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Published in: Cancer Cell International 1/2012

Open Access 01-12-2012 | Primary research

Cellular damage and apoptosis along with changes in NF-kappa B expression were induced with contrast agent enhanced ultrasound in gastric cancer cells and hepatoma cells

Authors: Zao Jiang, Wei Wu, Meng-lu Qian

Published in: Cancer Cell International | Issue 1/2012

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Abstract

Background

The effect of cell injury and apoptosis induced by ultrasound with contrast agent has been verified. Contrast agent enhanced apoptosis and expression of genes that related to apoptosis and are responsive to ultrasound. This effect was associated with reactive oxygen species (ROS) production induced by the sonochemical reaction, as reported in previous studies. NF-kappa B may be one of the factors involved in oxidizing reactions or modulation during the process of ultrasound inducing apoptosis.

Results

Ultrasound irradiated gastric cancer cells (SGC7901 cell line) and hepatocellular carcinoma cells (SMMC-771 cell line) cultured in medium containing contrast agent. Significant cellular damage and apoptosis were observed in the bath cells incubated for 24 hours following 120 seconds ultrasonic irradiation. I kappa B alfa expression synchronously increased in the treatment groups of both the cell lines, and the down-regulated expression of NF-kappa B influenced its-regulated expression of genes that related to apoptosis. Production of intracellular ROS and elevation of NF-kappa B level occurred after incubation of the cells for 1 hour following ultrasonic treatment.

Conclusions

Our result suggested that contrast agent enhanced the biological effect of ultrasound. Their reaction might stimulate the transitory expression of NF-kappaB, and subsequent elevation in IκBalfa expression could lead to the apoptosis of SGC7901 cells and SMMC-771 cells.
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Literature
1.
go back to reference Sergeeva NS, Sviridova IK, Nikolaev AL, Ambrozevich EG, Kabisov RK, Sarantseva OS, Kurilyak OA, Al'kov SV, Sokolov VV: Effects of various modes of sanitation with low frequency ultrasound on in vitro survival of human tumor cells. Bull Exp Biol Med. 2001, 131: 279-282. 10.1023/A:1017672003969.CrossRefPubMed Sergeeva NS, Sviridova IK, Nikolaev AL, Ambrozevich EG, Kabisov RK, Sarantseva OS, Kurilyak OA, Al'kov SV, Sokolov VV: Effects of various modes of sanitation with low frequency ultrasound on in vitro survival of human tumor cells. Bull Exp Biol Med. 2001, 131: 279-282. 10.1023/A:1017672003969.CrossRefPubMed
2.
go back to reference Lejbkowicz F, Salzberg S: Distinct sensitivity of normal and malignant cells to ultrasound in vitro. Environ Health Perspect. 1997, 105 (Suppl 6): 1575-1578. 10.1289/ehp.97105s61575.PubMedCentralCrossRefPubMed Lejbkowicz F, Salzberg S: Distinct sensitivity of normal and malignant cells to ultrasound in vitro. Environ Health Perspect. 1997, 105 (Suppl 6): 1575-1578. 10.1289/ehp.97105s61575.PubMedCentralCrossRefPubMed
3.
go back to reference Zhai BJ, Wu F, Shao ZY, Hu K, Zhao CL, Wang ZB: Establishment of human hepatocellular carcinoma multidrug-resistance cell line (HepG2/Adm) and study apoptosis induced by low-frequency pulse ultrasound exposure. Zhonghua Gan Zang Bing Za Zhi. 2004, 12: 95-98.PubMed Zhai BJ, Wu F, Shao ZY, Hu K, Zhao CL, Wang ZB: Establishment of human hepatocellular carcinoma multidrug-resistance cell line (HepG2/Adm) and study apoptosis induced by low-frequency pulse ultrasound exposure. Zhonghua Gan Zang Bing Za Zhi. 2004, 12: 95-98.PubMed
4.
go back to reference Fuciarelli AF, Sisk EC, Thomas RM, Miller DL: Induction of base damage in DNA solutions by ultrasonic cavitation. Free Radic Biol Med. 1995, 18: 231-238. 10.1016/0891-5849(94)00119-5.CrossRefPubMed Fuciarelli AF, Sisk EC, Thomas RM, Miller DL: Induction of base damage in DNA solutions by ultrasonic cavitation. Free Radic Biol Med. 1995, 18: 231-238. 10.1016/0891-5849(94)00119-5.CrossRefPubMed
5.
go back to reference Cheng Q, Qian ML: Low frequency dynamic behavior of ultrasound microbubble contrast agent. Tech Acoust. 2006, 25: 292-298. Cheng Q, Qian ML: Low frequency dynamic behavior of ultrasound microbubble contrast agent. Tech Acoust. 2006, 25: 292-298.
6.
go back to reference Feril LB, Kondo T, Zhao QL, Ogawa R, Tachibana K, Kudo N, Fujimoto S, Nakamura S: Enhancement of ultrasound-induced apoptosis and cell lysis by echo-contrast agents. Ultrasound Med Biol. 2003, 29: 331-337. 10.1016/S0301-5629(02)00700-7.CrossRefPubMed Feril LB, Kondo T, Zhao QL, Ogawa R, Tachibana K, Kudo N, Fujimoto S, Nakamura S: Enhancement of ultrasound-induced apoptosis and cell lysis by echo-contrast agents. Ultrasound Med Biol. 2003, 29: 331-337. 10.1016/S0301-5629(02)00700-7.CrossRefPubMed
7.
go back to reference Furusawa Yukihiro, Zhao Qing-Li, Ali Hassan Mariame, Tabuchi Yoshiaki, Takasaki Ichiro, Wada Shigehito, Kondo Takashi: Ultrasound-induced apoptosis in the presence of Sonazoid and associated alterations in gene expression levels: A possible therapeutic application. Cancer Letters. 2010, 288: 107-115. 10.1016/j.canlet.2009.06.029.CrossRefPubMed Furusawa Yukihiro, Zhao Qing-Li, Ali Hassan Mariame, Tabuchi Yoshiaki, Takasaki Ichiro, Wada Shigehito, Kondo Takashi: Ultrasound-induced apoptosis in the presence of Sonazoid and associated alterations in gene expression levels: A possible therapeutic application. Cancer Letters. 2010, 288: 107-115. 10.1016/j.canlet.2009.06.029.CrossRefPubMed
8.
go back to reference Ando Hidetaka, Feril Loreto, Kondo Takashi, Tabuchi Yoshiaki, Ogawa Ryohei, Zhao Qing-Li, Cui Zheng-Guo, Umemura Shin-ichiro, Yoshikawa Hideki, Misaki Takuro: An echo-contrast agent, Levovist, lowers the ultrasound intensity required to induce apoptosis of human leukemia cells. Cancer Letters. 2006, 242: 37-45. 10.1016/j.canlet.2005.10.032.CrossRefPubMed Ando Hidetaka, Feril Loreto, Kondo Takashi, Tabuchi Yoshiaki, Ogawa Ryohei, Zhao Qing-Li, Cui Zheng-Guo, Umemura Shin-ichiro, Yoshikawa Hideki, Misaki Takuro: An echo-contrast agent, Levovist, lowers the ultrasound intensity required to induce apoptosis of human leukemia cells. Cancer Letters. 2006, 242: 37-45. 10.1016/j.canlet.2005.10.032.CrossRefPubMed
9.
go back to reference Kondo T, Misík V, Riesz P: Effect of gas-containing microspheres and echo contrast agents on free radical formation by ultrasound. Free Radic Biol Med. 1998, 25: 605-612. 10.1016/S0891-5849(98)00106-3.CrossRefPubMed Kondo T, Misík V, Riesz P: Effect of gas-containing microspheres and echo contrast agents on free radical formation by ultrasound. Free Radic Biol Med. 1998, 25: 605-612. 10.1016/S0891-5849(98)00106-3.CrossRefPubMed
10.
go back to reference Millor DL, Quddus J: Sonoporation of monolayer cells by diagnostic ultrasound activation of contrast-agent gas bodies. Ultrasound Med Biol. 2000, 26: 661-667. 10.1016/S0301-5629(99)00170-2.CrossRef Millor DL, Quddus J: Sonoporation of monolayer cells by diagnostic ultrasound activation of contrast-agent gas bodies. Ultrasound Med Biol. 2000, 26: 661-667. 10.1016/S0301-5629(99)00170-2.CrossRef
11.
go back to reference Angelica RB-P, Marlene J-Del-R, Carlos V-P: Vitamin K3 and vitamin C alone or in combination induced apoptosis in leukemia cells by a similar oxidative stress signalling mechanism. Cancer Cell Int. 2011, 11: 19-10.1186/1475-2867-11-19.CrossRef Angelica RB-P, Marlene J-Del-R, Carlos V-P: Vitamin K3 and vitamin C alone or in combination induced apoptosis in leukemia cells by a similar oxidative stress signalling mechanism. Cancer Cell Int. 2011, 11: 19-10.1186/1475-2867-11-19.CrossRef
12.
go back to reference Hunot S, Brugg B, Ricard D, Michel PP, Muriel MP, Ruberg M, Faucheux BA, Agid Y, Hirsch EC: Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with parkinson disease. Proc Natl Acad Sci USA. 1997, 94: 7531-7536. 10.1073/pnas.94.14.7531.PubMedCentralCrossRefPubMed Hunot S, Brugg B, Ricard D, Michel PP, Muriel MP, Ruberg M, Faucheux BA, Agid Y, Hirsch EC: Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with parkinson disease. Proc Natl Acad Sci USA. 1997, 94: 7531-7536. 10.1073/pnas.94.14.7531.PubMedCentralCrossRefPubMed
13.
go back to reference Kaul N, Choi J, Forman HJ: Transmembrane redox signaling activates NF-kappa B in macrophages. Free Radic Biol Med. 1998, 24: 202-207. 10.1016/S0891-5849(97)00209-8.CrossRefPubMed Kaul N, Choi J, Forman HJ: Transmembrane redox signaling activates NF-kappa B in macrophages. Free Radic Biol Med. 1998, 24: 202-207. 10.1016/S0891-5849(97)00209-8.CrossRefPubMed
15.
go back to reference Liu ZG, Hsu H, Goeddel DV, Karin M: Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell. 1996, 87: 565-576. 10.1016/S0092-8674(00)81375-6.CrossRefPubMed Liu ZG, Hsu H, Goeddel DV, Karin M: Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell. 1996, 87: 565-576. 10.1016/S0092-8674(00)81375-6.CrossRefPubMed
16.
go back to reference Honda H, Zhao QL, Kondo T: Effects of dissolved gases and an echo contrast agent on apoptosis induced by ultrasound and its mechanism via the mitochondria-caspase pathway. Ultrasound Med Biol. 2002, 28: 673-682. 10.1016/S0301-5629(02)00509-4.CrossRefPubMed Honda H, Zhao QL, Kondo T: Effects of dissolved gases and an echo contrast agent on apoptosis induced by ultrasound and its mechanism via the mitochondria-caspase pathway. Ultrasound Med Biol. 2002, 28: 673-682. 10.1016/S0301-5629(02)00509-4.CrossRefPubMed
17.
go back to reference Honda H, Kondo T, Zhao QL, Feril LB, Kitagawa H: Role of intracellular calcium ions and reactive oxygen species in apoptosis induced by ultrasound. Ultrasound Med Biol. 2004, 30: 683-692. 10.1016/j.ultrasmedbio.2004.02.008.CrossRefPubMed Honda H, Kondo T, Zhao QL, Feril LB, Kitagawa H: Role of intracellular calcium ions and reactive oxygen species in apoptosis induced by ultrasound. Ultrasound Med Biol. 2004, 30: 683-692. 10.1016/j.ultrasmedbio.2004.02.008.CrossRefPubMed
18.
go back to reference Feril LB, Kondo T, Ogawa R, Zhao QL: Dose-dependent inhibition of ultrasound-induced cell killing and free radical production by carbon dioxide. Ultrason Sonochem. 2003, 10: 81-84. 10.1016/S1350-4177(02)00122-0.CrossRefPubMed Feril LB, Kondo T, Ogawa R, Zhao QL: Dose-dependent inhibition of ultrasound-induced cell killing and free radical production by carbon dioxide. Ultrason Sonochem. 2003, 10: 81-84. 10.1016/S1350-4177(02)00122-0.CrossRefPubMed
19.
go back to reference Skorpíková J, Dolníková M, Hrazdira I, Janisch R: Changes in microtubules and microfilaments due to a combined effect of ultrasound and cytostatics in HeLa cells. Folia Biol (Praha). 2001, 47: 143-147. Skorpíková J, Dolníková M, Hrazdira I, Janisch R: Changes in microtubules and microfilaments due to a combined effect of ultrasound and cytostatics in HeLa cells. Folia Biol (Praha). 2001, 47: 143-147.
20.
go back to reference Lagneaux L, de Meulenaer EC, 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. 2002, 30: 1293-1301. 10.1016/S0301-472X(02)00920-7.CrossRefPubMed Lagneaux L, de Meulenaer EC, 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. 2002, 30: 1293-1301. 10.1016/S0301-472X(02)00920-7.CrossRefPubMed
21.
go back to reference Kretz-Remy C, Arrigo AP: Selenium: a key element that controls NF-kappa B activation and I kappa B alpha half life. Biofactors. 2001, 14: 117-125. 10.1002/biof.5520140116.CrossRefPubMed Kretz-Remy C, Arrigo AP: Selenium: a key element that controls NF-kappa B activation and I kappa B alpha half life. Biofactors. 2001, 14: 117-125. 10.1002/biof.5520140116.CrossRefPubMed
22.
go back to reference Notarbartolo M, Poma P, Perri D, Dusonchet L, Cervello M, D'Alessandro N: Antitumor effects of curcumin, alone or in combination with cisplatin or doxorubicin, on human hepatic cancer cells. Analysis of their possible relationship to changes in NF-kB activation levels and in IAP gene expression. Cancer Lett. 2005, 224: 53-65. 10.1016/j.canlet.2004.10.051.CrossRefPubMed Notarbartolo M, Poma P, Perri D, Dusonchet L, Cervello M, D'Alessandro N: Antitumor effects of curcumin, alone or in combination with cisplatin or doxorubicin, on human hepatic cancer cells. Analysis of their possible relationship to changes in NF-kB activation levels and in IAP gene expression. Cancer Lett. 2005, 224: 53-65. 10.1016/j.canlet.2004.10.051.CrossRefPubMed
23.
go back to reference Zachary JF, Blue JP, Miller RJ, O'Brien WD: Vascular lesions and s-thrombomodulin concentrations from auricular arteries of rabbits infused with microbubble contrast agent and exposed to pulsed ultrasound. Ultrasound Med Biol. 2006, 32: 1781-1791. 10.1016/j.ultrasmedbio.2005.11.013.PubMedCentralCrossRefPubMed Zachary JF, Blue JP, Miller RJ, O'Brien WD: Vascular lesions and s-thrombomodulin concentrations from auricular arteries of rabbits infused with microbubble contrast agent and exposed to pulsed ultrasound. Ultrasound Med Biol. 2006, 32: 1781-1791. 10.1016/j.ultrasmedbio.2005.11.013.PubMedCentralCrossRefPubMed
24.
go back to reference Wu W, Lin XB, Qian JM, Ji ZL, Jiang Z: Ultrasonic aspiration hepatectomy for 136 patients with hepatocellular carcinoma. World J Gastroenterol. 2002, 8: 763-765.PubMed Wu W, Lin XB, Qian JM, Ji ZL, Jiang Z: Ultrasonic aspiration hepatectomy for 136 patients with hepatocellular carcinoma. World J Gastroenterol. 2002, 8: 763-765.PubMed
25.
go back to reference Wu W, Ning XB, Jiang Z, Guo XY, Feng R: Formation of micro-vessel embolization in rabbit liver induced by low power ultrasound irradiation combined with LEVOVIST agent. J Southeast Univ (Natural Science Edition, in chinese). 2003, 33: 300-302. Wu W, Ning XB, Jiang Z, Guo XY, Feng R: Formation of micro-vessel embolization in rabbit liver induced by low power ultrasound irradiation combined with LEVOVIST agent. J Southeast Univ (Natural Science Edition, in chinese). 2003, 33: 300-302.
26.
go back to reference Song H, Park H, Kim YS, Kim KD, Lee HK, Cho DH, Yang JW, Hur DY: L-kynurenine-induced apoptosis in human NK cells is mediated by reactive oxygen species. Int Immunopharmaco. 2011, 11: 932-938. 10.1016/j.intimp.2011.02.005.CrossRef Song H, Park H, Kim YS, Kim KD, Lee HK, Cho DH, Yang JW, Hur DY: L-kynurenine-induced apoptosis in human NK cells is mediated by reactive oxygen species. Int Immunopharmaco. 2011, 11: 932-938. 10.1016/j.intimp.2011.02.005.CrossRef
Metadata
Title
Cellular damage and apoptosis along with changes in NF-kappa B expression were induced with contrast agent enhanced ultrasound in gastric cancer cells and hepatoma cells
Authors
Zao Jiang
Wei Wu
Meng-lu Qian
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2012
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/1475-2867-12-8

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