S. Auge,, J. Vercauteren,, E. Wisingerova, and, G. Puzo. 1993. Structure of a novel glycopeptidolipid antigen containing a O-methylated serine isolated from Mycobacterium xenopi. Complete 1H-NMR and 13C-NMR assignment. Eur. J. Biochem. 214: 395– 403.
104. Rosenberg, M., and, S. Kjelleberg. 1986. Hydrophobic interactions in bacterial adhesion. Adv. Microb. Ecol. 9: 353– 393.
105. Rulong, S.,, A. P. Aguas,, P. P. da Silva, and, M. T. Silva. 1991. Intramacrophagic Mycobacterium avium bacilli are coated by a multiple lamellar structure: freeze fracture analysis of infected mouse liver. Infect. Immun. 59: 3895– 3902.
106. Schaefer, W. B. 1965. Serologic identification and classification of the atypical mycobacteria by their agglutination. Am. Rev. Respir. Dis. 92: 85– 93.
107. Sermet-Gaudelus, I.,, M. Le Bourgeois,, C. Pierre-Audigier,, C. Offredo,, D. Guillemot,, S. Halley,, C. Akoua-Koffi,, V. Vincent,, V. Sivadon-Tardy,, A. Ferroni,, P. Berche,, P. Scheinmann,, G. Lenoir, and, J. L. Gaillard. 2003. Mycobacterium abscessus and children with cystic fibrosis. Emerg. Infect. Dis. 9: 1587– 1591.
108. Shimada, K.,, H. Takimoto,, I. Yano, and, Y. Kumazawa. 2006. Involvement of mannose receptor in glycopeptidolipid-mediated inhibition of phagosome-lysosome fusion. Microbiol. Immunol. 50: 243– 251.
109. Smith, D. W.,, H. M. Randall,, A. P. Maclennan, and, E. Lederer. 1960a. Mycosides: a new class of type-specific glycolipids of Mycobacteria. Nature 186: 887– 888.
110. Smith, D. W.,, H. M. Randall,, A. P. Maclennan,, R. K. Putney, and, S. V. Rao. 1960b. Detection of specific lipids in mycobacteria by infrared spectroscopy. J. Bacteriol. 79: 217– 229.
111. Sonden, B.,, D. Kocincova,, C. Deshayes,, D. Euphrasie,, L. Rhayat,, F. Laval,, C. Frehel,, M. Daffe,, G. Etienne, and, J. M. Reyrat. 2005. Gap, a mycobacterial specific integral membrane protein, is required for glycolipid transport to the cell surface. Mol. Microbiol. 58: 426– 440.
112. Straight, P. D.,, M. A. Fischbach,, C. T. Walsh,, D. Z. Rudner, and, R. Kolter. 2007. A singular enzymatic megacomplex from Bacillus subtilis. Proc. Natl. Acad. Sci. USA 104: 305– 310.
113. Sut, A.,, S. Sirugue,, S. Sixou,, F. Lakhdar-Ghazal,, J. F. Tocanne, and, G. Laneelle. 1990. Mycobacteria glycolipids as potential pathogenicity effectors: alteration of model and natural membranes. Biochemistry 29: 8498– 8502.
114. Takegaki, Y. 2000. Effect of serotype specific glycopeptidolipid (GPL) isolated from Mycobacterium avium complex (MAC) on phagocytosis and phagosome-lysosome fusion of human peripheral blood monocytes. Kekkaku 75: 9– 18.
115. Tereletsky, M. J., and, W. W. Barrow. 1983. Postphagocytic detection of glycopeptidolipids associated with the superficial L1 layer of Mycobacterium intracellulare. Infect. Immun. 41: 1312– 1321.
116. Torrelles, J. B.,, D. Ellis,, T. Osborne,, A. Hoefer,, I. M. Orme,, D. Chatterjee,, P. J. Brennan, and, A. M. Cooper. 2002. Characterization of virulence, colony morphotype and the glycopeptidolipid of Mycobacterium avium strain 104. Tuberculosis (Edinburgh) 82: 293– 300.
117. Vergne, I.,, M. Prats,, J. F. Tocanne, and, G. Laneelle. 1995. Mycobacterial glycopeptidolipid interactions with membranes: a monolayer study. FEBS Lett. 375: 254– 258.
118. Vergne, I., and, B. Desbat. 2000. Influence of the glycopeptidic moiety of mycobacterial glycopeptidolipids on their lateral organization in phospholipid monolayers. Biochim. Biophys. Acta 1467: 113– 123.
119. Vestal, A. L., and, G. P. Kubica. 1966. Differential colonial characteristics of mycobacteria on Middlebrook and Cohn 7H10 agarbase medium. Am. Rev. Respir. Dis. 94: 247– 252.
120. Villeneuve, C.,, G. Etienne,, V. Abadie,, H. Montrozier,, C. Bordier,, F. Laval,, M. Daffe,, I. Maridonneau-Parini, and, C. Astarie-Dequeker. 2003. Surface-exposed glycopeptidolipids of Mycobacterium smegmatis specifically inhibit the phagocytosis of mycobacteria by human macrophages. Identification of a novel family of glycopeptidolipids. J. Biol. Chem. 278: 51291– 51300.
121. Villeneuve, C.,, M. Gilleron,, I. Maridonneau-Parini,, M. Daffe,, C. Astarie-Dequeker, and, G. Etienne. 2005. Mycobacteria use their surface-exposed glycolipids to infect human macrophages through a receptor-dependent process. J. Lipid Res. 46: 475– 483.
122. Vincent-Naulleau, S.,, T. Neway,, D. Thibault,, F. Barrat,, H. J. Boulouis, and, C. Pilet, 1995. Effects of polar glycopeptidolipids of Mycobacterium chelonae (pGPL-Mc) on granulomacrophage progenitors. Res. Immunol. 146: 363– 371.
123. Vincent-Naulleau, S.,, D. Thibault,, T. Neway, and, C. Pilet. 1997. Stimulatory effects of polar glycopeptidolipids of Mycobacterium chelonae on murine haematopoietic stem cells and megakaryocyte progenitors. Res. Immunol. 148: 127– 136.
124. Waagmeester, A.,, J. Thompson, and, J. M. Reyrat. 2005. Identifying sigma factors in Mycobacterium smegmatis by comparative genomic analysis. Trends Microbiol. 13: 505– 509.
125. Walsh, C. T. 2004. Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303: 1805– 1810.
126. Woodley, C. L., and, H. L. David. 1976. Effect of temperature on the rate of the transparent to opaque colony type transition in Mycobacterium avium. Antimicrob. Agents Chemother. 9: 113– 119.
127. Yamazaki, Y.,, L. Danelishvili,, M. Wu,, M. Macnab, and, L. E. Bermudez. 2006. Mycobacterium avium genes associated with the ability to form a biofilm. Appl. Environ. Microbiol. 72: 819– 825.

Tables

21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules
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Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21
/content/10.1128/9781555815783.ch21.ch21tab01
Table 1.
Structures of some haptenic oligosaccharide extensions of GPLs from MAC serovars
Generic image for table
Table 1.

Structures of some haptenic oligosaccharide extensions of GPLs from MAC serovars

Citation: Deshayes C, Kocíncová D, Etienne G, Reyrat J. 2008. 21 Glycopeptidolipids: a Complex Pathway for Small Pleiotropic Molecules, p 345-365. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch21

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