18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

Carolyn R. Bertozzi; Michael W. Schelle

doi:10.1128/9781555815783.ch18

18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

Authors: Carolyn R. Bertozzi¹, Michael W. Schelle²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Departments of Chemistry and Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720-1460; 2: Department of Chemistry, University of California, Berkeley, Berkeley, CA 94720-1460

Content Type: Monograph

Publication Year: 2008

Book DOI: 10.1128/9781555815783

Chapter DOI: 10.1128/9781555815783.ch18

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555815783/9781555814687_Chap18-1.gif /docserver/preview/fulltext/10.1128/9781555815783/9781555814687_Chap18-2.gif

Abstract:

Sulfated metabolites are abundant in higher eukaryotes, where they play roles in cell-to-cell communication. This chapter highlights recent advances in the understanding of sulfolipid-1 (SL-1) biosynthesis and discusses the potential biological significance of SL-1 and other sulfated metabolites in the context of both historical observations and modern experiments. Sequencing of the Mycobacterium tuberculosis genome in 1998 provided the tools necessary to draw links from gene to protein and metabolite. A signaturetag mutagenesis (STM) screen identified mmpL7 as a gene essential for M. tuberculosis growth in a mouse model of infection. Sulfate ester functionality distinguishes SL-1 from other well-characterized mycobacterial lipids. Recently, Gap, a small integral membrane protein from Mycobacterium smegmatis was shown to be required for transport of glycopeptidolipids to the cell surface. In vivo analysis of the Δpks2 mutants left the SL-1 community questioning the importance of the molecule that had previously garnered so much attention. Attenuation of the ΔmmpL8 mutant in the persistent stage of M. tuberculosis infection contrasts with the reported phenotype of the Δpks2 mutants. Although M. tuberculosis is the most extensively studied species of the mycobacterial genus, several other mycobacteria have medical importance owing to their synergism with human immunodeficiency virus. One such species is the opportunistic environmental mycobacterium Mycobacterium avium, which preferentially infects individuals with compromised immunity. This pathogen also encodes nine putative sulfotransferases, the largest number of sulfotransferases of any sequenced mycobacterial species. As one's knowledge of human immunity grows, better cellular and in vivo models for M. tuberculosis virulence will be created.

Citation: Bertozzi C, Schelle M. 2008. 18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond, p 291-303. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch18

Key Concept Ranking

Tumor Necrosis Factor alpha: 0.48685843
Nuclear Magnetic Resonance Spectroscopy: 0.474583

0.48685843

Highlighted Text: Show | Hide

Full text loading...

Figures

18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815783.ch18-1,webId=/content/author/10.1128/9781555815783.ch18-1,properties={foaf_givenname=Carolyn R., foaf_name=Carolyn R. Bertozzi, foaf_surname=Bertozzi, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815783.ch18-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815783.ch18-2,webId=/content/author/10.1128/9781555815783.ch18-2,properties={foaf_givenname=Michael W., foaf_name=Michael W. Schelle, foaf_surname=Schelle, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815783.ch18-aff2]]}]]

/content/10.1128/9781555815783.ch18.ch18fig01

Figure 1.

The chemical structure of sulfolipid-1 (SL-1) and trehalose. The hydroxy-bearing carbons in the trehalose ring are numbered.

10.1128/9781555815783/f0292-01_thmb.gif

10.1128/9781555815783/f0292-01.gif

Figure 1.

The chemical structure of sulfolipid-1 (SL-1) and trehalose. The hydroxy-bearing carbons in the trehalose ring are numbered.

/content/10.1128/9781555815783.ch18.ch18fig02

Figure 2.

The biosynthesis of SL1278. Trehalose is sulfated by Stf0 to form trehalose-2-sulfate (T2S), which then is acylated with a palmitoyl group by PapA2 at the 2′ position to form SL659. This product is then acylated at the 3′ position by PapA1 with a hydroxyphthioceranoyl group synthesized by Pks2 to yield SL1278.

10.1128/9781555815783/f0294-01_thmb.gif

10.1128/9781555815783/f0294-01.gif

Figure 2.

/content/10.1128/9781555815783.ch18.ch18fig03

Figure 3.

Two possible pathways for completion of SL-1 biosynthesis. (A) Intracellular acylation of SL1278 is accomplished in the presence of MmpL8 by PapA1 and Pks2. SL-1 is then transported by MmpL8. (B) Extracellular acylation is accomplished by transport of SL1278 by MmpL8. The hydroxyphthioceranoyl moiety is also transported by an unknown protein and then coupled to SL1278 by an extracellular acyltransferase.

10.1128/9781555815783/f0295-01_thmb.gif

10.1128/9781555815783/f0295-01.gif

Figure 3.

/content/10.1128/9781555815783.ch18.ch18fig04

Figure 4.

Genetic arrangement of the SL-1 biosynthetic cluster.

10.1128/9781555815783/f0297-01_thmb.gif

10.1128/9781555815783/f0297-01.gif

Figure 4.

Genetic arrangement of the SL-1 biosynthetic cluster.

/content/10.1128/9781555815783.ch18.ch18fig05

Figure 5.

The chemical structure of S-GPL.

10.1128/9781555815783/f0301-01_thmb.gif

10.1128/9781555815783/f0301-01.gif

Figure 5.

The chemical structure of S-GPL.

References

/content/book/10.1128/9781555815783.ch18

1. Armstrong, J. A., and, P. D. Hart. 1971. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J. Exp. Med. 134: 713– 740.

2. Asselineau, C., and, J. Asselineau. 1978. Trehalose-containing glycolipids. Prog. Chem. Fats Other Lipids 16: 59– 99.

3. Belisle, J. T.,, V. D. Vissa,, T. Sievert,, K. Takayama,, P. J. Brennan, and, G. S. Besra. 1997. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276: 1420– 1422.

4. Brozna, J. P.,, M. Horan,, J. M. Rademacher,, K. M. Pabst, and, M. J. Pabst. 1991. Monocyte responses to sulfatide from Mycobacterium tuberculosis: inhibition of priming for enhanced release of superoxide, associated with increased secretion of interleukin-1 and tumor necrosis factor alpha, and altered protein phosphorylation. Infect. Immun. 59: 2542– 2548.

5. 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.

6. Carroll, K. S.,, H. Gao,, H. Chen,, J. A. Leary, and, C. R. Bertozzi. 2005a. Investigation of the iron-sulfur cluster in Mycobacterium tuberculosis APS reductase: implications for substrate binding and catalysis. Biochemistry 44: 14647– 14657.

7. Carroll, K. S.,, H. Gao,, H. Chen,, C. D. Stout,, J. A. Leary, and, C. R. Bertozzi. 2005b. A conserved mechanism for sulfonucleotide reduction. PLoS Biol. 3: e250.

8. Carter, G.,, M. Wu,, D. C. Drummond, and, L. E. Bermudez. 2003. Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J. Med. Microbiol. 52: 747– 752.

9. Chapman, E.,, M. D. Best,, S. R. Hanson, and, C. H. Wong. 2004. Sulfotransferases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew. Chem. Int. Ed. Engl. 43: 3526– 3548.

10. Cole, S. T.,, R. Brosch,, J. Parkhill,, T. Garnier,, C. Churcher,, D. Harris,, S. V. Gordon,, K. Eiglmeier,, S. Gas,, C. E. Barry, 3rd,, 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.

11. 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.

12. 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.

13. Cronan, G. E., and, D. H. Keating. 2004. Sinorhizobium meliloti sulfotransferase that modifies lipopolysaccharide. J. Bacteriol. 186: 4168– 4176.

14. De Libero, G., and, L. Mori. 2005. Recognition of lipid antigens by T cells. Nat. Rev. Immunol. 5: 485– 496.

15. Desmarais, D.,, P. E. Jablonski,, N. S. Fedarko, and, M. F. Roberts. 1997. 2-Sulfotrehalose, a novel osmolyte in haloalkaliphilic archaea. J. Bacteriol. 179: 3146– 3153.

16. Domenech, P.,, M. B. Reed,, C. S. Dowd,, C. Manca,, G. Kaplan, and, C. E. Barry. 2004. The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis. J. Biol. Chem. 279: 21257– 21265.

17. Dubos, R. J., and, G. Middlebrook. 1948. Cytochemical reaction of virulent tubercle bacilli. Am. Rev. Tuberc. 58: 698– 699.

18. Fischer, K.,, E. Scotet,, M. Niemeyer,, H. Koebernick,, J. Zerrahn,, S. Maillet,, R. Hurwitz,, M. Kursar,, M. Bonneville,, S. H. Kaufmann, and, U. E. Schaible. 2004. Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells. Proc. Natl. Acad. Sci. USA 101: 10685– 10690.

19. Fisher, R. F., and, S. R. Long. 1992. Rhizobium-plant signal exchange. Nature 357: 655– 660.

20. Fray, G. I., and, N. Polgar. 1956. Synthesis of (+)-2(L)-4(L)-dimethyldocosanoic acid, an oxidation product of mycolipenic acid. Chem. Ind. 22– 23.

21. Gangadharam, P. R.,, M. L. Cohn, and, G. Middlebrook. 1963. Infectivity, pathogenicity and sulpholipid fraction of some Indian and British strains of tubercle bacilli. Tubercle 44: 452– 455.

22. Gilleron, M.,, S. Stenger,, Z. Mazorra,, F. Wittke,, S. Mariotti,, G. Bohmer,, J. Prandi,, L. Mori,, G. Puzo, and, G. De Libero. 2004. Diacylated sulfoglycolipids are novel mycobacterial antigens stimulating CD1-restricted T cells during infection with Mycobacterium tuberculosis. J. Exp. Med. 199: 649– 659.

23. Glickman, M. S.,, J. S. Cox, and, W. R. Jacobs. 2000. A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol. Cell 5: 717– 727.

24. Goren, M. B. 1970a. Sulfolipid-I of Mycobacterium tuberculosis, strain H37Rv.1. Purification and properties. Biochim. Biophys. Acta 210: 116– 126.

25. Goren, M. B. 1970b. Sulfolipid-I of Mycobacterium tuberculosis, strain H37Rv.2. Structural studies. Biochim. Biophys. Acta 210: 127– 138.

26. Goren, M. B. 1977. Phagocyte lysosomes: interactions with infectious agents, phagosomes, and experimental perturbations in function. Annu. Rev. Microbiol. 31: 507– 533.

27. Goren, M. B.,, O. Brokl, and, B. C. Das. 1976a. Sulfatides of Mycobacterium tuberculosis: the structure of the principal sulfatide (SL-I). Biochemistry 15: 2728– 2735.

28. Goren, M. B.,, O. Brokl,, B. C. Das, and, E. Lederer. 1971. Sulfolipid-I of Mycobacterium tuberculosis, Strain-H37Rv— nature of acyl substituents. Biochemistry 10: 72– 81.

29. Goren, M. B.,, O. Brokl, and, W. B. Schaeffe. 1974. Lipids of putative relevance to virulence in Mycobacterium tuberculosis: correlation of virulence with elaboration of sulfatides and strongly acidic lipids. Infect. Immun. 9: 142– 149.

30. Goren, M. B.,, P. D’Arcy Hart,, M. R. Young, and, J. A. Armstrong. 1976b. Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 73: 2510– 2514.

31. Goren, M. B.,, J. M. Grange,, V. R. Aber,, B. W. Allen, and, D. A. Mitchison. 1982. Role of lipid content and hydrogen peroxide susceptibility in determining the guinea-pig virulence of Mycobacterium tuberculosis. Br. J. Exp. Pathol. 63: 693– 700.

32. Goren, M. B.,, A. E. Vatter, and, J. Fiscus. 1987a. Polyanionic agents as inhibitors of phagosome-lysosome fusion in cultured macrophages: evolution of an alternative interpretation. J. Leukoc. Biol. 41: 111– 121.

33. Goren, M. B.,, A. E. Vatter, and, J. Fiscus. 1987b. Polyanionic agents do not inhibit phagosome-lysosome fusion in cultured macrophages. J. Leukoc. Biol. 41: 122– 129.

34. 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.

35. Kato, M., and, M. B. Goren. 1974. Enhancement of cord factortoxicity by sulfolipid. Jpn. J. Med. Sci. Biol. 27: 120– 124.

36. 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.

37. Kolattukudy, P. E.,, N. D. Fernandes,, A. K. Azad,, A. M. Fitzmaurice, and, T. D. Sirakova. 1997. Biochemistry and molecular genetics of cell-wall lipid biosynthesis in mycobacteria. Mol. Microbiol. 24: 263– 270.

38. Kumar, P.,, M. W. Schelle,, M. Jain,, F. L. Lin,, C. J. Petzold,, M. D. Leavell,, J. A. Leary,, J. S. Cox, and, C. R. Bertozzi. 2007. PapA1 and PapA2 are acyltransferases essential for the biosynthesis of the Mycobacterium tuberculosis virulence factor sulfolipid-1. Proc. Natl. Acad. Sci. USA 104: 11221– 11226.

39. 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.

40. Mathur, M., and, P. E. Kolattukudy. 1992. Molecular cloning and sequencing of the gene for mycocerosic acid synthase, a novel fatty acid elongating multifunctional enzyme, from Mycobacterium tuberculosis var. bovis Bacillus Calmette-Guerin. J. Biol. Chem. 267: 19388– 19395.

41. Middlebrook, G.,, C. M. Coleman, and, W. B. Schaefer. 1959. Sulfolipid from virulent tubercle bacilli. Proc. Natl. Acad. Sci. USA 45: 1801– 1804.

42. Minnikin, D. E.,, L. Kremer,, L. G. Dover, and, G. S. Besra. 2002. The methyl-branched fortifications of Mycobacterium tuberculosis. Chem. Biol. 9: 545– 553.

43. Moody, D. B.,, D. M. Zajonc, and, I. A. Wilson. 2005. Anatomy of CD1-lipid antigen complexes. Nat. Rev. Immunol. 5: 387– 399.

44. Mougous, J. D.,, R. E. Green,, S. J. Williams,, S. E. Brenner, and, C. R. Bertozzi. 2002a. Sulfotransferases and sulfatases in mycobacteria. Chem. Biol. 9: 767– 776.

45. Mougous, J. D.,, M. D. Leavell,, R. H. Senaratne,, C. D. Leigh,, S. J. Williams,, L. W. Riley,, J. A. Leary, and, C. R. Bertozzi. 2002b. Discovery of sulfated metabolites in mycobacteria with a genetic and mass spectrometric approach. Proc. Natl. Acad. Sci. USA 99: 17037– 17042.

46. Mougous, J. D.,, D. H. Lee,, S. C. Hubbard,, M. W. Schelle,, D. J. Vocadlo,, J. M. Berger, and, C. R. Bertozzi. 2006a. Molecular basis for G protein control of the prokaryotic ATP sulfurylase. Mol. Cell 21: 109– 122.

47. Mougous, J. D.,, C. J. Petzold,, R. H. Senaratne,, D. H. Lee,, D. L. Akey,, F. L. Lin,, S. E. Munchel,, M. R. Pratt,, L. W. Riley,, J. A. Leary,, J. M. Berger, and, C. R. Bertozzi. 2004. Identification, function and structure of the mycobacterial sulfotransferase that initiates sulfolipid-1 biosynthesis. Nat. Struct. Mol. Biol. 11: 721– 729.

48. Mougous, J. D.,, R. H. Senaratne,, C. J. Petzold,, M. Jain,, D. H. Lee,, M. W. Schelle,, M. D. Leavell,, J. S. Cox,, J. A. Leary,, L. W. Riley, and, C. R. Bertozzi. 2006b. A sulfated metabolite produced by stf3 negatively regulates the virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 103: 4258– 4263.

49. Noll, H.,, H. Bloch,, J. Asselineau, and, E. Lederer. 1956. The chemical structure of the cord factor of Mycobacterium tuberculosis. Biochim. Biophys. Acta 20: 299– 309.

50. Okamoto, Y.,, Y. Fujita,, T. Naka,, M. Hirai,, I. Tomiyasu, and, I. Yano. 2006. Mycobacterial sulfolipid shows a virulence by inhibiting cord factor induced granuloma formation and TNF-alpha release. Microb. Pathog. 40: 245– 253.

51. 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.

52. Otero, J.,, W. R. Jacobs, Jr., and, M. S. Glickman. 2003. Efficient allelic exchange and transposon mutagenesis in Mycobacterium avium by specialized transduction. Appl. Environ. Microbiol. 69: 5039– 5044.

53. Pabst, M. J.,, J. M. Gross,, J. P. Brozna, and, M. B. Goren. 1988. Inhibition of macrophage priming by sulfatide from Mycobacterium tuberculosis. J. Immunol. 140: 634– 640.

54. Pinto, R.,, Q. X. Tang,, W. J. Britton,, T. S. Leyh, and, J. A. Triccas. 2004. The Mycobacterium tuberculosis cysD and cysNC genes form a stress-induced operon that encodes a tri-functional sulfate-activating complex. Microbiology 150: 1681– 1686.

55. Rivera-Marrero, C. A.,, J. D. Ritzenthaler,, S. A. Newburn,, J. Roman, and, R. D. Cummings. 2002. Molecular cloning and expression of a novel glycolipid sulfotransferase in Mycobacterium tuberculosis. Microbiology 148: 783– 792.

56. Rousseau, C.,, O. C. Turner,, E. Rush,, Y. Bordat,, T. D. Sirakova,, P. E. Kolattukudy,, S. Ritter,, I. M. Orme,, B. Gicquel, and, M. Jackson. 2003. Sulfolipid deficiency does not affect the virulence of Mycobacterium tuberculosis H37Rv in mice and guinea pigs. Infect. Immun. 71: 4684– 4690.

57. Schelle, M. W., and, C. R. Bertozzi. 2006. Sulfate metabolism in mycobacteria. Chembiochem 7: 1516– 1524.

58. Shen, Y.,, P. Sharma,, F. G. da Silva, and, P. Ronald. 2002. The Xanthomonas oryzae pv. lozengeoryzae raxP and raxQ genes encode an ATP sulphurylase and adenosine-5′-phosphosulphate kinase that are required for AvrXa21 avirulence activity. Mol. Microbiol. 44: 37– 48.

59. Sieling, P. A.,, D. Chatterjee,, S. A. Porcelli,, T. I. Prigozy,, R. J. Mazzaccaro,, T. Soriano,, B. R. Bloom,, M. B. Brenner,, M. Kronenberg,, P. J. Brennan, et al. 1995. CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 269: 227– 230.

60. Sirakova, T. D.,, A. K. Thirumala,, V. S. Dubey,, H. Sprecher, and, P. E. Kolattukudy. 2001. The Mycobacterium tuberculosis pks2 gene encodes the synthase for the hepta- and octamethylbranched fatty acids required for sulfolipid synthesis. J. Biol. Chem. 276: 16833– 16839.

61. 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.

62. Stallberg-Stenhagen, S. 1954. Optically active higher aliphatic compounds. 12. Trans-2,5D-dimethyl-delta-2-3-heneicosenoic acid and trans-2,4d-dimethyl-delta-2-3-heneicosenoic acid. Ark. Kemi 6: 537– 559.

63. Sun, M.,, J. L. Andreassi II,, S. Liu,, R. Pinto,, J. A. Triccas, and, T. S. Leyh. 2005. The trifunctional sulfate-activating complex (SAC) of Mycobacterium tuberculosis. J. Biol. Chem. 280: 7861– 7866.

64. Sun, M., and, T. S. Leyh. 2006. Channeling in sulfate activating complexes. Biochemistry 45: 11304– 11311.

65. Trivedi, O. A.,, P. Arora,, A. Vats,, M. Z. Ansari,, R. Tickoo,, V. Sridharan,, D. Mohanty, and, R. S. Gokhale. 2005. Dissecting the mechanism and assembly of a complex virulence mycobacterial lipid. Mol. Cell 17: 631– 643.

66. Williams, S. J.,, R. H. Senaratne,, J. D. Mougous,, L. W. Riley, and, C. R. Bertozzi. 2002. 5′-Adenosinephosphosulfate lies at a metabolic branch point in mycobacteria. J. Biol. Chem. 277: 32606– 32615.

67. Wolf, A.,, R. Kramer, and, S. Morbach. 2003. Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress. Mol. Microbiol. 49: 1119– 1134.

68. Woodruff, P. J.,, B. L. Carlson,, B. Siridechadilok,, M. R. Pratt,, R. H. Senaratne,, J. D. Mougous,, L. W. Riley,, S. J. Williams, and, C. R. Bertozzi. 2004. Trehalose is required for growth of Mycobacterium smegmatis. J. Biol. Chem. 279: 28835– 28843.

69. Wu, C. W.,, J. Glasner,, M. Collins,, S. Naser, and, A. M. Talaat. 2006. Whole-genome plasticity among Mycobacterium avium subspecies: insights from comparative genomic hybridizations. J. Bacteriol. 188: 711– 723.

70. Yamazaki, Y.,, L. Danelishvili,, M. Wu,, E. Hidaka,, T. Katsuyama,, B. Stang,, M. Petrofsky,, R. Bildfell, and, L. E. Bermudez. 2006. The ability to form biofilm influences Mycobacterium avium invasion and translocation of bronchial epithelial cells. Cell. Microbiol. 8: 806– 814.

71. Yarkoni, E.,, M. B. Goren, and, H. J. Rapp. 1979. Effect of sulfolipid I on trehalose-6,6′-dimycolate (cord factor) toxicity and antitumor activity. Infect. Immun. 24: 586– 588.

72. Zhang, L.,, D. English, and, B. R. Andersen. 1991. Activation of human neutrophils by Mycobacterium tuberculosis-derived sulfolipid-1. J. Immunol. 146: 2730– 2736.

73. Zhang, L.,, J. C. Gay,, D. English, and, B. R. Andersen. 1994. Neutrophil priming mechanisms of sulfolipid-I and N-formyl-methionyl-leucyl-phenylalanine. J. Biomed. Sci. 1: 253– 262.

74. Zhang, L.,, M. B. Goren,, T. J. Holzer, and, B. R. Andersen. 1988. Effect of Mycobacterium tuberculosis-derived sulfolipid I on human phagocytic cells. Infect. Immun. 56: 2876– 2883.

Tables

18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

/content/10.1128/9781555815783.ch18.ch18tab01

Table 1.

Metabolite profiles and phenotypes of SL-1 mutants

Table 1.

Metabolite profiles and phenotypes of SL-1 mutants