Sunitinib potentiates the cytotoxic effect of electrochemotherapy in pancreatic carcinoma cells

1Pourshams A, Sepanlou SG, Ikuta KS, Bisignano C, Safiri S, Roshandel G, et al. The global, regional, and national burden of pancreatic cancer and its attributable risk factors in 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol 2019; 4: 934-47. doi: 10.1016/S2468-1253(19)30347-4Pourshams A Sepanlou SG Ikuta KS Bisignano C Safiri S Roshandel G et al. The global, regional, and national burden of pancreatic cancer and its attributable risk factors in 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017 Lancet Gastroenterol Hepatol 2019 4 934 47 10.1016/S2468-1253(19)30347-4702671131648972Open DOISearch in Google Scholar

2Morganti AG, Massaccesi M, La Torre G, Caravatta L, Piscopo A, Tambaro R, et al. A systematic review of resectability and survival after concurrent chemoradiation in primarily unresectable pancreatic cancer. Ann Surg Oncol 2010; 17: 194-205. doi: 10.1245/S10434-009-0762-4Morganti AG Massaccesi M La Torre G Caravatta L Piscopo A Tambaro R et al.A systematic review of resectability and survival after concurrent chemoradiation in primarily unresectable pancreatic cancer Ann Surg Oncol 2010 17 194 205 10.1245/S10434-009-0762-419856029Open DOISearch in Google Scholar

3Cemazar M, Sersa G. Recent advances in electrochemotherapy. Bioelectricity 2019; 1: 204-13. doi: 10.1089/BIOE.2019.0028Cemazar M Sersa G Recent advances in electrochemotherapy Bioelectricity 2019 1 204 13 10.1089/BIOE.2019.0028837029434471824Open DOISearch in Google Scholar

4Sersa G, Ursic K, Cemazar M, Heller R, Bosnjak M, Campana LG. Biological factors of the tumour response to electrochemotherapy: review of the evidence and a research roadmap. Eur J Surg Oncol 2021. 8: 1836-46. doi: 10.1016/j.ejso.2021.03.229Sersa G Ursic K Cemazar M Heller R Bosnjak M Campana LG Biological factors of the tumour response to electrochemotherapy: review of the evidence and a research roadmap Eur J Surg Oncol 2021 8 1836 46 10.1016/j.ejso.2021.03.22933726951Open DOISearch in Google Scholar

5Gehl J, Sersa G, Matthiessen LW, Muir T, Soden D, Occhini A, et al. Updated standard operating procedures for electrochemotherapy of cutaneous tumours and skin metastases. Acta Oncol 2018; 57: 874-82. doi: 10.1080/0284186X.2018.1454602Gehl J Sersa G Matthiessen LW Muir T Soden D Occhini A et al.Updated standard operating procedures for electrochemotherapy of cutaneous tumours and skin metastases Acta Oncol 2018 57 874 82 10.1080/0284186X.2018.145460229577784Open DOISearch in Google Scholar

6Djokic M, Cemazar M, Popovic P, Kos B, Dezman R, Bosnjak M, et al. Electrochemotherapy as treatment option for hepatocellular carcinoma, a prospective pilot study. Eur J Surg Oncol 2018; 44: 651-7. doi: 10.1016/J. EJSO.2018.01.090Djokic M Cemazar M Popovic P Kos B Dezman R Bosnjak M et al.Electrochemotherapy as treatment option for hepatocellular carcinoma, a prospective pilot study Eur J Surg Oncol 2018 44 651 7 10.1016/J.EJSO.2018.01.090Open DOISearch in Google Scholar

7Djokic M, Cemazar M, Bosnjak M, Dezman R, Badovinac D, Miklavcic D, et al. A prospective phase II study evaluating intraoperative electrochemotherapy of hepatocellular carcinoma. Cancers 2020; 12: 1-14. doi: 10.3390/ CANCERS12123778DjokicM CemazarM BosnjakM DezmanR BadovinacD Miklavcic D et al. A prospective phase II study evaluating intraoperative electrochemotherapy of hepatocellular carcinoma Cancers 2020 12 1 14 10.3390/CANCERS12123778776545433333941Open DOISearch in Google Scholar

8Djokic M, Dezman R, Cemazar M, Stabuc M, Petric M, Smid LM, et al. Percutaneous image guided electrochemotherapy of hepatocellular carcinoma: technological advancement. Radiol Oncol 2020; 54: 347-52. doi: 10.2478/RAON-2020-0038Djokic M Dezman R Cemazar M Stabuc M Petric M Smid LM et al.Percutaneous image guided electrochemotherapy of hepatocellular carcinoma: technological advancement Radiol Oncol 2020 54 347 52 10.2478/RAON-2020-0038Open DOISearch in Google Scholar

9Edhemovic I, Brecelj E, Cemazar M, Boc N, Trotovsek B, Djokic M, et al. Intraoperative electrochemotherapy of colorectal liver metastases: a prospective phase II study. Eur J Surg Oncol 2020; 46: 1628-33. doi: 10.1016/j. ejso.2020.04.037Edhemovic I Brecelj E Cemazar M Boc N Trotovsek B Djokic M et al.Intraoperative electrochemotherapy of colorectal liver metastases: a prospective phase II study Eur J Surg Oncol 2020 46 1628 33 10.1016/j.ejso.2020.04.03732387070Open DOISearch in Google Scholar

10Edhemovic I, Brecelj E, Gasljevic G, Marolt Music M, Gorjup V, Mali B, et al. Intraoperative electrochemotherapy of colorectal liver metastases. J Surg Oncol 2014; 110: 320-7. doi: 10.1002/JSO.23625Edhemovic I Brecelj E Gasljevic G Marolt Music M Gorjup V Mali B et al.Intraoperative electrochemotherapy of colorectal liver metastases J Surg Oncol 2014 110 320 7 10.1002/JSO.23625Open DOISearch in Google Scholar

11Dežman R, Čemažar M, Serša G, Seliškar A, Erjavec V, Trotovšek B, et al. Safety and feasibility of eElectrochemotherapy of the pancreas in a porcine model. Pancreas 2020; 49: 1168-73. doi: 10.1097/MPA.0000000000001642Dežman R Čemažar M Serša G Seliškar A Erjavec V Trotovšek B et al.Safety and feasibility of eElectrochemotherapy of the pancreas in a porcine model Pancreas 2020 49 1168 73 10.1097/MPA.000000000000164232898000Open DOISearch in Google Scholar

12Girelli R, Prejanò S, Cataldo I, Corbo V, Martini L, Scarpa A, et al. Feasibility and safety of electrochemotherapy (ECT) in the pancreas: a pre-clinical investigation. Radiol Oncol 2015; 49: 147-54. doi: 10.1515/RAON-2015-0013Girelli R Prejanò S Cataldo I Corbo V Martini L Scarpa A et al.Feasibility and safety of electrochemotherapy (ECT) in the pancreas: a pre-clinical investigation Radiol Oncol 2015 49 147 54 10.1515/RAON-2015-0013Open DOISearch in Google Scholar

13Granata V, Fusco R, Piccirillo M, Palaia R, Petrillo A, Lastoria S, et al. Electrochemotherapy in locally advanced pancreatic cancer: preliminary results. Int J Surg 2015; 18: 230-6. doi: 10.1016/J.IJSU.2015.04.055Granata V Fusco R Piccirillo M Palaia R Petrillo A Lastoria S et al.Electrochemotherapy in locally advanced pancreatic cancer: preliminary results Int J Surg 2015 18 230 6 10.1016/J.IJSU.2015.04.05525917204Open DOISearch in Google Scholar

14Granata V, Fusco R, Setola SV, Piccirillo M, Leongito M, Palaia R, et al. Early radiological assessment of locally advanced pancreatic cancer treated with electrochemotherapy. World J Gastroenterol 2017; 23: 4767. doi: 10.3748/ WJG.V23.I26.4767Granata V Fusco R Setola SV Piccirillo M Leongito M Palaia R et al.Early radiological assessment of locally advanced pancreatic cancer treated with electrochemotherapy World J Gastroenterol 2017 15 199 10.3748/WJG.V23.I26.4767 Open DOISearch in Google Scholar

15Casadei R, Ricci C, Ingaldi C, Alberici L, Di Marco M, Guido A, et al. Intraoperative electrochemotherapy in locally advanced pancreatic cancer: indications, techniques and results-a single-center experience. Updates Surg 2020; 72: 1089-96. doi: 10.1007/S13304-020-00782-XCasadei R Ricci C Ingaldi C Alberici L Di Marco M Guido A et al.Intraoperative electrochemotherapy in locally advanced pancreatic cancer: indications, techniques and results-a single-center experience Updates Surg 2020 72 1089 96 10.1007/S13304-020-00782-XOpen DOISearch in Google Scholar

16Spiliopoulos S, Zurlo MT, Casella A, Laera L, Surico G, Surgo A, et al. Current status of non-surgical treatment of locally advanced pancreatic cancer. World J Gastrointest Oncol 2021; 13: 2064-75. doi: 10.4251/WJGO.V13. I12.2064Spiliopoulos S Zurlo MT Casella A Laera L Surico G Surgo A et al.Current status of non-surgical treatment of locally advanced pancreatic cancer World J Gastrointest Oncol 2021 13 2064 75 10.4251/WJGO.V13.I12.2064 Open DOISearch in Google Scholar

17Tempero MA, Malafa MP, Chair V, Asbun H, Behrman SW, Benson III AB, et al. NCCN Guidelines Version 2.2015, Pancreatic Adenocarcinoma, American Joint Committee on Cancer (AJCC). Available at: https://www2.tri-kobe.org/nccn/guideline/archive/pancreas2015/english/pancreatic.pdfTempero MA Malafa MP Chair V Asbun H Behrman SW Benson III AB et al. NCCN Guidelines Version 2.2015, Pancreatic Adenocarcinoma, American Joint Committee on Cancer (AJCC). Available at https://www2.tri-kobe.org/nccn/guideline/archive/pancreas2015/english/pancreatic.pdfSearch in Google Scholar

18Raymond E, Dahan L, Raoul J-L, Bang Y-J, Borbath I, Lombard-Bohas C, et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med 2011; 364: 501-13. doi: 10.1056/NEJMOA1003825Raymond E Dahan L Raoul J-L Bang Y-J Borbath I Lombard-Bohas C et al.Sunitinib malate for the treatment of pancreatic neuroendocrine tumors N Engl J Med 2011 364 501 13 10.1056/NEJMOA1003825Open DOISearch in Google Scholar

19Carrato Mena A, Grande Pulido E, Guillén-Ponce C. Understanding the molecular-based mechanism of action of the tyrosine kinase inhibitor: sunitinib. Anticancer Drugs 2010; 21(Suppl 1): S3-11. doi: 10.1097/01. CAD.0000361534.44052.C5Carrato MenaA Grande PulidoE Guillén-PonceC. Understanding the molecular-based mechanism of action of the tyrosine kinase inhibitor: sunitinib Anticancer Drugs 2010 21 Suppl 1 S3 11 10.1097/01.CAD.0000361534.44052.C5 20110785Open DOISearch in Google Scholar

20Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22: 27-55. doi: 10.1016/0065-2571(84)90007-4Chou TC Talalay P Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors Adv Enzyme Regul 1984 22 27 55 10.1016/0065-2571(84)90007-46382953Open DOISearch in Google Scholar

21Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-8. doi: 10.1006/METH.2001.1262Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001 25 402 8 10.1006/METH.2001.1262Open DOISearch in Google Scholar

22D’onofrio M, Beleù A, de Robertis R. Ultrasound-guided percutaneous procedures in pancreatic diseases: new techniques and applications. Eur Radiol Exp 2019; 3: 2. doi: 10.1186/S41747-018-0081-2D’onofrioM BeleùA de RobertisR. Ultrasound-guided percutaneous procedures in pancreatic diseases: new techniques and applications Eur Radiol Exp 2019 3 2 10.1186/S41747-018-0081-2634274630671676Open DOISearch in Google Scholar

23Martin RCG, McFarland K, Ellis S, Velanovich V. Irreversible electroporation in locally advanced pancreatic cancer: potential improved overall survival. Ann Surg Oncol 2013; 20(Suppl 3): S443-9. doi: 10.1245/S10434-012-2736-1Martin RCG McFarland K Ellis S Velanovich V Irreversible electroporation in locally advanced pancreatic cancer: potential improved overall survival Ann Surg Oncol 2013 20(Suppl 3) S443 9 10.1245/S10434-012-2736-123128941Open DOISearch in Google Scholar

24Petrelli F, Comito T, Ghidini A, Torri V, Scorsetti M and Barni S. Stereotactic body radiation therapy for locally advanced pancreatic cancer: a systematic review and pooled analysis of 19 trials. Int J Radiat Oncol Biol Phys 2017; 97: 313-22. doi: 10.1016/j.ijrobp.2016.10.030.Petrelli F Comito T Ghidini A Torri V Scorsetti M Barni S. Stereotactic body radiation therapy for locally advanced pancreatic cancer: a systematic review and pooled analysis of 19 trials Int J Radiat Oncol Biol Phys 2017 97 313 22 10.1016/j.ijrobp.2016.10.03028068239Open DOISearch in Google Scholar

25Campana LG, Miklavčič D, Bertino G, Marconato R, Valpione S, Imarisio I, et al. Electrochemotherapy of superficial tumors - current status: basic principles, operating procedures, shared indications, and emerging applications. Semin Oncol 2019; 46: 173-91. doi: 10.1053/J.SEMINONCOL.2019.04.002Campana LG Miklavčič D Bertino G Marconato R Valpione S Imarisio I et al.Electrochemotherapy of superficial tumors - current status: basic principles, operating procedures, shared indications, and emerging applications Semin Oncol 2019 46 173 91 10.1053/J.SEMINONCOL.2019.04.00231122761Open DOISearch in Google Scholar

26Bonferoni MC, Rassu G, Gavini E, Sorrenti M, Catenacci L, Torre ML, et al. Electrochemotherapy of deep-seated tumors: state of art and perspectives as possible “EPR effect enhancer” to improve cancer nanomedicine efficacy. Cancers 2021; 13: 4437. doi: 10.3390/CANCERS13174437Bonferoni MC Rassu G Gavini E Sorrenti M Catenacci L Torre ML et al.Electrochemotherapy of deep-seated tumors: state of art and perspectives as possible “EPR effect enhancer” to improve cancer nanomedicine efficacy Cancers 2021 13 4437 10.3390/CANCERS13174437843157434503247Open DOISearch in Google Scholar

27Bosnjak M, Jesenko T, Markelc B, Janzic L, Cemazar M, Sersa G. PARP inhibitor olaparib has a potential to increase the effectiveness of electrochemotherapy in BRCA1 mutated breast cancer in mice. Bioelectrochemistry 2021; 140: 107832. doi: 10.1016/J.BIOELECHEM.2021.107832Bosnjak M Jesenko T Markelc B Janzic L Cemazar M Sersa G PARP inhibitor olaparib has a potential to increase the effectiveness of electrochemotherapy in BRCA1 mutated breast cancer in mice Bioelectrochemistry 2021 140 107832 10.1016/J.BIOELECHEM.2021.107832Open DOISearch in Google Scholar

28Jaroszeski MJ, Dang V, Pottinger C, Hickey J, Gilbert R, Heller R. Toxicity of anticancer agents mediated by electroporation in vitro. Anticancer Drugs 2000; 11: 201-8. doi: 10.1097/00001813-200003000-00008Jaroszeski MJ Dang V Pottinger C Hickey J Gilbert R Heller R Toxicity of anticancer agents mediated by electroporation in vitro Anticancer Drugs 2000 11 201 8 10.1097/00001813-200003000-0000810831279Open DOISearch in Google Scholar

29Ursic K, Kos S, Kamensek U, Cemazar M, Scancar J, Bucek S, et al. Comparable effectiveness and immunomodulatory actions of oxaliplatin and cisplatin in electrochemotherapy of murine melanoma. Bioelectrochemistry 2018; 119:161-71. doi: 10.1016/J.BIOELECHEM.2017.09.009Ursic K Kos S Kamensek U Cemazar M Scancar J Bucek S et al.Comparable effectiveness and immunomodulatory actions of oxaliplatin and cisplatin in electrochemotherapy of murine melanoma Bioelectrochemistry 2018 119 161 71 10.1016/J.BIOELECHEM.2017.09.009Open DOISearch in Google Scholar

30Michel O, Kulbacka J, Saczko J, Mączyńska J, Blasiak P, Rossowska J, et al. Electroporation with cisplatin against metastatic pancreatic cancer: in vitro study on human primary cell culture. BioMed Res Int 2018; 2018: 7364539. doi: 10.1155/2018/7364539Michel O Kulbacka J Saczko J Mączyńska J Blasiak P Rossowska J et al.Electroporation with cisplatin against metastatic pancreatic cancer: in vitro study on human primary cell culture BioMed Res Int 2018 2018 7364539 10.1155/2018/7364539588443829750170Open DOISearch in Google Scholar

31Fernandes P, O’Donovan TR, McKenna SL and Forde PF: Electrochemotherapy causes caspase-independent necrotic-like death in pancreatic cancer cells. Cancers 2019; 11: 1177. doi: 10.3390/cancers11081177Fernandes P O’DonovanTR McKennaSL FordePF Electrochemotherapy causes caspase-independent necrotic-like death in pancreatic cancer cells Cancers 2019 11 1177 10.3390/cancers11081177672153231416294Open DOISearch in Google Scholar

32Dhuriya YK, Sharma D. Necroptosis: a regulated inflammatory mode of cell death. J Neuroinflammation 2018; 15: 199. doi: 10.1186/S12974-018-1235-0.Dhuriya YK Sharma D Necroptosis: a regulated inflammatory mode of cell death J Neuroinflammation 2018 15 199 10.1186/S12974-018-1235-0.Open DOISearch in Google Scholar

33Ali MS, Gill KS, Saglio G, Cilloni D, Soden DM, Forde PF. Expressional changes in stemness markers post electrochemotherapy in pancreatic cancer cells. Bioelectrochemistry 2018; 122: 84-92. doi: 10.1016/J. BIOELECHEM.2018.03.009Ali MS Gill KS Saglio G Cilloni D Soden DM Forde PF Expressional changes in stemness markers post electrochemotherapy in pancreatic cancer cells Bioelectrochemistry 2018 122 84 92 10.1016/J. BIOELECHEM.2018.03.009Open DOISearch in Google Scholar

34Tran Cao HS, Bouvet M, Kaushal S, Keleman A, Romney E, Kim G, et al. Metronomic gemcitabine in combination with sunitinib inhibits multisite metastasis and increases survival in an orthotopic model of pancreatic cancer. Mol Cancer Ther 2010; 9: 2068-78. doi: 10.1158/1535-7163.MCT-10-0201Tran Cao HS Bouvet M Kaushal S Keleman A Romney E Kim G et al.Metronomic gemcitabine in combination with sunitinib inhibits multisite metastasis and increases survival in an orthotopic model of pancreatic cancer Mol Cancer Ther 2010 9 2068 78 10.1158/1535-7163.MCT-10-0201438308520606044Open DOISearch in Google Scholar

35Wey JS, Fan F, Gray MJ, Bauer TW, McCarty MF, Somcio R, et al. Vascular endothelial growth factor receptor-1 promotes migration and invasion in pancreatic carcinoma cell lines. Cancer 2005; 104: 427-38. doi: 10.1002/ CNCR.21145Wey JS Fan F Gray MJ Bauer TW McCarty MF Somcio R et al.Vascular endothelial growth factor receptor-1 promotes migration and invasion in pancreatic carcinoma cell lines Cancer 2005 104 427 38 10.1002/CNCR.21145Open DOISearch in Google Scholar