Treating cancer with sonodynamic therapy: A review

International Journal of Hyperthermia

Volumn 31, Issue 2, 2015, Pages 107-117

  Costley, David ^a   Mc Ewan, Conor ^a   Fowley, Colin ^a   McHale, Anthony P ^a   Atchison, Jordan ^a   Nomikou, Nikolitsa ^b   Callan, John F ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cancer; Photodynamic therapy; Reactive oxygen species; Sonodynamic therapy; Sonosensitiser; Ultrasound

Indexed keywords

ACRIDINE ORANGE; CURCUMIN; INDOCYANINE GREEN; METHYLENE BLUE; PORPHYRIN; REACTIVE OXYGEN METABOLITE; XANTHENE;

ANTINEOPLASTIC ACTIVITY; BREMS RADIATION; CANCER THERAPY; CELL INVASION; CELL MEMBRANE FLUIDITY; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; ELECTRON SPIN RESONANCE; HUMAN; IN VITRO STUDY; NONHUMAN; PHOTODYNAMIC THERAPY; PYROLYSIS; REVIEW; SONODYNAMIC THERAPY; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT; NEOPLASMS; ULTRASOUND THERAPY;

HUMANS; NEOPLASMS; REACTIVE OXYGEN SPECIES; ULTRASONIC THERAPY;

EID: 84928192108     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2014.992484     Document Type: Review

References (81)

1. Shibaguchi H, Tsuru H, Kuroki M, Kuroki M. Sonodynamic cancer therapy: A non-invasive and repeatable approach using lowintensity ultrasound with a sonosensitizer. Anticancer Res 2011; 31:2425-9.
2. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, et al. Photodynamic therapy. J Natl Cancer Inst 1998; 90:889-905.
3. Bailey M, Khokhlova V, Sapozhnikov O, Kargl S, Crum L. Physical mechanisms of the therapeutic effect of ultrasound. (A review). Acoust Phys 2003;49:369-88.
4. Niedre M, Patterson MS, Wilson BC. Direct near-infrared luminescence detection of singlet oxygen generated by photodynamic therapy in cells in vitro and tissues in vivo. Photochem Photobiol 2002;75:382-91.
5. Kremkau FW, Kaufmann JS, Walker MM, Burch PG, Spurr CL. Ultrasonic enhancement of nitrogen mustard cytotoxicity in mouse leukemia. Cancer 1976;37:1643-7.
6. Leighton TG. The principles of cavitation. In: Povey MJW, Mason TJ, editors. Ultrasound in Food Processing. London: Thomson Science; 1997. pp 151-82.
7. Rosenthal I, Sostaric JZ, Riesz P. Sonodynamic therapy-A review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem 2004;11:349-63.
8. Mis̈k V, Riesz P. Free radical intermediates in sonodynamic therapy. Ann N Y Acad Sci 2000;899:335-48.
9. Pickworth M, Dendy P, Leighton T, Walton A. Studies of the cavitational effects of clinical ultrasound by sonoluminescence: 2. Thresholds for sonoluminescence from a therapeutic ultrasound beam and the effect of temperature and duty cycle. Phys Med Biol 1988;33:1249-60.
10. Byun K, Kim KY, Kwak H. Sonoluminescence characteristics from micron and submicron bubbles. J Korean Phys Soc 2005;47: 1010-22.
11. Saksena T, Nyborg W. Sonoluminescence from stable cavitation. J Chem Phys 1970;53:1722-34.
12. Gaitan DF, Crum LA, Church CC, Roy RA. Sonoluminescence and bubble dynamics for a single, stable, cavitation bubble. J Acoust Soc Am 1992;91:3166-83.
13. Umemura S, Yumita N, Nishigaki R, Umemura K. Mechanism of cell damage by ultrasound in combination with hematoporphyrin. Cancer Sci 1990;81:962-6.
14. He Y, Xing D, Tan S, Tang Y, Ueda K. In vivo sonoluminescence imaging with the assistance of FCLA. Phys Med Biol 2002;47: 1535-41.
15. Hachimine K, Shibaguchi H, Kuroki M, Yamada H, Kinugasa T, Nakae Y, et al. Sonodynamic therapy of cancer using a novel porphyrin derivative, DCPH-P-Na(I), which is devoid of photosensitivity. Cancer Sci 2007;98:916-20.
16. Sazgarnia A, Shanei A, Eshghi H, Hassanzadeh-Khayyat M, Esmaily H, Shanei MM. Detection of sonoluminescence signals in a gel phantom in the presence of protoporphyrin IX conjugated to gold nanoparticles. Ultrasonics 2013;53:29-35.
17. Kessel D, Lo J, Jeffers R, Fowlkes JB, Cain C. Modes of photodynamic vs sonodynamic cytotoxicity. J Photochem Photobiol B 1995;28:219-21.
18. Li YS, Reid CN, McHale AP. Enhancing ultrasound-mediated cell membrane permeabilisation (sonoporation) using a high frequency pulse regime and implications for ultrasound-aided cancer chemotherapy. Cancer Lett 2008;266:156-62.
19. Tachibana K, Feril Jr LB, Ikeda-Dantsuji Y. Sonodynamic therapy. Ultrasonics 2008;48:253-9.
20. Hiraoka W, Honda H, Feril Jr LB, Kudo N, Kondo T. Comparison between sonodynamic effect and photodynamic effect with photosensitizers on free radical formation and cell killing. Ultrason Sonochem 2006;13:535-42.
21. Nomikou N, Fowley C, Byrne N, McCaughan B, McHale AP, Callan JF. Microbubble-sonosensitiser conjugates as therapeutics in sonodynamic therapy. Chem Commun (Camb) 2012;48:8332-4.
22. Yumita N, Han Q, Kitazumi I, Umemura S. Sonodynamically induced apoptosis, necrosis, and active oxygen generation by monol-aspartyl chlorin e6. Cancer science 2008;99:166-72.
23. Feril Jr LB, Kondo T, Cui Z, Tabuchi Y, Zhao Q, Ando H, et al. Apoptosis induced by the sonomechanical effects of low intensity pulsed ultrasound in a human leukemia cell line. Cancer Lett 2005; 221:145-52.
24. Rotenberg M, Margalit R. Porphyrin-membrane interactions: Binding or partition? Biochim Biophys Acta 1987;905:173-80.
25. Tang W, Liu Q, Wang X, Mi N, Wang P, Zhang J. Membrane fluidity altering and enzyme inactivating in sarcoma 180 cells post the exposure to sonoactivated hematoporphyrin in vitro. Ultrasonics 2008;48:66-73.
26. Yumita N, Umemura S. Ultrasonically induced cell damage and membrane lipid peroxidation by photofrin II: Mechanism of sonodynamic activation. J Med Ultrason 2004;31:35-40.
27. Yumita N, Iwase Y, Nishi K, Ikeda T, Umemura S, Sakata I, et al. Sonodynamically induced cell damage and membrane lipid peroxidation by novel porphyrin derivative, DCPH-P-Na(I). Anticancer Res 2010;30:2241-6.
28. Hsieh Y, Wu C, Chang C, Yu J. Subcellular localization of Photofrin determines the death phenotype of human epidermoid carcinoma A431 cells triggered by photodynamic therapy: When plasma membranes are the main targets. J Cell Physiol 2003;194: 363-75.
29. Brackett CM, Gollnick SO. Photodynamic therapy enhancement of anti-tumor immunity. Photochem Photobiol Sci 2011;10: 649-52.
30. Wrenn SP, Small E, Dan N. Bubble nucleation in lipid bilayers: A mechanism for low frequency ultrasound disruption. Biochim Biophys Acta 2013;1828:1192-7.
31. Guo S, Sun X, Cheng J, Xu H, Dan J, Shen J, et al. Apoptosis of THP-1 macrophages induced by protoporphyrin IX-mediated sonodynamic therapy. Int J Nanomedicine 2013;8:2239-46.
32. Ohmura T, Fukushima T, Shibaguchi H, Yoshizawa S, Inoue T, Kuroki M, et al. Sonodynamic therapy with 5-aminolevulinic acid and focused ultrasound for deep-seated intracranial glioma in rat. Anticancer Res 2011;31:2527-33.
33. Sugita N, Iwase Y, Yumita N, Ikeda T, Umemura S. Sonodynamically induced cell damage using rose bengal derivative. Anticancer Res 2010;30:3361-6.
34. Umemura S, Kawabata K, Yumita N, Nishigaki R, Umemura K. Sonodynamic approach to tumor treatment. Proc IEEE Ultrason Symposium 1992.
35. Liu Q, Wang X, Wang P, Xiao L, Hao Q. Comparison between sonodynamic effect with protoporphyrin IX and hematoporphyrin on sarcoma 180. Cancer Chemother Pharmacol 2007;60:671-80.
36. Umemura S, Yumita N, Umemura K, Nishigaki R. Sonodynamically induced effect of rose bengal on isolated sarcoma 180 cells. Cancer Chemother Pharmacol 1999;43:389-93.
37. McCaughan B, Rouanet C, Fowley C, Nomikou N, McHale AP, McCarron PA, et al. Enhanced ROS production and cell death through combined photo-and sono-activation of conventional photosensitising drugs. Bioorg Med Chem Lett 2011;21:5750-52.
38. Sugita N, Kawabata K, Sasaki K, Sakata I, Umemura S. Synthesis of amphiphilic derivatives of rose bengal and their tumor accumulation. Bioconjug Chem 2007;18:866-73.
39. Suzuki N, Okada K, Chida S, Komori C, Shimada Y, Suzuki T. Antitumor effect of acridine orange under ultrasonic irradiation in vitro. Anticancer Res 2007;27:4179-84.
40. Komori C, Okada K, Kawamura K, Chida S, Suzuki T. The sonodynamic antitumor effect of methylene blue on sarcoma180 cells in vitro. Anticancer Res 2009;29:2411-15.
41. Waksman R, McEwan PE, Moore TI, Pakala R, Kolodgie FD, Hellinga DG, et al. PhotoPoint photodynamic therapy promotes stabilization of atherosclerotic plaques and inhibits plaque progression. J Am Coll Cardiol 2008;52:1024-32.
42. Lee DK, Choi Y, Shon S, Schellingerhout D, Park JE, Kim D. Atorvastatin and clopidogrel interfere with photosensitization in vitro. Photochem Photobiol Sci 2011;10:1587-92.
43. Haibo C, Ye T. GW24-e0411 The sonodynamic effect of curcumin on THP-1 cell-derived macrophages. Heart 2013;99:A22-3.
44. Zheng L, Sun X, Zhu X, Lv F, Zhong Z, Zhang F, et al. Apoptosis of THP-1 derived macrophages induced by sonodynamic therapy using a new sonosensitizer hydroxyl acetylated curcumin. PLoS One 2014;9:e93133.
45. Urbanska K, Romanowska-Dixon B, Matuszak Z, Oszajca J, Nowak-Sliwinska P, Stochel G. Indocyanine green as a prospective sensitizer for photodynamic therapy of melanomas. Acta Biochim Pol 2002;49:387-91.
46. Nomikou N, Sterrett C, Arthur C, McCaughan B, Callan JF, McHale AP. The effects of ultrasound and light on indocyaninegreen-treated tumour cells and tissues. Chem Med Chem 2012;7: 1465-71.
47. Narang AS, Varia S. Role of tumor vascular architecture in drug delivery. Adv Drug Deliv Rev 2011;63:640-58.
48. Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv Drug Deliv Rev 2011;63:131-5.
49. Master A, Livingston M, Sen Gupta A. Photodynamic nanomedicine in the treatment of solid tumors: Perspectives and challenges. J Control Release 2013;168:88-102.
50. Ren Y, Wang R, Liu Y, Guo H, Zhou X, Yuan X, et al. A hematoporphyrin-based delivery system for drug resistance reversal and tumor ablation. Biomaterials 2014;35:2462-70.
51. Sazgarnia A, Shanei A, Meibodi NT, Eshghi H, Nassirli H. A novel nanosonosensitizer for sonodynamic therapy in vivo study on a colon tumor model. J Ultrasound Med 2011;30:1321-9.
52. Yumita N, Nishigaki R, Umemura K, Umemura S. Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound. Cancer Sci 1989;80:219-22.
53. Dellinger M. Apoptosis or necrosis following Photofrin photosensitization: influence of the incubation protocol. Photochem Photobiol 1996;64:182-7.
54. Oleinick NL, Morris RL, Belichenko I. The role of apoptosis in response to photodynamic therapy: What, where, why, and how. Photochem Photobiol Sci 2002;1:1-21.
55. Castano AP, Mroz P, Hamblin MR. Photodynamic therapy and antitumour immunity. Nature Rev Cancer 2006;6:535-45.
56. Kessel D, Vicente MGH, Reiners JJ. Initiation of apoptosis and autophagy by photodynamic therapy. Lasers Surg Med 2006;38: 482-8.
57. Yang Z, Klionsky DJ. An overview of the molecular mechanism of autophagy. Autophagy in infection and immunity: Springer, Curr Top Microbiol Immunol, 2009, pp. 1-32.
58. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nature Rev Cancer 2005;5:726-34.
59. Wang X, Liu Q, Wang Z, Wang P, Zhao P, Zhao X, et al. Role of autophagy in sonodynamic therapy-induced cytotoxicity in S180 cells. Ultrasound Med Biol 2010;36:1933-46.
60. Yumita N, Sasaki K, Umemura S, Yukawa A, Nishigaki R. Sonodynamically induced antitumor effect of gallium-porphyrin complex by focused ultrasound on experimental kidney tumor. Cancer Lett 1997;112:79-86.
61. Yumita N, Okuyama N, Sasaki K, Umemura S. Sonodynamic therapy on chemically induced mammary tumor: Pharmacokinetics, tissue distribution and sonodynamically induced antitumor effect of gallium-porphyrin complex ATX-70. Cancer Chemother Pharmacol 2007;60:891-7.
62. Ohmura T, Fukushima T, Shibaguchi H, Yoshizawa S, Inoue T, Kuroki M, et al. Sonodynamic therapy with 5-aminolevulinic acid and focused ultrasound for deep-seated intracranial glioma in rat. Anticancer Res 2011;31:2527-33.
63. Roberts D, Cairnduff F, Driver I, Dixon B, Brown S. Tumor vascular shutdown following photodynamic therapy based on polyhematoporphyrin or 5-aminolevulinic acid. Int J Oncol 1994; 5:763-8.
64. Yoshino S, Fukushima T, Hayashi S, Nonaka M, Ogawa K, Sasaki K, et al. Effects of focused ultrasound sonodynamic treatment on the rat blood-brain barrier. Anticancer Res 2009;29:889-95.
65. Wang X, Zhang W, Xu Z, Luo Y, Mitchell D, Moss RW. Sonodynamic and photodynamic therapy in advanced breast carcinoma: A report of 3 cases. Integr Cancer Ther 2009;8:283-7.
66. Roberts D, Cairnduff F, Driver I, Dixon B, Brown S. Tumor vascular shutdown following photodynamic therapy based on polyhematoporphyrin or 5-aminolevulinic acid. Int J Oncol 1994; 5:763-8.
67. Gao Z, Zheng J, Yang B, Wang Z, Fan H, Lv Y, et al. Sonodynamic therapy inhibits angiogenesis and tumor growth in a xenograft mouse model. Cancer Lett 2013;335:93-9.
68. Dolmans DE, Kadambi A, Hill JS, Flores KR, Gerber JN, Walker JP, et al. Targeting tumor vasculature and cancer cells in orthotopic breast tumor by fractionated photosensitizer dosing photodynamic therapy. Cancer Res 2002;62:4289-94.
69. Yumita N, Sasaki K, Umemura S, Nishigaki R. Sonodynamically induced antitumor effect of a gallium-porphyrin complex, ATX-70. Cancer Sci 1996;87:310-16.
70. Yumita N, Okuyama N, Sasaki K, Umemura S. Sonodynamic therapy on chemically induced mammary tumor: Pharmacokinetics, tissue distribution and sonodynamically induced antitumor effect of gallium-porphyrin complex ATX-70. Cancer Chemother Pharmacol 2007;60:891-7.
71. Shi H, Liu Q, Qin X, Wang P, Wang X. Pharmacokinetic study of a novel sonosensitizer chlorin-e6 and its sonodynamic anti-cancer activity in hepatoma-22 tumor-bearing mice. Biopharm Drug Dispos 2011;32:319-32.
72. Yumita N, Umemura S. Sonodynamic antitumour effect of chloroaluminum phthalocyanine tetrasulfonate on murine solid tumour. J Pharm Pharmacol 2004;56:85-90.
73. Meng Y, Zou C, Madiyalakan R, Woo T, Huang M, Yang X, et al. Water-soluble and biocompatible sono/photosensitizer nanoparticles for enhanced cancer therapy. Nanomedicine 2010;5:1559-69.
74. Tserkovsky D, Alexandrova E, Chalau V. Effects of combined sonodynamic and photodynamic therapies with Photolon on a glioma C6 tumor model. Exp Oncol 2012;34:322-35.
75. Shanei A, Sazgarnia A, Tayyebi Meibodi N, Eshghi H, Hassanzadeh-Khayyat M, Esmaily H, et al. Sonodynamic therapy using protoporphyrin IX conjugated to gold nanoparticles: An in vivo study on a colon tumor model. Iran J Basic Med Sci 2012; 15:759-67.
76. Inui T, Makita K, Miura H, Matsuda A, Kuchiike D, Kubo K, et al. Case report: A breast cancer patient treated with GcMAF, sonodynamic therapy and hormone therapy. Anticancer Res 2014; 34:4589-93.
77. Kenyon JN, Fulle RJ, Lewis TJ. Activated cancer therapy using light and ultrasound: A case series of sonodynamic photodynamic therapy in 115 patients over a 4-year period. Curr Drug Therapy 2009;4:179-93.
78. Anonymous. Sonodynamic therapy. 2013; Available at: http:// en.wikipedia.org/wiki/Sonodynamic-therapy. (accessed 15 October 2014).
79. Moseley H, Elijamel S, Moghissi K. Sonodynamic therapy. 2014; Available at: http://www.yorkshirelasercentre.org/sonodynamictherapy. html (accessed 2 October 2014).
80. Kolarova H, Tomankova K, Bajgar R, Kolar P, Kubinek R. Photodynamic sonodynamic treatment by phthalocyanine on cancer cell lines. Ultrasound Med Biol 2009;35:1397-404.
81. Miyoshi N, Igarashi T Riesz P. Evidence against singlet oxygen formation by sonolysis of aqueous oxygen-saturated solutions of hematoporphyrin and rose bengal: the mechanism of sonodynamic therapy. Ultrason Sonochem 2000;7:121-124.