Genetics of mycobacterial arabinogalactan and lipoarabinomannan assembly

Microbiology Spectrum

Volumn 2, Issue 4, 2014, Pages

  Jankute, Monika ^a   Grover, Shipra ^a   Birch, Helen L ^a   Besra, Gurdyal S ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOGALACTAN; GALACTAN; LIPOARABINOMANNAN; LIPOPOLYSACCHARIDE; TUBERCULOSTATIC AGENT;

BACTERIAL GENOME; BIOSYNTHESIS; DRUG EFFECTS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR BIOLOGY; MYCOBACTERIUM; PROCEDURES;

ANTITUBERCULAR AGENTS; BIOSYNTHETIC PATHWAYS; GALACTANS; GENOME, BACTERIAL; LIPOPOLYSACCHARIDES; MOLECULAR BIOLOGY; MYCOBACTERIUM;

EID: 84958811782     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.MGM2-0013-2013     Document Type: Article

References (157)

1. Jankute M, Grover S, Rana AK, Besra GS. 2012. Arabinogalactan and lipoarabinomannan biosynthesis: structure, biogenesis and their potential as drug targets. Future Microbiol 7:129-147.
2. Mishra AK, Driessen NN, Appelmelk BJ, Besra GS. 2011. Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction. FEMS Microbiol Rev 35:1126-1157.
3. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, 3rd, 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 MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
4. Stinear TP, Seemann T, Harrison PF, Jenkin GA, Davies JK, Johnson PD, Abdellah Z, Arrowsmith C, Chillingworth T, Churcher C, Clarke K, Cronin A, Davis P, Goodhead I, Holroyd N, Jagels K, Lord A, Moule S, Mungall K, Norbertczak H, Quail MA, Rabbinowitsch E, Walker D, White B, Whitehead S, Small PL, Brosch R, Ramakrishnan L, Fischbach MA, Parkhill J, Cole ST. 2008. Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 18:729-741.
5. Garnier T, Eiglmeier K, Camus JC, 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 PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson RG. 2003. The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci USA 100:7877-7882.
6. Bhatt A, Jacobs WR, Jr. 2009. Gene essentiality testing in Mycobacterium smegmatis using specialized transduction. Methods Mol Biol 465:325-336.
7. Amar C, Vilkas E. 1973. Isolation of arabinose phosphate from the walls of Mycobacterium tuberculosis H37Ra. CR Acad Sci Hebd Seances Acad Sci D 277:1949-1951.
8. McNeil M, Wallner SJ, Hunter SW, Brennan PJ. 1987. Demonstration that the galactosyl and arabinosyl residues in the cell-wall arabinogalactan of Mycobacterium leprae and Mycobacterium tuberculosis are furanoid. Carbohydr Res 166:299-308.
9. Besra GS, Khoo KH, McNeil MR, Dell A, Morris HR, Brennan PJ. 1995. A new interpretation of the structure of the mycolyl-arabinogalactan complex of Mycobacterium tuberculosis as revealed through characterization of oligoglycosylalditol fragments by fast-atom bombardment mass spectrometry and 1H nuclear magnetic resonance spectroscopy. Biochemistry 34:4257-4266.
10. Daffe M, Brennan PJ, McNeil M. 1990. Predominant structural features of the cell wall arabinogalactan of Mycobacterium tuberculosis as revealed through characterization of oligoglycosyl alditol fragments by gas chromatography/mass spectrometry and by 1H and 13C NMR analyses. J Biol Chem. 265:6734-6743.
11. McNeil M, Daffe M, Brennan PJ. 1990. Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J Biol Chem 265:18200-18206.
12. McNeil M, Daffe M, Brennan PJ. 1991. Location of the mycolyl ester substituents in the cell walls of mycobacteria. J Biol Chem 266:13217-13223.
13. Alderwick LJ, Radmacher E, Seidel M, Gande R, Hitchen PG, Morris HR, Dell A, Sahm H, Eggeling L, Besra GS. 2005. Deletion of Cg-emb in Corynebacterianeae leads to a novel truncated cell wall arabinogalactan, whereas inactivation of Cg-ubiA results in an arabinan-deficient mutant with a cell wall galactan core. J Biol Chem 280:32362-32371.
14. McNeil MR, Robuck KG, Harter M, Brennan PJ. 1994. Enzymatic evidence for the presence of a critical terminal hexa-arabinoside in the cell walls of Mycobacterium tuberculosis. Glycobiology 4:165-173.
15. Dong X, Bhamidi S, Scherman M, Xin Y, McNeil MR. 2006. Development of a quantitative assay for mycobacterial endogenous arabinase and ensuing studies of arabinase levels and arabinan metabolism in Mycobacterium smegmatis. Appl Environ Microbiol 72:2601-2605.
16. Draper P, Khoo KH, Chatterjee D, Dell A, Morris HR. 1997. Galactosamine in walls of slow-growing mycobacteria. Biochem J. 327:519-525.
17. Lee A, Wu SW, Scherman MS, Torrelles JB, Chatterjee D, McNeil MR, Khoo KH. 2006. Sequencing of oligoarabinosyl units released from mycobacterial arabinogalactan by endogenous arabinanase: identification of distinctive and novel structural motifs. Biochemistry 45:15817-15828.
18. Peng W, Zou L, Bhamidi S, McNeil MR, Lowary TL. 2012. The galactosamine residue in mycobacterial arabinogalactan is a-linked. J Org Chem 77:9826-9832.
19. Bhamidi S, Scherman MS, Rithner CD, Prenni JE, Chatterjee D, Khoo KH, McNeil MR. 2008. The identification and location of succinyl residues and the characterization of the interior arabinan region allow for a model of the complete primary structure of Mycobacterium tuberculosis mycolyl arabinogalactan. J Biol Chem 283:12992-13000.
20. Skovierova H, Larrouy-Maumus G, Pham H, Belanova M, Barilone N, Dasgupta A, Mikusova K, Gicquel B, Gilleron M, Brennan PJ, Puzo G, Nigou J, Jackson M. 2010. Biosynthetic origin of the galactosamine substituent of arabinogalactan in Mycobacterium tuberculosis. J Biol Chem 285:41348-41355.
21. Mengin-Lecreulx D, van Heijenoort J. 1996. Characterization of the essential gene glmM encoding phosphoglucosamine mutase in Escherichia coli. J Biol Chem 271:32-39.
22. Mengin-Lecreulx D, van Heijenoort J. 1994. Copurification of glucosamine-1-phosphate acetyltransferase and N-acetylglucosamine-1-phosphate uridyltransferase activities of Escherichia coli: characterization of the glmU gene product as a bifunctional enzyme catalyzing two subsequent steps in the pathway for UDP-N-acetylglucosamine synthesis. J Bacteriol. 176:5788-5795.
23. Mengin-Lecreulx D, van Heijenoort J. 1993. Identification of the glmU gene encoding N-acetylglucosamine-1-phosphate uridyltransferase in Escherichia coli. J Bacteriol 175:6150-6157.
24. Klein DJ, Ferre-D'Amare AR. 2006. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313:1752-1756.
25. Zhang W, Jones VC, Scherman MS, Mahapatra S, Crick D, Bhamidi S, Xin Y, McNeil MR, Ma Y. 2008. Expression, essentiality, and a microtiter plate assay for mycobacterial GlmU, the bifunctional glucosamine-1-phosphate acetyltransferase and N-acetylglucosamine-1-phosphate uridyltransferase. Int J Biochem Cell Biol 40:2560-2571.
26. Li S, Kang J, Yu W, Zhou Y, Zhang W, Xin Y, Ma Y. 2012. Identification of M. tuberculosis Rv3441c and M. smegmatis MSMEG_1556 and essentiality of M. smegmatis MSMEG_1556. PLoS One 7:e42769.
27. Zhang Z, Bulloch EM, Bunker RD, Baker EN, Squire CJ. 2009. Structure and function of GlmU from Mycobacterium tuberculosis. Acta Crystallogr D Biol Crystallogr 65:275-283.
28. Zhou Y, Xin Y, Sha S, Ma Y. 2011. Kinetic properties of Mycobacterium tuberculosis bifunctional GlmU. Arch Microbiol 193:751-757.
29. Zhou Y, Yu W, Zheng Q, Xin Y, Ma Y. 2012. Identification of amino acids involved in catalytic process of M. tuberculosis GlmU acetyltransferase. Glycoconj J 29:297-303.
30. Ma Y, Stern RJ, Scherman MS, Vissa VD, YanW, Jones VC, Zhang F, Franzblau SG, Lewis WH, McNeil MR. 2001. Drug targeting Mycobacterium tuberculosis cell wall synthesis: genetics of dTDP-rhamnose synthetic enzymes and development of a microtiter plate-based screen for inhibitors of conversion of dTDP-glucose to dTDP-rhamnose. Antimicrob Agents Chemother 45:1407-1416.
31. Kantardjieff KA, Kim CY, Naranjo C, Waldo GS, Lekin T, Segelke BW, Zemla A, Park MS, Terwilliger TC, Rupp B. 2004. Mycobacterium tuberculosis RmlC epimerase (Rv3465): a promising drug-target structure in the rhamnose pathway. Acta Crystallogr D Biol Crystallogr 60:895-902.
32. Babaoglu K, Page MA, Jones VC, McNeil MR, Dong C, Naismith JH, Lee RH. 2003. Novel inhibitors of an emerging target in Mycobacterium tuberculosis; substituted thiazolidinones as inhibitors of dTDP-rhamnose synthesis. Bioorg Med Chem Lett 13:3227-3230.
33. Ma Y, Mills JA, Belisle JT, Vissa V, Howell M, Bowlin K, Scherman MS, McNeil M. 1997. Determination of the pathway for rhamnose biosynthesis in mycobacteria: cloning, sequencing and expression of the Mycobacterium tuberculosis gene encoding a-d-glucose-1-phosphate thymidylyltransferase. Microbiology 143:937-945.
34. Qu H, Xin Y, Dong X, Ma Y. 2007. An rmlA gene encoding d-glucose-1-phosphate thymidylyltransferase is essential for mycobacterial growth. FEMS Microbiol Lett 275:237-243.
35. Li W, Xin Y, McNeil MR, Ma Y. 2006. rmlB and rmlC genes are essential for growth of mycobacteria. Biochem Biophys Res Commun 342:170-178.
36. Ma Y, Pan F, McNeil M. 2002. Formation of dTDP-rhamnose is essential for growth of mycobacteria. J Bacteriol 184:3392-3395.
37. Sha S, Zhou Y, Xin Y, Ma Y. 2012. Development of a colorimetric assay and kinetic analysis for Mycobacterium tuberculosis d-glucose-1-phosphate thymidylyltransferase. J Biomol Screen 17:252-257.
38. Lai X, Wu J, Chen S, Zhang X, Wang H. 2008. Expression, purification, and characterization of a functionally active Mycobacterium tuberculosis UDP-glucose pyrophosphorylase. Protein Expr Purif 61:50-56.
39. Lemaire HG, Muller-Hill B. 1986. Nucleotide sequences of the galE gene and the galT gene of E. coli. Nucleic Acids Res 14:7705-7711.
40. Weston A, Stern RJ, Lee RE, Nassau PM, Monsey D, Martin SL, Scherman MS, Besra GS, Duncan K, McNeil MR. 1997. Biosynthetic origin of mycobacterial cell wall galactofuranosyl residues. Tuber Lung Dis 78:123-131.
41. Nassau PM, Martin SL, Brown RE, Weston A, Monsey D, McNeil MR, Duncan K. 1996. Galactofuranose biosynthesis in Escherichia coli K-12: identification and cloning of UDP-galactopyranose mutase. J Bacteriol 178:1047-1052.
42. Pan F, Jackson M, Ma Y, McNeil M. 2001. Cell wall core galactofuran synthesis is essential for growth of mycobacteria. J Bacteriol 183:3991-3998.
43. Sanders DA, Staines AG, McMahon SA, McNeil MR, Whitfield C, Naismith JH. 2001. UDP-galactopyranose mutase has a novel structure and mechanism. Nat Struct Biol 8:858-863.
44. Beis K, Srikannathasan V, Liu H, Fullerton SW, Bamford VA, Sanders DA, Whitfield C, McNeil MR, Naismith JH. 2005. Crystal structures of Mycobacterium tuberculosis and Klebsiella pneumoniae UDP-galactopyranose mutase in the oxidised state and Klebsiella pneumoniae UDP-galactopyranose mutase in the (active) reduced state. J Mol Biol 348:971-982.
45. Wolucka BA. 2008. Biosynthesis of d-arabinose in mycobacteria: a novel bacterial pathway with implications for antimycobacterial therapy. FEBS J 275:2691-2711.
46. Alderwick LJ, Lloyd GS, Lloyd AJ, Lovering AL, Eggeling L, Besra GS. 2011. Biochemical characterization of the Mycobacterium tuberculosis phosphoribosyl-1-pyrophosphate synthetase. Glycobiology 21:410-425.
47. Tatituri RV, Alderwick LJ, Mishra AK, Nigou J, Gilleron M, Krumbach K, Hitchen P, Giordano A, Morris HR, Dell D, Eggeling L, Besra GS. 2007. Structural characterization of a partially arabinosylated lipoarabinomannan variant isolated from a Corynebacterium glutamicum ubiA mutant. Microbiology 153:2621-2629.
48. Jiang T, He L, Zhan Y, Zang S, Ma Y, Zhao X, Zhang C, Xin Y. 2011. The effect of MSMEG_6402 gene disruption on the cell wall structure of Mycobacterium smegmatis. Microb Pathog 51:156-160.
49. Mikusova K, Huang H, Yagi T, Holsters M, Vereecke D, D'Haeze W, Scherman MS, Brennan PJ, McNeil MR, Crick DC. 2005. Decaprenylphosphoryl arabinofuranose, the donor of the d-arabinofuranosyl residues of mycobacterial arabinan, is formed via a two-step epimerization of decaprenylphosphoryl ribose. J Bacteriol 187:8020-8025.
50. Meniche X, de Sousa-d'Auria C, Van-der-Rest B, Bhamidi S, Huc E, Huang H, De Paepe D, Tropis M, McNeil M, Daffe M, Houssin C. 2008. Partial redundancy in the synthesis of the d-arabinose incorporated in the cell wall arabinan of Corynebacterineae. Microbiology 154:2315-2326.
51. Crellin PK, Brammananth R, CoppelRL. 2011. Decaprenylphosphoryl-β-D-ribose 2'-epimerase, the target of benzothiazinones and dinitrobenzamides, is an essential enzyme in Mycobacterium smegmatis. PLoS One 6: e16869.
52. Christophe T, Jackson M, Jeon HK, Fenistein D, Contreras-Dominguez M, Kim J, Genovesio A, Carralot JP, Ewann F, Kim EH, Lee SY, Kang A, Seo MJ, Park EJ, Skovierova H, Pham H, Riccardi G, Nam JY, Marsollier L, Kempf M, Joly-Guillou ML, Oh T, Shin WK, No Z, Nehrbass U, Brosch R, Cole ST, Brodin P. 2009. High content screening identifies decaprenyl-phosphoribose 2' epimerase as a target for intracellular antimycobacterial inhibitors. PLoS Pathog 5:e1000645.
53. Makarov V, Manina G, Mikusova K, Mollmann U, Ryabova O, Saint-Joanis B, Dhar N, Pasca MR, Buroni S, Lucarelli AP, Milano A, De Rossi E, Belanova M, Bobovska A, Dianiskova P, Kordulakova J, Sala C, Fullam E, Schneider P, McKinney JD, Brodin P, Christophe T, Waddell S, Butcher P, Albrethsen J, Rosenkrands I, Brosch R, Nandi V, Bharath S, Gaonkar S, Shandil RK, Balasubramanian V, Balganesh T, Tyagi S, Grosset S, Riccardi G, Cole ST. 2009. Benzothiazinones kill Mycobacterium tuberculosis by blocking arabinan synthesis. Science 324:801-804.
54. Batt SM, Jabeen T, Bhowruth V, Quill L, Lund PA, Eggeling L, Alderwick LJ, Futterer K, Besra GS. 2012. Structural basis of inhibition of Mycobacterium tuberculosis DprE1 by benzothiazinone inhibitors. Proc Natl Acad Sci USA 109:11354-11359.
55. Jin Y, Xin Y, Zhang W, Ma Y. 2010. Mycobacterium tuberculosis Rv1302 and Mycobacterium smegmatis MSMEG_4947 have WecA function and MSMEG_4947 is required for the growth of M. smegmatis. FEMS Microbiol Lett 310:54-61.
56. Mikusova K, Mikus M, Besra GS, Hancock I, Brennan PJ. 1996. Biosynthesis of the linkage region of the mycobacterial cell wall. J Biol Chem 271:7820-7828.
57. Mills JA, Motichka K, Jucker M, Wu HP, Uhlik BC, Stern RJ, Scherman MS, Vissa VD, Pan F, Kundu M, Ma YF, McNeil M. 2004. Inactivation of the mycobacterial rhamnosyltransferase, which is needed for the formation of the arabinogalactan-peptidoglycan linker, leads to irreversible loss of viability. J Biol Chem 279:43540-43546.
58. Wu Q, Zhou P, Qian S, Qin X, Fan Z, Fu Q, Zhan Z, Pei H. 2011. Cloning, expression, identification and bioinformatics analysis of Rv3265c gene from Mycobacterium tuberculosis in Escherichia coli. Asian Pac J Trop Med 4:266-270.
59. Alderwick LJ, Dover LG, Veerapen N, Gurcha SS, Kremer L, Roper DL, Pathak AK, Reynolds RC, Besra GS. 2008. Expression, purification and characterisation of soluble GlfT and the identification of a novel galactofuranosyltransferase Rv3782 involved in priming GlfT-mediated galactan polymerisation in Mycobacterium tuberculosis. Protein Expr Purif 58:332-341.
60. Mikusova K, Belanova M, Kordulakova J, Honda K, McNeil MR, Mahapatra S, Crick DC, Brennan PJ. 2006. Identification of a novel galactosyl transferase involved in biosynthesis of the mycobacterial cell wall. J Bacteriol 188:6592-6598.
61. Belanova M, Dianiskova P, Brennan PJ, Completo GC, Rose NL, Lowary TL, Mikusova K. 2008. Galactosyl transferases in mycobacterial cell wall synthesis. J Bacteriol 190:1141-1145.
62. Kremer L, Dover LG, Morehouse C, Hitchin P, Everett M, Morris HR, Dell A, Brennan PJ, McNeil MR, Flaherty C, Duncan K, Besra GS. 2001. Galactan biosynthesis in Mycobacterium tuberculosis. Identification of a bifunctional UDP-galactofuranosyltransferase. J Biol Chem 276:26430-26440.
63. Rose NL, Completo GC, Lin SJ, McNeil M, Palcic MM, Lowary TL. 2006. Expression, purification, and characterization of a galactofuranosyltransferase involved in Mycobacterium tuberculosis arabinogalactan biosynthesis. J Am Chem Soc 128:6721-6729.
64. Wheatley RW, Zheng RB, Richards MR, Lowary TL, Ng KK. 2012. Tetrameric structure of the GlfT2 galactofuranosyltransferase reveals a scaffold for the assembly of mycobacterial arabinogalactan. J Biol Chem 287:28132-28143.
65. Alderwick LJ, Seidel M, Sahm H, Besra GS, Eggeling L. 2006. Identification of a novel arabinofuranosyltransferase (AftA) involved in cell wall arabinan biosynthesis in Mycobacterium tuberculosis. J Biol Chem 281:15653-15661.
66. Escuyer VE, Lety MA, Torrelles JB, Khoo KH, Tang JB, Rithner CD, Frehel C, McNeil MR, Brennan PJ, Chatterjee D. 2001. The role of the embA and embB gene products in the biosynthesis of the terminal hexaarabinofuranosyl motif of Mycobacterium smegmatis arabinogalactan. J Biol Chem 276:48854-48862.
67. Dover LG, Cerdeno-Tarraga AM, Pallen MJ, Parkhill J, Besra GS. 2004. Comparative cell wall core biosynthesis in the mycolated pathogens, Mycobacterium tuberculosis and Corynebacterium diphtheriae. FEMS Microbiol Rev 28:225-250.
68. Birch HL, Alderwick LJ, Bhatt A, Rittmann D, Krumbach K, Singh A, Bai Y, Lowary TL, Eggeling L, Besra GS. 2008. Biosynthesis of mycobacterial arabinogalactan: identification of a novel α(1→3) arabinofuranosyltransferase. Mol Microbiol 69:1191-1206.
69. Birch HL, Alderwick LJ, Appelmelk BJ, Maaskant J, Bhatt A, Singh A, Nigou J, Eggeling L, Geurtsen J, Besra GS. 2010. A truncated lipoglycan from mycobacteria with altered immunological properties. Proc Natl Acad Sci USA 107:2634-2639.
70. Skovierova H, Larrouy-Maumus G, Zhang J, Kaur D, Barilone N, Kordulakova J, Gilleron M, Guadagnini S, Belanova M, Prevost MC, Gicquel B, Puzo G, Chatterjee D, Brennan PJ, Nigou J, Jackson M. 2009. AftD, a novel essential arabinofuranosyltransferase from mycobacteria. Glycobiology 19:1235-1247.
71. Seidel M, Alderwick LJ, Birch HL, Sahm H, Eggeling L, Besra GS. 2007. Identification of a novel arabinofuranosyltransferase AftB involved in a terminal step of cell wall arabinan biosynthesis in Corynebacterianeae, such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J Biol Chem 282:14729-14740.
72. Yagi T, Mahapatra S, Mikusova K, Crick DC, Brennan PJ. 2003. Polymerization of mycobacterial arabinogalactan and ligation to peptidoglycan. J Biol Chem 278:26497-26504.
73. Belisle JT, Vissa VD, Sievert T, Takayama K, Brennan PJ, Besra GS. 1997. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276:1420-1422.
74. Jackson M, Raynaud C, Laneelle MA, Guilhot C, Laurent-Winter C, Ensergueix D, Gicquel B, Daffe M. 1999. 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.
75. Kacem R, De Sousa-D'Auria C, Tropis M, Chami M, Gounon P, Leblon G, Houssin C, Daffe M. 2004. Importance of mycoloyltransferases on the physiology of Corynebacterium glutamicum. Microbiology 150: 73-84.
76. Zhang J, Angala SK, Pramanik PK, Li K, Crick DC, Liav A, Jozwiak A, Swiezewska E, Jackson M, Chatterjee D. 2011. Reconstitution of functional mycobacterial arabinosyltransferase AftC proteoliposome and assessment of decaprenylphosphorylarabinose analogues as arabinofuranosyl donors. ACS Chem Biol 6:819-828.
77. Pitarque S, Larrouy-Maumus G, Payre B, Jackson M, Puzo G, Nigou J. 2008. The immunomodulatory lipoglycans, lipoarabinomannan and lipomannan, are exposed at the mycobacterial cell surface. Tuberculosis (Edinb) 88:560-565.
78. Kordulakova J, Gilleron M, Puzo G, Brennan PJ, Gicquel B, Mikusova K, Jackson M. 2003. Identification of the required acyltransferase step in the biosynthesis of the phosphatidylinositol mannosides of mycobacterium species. J Biol Chem 278:36285-36295.
79. Guerin ME, Kordulakova J, Schaeffer F, Svetlikova Z, Buschiazzo A, Giganti D, Gicquel B, Mikusova K, Jackson M, Alzari PM. 2007. Molecular recognition and interfacial catalysis by the essential phosphatidylinositol mannosyltransferase PimA from mycobacteria. J Biol Chem 282:20705-20714.
80. Kordulakova J, Gilleron M, Mikusova K, Puzo G, Brennan PJ, Gicquel B, Jackson M. 2002. Definition of the first mannosylation step in phosphatidylinositol mannoside synthesis. PimA is essential for growth of mycobacteria. J Biol Chem 277:31335-31344.
81. Belanger AE, Besra GS, Ford ME, Mikusova K, Belisle JT, Brennan PJ, Inamine JM. 1996. The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol. Proc Natl Acad Sci USA 93:11919-11924.
82. Telenti A, Philipp WJ, Sreevatsan S, Bernasconi C, Stockbauer KE, Wieles B, Musser JM, Jacobs, WR, Jr. 1997. The emb operon, a gene cluster of Mycobacterium tuberculosis involved in resistance to ethambutol. Nat Med 3:567-570.
83. Zhang N, Torrelles JB, McNeil MR, Escuyer VE, Khoo KH, Brennan PJ, Chatterjee D. 2003. The Emb proteins of mycobacteria direct arabinosylation of lipoarabinomannan and arabinogalactan via an N-terminal recognition region and a C-terminal synthetic region. Mol Microbiol 50:69-76.
84. Besra GS, Brennan PJ. 1997. The mycobacterial cell wall: biosynthesis of arabinogalactan and lipoarabinomannan. Biochem Soc Trans 25:845-850.
85. Hunter SW, Brennan PJ. 1990. Evidence for the presence of a phosphatidylinositol anchor on the lipoarabinomannan and lipomannan of Mycobacterium tuberculosis. J Biol Chem 265:9272-9279.
86. Nigou J, Gilleron M, Puzo G. 2003. Lipoarabinomannans: from structure to biosynthesis. Biochimie 85:153-166.
87. Ballou CE, Vilkas E, Lederer E. 1963. Structural studies on the myoinositol phospholipids of Mycobacterium tuberculosis (var. bovis, strain BCG). J Biol Chem 238:69-76.
88. Ballou CE, Lee YC. 1964. The structure of a myoinositol mannoside from Mycobacterium tuberculosis glycolipid. Biochemistry 3:682-685.
89. Nigou J, Gilleron M, Brando T, Puzo G. 2004. Structural analysis of mycobacterial lipoglycans. Appl Biochem Biotechnol 118:253-267.
90. Severn WB, Furneaux RH, Falshaw R, Atkinson PH. 1998. Chemical and spectroscopic characterisation of the phosphatidylinositol mannooligosaccharides from Mycobacterium bovis AN5 and WAg201 and Mycobacterium smegmatis MC2 155. Carbohydr Res 308:397-408.
91. Brennan P, Ballou CE. 1968. Biosynthesis of mannophosphoinositides by Mycobacterium phlei. Enzymatic acylation of the dimannophosphoinositides. J Biol Chem 243:2975-2984.
92. Khoo KH, Douglas E, Azadi P, Inamine JM, Besra GS, Mikusova K, Brennan PJ, Chatterjee D. 1996. Truncated structural variants of lipoarabinomannan in ethambutol drug-resistant strains of Mycobacterium smegmatis. Inhibition of arabinan biosynthesis by ethambutol. J Biol Chem 271:28682-28690.
93. Chatterjee D, Hunter SW, McNeil M, Brennan PJ. 1992. Lipoarabinomannan. Multiglycosylated form of the mycobacterial mannosylphosphatidylinositols. J Biol Chem 267:6228-6233.
94. Chatterjee D, Bozic CM, McNeil M, Brennan PJ. 1991. Structural features of the arabinan component of the lipoarabinomannan of Mycobacterium tuberculosis. J Biol Chem 266:9652-9660.
95. Guerardel Y, Maes E, Elass E, Leroy Y, Timmerman P, Besra GS, Locht C, Strecker G, Kremer L. 2002. Structural study of lipomannan and lipoarabinomannan from Mycobacterium chelonae. Presence of unusual components with a1, 3-mannopyranose side chains. J Biol Chem 277: 30635-30648.
96. Kaur D, Obregon-Henao A, Pham H, Chatterjee D, Brennan PJ, Jackson M. 2008. Lipoarabinomannan of Mycobacterium: mannose capping by a multifunctional terminal mannosyltransferase. Proc Natl Acad Sci USA 105:17973-17977.
97. Chatterjee D, Khoo KH, McNeil MR, Dell A, Morris HR, Brennan PJ. 1993. Structural definition of the non-reducing termini of mannosecapped LAM from Mycobacterium tuberculosis through selective enzymatic degradation and fast atom bombardment-mass spectrometry. Glycobiology 3:497-506.
98. Khoo KH, Dell A, Morris HR, Brennan PJ, Chatterjee D. 1995. Structural definition of acylated phosphatidylinositol mannosides from Mycobacterium tuberculosis: definition of a common anchor for lipomannan and lipoarabinomannan. Glycobiology 5:117-127.
99. Delmas C, Gilleron M, Brando T, Vercellone A, Gheorghui M, Riviere M, Puzo G. 1997. Comparative structural study of the mannosylated-lipoarabinomannans from Mycobacterium bovis BCG vaccine strains: characterization and localization of succinates. Glycobiology 7:811-817.
100. Jackson M, Brennan PJ. 2009. Polymethylated polysaccharides from Mycobacterium species revisited. J Biol Chem 284:1949-1953.
101. KowalskaH, Pastuszak I, Szymona M. 1980. A mannoglucokinese of Mycobacterium tuberculosis H37Ra. Acta Microbiol Pol. 29:249-257.
102. Patterson JH, Waller RF, Jeevarajah D, Billman-Jacobe H, McConville MJ. 2003. Mannose metabolism is required for mycobacterial growth. Biochem J 372:77-86.
103. McCarthy TR, Torrelles JB, MacFarlane AS, Katawczik M, Kutzbach B, Desjardin LE, Clegg S, Goldberg JB, Schlesinger LS. 2005. Overexpression of Mycobacterium tuberculosis manB, a phosphomannomutase that increases phosphatidylinositol mannoside biosynthesis in Mycobacterium smegmatis and mycobacterial association with human macrophages. Mol Microbiol 58:774-790.
104. Ning B, Elbein AD. 1999. Purification and properties of mycobacterial GDP-mannose pyrophosphorylase. Arch Biochem Biophys 362:339-345.
105. Liu J, Mushegian A. 2003. Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci 12: 1418-1431.
106. Takayama K, Goldman DS. 1970. Enzymatic synthesis of mannosyl-1-phosphoryl-decaprenol by a cell-free system of Mycobacterium tuberculosis. J Biol Chem 245:6251-6257.
107. Wolucka BA, de Hoffmann E. 1998. Isolation and characterization of the major form of polyprenyl-phospho-mannose from Mycobacterium smegmatis. Glycobiology 8:955-962.
108. Gurcha SS, Baulard AR, Kremer L, Locht C, Moody DB, Muhlecker W, Costello CE, Crick DC, Brennan PJ, Besra GS. 2002. Ppm1, a novel polyprenol monophosphomannose synthase from Mycobacterium tuberculosis. Biochem J 365:441-450.
109. Scherman H, Kaur D, Pham H, Skovierova H, Jackson M, Brennan PJ. 2009. Identification of a polyprenylphosphomannosyl synthase involved in the synthesis of mycobacterial mannosides. J Bacteriol 191: 6769-6772.
110. Rana AK, Singh A, Gurcha SS, Cox LR, Bhatt A, Besra GS. 2012. Ppm1-encoded polyprenyl monophosphomannose synthase activity is essential for lipoglycan synthesis and survival in mycobacteria. PLoS One 7:e48211.
111. Movahedzadeh F, Smith DA, Norman RA, Dinadayala P, Murray-Rust J, Russell DG, Kendall SL, Rison SC, McAlister MS, Bancroft GJ, McDonald NQ, Daffe M, Av-Gay Y, Stoker NG. 2004. The Mycobacterium tuberculosis ino1 gene is essential for growth and virulence. Mol Microbiol 51:1003-1014.
112. Bachhawat N, Mande SC. 1999. Identification of the INO1 gene of Mycobacterium tuberculosis H37Rv reveals a novel class of inositol-1-phosphate synthase enzyme. J Mol Biol 291:531-536.
113. Jackson M, Crick DC, Brennan PJ. 2000. Phosphatidylinositol is an essential phospholipid of mycobacteria. J Biol Chem 275:30092-30099.
114. Movahedzadeh F, Wheeler PR, Dinadayala P, Av-Gay Y, Parish T, Daffe M, Stoker NG. 2010. Inositol monophosphate phosphatase genes of Mycobacterium tuberculosis. BMC Microbiol 10:50.
115. Lea-Smith DJ, Martin KL, Pyke JS, Tull D, McConville MJ, Coppel RL, Crellin PK. 2008. Analysis of a new mannosyltransferase required for the synthesis of phosphatidylinositol mannosides and lipoarbinomannan reveals two lipomannan pools in corynebacterineae. J Biol Chem 283: 6773-6782.
116. Mishra AK, Alderwick LJ, Rittmann D, Wang C, Bhatt A, Jacobs WR, Jr, Takayama K, Eggeling L, Besra GS. 2008. Identification of a novel α(1→6) mannopyranosyltransferase MptB from Corynebacterium glutamicum by deletion of a conserved gene, NCgl1505, affords a lipomannan-and lipoarabinomannan-deficient mutant. Mol Microbiol 68:1595-1613.
117. Guerin ME, Kaur D, Somashekar BS, Gibbs S, Gest P, Chatterjee D, Brennan PJ, Jackson M. 2009. New insights into the early steps of phosphatidylinositol mannoside biosynthesis in mycobacteria: PimB' is an essential enzyme of Mycobacterium smegmatis. J Biol Chem 284:25687-25696.
118. Kaur D, McNeil MR, Khoo KH, Chatterjee D, Crick DC, Jackson M, Brennan PJ. 2007. New insights into the biosynthesis of mycobacterial lipomannan arising from deletion of a conserved gene. J Biol Chem 282:27133-27140.
119. Torrelles JB, DesJardin LE, MacNeil J, Kaufman TM, Kutzbach B, Knaup R, McCarthy TR, Gurcha SS, Besra GS, Clegg S, Schlesinger LS. 2009. Inactivation of Mycobacterium tuberculosis mannosyltransferase pimB reduces the cell wall lipoarabinomannan and lipomannan content and increases the rate of bacterial-induced human macrophage cell death. Glycobiology 19:743-755.
120. Mishra AK, Batt S, Krumbach K, Eggeling L, Besra GS. 2009. Characterization of the Corynebacterium glutamicum ΔpimB' ΔmgtA double deletion mutant and the role of Mycobacterium tuberculosis orthologues Rv2188c and Rv0557 in glycolipid biosynthesis. J Bacteriol 191:4465-4472.
121. Kremer L, Gurcha SS, Bifani P, Hitchen PG, Baulard A, Morris HR, Dell A, Brennan PJ, Besra GS. 2002. Characterization of a putative a-mannosyltransferase involved in phosphatidylinositol trimannoside biosynthesis in Mycobacterium tuberculosis. Biochem J 363: 437-447.
122. Guerin ME, J Kordulakova, PM Alzari, PJ Brennan, M Jackson. 2010. Molecular basis of phosphatidyl-myo-inositol mannoside biosynthesis and regulation in mycobacteria. J Biol Chem 285:33577-33583.
123. Morita YS, Patterson JH, Billman-Jacobe H, McConville MJ. 2004. Biosynthesis of mycobacterial phosphatidylinositol mannosides. Biochem J 378:589-597.
124. Morita YS, Sena CB, Waller RF, Kurokawa K, Sernee MF, Nakatani M, Haites RE, Billman-Jacobe H, McConville MJ, Maeda Y, Kinoshita T. 2006. PimE is a polyprenol-phosphate-mannose-dependent mannosyltransferase that transfers the fifthmannose of phosphatidylinositol mannoside in mycobacteria. J Biol Chem 281:25143-25155.
125. Crellin PK, Kovacevic S, Martin KL, Brammananth R, Morita YS, Billman-Jacobe H, McConville MJ, Coppel RL. 2008. Mutations in pimE restore lipoarabinomannan synthesis and growth in a Mycobacterium smegmatis lpqW mutant. J Bacteriol 190:3690-3699.
126. Kovacevic S, Anderson D, Morita YS, Patterson J, Haites R, McMillan BN, Coppel R, McConville MJ, Billman-Jacobe H. 2006. Identification of a novel protein with a role in lipoarabinomannan biosynthesis in mycobacteria. J Biol Chem 281:9011-9017.
127. Rainczuk AK, Yamaryo-Botte Y, Brammananth R, Stinear TP, Seemann T, Coppel RL, McConville MJ, Crellin PK. 2012. The lipoprotein LpqW is essential for the mannosylation of periplasmic glycolipids in Corynebacteria. J Biol Chem 287:42726-42738.
128. Mishra AK, Alderwick LJ, Rittmann D, Tatituri RV, Nigou J, Gilleron M, Eggeling L, Besra GS. 2007. Identification of an α(1→6) mannopyranosyltransferase (MptA), involved in Corynebacterium glutamicum lipomanann biosynthesis, and identification of its orthologue in Mycobacterium tuberculosis. Mol Microbiol 65:1503-1517.
129. Kaur D, Berg S, Dinadayala P, Gicquel B, Chatterjee D, McNeil MR, Vissa VD, Crick DC, Jackson M, Brennan PJ. 2006. Biosynthesis of mycobacterial lipoarabinomannan: role of a branching mannosyltransferase. Proc Natl Acad Sci USA 103:13664-13669.
130. Alderwick LJ, Lloyd GS, Ghadbane H, May JW, Bhatt A, Eggeling L, Futterer K, Besra GS. 2011. The C-terminal domain of the arabinosyltransferase Mycobacterium tuberculosis EmbC is a lectin-like carbohydrate binding module. PLoS Pathog 7:e1001299.
131. Shi L, Berg S, Lee A, Spencer JS, Zhang J, Vissa V, McNeil MR, Khoo KH, Chatterjee D. 2006. The carboxy terminus of EmbC from Mycobacterium smegmatis mediates chain length extension of the arabinan in lipoarabinomannan. J Biol Chem 281:19512-19526.
132. Dinadayala P, Kaur D, Berg S, Amin AG, Vissa VD, Chatterjee D, Brennan PJ, Crick DC. 2006. Genetic basis for the synthesis of the immunomodulatory mannose caps of lipoarabinomannan in Mycobacterium tuberculosis. J Biol Chem 281:20027-20035.
133. Appelmelk BJ, den Dunnen J, Driessen NN, Ummels R, Pak M, Nigou J, Larrouy-Maumus G, Gurcha SS, Movahedzadeh F, Geurtsen J, Brown EJ, Eysink Smeets MM, Besra GS, Willemsen PT, Lowary TL, van Kooyk Y, Maaskant JJ, Stoker NG, van der Ley P, Puzo G, Vandenbroucke-Grauls CM, Wieland CW, van der Poll T, Geijtenbeek TB, van der Sar AM, Bitter W. 2008. The mannose cap of mycobacterial lipoarabinomannan does not dominate the mycobacterium-host interaction. Cell Microbiol 10: 930-944.
134. Thomas JP, Baughn CO, Wilkinson RG, Shepherd RG. 1961. A new synthetic compound with antituberculous activity in mice: ethambutol (dextro-2, 2'-(ethylenediimino)-di-l-butanol). Am Rev Respir Dis 83:891-893.
135. Kilburn JO, Greenberg J. 1977. Effect of ethambutol on the viable cell count in Mycobacterium smegmatis. Antimicrob Agents Chemother 11:534-540.
136. Kilburn JO, Takayama K, Armstrong EL, Greenberg J. 1981. Effects of ethambutol on phospholipid metabolism in Mycobacterium smegmatis. Antimicrob Agents Chemother 19:346-348.
137. Takayama K, Armstrong EL, Kunugi KA, Kilburn JO. 1979. Inhibition by ethambutol of mycolic acid transfer into the cell wall of Mycobacterium smegmatis. Antimicrob Agents Chemother 16:240-242.
138. Takayama K, Kilburn JO. 1989. Inhibition of synthesis of arabinogalactan by ethambutol in Mycobacterium smegmatis. Antimicrob Agents Chemother 33:1493-1499.
139. Mikusova K, Slayden RA, Besra GS, Brennan PJ. 1995. Biogenesis of the mycobacterial cell wall and the site of action of ethambutol. Antimicrob Agents Chemother 39:2484-2489.
140. Deng L, Mikusova K, Robuck KG, Scherman M, Brennan PJ, McNeil MR. 1995. Recognition of multiple effects of ethambutol on metabolism of mycobacterial cell envelope. Antimicrob Agents Chemother 39:694-701.
141. Lee M, Mikusova K, Brennan PJ, Besra GS. 1995. Synthesis of the arabinose donor β-d-arabinofuranosyl-1-monophosphoryldecaprenol, development of a basic arabinosyl-transferase assay, and identification of ethambutol as an arabinosyl transferase inhibitor. J Am Chem Soc 117: 11829-11832.
142. Wolucka BA, McNeil MR, de Hoffmann E, Chojnacki T, Brennan PJ. 1994. Recognition of the lipid intermediate for arabinogalactan/arabinomannan biosynthesis and its relation to the mode of action of ethambutol on mycobacteria. J Biol Chem 269:23328-23335.
143. Lety MA, Nair S, Berche P, Escuyer V. 1997. A single point mutation in the embB gene is responsible for resistance to ethambutol in Mycobacterium smegmatis. Antimicrob Agents Chemother 41:2629-2633.
144. Khasnobis S, Zhang J, Angala SK, Amin AG, McNeil MR, Crick DC, Chatterjee D. 2006. Characterization of a specific arabinosyltransferase activity involved in mycobacterial arabinan biosynthesis. Chem Biol 13: 787-795.
145. Alcaide F, Pfyffer GE, Telenti A. 1997. Role of embB in natural and acquired resistance to ethambutol in mycobacteria. Antimicrob Agents Chemother 41:2270-2273.
146. Ramaswamy SV, Amin AG, Goksel S, Stager CE, Dou SJ, El Sahly H, Moghazeh SL, Kreiswirth BN, Musser JM. 2000. Molecular genetic analysis of nucleotide polymorphisms associated with ethambutol resistance in human isolates of Mycobacterium tuberculosis. Antimicrob Agents Chemother 44:326-336.
147. Sreevatsan S, Stockbauer KE, Pan X, Kreiswirth BN, Moghazeh SL, Jacobs WR, Jr, Telenti A, Musser JM. 1997. Ethambutol resistance in Mycobacterium tuberculosis: critical role of embB mutations. Antimicrob Agents Chemother 41:1677-1681.
148. Protopopova M, Hanrahan C, Nikonenko B, Samala R, Chen P, Gearhart J, Einck L, Nacy CA. 2005. Identification of a new antitubercular drug candidate, SQ109, from a combinatorial library of 1, 2-ethylenediamines. J Antimicrob Chemother 56:968-974.
149. Nikonenko BV, Protopopova M, Samala R, Einck L, Nacy CA. 2007. Drug therapy of experimental tuberculosis (TB): improved outcome by combining SQ109, a new diamine antibiotic, with existing TB drugs. Antimicrob Agents Chemother 51:1563-1565.
150. Reddy VM, Einck L, Andries K, Nacy CA. 2010. In vitro interactions between new antitubercular drug candidates SQ109 and TMC207. Antimicrob Agents Chemother 54:2840-2846.
151. Engohang-Ndong J. 2012. Antimycobacterial drugs currently in phase II clinical trials and preclinical phase for tuberculosis treatment. Expert Opin Investig Drugs 21:1789-1800.
152. Tahlan K, Wilson R, Kastrinsky DB, Arora K, Nair V, Fischer E, Barnes SW, Walker JR, AllandD, Barry, CE, 3rd, BoshoffHI. 2012. SQ109 targets MmpL3, a membrane transporter of trehalose monomycolate involved in mycolic acid donation to the cell wall core of Mycobacterium tuberculosis. Antimicrob Agents Chemother 56:1797-1809.
153. Trefzer C, Skovierova H, Buroni S, Bobovska A, Nenci S, Molteni E, Pojer F, Pasca MR, Makarov V, Cole ST, Riccardi G, Mikusova K, Johnsson K. 2012. Benzothiazinones are suicide inhibitors of mycobacterial decaprenylphosphoryl-β-D-ribofuranose 2'-oxidase DprE1. J Am Chem Soc 134:912-915.
154. Trefzer C, Rengifo-Gonzalez M, Hinner MJ, Schneider P, Makarov V, Cole ST, Johnsson K. 2010. Benzothiazinones: prodrugs that covalently modify the decaprenylphosphoryl-β-D-ribose 2'-epimerase DprE1 of Mycobacterium tuberculosis. J Am Chem Soc 132:13663-13665.
155. Manina G, Bellinzoni M, Pasca MR, Neres J, Milano A, Ribeiro AL, Buroni S, Skovierova H, Dianiskova P, Mikusova K, Marak J, Makarov V, Giganti D, Haouz A, Lucarelli AP, Degiacomi G, Piazza A, Chiarelli LR, De Rossi E, Salina E, Cole ST, Alzari PM, Riccardi G. 2010. Biological and structural characterization of the Mycobacterium smegmatis nitroreductase NfnB, and its role in benzothiazinone resistance. Mol Microbiol 77:1172-1185.
156. Pasca MR, Degiacomi G, Ribeiro AL, Zara F, De Mori P, HeymB, Mirrione M, Brerra R, Pagani L, Pucillo L, Troupioti P, Makarov V, Cole ST, Riccardi G. 2010. Clinical isolates of Mycobacterium tuberculosis in four European hospitals are uniformly susceptible to benzothiazinones. Antimicrob Agents Chemother 54:1616-1618.
157. Larrouy-Maumus G, Skovierova H, Dhouib R, Angala SK, Zuberogoitia S, Pham H, Villela AD, Mikusova K, Noguera A, Gilleron M, Valentinova L, Kordulakova J, Brennan PJ, Puzo G, Nigou J, Jackson M. 2012. A small multidrug resistance-like transporter involved in the arabinosylation of arabinogalactan and lipoarabinomannan in mycobacteria. J Biol Chem 287:39933-39941.