A novel cross-linked RNase A dimer with enhanced enzymatic properties

Proteins: Structure, Function and Genetics

Volumn 66, Issue 1, 2007, Pages 183-195

  Simons, Brigitte L ^a,b   Kaplan, Harvey ^b   Fournier, Sylvie M ^a   Cyr, Terry ^a   Hefford, Mary Alice ^a  

^a HEALTH CANADA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Covalent cross linking; Dimer; Enzymatic activity; In vacuo; Ribonuclease A

Indexed keywords

AMIDE; DIMER; DOUBLE STRANDED RNA; GLUTAMIC ACID; LYSINE; MONOMER; RIBONUCLEASE A; RIBONUCLEASE INHIBITOR; SINGLE STRANDED RNA; WATER;

ARTICLE; CONFORMATIONAL TRANSITION; COVALENT BOND; CROSS LINKING; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA DEGRADATION; VACUUM; X RAY CRYSTALLOGRAPHY;

ANIMALS; CATTLE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; FREEZE DRYING; GLUTAMIC ACID; LYSINE; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; RIBONUCLEASE, PANCREATIC; RNA; RNA, DOUBLE-STRANDED; TEMPERATURE;

EID: 33845631920     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21144     Document Type: Article

References (50)

1. Crestfield AM, Stein WH, Moore S. On the aggregation of bovine pancreatic ribonuclease. Arch Biochem Biophys 1962;Suppl 1:217-222.
2. Crestfield AM, Fruchter RG. The homologous and hybride dimers of ribonuclease A and its carboxymethyl histidine derivatives. J Biol Chem 1967;242:3279-3284.
3. Mazzarella L, Capasso S, Demasi D, Di LG, Mattia CA, Zagari A. Bovine seminal ribonuclease: structure at 1.9 A resolution. Acta Crystallogr D Biol Crystallogr 1993;49:389-402.
4. Di Donato A, Cafaro V, D'Alessio G. Ribonuclease A can be transformed into a dimeric ribonuclease with antitumor activity. J Biol Chem 1994;269:17394-17396.
5. Gotte G, Libonati M. Two different forms of aggregated dimers of ribonuclease A. Biochim Biophys Acta 1998;1386:106-112.
6. Sorrentino S, Barone R, Bucci E, Gotte G, Russo N, Libonati M, D'Alessio G. The two dimeric forms of RNase A. FEBS Lett 2000; 466:35-39.
7. Park C, Raines RT. Dimer formation by a "monomeric" protein. Protein Sci 2000;9:2026-2033.
8. Liu Y, Hart PJ, Schlunegger MP, 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 1998;95:3437-3442.
9. Liu Y, Gotte G, Libonati M, Eisenberg D. A domain-swapped RNase A dimer with implications for amyloid formation. Nat Struct Biol 2001;8:211-214.
10. Gotte G, Bertoldi M, Libonati M. Structural versatility of bovine ribonuclease A. Distinct conformers of trimeric and tetrameric aggregates of the enzyme. Eur J Biochem 1999;265:680-687.
11. Nenci A, Gotte G, Bertoldi M, Libonati M. Structural properties of trimers and tetramers of ribonuclease A. Protein Sci 2001;10:2017-2027.
12. Bartholeyns J, Baudhuin P. Inhibition of tumor cell proliferation by dimerized ribonuclease. Proc Natl Acad Sci USA 1976;73:573-576.
13. Matousek J. Ribonucleases and their antitumor activity. Comp Biochem Physiol C Toxicol Pharmacol 2001;129:175-191.
14. Libonati M, Gotte G. Oligomerization of bovine ribonuclease A: structural and functional features of its multimers. Biochem J 2004;360:311-327.
15. Matousek J, Soucek J, Salvík T, Tománek M, Lee JE, Raines RT. Comprehensive comparison of the cytotoxic activities of onconase and bovine seminal ribonuclease. Comp Biochem Physiol C Toxicol Pharmacol 2003;136:343-356.
16. Haigis MC, Kurten EL, Raines RT. Ribonuclease inhibitor as an intracellular sentry. Nucleic Acids Res 2003;31:1024-1032.
17. Kim JS, Soucek J, Matousek J, Raines RT. Mechanism of ribonuclease cytotoxicity. J Biol Chem 1995;270:31097-31102.
18. Piccoli R, Tamburrini M, Piccialli G, Di DA, Parente A, D'Alessio G. The dual-mode quaternary structure of seminal RNase. Proc Natl Acad Sci USA 1992;89:1870-1874.
19. Bennett MJ, Schlunegger MP, Eisenberg D. 3D domain swapping: a mechanism for oligomer assembly. Protein Sci 1995;4:2455-2468.
20. Naddeo M, Vitagliano L, Russo A, Gotte G, D'Alessio G, Sorrentino S. Interactions of the cytotoxic Rnase A dimers with the cytosolic ribonuclease inhibitor. FEBS Lett 2005;579:2663-2668.
21. Sica F, Di Fiore A, Merlino A, Mazzarella L. Structure and stability of the non-covalent dimer of bovine simeinal ribonuclease: an enzyme tailored to evade ribonuclease protein inhibitor. J Biol Chem 2004;279:36753-36760.
22. Tarnowski GS, Kassel RL, Mountain IM, Blackburn P, Wilson G Wang D. Comparison of antitumor activities of pancreatic ribonuclease and its cross-linked dimer. Cancer Res 1976;36:4074-4078.
23. Gotte G, Testolin L, Costanzo C, Sorrentino S, Armato U, Libonati M. Cross-linked trimers of bovine ribonuclease A: activity on double-stranded RNA and antitumor action. FEBS Lett 1997;415:308-312.
24. Wang D, Wilson G, Moore S. Preparation of cross-linked dimers of pancreatic ribonuclease. Biochemistry 1976;15:660-665.
25. Leland PA, Schultz LW, Kim BM, Raines RT. Ribonuclease A variants with poten cytotoxic activity. Proc Natl Acad Sci USA 1998;95:10407-10412.
26. Simons BL, King MC, Cyr T, Hefford MA, Kaplan H. Covalent cross-linking of proteins without chemical reagents. Protein Sci 2002;11:1558-1564.
27. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985; 150:76-85.
28. Wiechelman KJ, Braun RD, Fitzpatrick JD. Investigation of the bicinchoninic acid protein assay: identification of the groups responsible for color formation. Anal Biochem 1998;175:231-237.
29. Navon A, Ittah V, Laity JH, Scheraga HA, Haas E, Gussakovsky EE. Local and long-range interactions in the thermal unfolding transition of bovine pancreatic ribonuclease A. Biochemistry 2001; 40:93-104.
30. Kunitz M. Crystalline desoxyribonuclease. I. Isolation and general properties spectrometric method for measurement of desoxyribonuclease activity. J Gen Physiol 1950;33:349-362.
31. McWherter CA, Thanhauser TW, Fredrickson RA, Zagotta MT, Scheraga HA. Peptide mapping of bovine pancreatic ribonuclease A by reverse phase high-performance liquid chromatography. I. Application to the reduced and S-carboxymethylated protein. Anal Biochem 1984;141:523-537.
32. Stelea SD, Pancoska P, Benight AS, Keiderling TA. Thermal unfolding of ribonuclease A in phosphate at neutral pH: deviations from the two-state model. Protein Sci 2001;10:970-978.
33. Klink TA, Raines RT. Conformational stability is a determinant of ribonuclease A cytotoxicity. J Biol Chem 2000;275:17463-17467.
34. Hirs CH, Moore S, Stein WH. Peptides obtained by tryptic hydrolysis of performic acid-oxidized ribonuclease. J Biol Chem 1956;219: 623-642.
35. Evans SV. SETOR: hardward-lighted three dimensional solid model representations of macromolecules. J Mol Graph 1993;11: 134-138.
36. Griebenow K, Klibanov AM. Lyophilization-induced reversible changes in the secondary structure of proteins. Proc Natl Acad Sci USA 1995;92:10969-10976.
37. Dong A, Meyer JD, Kendrick BS, Manning MC, Carpenter JT. Effect of secondary structure on the activity of enzymes suspended in organic solvents. Arch Biochem Biophys 1996;334:406-414.
38. Bell JA. X-ray crystal structure of severely desiccated protein. Protein Sci 1999;8:2033-2040.
39. Fedorov AA, Joseph-McCarthy D, Fedorov E, Sirakova D, Graf I, Almo SC. Ionic interactions in crystalline bovine pancreatic ribonuclease A. Biochemistry 1996;35:15962-15979.
40. Cuchillo CM, Moussaoui M, Barman T, Travers F, Nogués MV. The exo- or endonucleolytic prefence of bovines pancreatic ribonuclease A depends on its subsites structure and on the substrate size. Protein Sci 2002;11:117-128.
41. Nogués MV, Moussaoui M, Boix E, Vilanova M, Ribó, M, Cuchillo CM. The contribution of noncatalytic phosphate-binding subsites to the mechanism of bovine pancreatic ribonuclease A. Cell Mol Life Sci 1998;54:766-774.
42. Fruchter RG, Crestfield AM. On the structure of ribonuclease dimer. Isolation and identification of monomers derived from inactive carboxymethyl dimers. J Biol Chem 1965;240:3875-3882.
43. Creighton TE. Chemical properties of peptides. In: Proteins, structures and molecular properties, 2nd ed. New York: W. H. Freeman; 1993;1-47.
44. Yu W, Vath JE, Huberty MC, Martin SA. Identification of the facile gas-phase cleavage of the Asp-Pro and Asp-Xxx peptide bonds in matrix-assisted laser desorption time-of-flight mass spectrometry. Anal Chem 1993;65:3015-3023.
45. Skribanek Z, Mezo G, Mak M, Hudecz F. Mass spectrometric and chemical stability of the Asp-Pro bond in herpes simplex virus epitope peptides compared with X-Pro bonds of related sequences. J Pept Sci 2002;8:398-406.
46. Matousek J, Gotte G, Pouckova P, Soucek J, Slavik T, Vottariello F, Libonati M. Antitumor activity and other biological actions of oligomers of ribonuclease A. J Biol Chem 2003;278:23817-23822.
47. Wu YN, Mikulski SM, Ardelt W, Rybak SM, Youle RJ. A cytotoxi ribonuclease: study of the mechanism of onconase cytotoxicity. J Biol Chem 1993;268:10686-10693.
48. Monti DM, D'Alessio G. Cytosolic RNase inhibitor only affects RNases and intrinsic cytotoxicity cytosolic. J Biol Chem 2004;279: 39195-39198.
49. Taylor RH, Fournier SM, Simons BL, Kaplan H, Hefford MA. Covalent protein immobilization on glass surfaces: application to alkaline phosphatase. J Biotechnol 2005;118:265-269.
50. El-Shafey A, Tolic N, Young, MM, Sale K, Smith RD, Kery V. "Zero-length" cross-linking in solid state as an approach for analysis of protein-protein interactions. Protein Sci. 2006;15:429-440.