Mycobacterium bovis lipids: Virulence and vaccines

Veterinary Microbiology

Volumn 151, Issue 1-2, 2011, Pages 91-98

  Hotter, Grant S ^a   Collins, Desmond M ^b  

^a AGRESEARCH GRASSLANDS   (New Zealand)

^b AGRESEARCH   (New Zealand)

Author keywords

Lipopeptide; Mycobacterium; PDIM; PGL; Vaccines; Virulence

Indexed keywords

MYCOBACTERIUM VACCINE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; HUMAN; INFECTION PREVENTION; LIPOGENESIS; MYCOBACTERIOSIS; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; VACCINATION;

ANIMALS; ANTIGENS, BACTERIAL; HUMANS; LIPIDS; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS; TUBERCULOSIS VACCINES; VIRULENCE; VIRULENCE FACTORS;

ANIMALIA; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS COMPLEX;

EID: 79957486486     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2011.02.030     Document Type: Article

References (64)

1. Arora P., Goyal A., Natarajan V.T., Rajakumara E., Verma P., Gupta R., Yousuf M., Trivedi O.A., Mohanty D., Tyagi A., Sankaranarayanan R., Gokhale R.S. Mechanistic and functional insights into fatty acid activation in Mycobacterium tuberculosis. Nat. Chem. Biol. 2009, 5:166-173.
2. Astarie-Dequeker C., Le Guyader L., Malaga W., Seaphanh F.-K., Chalut C., Lopez A., Guilhot C. Phthiocerol dimycocerosates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog. 2009, 5:e1000289.
3. Azad A.K., Sirakova T.D., Fernandes N.D., Kolattukudy P.E. Gene knockout reveals a novel gene cluster for the synthesis of a class of cell wall lipids unique to pathogenic mycobacteria. J. Biol. Chem. 1997, 272:16741-16745.
4. Azad A.K., Sirakova T.D., Rogers L.M., Kolattukudy P.E. Targeted replacement of the mycocerosic acid synthase gene in Mycobacterium bovis BCG produces a mutant that lacks mycosides. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:4787-4792.
5. Bhatnagar S., Schorey J.S. Elevated mitogen-activated protein kinase signalling and increased macrophage activation in cells infected with a glycopeptidolipid-deficient Mycobacterium avium. Cell. Microbiol. 2006, 8:85-96.
6. Biet F., Bay S., Thibault V.C., Euphrasie D., Grayon M., Ganneau C., Lanotte P., Daffeó M., Gokhale R., Etienne G., Reyrat J.-M. Lipopentapeptide induces a strong host humoral response and distinguishes Mycobacterium avium subsp. paratuberculosis from M. avium subsp. avium. Vaccine 2008, 26:257-268.
7. Billman-Jacobe H., McConville M.J., Haites R.E., Kovacevic S., Coppel R.L. Identification of a peptide synthetase involved in the biosynthesis of glycopeptidolipids of Mycobacterium smegmatis. Mol. Microbiol. 1999, 33:1244-1253.
8. Brosch R., Gordon S.V., Garnier T., Eiglmeier K., Frigui W., Valenti P., Dos Santos S., Duthoy S., Lacroix C., Garcia-Pelayo C., Inwald J.K., Golby P., Garcia J.N., Hewinson R.G., Behr M.A., Quail M.A., Churcher C., Barrell B.G., Parkhill J., Cole S.T. Genome plasticity of BCG and impact on vaccine efficacy. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5596-5601.
9. Camacho L.R., Ensergueix D., Perez E., Gicquel B., Guilhot C. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol. Microbiol. 1999, 34:257-267.
10. Camacho L.R., Constant P., Raynaud C., Lanéelle M.-A., Triccas J.A., Gicquel B., Daffé M., Guilhot C. Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J. Biol. Chem. 2001, 276:19845-19854.
11. Chen J.M., Islam S.T., Ren H., Liu J. Differential productions of lipid virulence factors among BCG vaccine strains and implications on BCG safety. Vaccine 2007, 25:8114-8122.
12. Chopra T., Gokhale R.S. Polyketide versatility in the biosynthesis of complex mycobacterial cell wall lipids. Methods Enzymol. 2009, 459:259-294.
13. Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S.V., Eiglmeier K., Gas S., Barry C.E., Tekaia F., Badcock K., Basham D., Brown D., Chillingworth T., Connor R., Davies R., Devlin K., Feltwell T., Gentles S., Hamlin N., Holroyd S., Hornsby T., Jagels K., Krogh A., McLean J., Moule S., Murphy L., Oliver K., Osborne J., Quail M.A., Rajandream M.-A., Rogers J., Rutter S., Seeger K., Skelton J., Squares R., Squares S., Sulston J.E., Taylor K., Whitehead S., Barrell B.G. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393:537-544.
14. Collins D.M., de Lisle G.W., Aldwell F.E., Buddle B.M. A new attenuated Mycobacterium bovis vaccine protects brushtail possums (Trichosurus vulpecula) against experimental tuberculosis infection. Vaccine 2007, 25:4659-4664.
15. Constant P., Perez E., Malaga W., Laneelle M.-A., Saurel O., Daffe M., Guilhot C. Role of the pks15/1 gene in the biosynthesis of phenolglycolipids in the Mycobacterium tuberculosis complex. Evidence that all strains synthesize glycosylated p-hydroxybenzoic methyl esters and that strains devoid of phenolglycolipids harbor a frameshift mutation in the pks15/1 gene. J. Biol. Chem. 2002, 277:38148-38158.
16. Cox J.S., Chen B., McNeil M., Jacobs W.R. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 1999, 402:79-83.
17. Deshayes C., Kocincova D., Etienne G., Reyrat J.-M. Glycopeptidolipids: a complex pathway for small pleiotropic molecules. The Mycobacterial Cell Envelope 2008, 345-366. ASM Press, Washington DC. M. Daffe, J.-M. Reyrat (Eds.).
18. Domenech P., Reed M.B. Rapid and spontaneous loss of phthiocerol dimycocerosate (PDIM) from Mycobacterium tuberculosis grown in vitro: implications for virulence studies. Microbiol. 2009, 155:3532-3543.
19. Eckstein T.M., Chandrasekaran S., Mahapatra S., McNeil M.R., Chatterjee D., Rithner C.D., Ryan P.W., Belisle J.T., Inamine J.M. A major cell wall lipopeptide of Mycobacterium avium subspecies paratuberculosis. J. Biol. Chem. 2006, 281:5209-5215.
20. Ferreras J.A., Stirrett K.L., Lu X., Ryu J.-S., Soll C., Tan D.S., Quadri L.E.N. Mycobacterial phenolic glycolipid virulence factor biosynthesis: mechanism and small-molecule inhibition of polyketide chain initiation. Chem. Biol. 2008, 15:51-61.
21. Frigui W., Bottai D., Majlessi L., Monot M., Josselin E., Brodin P., Garnier T., Gicquel B., Martin C., Leclerc C., Cole S.T., Brosch R. Control of M. tuberculosis ESAT-6 secretion and specific T cell recognition by PhoP. PLoS Pathog. 2008, 4:e33.
22. Garcia Pelayo M.C., Uplekar S., Keniry A., Mendoza Lopez P., Garnier T., Nunez Garcia J., Boschiroli L., Zhou X., Parkhill J., Smith N., Hewinson R.G., Cole S.T., Gordon S.V. A comprehensive survey of single nucleotide polymorphisms (SNPs) across Mycobacterium bovis strains and M. bovis BCG vaccine strains refines the genealogy and defines a minimal set of SNPs that separate virulent M. bovis strains and M. bovis BCG strains. Infect. Immun. 2009, 77:2230-2238.
23. Garnier T., Eiglmeier K., Camus J.-C., Medina N., Mansoor H., Pryor M., Duthoy S., Grondin S., Lacroix C., Monsempe C., Simon S., Harris B., Atkin R., Doggett J., Mayes R., Keating L., Wheeler P.R., Parkhill J., Barrell B.G., Cole S.T., Gordon S.V., Hewinson R.G. The complete genome sequence of Mycobacterium bovis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:7877-7882.
24. Gokhale R.S., Sankaranarayanan R., Mohanty D. Versatility of polyketide synthases in generating metabolic diversity. Curr. Opin. Struct. Biol. 2007, 17:736-743.
25. Gokhale R.S., Saxena P., Chopra T., Mohanty D. Versatile polyketide enzymatic machinery for the biosynthesis of complex mycobacterial lipids. Nat. Prod. Rep. 2007, 24:267-277.
26. Guenin-Mace L., Simeone R., Demangel C. Lipids of pathogenic mycobacteria: contributions to virulence and host immune suppression. Transbound. Emerg. Dis. 2009, 56:255-268.
27. Guilhot C., Chalut C., Daffe M. Biosynthesis and roles of phenolic glycolipids and related molecules in Mycobacterium tuberculosis. The Mycobacterial Cell Envelope 2008, 273-289. ASM Press, Washington DC. M. Daffe, J.-M. Reyrat (Eds.).
28. Hotter G.S., Wards B.J., Mouat P., Besra G.S., Gomes J., Singh M., Bassett S., Kawakami P., Wheeler P.R., de Lisle G.W., Collins D.M. Transposon mutagenesis of Mb0100 at the PPE1-Nrp locus in Mycobacterium bovis disrupts phthiocerol dimycocerosate (PDIM) and glycosylphenol-PDIM biosynthesis, producing an avirulent strain with vaccine properties at least equal to those of M. bovis BCG. J. Bacteriol. 2005, 187:2267-2277.
29. Infante E., Aguilar L.D., Gicquel B., Pando R.H. Immunogenicity and protective efficacy of the Mycobacterium tuberculosis fadD26 mutant. Clin. Exp. Immunol. 2005, 141:21-28.
30. Jackson M., Stadthagen G., Gicquel B. Long-chain multiple methyl-branched fatty acid-containing lipids of Mycobacterium tuberculosis: biosynthesis, transport, regulation and biological activities. Tuberculosis 2007, 87:78-86.
31. Kano H., Doi T., Fujita Y., Takimoto H., Yano I., Kumazawa Y. Serotype-specific modulation of human monocyte functions by glycopeptidolipid (GPL) isolated from Mycobacterium avium complex. Biol. Pharm. Bull. 2005, 28:335-339.
32. Krzywinska E., Bhatnagar S., Sweet L., Chatterjee D., Schorey J.S. Mycobacterium avium 104 depleted of the methyltransferase D gene by allelic replacement lacks serotype-specific glycopeptidolipids and shows attenuated virulence in mice. Mol. Microbiol. 2005, 56:1262-1273.
33. Krithika R., Marathe U., Saxena P., Ansari M.Z., Mohanty D., Gokhale R.S. A genetic locus required for iron acquisition in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2069-2074.
34. Leger M., Gavalda S., Guillet V., van der Rest B., Slama N., Montrozier H., Mourey L., Quemard A., Daffe M., Marrakchi H. The dual function of the Mycobacterium tuberculosis FadD32 required for mycolic acid biosynthesis. Chem. Biol. 2009, 16:510-519.
35. Leung A.S., Tran V., Wu Z., Yu X., Alexander D.C., Gao G.F., Zhu B., Liu J. Novel genome polymorphisms in BCG vaccine strains and impact on efficacy. BMC Genomics 2008, 9:413. 10.1186/1471-2164-9-413.
36. Miao V., Coeffet-LeGal M.-F., Brian P., Brost R., Penn J., Whiting A., Martin S., Ford R., Parr I., Bouchard M., Silva C.J., Wrigley S.K., Baltz R.H. Daptomycin biosynthesis in Streptomyces roseosporus: cloning and analysis of the gene cluster and revision of peptide stereochemistry. Microbiology 2005, 151:1507-1523.
37. Minnikin D.E., Kremer L., Dover L.G., Besra G.S. The methyl-branched fortifications of Mycobacterium tuberculosis. Chem. Biol. 2002, 9:545-553.
38. Moody D.B., Young D.C., Cheng T.-Y., Rosatm J.-P., Roura-Mir C., O'Connor P.B., Zajonc D.M., Walz A., Miller M.J., Levery S.B., Wilson I.A., Costello C.E., Brenner M.B. T cell activation by lipopeptide antigens. Science 2004, 303:527-531.
39. Moody D.B., Zajonc D.M., Wilson I.A. Anatomy of CD1-lipid antigen complexes. Nat. Rev. Immunol. 2005, 5:387-399.
40. Natarajan V.T., Mohanty D., Gokhale R.S. Biosynthesis of mycobacterial lipids by multifunctional polyketide synthases. The Mycobacterial Cell Envelope 2008, 235-248. ASM Press, Washington DC. M. Daffe, J.-M. Reyrat (Eds.).
41. Onwueme K.C., Ferreras J.A., Buglino J., Lima C.D., Quadri L.E.N. Mycobacterial polyketide-associated proteins are acyltransferases: proof of principle with Mycobacterium tuberculosis PapA5. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:4608-4613.
42. Onwueme K.C., Vos C.J., Zurita J., Ferreras J.A., Quadri L.E.N. The dimycocerosate ester polyketide virulence factors of mycobacteria. Prog. Lipid Res. 2005, 44:259-302.
43. Onwueme K.C., Vos C.J., Zurita J., Soll C.E., Quadri L.E.N. Identification of phthiodiolone ketoreductase, and enzyme required for production of mycobacterial diacyl phthiocerol virulence factors. J. Bacteriol. 2005, 187:4760-4766.
44. Perez E., Constant P., Lemassu A., Laval F., Daffe M., Guilhot C. Characterization of three glycosyltransferases involved in the biosynthesis of the phenolic glycolipid antigens from the Mycobacterium tuberculosis complex. J. Biol. Chem. 2004, 279:42574-42583.
45. Perez E., Constant P., Laval F., Lemassu A., Laneelle M.-A., Daffe M., Guilhot C. Molecular dissection of the role of two methyltransferases in the biosynthesis of phenolglycolipids and phthiocerol dimycoserosate in the Mycobacterium tuberculosis complex. J. Biol. Chem. 2004, 279:42584-42592.
46. Pethe K., Swenson D.L., Alonso S., Anderson J., Wang C., Russell D.G. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13642-13647.
47. Pinto R., Saunders B.M., Camacho L.R., Britton W.J., Gicquel B., Triccas J.A. Mycobacterium tuberculosis defective in phthiocerol dimycocerosate translocation provides greater protective immunity against tuberculosis than the existing Bacille Calmette-Guerin vaccine. J. Infect. Dis. 2004, 189:105-112.
48. Quadri L.E.N., Sello J., Keating T.A., Weinreb P.H., Walsh C.T. Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin. Chem. Biol. 1998, 5:631-645.
49. Reed M.B., Domenech P., Manca C., Su H., Barczak A.K., Kreiswirth B.N., Kaplan G., Barry C.E. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 2004, 431:84-87.
50. Reed M.B., Gagneux S., DeRiemer K., Small P.M., Barry C.E. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively unregulated. J. Bacteriol. 2007, 189:2583-2589.
51. Rousseau C., Winter N., Pivert E., Bordat Y., Neyrolles O., Ave P., Huerre M., Gicquel B., Jackson M. Production of phthiocerol dimycocerosates protects Mycobacterium tuberculosis from the cidal activity of reactive nitrogen intermediates produced by macrophages and modulates the early immune response to infection. Cell. Microbiol. 2004, 6:277-287.
52. Sassetti C.M., Boyd D.H., Rubin E.J. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 2003, 48:77-84.
53. Sassetti C.M., Rubin E.J. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:12989-12994.
54. Schorey J.S., Sweet L. The mycobacterial glycopeptidolipids: structure, function, and their role in pathogenesis. Glycobiology 2008, 18:832-841.
55. Seki M., Honda I., Fujita I., Yano I., Yamamoto S., Koyama A. Whole genome sequence analysis of Mycobacterium bovis bacillus Calmette-Guérin (BCG) Tokyo 172: a comparative study of BCG vaccine substrains. Vaccine 2009, 27:1710-1716.
56. Simeone R., Constant P., Malaga W., Guilhot C., Daffe M., Chalut C. Molecular dissection of the biosynthetic relationship between phthiocerol and phthiodiolone dimycocerosates and their critical role in the virulence and permeability of Mycobacterium tuberculosis. FEBS J. 2007, 274:1957-1969.
57. Sinsimer D., Huet G., Manca C., Tsenova L., Koo M.-S., Kurepina N., Kana B., Mathema B., Marras S.A.E., Krieswirth B.N., Guilhot C., Kaplan G. The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect. Immun. 2008, 76:3027-3036.
58. Trivedi O.A., Arora P., Sridharan V., Tickoo R., Mohanty D., Gokhale R.S. Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 2004, 428:441-445.
59. Trivedi O.A., Arora P., Vats A., Ansari M.Z., Tickoo R., Sridharan V., Mohanty D., Gokhale R.S. Dissecting the mechanism and assembly of a complex virulence mycobacterial lipid. Mol. Cell 2005, 17:631-643.
60. Tsenova L., Ellison E., Harbacheuski R., Moreira A.L., Kurepina N., Reed M.B., Mathema B., Barry C.E., Kaplan G. Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J. Infect. Dis. 2005, 192:98-106.
61. Villeneuve C., Etienne G., Abadie V., Montrozier H., Bordier C., Laval F., Daffe M., Maridonneau-Parini I., Astarie-Dequeker C. 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. 2003, 278:51291-51300.
62. Wang F., Langley R., Gulten G., Wang L., Sacchettini J.C. Identification of a type III thioesterase reveals the function of an operon critical for Mtb virulence. Chem. Biol. 2007, 14:543-551.
63. Willcox B.E., Willcox C.R., Dover L.G., Besra G. Structures and functions of microbial lipid antigens presented by CD1. Curr. Top. Microbiol. Immunol. 2007, 314:73-110.
64. Zheng H., Lu L., Wang B., Pu S., Zhang X., Zhu G., Shi W., Lu Z., Wang H., Wang S., Zhao G., Zhang Y. Genetic basis of virulence attenuation revealed by comparative genomic analysis of Mycobacterium tuberculosis strain H37Ra versus H37Rv. PLoS ONE 2008, 3:e2375.