Contribution of active-site residues to the function of onconase, a ribonuclease with antitumoral activity

Biochemistry

Volumn 42, Issue 39, 2003, Pages 11443-11450

  Lee, J Eugene ^a   Raines, Ronald T ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSTS; ENZYMES; HYDROGEN BONDS; ISOTHERMS; TUMORS;

BINDING ISOTHERMS;

BIOCHEMISTRY;

ALANINE; FLUORESCENT DYE; GLUTAMINE; HISTIDINE; LACTAM; LYSINE; NUCLEIC ACID BASE; PYROGLUTAMIC ACID; RANPIRNASE; RIBONUCLEASE A;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER CHEMOTHERAPY; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXICITY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS; THERMOSTABILITY;

AMINO ACID SUBSTITUTION; AMINO ACIDS; ANIMALS; ANTINEOPLASTIC AGENTS; BINDING SITES; CIRCULAR DICHROISM; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; HUMANS; K562 CELLS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; RADIOLIGAND ASSAY; RANA PIPIENS; RIBONUCLEASE, PANCREATIC; RIBONUCLEASES; THERMODYNAMICS;

EID: 0141483327     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035147s     Document Type: Article

References (52)

1. Cuchillo, C. M., Vilanova, M., and Nogués, M. V. (1997) Pancreatic ribonucleases, in Ribonucleases: Structures and Functions (Riordan, J. F., Ed.) pp 271-304, Academic Press, New York.
2. Raines, R. T. (1998) Ribonuclease A, Chem. Rev. 98, 1045-1065.
3. Youle, R. J., and D'Alessio, G. (1997) Antitumor RNases, in Ribonucleases: Structures and Functions (Riordan, J. F., Ed.) pp 491-514, Academic Press, New York.
4. Leland, P. A., and Raines, R. T. (2001) Cancer chemotherapy-ribonucleases to the rescue, Chem. Biol. 8, 405-413.
5. Matousek, J. (2001) Ribonucleases and their antitumor activity, Comp. Biochem. Physiol. 129C, 175-191.
6. Makarov, A. A., and Ilinskaya, O. N. (2003) Cytotoxic ribonucleases: Molecular weapons and their targets, FEBS Lett. 540, 15-20.
7. Saxena, S. K., Sirdeshmukh, R., Ardelt, W., Mikulski, S. M., Shogen, K., and Youle, R. J. (2002) Entry into cells and selective degradation of tRNAs by a cytotoxic member of the RNase A family, J. Biol. Chem. 277, 15142-15146.
8. Haigis, M. C., and Raines, R. T. (2003) Secretory ribonucleases are internalized by a dynamin-independent endocytic pathway, J. Cell Sci. 116, 313-324.
9. Mikulski, S. M., Costanzi, J. J., Vogelzang, N. J., McCachren, S., Taub, R. N., Chun, H., Mittelman, A., Panella, T., Puccio, C., Fine, R., and Shogen, K. (2002) Phase II trial of a single weekly intravenous dose of ranpimase in patients with unresectable malignant mesothelioma, J. Clin. Oncol. 20, 274-281.
10. Ardelt, W., Mikulski, S. M., and Shogen, K. (1991) Amino acid sequence of an anti-tumor protein from Rana pipiens oocytes and early embryos, J. Biol. Chem. 266, 245-251.
11. Mosimann, S. C., Ardelt, W., and James, M. N. G. (1994) Refined 1.7 A X-ray crystallographic structure of P-30 protein, an amphibian ribonuclease with anti-tumor activity, J. Mol. Biol. 236, 1141-1153.
12. Wu, Y., Mikulski, S. M., Ardelt, W., Rybak, S. M., and Youle, R. J. (1993) A cytotoxic ribonuclease, J. Biol. Chem. 268, 10686-10693.
13. Dickson, K. A., Dahlberg, C. L., and Raines, R. T. (2003) Compensating effects on the cytotoxicity of ribonuclease A variants, Arch. Biochem. Biophys. 415, 172-177.
14. Haigis, M. C., Kurten, E. L., and Raines, R. T. (2003) Ribonuclease inhibitor as an intracellular sentry, Nucleic Acids Res. 31, 1024-1032.
15. Leland, P. A., Staniszewski, K. E., Kim, B.-M., and Raines, R. T. (2000) A synapomorphic disulfide bond is critical for the conformational stability and cytotoxicity of an amphibian ribonuclease, FEBS Lett. 477, 203-207.
16. Notomista, E., Catanzano, F., Graziano, G., Gaetano, S. D., Barone, G., and Donato, A. D. (2001) Contribution of chain termini to the conformational stability and biological activity of onconase, Biochemistry 40, 9097-9103.
17. Kartha, G., Bello, J., and Harker, D. (1967) Tertiary structure of ribonuclease, Nature 213, 862-865.
18. Beintema, J. J., Breukelman, H. J., Carsana, A., and Furia, A. (1997) Evolution of vertebrate ribonucleases: Ribonuclease A superfamily, in Ribonucleases: Structures and Functions (Riordan, J. F., Ed.) pp 245-269, Academic Press, New York.
19. Irie, M., Nitta, K., and Nonaka, T. (1998) Biochemistry of frog ribonucleases, Cell. Mol. Life Sci. 54, 775-784.
20. Busby, W. H., Quackenbush, G. E., Humm, J., Youngblood, W. W., and Kizer, J. S. (1987) An enzyme(s) that converts glutaminyl-peptides into pyroglutamyl-peptides. Presence in pituitary, brain, adrenal medulla, and lymphocytes, J. Biol. Chem. 262, 8532-8536.
21. Fischer, W. H., and Spiess, J. (1987) Identification of a mammalian glutaminyl cyclase converting glutaminyl into pyroglutamyl peptides, Proc. Natl. Acad. Sci. U.S.A. 84, 3628-3632.
22. Bateman, R. C., Temple, J. S., Misquitta, S. A., and Booth, R. E. (2001) Evidence for essential histidines in human pituitary glutaminyl cyclase, Biochemistry 40, 11246-11250.
23. Lechan, R. M., Wu, P., Jackson, I. M., Wolf, H., Cooperman, S., Mandel, G., and Goodman, R. H. (1986) Thyrotropin-releasing hormone precursor: Characterization in rat brain, Science 231, 159-161.
24. Wlodawer, A., Svensson, L. A., Sjölin, L., and Gilliland, G. L. (1988) Structure of phosphate-free ribonuclease A refined at 1.26 Å, Biochemistry 27, 2705-2717.
25. Merritt, E. A., and Murphy, M. E. P. (1994) Raster3D Version 2.0, a program for photorealistic molecular graphics, Acta Crystallogr., Sect. D 50, 869-873.
26. Boix, E., Wu, Y., Vasandani, V. M., Saxena, S. K., Ardelt, W., Ladner, J., and Youle, R. J. (1996) Role of the N terminus in RNase A homologues: Differences in catalytic activity, ribonuclease inhibitor interaction and cytotoxicity, J. Mol. Biol. 257, 992-1007.
27. Newton, D. L., Boque, L., Wlodawer, A., Huang, C. Y., and Rybak, S. M. (1998) Single amino acid substitutions at the N-terminus of a recombinant cytotoxic ribonuclease markedly influence biochemical and biological properties, Biochemistry 37, 5173-5183.
28. Smith, B. D., Soellner, M. B., and Raines, R. T. (2003) Potent inhibition of ribonuclease A by oligo(vinylsulfonic acid), J. Biol. Chem. 278, 20934-20938.
29. Leland, P. A., Schultz, L. W., Kim, B.-M., and Raines, R. T. (1998) Ribonuclease A variants with potent cytotoxic activity, Proc. Natl. Acad. Sci. U.S.A. 98, 10407-10412.
30. Kelemen, B. R., Klink, T. A., Behlke, M. A., Eubanks, S. R., Leland, P. A., and Raines, R. T. (1999) Hypersensitive substrate for ribonucleases, Nucleic Acids Res. 27, 3696-3701.
31. delCardayré, S. B., and Raines, R. T. (1995) A residue to residue hydrogen bond mediates the nucleotide specificity of ribonuclease A, J. Mol. Biol. 252, 328-336.
32. Radzicka, A., and Wolfenden, R. (1995) Transition state and multisubstrate analog inhibitors, Methods Enzymol. 249, 284-312.
33. Mildvan, A. S., Weber, D. J., and Kuliopulos, A. (1992) Quantitative interpretations of double mutations of enzymes, Arch. Biochem. Biophys. 294, 327-340.
34. Fisher, B. M., Ha, J.-H., and Raines, R. T. (1998) Coulombic forces in protein-RNA interactions: Binding and cleavage by ribonuclease A and variants at Lys7, Arg10, and Lys66, Biochemistry 37, 12121-12132.
35. Park, C., Schultz, L. W., and Raines, R. T. (2001) Contribution of the active site histidine residues of ribonuclease A to nucleic acid binding, Biochemistry 40, 4949-4956.
36. Moore, G. E., Gerner, R. E., and Franklin, H. A. (1967) Culture of normal human leukocytes, J. Am. Med. Assoc. 199, 519-524.
37. Leland, P. A., Staniszewski, K. E., Park, C., Kelemen, B. R., and Raines, R. T. (2002) The ribonucleolytic activity of angiogenin, Biochemistry 41, 1343-1350.
38. Brown, D. M., and Todd, A. R. (1952) Nucleotides. Part X. Some observations on the structure and chemical behaviour of the nucleic acids, J. Chem. Soc., 52-58.
39. Richards, F. M., and Wyckoff, H. W. (1971) Bovine pancreatic ribonuclease, The Enymes IV, 647-806.
40. Okabe, Y., Katayama, N., Iwama, M., Watanabe, H., Ohgi, K., Irie, M., Nitta, K., Kawauchi, H., Takayanagi, Y., Oyama, F., Titani, K., Abe, Y., Oakzaki, T., Inokuchi, N., and Koyama, T. (1991) Comparative base specificity, stability, and lectin activity of two lectins from eggs of Rana catesbeiana and R. japonica and liver ribonuclease from R. catesbeiana, J. Biochem. (Tokyo) 109, 786-790.
41. Leu, Y.-J., Chem, S.-S., Wang, S.-C., Hsiao, Y.-Y., Amiraslanov, I., Liaw, Y.-C., and Liao, Y.-D. (2003) Residues involved in the catalysis, base specificity, and cytotoxicity of ribonuclease from Rana catesbeiana based upon mutagenesis and X-ray crystallography, J. Biol. Chem. 278, 7300-7309.
42. Darzynkiewicz, Z., Carter, S. P., Mikulski, S. M., Ardelt, W. J., and Shogen, K. (1988) Cytostatic and cytotoxic effect of Pannon (P-30 Protein), a novel anticancer agent, Cell Tissue Kinet. 21, 169-182.
43. Shindyalov, I. N., and Bourne, P. E. (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path, Protein Eng. 11, 739-747.
44. Findlay, D., Herries, D. G., Mathias, A. P., Rabin, B. R., and Ross, C. A. (1961) The active site and mechanism of action of bovine pancreatic ribonuclease, Nature 190, 781-784.
45. Thompson, J. E., and Raines, R. T. (1994) Value of general acid-base catalysis to ribonuclease A, J. Am. Chem. Soc. 116, 5467-5468.
46. Messmore, J. M., Fuchs, D. N., and Raines, R. T. (1995) Ribonuclease A: Revealing structure-function relationships with semisynthesis, J. Am. Chem. Soc. 117, 8057-8060.
47. Messmore, J. M., and Raines, R. T. (2000) Pentavalent organovanadates as transition state analogues for phosphoryl transfer reactions, J. Am. Chem. Soc. 122, 9911-9916.
48. delCardayré, S. B., Ribó, M., Yokel, E. M., Quirk, D. J., Rutter, W. J., and Raines, R. T. (1995) Engineering ribonuclease A: Production, purification, and characterization of wild-type enzyme and mutants at Gln11, Protein Eng. 8, 261-273.
49. Kim, J.-S., Soucek, J., Matousek, J., and Raines, R. T. (1995) Catalytic activity of bovine seminal ribonuclease is essential for its immunosuppressive and other biological activities, Biochem. J. 308, 547-550.
50. Cummins, P. M., and O'Connor, B. (1998) Pyroglutamyl peptidase: An overview of the three known enzymatic forms, Biochim. Biophys. Acta 1429, 1-17.
51. Bateman, R. C. (1989) A spectrophotometric assay for glutaminyl-peptide cyclizing enzymes, J. Neurosci. Methods 30, 23-28.
52. Plainkum, P., Fuchs, S. M., Wiyakrutta, S., and Raines, R. T. (2003) Creation of a zymogen, Nat. Struct. Biol. 10, 115-119.