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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 ( ).
10.1128/9781555815783/f0349-01_thmb.gif
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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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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