Shikimate kinase (EC 2.7.1.71) from Mycobacterium tuberculosis: Kinetics and structural dynamics of a potential molecular target for drug development

Current Medicinal Chemistry

Volumn 18, Issue 9, 2011, Pages 1299-1310

  Saidemberg, D M ^a,b   Passarelli, A W ^a,b   Rodrigues, A V ^a,b   Basso, L A ^c,d   Santos, D S ^c,d   Palma, M S ^a,b  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b National Institute of Science and Technology on Immunology (INCT/ iii)   (Brazil)

^c PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^d National Institute of Science and Technology on Tuberculosis (INCT TB)   (Brazil)

Author keywords

Drug development; H D exchange; Mass spectrometry; Shikimate kinase; Tuberculosis

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; PHOSPHOTRANSFERASE; RECOMBINANT ENZYME; SHIKIMATE KINASE; SHIKIMIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME STRUCTURE; HIGH TEMPERATURE; MYCOBACTERIUM TUBERCULOSIS; NUCLEOTIDE BINDING SITE; PROTEIN DOMAIN; TEMPERATURE DEPENDENCE;

AMINO ACID SEQUENCE; ANTITUBERCULAR AGENTS; DEUTERIUM EXCHANGE MEASUREMENT; DEUTERIUM OXIDE; ENZYME INHIBITORS; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TEMPERATURE; TUBERCULOSIS;

EID: 79952800036     PISSN: 09298673     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986711795029500     Document Type: Article

References (108)

1. World Health Organization. Global tuberculosis control: A short update to the 2009 report, Geneva, Switzerland, WHO /HTM/TB/2009.426.
2. Levin, B. R.; Rozen, D. E. Non-inherited antibiotic resistance. Nat. Rev. Microbiol. 2006, 4, 556-562. (Pubitemid 43905615)
3. White, M. J.; Hongjun, H.; Penoske, R.M.; Twining, S.S.; Zahrt, T.C. PepD participates in the Mycobacterial stress response mediated through MprAB and SigE. J. Bacteriol., 2010, 192, 1498-1510.
4. James P.E.; Grinberg O.Y.; Michaels G.; Swartz H.M. Intraphagosomal oxygen in stimulated macrophages. J. Cell. Physiol. 1995, 163, 241-247.
5. Cui, T.; Zhang, L.; Wang, X.; He, Z. Uncovering new signaling proteins and potential drug targets through the interactome analysis of Mycobacterium tuberculosis. BMC Genomics, 2009, 10, 118.
6. Weinstein, E. A.; Yano, T. Li, L.S.; Avarbock, D.; Avarbock, A.; Helm, D.; McColm, A. A.; Duncan, K.; Lonsdale, J. T.; Rubin, H. Inhibitors of type II NADH:menaquinone oxidoreductase represent a class of antitubercular drugs. PNAS, 2005, 102, 4548-4553. (Pubitemid 40397149)
7. Briken, V.; Miller, J. L. Living on the edge: Inhibition of host cell apoptosis by Mycobacterium tuberculosis. Future Microbiol., 2008, 3, 415-422.
8. World Health Organization. Global Tuberculosis Control; WHO Report 2001, Geneva, Switzerland, WHO/CDS/TB/2001.287.
9. Pereira, J. H.; Canduri, F.; Oliveira, J. S.; Silveira, N. J. F.; Basso, L. A.; Palma, M. S.; Santos, D.S. Structural bioinformatics study of EPSP synthase from Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun., 2003, 312, 608-614. (Pubitemid 37468214)
10. Marques, M.R.; Vaso, A.; Ruggiero-Neto, J.; Fossey, M.A.; Oliveira, J.S.; Basso, L.A.; dos Santos, D.S.; de Azevedo Junior, W.F. ; Palma, M.S. Dynamics of glyphosate-induced conformational changes of Mycobacterium tuberculosis 5-enolpyruvylshikimate-3-phosphate synthase (EC 2.5.1.19) determined by hydrogen/deuterium exchange and electrospray mass spectrometry. Biochemistry, 2008, 47, 7508-7522.
11. Marques, M. R.; Pereira, J.H.; Oliveira, J. S.; Basso, L. A.; Santos, D. S.; Palma, M. S. The inhibition of 5-enolpyruvylshikimate-3-phosphate synthase as a model for development of novel antimicrobials. Curr. Drug Targets, 2007, 8 , 445-457. (Pubitemid 46381295)
12. Roberts, F.; Roberts, C. W.; Johnson, J. J.; Kyle, D. E.; Krell, T.; Coggins, J. R.; Coombs, G. H.; Milhous, W. K.; Tzipori, S.; Ferguson, D. J. P.; Chakrabarti, D. and McLeod, R. Evidence for the shikimate pathway in apicomplexan parasites. Nature, 1998, 393, 801-805. (Pubitemid 28299493)
13. Koul, S.; Somayajulu, A.; Advani, M.J.; Reddy, H. A novel calcium binding protein in Mycobacterium tuberculosis- potential target for trifluoperazine. Indian J. Exp. Biol., 2009, 47, 480-488.
14. Petrelli, R.; Sham, Y. Y.; Chen, L.; Felczak, K.; Bennett, E.; Wilson, D.; Aldrich, C.; Yu, J. S.; Cappellacci, L.; Franchetti, P.; Grifantini, M.; Mazzola, F.; Di Stefano, M.; Magni, G.; Pankiewicz, K. W. Selective inhibition of nicotinamide adenine dinucleotide kinases by dinucleoside disulfide mimics of nicotinamide adenine dinucleotide analogues. Bioorg. Med. Chem., 2009, 17 , 5656-64.
15. Carvalho, L. P. S; Frantom, P. A.; Argyrou, A.; Blanchard, J. S. Kinetic evidence for interdomain communication in the allosteric regulation of β- isopropylmalate synthase from Mycobacterium tuberculosis. Biochemistry, 2009, 48, 1996-2004.
16. Kumar, P.; Chhibber, M.; Surolia, A. How pantothenol intervenes in Coenzyme- A biosynthesis of Mycobacterium tuberculosis. Biochem Biophys. Res. Commun., 2007, 361, 903-909. (Pubitemid 47259024)
17. Wooff, E.; Michell, S. L.; Gordon, S. V.; Chambers, M. A.; Bardarov, S.; Jacobs, W. R.; Hewinson, R. G.; Wheeler, P. R. Functional genomics reveals the sole sulphate transporter of the Mycobacterium tuberculosis complex and its relevance to the acquisition of sulphur in vivo. Mol. Microbiol., 2002, 43, 653-63. (Pubitemid 34597260)
18. Pochet, S.; Dugue, L.; Douguet, D.; Labesse, G.; Munier-Lehmann, H. Nucleoside analogues as inhibitors of thymidylate kinases: Possible therapeutic applications. Chembiochem., 2002, 3, 108-110. (Pubitemid 34464803)
19. Van Daele, I.; Munier-Lehmann, H.; Froeyen, M.; Balzarini, J.; Van Calenbergh, S. Rational design of 5'-thiourea-substituted alpha-thymidine analogues as thymidine monophosphate kinase inhibitors capable of inhibiting mycobacterial growth. J. Med. Chem., 2007, 50 , 5281-92. (Pubitemid 350057840)
20. Lin, T. W.; Melgar, M. M.; Kurth, D.; Swamidass, S. J.; Purdon, J.; Tseng, T.; Gago, G.; Baldi, P.; Gramajo, H.; Tsai, S. C. Structure-based inhibitor design of AccD5, an essential acyl-CoA carboxylase carboxyltransferase domain of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A., 2006, 103 , 3072-3077. (Pubitemid 43346426)
21. Young, P. G.; Smith, C. A.; Metcalf, P.; Baker, E. N. Structures of Mycobacterium tuberculosis folylpolyglutamate synthase complexed with ADP and AMPPCP. Acta Crystallogr. D Biol. Crystallogr., 2008, D64, 745-53. (Pubitemid 351872054)
22. Janowski, R.; Kefala, G.; Weiss, M. S. The structure of dihydrodipicolinate reductase (DapB) from Mycobacterium tuberculosis in three crystal forms. Acta Crystallogr. D Biol. Crystallogr., 2010, 66, 61-72.
23. Mitsakos, V.; Dobson, R. C.; Pearce, F. G.; Devenish, S. R.; Evans, G. L.; Burgess, B. R.; Perugini, M. A.; Gerrard, J. A.; Hutton, C. A. Inhibiting dihydrodipicolinate synthase across species: Towards specificity for pathogens? Bioorg. Med. Chem. Lett., 2008, 18, 842 844.
24. Chalut, C.; Botella, L.; de Sousa-D'Auria, C.; Houssin, C.; Guilhot, C. The nonredundant roles of two 4'-phosphopantetheinyl transferases in vital processes of Mycobacteria. PNAS, 2006, 103, 8511-8516. (Pubitemid 43838486)
25. Foley, T. L.; Young, B. S.; Burkart, M. D. Phosphopantetheinyl transferase inhibition and secondary metabolism. FEBS J., 2009, 276, 7134-7145.
26. McGrath Jr, H.; Rigby, P. G. Hepcidin: Inflammation's iron curtain. Rheumatology, 2004, 43, 1323-1325. (Pubitemid 39480917)
27. Wei, C.-J.; Lei, B.; Musser, J. M.; Tu, S.-C. Isoniazid activation defects in recombinant Mycobacterium tuberculosis catalase-peroxidase (KatG) mutants evident in InhA inhibitor production. Antimicrob. Agents Chemother., 2003, 47, 670-675. (Pubitemid 36158099)
28. Sun, Z.; Scorpio, A.; Zhang, Y. The pncA gene from naturally pyrazinamideresistant Mycobacterium avium encodes pyrazinamidase and confers pyrazinamide susceptibility to resistant M. tuberculosis complex organisms. Microbiology, 1997, 143, 3367-3373. (Pubitemid 27470186)
29. Yang, X.; Dubnau, E.; Smith, I.; Sampson, N. S. Rv1106c is a 3β- hydroxysteroid dehydrogenase. Biochemistry, 2007, 46(31), 9058-9067.
30. Brown, A. K.; Papaemmanouil, A.; Bhowruth, V.; Bhatt, A.; Dover, L. G.; Besra, G. S. Flavonoid inhibitors as novel antimycobacterial agents targeting Rv0636, a putative dehydratase enzyme involved in Mycobacterium tuberculosis fatty acid synthase II. Microbiology, 2007, 153, 3314-3322. (Pubitemid 47629537)
31. Ma, Y.; Stern, R. J.; Scherman, M. S.; Vissa, V. D.; Yan, W.; Jones, V. C.; Zhang, F.; Franzblau, S. G.; Lewis, W. H.; McNeil, M. R. 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., 2001, 45, 1407-1416. (Pubitemid 32374110)
32. Dayan, F. E.; Ferreira, D.; Wang, Y.-H.; Khan, I. A.; McInroy, J. A.; Pan, Z. A pathogenic fungi diphenyl ether phytotoxin targets plant enoyl (acyl carrier protein) reductase. Plant Physiol., 2008, 147, 1062-1071. (Pubitemid 352844262)
33. Camus, J. C.; Pryor, M. J.; Medigue, C.; Cole, S. T. Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology, 2002, 148, 2967-2973. (Pubitemid 35243696)
34. Russell, A. D. Whither triclosan? J. Antimicrob. Chemother., 2004, 53, 693-695. (Pubitemid 38660266)
35. Gu, Y.; Reshetnikova, L.; Li, Y.; Wu, Y; Yan, H.; Singh, S.; Ji, X. Crystal structure of shikimate kinase from Mycobacterium tuberculosis reveals the dynamic role of the LID domain in catalysis. J. Mol. Biol. 2002, 319, 779-789. (Pubitemid 34729450)
36. Romanowski, M. J.; Burley, S. K. Crystal structure of the Escherichia coli shikimate kinase I (AroK) that confers sensitivity to mecillinam. Proteins Struct. Funct. Bioinf., 2002, 47, 558-562. (Pubitemid 34614736)
37. Bentley, R. The shikimate pathway- A metabolic tree with many branches. Crit. Rev. Biochem. Mol. Biol., 1990, 25, 307-384. (Pubitemid 120012279)
38. Haslam, E. J. Shikimic Acid: Metabolism and Metabolites. Wiley and Sons: Chichester, 1993.
39. Herrmann, K. M. The shikimate pathway: Early steps in the biosynthesis of aromatic compounds. Plant Cell, 1995, 7, 907-919.
40. Cole, S. T.; Brosch, R.; Parkhill, J.; Garnier, T.; Churcher, C.;Harris, D.; Gordon, S. V.; Eiglmeier, K.; Gas, S.; Barry III, 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. and Barrell, B. G. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence Nature, 1998, 393, 537-544. (Pubitemid 28319235)
41. Oliveira, J. S.; Mendes, M. A.; Palma, M. S.; Basso, L. A. and Santos, D. S. One-step purification of 5-enolpyruvylshikimate-3-phosphate synthase enzyme from Mycobaterium tuberculosis. Prot. Expres. Purif., 2003, 28, 287-292. (Pubitemid 36562419)
42. McDevitt, D.; Payne, D. J.; Holmes, D. J.; Rosenberg, M. Novel targets for the future development of antibacterial agents. J. Appl. Microbiol., 2002, 92, 28S-34S. (Pubitemid 34535503)
43. McArthur, J. D.; West, N. P.; Cole, J. N.; Jungnitz, H.; Guzman, C. A.; Chin, J.; Lehrbach, P. R.; Djordjevic, S. P.; and Walker, M. J. An aromatic amino acid auxotrophic mutant of Bordetella bronchiseptica is attenuated and immunogenic in a mouse model of infection. FEMS Microbiol. Lett., 2003, 221, 7-16. (Pubitemid 36407746)
44. Parish, T.; Stroker, N. G. The common aromatic amino acid biosynthesis pathway is essential in Mycobacterium tuberculosis. Microbiology, 2002, 148, 3069-3077. (Pubitemid 35243706)
45. Dieckmann, A.; Jung, A. Stage-specific sensitivity of Plasmodium falciparum to antifolates. Mol. Biochem. Parasitol., 1986, 19, 143-147. (Pubitemid 16076528)
46. Rogers, M. J.; Cundliffe, E.; McCutchan, T. F. The antibiotic micrococcin is a potent inhibitor of growth and protein synthesis in the malaria parasite. Antimicrob. Agents Chemother., 1998, 42, 715-716. (Pubitemid 28114837)
47. McConkey, G.A.; Rogers, M.J.; McCutchan, T.F. Inhibition of Plasmodium falciparum protein synthesis: Targeting the plastid-like organelle with thiostrepton. J. Biol. Chem., 1997, 272, 2046-2049. (Pubitemid 27058476)
48. Fichera, M. E. and Roos, D. S. A plastid organelle as a drug target in apicomplexan parasites. Nature, 1997, 390,407-409. (Pubitemid 28027322)
49. Köhler, S.; Delwiche, C. F.; Denny, P. W.; Tilney, L. G.; Webster, P.; Wilson, R. J.; Palmer, J. D.; Roos, D. S. A plastid of probable green algal origin in Apicomplexan parasites. Science, 1997, 275 , 1485-1489. (Pubitemid 27111298)
50. McConkey, G.A. Targeting the shikimate pathway in the malaria parasite Plasmodium falciparum. Antimicrob. Agents and Chemother., 1999, 43, 175-177.
51. Priestman, M.A.; Healy, M.L.; Becker, A.; Alberg, D.G.; Bartlett, P;A.; Lushington, G.H.; Schönbrunn, E. Interaction of phosphonate analogues of the tetrahedral reaction intermediate with 5-enolpyruvylshikimate-3- phosphate synthase in atomic detail. Biochemistry, 2005, 44, 3241-3248. (Pubitemid 40321995)
52. Kishore, G. M.; Shah, D. M. Amino acids biosynthesis inhibitors as pesticides. Ann. Rev. Biochem., 1998, 27, 627-663.
53. Han, C.; Zhang, J.; Chen, L.; Chen, K.; Shen, X.; Jiang, H. Discovery of Helicobacter pylori shikimate kinase inhibitors: Bioassay and molecular modeling Bioorg. Med. Chem. 2007, 15, 656-662. (Pubitemid 44895506)
54. Cheng, W. C.; Chang, Y. N.; Wang, W. C. Structural basis for shikimatebinding specificity of Helicobacter pylori shikimate kinase. J. Bacteriol., 2005, 187, 8156-8163.
55. Krell, T.; Coggins, J. R.; Lapthorn, A. J. The three-dimensional structure of shikimate kinase. J. Mol. Biol., 1998, 278, 983-997. (Pubitemid 28239699)
56. Gan, J.; Gu, Y.; Li, Y.; Yan, H.; Ji, X. Crystal structure of Mycobacterium tuberculosis shikimate kinase in complex with shikimic acid and an ATP analogue. Biochemistry, 2006, 45, 8539-8545. (Pubitemid 44078873)
57. Vonrhein, C.; Schlauderer, G.J.; Schulz, G. E. Movie of the structural changes during a catalytic cycle of nucleoside monophosphate kinases. Structure. 1995, 3 , 483-490.
58. Walker, J. E.; Saraste, M.; Runswick, M. J.; Gay, N. J. Distantly related sequences in the alpha- And beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J., 1982, 1 , 945-951.
59. De Azevedo, W. F. Jr; Canduri, F.; de Oliveira, J. S.; Basso, L. A.; Palma, M. S.; Pereira, J. H.; Santos, D. S. Molecular model of shikimate kinase from Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun., 2002, 295, 142-148. (Pubitemid 34743789)
60. Pereira, J. H.; de Oliveira, J. S.; Canduri, F.; Dias, M. V.; Palma, M. S.; Basso, L. A.; Santos, D. S.; de Azevedo, W. F. Jr. Structure of shikimate kinase from Mycobacterium tuberculosis reveals the binding of shikimic acid. Acta Crystallogr D Biol Crystallogr., 2004, 60, 2310-2319. (Pubitemid 41327648)
61. Hartmann, M.D.; Bourenkov, G.P.; Obershal, A.; Strizhov, N.; Bartunik, H.D. Mechanism of phosphoryl transfer catalyzed by shikimate kinase from Mycobacterium tuberculosis. J. Mol. Biol., 2006, 364, 411-423. (Pubitemid 44780995)
62. Jardetzky, O. Protein dynamics and conformational transitions in allosteric proteins. Prog. Biophys. Mol. Biol., 1996, 65, 171-219. (Pubitemid 27164026)
63. Haurowitz, F. Das gleichgewicht swischen htimoglobin und sauerstoff. Hoppe-Seyler's Z. Physiol. Chem., 1938, 254, 266-274.
64. Perutz, M. F. Proteins and Nucleic Acids; Elsevier: Amsterdam, 1962.
65. Kim, H. W.; Shen, T. J.; Sun, D. P.; Ho, N. T.; Madrid, M.; Chien, H. A novel low oxygen affinity recombinant hemoglobin (ct96Val~Trp): Switching quaternary structure without changing the ligation state. J. Mol. Biol., 1995, 248, 867-882.
66. Holt, J. M.; Ackers, G. K. The pathway of allosteric control as revealed by hemoglobin intermediate states. Fedn Am. Socs Exp. Biol. J., 1995, 9, 210-218.
67. Linderstrøm-Lang, K. Deuterium exchange between peptides and water. Chem. Soc. Spec. Publ., 1955, 2, 1-20.
68. Hvidt, A.; Nielsen, S. O. Hydrogen exchange in proteins. Adv. Prot. Chem., 1966, 21, 287-386.
69. Jardetzky, O.; Jardetzky, C. D. In Methods of biochemical analysis, Glick, D., Ed. Interscience: NY, IX, pp. 235-410, 1962.
70. Jardetzky, O. Magnetic resonance in biological systems. Science, 1964, 146, 552-553.
71. Jardetzky, O.; Wade-Jardetzky, N. G. On the mechanism of the binding of sulfonamides to bovine serum albumin. Mol. Pharmacol., 1965, 1, 214-230.
72. Campbell, I. D.; Dobson, C. M.; Moore, G. R.; Perkins, S. J.; Williams, R. J. P. Temperature dependent molecular motion of a tyrosine residue of ferrocytochrome C. Fedn. Eur. Biochem. Socs Lett., 1976, 70, 96-101.
73. Jardetzky, O.; Akasaka, K.; Vogel, D.; Morris, S.; Holmes, K. C. Unusual segmental flexibility in a region of tobacco mosaic virus coat protein. Nature, 1978, 273, 564-566. (Pubitemid 8346596)
74. Wade-Jardetzky, N.; Bray, R.P.; Conover, W. W.; Jardetzky, O.; Geisler, N.; Weber, K. Differential mobility of the N-terminal headpiece in the lacrepressor protein. J. Mol. Biol. 1979, 128, 259-264.
75. Anderegg, R.; Wagner, D. Mass spectrometric characterization of proteinligand interaction. J. Am. Chem. Soc. 1995, 117, 1374-1377.
76. Remigy, H.; Jaquinod, M.; Petillot, Y.; Gagnon, J.; Cheng, H.; Xia, B.; Markley, J. L.; Hurley, J. K.; Tollin, G.; Forest, E. Probing the influence of mutations on the stability of a ferredoxin by mass spectrometry. J. Prot. Chem. 1997, 16, 527-532. (Pubitemid 27306559)
77. Chalmers, M. J.; Busby, S. A.; Pascal, B. D.; He, Y.; Hendrickson, C. L.; Marshall, A. G.; Griffin, P. R. Probing protein ligand interactions by automated hydrogen/deuterium exchange mass spectrometry. Anal. Chem., 2006, 78, 1005-1014. (Pubitemid 43271829)
78. Englander, J. J. ; Del Mar, C.; Li, W.; Englander, S. W.; Kim, J. S.; Stranz, D. D.; Hamuro, Y.; Woods Jr., V. L. Protein structure change studied by hydrogen- deuterium exchange, functional labeling, and mass spectrometry. PNAS, 2003, 100 , 7057-7062. (Pubitemid 36706392)
79. Kim,M-Y.; Maier, C. S.; Reed, D. J.; Deinzer, M. L. Site-specific amide hydrogen/deuterium exchange in E. coli thioredoxins measured by electrospray ionization mass spectrometry. J. Am. Chem. Soc., 2001, 123, 9860-9866. (Pubitemid 32929393)
80. Engen, J. R.; Smith, D. L. Investigating the higher order structure of proteins. Hydrogen exchange, proteolytic fragmentation, and mass spectrometry. Methods Mol. Biol., 2000, 146, 95-112.
81. Dharmasiri, K.; Smith, D. L. Mass spectrometric determination of isotopic exchange rates of amide hydrogens located on the surface of proteins. J. Am. Soc. Mass. Spectrom., 1997, 8, 1039-1045.
82. Shi, J. S.; Koeppe, J. R.; Komives, E. A.; Paylor, P. Ligand-induced conformational changes in the acetylcholinebinding protein analyzed by hydrogendeuterium exchange mass spectrometry. J. Biol. Chem., 2006, 281, 12170-12177. (Pubitemid 43855481)
83. Wales, T. E.; Engen, J. R. Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spec. Rev., 2006, 25, 158-170.
84. Zhang, Z.; Smith, D.L. Thermal-induced unfolding domains in aldolase identified by amide hydrogen exchange and mass spectrometry. Protein Sci., 1996, 5 , 1282-1289. (Pubitemid 26239436)
85. Neri, D.; Billeter, M.; Wider, G.; Wuthrich, K. NMR determination of residual structure in a urea-denatured protein, the 434-repressor. Science, 1992, 257, 1559-1563.
86. Kim, K. S.; Woodward, C. Protein internal flexibility and global stability: Effect of urea on hydrogen exchange rates of bovine pancreatic trypsin inhibitor. Biochemistry, 1993, 32, 9609-9013.
87. Loh, S. N.; Prehoda, K. E.; Wang, J.; Markley, J. L. Hydrogen exchange in unligated and ligated staphylococcal nuclease. Biochemistry. 1993, 32, 11022-8. (Pubitemid 23332008)
88. Mayo, S. L.; Baldwin, R. L. Guanidinium chloride induction of partial unfolding in amide proton exchange in RNase A. Science, 1993, 262, 873-876. (Pubitemid 24014074)
89. Bai, Y.; Milne, J. S.; Mayne, L.; Englander, S. W. Protein stability parameters measured by hydrogen exchange. Proteins, 1994, 20, 1775-86.
90. Bai, Y; Sosnick, T.R; Mayne, L; Englander, S.W. Protein folding intermediates: Native-state hydrogen exchange. Science, 1995, 269, 192-197.
91. Buck, M.; Radford, S. E.; Dobson, C. M. Amide hydrogen exchange in a highly denatured state: Hen egg-white lysozyme in urea. J. Mol. Biol., 1994, 237, 247-254.
92. Elove, G. A.; Bhuyan, A. K.; Roder, H. Kinetic mechanism of cytochrome c folding: Involvement of the heme and its ligands. Biochemistry, 1994, 33, 6925-6935. (Pubitemid 24190817)
93. Ray J.; Englander, S. W. Allosteric sensitivity in hemoglobin at the alphasubunit N-terminus studied by hydrogen exchange. Biochemistry, 1986, 25, 3000-3007. (Pubitemid 16073837)
94. Louie G.; Tran, T.; Englander, J. J.; Englander, S. W. Allosteric energy at the hemoglobin beta chain C-terminus studied by hydrogen exchange. J. Mol. Biol., 1988, 201, 755-64.
95. Englander, S. W.; Englander, J. J.; McKinnie, R. E.; Ackers, G. K.; Turner, G. J.; Westrick, J. A.; Gill, S. J. Hydrogen exchange measurement of the free energy of structural and allosteric change in hemoglobin. Science, 1992, 256, 1684-1687.
96. Roder, H.; Wagner, G.; Wuethrich, K. Individual amide proton exchange rates in thermally unfolded basic pancreatic trypsin inhibitor. Biochemistry, 1985, 24 , 7407-7411. (Pubitemid 16165358)
97. Roder, H.; Wagner, G.; Wuethrich, K. Amide proton exchange in proteins by EX1 kinetics: Studies of the basic pancreatic trypsin inhibitor at variable p2H and temperature. Biochemistry, 1985, 24, 7396-407. (Pubitemid 16165357)
98. Robertson, A. D.; Baldwin R. L. Hydrogen exchange in thermally denatured ribonuclease A. Biochemistry, 1991, 30, 9907-14.
99. Liang, Z.X.; Lee, T.; Resing, K. A.; Ahn, N. G.; Klinman, J. P. Thermalactivated protein mobility and its correlation with catalysis in thermophilic alcohol dehydrogenase. PNAS, 2004, 101, 9556-9561. (Pubitemid 38869274)
100. Valentine S. J.; Clemmer D.E. Temperature-dependent H/D exchange of compact and elongated cytochrome C ions in the gas phase. J. Am. Soc. Mass Spec., 2002, 13, 506-517. (Pubitemid 36870945)
101. Durazo A.; Shaw, B. F.; Chattopadhyay, M.; Faull, K. F.; Nersissian, A. M.; Valentine, J. S.; Whitelegge, J. P. Metal-free superoxide dismutase-1 and three different amyotrophic lateral sclerosis variants share a similar partially unfolded beta-barrel at physiological temperature. J. Biol. Chem., 2009, 284, 34382-34389.
102. Oliveira, J. S.; Pinto, C. A.; Basso, L. A.; Santos, D. S. Cloning and overexpression in soluble form of functional shikimate kinase and 5- enolpyruvylshikimate 3- phosphate synthase enzymes from Mycobacterius tuberculosis. Protein Expr. Purif., 2001, 22, 430-435. (Pubitemid 32745334)
103. Zhang, Z.; Smith, D. L. Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation. Protein Sci., 1993, 2 , 522-531. (Pubitemid 23119303)
104. Wintrode, P. L.; Friedrich, K. L.; Vierling, E.; Smith, J. B.; Smith, D. L. Solution structure and dynamics of a heat shock protein assembly probed by hydrogen exchange and mass spectrometry. Biochemistry, 2003, 42, 10667-10673. (Pubitemid 37102106)
105. Tsutsui, Y.; Liu, L.; Gershenson, A.; Wintrode, P. L. The conformational dynamics of a metastable serpin studied by hydrogen exchange and mass spectrometry. Biochemistry, 2006, 45, 6561-6569. (Pubitemid 43825356)
106. Kraulis, P. J. Molscript: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 1991, 24, 946-950.
107. Yan, X.; Broderick, D.; Leid, M. E.; Schmerlik, M. I.; Deizer, M. L. Dynamics and Ligand-Induced Solvent AccessibilityChanges in Human Retinoid X Receptor Homodimer determined by Hydrogen Deuterium Exchange and from Mycobacterium tuberculosis Mass Spectrometry. Biochemistry 2004, 43, 909-917. (Pubitemid 38141488)
108. Pereira, J.H.; Vasconcelos, I.B.; Oliveira, J.S.; Caceres, R.A.; de Azevedo Jr., W.F.; Basso, L.A.; Santos, D.S. Shikimate kinase: A potential target for development of novel antitubercular agents. Curr. Drug Targets, 2007; 8, 459-468. (Pubitemid 46381296)