Generic placeholder image

Letters in Drug Design & Discovery

Editor-in-Chief

ISSN (Print): 1570-1808
ISSN (Online): 1875-628X

General Research Article

Cytotoxicity of Sodium Arsenite-loaded Anti-HER2 Immunoliposomes Against HER2-expressing Human Breast Cancer Cell Lines

Author(s): Moslem Afrakhteh, Alireza Kheirollah, Aminollah Pourshohod, Mohammad Ali Ghaffari, Mostafa Jamalan* and Majid Zeinali*

Volume 16, Issue 5, 2019

Page: [556 - 562] Pages: 7

DOI: 10.2174/1570180815666180803120409

Price: $65

Abstract

Background: Chemotherapy is a routine approach in treatment of patients with cancer, while side effects of chemotherapeutic drugs are inevitable. To minimize side effects, specific targeting of neoplastic cells is a promising strategy in cancer therapy. Sodium arsenite is a metalloid toxin with anti-neoplastic properties, but low selectivity and carcinogenic activity have limited its clinical usage.

Methods: Targeting of HER2-overexpressing (SK-BR-3) and HER2-low expressing (MCF-7) cancerous breast cell lines by two different liposomal forms of sodium arsenite (bare liposome and trastuzumab-conjugated liposome) was investigated in the current study. Levels of HER2 expression in the above mentioned cell lines were confirmed by western blotting. Size and morphology of the constructed liposomes were characterized by atomic force microscopy (AFM) and dynamic light scattering (DLS). Viability of the cells after treatment was assessed using MTT assay.

Results: Sodium arsenite in the free and liposomal forms showed growth inhibitory effects against both SK-BR-3 and MCF-7 cell lines in an examined concentration range of 1-20 µM, although this effect was more significant in SK-BR-3 cell line. Loading of sodium arsenite in anti-HER2 immunoliposomes significantly enhanced its cytotoxicity while the specificity was also improved. By encapsulation of sodium arsenite in anti-HER2 immunoliposomes, its efficacy in ablation of SKBR- 3 cells was increased about 1.4-fold compared to the free or liposomal forms.

Conclusion: In conclusion, targeted delivery of sodium arsenite using anti-HER2 immunoliposomes can be considered as an alternative strategy for specific treatment of HER2-positive breast cancers.

Keywords: Sodium arsenite, liposome, anti-HER2 immunoliposome, chemotherapy, specific targeting.

Graphical Abstract
[1]
(a)Carter, P.; Presta, L.; Gorman, C.M.; Ridgway, J.; Henner, D.; Wong, W.; Rowland, A.M.; Kotts, C.; Carver, M.E.; Shepard, H.M. Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc. Nat. Acad. Sci., 1992, 89, 4285-4289.
(b)Yamamoto, T.; Ikawa, S.; Akiyama, T.; Semba, K.; Nomura, N.; Miyajima, N.; Saito, T.; Toyoshima, K. Similarity of protein encoded by the human c-erb-B-2 gene to epidermal growth factor receptor. Nature, 1986, 319, 230-234.
[2]
Yarden, Y.; Sliwkowski, M.X. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol., 2001, 2, 127-137.
[3]
Venter, D.; Kumar, S.; Tuzi, N.; Gullick, W. Overexpression of the c-erbB-2 oncoprotein in human breast carcinomas: Immunohistological assessment correlates with gene amplification. Lancet, 1987, 330, 69-72.
[4]
(a)Hirsch, F.R.; Franklin, W.A.; Veve, R.; Varella-Garcia, M.; Bunn, P.A. In: HER2/neu expression in malignant lung tumors; Seminars in oncology, Elsevier:, 2002; pp. 51-58.
(b)Hofmann, M.; Stoss, O.; Shi, D.; Büttner, R.; Van de Vijver, M.; Kim, W.; Ochiai, A.; Rüschoff, J.; Henkel, T. Assessment of a HER2 scoring system for gastric cancer: Results from a validation study. Histopathology, 2008, 52, 797-805.
[5]
Slamon, D.J.; Leyland-Jones, B.; Shak, S.; Fuchs, H.; Paton, V.; Bajamonde, A.; Fleming, T.; Eiermann, W.; Wolter, J.; Pegram, M. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. New. Eng. J. Med., 2001, 344, 783-792.
[6]
(a)Goldenberg, M.M. Trastuzumab, a recombinant DNA-derived humanized monoclonal antibody, a novel agent for the treatment of metastatic breast cancer. Clin. Therapeut., 1999, 21, 309-318.
(b)Hudis, C.A. Trastuzumab-mechanism of action and use in clinical practice. New. Eng. J. Med., 2007, 357, 39-51.
[7]
Cobleigh, M.A.; Vogel, C.L.; Tripathy, D.; Robert, N.J.; Scholl, S.; Fehrenbacher, L.; Wolter, J.M.; Paton, V.; Shak, S.; Lieberman, G. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J. Clin. Oncol.,1999, 17, 2639-2639; (b) Hubbard, S.R. EGF receptor inhibition: Attacks on multiple fronts. Cancer cell, 2005, 7, 287-288.
[8]
Banerjee, P.; Bhattacharyya, S.S.; Bhattacharjee, N.; Pathak, S.; Boujedaini, N.; Belon, P.; Khuda-Bukhsh, A.R. Ascorbic acid combats arsenic-induced oxidative stress in mice liver. Ecotoxicol. Envir. Safety.,2009, 72, 639-649; (b) Tapio, S.; Grosche, B., Arsenic in the aetiology of cancer. Mut. Res. Rev. Mut. Res., 2006, 612, 215-246.
[9]
Barrett, J.C.; Lamb, P.W.; Wang, T.; Te Lee, C. Mechanisms of arsenic-induced cell transformation. Biol. Trace Element. Res., 1989, 21, 421-429.
[10]
Yao, X-F.; Zheng, B-L.; Bai, J.; Jiang, L-P.; Zheng, Y.; Qi, B-X.; Geng, C-Y.; Zhong, L-F.; Yang, G.; Chen, M. Low-level sodium arsenite induces apoptosis through inhibiting TrxR activity in pancreatic β-cells. Environ. Toxicol. Pharmacol., 2015, 40, 486-491.
[11]
Zhu, X-X.; Yao, X-F.; Jiang, L-P.; Geng, C-Y.; Zhong, L-F.; Yang, G.; Zheng, B-L.; Sun, X-C. Sodium arsenite induces ROS-dependent autophagic cell death in pancreatic β-cells. Food Chem. Toxicol., 2014, 70, 144-150.
[12]
(a)Muenyi, C.S.; Trivedi, A.P.; Helm, C.W.; States, J.C. Cisplatin plus sodium arsenite and hyperthermia induces pseudo-G1 associated apoptotic cell death in ovarian cancer cells. Toxicol. Sci., 2014, 139, 74-82.
(b)Muenyi, C.S.; Pinhas, A.R.; Fan, T.W.; Brock, G.N.; Helm, C.W.; States, J.C. Sodium arsenite +/- hyperthermia sensitizes p53-expressing human ovarian cancer cells to cisplatin by modulating platinum-DNA damage responses. Toxicol. Sci., 2012, 127, 139-149.
(c)Muenyi, C.S.; States, V.A.; Masters, J.H.; Fan, T.W.; Helm, C.W.; States, J.C. Sodium arsenite and hyperthermia modulate cisplatin-DNA damage responses and enhance platinum accumulation in murine metastatic ovarian cancer xenograft after hyperthermic intraperitoneal chemotherapy (HIPEC). J. Ovarian Res., 2011, 4, 9.
(d)Taylor, B.F.; McNeely, S.C.; Miller, H.L.; States, J.C. Arsenite-induced mitotic death involves stress response and is independent of tubulin polymerization. Toxicol. Appl. Pharmacol., 2008, 230, 235-246.
[13]
Chou, Y.; Chao, P.; Tsai, M.; Cheng, H.; Chen, K.; Yang, D.; Yang, C.; Lin, A. Arsenite-induced cytotoxicity in dorsal root ganglion explants. Free Radical. Biol. Med., 2008, 44, 1553-1561.
[14]
Muenyi, C.S.; Trivedi, A.P.; Helm, C.W. Cisplatin plus sodium arsenite and hyperthermia induces pseudo-G1 associated apoptotic cell death in ovarian cancer cells. Toxicol. Sci., 2014, 139, 74-82.
[15]
Huwyler, J.; Yang, J.; Pardridge, W.M. Receptor mediated delivery of daunomycin using immunoliposomes: Pharmacokinetics and tissue distribution in the rat. J. Pharmacol. Experimen. Therapeut., 1997, 282, 1541-1546.
[16]
Allen, T.M.; Cullis, P.R. Drug delivery systems: Entering the mainstream. Science, 2004, 303, 1818-1822.
[17]
Lasic, D. General introduction to liposomes. Liposomes Phy. App. Elsevier Sci., 1993, 3, 1-43.
[18]
Ahmad, I.; Longenecker, M.; Samuel, J.; Allen, T.M. Antibody-targeted delivery of doxorubicin entrapped in sterically stabilized liposomes can eradicate lung cancer in mice. Cancer Res., 1993, 53, 1484-1488.
[19]
Barrajón-Catalán, E.; Menéndez-Gutiérrez, M.P.; Falco, A.; Carrato, A.; Saceda, M.; Micol, V. Selective death of human breast cancer cells by lytic immunoliposomes: Correlation with their HER2 expression level. Cancer Lett., 2010, 290, 192-203.
[20]
Johnson, D.L.; Pilson, M.E. Spectrophotometric determination of arsenite, arsenate, and phosphate in natural waters. Anal. Chim. Acta, 1972, 58, 289-299.
[21]
Peterson, G.L. A simplification of the protein assay method of Lowry. which is more generally applicable. Anal. Biochem., 1977, 83, 346-356.
[22]
Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Meth, 1983, 65, 55-63.
[23]
(a)Richardson, V.J.; Jeyasingh, K.; Jewkes, R.; Ryman, B.E.; Tattersall, M. Possible tumor localization of Tc-99m-labeled liposomes: effects of lipid composition, charge, and liposome size. J. Nuc. Med. Off. Pub. Soc. Nuc. Med., 1978, 19, 1049-1054.
(b)He, C.; Hu, Y.; Yin, L.; Tang, C.; Yin, C. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials, 2010, 31, 3657-3666.
(c)Hsu, M.; Juliano, R.L. Interactions of liposomes with the reticuloendothelial system: II. Nonspecific and receptor-mediated uptake of liposomes by mouse peritoneal macrophages. Biochimica et Biophysica Acta (BBA)-. Mol. Cell Res., 1982, 720, 411-419.
[24]
Richardson, V.J.; Jeyasingh, K.; Jewkes, R.F.; Ryman, B.E.; Tattersall, M.H. Possible tumor localization of Tc-99m-labeled liposomes: effects of lipid composition, charge, and liposome size. J. Nucl. Med., 1978, 19, 1049-1054.
[25]
Lattrich, C.; Juhasz-Boess, I.; Ortmann, O.; Treeck, O. Detection of an elevated HER2 expression in MCF-7 breast cancer cells overexpressing estrogen receptor β1. Oncol. Rep., 2008, 19, 811-817.
[26]
Jeon, B-G.; Kumar, B.M.; Kang, E-J.; Maeng, G-H.; Lee, Y-M.; Hah, Y-S.; Ock, S-A.; Kwack, D-O.; Park, B-W.; Rho, G-J. Differential cytotoxic effects of sodium meta-arsenite on human cancer cells, dental papilla stem cells and somatic cells correlate with telomeric properties and gene expression. Anticancer Res., 2011, 31, 4315-4328.
[27]
Watcharasit, P.; Thiantanawat, A.; Satayavivad, J. GSK3 promotes arsenite‐induced apoptosis via facilitation of mitochondria disruption. J. Appl. Toxicol., 2008, 28, 466-474.
[28]
Ruiz-Ramos, R.; Lopez-Carrillo, L.; Rios-Perez, A.D.; De Vizcaya-Ruíz, A.; Cebrian, M.E. Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-κB activation and cell proliferation in human breast cancer MCF-7 cells. Mut. Res. Gene. Toxicol. Enviro. Mutagenesis., 2009, 674, 109-115.
[29]
(a)Yang, P.; He, X-Q.; Peng, L.; Li, A-P.; Wang, X-R.; Zhou, J-W.; Liu, Q-Z. The role of oxidative stress in hormesis induced by sodium arsenite in Human Embryo Lung Fibroblast (HELF) cellular proliferation model. J. Toxicol. Environ. Health, 2007, 70, 976-983.
(b)Calabrese, E.J.; Baldwin, L.A. Inorganics and hormesis. Critic. Rev. Toxicol., 2003, 33, 215-304.
[30]
Stoica, A.; Pentecost, E.; Martin, M.B. Effects of arsenite on estrogen receptor-α expression and activity in MCF-7 breast cancer cells 1. Endocrinology, 2000, 141, 3595-3602.
[31]
Fathi, S.; Oyelere, A.K. Liposomal drug delivery systems for targeted cancer therapy: Is active targeting the best choice? Future Med. Chem., 2016, 8, 2091-2112.
[32]
(a)Allen, T.M.; Cullis, P.R. Drug delivery systems: Entering the mainstream. Science, 2004, 303, 1818-1822.
(b)Malam, Y.; Loizidou, M.; Seifalian, A.M. Liposomes and nanoparticles: Nanosized vehicles for drug delivery in cancer. Trends Pharmacol. Sci., 2009, 30, 592-599.
[33]
Park, J.W. Liposome-based drug delivery in breast cancer treatment. Breast Cancer Res., 2002, 4, 95-99.
[34]
(a)Guo, J.; Lu, W-L. Effects of stealth liposomal daunorubicin plus tamoxifen on the breast cancer and cancer stem cells. J. Pharm. Pharmaceu. Sci., 2010, 13, 136-151.
(b)Lin, Y-L.; Chen, C-H.; Wu, H-Y.; Tsai, N-M.; Jian, T-Y.; Chang, Y-C.; Lin, C-H.; Wu, C-H.; Hsu, F-T.; Leung, T.K. Inhibition of breast cancer with transdermal tamoxifen-encapsulated lipoplex. J. Nanobiotechnol, 2016, 14, 1.
[35]
O’brien, M.; Wigler, N.; Inbar, M.; Rosso, R.; Grischke, E.; Santoro, A.; Catane, R.; Kieback, D.; Tomczak, P.; Ackland, S. Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (CAELYX™/Doxil®) versus conventional doxorubicin for first-line treatment of metastatic breast cancer. Annals. Oncol., 2004, 15, 440-449.
[36]
Shin, D.H.; Koo, M.J.; Kim, J.S.; Kim, J.S. Herceptin-conjugated temperature-sensitive immunoliposomes encapsulating gemcitabine for breast cancer. Arch. Pharm. Res., 2016, 39, 350-358.
[37]
Zhang, Y.; Chan, H.F.; Leong, K.W. Advanced materials and processing for drug delivery: The past and the future. Adv. Drug Deliv. Rev., 2013, 65, 104-120.
[38]
Park, J.W.; Hong, K.; Carter, P.; Asgari, H.; Guo, L.Y.; Keller, G.A.; Wirth, C.; Shalaby, R.; Kotts, C.; Wood, W.I. Development of anti-p185HER2 immunoliposomes for cancer therapy. Proc. Natl. Acad. Sci. USA, 1995, 92, 1327-1331.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy