Nonspecific base recognition mediated by water bridges and hydrophobic stacking in ribonuclease I from Escherichia coli

Protein Science

Volumn 17, Issue 4, 2008, Pages 681-690

  Martinez Rodriguez, Sergio ^a,b   Panjikar, Santosh ^c   Van Belle, Karolien ^a,b,d   Wyns, Lode ^a,b   Messens, Joris ^a,b,d   Loris, Remy ^a,b,d  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d Brussels Center for Redox Biology   (Belgium)

Author keywords

Base specificity; Ribonuclease; RNase; Structure function relation; Substrate specificity; X ray

Indexed keywords

CYTOSINE; DECADEOXYNUCLEOTIDE D; GUANINE; NUCLEOTIDE DERIVATIVE; PANCREATIC RIBONUCLEASE; THYMINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CATALYSIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME SPECIFICITY; ENZYME STRUCTURE; ESCHERICHIA COLI; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR RECOGNITION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYTOSINE; ENDORIBONUCLEASES; ESCHERICHIA COLI; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN FOLDING; RHIZOPUS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY; TOBACCO; WATER;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 41649111588     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.073420708     Document Type: Article

References (46)

1. Aguilar, C.F., Thomas, P.J., Mills, A., Moss, D.S., and Palmer, R.A. 1992. Newly observed binding mode in pancreatic ribonuclease. J. Mol. Biol. 224: 265-267.
2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
3. Armon, A., Graur, D., and Ben-Tal, N. 2001. ConSurf: An algorithmic tool for the identification of functional regions in proteins by surface mapping of phylogenetic information. J. Mol. Biol. 307: 447-463.
4. Boeckmann, B., Bairoch, A., Apweiler, R., Blatter, M.C., Estreicher, A., Gasteiger, E., Martin, M.J., Michoud, K., O'Donovan, C., Phan, I., et al. 2003. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 31: 365-370.
5. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
6. Buts, L., Lah, J., Dao-Thi, M.H., Wyns, L., and Loris, R. 2005. Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem. Sci. 30: 672-679.
7. Cannistraro, V.J. and Kennell, D. 1991. RNase I*, a form of RNase I, and mRNA degradation in Escherichia coli. J. Bacteriol. 173: 4653-4659.
8. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50: 760-763.
9. Emsley, P. and Cowtan, K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132.
10. Hutchinson, E.G. and Thornton, J.M. 1996. PROMOTIF-a program to identify and analyze structural motifs in proteins. Protein Sci. 5: 212-220.
11. Ida, K., Norioka, S., Yamamoto, M., Kumasaka, T., Yamashita, E., Newbigin, E., Clarke, A.E., Sakiyama, F., and Sato, M. 2001. The 1.55 Å resolution structure of Nicotiana alata S(F11)-RNase associated with gametophytic self-incompatibility. J. Mol. Biol. 314: 103-112.
12. Irie, M. 1997. RNaseT1/Rnase T2 family RNases. In Ribonucleases: Structures and functions (eds. G. D'Alessio, and J.F. Riordan), pp. 101-129. Academic Press, New York.
13. Irie, M. 1999. Structure-function relationships of acid ribonucleases: Lysosomal, vacuolar, and periplasmic enzymes. Pharmacol. Ther. 81: 77-89.
14. Janin, J. 1999. Wet and dry interfaces: The role of solvent in protein-protein and protein-DNA recognition. Structure 7: R277-R279. doi: 10.1016/S0969-2126(00)88333-1.
15. Joachimiak, A., Haran, T.E., and Sigler, P.B. 1994. Mutagenesis supports water mediated recognition in the trp repressor-operator system. EMBO J. 13: 367-372.
16. Kabsch, W. and Sander, C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
17. Kawano, S., Kakuta, Y., and Kimura, M. 2002. Guanine binding site of the Nicotiana glutinosa ribonuclease NW revealed by X-ray crystallography. Biochemistry 41: 15195-15202.
18. Kawano, S., Kakuta, Y., Nakashima, T., and Kimura, M. 2006. Crystal structures of the Nicotiana glutinosa ribonuclease NT in complex with nucleoside monophosphates. J. Biochem. 140: 375-381.
19. Kurihara, H., Nonaka, T., Mitsui, Y., Ohgi, K., Irie, M., and Nakamura, K.T. 1996. The crystal structure of ribonuclease Rh from Rhizopus niveus at 2.0 Å resolution. J. Mol. Biol. 255: 310-320.
20. Langhorst, U., Backmann, J., Loris, R., and Steyaert, J. 2000. Analysis of a water mediated protein-protein interactions within RNase T1. Biochemistry 39: 6586-6593.
21. Matsuura, T., Sakai, H., Unno, M., Ida, K., Sato, M., Sakiyama, F., and Norioka, S. 2001. Crystal structure at 1.5 Å resolution of Pyrus pyrifolia pistil ribonuclease responsible for gametophytic self-incompatibility. J. Biol. Chem. 276: 45261-45269.
22. McClure, B.A., Haring, V., Ebert, P.R., Anderson, M.A., Simpson, R.J., Sakiyama, F., and Clarke, A.E. 1989. Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342: 955-957.
23. McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C., and Read, R.J. 2005. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61: 458-464.
24. Meador III, J. and Kennell, D. 1990. Cloning and sequencing the gene encoding Escherichia coli ribonuclease I: Exact physical mapping using the genome library. Gene 95: 1-7.
25. Messens, J., Collet, J.F., Van Belle, K., Brosens, E., Loris, R., and Wyns, L. 2007. The oxidase DsbA folds a protein with a nonconsecutive disulfide. J. Biol. Chem. 282: 31302-31307.
26. Morris, R.J., Perrakis, A., and Lamzin, V.S. 2002. ARP/wARP's model-building algorithms. I. The main chain. Acta Crystallogr. D Biol. Crystallogr. 58: 968-975.
27. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53: 240-255.
28. Nakagawa, A., Tanaka, I., Sakai, R., Nakashima, T., Funatsu, G., and Kimura, M. 1999. Crystal structure of a ribonuclease from the seeds of bitter gourd (Momordica charantia) at 1.75Å resolution. Biochim. Biophys. Acta 1433: 253-260.
29. Neu, H.C. and Heppel, L.A. 1964. The release of ribonuclease into the medium when Escherichia coli cells are converted to spheroplasts. J. Biol. Chem. 239: 3893-3900.
30. Nicholson, A.W. 1997. Escherichia coli ribonucleases: Paradigms for understanding cellular RNA metabolism and regulation. In Ribonucleases: Structures and functions (eds. G. D'Alessio, and J.F. Riordan), pp. 1-49. Academic Press, New York.
31. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
32. Otwinowski, Z., Schevitz, R.W., Zhang, R.G., Lawson, C.L., Joachimiak, A., Marmorstein, R.Q., Luisi, B.F., and Sigler, P.B. 1988. Crystal structure of trp repressor/operator complex at atomic resolution. Nature 335: 321-329.
33. Padmanabhan, S., Zhou, K., Chu, C.Y., Lim, R.W., and Lim, L.W. 2001. Overexpression, biophysical characterization, and crystallization of ribonuclease I from Escherichia coli, a broad-specificity enzyme in the RNase T2 family. Arch. Biochem. Biophys. 390: 42-50.
34. Panjikar, S., Parthasarathy, V., Lamzin, V.S., Weiss, M.S., and Tucker, P.A. 2005. Auto-Rickshaw: An automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr. D Biol. Crystallogr. 61: 449-457.
35. Quaas, R., Landt, O., Grunert, H.P., Beineke, M., and Hahn, U. 1989. Indicator plates for rapid detection of ribonuclease T1 secreting Escherichia coli clones. Nucleic Acids Res. 17: 3318.
36. Rabijns, A., Verboven, C., Rouge, P., Barre, A., Van Damme, E.J., Peumans, W.J., and De Ranter, C.J. 2002. Structure of an RNase-related protein from Calystegia sepium. Acta Crystallogr. D Biol. Crystallogr. 58: 627-633.
37. Raschke, T.M. 2006. Water structure and interactions with protein surfaces. Curr. Opin. Struct. Biol. 16: 152-159.
38. Roos, G., Garcia-Pino, A., Van Belle, K., Brosens, E., Wahni, K., Vandenbussche, G., Wyns, L., Loris, R., and Messens, J. 2007. The conserved active site proline determines the reducing power of Staphylococcus aureus thioredoxin. J. Mol. Biol. 368: 800-811.
39. Schneider, T.R. and Sheldrick, G.M. 2002. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58: 1772-1779.
40. Sevcik, J., Zegers, I., Wyns, L., Dauter, Z., and Wilson, K.S. 1993. Complex of ribonuclease Sa with a cyclic nucleotide and a proposed model for the reaction intermediate. Eur. J. Biochem. 216: 301-305.
41. Storoni, L.C., McCoy, A.J., and Read, R.J. 2004. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60: 432-438.
42. Suzuki, A., Yao, M., Tanaka, I., Numata, T., Kikukawa, S., Yamasaki, N., and Kimura, M. 2000. Crystal structures of the ribonuclease MC1 from bitter gourd seeds, complexed with 2′-UMP or 3′-UMP, reveal structural basis for uridine specificity. Biochem. Biophys. Res. Commun. 275: 572-576.
43. Tanaka, N., Arai, J., Inokuchi, N., Koyama, T., Ohgi, K., Irie, M., and Nakamura, K.T. 2000. Crystal structure of a plant ribonuclease, RNase LE. J. Mol. Biol. 298: 859-873.
44. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
45. Vriend, G. 1990. WHAT IF: A molecular modeling and drug design program. J. Mol. Graph. 8: 52-56.
46. Zegers, I., Loris, R., Dehollander, G., Fattah Haikal, A., Poortmans, F., Steyaert, J., and Wyns, L. 1998. Hydrolysis of a slow cyclic thiophosphate substrate of RNase T1 analyzed by time-resolved crystallography. Nat. Struct. Biol. 5: 280-283.