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Carbohydrate recognition by RpfB from mycobacterium tuberculosis unveiled by crystallographic and molecular dynamics analyses (119 visite)

Squeglia F, Romanò MF, Ruggiero A, Vitagliano L, De Simone A, Berisio R

Biophysical Journal (ISSN: 0006-3495, 1542-0086), 2013 Jun 4; 104(11): 2530-2539.

Tipo di articolo: Journal Article, Research Support, Non-U. S. Gov'T, , Impact factor: 3.832, Impact factor a 5 anni: 3.976, Url: http://www.scopus.com/inward/record.url?eid=2-s2.0-84878888480&partnerID=40&md5=93c71840b30a03cea23bc0a2dd9fc524

Parole chiave: Bacterial Protein, Enzyme Inhibitor, Ligand, Article, Carbohydrate Metabolism, Chemistry, Drug Antagonism, Enzyme Active Site, Molecular Dynamics, Mycobacterium Tuberculosis, Protein Binding, X Ray Crystallography, Catalytic Domain, X-Ray, Molecular Dynamics Simulation, Bacterial Proteins Antagonists, Inhibitors Chemistry Metabolism, Enzyme Inhibitors Metabolism,

Affiliazioni: *** IBB - CNR ***
Institute of Biostructures and Bioimaging, C.N.R., Naples, Italy
Department of Chemistry, University of Naples Federico II, Napoli, Italy
Seconda Università di Napoli, Caserta, Italy
Division of Molecular Biosciences, Imperial College London, United Kingdom
Seconda Universit di Napoli, Caserta, Italy


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Kaufmann, S.H., McMichael, A.J., Annulling a dangerous liaison: Vaccination strategies against AIDS and tuberculosis (2005) Nat. Med., 11 (SUPPL. 4), pp. 33-S44

Kell, D.B., Young, M., Bacterial dormancy and culturability: The role of autocrine growth factors (2000) Curr. Opin. Microbiol., 3, pp. 238-243

Squeglia, F., Marchetti, R., Silipo, A., Chemical basis of peptidoglycan discrimination by PrkC, a key kinase involved in bacterial resuscitation from dormancy (2011) J. Am. Chem. Soc., 133, pp. 20676-20679

Ruggiero, A., Marasco, D., Berisio, R., Structure and functional regulation of RipA, a mycobacterial enzyme essential for daughter cell separation (2010) Structure, 18, pp. 1184-1190

Ruggiero, A., Squeglia, F., Berisio, R., X-ray structural studies of the entire extracellular region of the serine/threonine kinase PrkC from Staphylococcus aureus (2011) Biochem. J., 435, pp. 33-41

Mukamolova, G.V., Turapov, O.A., Young, M., A family of autocrine growth factors in Mycobacterium tuberculosis (2002) Mol. Microbiol., 46, pp. 623-635

Cole, S.T., Brosch, R., Barrell, B.G., Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence (1998) Nature, 393, pp. 537-544

Tufariello, J.M., Mi, K., Chan, J., Deletion of the Mycobacterium tuberculosis resuscitation-promoting factor Rv1009 gene results in delayed reactivation from chronic tuberculosis (2006) Infect. Immun., 74, pp. 2985-2995

Ruggiero, A., Tizzano, B., Berisio, R., Crystal structure of the resuscitation-promoting factor (DeltaDUF)RpfB from M. tuberculosis (2009) J. Mol. Biol., 385, pp. 153-162

Cohen-Gonsaud, M., Barthe, P., Keep, N.H., The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes (2005) Nat. Struct. Mol. Biol., 12, pp. 270-273

Ruggiero, A., Marchant, J., Berisio, R., Molecular determinants of inactivation of the resuscitation promoting factor B from Mycobacterium tuberculosis (2013) J. Biomol. Struct. Dyn., 31, pp. 195-205

Phillips, D.C., The hen egg white lysozyme molecule (1967) Proc. Natl. Acad. Sci. USA, 57, pp. 483-495

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Vocadlo, D.J., Davies, G.J., Withers, S.G., Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate (2001) Nature, 412, pp. 835-838

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Morris, R.J., Perrakis, A., Lamzin, V.S., ARP/wARP and automatic interpretation of protein electron density maps (2003) Methods Enzymol., 374, pp. 229-244

Kirschner, K.N., Yongye, A.B., Woods, R.J., GLYCAM06: A generalizable biomolecular force field. Carbohydrates (2008) J. Comput. Chem., 29, pp. 622-655

Berisio, R., Vitagliano, L., Polyproline and triple helix motifs in host-pathogen recognition (2012) Curr. Protein Pept. Sci., 13, pp. 855-865

Vitagliano, L., Berisio, R., De Simone, A., Role of hydration in collagen recognition by bacterial adhesins (2011) Biophys. J., 100, pp. 2253-2261

De Simone, A., Vitagliano, L., Berisio, R., Role of hydration in collagen triple helix stabilization (2008) Biochem. Biophys. Res. Commun., 372, pp. 121-125

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Peric-Hassler, L., Hansen, H.S., Hünenberger, P.H., Conformational properties of glucose-based disaccharides investigated using molecular dynamics simulations with local elevation umbrella sampling (2010) Carbohydr. Res., 345, pp. 1781-1801

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Ruggiero, A., De Simone, P., Berisio, R., Bacterial cell division regulation by Ser/Thr kinases: A structural perspective (2012) Curr. Protein Pept. Sci., 13, pp. 756-766

Fernandez-Alonso, M.D., Diaz, D., Jimenez-Barbero, J., Protein-carbohydrate interactions studied by NMR: From molecular recognition to drug design (2012) Curr. Protein Pept. Sci., 13, pp. 816-830

Asensio, J.L., Arda, A., Jimenez-Barbero, J., Carbohydrate-aromatic interactions (2013) Acc. Chem. Res., 46, pp. 946-954

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Sterpone, F., Stirnemann, G., Laage, D., Magnitude and molecular origin of water slowdown next to a protein (2012) J. Am. Chem. Soc., 134, pp. 4116-4119

Bianco, V., Iskrov, S., Franzese, G., Understanding the role of hydrogen bonds in water dynamics and protein stability (2012) J. Biol. Phys., 38, pp. 27-48

Mazza, M.G., Stokely, K., Franzese, G., More than one dynamic crossover in protein hydration water (2011) Proc. Natl. Acad. Sci. USA, 108, pp. 19873-19878

Sharma, S., Debenedetti, P.G., Evaporation rate of water in hydrophobic confinement (2012) Proc. Natl. Acad. Sci. USA, 109, pp. 4365-4370

Hirakawa, H., Ochi, A., Kuhara, S., Catalytic reaction mechanism of goose egg-white lysozyme by molecular modelling of enzyme-substrate complex (2008) J. Biochem., 144, pp. 753-761

Meroueh, S.O., Bencze, K.Z., Mobashery, S., Three-dimensional structure of the bacterial cell wall peptidoglycan (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 4404-4409

Tufariello, J.M., Jacobs, Jr.W.R., Chan, J., Individual Mycobacterium tuberculosis resuscitation-promoting factor homologues are dispensable for growth in vitro and in vivo (2004) Infect. Immun., 72, pp. 515-526

Kana, B.D., Gordhan, B.G., Mizrahi, V., The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro (2008) Mol. Microbiol., 67, pp. 672-684

Venditti, V., Bernini, A., Niccolai, N., MD and NMR studies of alpha-bungarotoxin surface accessibility (2007) Biochem. Biophys. Res. Commun., 356, pp. 114-117

Biedermann, F., Uzunova, V.D., De Simone, A., Release of high-energy water as an essential driving force for the high-affinity binding of cucurbit[n]urils (2012) J. Am. Chem. Soc., 134, pp. 15318-15323

Perić-Hassler, L., Hansen, H.S., Hünenberger, P.H., Conformational properties of glucose-based disaccharides investigated using molecular dynamics simulations with local elevation umbrella sampling (2010) Carbohydr. Res., 345, pp. 1781-1801

Velayati, A. A., Masjedi, M. R., Hoffner, S. E., Emergence of new forms of totally drug-resistant tuberculosis bacilli: Super extensively drug-resistant tuberculosis or totally drug-resistant strains in Iran (2009) Chest, 136, pp. 420-42

Migliori, G. B., De Iaco, G., Cirillo, D. M., First tuberculosis cases in Italy resistant to all tested drugs (2007) Euro. Surveill., 12. , E070517. 1

Kaufmann, S. H., McMichael, A. J., Annulling a dangerous liaison: Vaccination strategies against AIDS and tuberculosis (2005) Nat. Med., 11 (SUPPL. 4), pp. 33-S44

Kell, D. B., Young, M., Bacterial dormancy and culturability: The role of autocrine growth factors (2000) Curr. Opin. Microbiol., 3, pp. 238-243

Mukamolova, G. V., Turapov, O. A., Young, M., A family of autocrine growth factors in Mycobacterium tuberculosis (2002) Mol. Microbiol., 46, pp. 623-635

Cole, S. T., Brosch, R., Barrell, B. G., Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence (1998) Nature, 393, pp. 537-544

Tufariello, J. M., Mi, K., Chan, J., Deletion of the Mycobacterium tuberculosis resuscitation-promoting factor Rv1009 gene results in delayed reactivation from chronic tuberculosis (2006) Infect. Immun., 74, pp. 2985-2995

Phillips, D. C., The hen egg white lysozyme molecule (1967) Proc. Natl. Acad. Sci. USA, 57, pp. 483-495

Koshland, D. E., Stereochemistry and mechanism of enzymatic reactions (1953) Biol. Rev. Camb. Philos. Soc., 28, pp. 416-436

Vocadlo, D. J., Davies, G. J., Withers, S. G., Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate (2001) Nature, 412, pp. 835-838

Murshudov, G. N., Vagin, A. A., Dodson, E. J., Refinement of macromolecular structures by the maximum-likelihood method (1997) Acta Crystallogr. D Biol. Crystallogr., 53, pp. 240-255

Morris, R. J., Perrakis, A., Lamzin, V. S., ARP/wARP and automatic interpretation of protein electron density maps (2003) Methods Enzymol., 374, pp. 229-244

Kirschner, K. N., Yongye, A. B., Woods, R. J., GLYCAM06: A generalizable biomolecular force field. Carbohydrates (2008) J. Comput. Chem., 29, pp. 622-655

Laskowski, R. A., Macarthur, M. W., Thornton, J. M., PROCHECK: A program to check the stereochemical quality of protein structures (1993) J. Appl. Cryst., 26, pp. 283-291

Peri -Hassler, L., Hansen, H. S., H nenberger, P. H., Conformational properties of glucose-based disaccharides investigated using molecular dynamics simulations with local elevation umbrella sampling (2010) Carbohydr. Res., 345, pp. 1781-1801

Asensio, J. L., Arda, A., Jimenez-Barbero, J., Carbohydrate-aromatic interactions (2013) Acc. Chem. Res., 46, pp. 946-954

Mazza, M. G., Stokely, K., Franzese, G., More than one dynamic crossover in protein hydration water (2011) Proc. Natl. Acad. Sci. USA, 108, pp. 19873-19878

Meroueh, S. O., Bencze, K. Z., Mobashery, S., Three-dimensional structure of the bacterial cell wall peptidoglycan (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 4404-4409

Tufariello, J. M., Jacobs, Jr. W. R., Chan, J., Individual Mycobacterium tuberculosis resuscitation-promoting factor homologues are dispensable for growth in vitro and in vivo (2004) Infect. Immun., 72, pp. 515-526

Kana, B. D., Gordhan, B. G., Mizrahi, V., The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro (2008) Mol. Microbiol., 67, pp. 672-684



Resuscitation of Mtb is crucial to the etiology of Tuberculosis, because latent tuberculosis is estimated to affect one-third of the world population. The resuscitation-promoting factor RpfB is mainly responsible for Mtb resuscitation from dormancy. Given the impact of latent Tuberculosis, RpfB represents an interesting target for tuberculosis drug discovery. However, no molecular models of substrate binding and catalysis are hitherto available for this enzyme. Here, we identified key interactions involved in substrate binding to RpfB by combining x-ray diffraction studies and computational approaches. The crystal structure of RpfB catalytic domain in complex with N,N',N?- triacetyl-chitotriose, as described here, provides the first, to our knowledge, atomic representation of ligand recognition by RpfB and demonstrates that the strongest interactions are established by the N-acetylglucosamine moiety in the central region of the enzyme binding cleft. Molecular dynamics analyses provided information on the dynamic behavior of protein-substrate interactions and on the role played by the solvent in RpfB function. These data combined with sequence conservation analysis suggest that Glu-292 is the sole residue crucial for catalysis, implying that RpfB acts via the formation of an oxocarbenium ion rather than a covalent intermediate. Present data represent a solid base for the design of effective drug inhibitors of RpfB. Moreover, homology models were generated for the catalytic domains of all members of the Mtb Rpf family (RpfA-E). The analysis of these models unveiled analogies and differences among the different members of the Rpf protein family. © 2013 Biophysical Society.
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16 Records (14 escludendo Abstract e Conferenze).
Impact factor totale: 95.559 (90.25 escludendo Abstract e Conferenze).
Impact factor a 5 anni totale: 99.667 (93.829 escludendo Abstract e Conferenze).







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