Electroporation increases antitumoral efficacy of the bcl-2 antisense G3139 and chemotherapy in a human melanoma xenograft

Journal of Translational Medicine

Volumn 9, Issue 1, 2011, Pages

  Spugnini, Enrico P ^a   Biroccio, Annamaria ^a   De Mori, Roberta ^a   Scarsella, Marco ^a   D'Angelo, Carmen ^a   Baldi, Alfonso ^b   Leonetti, Carlo ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; CISPLATIN; MESSENGER RNA; OBLIMERSEN; PROTEIN BCL 2; ANTINEOPLASTIC AGENT; ANTISENSE OLIGONUCLEOTIDE; NUCLEOTIDE; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL PROLIFERATION; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; ELECTROPORATION; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MELANOMA; MONOTHERAPY; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTO ONCOGENE; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; THERAPY EFFECT; TREATMENT PLANNING; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; DRUG EFFECT; DRUG SCREENING; ELECTRODE; GENETICS; METABOLISM; METHODOLOGY; MULTIMODALITY CANCER THERAPY; PATHOLOGY; SKELETAL MUSCLE; TREATMENT OUTCOME; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; COMBINED MODALITY THERAPY; DOWN-REGULATION; ELECTRODES; ELECTROPORATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MICE; MUSCLE, SKELETAL; NEOPLASM PROTEINS; OLIGONUCLEOTIDES, ANTISENSE; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, MESSENGER; THIONUCLEOTIDES; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79960655569     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-9-125     Document Type: Article

References (60)

1. Eckstein F. Phosphorothioate oligodeoxynucleotides: what is their origin and what is unique about them?. Antisense Nucleic Acid Drug Dev 2000, 10:117-121. 10.1089/oli.1.2000.10.117, 10805163.
2. Gleave ME, Monia BP. Antisense therapy for cancer. Nat Rev Cancer 2005, 5:468-479. 10.1038/nrc1631, 15905854.
3. Leonetti C, D'Agnano I, Lozupone F, Valentini A, Geiser T, Zon G, Calabretta B, Citro GC, Zupi G. Antitumor effect of c-myc antisense phosphorothioate oligodeoxynucleotides on human melanoma cells in vitro and and in mice. J Natl Cancer Inst 1996, 88:419-429. 10.1093/jnci/88.7.419, 8618233.
4. Leonetti C, Biroccio A, Candiloro A, Citro G, Fornari C, Mottolese M, Del Bufalo D, Zupi G. Increase of cisplatin sensitivity by c-myc antisense oligodeoxynucleotides in a human metastatic melanoma inherently resistant to cisplatin. Clin Cancer Res 1999, 5:2588-2595.
5. Zupi G, Scarsella M, Semple SC, Mottolese M, Natali PG, Leonetti C. Antitumor efficacy of bcl-2 and c-myc antisense oligonucleotides in combination with cisplatin in human melanoma xenografts: relevance of administration sequence. Clinical Cancer Res 2005, 11:1990-1995.
6. Leonetti C, Biroccio A, D'Angelo C, Semple SC, Scarsella M, Zupi G. Therapeutic integration of c-myc and bcl-2 antisense molecules with docetaxel in a preclinical model of hormone-refractory prostate cancer. Prostate 2007, 67:1475-1485. 10.1002/pros.20636, 17654511.
7. Jansen B, Schlagbauer-Wadl H, Brown BD, Bryan RN, van Elsas A, Müller M, Wolff K, Eichler HG, Pehamberger H. bcl-2 antisense therapy chemosensitizes human melanoma in SCID mice. Nat Med 1998, 4:232-234. 10.1038/nm0298-232, 9461199.
8. Jansen B, Wacheck V, Heere-Ress E, Schlagbauer-Wadl H, Hoeller C, Lucas T, Hoermann M, Hollenstein U, Wolff K, Pehamberger H. Chemosensitisation of malignant melanoma by BCL2 antisense therapy. Lancet 2000, 356:1728-1733. 10.1016/S0140-6736(00)03207-4, 11095261.
9. Bedikian AY, Millward M, Pehamberger H, Conry R, Gore M, Trefzer U, Pavlick AC, DeConti R, Hersh EM, Hersey P, Kirkwood JM, Haluska FG, . Oblimersen Melanoma Study Group Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma. J Clin Oncol 2006, 24:4738-4745. 10.1200/JCO.2006.06.0483, 16966688, Oblimersen Melanoma Study Group.
10. Putney SD, Brown J, Cucco C, Lee R, Skorski T, Leonetti C, Geiser T, Calabretta B, Zupi G, Zon G. Enhanced anti-tumor effects with microencapsulated c-myc antisense oligonucleotide. Antisense Nucleic Acid Drug Dev 1999, 9:451-458. 10.1089/oli.1.1999.9.451, 10555152.
11. Gokhale PC, Soldatenkov V, Wang F-H, Rahman A, Dritschilo A, Kasid U. Antisense raf oligodeoxynucleotide is protected by liposomal encapsulation and inhibit Raf-1 protein expression in vitro and in vivo: Implications for gene therapy of radioresistant cancer. Gene Ther 1997, 4:1289-1299. 10.1038/sj.gt.3300543, 9472552.
12. Gokhale PC, McRae D, Monia BP, Bagg A, Rahman A, Dritschilo A, Kasid U. Antisense raf oligodeoxyribonucleotide is a radiosensitizer in vivo. Antisense Nucleic Acid Drug Dev 1999, 9:191-201. 10.1089/oli.1.1999.9.191, 10355825.
13. Pagnan G, Stuart DD, Pastorino F, Raffaghello L, Montaldo PG, Allen TM, Calabretta B, Ponzoni M. Delivery of c-myb antisense oligodeoxynucleotides to human neuroblastoma cells via disialoganglioside GD2-targeted immunoliposomes: antitumor effects. J Natl Cancer Inst 2000, 92:253-261. 10.1093/jnci/92.3.253, 10655443.
14. Stuart DD, Kao GY, Allen TM. A novel, long-circulating, and functional liposomal formulation of antisense oligodeoxynucleotides targeted against MDR1. Cancer Gene Ther 2000, 7:466-475. 10.1038/sj.cgt.7700145, 10766353.
15. Leonetti C, Biroccio A, Benassi B, Stringaro A, Stoppacciaro A, Semple SC, Zupi G. Encapsulation of c-myc antisense oligodeoxynucleotides in lipid particles improves antitumoral efficacy in vivo in a human melanoma line. Cancer Gene Ther 2001, 8:459-468. 10.1038/sj.cgt.7700326, 11498766.
16. Senda M, Takeda J, Abe S, Nakamura T. Induction of cell fusion of plant protoplasts by electrical stimulation. Plant Cell Physiol 1979, 20:1441-1443.
17. Zimmermann U, Scheurich P. High frequency fusion of plant protoplasts by electric fields. Planta 1981, 151:26-32.
18. Sugar IP, Neumann E. Stochastic model for electric field-induced membrane pores. Biophysical Chemistry 1984, 19:211-225. 10.1016/0301-4622(84)87003-9, 6722274.
19. Mir LM, Banoun H, Paoletti C. Introduction of definite amounts of nonpermanent molecules into living cells after electropermeabilization: direct access to cytosol. Exp Cell Res 1988, 175:15-25. 10.1016/0014-4827(88)90251-0, 3345798.
20. Lo MMS, Tsong TY, Conrad MK, Strittmatter SM, Hester LD, Snyder SH. Monoclonal antibody production by receptor-mediated electrically induced cell fusion. Nature 1984, 31:792-794.
21. Orlowski S, Belehradec J, Paoletti C, Mir LM. Transient electropermeabilization of cells in culture. Increase of the cytotoxicity of anticancer drugs. Biochem Pharmacol 1988, 37:4727-4733. 10.1016/0006-2952(88)90344-9, 2462423.
22. Fromm M, Taylor LP, Walbot V. Expression of genes transferred into monocot and dicot plant cells by electroporation. Proc Nat Acad Sci USA 1985, 82:5824-5828. 10.1073/pnas.82.17.5824, 390645, 3862099.
23. Poddevin B, Orlowski S, Belehradek J, Mir LM. Very high cytotoxicity of bleomycin introduced into the cytosol of cells in culture. Biochem Pharmacol 1991, 42(Suppl):67-75.
24. Belehradek M, Domenge C, Luboinski B, Orlowski S, Belehradek J, Mir LM. Electrochemotherapy, a new antitumor treatment. First clinical phase I-II trial. Cancer 1993, 72:3694-3700. 10.1002/1097-0142(19931215)72:12<3694::AID-CNCR2820721222>3.0.CO;2-2, 7504576.
25. Rudolf Z, Stabuc B, Cemazar M, Miklavcic D, Vodovnik L, Sersa G. Electrochemotherapy with bleomycin. The first clinical experience in malignant melanoma patients. Radiol Oncol 1995, 29:229-235.
26. Heller R, Jaroszeski M, Glass FL, Messina JL, Rapaport DP, DeConti RC, Fenske NA, Gilbert RA, Mir LM, Reintgen DS. Phase I/II trial for the management of cutaneous and subcutaneous tumors using electrochemotherapy. Cancer 1996, 77:964-971. 10.1002/(SICI)1097-0142(19960301)77:5<964::AID-CNCR24>3.0.CO;2-0, 8608491.
27. Daskalov I, Mudrov N, Peycheva E. Exploring new instrumentation parameters for electrochemotherapy. IEEE Eng Med Biol Mag 1999, 18:62-66. 10.1109/51.740982, 9934602.
28. Spugnini EP, Dotsinsky I, Mudrov N, Citro G, D'Avino A, Baldi A. Biphasic pulses enhance bleomycin efficacy in a spontaneous canine genital tumor model of chemoresistance: Sticker sarcoma. J Exp Clin Cancer Res 2008, 27:58. 10.1186/1756-9966-27-58, 2596090, 18980687.
29. Spugnini EP, Porrello A. Potentiation of chemotherapy in companion animals with spontaneous large neoplasms by application of biphasic electric pulses. J Exp Clin Cancer Res 2003, 22:571-580.
30. Spugnini EP, Vincenzi B, Baldi F, Citro G, Baldi A. Adjuvant electrochemotherapy for the treatment of incompletely resected canine mast cell tumors. Anticancer Res 2006, 26:4585-4589.
31. Spugnini EP, Baldi A, Vincenzi B, Bongiorni F, Bellelli C, Porrello A. Intraoperative versus postoperative electrochemotherapy in soft tissue sarcomas: a preliminary study in a spontaneous feline model. Cancer Chemother Pharmacol 2007, 59:375-381.
32. Spugnini EP, Vincenzi B, Citro G, Santini D, Dotsinsky I, Mudrov N, Montesarchio V, Laieta MT, Esposito V, Baldi A. Adjuvant electrochemotherapy for the treatment of incompletely excised spontaneous canine sarcomas. In Vivo 2007, 21:819-822.
33. Spugnini EP, Baldi F, Mellone P, Feroce F, D'Avino A, Bonetto F, Vincenzi B, Citro G, Baldi A. Patterns of tumor response in canine and feline cancer patients treated with electrochemotherapy: preclinical data for the standardization of this treatment in pets and humans. J Transl Med 2007, 5:48. 10.1186/1479-5876-5-48, 2082020, 17910745.
34. Spugnini EP, Citro G, Mellone P, Dotsinsky I, Mudrov N, Baldi A. Electrochemotherapy for localized lymphoma: a preliminary study in companion animals. J Exp Clin Cancer Res 2007, 26:343-346.
35. Peycheva E, Daskalov I, Tsoneva I. Electrochemotherapy of Mycosis fungoides by interferon-alpha. Bioelectrochemistry 2007, 70:283-286. 10.1016/j.bioelechem.2006.10.006, 17150416.
36. Mennuni C, Calvaruso F, Zampaglione I, Rizzuto G, Rinaudo D, Dammassa E, Ciliberto G, Fattori E, La Monica N. Hyaluronidase increases electrogene transfer efficiency in skeletal muscle. Hum Gene Ther 2002, 13:355-365. 10.1089/10430340252792495, 11860703.
37. Zaharoff DA, Barr RC, Yuan F. Electromobility of plasmid DNA in tumor tissues during electric field-mediated gene delivery. Gene Ther 2002, 9:1286-1290. 10.1038/sj.gt.3301799, 12224011.
38. Spugnini EP, Citro G, Porrello A. Rational design of new electrodes for electrochemotherapy. J Exp Clin Cancer Res 2005, 24:245-254.
39. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta CT). Method Methods 2001, 25:402-408.
40. Dummer R, Hauschild A, Jost L, . ESMO Guidelines Working Group Cutaneous malignant melanoma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 2008, 19(Suppl 2):ii86-ii88. ESMO Guidelines Working Group.
41. Mouawad R, Sebert M, Michels J, Bloch J, Spano JP, Khayat D. Treatment for metastatic malignant melanoma: old drugs and new strategies. Crit Rev Oncol Hematol 2010, 74:27-39. 10.1016/j.critrevonc.2009.08.005, 19781957.
42. Argawala SS, Neuberg D, Park Y, Kirkwood JM. Mature results of a phase III, randomized trial of bacillus Calmette-Guerin (BCG) versus observation and BCG plus dacarbazine versus BCG in the adjuvant therapy of American Joint Committee on Cancer stage I-III melanoma (E1673): a trial of the Eastern Oncology Group. Cancer 2004, 100:1692-1698. 10.1002/cncr.20166, 15073858.
43. Sersa G, Stabuc B, Cemazar M, Miklavcic D, Rudolf Z. Electrochemotherapy with cisplatin: clinical experience in malignant melanoma patients. Clin Cancer Res 2000, 6:863-867.
44. Rols MP, Bachaud JM, Giraud P, Chevreau C, Roche H, Teissie J. Electrochemotherapy of cutaneous metastases in malignant melanoma. Melanoma Res 2000, 10:468-474. 10.1097/00008390-200010000-00009, 11095408.
45. Byrne CM, Thompson JF, Johnston H, Hersey P, Quinn MJ, Michael Hughes T, McCarthy WH. Treatment of metastatic melanoma using electroporation therapy with bleomycin (electrochemotherapy). Melanoma Res 2005, 15:45-51. 10.1097/00008390-200502000-00008, 15714120.
46. Gehl J, Geertsen PF. Efficient palliation of haemorrhaging malignant melanoma skin metastases by electrochemotherapy. Melanoma Res 2000, 10:1-5.
47. Landström FJ, Nilsson CO, Crafoord S, Reizenstein JA, Adamsson GB, Löfgren LA. Electroporation therapy of skin cancer in the head and neck area. Dermatol Surg 2010, 36:1245-1250. 10.1111/j.1524-4725.2010.01617.x, 20666812.
48. Pech M, Janitzky A, Wendler JJ, Strang C, Blaschke S, Dudeck O, Ricke J, Liehr UB. Irreversible electroporation of renal cell carcinoma: A first-in-man Phase I clinical study. Cardiovasc Intervent Radiol 2011, 34:132-138. 10.1007/s00270-010-9964-1, 20711837.
49. Lee EW, Chen C, Prieto VE, Dry SM, Loh CT, Kee ST. Advanced hepatic ablation technique for creating complete cell death: irreversible electroporation. Radiology 2010, 255:426-433. 10.1148/radiol.10090337, 20413755.
50. Neal RE, Singh R, Hatcher HC, Kock ND, Torti SV, Davalos RV. Treatment of breast cancer through the application of irreversible electroporation using a novel minimally invasive single needle electrode. Breast Cancer Res Treat 2010, 123:295-301. 10.1007/s10549-010-0803-5, 3021965, 20191380.
51. Reed SD, Fulmer A, Buckholz J, Zhang B, Cutrera J, Shiomitsu K, Li S. Bleomycin/interleukin-12 electrochemogenetherapy for treating naturally occurring spontaneous neoplasms in dogs. Cancer Gene Ther 2010, 17:571-578. 10.1038/cgt.2010.13, 3148143, 20414325.
52. Horton HM, Lalor PA, Rolland AP. IL-2 plasmid electroporation: from preclinical studies to phase I clinical trial. Methods Mol Biol 2008, 423:361-372. 10.1007/978-1-59745-194-9_28, 18370214.
53. Spugnini EP, Dragonetti E, Vincenzi B, Onori N, Citro G, Baldi A. Pulse mediated chemotherapy enhances local control and survival in a spontaneous canine model of primary mucosal melanoma. Melanoma Res 2006, 16:23-27. 10.1097/01.cmr.0000195702.73192.a0, 16432452.
54. Reed JC. Bcl-2-family proteins and hematologic malignancies: history and future prospects. Blood 2008, 111:3322-3330. 10.1182/blood-2007-09-078162, 2275002, 18362212.
55. Lopes de Menezes DE, Mayer LD. Pharmacokinetics of Bcl-2 antisense oligonucleotide (G3139) combined with doxorubicin in SCID mice bearing human breast cancer solid tumor xenografts. Cancer Chemother Pharmacol 2002, 49:57-68. 10.1007/s00280-001-0385-3, 11855753.
56. Mita MM, Ochoa L, Rowinsky EK, Kuhn J, Schwartz G, Hammond LA, Patnaik A, Yeh IT, Izbicka E, Berg K, Tolcher AW. A phase I, pharmacokinetic and biologic correlative study of oblimersen sodium (Genasense, G3139) and irinotecan in patients with metastatic colorectal cancer. Ann Oncol 2006, 17:313-321.
57. Lai JC, Benimetskaya L, Santella RM, Wang Q, Miller PS, Stein CA. ODN bcl-2 (oblimersen) may inhibit prostate cancer cell growth in a partially bis-CpG-dependent non-antisense manner. Mol Cancer Ther 2003, 2:1031-1043.
58. Cemazar M, Miklavcic D, Scancar J, Dolzan V, Golouh R, Sersa G. Increased platinum accumulation in SA-1 tumour cells after in vivo electrochemotherapy with cisplatin. Br J Cancer 1999, 79:1386-1391. 10.1038/sj.bjc.6690222, 2374264, 10188880.
59. Sersa G, Cemazar M, Miklavcic D, Chaplin DJ. Tumor blood flow modifying effect of electrochemotherapy with bleomycin. Anticancer Research 1999, 19:4017-4022.
60. Sersa G, Jarm T, Kotnik T, Coer A, Podkrajsek M, Sentjurc M, Miklavcic D, Kadivec M, Kranjc S, Secerov A, Cemazar M. Vascular disrupting action of electroporation and electrochemotherapy with bleomycin in murine sarcoma. Br J Cancer 2008, 98:388-398. 10.1038/sj.bjc.6604168, 2361464, 18182988.