GtrA protein Rv3789 is required for arabinosylation of arabinogalactan in Mycobacterium tuberculosis

Journal of Bacteriology

Volumn 197, Issue 23, 2015, Pages 3686-3697

  Kolly, Gaëlle S ^a,b   Mukherjee, Raju ^a,b,d   Kilacsková, Emöke ^a,c   Abriata, Luciano A ^b   Raccaud, Mahé ^b   Blaško, Jaroslav ^a,c   Sala, Claudia ^a,b   Dal Peraro, Matteo ^b   Mikušová, Katarína ^a,c   Cole, Stewart T ^a,b  

^a Global Health Institute   (Switzerland)

^b EPFL   (Switzerland)

^c Faculty of Natural Sciences   (Slovakia)

^d UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINAN; ARABINOGALACTAN; ARABINOSE DERIVATIVE; ARABINOSYLTRANSFERASE AFTA; BACTERIAL PROTEIN; DECAPRENYLPHOSPHOARABINOSE; DPRE1 PROTEIN; GTRA PROTEIN RV3789; MEMBRANE PROTEIN; TRANSFERASE; UNCLASSIFIED DRUG; ALDEHYDE DEHYDROGENASE; ARABINOSE; DECAPRENYL-P-ARABINOSE; GALACTAN; GLUTAMYL TRNA REDUCTASE; TERPENE;

ARABINOSYLATION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BIOACCUMULATION; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; CHEMICAL REACTION; CONTROLLED STUDY; DELETION MUTANT; DPRE1 GENE; MOLECULAR MODEL; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RV3789 GENE; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION SITE; TWO HYBRID SYSTEM; WILD TYPE; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

ALDEHYDE OXIDOREDUCTASES; AMINO ACID SEQUENCE; ARABINOSE; BACTERIAL PROTEINS; BASE SEQUENCE; GALACTANS; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; SEQUENCE ALIGNMENT; TERPENES;

EID: 84946229029     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00628-15     Document Type: Article

References (45)

1. 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.
2. 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.
3. 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.
4. Angala SK, Belardinelli JM, Huc-Claustre E, Wheat WH, Jackson M. 2014. The cell envelope glycoconjugates of Mycobacterium tuberculosis. Crit Rev Biochem Mol Biol 49:361-399. http://dx.doi.org/10.3109/10409238.2014.925420.
5. 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. http://dx.doi.org/10.2217/fmb.11.123.
6. 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.
7. Mikusová 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. http://dx.doi.org/10.1128/JB.187.23.8020-8025.2005.
8. Trefzer C, Škovierová H, Buroni S, Bobovská A, Nenci S, Molteni E, Pojer F, Pasca MR, Makarov V, Cole ST, Riccardi G, Mikušová K, Johnsson K. 2012. Benzothiazinones are suicide inhibitors of mycobacterial decaprenylphosphoryl-ß-D-ribofuranose 2'-oxidase DprE1. J Am Chem Soc 134:912-915. http://dx.doi.org/10.1021/ja211042r.
9. 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. http://dx.doi.org/10.1074/jbc. M600045200.
10. 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. http://dx.doi.org/10.1074/jbc. M700271200.
11. 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 U S A 93:11919-11924. http://dx.doi.org/10.1073/pnas.93.21.11919.
12. 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. http://dx.doi.org/10.1074/jbc. M102272200.
13. Goude R, Amin AG, Chatterjee D, Parish T. 2008. The critical role of embC in Mycobacterium tuberculosis. J Bacteriol 190:4335-4341. http://dx.doi.org/10.1128/JB.01825-07.
14. 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 alpha(1→3) arabinofuranosyltransferase. Mol Microbiol 69:1191-1206. http://dx.doi.org/10.1111/j.1365-2958.2008.06354.x.
15. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, III, 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. http://dx.doi.org/10.1038/31159.
16. Belanger AE, Inamine JM. 2000. Genetics of cell wall biosynthesis, p 191-202. In Hatfull GF, Jacobs WR, Jr (ed), Molecular genetics of mycobacteria. ASM Press, Washington, DC.
17. Guan S, Bastin DA, Verma NK. 1999. Functional analysis of the O antigen glucosylation gene cluster of Shigella flexneri bacteriophage SfX. Microbiology 145(Pt 5):1263-1273.
18. Korres H, Mavris M, Morona R, Manning PA, Verma NK. 2005. Topological analysis of GtrA and GtrB proteins encoded by the serotypeconverting cassette of Shigella flexneri. Biochem Biophys Res Commun 328:1252-1260. http://dx.doi.org/10.1016/j.bbrc.2005.01.087.
19. Larrouy-Maumus G, Škovierová H, Dhouib R, Angala SK, Zuberogoitia S, Pham H, Villela AD, Mikušová 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. http://dx.doi.org/10.1074/jbc. M112.400986.
20. Gomez JE, Bishai WR. 2000. whmD is an essential mycobacterial gene required for proper septation and cell division. Proc Natl Acad Sci U S A 97:8554-8559. http://dx.doi.org/10.1073/pnas.140225297.
21. Muñoz-Elías EJ, Upton AM, Cherian J, McKinney JD. 2006. Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol Microbiol 60:1109-1122. http://dx.doi.org/10.1111/j.1365-2958.2006.05155.x.
22. Kolly GS, Boldrin F, Sala C, Dhar N, Hartkoorn RC, Ventura M, Serafini A, McKinney JD, Manganelli R, Cole ST. 2014. Assessing the essentiality of the decaprenyl-phospho-D-arabinofuranose pathway in Mycobacterium tuberculosis using conditional mutants. Mol Microbiol 92:194-211. http://dx.doi.org/10.1111/mmi.12546.
23. Singh A, Mai D, Kumar A, Steyn AJ. 2006. Dissecting virulence pathways of Mycobacterium tuberculosis through protein-protein association. Proc Natl Acad Sci U S A 103:11346-11351. http://dx.doi.org/10.1073/pnas.0602817103.
24. Reed MB, Gagneux S, Deriemer K, Small PM, Barry CE, III. 2007. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol 189:2583-2589. http://dx.doi.org/10.1128/JB.01670-06.
25. Scherman MS, Kalbe-Bournonville L, Bush D, Xin Y, Deng L, McNeil M. 1996. Polyprenylphosphate-pentoses in mycobacteria are synthesized from 5-phosphoribose pyrophosphate. J Biol Chem 271:29652-29658. http://dx.doi.org/10.1074/jbc.271.47.29652.
26. Bhamidi S, Scherman MS, Jones V, Crick DC, Belisle JT, Brennan PJ, McNeil MR. 2011. Detailed structural and quantitative analysis reveals the spatial organization of the cell walls of in vivo grown Mycobacterium leprae and in vitro grown Mycobacterium tuberculosis. J Biol Chem 286:23168-23177. http://dx.doi.org/10.1074/jbc. M110.210534.
27. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugar and related substances. Anal Chem 28:350-356. http://dx.doi.org/10.1021/ac60111a017.
28. Wolucka BA, de Hoffmann E. 1995. The presence of ß-D-ribosyl-1-monophosphodecaprenol in mycobacteria. J Biol Chem 270:20151-20155. http://dx.doi.org/10.1074/jbc.270.34.20151.
29. Rombouts Y, Brust B, Ojha AK, Maes E, Coddeville B, Elass-Rochard E, Kremer L, Guerardel Y. 2012. Exposure of mycobacteria to cell wallinhibitory drugs decreases production of arabinoglycerolipid related to mycolyl-arabinogalactan-peptidoglycan metabolism. J Biol Chem 287:11060-11069. http://dx.doi.org/10.1074/jbc. M111.327387.
30. Ciucanu I, Kerek F. 1984. A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131:209-217. http://dx.doi.org/10.1016/0008-6215(84)85242-8.
31. Thompson JD, Gibson TJ, Higgins DG. 2002. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2:Unit 2.3.
32. Flores AR, Parsons LM, Pavelka MS, Jr. 2005. Genetic analysis of the beta-lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to beta-lactam antibiotics. Microbiology 151:521-532. http://dx.doi.org/10.1099/mic.0.27629-0.
33. Roy A, Kucukural A, Zhang Y. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725-738. http://dx.doi.org/10.1038/nprot.2010.5.
34. Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, Zecchina R, Sander C. 2011. Protein 3D structure computed from evolutionary sequence variation. PLoS One 6:e28766. http://dx.doi.org/10.1371/journal.pone.0028766.
35. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. 2006. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65:712-725. http://dx.doi.org/10.1002/prot.21123.
36. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K. 2005. Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802. http://dx.doi.org/10.1002/jcc.20289.
37. Comeau SR, Gatchell DW, Vajda S, Camacho CJ. 2004. ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20:45-50. http://dx.doi.org/10.1093/bioinformatics/btg371.
38. Uplekar S, Rougemont J, Cole ST, Sala C. 2013. High-resolution transcriptome and genome-wide dynamics of RNA polymerase and NusA in Mycobacterium tuberculosis. Nucleic Acids Res 41:961-977. http://dx.doi.org/10.1093/nar/gks1260.
39. Hopf TA, Colwell Lucy J, Sheridan R, Rost B, Sander C, Marks Debora S. 2012. Three-dimensional structures of membrane proteins from genomic sequencing. Cell 149:1607-1621. http://dx.doi.org/10.1016/j.cell.2012.04.012.
40. von Heijne G. 1986. The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J 5:3021-3027.
41. Jankute M, Byng C, Alderwick L, Besra G. 2014. Elucidation of a proteinprotein interaction network involved in Corynebacterium glutamicum cell wall biosynthesis as determined by bacterial two-hybrid analysis. Glycoconj J 31:475-483. http://dx.doi.org/10.1007/s10719-014-9549-3.
42. Islam ST, Fieldhouse RJ, Anderson EM, Taylor VL, Keates RAB, Ford RC, Lam JS. 2012. A cationic lumen in the Wzx flippase mediates anionic O-antigen subunit translocation in Pseudomonas aeruginosa PAO1. Mol Microbiol 84:1165-1176. http://dx.doi.org/10.1111/j.1365-2958.2012.08084.x.
43. Brecik M, Centarova I, Mukherjee R, Kolly GS, Huszar S, Bobovska A, Kilacskova E, Mokosova V, Svetlikova Z, Sarkan M, Neres J, Kordulakova J, Cole ST, Mikusova K. 2015. DprE1 is a vulnerable tuberculosis drug target due to its cell wall localization. ACS Chem Biol 10:1631-1636. http://dx.doi.org/10.1021/acschembio.5b00237.
44. Lew JM, Kapopoulou A, Jones LM, Cole ST. 2011. TubercuList-10 years after. Tuberculosis (Edinb) 91:1-7. http://dx.doi.org/10.1016/j.tube.2010.09.008.
45. Kapopoulou A, Lew JM, Cole ST. 2011. The MycoBrowser portal: a comprehensive and manually annotated resource for mycobacterial genomes. Tuberculosis (Edinb) 91:8-13. http://dx.doi.org/10.1016/j.tube.2010.09.006.