Ranpirnase (Onconase®), a cytotoxic amphibian ribonuclease, manipulates tumour physiological parameters as a selective killer and a potential enhancer for chemotherapy and radiation in cancer therapy

Expert Opinion on Biological Therapy

Volumn 8, Issue 6, 2008, Pages 813-827

  Lee, Intae ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cancer therapy; Chemotherapy; Cytotoxic amphibian ribonuclease; Radiation; Ranpirnase

Indexed keywords

ANTIMITOTIC AGENT; BINDING PROTEIN; CISPLATIN; DOXORUBICIN; LYSOSOME ENZYME; PANCREATIC RIBONUCLEASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN P53; RANPIRNASE; TAMOXIFEN; VINCRISTINE; ANTINEOPLASTIC AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; RADIOSENSITIZING AGENT; RIBONUCLEASE; RNA; TUMOR PROTEIN;

ADENOCARCINOMA; ALOPECIA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOPHAGY; BONE MARROW SUPPRESSION; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RADIOTHERAPY; CANCER SURVIVAL; CARDIOTOXICITY; CELL AGGLUTINATION; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CLINICAL TRIAL; CLONOGENESIS; CLONOGENIC ASSAY; COLON CANCER; COMBINATION CHEMOTHERAPY; CONTRAST ENHANCEMENT; DIZZINESS; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DRUG CYTOTOXICITY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG FATALITY; DRUG MECHANISM; DRUG METABOLISM; DRUG POTENTIATION; DRUG SAFETY; DRUG UPTAKE; DRUG URINE LEVEL; ENDOCYTOSIS; FIBROSARCOMA; FLUSHING; GLYCOLYSIS; HUMAN; LD 50; LIVER TOXICITY; LUNG CANCER; MEDICAL PARAMETERS; MESOTHELIOMA; METABOLIC DISORDER; MONOTHERAPY; MUCOSA INFLAMMATION; MULTIPLE CYCLE TREATMENT; MYALGIA; NEPHROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OVERALL SURVIVAL; OXYGEN CONSUMPTION; PROSTATE TUMOR; RADIOSENSITIVITY; RECOMMENDED DRUG DOSE; REVIEW; SIDE EFFECT; STATISTICAL SIGNIFICANCE; SURVIVAL RATE; SURVIVAL TIME; TISSUE OXYGENATION; TISSUE PRESSURE; TUMOR BLOOD FLOW; TUMOR CELL; TUMOR VOLUME; WEIGHT REDUCTION; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; DRUG SCREENING; EXTRACELLULAR FLUID; FROG; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; NEOPLASM; NUDE MOUSE; RNA STABILITY; SIGNAL TRANSDUCTION; STATISTICS; VASCULARIZATION;

AMPHIBIA; ANIMALIA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CLINICAL TRIALS AS TOPIC; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; EXTRACELLULAR FLUID; HUMANS; MICE; MICE, NUDE; MICE, SCID; NEOPLASM PROTEINS; NEOPLASMS; OXYGEN CONSUMPTION; RADIATION-SENSITIZING AGENTS; RANA PIPIENS; RIBONUCLEASES; RNA STABILITY; RNA, NEOPLASM; SIGNAL TRANSDUCTION;

EID: 45549103591     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.8.6.813     Document Type: Review

References (68)

1. Penketh PG, Shyam K, Sartorelli AC. Mechanisms of resistance to alkylating agents. Cancer Treat Res 1996;87:65-81
2. Iordanov MS, Ryabinina OP, Wong J, et al. Molecular determinants of apoptosis induced by the cytotoxic ribonuclease onconase: evidence for cytotoxic mechanisms different from inhibition of protein synthesis. Cancer Res 2000;60:1983-94
3. Ledoux L. Action of ribonuclease on certain ascites tumours. Nature 1955;175:258-9
4. Ledoux L. Action of ribonuclease on two solid tumours in vivo. Nature 1955;176:35-7
5. Ardelt W, Mikulski SM, Shogen K. Amino acid sequence of an anti-tumor protein from Rana pipiens oocytes and early embryos: homology to pancreatic ribonucleases. J Biol Chem 1991;266:245-51
6. Constanzi J, Sidransky D, Navon A, et al. Ribonucleases as a novel pro-apoptotic anticancer strategy: review of the preclinical and clinical data for ranpirnase. Cancer Invest 2005;23:643-50
7. Mikulski SM, Costanzi JJ, Vogelzang NJ, et al. Phase II trial of a single weekly intravenous dose of ranpirnase in patients with unresectable malignant mesothelioma. J Clin Oncol 2002;20:274-81
8. Rybak SM, Newton DL. Natural and engineered cytotoxic ribonucleases: therapeutic potential. Exp Cell Res 1999;253:325-35
9. Saxena SK, Sirdeshmukh R, Ardelts W, et al. Entry into cells and selective degradation of tRNA by a cytotoxic member of the RNase A family. J Biol Chem 2002;277:15142-6
10. Rutkoski TJ, Kurten EL, Mitchell JC, et al. Disruption of shape-complementary markers to create cytotoxic variants of ribonuclease A. J Mol Biol 2005;354:41-54
11. Grabarek J, Ardelt B, Du L, Darzynkiewicz Z. Activation of caspases and serine proteases during apoptosis induced by onconase (ranpirnase). Exp Cell 2002;278:61-71
12. Benito A, Ribo M, Vilanova M. On the track of antitumor ribonucleases. Mol BioSys 2005;1:294-302
13. Newton DL, Rybak SM. Antibody targeted therapeutics for lymphoma: new focus on the CD22 antigen and RNA. Expert Opin Biol Ther 2001;1:995-1003
14. Matousek J. The effect of bovine seminal ribonuclease (AS RNase) on cells of Crocker tumour in mice. Experientia 1973;29:858-9
15. Matousek J. Ribonucleases and their antitumor activity. Comp Biochem Physiol Toxicol Pharmacol 2001;129:175-91
16. D'Alessio G, Parente A, Guida C, et al. Dimeric structure of seminal ribonuclease. FEBS Lett 1972;27:285-8
17. Sakakibara F, Takayanagi G, Kawauchi H, et al. An anti-A-like lectin of Rana catesbiana eggs showing unusual reactivity. Biochim Biophys Acta 1976;444:386-95
18. Nitta K, Ozaki K, Tsukamoto Y, et al. Characterization of a Rana catesbeiana lectin-resistant mutant of leukemia P388 cells. Cancer Res 1994;54:928-34
19. Darzynkiewicz Z, Carter M, Mikulski S, et al. Cytostatic and cytotoxic effects of Pannon (P-30 Protein), a novel anticancer agent. Cell Tissue Kinet 1988;21:169-82
20. Ardelt W, Mikulski SM, Shogen K. Amino acid sequence of an anti-tumor protein from Rana pipiens oocytes and early embryos: homology to pancreatic ribonucleases. J Biol Chem 1991;266:245-51
21. Arnold U, Ulbrich-Hofmann R. Natural and engineered ribonucleases as potential cancer therapies. Biotechnol Lett 2006;28:1615-22
22. Youle RJ, D'Alessio G. Antitumor RNases. In: D'Alessio G, Riordan JF, editors, "Ribonucleases: structures and functions". Academic Press: New York; 1997. p. 491-514
23. Mosimann S, Johns K, Ardelt W, et al. Comparative molecular modeling and crystallization of P-30 protein; a novel antitumor protein of Rana pipiens oocytes and early embryos. Protein struct Funct Genet 1992;14:392-400
24. Notomista E, Catanzano F, Graziano G, et al. Onconase: an unusually stable protein. Biochemistry 2000;39:8711-8
25. Rodriguez M, Torrent G, Bosch M, et al. Intracellular pathway of onconase that enables its delivery to the cytosol. J Cell Sci 2007;120:1405-11
26. Kim DH, Kim EJ, Kalota A, et al. Possible mechanisms of improved radiation response by cytotoxic RNase, ONCONASE®, on A549 human lung cancer xenografts of nude mice. Adv Exp Med Biol 2007;599:53-9
27. Lee I, Kalota A, Gerwirtz AM, et al. Antitumor efficacy of the cytotoxic RNase, ranpirnase, on A549 human lung cancer xenografts of nude mice. Anticancer Res 2007;27:299-308
28. Michaelis M, Cinatl J, Anand P, et al. Onconase induces caspase-independent cell death in chemoresistant neuroblastoma cells. Cancer Lett 2007;250:107-16
29. Lee I, Shogen K. Mechanisms of enhanced tumoricidal efficacy of multiple small dosages of ranpirnase, the neovel cytotoxic ribonuclease, on lung cancer. Cancer Chemother Pharmacol Published online: 5 December 2007, doi:10.1007/s00280-007-0637-y.
30. Jain RK. Determinants of tumor blood flow: a review. Cancer Res 1988;48:2641-58
31. Lee I, Boucher Y, Jain RK. Nicotinamide can lower tumor interstitial fluid pressure: mechanistic and therapeutic implications. Cancer Res 1992;52:3237-40
32. Horsman MR, Chaplin DJ, Brown JM. Radiosensitization by nicotinamide in vivo: a greater enhancement of tumor damge compare to that of normal tissues. Radiat Res 1987;109:479-89
33. Coleman CN. Hypoxia in tumors: a paradigm or the approach to biochemical and physiological heterogeneity. JNCI 1988;80:310-7
34. Lee I, Cunningham WP, Levitt SH. Improvement in RBC flux, acidosis and oxygenation in the tumour microregions by Fluosol-DA 20%. Int J Radiat Biol 1991;60:695-705
35. Zlotecki RA, Boucher Y, Lee I, et al. Effect of angiotensin II induced hypertension on tumor blood flow and interstitial fluid pressure. Cancer Res 1993;53:2466-8
36. Nozue M, Lee I, Manning JM, et al. Oxygenation in tumors by modified hemoglobin. J Surg Oncol 1996;62:109-14
37. Donelly ET, Liu Y, Fatunmbi YO, et al. Effects of Texaphyrines on the oxygenation of EMT6 mouse mammary tumors. Int J Radiat Oncol Biol Phys 2004;58:1570-6
38. Mikulski EM, Shogen K, Bernstein EH, et al. Striking increase of survival of mice bearing M109 Madison carcinoma treated with a novel protein from amphibian embryos. JNCI 1990;82:151-3
39. Lee I, Lee YH, Mikulski SM, et al. Tumoricidal effects of onconase on various tumors. J Surg Oncol 2000;73:164-71
40. Servick EM, Jain RK. Geometric resistance in solid tumors perfused ex vivo: effects of tumor size and perfusion pressure. Cancer Res 1989;49:3506-12
41. Servick EM, Jain RK. Viscous resistance in solid tumors: effects of hematocrit on intratumor blood viscosity. Cancer Res 1989;49:3513-9
42. Jain RK. Transport of molecules in the tumor interstitium: a review. Cancer Res 1987;47:3039-51
43. Jain RK. Delivery of novel therapeutic agents in tumors: physiological barriers and strategies. JNCI 1989;81:570-6
44. Lee I, Kim DH, Sunar U, et al. The physiological mechanisms of ranpirnase-induced enhancement in radiation response on A549 human lung carcinoma xenografts in nude mice. Int J Radiat Oncol Biol Phys 2006;66:s580-1
45. Lee I, Kim DH, Sunar U, et al. The therapeutic mechanisms of ranpirnase-induced enhancement of radiation response on A549 human lung cancer. In Vivo 2007;21:721-8
46. Lee I, Glickson JD, Dewhirst MW, et al. Effect of mild hyperglycemia ± meta-iodo-benzylguanidine on the radiation response of two solid tumors. Adv Exp Med Biol 2003;530:177-86
47. Burd R, Wachsberger PR, Biaglow JE, et al. Absence of Crabtree effect in human melanoma cells adapted to growth at low pH: reversal by respiratory inhibitors. Cancer Res 2001;61:5630-5
48. Lee I, Lee YH, Mikulski SM, et al. Enhanced cellular radiation sensitivity of androgen-independent human prostate tumor cells by onconase. Anticancer Res 2000;20:1037-40
49. Sun H, Dai H, Shaik N. Drug efflux transporters in the CNS. Adv Drug Deliv Rev 2003;55:83-105
50. Lee I, Lee YH, Mikulski SM, et al. Effect of onconase ±tamoxifen on AsPC-1 human pancreatic tumors in nude mice. Adv Exp Med Biol 2003;530:187-96
51. Ramos-Nino ME, Vianale G, Sabo-Attwood T, et al. Human mesothelioma cells exhibit tumor cell-specific differences in phoshatidyllinositol 3-kinease/AKT activity that predict the efficacy of Onconase. Mol Cancer Ther 2005;4:835-42
52. Tsai SY, Ardelt B, Hsieh TC, et al. Treatment of Jurkat acute T-lymphocytic leukemia cells by Onconase (ranpirnase) is accompanied by an altered nucleocytoplasmic distribution and reduced expression of transcription factor NF-κB. Int J Oncol 2004;25:1745-52
53. Mikulski S. Phase I human clinical trial of Onconase (P-30 Protein) administered intravenously on a weekly schedule in cancer patients with solid tumors. Int J Oncol 1993;3:57-64
54. Mikulski S. Relationship between response rate and median survival in patients with advanced nonsmall cell lung cancer: comparison of ONCONASE with other cancer agents. Int J Oncol 1995;6:889-97
55. Vasandani VM, Burris JA, Sung C. Reversible nephrotoxicity of onconase and effect of lysine pH on renal onconase uptake. Cancer Chemother Pharmacol 1999;44:164-9
56. Pavlaskis N, Vogelzang NJ. Ranpirnase-an antitumour ribonuclease: its potential role in malignant mesothelioma. Expert Opin Biol Ther 2006;6:391-9
57. Mikulski SM, Viera A, Darzynkiewicz Z, et al. Synergism between a novel amphibian oocyte ribonuclease and lovastatin in inducing cytostatic and cytotoxic effects in human lung and pancreatic carcinoma cell lines. Br J Cancer 1992;66:304-10
58. Rybak SM, Pearson JW, Fogler WE, et al. Enhancement of vincristine cytotoxicity in drug-resistant cells by simultaneous treatment with onconase, an antitumor ribonuclease. JNCI 1996;88:747-53
59. Wu Y, Mikulski SM, Ardelt W, et al. A cytotoxic ribonuclease. Study of the mechanism of onconase cytotoxicity. J Biol Chem 1993;268:10686-93
60. Wu Y, Saxena SK, Ardelt W, et al. A study of the intracellular routing of cytotoxic ribonucleases. J Biol Chem 1995;270:17476-81
61. Mikulski SM, Viera A, Deptala A, et al. Enhanced in vitro cytotoxicity and cytostasis of the combination of onconase with a proteasome inhibitor. Int J Oncol 1998;13:633-44
62. Henk JM, Smith CW. Radiotherapy and hyperbaric oxygen in head and neck cancer. Lancet 1977;1:104-5
63. Varnes ME, Dethlefsen LA, Biaglow JE. The effect of pH on potentially lethal damage recovery in A549 cells. Radiat Res 1986;108:80-90
64. Jayanth VR, Bayne MT, Varnes ME. Effects of extracellular and intracellular pH on repair of potentially lethal damage, chromosome aberrations and DNA double-strand breaks in irradiated plateau-phase A549 cells. Radiat Res 1994;139:152-62
65. Vogelzang NJ, Aklilu M, Stadler WM, et al. A phase II trial of weekly intravenous ranpirnase (Onconase), a novel ribonuclease in patients with metastatic kidney cancer. Invest New Drugs 2001;19:255-60
66. L858R non-small-cell lung cancer line H3255. Cancer Res 2004;64:7241-4
67. Johnson BE, Jaenne PA. Epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Cancer Res 2005;65:7525-9
68. Sordella R, Bell DW, Harber DA, et al. Gefitinib-sensitizing EFGR mutations in lung cancer activate anti-apoptotic pathway. Science 2004;305:1163-7