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High Energy Shock Waves (HESW) Enhance Paclitaxel Cytotoxicity in MCF-7 Cells

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Abstract

High energy shock waves (HESW) produced by a piezoelectric generator were studied for their effect on human breast cancer cell (MCF-7) viability and sensitivity to paclitaxel. A dose-dependent impairment of cell viability was observed after HESW treatment (250–2000 shock waves, rate = 4/s, energy flux density = 0.25 mJ/mm2). Single treatment with shock waves produced no significant growth inhibition. Combined exposure to paclitaxel (ranging 0.1 nM to 20µM) and shock waves (100, 500 and 1000 shots, respectively) resulted in a significant reduction of MCF-7 cell proliferation at day 3 after treatment in respect with cells treated with paclitaxel alone. Notably, a cell viability reduction of about 50% was obtained after combined treatment with HESW and 10 nM paclitaxel, in front of a reduction of only 40% using 10 µM paclitaxel alone. Moreover, an earlier induction as well as an enhancement of apoptotis was observed in cells subjected to combined treatment with shock waves and paclitaxel (200 nM; 20 µM). In conclusion, HESW can enhance paclitaxel cytotoxicity in MCF-7 cells, thus allowing the treatment with lower doses of drug.

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References

  1. Russo P, Stephenson RA, Mies C, Huryk R, Heston WDW, Melamed MR, Fair WR: High energy shock waves suppress tumor growth in vitro and in vivo. J Urol 135: 626–628, 1986

    Google Scholar 

  2. Randazzo RF, Chaussy GC, Fuchs GJ, Bhuta SM, Lovrekovich H, de Kernion JB: The in vitro and in vivo effects of extracorporeal shock waves on malignant cells. Urol Res 16: 419–426, 1988

    Google Scholar 

  3. Gambihler S, Delius M, Brendel W: Biological effects of shock waves: cell disruption, viability, and proliferation of L1210 cells exposed to shock waves in vitro. Ultrasound Med Biol 16: 587–593, 1990

    Google Scholar 

  4. Gamarra F, Spelsberg F, Dellian M, Goetz AE: Complete local tumor remission after therapy with extra-corporeally applied high-energy shock waves (HESW). Int J Cancer 55: 153–156, 1993

    Google Scholar 

  5. Huber PE, Debus J: Tumor cytotoxicity in vivo and radical formation in vitro depend on the shock wave-induced cavitation dose. Radiat Res 156: 301–309, 2001

    Google Scholar 

  6. Oosterhof GON, Smits GAHJ, de Ruyter JE, van Moorselar RJA, Schalken JA, Debruyne FMJ: The in vitro effect of electromagnetically generated shock waves (Lithostar) on the Dunning R3327 PAT-2 rat prostatic cancer cell-line. A potentiating effect on the in vitro cytotoxicity of vinblastin. Urol Res 17: 13–19, 1989

    Google Scholar 

  7. Clayman RV, Long S, Marcus M: High energy shock waves: in vitro effects. Am J Kidney Dis 17: 436–444, 1991

    Google Scholar 

  8. Jones BJ, McHale AP, Butler MR: Effect of high-energy shock wave frequency on viability of malignant cell lines in vitro. Eur Urol 22: 70–73, 1992

    Google Scholar 

  9. Yao CZ, Ishizuka J, Bold RJ, Townsend Jr CM, Thompson JC: Cytocidal effect of high energy shock wave on tumor cells enhanced with larger dose and multiple exposures. Surg Oncol 3: 229–235, 1994

    Google Scholar 

  10. Roessler W, Rothgangel B, Hofstaedter F, Wieland WF: Treatment of human renal cell carcinoma with high-energy shock waves: a new in vivo/in vitro model. Urol Intern 55: 1–5, 1995

    Google Scholar 

  11. Wilmer A, Gambihler S, Delius M, Brendel W: In vitro cytotoxicity activity of lithotripter shock waves combined with adriamycin or with cisplatin on L1210 mouse leukemia cells. J Cancer Res Clin Oncol 115: 229–234, 1989

    Google Scholar 

  12. Gambihler S, Delius M: In vitro effects of lithotripter shock waves and cytotoxic drugs. Br J Cancer 66: 69–73, 1992

    Google Scholar 

  13. Wörle K, Steinbach P, Hofstädter F: The combined effects of high-energy shock waves and cytostatic drugs or cytokines on human bladder cancer cells. Br J Cancer 69: 58–65, 1994

    Google Scholar 

  14. Prat F, Sibille A, Luccioni C, Pansu D, Chapelon JY, Beaumatin J, Ponchon T, Cathignol D: Increased chemocytotoxicity to colon cancer cells by shock wave-induced cavitation. Gastroenterology 106: 937–944, 1994

    Google Scholar 

  15. Kambe M, Ioritani N, Kanamaru R: Enhancement of chemotherapeutic effects with focused shock waves: extracorporeal shock wave chemotherapy (ESWC). Hum Cell 10: 87–94, 1997

    Google Scholar 

  16. Kato M, Ioritani N, Suzuki T, Kambe M, Inaba Y, Watanabe R, Sasano H, Orikasa S: Mechanism of anti-tumor effect of combination of bleomycin and shock waves. Jpn J Cancer Res 91: 1065–1072, 2000

    Google Scholar 

  17. Ferlazzo G, Scisca C, Iemmo R, Quartarone G, Cicciarello R, Gagliardi ME, Mesiti M: Cytotoxic effects of high energy shock waves on cancer cells linked to metallic beads vehicled by monoclonal antibodies. J Urol 157: 366–370, 1997

    Google Scholar 

  18. Perez EA: Paclitaxel in breast cancer. Oncologist 3: 373–389, 1998

    Google Scholar 

  19. Wang LG, Liu XM, Kreis W, Budman DR: The effect of antimicrotubule agents on signal transduction pathways of apoptosis: a review. Cancer Chemother Pharmacol 44: 355–361, 1999

    Google Scholar 

  20. Gambaihler S, Delius M, Ellwart JW: Permeabilization of the plasma membrane of L1210 mouse leukemia cells using lithotripter shock waves. J Membr Biol 141: 267–275, 1994

    Google Scholar 

  21. Delius M, Adams G: Shock wave permeabilization with ribosome inactivating proteins: a new approach to tumor therapy. Cancer Res 59: 5227–5232, 1999

    Google Scholar 

  22. Kodama T, Hamblin MR, Doukas AG: Cytoplasmic molecular delivery with shock waves: importance of impulse. Biophys J 79: 1821–1832, 2000

    Google Scholar 

  23. Kodama T, Doukas AG, Hamblin MR: Shock wave-mediated molecular delivery into cells. Biochim Biophys Acta 1542: 186–194, 2002

    Google Scholar 

  24. Cohen JJ: Apoptosis. Immunol Today 14: 126–130, 1993

    Google Scholar 

  25. Steller H: Mechanism and genes of cellular suicide. Science (Washington DC) 267: 1445–1449, 1995

    Google Scholar 

  26. Quintans J, Kilkus J, McShan CL, Gottschalk AR, Dawson G: Ceramide mediates the apoptotic response of WEHI 231 cells to anti-immunoglobulin, corticosteroids and irradiation. Biochem Biophys Res Commun 202: 710–714, 1994

    Google Scholar 

  27. Ashus H, Rozenszajn LA, Blass M, Barda-Saad M, Azimov D, Radnay J, Zipori D, Rosenschein U: Apoptosis induction of human myeloid leukemia cells by ultrasound exposure. Cancer Res 60: 1014–1020, 2000

    Google Scholar 

  28. Feril Jr LB, Kondo T, Zhao Ql, Ogawa R: Enhancement of hypertermia-induced apoptosis by non-thermal effects of ultrasound. Cancer Lett 178: 63–70, 2002

    Google Scholar 

  29. Lagneaux L, Cordemans de Meulenaer E, Delforge A, Dejeneffe M, Massy M, Moerman C, Hannecart B, Canivet Y, Lepeltier MF, Bron D: Ultrasonic low-energy treatment: a novel approach to induce apoptosis in human leukemic cells. Exp Hematol 30: 1293–1301, 2002

    Google Scholar 

  30. Folberth W, Kohler G, Rohwedder A, Matura E: Pressure distribution and energy flow in the focal region of two different electromagnetic shock wave sources. J Stone Dis 4Z: 1–7, 1992

    Google Scholar 

  31. Ogden JA, Alvarez RG, Levitt R, Marlow M: Shock wave therapy (Orthotripsy®) in musculoskeletal disorders. Clin Orthop 387: 22–40, 2001

    Google Scholar 

  32. Wess O, Ueberle F, Dürβen RN, Hilcken D, Krauβ W, Reuner T, Schultheiβ R, Staudenraus I, Rattner M, Haaks W, Granz B: Working group technical developments-consensus report. In: Chaussy C, Eisenberger F, Jocham D, Wilbert D (eds) High Energy Shock Waves in Medicine. Clinical Application in Urology, Gastroenterology and Orthopedics. Georg Thieme Verlag, Stuttgart, New York, 1997, pp 59–71

    Google Scholar 

  33. Mosmann T: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55–63, 1983

    Google Scholar 

  34. Delius M, Denk R, Berding C, Liebich HG, Jordan M, Brendel W: Biological effects of shock waves: cavitation by shock waves in piglet liver. Ultrasound Med Biol 16: 467–472, 1990

    Google Scholar 

  35. Miller DL, Thomas RM: The role of cavitation in the induction of cellular DNA damage by ultrasound and lithotripter shock waves in vitro. Ultrasound Med Biol 22: 681–687, 1996

    Google Scholar 

  36. Paridaens R, Biganzoli L, Bruning P, Klijn JG, Gamucci T, Houston S, Coleman R, Schachter J, Van Vreckem A, Sylvester R, Awada A, Wildiers J, Piccart M: Paclitaxel versus doxorubicin as first-line single-agent chemotherapy for metastatic breast cancer: a European Organization for Research and Treatment of Cancer Randomized Study with cross-over. J Clin Oncol 18: 724–733, 2000

    Google Scholar 

  37. Jordan MA, Toso RJ, Thrower D, Wilson L: Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc Natl Acad Sci USA 90: 9552–9556, 1993

    Google Scholar 

  38. Bacus SS, Gudkov AV, Lowe M, Lyass L, Yung Y, Komarov AP, Keyomarsi K, Yarden Y, Seger R: Taxol-induced apoptosis depend on MAP kinase pathways (ERK and p38) and is independent of p53. Oncogene 20: 147–155, 2001

    Google Scholar 

  39. Charles AG, Han T-Y, Liu YY, Hansen N, Giuliano AE, Cabot MC: Taxol-induced ceramide generation and apoptosis in human breast cancer cells. Cancer Chemother Pharmacol 47: 444–450, 2001

    Google Scholar 

  40. Lee S, Yang W, Lan K-H, Sellappan S, Klos K, Hortobagyi G, Hung M-C, Yu D: Enhanced sensitization to taxol-induced apoptosis by herceptin pretreatment in ErbB2-overexpressing breast cancer cells. Cancer Res 62: 5703–5710, 2002

    Google Scholar 

  41. Beherens P, Brinkmann U, Wellman A: CSE1L/CAS: its role in proliferation and apoptosis. Apoptosis 8: 39–44, 2003

    Google Scholar 

  42. Oldham EA, Li C, Ke S, Wallace S, Huang P: Comparison of action of paclitaxel and poly(L-glutamic acid)-paclitaxel conjugate in human breast cancer cells. Int J Oncol 16: 125–132, 2000

    Google Scholar 

  43. Blajeski AL, Kottke TJ, Kaufmann SH: A multistep model for paclitaxel-induced apoptosis in human breast cancer cell lines. Exp Cell Res 270: 277–288, 2001

    Google Scholar 

  44. Au JL-S, Li D, Gan Y, Gao X, Johnson AL, Johnston J, Millenbaugh NJ, Jang SH, Kuh H-J, Chen C-T, Wienjes MG: Pharmacodynamics of immediate and delayed effects of paclitaxel: role of slow apoptosis and intracellular drug retention. Cancer Res 58: 2141–2148, 1998

    Google Scholar 

  45. Lindahl T, Satoh MS, Poirier GG, Klungland A: Posttranslational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20: 405–411, 1995

    Google Scholar 

  46. Janicke RU, Sprengart ML, Wati MR, Porter AG: Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273: 9357–9360, 1998

    Google Scholar 

  47. Rossini GP, Sgarbi N, Malaguti C: The toxic responses induced by okadaic acid involve processing of multiple caspase isoforms. Toxicon 39: 763–770, 2001

    Google Scholar 

  48. Liu XM, Wang LG, Kreis W, Budman DR, Adams LM: Differential effect of vinorelbine versus paclitaxel on ERK2 kinase activity during apoptosis in MCF-7 cells. Br J Cancer 85: 1403–1411, 2001

    Google Scholar 

  49. Lauer U, Burgelt E, Squire Z, Messmer K, Hofschneider PH, Gregor M, Delius M: Shock wave permeabilization as a new gene transfer method. Gene Ther 4: 710–715, 1997

    Google Scholar 

  50. Tschoep K, Hartmann G, Jox R, Thompson S, Eigler A, Krug A, Erhardt S, Adams G, Endres S, Delius M: Shock waves: a novel method for cytoplasmic delivery of antisense nucleotides. J Mol Med 79: 306–323, 2001

    Google Scholar 

  51. Kodama T, Doukas AG, Hamblin MR: Delivery of ribosomeinactivating protein toxin into cancer cells with shock waves. Cancer Lett 189: 69–75, 2003

    Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Fisiopatologia Clinica, Torino University Medical School, A.S.O. San Giovanni Battista, Torino, Italy

    Roberto Frairia, Annamaria Fazzari, Mariangela Raineri & Laura Berta

  2. Lab. Endocrinologia Oncologica, Dipartimento di Oncologia, A.S.O. San Giovanni Battista, Torino, Italy

    Maria G. Catalano & Nicoletta Fortunati

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  1. Roberto Frairia
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  2. Maria G. Catalano
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  5. Mariangela Raineri
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Frairia, R., Catalano, M.G., Fortunati, N. et al. High Energy Shock Waves (HESW) Enhance Paclitaxel Cytotoxicity in MCF-7 Cells. Breast Cancer Res Treat 81, 11–19 (2003). https://doi.org/10.1023/A:1025477421467

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