Subtle functional collective motions in pancreatic-like ribonucleases: From ribonuclease A to angiogenin(386 views) Merlino A, Vitagliano L, Ceruso MA, Mazzarella L
Proteins (ISSN: 0887-3585, 1097-0134, 1097-0134electronic), 2003 Oct 1; 53(1): 101-110.
Dipartimento di Chimica, Univ. degli Studi Napoli Federico II, Napoli, Italy
Istituto di Biostrutture/Bioimmagini, CNR, Napoli, Italy
Dept. of Physiology and Biophysics, Mt. Sinai School of Medicine, One Gustave L. Levy Place, New York, NY, United States
References: Youle, R.J., D'Alessio, G., Antitumoral RNases (1997) Ribonuclease: Structures and Functiones, pp. 491-514. , Riordan JF, D'Alessio G, editors. San Diego, CA: Academic Pres
Blackburn, P., Moore, S., Pancreatic ribonuclease (1982) The Enzymes, pp. 317-433. , Boyer PD, editor. New York: Academic Press
Raines, R.T., Ribonuclease A (1998) Chem Rev, 98, pp. 1045-1065
Rasmussen, B.F., Stock, A.M., Ringe, D., Petsko, G.A., Crystalline ribonuclease A loses function below the dynamical transition at 220 K (1992) Nature, 357, pp. 423-424
Vitagliano, L., Merlino, A., Zagari, A., Mazzarella, L., Reversible substrate-induced domain motions in ribonuclease A (2002) Proteins, 46, pp. 97-104
Radha Kishan, K.V., Chandra, N.R., Sudarsanakumar, C., Suguna, K., Vijayan, M., Water-dependent domain motion and flexibility in ribonuclease A and the invariant features in its hydration shell. An X-ray study of two low-humidity crystal forms of the enzyme (1995) Acta Crystallogr D, 51, pp. 703-710
Sadasivan, C., Nagendra, H.G., Vijayan, M., Plasticity, hydration and accessibility in ribonuclease A. The structure of a new crystal form and its low-humidity variant (1998) Acta Crystallogr, 54, pp. 1343-1352
Berisio, R., Sica, F., Lamzin, V.S., Wilson, K.S., Zagari, A., Mazzarella, L., Atomic resolution of RNase A at six pH values (2002) Acta Crystallogr D, 58, pp. 441-450
Merlino, A., Vitagliano, L., Ceruso, M.A., Di Nola, A., Mazzarella, L., Global and local motions in ribonuclease A: A molecular dynamics study (2002) Biopolymers, 65, pp. 274-283
Leland, P.A., Schultz, L.W., Kim, B.M., Raines, R.T., Ribonuclease A variants with potent cytotoxic activity (1998) Proc Natl Acad Sci USA, 95, pp. 10407-10412
Klink, T.A., Raines, R.T., Conformational stability is a determinant of ribonuclease A cytotoxicity (2000) J Biol Chem, 275, pp. 17463-17467
Bretscher, L.E., Abel, R.L., Raines, R.T., A ribonuclease A variant with low catalytic activity but high cytotoxicity (2000) J Biol Chem, 275, pp. 9893-9896
Cafaro, V., De Lorenzo, C., Piccoli, R., Bracale, A., Mastronicola, M.R., Di Donato, A., D'Alessio, G., The antitumor action of seminal ribonuclease and its quaternary conformations (1995) FEBS Lett, 359, pp. 31-34
Saxena, S.K., Rybak, S.M., Davey R.T., Jr., Youle, R.J., Ackerman, E.J., Angiogenin is a cytotoxic, tRNA-specific ribonuclease in the RNase A superfamily (1992) J Biol Chem, 267, pp. 21982-21986
Matousek, J., Ribonucleases and their antitumor activity (2001) Comp Biochem Physiol C Toxicol Pharmacol, 129, pp. 175-191
Leland, P.A., Staniszewski, K.E., Park, C., Kelemen, B.R., Raines, R.T., The ribonucleolytic activity of angiogenin (2002) Biochemistry, 41, pp. 1343-1350
Acharya, K.R., Shapiro, R., Allen, S.C., Riordan, J.F., Vallee, B.L., Crystal structure of human angiogenin reveals the structural basis for its functional divergence from ribonuclease (1994) Proc Natl Acad Sci USA, 91, pp. 2915-2919
Shapiro, R., Riordan, J.F., Vallee, B.L., Characteristic ribonucleolytic activity of human angiogenin (1986) Biochemistry, 25, pp. 3527-3532
Russo, N., Acharya, K.R., Vallee, B.L., Shapiro, R., A combined kinetic and modeling study of the catalytic center subsites of human angiogenin (1996) Proc Natl Acad Sci USA, 93, pp. 804-808
Ceruso, M.A., Amadei, A., Di Nola, A., Mechanics and dynamics of B1 domain of protein G: Role of packing and surface hydrophobic residues (1999) Protein Sci, 8, pp. 147-160
Keskin, O., Jernigan, R.L., Bahar, I., Proteins with similar architecture exhibit similar large-scale dynamic behavior (2000) Biophys J, 78, pp. 2093-2106
Madhusudhan, M.S., Vishveshwara, S., Comparison of the dynamics of bovine and human angiogenin: A molecular dynamics study (1999) Biopolymers, 49, pp. 131-144
Leonidas, D.D., Shapiro, R., Allen, S.C., Subbarao, G.V., Veluraja, K., Acharya, K.R., Refined crystal structures of native human angiogenin and two active site variants: Implications for the unique functional properties of an enzyme involved in neovascularisation during tumour growth (1999) J Mol Biol, 285, pp. 1209-1233
Van der Spoel, D., Van Druner, R., Berendsen, H.J.C., (1994) GROningen MAchine for CHemical Simulation, , Department of Biophysical Chemistry. Groningen: Bioson Research Institute
Berendsen, H.J.C., Postma, J.P.M., Van Gusteren, W.F., Hermans, J., (1981) Interaction Models for Water in Relation to Protein Hydration, pp. 331-342. , Dordrecht: Reidel
Lequin, O., Thuring, H., Robin, M., Lallemand, J.Y., Three-dimensional solution structure of human angiogenin determined by 1H, 15N-NMR spectroscopy - Characterization of histidine protonation states and pKa values (1997) Eur J Biochem, 250, pp. 712-726
Darden, T., York, D., Pedersen, L., Part Mesh Ewald: A log (N) method for Ewald sums in large systems (1993) J Chem Phys, 98, pp. 10089-10092
Hess, B., Bekker, H., Berendsen, H.J.C., Freaje, J.G.E.M., LINCS: A linear constraint solver for molecular simulations (1997) J Comp Chem, 18, pp. 1463-1472
Garcia, A.E., Large-amplitude nonlinear motions in proteins (1992) Phys Rev Lett, 68, pp. 2696-2699
Amadei, A., Linssen, A.B., Berendsen, H.J.C., Essential dynamics of proteins (1993) Proteins, 17, pp. 412-425
Amadei, A., Ceruso, M.A., Di Nola, A., On the convergence of the conformational coordinates basis set obtained by the essential dynamics analysis of proteins' molecular dynamics simulations (1999) Proteins, 36, pp. 419-424
Van Aalten, D.M.F., Grotewold, E., Joshua-Tor, L., Essential dynamics from NMR clusters: Dynamic properties of the Myb DNA-binding domain and a hinge-bending enhancing variant (1998) Methods, 14, pp. 318-328
Abseher, R., Horstink, L., Hilbers, C.W., Nilges, M., Essential spaces defined by NMR structure ensembles and molecular dynamics simulation show significant overlap (1998) Proteins, 31, pp. 370-382
De Groot, B.L., Hayward, S., Van Aalten, D.M., Amadei, A., Berendsen, H.J.C., Domain motions in bacteriophage T4 lysozyme: A comparison between molecular dynamics and crystallographic data (1998) Proteins, 31, pp. 116-127
Van Aalten, D.M., Conn, D.A., De Groot, B.L., Berendsen, H.J., Findlay, J.B., Amadei, A., Protein dynamics derived from clusters of crystal structures (1997) Biophys J, 73, pp. 2891-2896
Santoro, J., Gonzalez, C., Bruix, M., Neira, J.L., Nieto, J.L., Herranz, J., Rico, M., High-resolution three-dimensional structure of ribonuclease A in solution by nuclear magnetic resonance spectroscopy (1993) J Mol Biol, 229, pp. 722-734
Gilliland, G., Crystallographic studies of ribonuclease complexes (1997) Ribonuclease: Structures and Functiones, pp. 306-341. , Riordan JF, D'Alessio G, editors. San Diego, CA: Academic Press
Leonidas, D.D., Chavali, G.B., Jardine, A.M., Li, S., Shapiro, R., Acharya, K.R., Binding of phosphate and pyrophosphate ions at the active site of human angiogenin as revealed by X-ray crystallography (2001) Protein Sci, 10, pp. 1669-1676
Vitagliano, L., Adinolfi, S., Riccio, A., Sica, F., Zagari, A., Mazzarella, L., Binding of a substrate analog to a domain swapping protein: X-ray structure of the complex of bovine seminal ribonuclease with uridylyl(2′,5′)adenosine (1998) Protein Sci, 7, pp. 1691-1699
Youle, R. J., D'Alessio, G., Antitumoral RNases (1997) Ribonuclease: Structures and Functiones, pp. 491-514. , Riordan JF, D'Alessio G, editors. San Diego, CA: Academic Pres
Raines, R. T., Ribonuclease A (1998) Chem Rev, 98, pp. 1045-1065
Rasmussen, B. F., Stock, A. M., Ringe, D., Petsko, G. A., Crystalline ribonuclease A loses function below the dynamical transition at 220 K (1992) Nature, 357, pp. 423-424
Radha Kishan, K. V., Chandra, N. R., Sudarsanakumar, C., Suguna, K., Vijayan, M., Water-dependent domain motion and flexibility in ribonuclease A and the invariant features in its hydration shell. An X-ray study of two low-humidity crystal forms of the enzyme (1995) Acta Crystallogr D, 51, pp. 703-710
Leland, P. A., Schultz, L. W., Kim, B. M., Raines, R. T., Ribonuclease A variants with potent cytotoxic activity (1998) Proc Natl Acad Sci USA, 95, pp. 10407-10412
Klink, T. A., Raines, R. T., Conformational stability is a determinant of ribonuclease A cytotoxicity (2000) J Biol Chem, 275, pp. 17463-17467
Bretscher, L. E., Abel, R. L., Raines, R. T., A ribonuclease A variant with low catalytic activity but high cytotoxicity (2000) J Biol Chem, 275, pp. 9893-9896
Saxena, S. K., Rybak, S. M., Davey R. T., Jr., Youle, R. J., Ackerman, E. J., Angiogenin is a cytotoxic, tRNA-specific ribonuclease in the RNase A superfamily (1992) J Biol Chem, 267, pp. 21982-21986
Leland, P. A., Staniszewski, K. E., Park, C., Kelemen, B. R., Raines, R. T., The ribonucleolytic activity of angiogenin (2002) Biochemistry, 41, pp. 1343-1350
Acharya, K. R., Shapiro, R., Allen, S. C., Riordan, J. F., Vallee, B. L., Crystal structure of human angiogenin reveals the structural basis for its functional divergence from ribonuclease (1994) Proc Natl Acad Sci USA, 91, pp. 2915-2919
Ceruso, M. A., Amadei, A., Di Nola, A., Mechanics and dynamics of B1 domain of protein G: Role of packing and surface hydrophobic residues (1999) Protein Sci, 8, pp. 147-160
Madhusudhan, M. S., Vishveshwara, S., Comparison of the dynamics of bovine and human angiogenin: A molecular dynamics study (1999) Biopolymers, 49, pp. 131-144
Leonidas, D. D., Shapiro, R., Allen, S. C., Subbarao, G. V., Veluraja, K., Acharya, K. R., Refined crystal structures of native human angiogenin and two active site variants: Implications for the unique functional properties of an enzyme involved in neovascularisation during tumour growth (1999) J Mol Biol, 285, pp. 1209-1233
Garcia, A. E., Large-amplitude nonlinear motions in proteins (1992) Phys Rev Lett, 68, pp. 2696-2699
Van Aalten, D. M. F., Grotewold, E., Joshua-Tor, L., Essential dynamics from NMR clusters: Dynamic properties of the Myb DNA-binding domain and a hinge-bending enhancing variant (1998) Methods, 14, pp. 318-328
De Groot, B. L., Hayward, S., Van Aalten, D. M., Amadei, A., Berendsen, H. J. C., Domain motions in bacteriophage T4 lysozyme: A comparison between molecular dynamics and crystallographic data (1998) Proteins, 31, pp. 116-127
Van Aalten, D. M., Conn, D. A., De Groot, B. L., Berendsen, H. J., Findlay, J. B., Amadei, A., Protein dynamics derived from clusters of crystal structures (1997) Biophys J, 73, pp. 2891-2896
Leonidas, D. D., Chavali, G. B., Jardine, A. M., Li, S., Shapiro, R., Acharya, K. R., Binding of phosphate and pyrophosphate ions at the active site of human angiogenin as revealed by X-ray crystallography (2001) Protein Sci, 10, pp. 1669-1676
Subtle functional collective motions in pancreatic-like ribonucleases: From ribonuclease A to angiogenin
The analysis of the dynamic behavior of enzymes is fundamental to structural biology. A direct relationship between protein flexibility and biological function has been shown for bovine pancreatic ribonuclease (RNase A) (Rasmussen et al., Nature 1992;357:423-424). More recently, crystallographic studies have shown that functional motions in RNase A involve the enzyme beta-sheet regions that move concertedly on substrate binding and release (Vitagliano et al., Proteins 2002;46:97-104). These motions have been shown to correspond to intrinsic dynamic properties of the native enzyme by molecular dynamics (MD) simulations. To unveil the occurrence of these collective motions in other members of pancreatic-like superfamily, we carried out MD simulations on human angiogenin (Ang). Essential dynamics (ED) analyses performed on the trajectories reveal that Ang exhibits collective motions similar to RNase A, despite the limited sequence identity (33%) of the two proteins. Furthermore, we show that these collective motions are also present in ensembles of experimentally determined structures of both Ang and RNase A. Finally, these subtle concerted beta-sheet motions were also observed for other two members of the pancreatic-like superfamily by comparing the ligand-bound and ligand-free structures of these enzymes. Taken together, these findings suggest that pancreatic-like ribonucleases share an evolutionary conserved dynamic behavior consisting of subtle beta-sheet motions, which are essential for substrate binding and release. Proteins 2003; 52:101-110. (C) 2003Wiley-Liss,Inc.
Subtle functional collective motions in pancreatic-like ribonucleases: From ribonuclease A to angiogenin