Modulation of Activity of Known Cytotoxic Ruthenium(III) Compound (KP418) with Hampered Transmembrane Transport in Electrochemotherapy In Vitro and In Vivo

Journal of Membrane Biology

Volumn 247, Issue 12, 2014, Pages 1239-1251

  Hudej, Rosana ^a,b   Miklavcic, Damijan ^a   Cemazar, Maja ^c,d   Todorovic, Vesna ^c   Sersa, Gregor ^c   Bergamo, Alberta ^e   Sava, Gianni ^e,f   Martincic, Anze ^g   Scancar, Janez ^g   Keppler, Bernhard K ^h   Turel, Iztok ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b BIA SEPARATIONS D O O   (Slovenia)

^c INSTITUTE OF ONCOLOGY   (Slovenia)

^d UNIVERSITY OF PRIMORSKA   (Slovenia)

^e Callerio Foundation   (Italy)

^f UNIVERSITY OF TRIESTE   (Italy)

^g JO EF STEFAN INSTITUTE   (Slovenia)

^h UNIVERSITY OF VIENNA   (Austria)

Author keywords

Electrochemotherapy; In vitro; In vivo; KP418; Metastatic potential; Ruthenium

Indexed keywords

ANTINEOPLASTIC AGENT; IMIDAZOLIUM TETRACHLOROBIS(1H-IMIDAZOLE)RUTHENATE(III); ORGANOMETALLIC COMPOUND; RUTHENIUM;

ANIMAL; CELL MEMBRANE; ELECTROCHEMOTHERAPY; ELECTROPORATION; FIBROSARCOMA; IN VITRO STUDY; MELANOMA, EXPERIMENTAL; METABOLISM; MOUSE; PHYSIOLOGY; PROCEDURES; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; CELL MEMBRANE; ELECTROCHEMOTHERAPY; ELECTROPORATION; FIBROSARCOMA; IN VITRO TECHNIQUES; MELANOMA, EXPERIMENTAL; MICE; ORGANOMETALLIC COMPOUNDS; RUTHENIUM;

EID: 84936126475     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-014-9696-2     Document Type: Article

References (45)

1. Antonarakis ES, Emadi A (2010) Ruthenium-based chemotherapeutics: are they ready for prime time? Cancer Chemoth Pharm 66:1–9
2. Bergamo A, Masi A, Jakupec MA, Keppler BK, Sava G (2009) Inhibitory effect of the ruthenium complex KP1019 in models of mammary cancer cell migration and invasion. Met-Based Drugs. doi:10.1155/2009/681270
3. Berger MR, Garzon FT, Keppler BK, Schmähl D (1989) Efficacy of new ruthenium complexes against chemically induced autochthonous colorectal carcinoma in rats. Anticancer Res 9:761–766
4. Bicek A, Turel I, Kanduser M, Miklavcic D (2007) Combined therapy of the antimetastatic compound NAMI-A and electroporation on B16F1 tumour cells in vitro. Bioelectrochemistry 71:113–117
5. Brincker H (1993) Direct intratumoral chemotherapy. Crit Rev Oncol Hemat 15:91–98
6. Cemazar M, Miklavcic D, Vodovnik L, Jarm T, Rudolf Z, Stabuc B, Cufer T, Sersa G (1995) Improved therapeutic effect of electrochemotherapy with cisplatin by intratumoral drug administration and changing of electrode orientation for electropermeabilization on EAT tumor model in mice. Radiol Oncol 29:121–127
7. Cemazar M, Jarm T, Miklavcic D, Macek Lebar A, Ihan A, Kopitar NA, Sersa G (1998) Effect of electric field intensity on electropermeabilization and electrosensitivity of various tumor-cell lines in vitro. Electro Magnetobiol 17:263–272
8. Cemazar M, Miklavcic D, Scancar J, Dolzan V, Golouh R, Sersa G (1999) Increased platinum accumulation in SA-1 tumor cells after in vivo electrochemotherapy with cisplatin. Br J Cancer 79:1386–1391
9. Cemazar M, Parkins CS, Holder AL, Chaplin DJ, Tozer GM, Sersa G (2001) Electroporation of human microvascular endothelial cells: evidence for an anti-vascular mechanism of electrochemotherapy. Brit J Cancer 84:565–570
10. Cepeda V, Fuertes MA, Castilla J, Alonso C, Quevedo C, Pérez JM (2007) Biochemical machanisms of cisplatin cytotoxicity. Anticancer Agents Med Chem 7:3–18
11. Corovic S, Lackovic I, Sustaric P, Sustar T, Rodic T, Miklavcic D (2013) Modeling of electric field distribution in tissues during electroporation. Biomed Eng Online 12:16
12. Edhemovic I, Gadzijev EM, Brecelj E, Miklavcic D, Kos B, Zupanic A, Mali B, Jarm T, Pavliha D, Marcan M, Gasljevic G, Gorjup V, Music M, Pecnik Vavpotic T, Cemazar M, Snoj M, Sersa G (2011) Electrochemotherapy: a new technological approach in treatment of metastases in the liver. Technol Cancer Res Treat 10:475–485
13. Gava B, Zorzet P, Spessotto P, Cocchietto M, Sava G (2006) Inhibition of B16 melanoma metastases with the ruthenium complex imidazolium trans-imidazoledimethylsulfoxide-tetrachlororuthenate and down-regulation of tumor cell invasion. J Pharmacol Exp Ther 317(1):284–291
14. Haberl S, Miklavcic D, Sersa G, Frey W, Rubinsky B (2013) Cell membrane electroporation—Part 2: The applications. IEEE Electr Insul M 29(1):29–37
15. Hartinger CG, Jakupec MA, Zorbas-Seifried S, Groessl M, Egger A, Berger W, Zorbas H, Dyson PJ, Keppler BK (2008) KP1019, a new redox-active anticancer agent-preclinical development and results of a clinical phase I study in tumor patients. Chem Biodivers 5:2140–2155
16. Heffeter P, Böck K, Atil B, Hoda MAR, Körner W, Bartel C, Jungwirth U, Keppler BK, Micksche M, Berger W, Koellensperger G (2010) Intracellular protein binding patterns of the anticancer ruthenium drugs KP1019 and KP1339. J Biol Inorg Chem 15:737–748
17. Heller R, Gilbert R, Jaroszeski MJ (2000) Clinical trials for solid tumors using electrochemotherapy. In: Electrochemotherapy, Electrogenetherapy, and Transdermal Drug Delivery. Electrically Mediated Delivery of Molecules to Cells. Jaroszeski MJ, Heller R and Gilbert R (eds.). New Jersey: Humana Press, pp. 137-156
18. Hudej R, Turel I, Kanduser M, Scancar J, Kranjc S, Sersa G, Miklavcic D, Jakupec MA, Keppler BK, Cemazar M (2010) The influence of electroporation on cytotoxicity of anticancer ruthenium(III) complex KP1339 in vitro and in vivo. Anticancer Res 30:2055–2064
19. Hudej R, Kljun J, Kandioller W, Repnik U, Turk B, Hartinger CG, Keppler BK, Miklavcic D, Turel I (2012) Synthesis and Biological Evaluation of the Thionated Antibacterial Agent Nalidixic Acid and its Organoruthenium(II) Complex. Organometallics 31:5867–5874
20. Jaroszeski MJ, Dang V, Pottinger C, Hickey J, Gilbert R, Heller R (2000) Toxicity of anticancer agents mediated by electroporation in vitro. Anti-Cancer Drug 11:201–208
21. Kapitza S, Pongratz M, Jakupec MA, Heffeter P, Berger W, Lackinger L, Keppler BK, Marian B (2005) Heterocyclic complexes of ruthenium(III) induce apoptosis in colorectal carcinoma cells. J Cancer Res Clin Oncol 131:101–110
22. Kersten L, Bräunlich H, Keppler BK, Gliesing C, Wendelin M, Westphal J (1998) Comparative nephrotoxicity of some antitumour-active platinum and ruthenium complexes in rats. J Appl Toxicol 18:93–101
23. Kljun J, Petricek S, Zigon D, Hudej R, Miklavcic D, Turel I (2010) Synthesis and Characterization of Novel Ruthenium(III) Complexes with Histamine. Bioinorg Chem Appl 183097:1–6
24. Mali B, Jarm T, Snoj M, Sersa G, Miklavcic D (2013a) Antitumor effectiveness of electrochemotherapy: a systematic review and meta-analysis. Eur J SurgOncol 39:4–16
25. Mali B, Miklavcic D, Campana LG, Cemazar M, Sersa G, Snoj M, Jarm T (2013b) Tumor size and effectiveness of electrochemotherapy. Radiol Oncol 47:32–41
26. Marty M, Sersa G, Garbay JR, Gehl J, Collins CG, Snoj M, Billard V, Geertsen PF, Larkin JO, Miklavcic D (2006) Electrochemotherapy—an easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study. Eur J Cancer (Suppl 4): 3-13
27. Miklavcic D, Snoj M, Zupanic A, Kos B, Cemazar M, Kropivnik M, Bracko M, Pecnik T, Gadzijev E, Sersa G (2010) Towards treatment planning and treatment of deep-seated solid tumors by electrochemotherapy. Biomed Eng Online 9:10
28. Miklavcic D, Sersa G, Brecelj E, Gehl J, Soden D, Bianchi G, Ruggieri P, Rossi CR, Campana LG, Jarm T (2012) Electrochemotherapy: technological advancements for efficient electroporation-based treatment of internal tumors. Med Biol Eng Comput 50:1213–1225
29. Miklavcic D, Mali B, Kos B, Heller R, Sersa G (2014) Electrochemotherapy: from the drawing board into medical practice. Biomed Eng Online 13:29
30. Mir LM, Gehl J, Sersa G, Collins CG, Garbay JR, Billard V, Geertsen PF, Rudolf Z, O’Sullivan GC, Marty M (2006) Standard operating procedures of the electrochemotherapy: instructions for the use of bleomycin or CDDP administered either systemically or locally and electric pulses delivered by the CliniporatorTM by means of invasive or non-invasive electrodes. Eur J Cancer 4:14–25
31. Orlowski S, Belehradek J Jr, Paoletti C, Mir LM (1988) Transient electropermeabilization of cells in culture: increase of the cytotoxicity of anticancer drugs. Biochem Pharmacol 37(24):4727–4733
32. Pavliha D, Kos B, Marcan M, Zupanic A, Sersa G, Miklavcic D (2013a) Planning of electroporation-based treatments using web-based treatment-planning software. J Membrane Biol 246:833–842
33. Pavliha D, Music MM, Sersa G, Miklavcic D (2013b) Electroporation-based treatment planning for deep-seated tumors based on automatic liver segmentation of MRI images. PLoS ONE 8(8):e69068
34. Pucihar G, Kotnik T, Valic B, Miklavcic D (2006) Numerical determination of transmembrane voltage induced on irregularly shaped cells. Annals Biomed Eng 34:642–652
35. Sava G, Zorzet S, Turrin C, Vita F, Soranzo MR, Zabucchi G, Cocchietto M, Bergamo A, DiGiovine S, Pezzoni G, Sartor L, Garbisa S (2003) Dual action of NAMI-A in inhibition of solid tumor metastasis: selective targeting of metastatic cells and binding to collagen. Clin Cancer Res 9:1898–1905
36. Seelig MH, Berger MR, Keppler BK (1992) Antineoplastic activity of three ruthenium derivatives against chemically induced colorectal carcinoma in rats. J Cancer Res Clin Oncol 118:195–200
37. Sersa G, Cemazar M, Miklavcic D, Mir LM (1994) Electrochemotherapy: variable anti-tumor effect on different tumor models. Bioelectrochem Bioenerg 35:23–27
38. Sersa G, Cemazar M, Miklavcic D (1995) Antitumor effectiveness of electrochemotherapy with cis-diamminedichloroplatinum(II) in mice. Cancer Res 55:3450–3455
39. Sersa G, Krzic M, Sentjurc M, Ivanusa T, Beravs K, Kotnik V, Coer A, Swartz HM, Cemazar M (2002) Reduced blood flow and oxygenation in SA-1 tumours after electrochemotherapy with cisplatin. Brit J Cancer. 87:1047–1054
40. Sersa G, Miklavcic D, Cemazar M, Rudolf Z, Pucihar G, Snoj M (2008) Electrochemotherapy in treatment of tumours. Eur J Surg Oncol 34:232–240
41. Speelmans G, Sips WHHM, Grisel RJH, Staffhorst RWHM, Fichtinger-Schepman AMJ, Reedijk J, de Kruijff B (1996) The interaction of the anti-cancer drug cisplatin with phospholipids is specific for negatively charged phospholipids and takes place at low chloride ion concentration. Biochim Biophys Acta 1283:60–66
42. Spugnini EP, Citro G, Porrello A (2005) Rational design of new electrodes for electrochemotherapy. J ExpClin Cancer Res 24(2):245–254
43. Todorovic V, Sersa G, Mlakar V, Glavac D, Flisar K, Cemazar M (2011) Metastatic potential of melanoma cells is not affected by electrochemotherapy. Melanoma Res 21:196–205
44. Todorovic V, Sersa G, Mlakar V, Glavac D, Cemazar M (2012) Assessment of the tumourigenic and metastatic properties of SK-MEL28 melanoma cells surviving electrochemotherapy with bleomycin. Radiol Oncol 46(1):32–45
45. Zorzet S, Bergamo A, Cocchietto M, Sorc A, Gava B, Alessio E, Iengo E, Sava G (2000) Lack of in vitro cytotoxicity, associated to increased G2-M cell fraction and inhibition of matrigel invasion, may predict in vivo-selective antimetastasis activity of ruthenium complexes. JPET 295(3):927–933