Comprehensive comparison of the cytotoxic activities of onconase and bovine seminal ribonuclease

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 136, Issue 4, 2003, Pages 343-356

  Matousek, Josef ^a   Soucek, Josef ^b   Slavík, Tomás ^a   Tománek, Milan ^c   Lee, J Eugene ^d   Raines, Ronald T ^d  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b INSTITUTE OF HEMATOLOGY AND BLOOD TRANSFUSION   (Czech Republic)

^c INSTITUTE OF ANIMAL SCIENCE   (Czech Republic)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Aspermatogenesis; Cancer; Chemotherapy; Embryotoxicity; Epididymides; Immunogenicity; Leydig cells; Ribonuclease A; Ribonuclease inhibitor; Testes

Indexed keywords

BOVINE SEMINAL RIBONUCLEASE; CYTOTOXIN; RANPIRNASE; RIBONUCLEASE; RIBONUCLEASE A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL FUNCTION; COLONY FORMING UNIT GM; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACTIVITY; DRUG DETERMINATION; DRUG EFFECT; DRUG EXPOSURE; DRUG POTENCY; EMBRYO; EMBRYOTOXICITY; EPIDIDYMIS; FEMALE; HUMAN; HUMAN CELL; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; INJECTION; LEYDIG CELL; LYMPHOCYTE CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SPERM; TESTIS; TUMOR CELL LINE;

BOVINAE;

EID: 0842281345     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cca.2003.10.005     Document Type: Article

References (75)

1. Alexsandrowicz J. Intracutaneous ribonuclease in chronic myelocytic leukaemia. Lancet. 2:1958;420.
2. Ardelt W., Mikulski S.M., Shogen K. Amino acid sequence of an anti-tumor protein from Rana pipiens oocytes and early embryos. J. Biol. Chem. 266:1991;245-251.
3. Berisio R., Sica F., De Lorenzo C., Di Fiore A., Piccoli R., Zagari A., et al. Crystal structure of the dimeric unswapped form of bovine seminal ribonuclease. FEBS Lett. 554:2003;105-110.
4. Boix E., Wu Y., Vasandani V.M., Saxena S.K., Ardelt W., Ladner J., et al. Role of the N terminus in RNase A homologues: Differences in catalytic activity, ribonuclease inhibitor interaction and cytotoxicity. J. Mol. Biol. 257:1996;992-1007.
5. Bretscher L.E., Abel R.L., Raines R.T. A ribonuclease A variant with low catalytic activity but high cytotoxicity. J. Biol. Chem. 275:2000;9893-9896.
6. Chatot C.L., Ziomek C.A., Bavister B.D., Lewis J.L., Tores I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J. Reprod. Fert. 86:1989;679-688.
7. Cinatl J. Jr, Cinatl J., Kotchetkov R., Vogel J.U., Woodcock B.G., Matousek J., et al. Bovine seminal ribonuclease selectively kills human multidrug-resistant neuroblastoma cells via induction of apoptosis. Int. J. Oncol. 15:1999;1001-1009.
8. Cinatl J., Matousek J., Stanek R. Action of A RNase and AS RNase on growth of cells in vitro. Folia Biol. (Praha). 23:1977;235-242.
9. D'Alessio G., Di Donato A., Mazzarella L., Piccoli R. Seminal ribonuclease: the importance of diversity. D'Alessio G., Riordan J.F. Ribonucleases: Structures and Functions. 1997;383-423 Academic Press, New York.
10. D'Alessio G., Floridi A., De Prisco R., Pignero A., Leone E. Bull semen ribonucleases 1. Purification and physico-chemical properties of the major component. Eur. J. Biochem. 26:1972;153-161.
11. D'Alessio G., Riordan J.F. Ribonucleases: Structures and Functions. 1997;Academic Press, New York.
12. Darzynkiewicz Z., Carter S.P., Mikulski S.M., Ardelt W.J., Shogen K. Cytostatic and cytotoxic effect of Pannon (P-30 Protein), a novel anticancer agent. Cell Tissue Kinet. 21:1988;169-182.
13. Dickson K.A., Dahlberg C.L., Raines R.T. Compensating effects on the cytotoxicity of ribonuclease A variants. Arch. Biochem. Biophys. 415:2003;172-177.
14. Dostál J., Matousek J. Purification of aspermatogenic substance (AS) from the bull seminal vesicle fluid. J. Reprod. Fert. 31:1972;273-275.
15. Dostál J., Matousek J. Isolation and some chemical properties of aspermatogenic substance form bull seminal vesicle fluid. J. Reprod. Fertil. 33:1973;263-274.
16. Haigis M.C., Kurten E.L., Abel R.L., Raines R.T. KFERQ sequence in ribonuclease A-mediated cytotoxicity. J. Biol. Chem. 277:2002;11 576-11 581.
17. Haigis M.C., Kurten E.L., Raines R.T. Ribonuclease inhibitor as an intracellular sentry. Nucleic Acids Res. 31:2003;1024-1032.
18. Hirsfeld L., Halber W. Untersuchungen über Verwandtschaftsreaktionen zwischen Embryonal-und Krebsgewebe. I. Mitteilung-Rattenembryonen und Menschentumoren. Z. Immunitätsforsch. 75:1932;193-208.
19. Hlinák A., Matousek J., Madlafousek J. The effect of bull seminal ribonuclease on reproductive organs and sexual behaviour in male rats. Physiol Bohemoslov. 30:1981;539-542.
20. Hofsteenge J. Ribonuclease inhibitor. D'Alessio G., Riordan J.F. Ribonucleases: Structures and Functions. 1997;621-658 Academic Press, New York.
21. Hosokawa S., Irie M. Purification and properties of seminal vesicle ribonucleases. J. Biochem. (Tokyo). 69:1971;683-697.
22. Hwang C., Sinskey A.J., Lodish H.F. Oxidized redox state of glutathione in the endoplasmic reticulum. Science. 257:1992;1496-1502.
23. Kim J.-S., Soucek J., Matousek J., Raines R.T. Catalytic activity of bovine seminal ribonuclease is essential for its immunosuppressive and other biological activities. Biochem. J. 308:1995;547-550.
24. Kim J.-S., Soucek J., Matousek J., Raines R.T. Mechanism of ribonuclease cytotoxicity. J. Biol. Chem. 270:1995;31 097-31 102.
25. Kim J.-S., Soucek J., Matousek J., Raines R.T. Structural basis for the biological activities of bovine seminal ribonuclease. J. Biol. Chem. 270: 1995;10 525-10 530.
26. Ledoux L. Action of ribonuclease on certain ascites tumours. Nature. 175:1955;258-259.
27. Ledoux L. Action of ribonuclease on two solid tumours in vivo. Nature. 176:1955;36-37.
28. Ledoux L., Baltus E. Action de la ribonucléase sur les cellules du carcinome d'Ehrlich. Experientia. 10:1954;500-501.
29. Lee F.S., Shapiro R., Vallee B.L. Tight-binding inhibition of angiogenin and ribonuclease A by placental ribonuclease inhibitor. Biochemistry. 28:1989;225-230.
30. Lee J.E., Raines R.T. Contribution of active-site residues to the function of onconase, a ribonuclease with antitumoral activity. Biochemistry. 42:2003;11 443-11 450.
31. Leland P.A., Raines R.T. Cancer chemotherapy-ribonucleases to the rescue. Chem. Biol. 8:2001;405-413.
32. Leland P.A., Schultz L.W., Kim B.-M., Raines R.T. Ribonuclease A variants with potent cytotoxic activity. Proc. Natl. Acad. Sci. USA. 98:1998;10 407-10 412.
33. Leland P.A., Staniszewski K.E., Kim B.-M., Raines R.T. Endowing human pancreatic ribonuclease with toxicity for cancer cells. J. Biol. Chem. 276:2001;43 095-43 102.
34. Leone E., Greco L., Rastogi R.K., Ieala L. Antispermatogenic properties of bull seminal ribonuclease. J. Reprod. Fert. 34:1973;197-200.
35. Makarov A.A., Ilinskaya O.N. Cytotoxic ribonucleases: Molecular weapons and their targets. FEBS Lett. 540:2003;15-20.
36. Matousek J. Antiembryonic effect of bull seminal vesicle fluid in mice. J. Reprod. Fert. 32:1973;175-184.
37. Matousek J. The effect of bovine seminal ribonuclease (AS RNase) on cells of crocker tumour in mice. Experientia. 29:1973;858-859.
38. Matousek J. Antigenicity of bull seminal ribonuclease and the effect of antibodies on activity. J. Reprod. Fert. 40:1974;7-17.
39. Matousek J. Embryotoxic effect of bull seminal ribonuclease and tissue absorption studies in rats. J. Reprod. Fert. 43:1975;171-174.
40. Matousek J. Complete ischemia of the normal mouse, rat and rabbit testes and of mouse testes with SAI sarcoma. Folia Biol. (Praha). 29:1983;262-271.
41. Matousek J. Aspermatogenic effect of the bull seminal ribonuclease (BS RNase) in the presence of anti BS RNase antibodies in mice. Animal Genet. 25:(Suppl 1):1994;45-50.
42. Matousek J. Ribonucleases and their antitumor activity. Comp. Biochem. Physiol. C. 129:2001;175-191.
43. Matousek J., Gotte G., Poucková P., Soucek J., Slavík T., Vottariello F., et al. Antitumor activity and other biological actions of oligomers of ribonuclease A. J. Biol. Chem. 278:2003;23 817-23 822.
44. Matousek J., Grozdanovic J. Specific effect of bull seminal ribonuclease (AS RNase) on cell systems in mice. Comp. Biochem. Physiol. A. 46:1973;241-248.
45. Matousek J., Hruban V., Hradecki H., Hrubá A., Soucek J. Effect of bovine seminal ribonuclease (BS-RNase) on pig's bone marrow cells. Arch. Tierz. 44:2001;53-63.
46. Matousek J., Kim J.-S., Soucek J., Rihà J., Ribò M., Leland P.A., et al. Ribonucleases endowed with specific toxicity for spermatogenic layers. Comp. Biochem. Physiol. B. 118:1997;881-888.
47. Matousek J., Pavlok A., Dostál J., Grozdanovic J. Some biological properties of bull seminal vesicle aspermatogenic substance and its effect on mice. J. Reprod. Fert. 34:1973;9-22.
48. Matousek J., Poucková P., Soucek J., Skvor J. PEG chains increase aspermatogenic and antitumor activity of RNase A and BS-RNase enzymes. J. Control. Release. 82:2002;29-37.
49. Matousek J., Stanek R. Action of bull seminal vesicle ribonuclease on mouse leukaemic cells. Folia Biol. (Prague). 23:1977;56-65.
50. Matousek J., Veselski L., Baie J., Dostál J. The effect of bull seminal ribonuclease on spermatogenesis in the rabbit. Anim. Reprod. Sci. 1:1978;49-59.
51. Mazzarella L., Capasso S., Demasi D., Di Lorenzo G., Mattia C.A., Zagari A. Bovine seminal ribonuclease: Structure at 1.9 Å resolution. Acta Crystallogr. Sect. D. 49:1993;389-402.
52. Metcalf D. Hemopoietic Colonies: In vitro Cloning of Normal and Leukemic Cells. 1977;Springer-Verlag, Berlin.
53. Michaelis M., Cinatl J., Cinatl J., Poucková P., Langer K., Kreuter J., et al. Coupling of the antitumoral enzyme bovine seminal ribonuclease to polyethylene glycol chains increases its systemic efficacy in mice. Anticancer Drugs. 13:2002;149-154.
54. Mikulski S.M., Costanzi J.J., Vogelzang N.J., McCachren S., Taub R.N., Chun H., et al. Phase II trial of a single weekly intravenous dose of ranpirnase in patients with unresectable malignant mesothelioma. J. Clin. Oncol. 20:2002;274-281.
55. Mosimann S.C., Ardelt W., James M.N.G. Refined 1.7 Å X-ray crystallographic structure of P-30 protein, an amphibian ribonuclease with anti-tumor activity. J. Mol. Biol. 236:1994;1141-1153.
56. Murthy B.S., Sirdeshmukh R. Sensitivity of monomeric and dimeric forms of bovine seminal ribonuclease to human placental ribonuclease inhibitor. Biochem. J. 281:1992;343-348.
57. Natomista E., Cafaro V., Fusiello R., Bracale A., D'Alessio G., Di Donato A. Effective expression and purification of recombinant onconase, an antitumor protein. FEBS Lett. 463:1999;211-215.
58. Newton D.L., Walbridge S., Mikulski S.M., Ardelt W., Shogen K., Ackerman S.J., et al. Toxicity of an antitumor ribonuclease to Purkinje neurons. J. Neurosci. 14:1994;538-544.
59. Raines R.T. Ribonuclease A. Chem. Rev. 98:1998;1045-1065.
60. Shapiro R. Cytoplasmic ribonuclease inhibitor. Methods Enzymol. 341:2001;611-628.
61. Slavík T., Matousek J., Fulka J., Raines R.T. Effect of bovine seminal ribonuclease and bovine pancreatic ribonuclease A on bovine oocyte maturation. J. Exp. Zool. 287:2000;394-399.
62. Soucek J., Chudomel V., Potmesilová I., Novák J.T. Effect of ribonucleases on cell-mediated lympholysis reaction and on cfv-c colonies in bone marrow culture. Nat. Immun. Cell Growth Regul. 5:1986;250-258.
63. Soucek J., Marinov I., Benes J., Hilgert I., Matousek J., Raines R.T. Immunosuppressive activity of bovine seminal ribonuclease and its mode of action. Immunobiology. 195:1996;271-285.
64. Soucek J., Poucková P., Matousek J., Stockbauer P., Dostal J., Zadinova M. Antitumor action of bovine seminal ribonuclease. Neoplasma. 43:1996;335-340.
65. Soucek J., Matousek J. The binding of bull seminal ribonuclease and its carboxymethylated derivative to human leukaemic cells. Folia Biol. (Praha). 25:1979;142-144.
66. Soucek J., Pouckova P., Strohalm J., Plocova D., Hlouskova D., Zadinova M., et al. Poly[N-(2-hydroxypropyl)methyacrylamide] conjugates of bovine pancreatic ribonuclease (RNase A) inhibit growth of human melanoma in nude mice. J. Drug Target. 10:2002;175-183.
67. Soucek J., Raines R.T., Haugg M., Raillard-Yoon S.-A., Benner S.A. Structural changes to ribonuclease A and their effects on biological activity. Comp. Biochem. Physiol. C. 123:1999;103-111.
68. Stanek R., Matousek J. The effect of bull seminal vesicle ribonuclease on cells of Walker carcinosarcoma and Sajdel hepatoma of rats. Folia Biol. (Praha). 22:1976;33-40.
69. Tahara T., Usuki K., Sato H., Ohashi H., Morita H., Tsumura H., et al. A sensitive sandwich ELISA for measuring thrombopoietin in human serum: Serum thrombopoietin levels in healthy volunteers and in patients with haemopoietic disorders. Br. J. Haematol. 93:1996;783-788.
70. Tam J.P. Synthetic peptide vaccine design-synthesis and properties of a high-density multiple antigenic peptide system. Proc. Natl. Acad. Sci. USA. 85:1988;5409-5413.
71. Ulbrich K., Strohalm J., Plocová D., Oupicky D., Subr V., Soucek J., et al. Poly[N-(2-hydroxypropyl)methacrylamide] conjugates of bovine seminal ribonuclease. Synthesis, physicochemical, and preliminary biological evaluation. J. Bioact. Comp. Pol. 15:2000;4-26.
72. Vicentini A.M., Kieffer B., Mathies R., Meyhack B., Hemmings B.A., Stone S.R., et al. Protein chemical and kinetic characterization of recombinant porcine ribonuclease inhibitor expressed in Saccharomyces cerevisiae. Biochemistry. 29:1990;8827-8834.
73. Vorobiev I.I., Ponomarenko N.A., Durova O.M., Kazyr A.V., Denun A.V., Kolesnikov A.V., et al. Structure-function study of recombinant onconase variants. Russ. J. Bioorg. Chem. 27:2001;225-231.
74. Wu Y., Mikulski S.M., Ardelt W., Rybak S.M., Youle R.J. A cytotoxic ribonuclease. J. Biol. Chem. 268:1993;10 686-10 693.
75. Youle R.J., D'Alessio G. Antitumor RNases. D'Alessio G., Riordan J. F. Ribonucleases: Structures and Functions. 1997;491-514 Academic Press, New York.