Sonoporation as an enhancing method for boron neutron capture therapy for squamous cell carcinomas

Radiation Oncology

Yoshiaki Yura²  Koji Ono¹  Mitsuhiro Nakazawa²  Soichi Iwai²  Yoshinori Sakurai¹  Shin-Ichiro Masunaga¹  Itsuro Kato²  Takaki Iwagami²  Naofumi Yamatomo³ 

[1] Research Reactor Institute, Kyoto University, Kumatori-cho, Sennan-gun, Osaka, 590-0494, Japan;Department of Oral and Maxillofacial Surgery, Osaka University Graduate School of Dentistry, Yamadaoka 1-8, Suita, Osaka, 565-0871, Japan;Dental and Oral Surgery, Osaka Saiseikai Senri Hospital, Tsukumodai 1-1, Suita, Osaka, 565-0862, Japan

关键词: Oral squamous cell carcinoma;    Boron neutron capture therapy;    Microbubble;    Ultrasound;   

Others  :  829594
DOI  :  10.1186/1748-717X-8-280

 received in 2013-08-16, accepted in 2013-11-17,  发布年份 2013

【 摘 要 】

Background

Boron neutron capture therapy (BNCT) is a selective radiotherapy that is dependent on the accumulation of ¹⁰B compound in tumors. Low-intensity ultrasound produces a transient pore on cell membranes, sonoporation, which enables extracellular materials to enter cells. The effect of sonoporation on BNCT was examined in oral squamous cell carcinoma (SCC) xenografts in nude mice.

Materials and methods

Tumor-bearing mice were administrated boronophenylalanine (BPA) or boronocaptate sodium (BSH) intraperitoneally. Two hours later, tumors were subjected to sonoporation using microbubbles followed by neutron irradiation.

Results

The ¹⁰B concentration was higher in tumors treated with sonoporation than in untreated tumors, although the difference was not significant in BPA. When tumors in mice that received BPA intraperitoneally were treated with sonoporation followed by exposure to thermal neutrons, tumor volume was markedly reduced and the survival rate was prolonged. Such enhancements by sonoporation were not observed in mice treated with BSH-mediated BNCT.

Conclusions

These results indicate that sonoporation enhances the efficiency of BPA-mediated BNCT for oral SCC. Sonoporation may modulate the microlocalization of BPA and BSH in tumors and increase their intracellular levels.

【 授权许可】

   
2013 Yamatomo et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Cooper JS, Porter K, Mallin K, Hoffman HT, Weber RS, Ang KK, Gay EG, Langer CJ: National Cancer Database report on cancer of the head and neck: 10-year update. Head Neck 2009, 31:748-758.
• [2]Forastiere A, Koch W, Trotti A, Sidransky D: Head and neck cancer. N Engl J Med 2002, 345:1890-1900.
• [3]Carvalho AL, Nishimoto IN, Califano JA, Kowalski LP: Trends in incidence and prognosis for head and neck cancer in the United States: a site-specific analysis of the SEER database. Int J Cancer 2005, 114:806-816.
• [4]Coderre JA, Morris GM: The radiation biology of boron neutron capture therapy. Radiat Res 1999, 151:1-18.
• [5]Barth RF, Coderre JA, Vicente MG, Blue TE: Boron neutron capture therapy of cancer: Current status and future prospects. Clin Cancer Res 2005, 11:3987-4002.
• [6]Tachibana K, Uchida T, Ogawa K, Yamashita N, Tamura K: Induction of cell-membrane porosity by ultrasound. Lancet 1999, 353:1409.
• [7]Newman CM, Lawrie A, Brisken AF, Cumberland DC: Ultrasound gene therapy: on the road from concept to reality. Echocardiography 2001, 18:339-347.
• [8]Fechheimer M, Boylan JF, Parker S, Sisken JE, Patel GL, Zimmer SG: Transfection of mammalian cells with plasmid DNA by scrape loading and sonication loading. Proc Natl Acad Sci U S A 1987, 84:8463-8467.
• [9]Escoffre JM, Zeghimi A, Novell A, Bouakaz A: In-vivo gene delivery by sonoporation: recent progress and prospects. Curr Gene Ther 2013, 13:2-14.
• [10]Tsutsui JM, Xie F, Porter RT: The use of microbubbles to target drug delivery. Cardiovasc Ultrasound 2004, 2:23. BioMed Central Full Text
• [11]Hernot S, Klibanov AL: Microbubbles in ultrasound-triggered drug and gene delivery. Adv Drug Deliv Rev 2008, 60:1153-1166.
• [12]Watanabe Y, Aoi A, Horie S, Tomita N, Mori S, Morikawa H, Matsumura Y, Vassaux G, Kodama T: Low-intensity ultrasound and microbubbles enhance the antitumor effect of cisplatin. Cancer Sci 2008, 99:2525-2531.
• [13]Li HL, Zheng XZ, Wang HP, Li F, Wu Y, Du LF: Ultrasound-targeted microbubble destruction enhances AAV-mediated gene transfection in human RPE cells in vitro and rat retina in vivo. Gene Ther 2009, 16:1146-1153.
• [14]Kowalczuk L, Boudinet M, el Sanharawi M, Touchard E, Naud MC, Saïed A, Jeanny JC, Behar-Cohen F, Laugier P: In vivo gene transfer into the ocular ciliary muscle mediated by ultrasound and microbubbles. Ultrasound Med Biol 2011, 37:1814-1827.
• [15]Bokor D: Diagnostic efficacy of SonoVue. Am J Cardiol 2000, 86(4A):19G-24G.
• [16]Sidhu PS, Allan PL, Cattin F, Cosgrove DO, Davies AH, Do DD, Karakagil S, Langholz J, Legemate DA, Martegani A, Llull JB, Pezzoli C, Spinazzi A: Diagnostic efficacy of SonoVue, a second generation contrast agent, in the assessment of extracranial carotid or peripheral arteries using colour and spectral Doppler ultrasound: a multicentre study. Br J Radiol 2006, 79:44-51.
• [17]Shintani M, Takahashi G, Hamada M, Okunaga S, Iwai S, Yura Y: Effect of ultrasound on herpes simplex virus infection in cell culture. Virology J 2011, 8:446. BioMed Central Full Text
• [18]Coderre JA, Button TM, Micca PL, Fisher CD, Nawrocky MM, Liu HB: Neutron capture therapy of the 9L rat gliosarcoma using the p-boronophenylalanine-fructose complex. Int J Radiat Oncol Biol Phys 1994, 30:643-652.
• [19]Kamida A, Fujita Y, Kato I, Iwai S, Ono K, Suzuki M, Sakurai Y, Yura Y: Effect of neutron capture therapy on the cell cycle of human squamous cell carcinoma cells. Int J Radiat Biol 2008, 84:191-199.
• [20]Obayashi S, Kato I, Ono K, Masunaga S, Suzuki M, Nagata K, Sakurai Y, Yura Y: Delivery of 10boron to oral squamous cell carcinoma using boronophenylalanine and borocaptate sodium for boron neutron capture therapy. Oral Oncol 2004, 40:474-482.
• [21]Mishima Y, Honda C, Ichihashi M, Obara H, Hiratsuka J, Fukuda H, Karashima H, Kobayashi T, Kanda K, Yoshino K: Treatment of malignant melanoma by single thermal neutron capture therapy with melanoma-seeking 10B-compound. Lancet 1989, 2:388-389.
• [22]Ono K, Masunaga SI, Kinashi Y, Takagaki M, Akaboshi M, Kobayashi T, Akuta K: Radiobiological evidence suggesting heterogeneous microdistribution of boron compounds in tumors: its relation to quiescent cell population and tumor cure in neutron capture therapy. Int J Radiat Oncol Biol Phys 1996, 34:1081-1086.
• [23]Masunaga S, Ono K, Takahashi A, Sakurai Y, Ohnishi K, Kobayashi T, Kinashi Y, Takagaki M, Ohnishi T: Impact of the p53 status of the tumor cells on the effect of reactor neutron beam irradiation, with emphasis on the response of intratumor quiescent cells. Jpn J Cancer Res 2002, 93:1366-1377.
• [24]Detta A, Cruickshank GS: L-amino acid transporter-1 and boronophenylalanine-based boron neutron capture therapy of human brain tumors. Cancer Res 2009, 69:2126-2132.
• [25]Haase C, Bergmann R, Fuechtner F, Hoepping A, Pietzsch J: L-type amino acid transporters LAT1 and LAT4 in cancer: uptake of 3-O-methyl-6-18F-fluoro-L-dopa in human adenocarcinoma and squamous cell carcinoma in vitro and in vivo. J Nucl Med 2007, 48:2063-2071.
• [26]Teissié J, Escoffre JM, Paganin A, Chabot S, Bellard E, Wasungu L, Rols MP, Golzio M: Drug delivery by electropulsation: Recent developments in oncology. Int J Pharm 2012, 423:3-6.
• [27]Cemazar M, Skrk J, Mitrovic B, Sersa G: Changed delivery of boron to tumours using electroporation for boron neutron capture therapy with BSH. Br J Radiol 2000, 73:195-200.
• [28]Doi A, Kawabata S, Iida K, Yokoyama K, Kajimoto Y, Kuroiwa T, Shirakawa T, Kirihata M, Kasaoka S, Maruyama K, Kumada H, Sakurai Y, Masunaga S, Ono K, Miyatake S: Tumor-specific targeting of sodium borocaptate (BSH) to malignant glioma by transferrin-PEG liposomes: a modality for boron neutron capture therapy. J Neurooncol 2008, 87:287-294.
• [29]El-Zaria ME, Nakamura H: New strategy for synthesis of mercaptoundecahydrododecaborate derivatives via click chemistry: possible boron carriers and visualization in cells for neutron capture therapy. Inorg Chem 2009, 48:11896-11902.
• [30]Carmeliet P, Jain RK: Angiogenesis in cancer and other diseases. Nature 2000, 407:249-257.