Assessment of the tumourigenic and metastatic properties of SK-MEL28 melanoma cells surviving electrochemotherapy with bleomycin

Radiology and Oncology

Volumn 46, Issue 1, 2012, Pages 32-45

  Todorovic, Vesna ^a,b   Sersa, Gregor ^a   Mlakar, Vid ^c   Glavac, Damjan ^c   Cemazar, Maja ^a,b  

^a INSTITUTE OF ONCOLOGY   (Slovenia)

^b UNIVERSITY OF PRIMORSKA   (Slovenia)

^c INSTITUTE OF PATHOLOGY   (Slovenia)

Author keywords

bleomycin; electrochemotherapy; electroporation; melanoma; metastatic potential; microarray analysis

Indexed keywords

BLEOMYCIN SULFATE; MATRIGEL;

ARTICLE; CANCER INVASION; CARCINOGENESIS; CARCINOGENIC ACTIVITY; CELL INVASION; CELL MIGRATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ELECTROCHEMOTHERAPY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MELANOMA; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE;

EID: 84858234951     PISSN: 13182099     EISSN: 15813207     Source Type: Journal    
DOI: 10.2478/v10019-012-0010-6     Document Type: Article

References (62)

1. Coghlin C, Murray GI. Current and emerging concepts in tumour metastasis. J Pathol 2010; 222: 1-15.
2. Nguyen DX. Tracing the origins of metastasis. J Pathol 2011; 223: 195-204.
3. Chiang AC, Massague J. Molecular basis of metastasis. N Engl J Med 2008; 359: 2814-23.
4. Roh JL, Sung MW, Kim KH. Suppression of accelerated tumor growth in surgical wounds by celecoxib and indomethacin. Head Neck 2005; 27: 326-32. (Pubitemid 40418605)
5. Brown LM, Welch DR, Rannels SR. B16F10 melanoma cell colonization of mouse lung is enhanced by partial pneumonectomy. Clin Exp Metastasis 2002; 19: 369-76. (Pubitemid 34876204)
6. Hofer SO, Shrayer D, Reichner JS, Hoekstra HJ, Wanebo HJ. Wound-induced tumor progression: a probable role in recurrence after tumor resection. Arch Surg 1998; 133: 383-9. (Pubitemid 28193522)
7. Rofstad EK, Mathiesen B, Galappathi K. Increased metastatic dissemination in human melanoma xenografts after subcurative radiation treatment: radiation-induced increase in fraction of hypoxic cells and hypoxia-induced up-regulation of urokinase-type plasminogen activator receptor. Cancer Res 2004; 64: 13-8. (Pubitemid 38114074)
8. Goetze K, Scholz M, Taucher-Scholz G, Mueller-Klieser W. The impact of conventional and heavy ion irradiation on tumor cell migration in vitro. Int J Radiat Biol 2007; 83: 889-96. (Pubitemid 350219105)
9. Ogata T, Teshima T, Kagawa K, Hishikawa Y, Takahashi Y, Kawaguchi A, et al. Particle irradiation suppresses metastatic potential of cancer cells. Cancer Res 2005; 65: 113-20. (Pubitemid 40070802)
10. Wild-Bode C, Weller M, Rimner A, Dichgans J, Wick W. Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma. Cancer Res 2001; 61: 2744-50. (Pubitemid 32685864)
11. Cheng JC, Chou CH, Kuo ML, Hsieh CY. Radiation-enhanced hepatocellular carcinoma cell invasion with MMP-9 expression through PI3K/Akt/NFkappaB signal transduction pathway. Oncogene 2006; 25: 7009-18. (Pubitemid 44722069)
12. Mir LM, Orlowski S, Belehradek J, Jr., Paoletti C. Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses. Eur J Cancer 1991; 27: 68-72.
13. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1982; 1: 841-5.
14. Rols MP. Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells. Biochim Biophys Acta 2006; 1758: 423-8.
15. Sersa G, Miklavcic D, Cemazar M, Rudolf Z, Pucihar G, Snoj M. Electrochemotherapy in treatment of tumours. Eur J Surg Oncol 2008; 34: 232-40.
16. Sersa G, Stabuc B, Cemazar M, Miklavcic D, Rudolf Z. Electrochemotherapy with cisplatin: clinical experience in malignant melanoma patients. Clin Cancer Res 2000; 6: 863-7. (Pubitemid 30159341)
17. Belehradek M, Domenge C, Luboinski B, Orlowski S, Belehradek J, Jr., Mir LM. Electrochemotherapy, a new antitumor treatment. First clinical phase I-II trial. Cancer 1993; 72: 3694-700. (Pubitemid 24000606)
18. Quaglino P, Mortera C, Osella-Abate S, Barberis M, Illengo M, Rissone M, et al. Electrochemotherapy with intravenous bleomycin in the local treatment of skin melanoma metastases. Ann Surg Oncol 2008; 15: 2215-22.
19. 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: 229-35.
20. Marty M, Sersa G, Garbay JR, Gehl J, Collins CG, Snoj M, et al. Electrochemotherapy - An easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: Results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study. EJC Suppl 2006; 4: 3-13. (Pubitemid 44755131)
21. Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat Rev Cancer 2006; 6: 583-92. (Pubitemid 44140857)
22. Miklavcic D, Corovic S, Pucihar G, Pavselj N. Importance of tumour coverage by sufficiently high local electric field for effective electrochemotherapy. EJC Suppl 2006; 4: 45-51. (Pubitemid 44666531)
23. Ramirez LH, Orlowski S, An D, Bindoula G, Dzodic R, Ardouin P, et al. Electrochemotherapy on liver tumours in rabbits. Br J Cancer 1998; 77: 2104-11. (Pubitemid 28263929)
24. Mlakar V, Todorovic V, Cemazar M, Glavac D, Sersa G. Electric pulses used in electrochemotherapy and electrogene therapy do not significantly change the expression profile of genes involved in the development of cancer in malignant melanoma cells. BMC Cancer 2009; 9: 299.
25. Todorovic V, Sersa G, Mlakar V, Glavac D, Flisar K, Cemazar M. Metastatic potential of melanoma cells is not affected by electrochemotherapy. Melanoma Res 2011; 21: 196-205.
26. Hague A, Jones GE. Cell motility assays. Cell Biol Toxicol 2008; 24: 381-9.
27. Spessotto P, Giacomello E, Perri R. Improving fluorescence-based assays for the in vitro analysis of cell adhesion and migration. Mol Biotechnol 2002; 20: 285-304. (Pubitemid 34252639)
28. Wach F, Eyrich AM, Wustrow T, Krieg T, Hein R. Comparison of migration and invasiveness of epithelial tumor and melanoma cells in vitro. J Dermatol Sci 1996; 12: 118-26. (Pubitemid 26201796)
29. Li L, Dragulev B, Zigrino P, Mauch C, Fox JW. The invasive potential of human melanoma cell lines correlates with their ability to alter fibroblast gene expression in vitro and the stromal microenvironment in vivo. Int J Cancer 2009; 125: 1796-804.
30. Cleveland WS, Devlin SJ. Locally Weighted Regression - an Approach to Regression-Analysis by Local Fitting. J Am Stat Assoc 1988; 83: 596-610.
31. Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res 2005; 33: W741-8. (Pubitemid 44530021)
32. 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: 1386-91. (Pubitemid 29116794)
33. Cemazar M, Parkins CS, Holder AL, Chaplin DJ, Tozer GM, Sersa G. Electroporation of human microvascular endothelial cells: evidence for an anti-vascular mechanism of electrochemotherapy. Br J Cancer 2001; 84: 565-70. (Pubitemid 32215887)
34. Cemazar M, Miklavcic D, Sersa G. Intrinsic sensitivity of tumor cells to bleomycin as an indicator of tumor response to electrochemotherapy. Jpn J Cancer Res 1998; 89: 328-33. (Pubitemid 28197299)
35. Ogihara M, Yamaguchi O. Potentiation of effects of anticancer agents by local electric pulses in murine bladder cancer. Urol Res 2000; 28: 391-7. (Pubitemid 32039609)
36. Todorovic V, Sersa G, Flisar K, Cemazar M. Enhanced cytotoxicity of bleomycin and cisplatin after electroporation in murine colorectal carcinoma cells. Radiol Oncol 2009; 43: 264-73.
37. Demicheli R, Retsky MW, Hrushesky WJ, Baum M, Gukas ID. The effects of surgery on tumor growth: a century of investigations. Ann Oncol 2008; 19: 1821-8.
38. Paganin-Gioanni A, Bellard E, Paquereau L, Ecochard V, Golzio M, Teissie J. Fluorescence imaging agents in cancerology. Radiol Oncol 2010; 44: 142-48.
39. Singh RK, Gutman M, Reich R, Bar-Eli M. Ultraviolet B irradiation promotes tumorigenic and metastatic properties in primary cutaneous melanoma via induction of interleukin 8. Cancer Res 1995; 55: 3669-74.
40. Strojan P. Role of radiotherapy in melanoma management. Radiol Oncol 2010; 44: 1-12.
41. Testori A, Tosti G, Martinoli C, Spadola G, Cataldo F, Verrecchia F, et al. Electrochemotherapy for cutaneous and subcutaneous tumor lesions: a novel therapeutic approach. Dermatol Ther 2010; 23: 651-61.
42. Zupanic A, Corovic S, Miklavcic D. Optimization of electrode position and electric pulse amplitude in electrochemotherapy. Radiol Oncol 2008; 42: 93-101. (Pubitemid 351841993)
43. Cordes N, Blaese MA, Meineke V, Van Beuningen D. Ionizing radiation induces up-regulation of functional beta1-integrin in human lung tumour cell lines in vitro. Int J Radiat Biol 2002; 78: 347-57. (Pubitemid 34496887)
44. Hojman P, Zibert JR, Gissel H, Eriksen J, Gehl J. Gene expression profiles in skeletal muscle after gene electrotransfer. BMC Mol Biol 2007; 8: 56.
45. Rubenstrunk A, Mahfoudi A, Scherman D. Delivery of electric pulses for DNA electrotransfer to mouse muscle does not induce the expression of stress related genes. Cell Biol Toxicol 2004; 20: 25-31. (Pubitemid 38478128)
46. Heller LC, Cruz YL, Ferraro B, Yang H, Heller R. Plasmid injection and application of electric pulses alter endogenous mRNA and protein expression in B16.F10 mouse melanomas. Cancer Gene Ther 2010; 17: 864-71.
47. Dallas PB, Gottardo NG, Firth MJ, Beesley AH, Hoffmann K, Terry PA, et al. Gene expression levels assessed by oligonucleotide microarray analysis and quantitative real-time RT-PCR - how well do they correlate? BMC Genomics 2005; 6: 59-68.
48. Morey JS, Ryan JC, Van Dolah FM. Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 2006; 8: 175-93. (Pubitemid 44942143)
49. Putnam AJ, Schulz VV, Freiter EM, Bill HM, Miranti CK. Src, PKCalpha, and PKCdelta are required for alphavbeta3 integrin-mediated metastatic melanoma invasion. Cell Commun Signal 2009; 7: 10-27.
50. La Porta CA, Comolli R. Overexpression of nPKCdelta in BL6 murine melanoma cells enhances TGFbeta1 release into the plasma of metastasized animals. Melanoma Res 2000; 10: 527-34. (Pubitemid 32011974)
51. La Porta CA, Di Dio A, Porro D, Comolli R. Overexpression of novel protein kinase C delta in BL6 murine melanoma cells inhibits the proliferative capacity in vitro but enhances the metastatic potential in vivo. Melanoma Res 2000; 10: 93-102. (Pubitemid 30256871)
52. Dissanayake SK, Wade M, Johnson CE, O'Connell MP, Leotlela PD, French AD, et al. The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J Biol Chem 2007; 282: 17259-71. (Pubitemid 47093253)
53. Hendrix MJ, Seftor EA, Seftor RE, Trevor KT. Experimental co-expression of vimentin and keratin intermediate filaments in human breast cancer cells results in phenotypic interconversion and increased invasive behavior. Am J Pathol 1997; 150: 483-95. (Pubitemid 27073779)
54. McInroy L, Maatta A. Down-regulation of vimentin expression inhibits carcinoma cell migration and adhesion. Biochem Biophys Res Commun 2007; 360: 109-14. (Pubitemid 46990330)
55. Miyazaki K. Laminin-5 (laminin-332): Unique biological activity and role in tumor growth and invasion. Cancer Sci 2006; 97: 91-8. (Pubitemid 43379475)
56. Tsuji T, Kawada Y, Kai-Murozono M, Komatsu S, Han SA, Takeuchi K, et al. Regulation of melanoma cell migration and invasion by laminin-5 and alpha-3beta1 integrin (VLA-3). Clin Exp Metastasis 2002; 19: 127-34. (Pubitemid 34264082)
57. Lohi J. Laminin-5 in the progression of carcinomas. Int J Cancer 2001; 94: 763-7. (Pubitemid 33032821)
58. Lee MP, Feinberg AP. Genomic imprinting of a human apoptosis gene homologue, TSSC3. Cancer Res 1998; 58: 1052-6. (Pubitemid 28182478)
59. Stiban J, Tidhar R, Futerman AH. Ceramide synthases: roles in cell physiology and signaling. Adv Exp Med Biol 2010; 688: 60-71.
60. Mekid H, Tounekti O, Spatz A, Cemazar M, El Kebir FZ, Mir LM. In vivo evolution of tumour cells after the generation of double-strand DNA breaks. Br J Cancer 2003; 88: 1763-71. (Pubitemid 36760422)
61. Nagy E, Balogi Z, Gombos I, Akerfelt M, Bjorkbom A, Balogh G, et al. Hyperfluidization-coupled membrane microdomain reorganization is linked to activation of the heat shock response in a murine melanoma cell line. Proc Natl Acad Sci U S A 2007; 104: 7945-50. (Pubitemid 47185856)
62. Vigh L, Horvath I, Maresca B, Harwood JL. Can the stress protein response be controlled by 'membrane-lipid therapy'? Trends Biochem Sci 2007; 32: 357-63. (Pubitemid 47126860)