The Buried Diversity of Bovine Seminal Ribonuclease: Shape and Cytotoxicity of the Swapped Non-covalent Form of the Enzyme

Journal of Molecular Biology

Volumn 376, Issue 2, 2008, Pages 427-437

  Merlino, Antonello ^a   Ercole, Carmine ^a   Picone, Delia ^a   Pizzo, Elio ^a   Mazzarella, Lelio ^a,b   Sica, Filomena ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

Author keywords

3 D domain swapping; antitumor activity; bovine seminal ribonuclease; crystal structure; non covalent dimer

Indexed keywords

ENZYME; LEUCINE; PROLINE; PROTEIN L 28 Q; PROTEIN PALQ; RIBONUCLEASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CONTROLLED STUDY; COW; CYTOSOL; CYTOTOXICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEMINAL VESICLE; WILD TYPE; X RAY DIFFRACTION;

BOVINAE;

EID: 38349091102     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.11.008     Document Type: Article

References (46)

1. Arnold U., and Ulrich-Hofmann R. Natural and engineered ribonucleases as potential cancer therapeutics. Biotechnol. Lett. 28 (2006) 1615-1622
2. Makarov A.A., and Ilinskaya O.N. Cytotoxic ribonucleases: molecular weapons and their targets. FEBS Lett. 540 (2003) 15-20
3. Leland P.A., and Raines R.T. Cancer chemotherapy-ribonucleases to the rescue. Chem. Biol. 8 (2001) 405-413
4. Bretscher L.E., Abel R.L., and Raines R.T. A ribonuclease A variant with low catalytic activity but high cytotoxicity. J. Biol. Chem. 275 (2000) 9893-9896
5. Merlino A., Mazzarella L., Carannante A., Di Fiore A., Di Donato A., Notomista E., and Sica F. The importance of dynamic effects on the enzyme activity: X-ray structure and molecular dynamics of onconase mutants. J. Biol. Chem. 280 (2005) 17953-17960
6. Leland P.A., Schultz L.W., Kim B.M., and Raines R.T. Ribonuclease A variants with potent cytotoxic activity. Proc. Natl Acad. Sci. USA 95 (1998) 10407-10412
7. Bosch M., Benito A., Ribo M., Puig T., Beaumelle B., and Vilanova M. A nuclear localization sequence endows human pancreatic ribonuclease with cytotoxic activity. Biochemistry 43 (2004) 2167-2177
8. Rodriguez M., Benito A., Tubert P., Castro J., Ribo M., Beaumelle B., and Vilanova M. A cytotoxic ribonuclease variant with a discontinuous nuclear localization signal constituted by basic residues scattered over three areas of the molecule. J. Mol. Biol. 360 (2006) 548-557
9. Newton D.L., Xue Y., Boqué L., Wlodawer A., Kung H.F., and Rybak S.M. Expression and characterization of a cytotoxic human-frog chimeric ribonuclease: potential for cancer therapy. Protein Eng. 10 (1997) 463-470
10. Gaur D., Swaminathan S., and Batra J.K. Interaction of human pancreatic ribonuclease with human ribonuclease inhibitor. Generation of inhibitor-resistant cytotoxic variants. J. Biol. Chem. 276 (2001) 24978-24984
11. Matousek J., Gotte G., Pouckova P., Soucek J., Slavick T., Vottariello F., and Libonati M. Antitumor and other biological actions of oligomers of RNase A. J. Biol. Chem. 278 (2003) 23817-23822
12. Libonati M. Biological actions of the oligomers of ribonuclease A. Cell. Mol. Life Sci. 61 (2004) 2431
13. Libonati M., and Gotte G. Oligomerization of bovine ribonuclease A: structural and functional features of its multimers. Biochem. J. 380 (2004) 311-327
14. Piccoli R., Di Gaetano S., De Lorenzo C., Grauso M., Monaco C., Spalletti-Cernia D., et al. A dimeric mutant of human pancreatic ribonuclease with selective cytotoxicity toward malignant cells. Proc. Natl Acad. Sci. USA 96 (1999) 7768-7773
15. Piccoli R., Vescia S., Bridges S.H., and D'Alessio G. The antitumor action of seminal ribonuclease tested with the plasmacytoma spleen colonization assay. Ital. J. Biochem. 39 (1990) 242-249
16. Cafaro V., De Lorenzo C., Piccoli R., Bracale A., Mastronicola M.R., Di Donato A., and D'Alessio G. The antitumor action of seminal ribonuclease and its quaternary conformations. FEBS Lett. 359 (1995) 31-34
17. Mazzarella L., Capasso S., Demasi D., Di Lorenzo G., Mattia C.A., and Zagari A. Bovine seminal ribonuclease: structure at 1.9 Å resolution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 49 (1993) 389-402
18. Berisio R., Sica F., De Lorenzo C., Di Fiore A., Piccoli R., Zagari A., and Mazzarella L. Crystal structure of the dimeric unswapped form of bovine seminal ribonuclease. FEBS Lett. 554 (2003) 105-110
19. Piccoli R., Tamburrini M., Piccialli G., Di Donato A., Parente A., and D'Alessio G. The dual-mode quaternary structure of seminal RNase. Proc. Natl Acad. Sci. USA 89 (1992) 1870-1874
20. Merlino A., Vitagliano L., Sica F., Zagari A., and Mazzarella L. Population shift versus induced fit: the case of bovine seminal ribonuclease swapping dimer. Biopolymers 73 (2004) 689-695
21. Sica F., Di Fiore A., Merlino A., and Mazzarella L. Structure and stability of the non-covalent swapped dimer of bovine seminal ribonuclease: an enzyme tailored to evade ribonuclease protein inhibitor. J. Biol. Chem. 279 (2004) 36753-36760
22. Liu Y., Gotte G., Libonati M., and Eisenberg D. A domain-swapped RNase A dimer with implications for amyloid formation. Nat. Struct. Biol. 8 (2001) 211-214
23. Liu Y., Hart P.J., Schlunegger M.P., and Eisenberg D. The crystal structure of a 3D domain-swapped dimer of RNase A at a 2.1 Å resolution. Proc. Natl Acad. Sci. USA 95 (1998) 3437-3442
24. Canals A., Pous J., Guasch A., Benito A., Ribo M., Vilanova M., and Coll M. The structure of an engineered domain-swapped ribonuclease dimer and its implications for the evolution of proteins toward oligomerization. Structure 9 (2001) 967-976
25. Naddeo M., Vitagliano L., Russo A., Gotte G., D'Alessio G., and Sorrentino S. Interactions of the cytotoxic RNase A dimers with the cytosolic ribonuclease inhibitor. FEBS Lett. 579 (2005) 2663-2668
26. Merlino A., Vitagliano L., Ceruso M.A., and Mazzarella L. Dynamic properties of the N-terminal swapped dimer of ribonuclease A. Biophys J. 86 (2004) 2383-2391
27. Ercole C., Avitabile F., Del Vecchio P., Crescenzi O., Tancredi T., and Picone D. Role of the hinge peptide and the intersubunit interface in the swapping of N-termini in dimeric bovine seminal RNase. Eur. J. Biochem. 270 (2003) 4729-4735
28. Picone D., Di Fiore A., Ercole C., Franzese M., Sica F., Tomaselli S., and Mazzarella L. The role of the hinge loop in domain swapping. The special case of bovine seminal ribonuclease. J. Biol. Chem. 280 (2005) 13771-13778
29. Bennett M.J., Schlunegger M.P., and Eisenberg D. 3D Domain swapping: a mechanism for oligomer assembly. Protein Sci. 4 (1995) 2455-2468
30. Liu Y., and Eisenberg D. 3D domain swapping: as domains continue to swap. Protein Sci. 11 (2002) 1285-1299
31. Avitabile F., Alfano C., Spadaccini R., Crescenzi O., D'Ursi A.M., D'Alessio G., et al. The swapping of terminal arms in ribonucleases: comparison of the solution structure of monomeric bovine seminal and pancreatic ribonucleases. Biochemistry 42 (2003) 8704-8711
32. Otwinowski Z., and Minor W. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
33. Navaza J., and Saludjian P. AMoRe: an automated molecular replacement program package. Methods Enzymol. 276 (1997) 581-594
34. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., and Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. D 61 (2005) 458-464
35. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. D 54 (1998) 905-921
36. Jones T.A., Bergdoll M., and Kjeldgaard M. O: a macromolecular modeling environment. In: Bugg C., and Ealick S. (Eds). Crystallographic and Modeling Methods in Molecular Design (1990), Springer-Verlag Press, Heidelberg 189-199
37. Laskowski R.A., MacArthur M.W., Moss M.D., and Thorton J.M. PROCHECK: a program to check the stereochemical quality of protein structure. J. Appl. Crystallogr. 26 (1993) 283-291
38. Hooft R.W., Vriend G., Sander C., and Abola E.E. Errors in protein structures. Nature 381 (1996) 272
39. Kobe B., and Deisenhofer J. Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A. J. Mol. Biol. 264 (1996) 1028-1043
40. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24 (1991) 946-950
41. Esnouf R.M. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 (1999) 938-940
42. McDonald I.K., and Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238 (1994) 777-793
43. Brunger A.T. X-PLOR Version 3.8 (1996), Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT
44. Adinolfi B.S., Cafaro V., D'Alessio G., and Di Donato A. Full antitumor action of recombinant seminal ribonuclease depends on the removal of its N-terminal methionine. Biochem. Biophys. Res. Commun. 213 (1995) 525-532
45. Abe K., and Kimura H. Amyloid beta toxicity consists of a Ca(2+)-independent early phase and a Ca(2+)-dependent late phase. J. Neurochem. 67 (1996) 2074-2078
46. Bracale A., Spalletti-Cernia D., Mastronicola M., Castaldi F., Mannucci R., Nitsch L., and D'Alessio G. Essential stations in the intracellular pathway of cytotoxic bovine seminal ribonuclease. Biochem. J. 362 (2002) 553-560