Mechanism of dephosphorylation of glucosyl-3-phosphoglycerate by a histidine phosphatase

Journal of Biological Chemistry

Volumn 289, Issue 31, 2014, Pages 21242-21251

  Zheng, Qianqian ^a   Jiang, Dunquan ^a   Zhang, Wei ^a   Zhang, Qingqing ^a   Zhao, Qi ^e   Jin, Jin ^a   Li, Xin ^a   Yang, Haitao ^b   Bartlam, Mark ^a   Shaw, Neil ^a,c   Zhou, Weihong ^a   Rao, Zihe ^a,c,d  

^a NANKAI UNIVERSITY   (China)

^b TIANJIN UNIVERSITY   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

^d Tsinghua University   (China)

^e YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; CATALYSIS; DIMERS; ENZYME ACTIVITY; FATTY ACIDS; PHOSPHATASES; POLYSACCHARIDES;

CONFORMATIONAL CHANGE; ENZYMATIC ACTIVITIES; FATTY ACID BIOSYNTHESIS; LIPOPOLYSACCHARIDES; LONG CHAIN FATTY ACID; MYCOBACTERIUM TUBERCULOSIS; POSITIVELY CHARGED; SITE DIRECTED MUTAGENESIS;

BIOSYNTHESIS;

ARGININE; ASPARAGINE; GLUTAMIC ACID; GLYCOSYL 3 PHOSPHOGLYCERATE PHOSPHATASE; HISTIDINE; HISTIDINE PHOSPHATASE; LEUCINE; PROTEIN HISTIDINE KINASE; PROTEIN LOOP2; UNCLASSIFIED DRUG; VANADIC ACID; 3-PHOSPHOGLYCERATE; GLYCERIC ACID; PHOSPHATASE;

ALPHA HELIX; ARTICLE; BETA SHEET; BINDING AFFINITY; CATALYSIS; CRYSTAL STRUCTURE; DENSITY; DIMERIZATION; ELECTRON; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME STRUCTURE; FEEDBACK SYSTEM; LIGAND BINDING; MUTATIONAL ANALYSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS; CHEMICAL STRUCTURE; METABOLISM; OPEN READING FRAME; PHOSPHORYLATION;

DIMERIZATION; GLYCERIC ACIDS; MODELS, MOLECULAR; OPEN READING FRAMES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION;

EID: 84905367179     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.569913     Document Type: Article

References (47)

1. Daffé, M., and Draper, P. (1998) The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39, 131-203 (Pubitemid 29077883)
2. Hett, E. C., and Rubin, E. J. (2008) Bacterial growth and cell division: a mycobacterial perspective. Microbiol. Mol. Biol. Rev. 72, 126-156 (Pubitemid 351398058)
3. Brennan, P. J. (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis (Edinb.) 83, 91-97
4. Riley, L. W. (2006) Of mice, men, and elephants: Mycobacterium tuberculosis cell envelope lipids and pathogenesis. J. Clin. Invest. 116, 1475-1478
5. Ilton, M., Jevans, A. W., McCarthy, E. D., Vance, D., White, H. B., 3rd, and Bloch, K. (1971) Fatty acid synthetase activity in Mycobacterium phlei: regulation by polysaccharides. Proc. Natl. Acad. Sci. U.S.A. 68, 87-91
6. Sassetti, C. M., Boyd, D. H., and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84 (Pubitemid 36411469)
7. Tuffal, G., Albigot, R., Rivière, M., and Puzo, G. (1998) Newly found 2-N-acetyl-2,6-dideoxy-βglucopyranose containing methyl glucose polysaccharides in M. bovis BCG: revised structure of the mycobacterial methyl glucose lipopolysaccharides. Glycobiology 8, 675-684 (Pubitemid 28331443)
8. Tuffal, G., Ponthus, C., Picard, C., Rivière, M., and Puzo, G. (1995) Structural elucidation of novel methylglucose-containing polysaccharides from Mycobacterium xenopi. Eur. J. Biochem. 233, 377-383
9. Kamisango, K., Dell, A., and Ballou, C. E. (1987) Biosynthesis of the mycobacterial O-methylglucose lipopolysaccharide. Characterization of putative intermediates in the initiation, elongation, and termination reactions. J. Biol. Chem. 262, 4580-4586 (Pubitemid 17102822)
10. Saier, M. H., Jr., and Ballou, C. E. (1968) The 6-O-methylglucose- containig lipopolysaccharide of Mycobacterium phlei: complete structure of the polysaccharide. J. Biol. Chem. 243, 4332-4341
11. Costa, J., Empadinhas, N., Gonçalves, L., Lamosa, P., Santos, H., and da Costa, M. S. (2006) Characterization of the biosynthetic pathway of glucosylglycerate in the archaeon Methanococcoides burtonii. J. Bacteriol. 188, 1022-1030 (Pubitemid 43146418)
12. Machida, Y., and Bloch, K. (1973) Complex formation between mycobacterial polysaccharides and fatty acyl-CoA derivatives. Proc. Natl. Acad. Sci. U.S.A. 70, 1146-1148
13. Bergeron, R., Machida, Y., and Bloch, K. (1975) Complex formation between mycobacterial polysaccharides or cyclodextrins and palmitoyl co-enzyme A. J. Biol. Chem. 250, 1223-1230
14. Mendes, V., Maranha, A., Alarico, S., da Costa, M. S., and Empadinhas, N. (2011) Mycobacterium tuberculosis Rv2419c, the missing glucosyl-3- phosphoglycerate phosphatase for the second step in methylglucose lipopolysaccharide biosynthesis. Sci. Rep. 1, 177
15. Empadinhas, N., Marugg, J. D., Borges, N., Santos, H., and da Costa, M. S. (2001) Pathway for the synthesis of mannosylglycerate in the hyperthermophilic archaeon Pyrococcus horikoshii. Biochemical and genetic characterization of key enzymes. J. Biol. Chem. 276, 43580-43588
16. Costa, J., Empadinhas, N., and da Costa, M. S. (2007) Glucosylglycerate biosynthesis in the deepest lineage of the bacteria: characterization of the thermophilic proteins GpgS and GpgP from Persephonella marina. J. Bacteriol. 189, 1648-1654 (Pubitemid 46446127)
17. Empadinhas, N., Albuquerque, L., Henne, A., Santos, H., and da Costa, M. S. (2003) The bacterium Thermus thermophilus, like hyperthermophilic archaea, uses a two-step pathway for the synthesis of mannosylglycerate. Appl. Environ. Microbiol. 69, 3272-3279 (Pubitemid 36693331)
18. Rigden, D. J. (2008) The histidine phosphatase superfamily: structure and function. Biochem. J. 409, 333-348
19. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
20. Long, F., Vagin, A. A., Young, P., and Murshudov, G. N. (2008) BALBES: a molecular-replacement pipeline. Acta Crystallogr. D Biol. Crystallogr. 64, 125-132 (Pubitemid 350308686)
21. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for x-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179
22. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
23. Afonine, P. V., Grosse-Kunstleve, R. W., Echols, N., Headd, J. J., Moriarty, N. W., Mustyakimov, M., Terwilliger, T. C., Urzhumtsev, A., Zwart, P. H., and Adams, P. D. (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367
24. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
25. Terwilliger, T. C., Klei, H., Adams, P. D., Moriarty, N. W., and Cohn, J. D. (2006) Automated ligand fitting by core-fragment fitting and extension into density. Acta Crystallogr. D Biol. Crystallogr. 62, 915-922 (Pubitemid 44125669)
26. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
27. Takai, A., and Mieskes, G. (1991) Inhibitory effect of okadaic acid on the p-nitrophenyl phosphate phosphatase activity of protein phosphatases. Biochem. J. 275, 233-239
28. Some, D. (2013) Light-scattering-based analysis of biomolecular interactions. Biophys. Rev. 5, 147-158
29. Rigden, D. J., Littlejohn, J. E., Henderson, K., and Jedrzejas, M. J. (2003) Structures of phosphate and trivanadate complexes of Bacillus stearothermophilus phosphatase PhoE: structural and functional analysis in the cofactor-dependent phosphoglycerate mutase superfamily. J. Mol. Biol. 325, 411-420 (Pubitemid 36062672)
30. Rigden, D. J., Mello, L. V., Setlow, P., and Jedrzejas, M. J. (2002) Structure and mechanism of action of a cofactor-dependent phosphoglycerate mutase homolog from Bacillus stearothermophilus with broad specificity phosphatase activity. J. Mol. Biol. 315, 1129-1143 (Pubitemid 34729291)
31. Bond, C. S., White, M. F., and Hunter, W. N. (2001) High resolution structure of the phosphohistidine-activated form of Escherichia coli cofactor-dependent phosphoglycerate mutase. J. Biol. Chem. 276, 3247-3253 (Pubitemid 37411618)
32. Fothergill-Gilmore, L. A., and Watson, H. C. (1989) The phosphoglycerate mutases. Adv. Enzymol. Relat. Areas Mol. Biol. 62, 227-313
33. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
34. Chiba, Y., Horita, S., Ohtsuka, J., Arai, H., Nagata, K., Igarashi, Y., Tanokura, M., and Ishii, M. (2013) Structural units important for activity of a novel-type phosphoserine phosphatase from Hydrogenobacter thermophilus TK-6 revealed by crystal structure analysis. J. Biol. Chem. 288, 11448-11458
35. Davies, D. R., Staker, B. L., Abendroth, J. A., Edwards, T. E., Hartley, R., Leonard, J., Kim, H., Rychel, A. L., Hewitt, S. N., Myler, P. J., and Stewart, L. J. (2011) An ensemble of structures of Burkholderia pseudomallei 2,3-bisphosphoglycerate-dependent phosphoglycerate mutase. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 67, 1044-1050
36. Koonin, E. V., and Tatusov, R. L. (1994) Computer analysis of bacterial haloacid dehalogenases defines a large superfamily of hydrolases with diverse specificity. Application of an iterative approach to database search. J. Mol. Biol. 244, 125-132
37. Thaller, M. C., Schippa, S., and Rossolini, G. M. (1998) Conserved sequence motifs among bacterial, eukaryotic, and archaeal phosphatases that define a new phosphohydrolase superfamily. Protein Sci. 7, 1647-1652 (Pubitemid 28331288)
38. Ashkenazy, H., Erez, E., Martz, E., Pupko, T., and Ben-Tal, N. (2010). ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529-W533
39. Lee, Y. H., Ogata, C., Pflugrath, J. W., Levitt, D. G., Sarma, R., Banaszak, L. J., and Pilkis, S. J. (1996) Crystal structure of the rat liver fructose-2,6-bisphosphatase based on selenomethionine multiwavelength anomalous dispersion phases. Biochemistry 35, 6010-6019 (Pubitemid 26147572)
40. Yuen, M. H., Mizuguchi, H., Lee, Y. H., Cook, P. F., Uyeda, K., and Hasemann, C. A. (1999) Crystal structure of the H256A mutant of rat testis fructose-6-phosphate,2-kinase/fructose-2,6-bisphosphatase. Fructose 6-phosphate in the active site leads to mechanisms for both mutant and wild type bisphosphatase activities. J. Biol. Chem. 274, 2176-2184
41. Bond, C. S., White, M. F., and Hunter, W. N. (2002) Mechanistic implications for Escherichia coli cofactor-dependent phosphoglycerate mutase based on the high-resolution crystal structure of a vanadate complex. J. Mol. Biol. 316, 1071-1081 (Pubitemid 34729226)
42. Stadthagen, G., Sambou, T., Guerin, M., Barilone, N., Boudou, F., Korduláková, J., Charles, P., Alzari, P. M., Lemassu, A., Daffé, M., Puzo, G., Gicquel, B., Rivière, M., and Jackson, M. (2007) Genetic basis for the biosynthesis of methylglucose lipopolysaccharides in Mycobacterium tuberculosis. J. Biol. Chem. 282, 27270-27276 (Pubitemid 47501941)
43. Empadinhas, N., Albuquerque, L., Mendes, V., Macedo-Ribeiro, S., and da Costa, M. S. (2008) Identification of the mycobacterial glucosyl-3- phosphoglycerate synthase. FEMS Microbiol. Lett. 280, 195-202 (Pubitemid 351287519)
44. Mendes, V., Maranha, A., Alarico, S., and Empadinhas, N. (2012) Biosynthesis of mycobacterial methylglucose lipopolysaccharides. Nat. Prod Rep. 29, 834-844
45. Mendes, V., Maranha, A., Lamosa, P., da Costa, M. S., and Empadinhas, N. (2010) Biochemical characterization of the maltokinase from Mycobacterium bovis BCG. BMC Biochem. 11, 21
46. Garg, S. K., Alam, M. S., Kishan, K. V., and Agrawal, P. (2007) Expression and characterization of α-(1,4)-glucan branching enzyme Rv1326c of Mycobacterium tuberculosis H37Rv. Protein Expr. Purif. 51, 198-208 (Pubitemid 44821882)
47. Syson, K., Stevenson, C. E., Rejzek, M., Fairhurst, S. A., Nair, A., Bruton, C. J., Field, R. A., Chater, K. F., Lawson, D. M., and Bornemann, S. (2011) Structure of Streptomyces maltosyltransferase GlgE, a homologue of a genetically validated anti-tuberculosis target. J. Biol. Chem. 286, 38298-38310