Targeted delivery of doxorubicin for the treatment of bone metastasis from breast cancer using alendronate-functionalized graphene oxide nanosheets

Tung Thanh Pham; Hanh Thuy Nguyen; Cao Dai Phung; Shiva Pathak; Shobha Regmi; Dong-Ho Ha; Jong Oh Kim; Chul Soon Yong; Sang Kyoon Kim; Ji-Eun Choi; Simmyung Yook; Jun-Beom Park; Jee-Heon Jeong

Journal of Industrial and Engineering Chemistry, Vol.76, 310-317, August, 2019

DOI10.1016/j.jiec.2019.03.055 Export Citation

Targeted delivery of doxorubicin for the treatment of bone metastasis from breast cancer using alendronate-functionalized graphene oxide nanosheets

Tung Thanh Pham, Hanh Thuy Nguyen, Cao Dai Phung, Shiva Pathak, Shobha Regmi, Dong-Ho Ha, Jong Oh Kim, Chul Soon Yong, Sang Kyoon Kim¹, Ji-Eun Choi², Simmyung Yook^{3, †}, Jun-Beom Park^{4, †}, and Jee-Heon Jeong^†

College of Pharmacy, Yeungnam University, Gyeongsan, Gyeongbuk 38541, South Korea
¹Laboratory Animal Center, Daegu–Gyeongbuk Medical Innovation Foundation (DGMIF), Daegu 41061, South Korea
²Department of Clinical Medicinal Sciences, PRIME College of Interdisciplinary & Creative Studies, Konyang University, Nonsan, Chungnam 32992, South Korea
³College of Pharmacy, Keimyung University, Daegu 42601, South Korea
⁴Department of Periodontics, Seoul St Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul 06591, South Korea

E-mail:, ,

Selective delivery of anti-cancer drugs to bone tumors remains an on-going developmental issue due to problems of drug availability and the physiological nature of bone. This study was undertaken to enhance accumulation of doxorubicin (DOX) in bone metastasis microenvironments using alendronate-functionalized graphene oxide nanosheets (NGO-ALs). In vivo biodistribution study showed NGO-ALs were retained for longer and at higher concentrations in bone tumor areas than non-functionalized NGOs. Our findings suggest that NGO-ALs could be used as a promising carrier to enhance antitumor effects and diminish the off-target effects of DOX for the treatment of bone metastasis.

Keywords:Bone metastasis;Graphene oxides;Alendronate;Targeted delivery

[References]

Coleman RE, Clin. Cancer Res., 12, 6243 (2006)
Coleman RE, Rubens RD, Br. J. Cancer, 55, 61 (1987)
Coleman RE, Cancer Treat. Rev., 27, 165 (2001)
Delea T, McKiernan J, Brandman J, Edelsberg J, Sung J, Raut M, et al., J. Support. Oncol., 4, 341 (2006)
Costa L, Badia X, Chow E, Lipton A, Wardley A, Support. Care Cancer, 16, 879 (2008)
Athanasiou KA, Zhu C, Lanctot DR, Agrawal CM, Wang X, Tissue Eng., 6, 361 (2000)
Jiang T, Yu X, Carbone EJ, Nelson C, Kan HM, Lo KWH, Int. J. Pharm., 475, 547 (2014)
Culpepper BK, Bonvallet PP, Reddy MS, Ponnazhagan S, Bellis SL, Biomaterials, 34, 1506 (2013)
Culpepper BK, Morris DS, Prevelige PE, Bellis SL, Biomaterials, 34, 2455 (2013)
Zhang G, Guo B, Wu H, Tang T, Zhang BT, Zheng L, et al., Nat. Med., 18, 307 (2012)
Wang H, Liu J, Tao S, Chai G, Wang J, Hu FQ, et al., Int. J. Nanomed., 10, 5671 (2015)
Neale JR, Richter NB, Merten KE, Taylor KG, Singh S, Waite LC, et al., Bioorg. Med. Chem. Lett., 19, 680 (2009)
Xie Y, Tan X, Huang J, Huang H, Zou P, Hu J, Drug Deliv., 24, 1067 (2017)
Chaudhari KR, Kumar A, Khandelwal VKM, Ukawala M, Manjappa AS, Mishra AK, et al., J. Control. Release, 158, 470 (2012)
Ye WI, Zhao YP, Li HQ, Na R, Li F, Mei QB, et al., Sci. Rep., 5, 14614 (2015)
Karacivi M, Bolu BS, Sanyal R, Mol. Pharm., 14, 1373 (2017)
Swami A, Reagan MR, Basto P, Mishima Y, Kamaly N, Glavey S, et al., Proc. Natl. Acad. Sci. U. S. A., 111, 10287 (2014)
Shane E, N. Engl. J. Med., 362, 1825 (2010)
Goeckeler WF, Edwards B, Volkert WA, Holmes RA, Simon J, Wilson D, J. Nucl. Med., 28, 495 (1987)
Bayouth JE, Macey DJ, Kasi LP, Fossella FV, J. Nucl. Med., 35, 63 (1994)
Hirabayashi H, Sawamoto T, Fujisaki J, Tokunaga Y, Kimura S, Hata T, Pharm. Res., 18, 646 (2001)
Yang X, Zhang X, Liu Z, Ma Y, Huang Y, Chen Y, J. Phys. Chem. C, 112, 17554 (2008)
Tran TH, Thapa RK, Nguyen HT, Pham TT, Ramasamy T, Kim DS, et al., J. Pharm. Invest., 46, 505 (2016)
Lee JS, Youn YH, Kwon IK, Ko NR, J. Pharm. Invest., 48, 209 (2018)
Stankovich S, Piner RD, Nguyen ST, Ruoff RS, Carbon, 44, 3342 (2006)
Ames BN, Assay of Inorganic Phosphate, Total Phosphate and Phosphatases. Methods in Enzymology, Academic Press, 1966.Methods in Enzymology, Academic Press, p.115 1966
Wright LE, Ottewell PD, Rucci N, Peyruchaud O, Pagnotti GM, Chiechi A, et al., Bonekey Rep., 5, 804 (2016)
Hummers WS, Offeman RE, J. Am. Chem. Soc., 80, 1339 (1958)
Goncalves G, Vila M, Bdikin I, de Andres A, Emami N, Ferreira RAS, et al., Sci. Rep., 4, 6735 (2014)
Szabo T, Tombacz E, Illes E, Dekany I, Carbon, 44, 537 (2006)
Liu J, Cui L, Losic D, Acta Biomater., 9, 9243 (2013)
Kingsley LA, Fournier PG, Chirgwin JM, Guise TA, Mol. Cancer Ther., 6, 2609 (2007)
Baron R, Neff L, Louvard D, Courtoy PJ, J. Cell Boil., 101, 2210 (1985)
Teitelbaum SL, Science, 289, 1504 (2000)
Hong BJ, Compton OC, An Z, Eryazici I, Nguyen ST, ACS Nano., 6, 63 (2012)
Yan L, Chang YN, Zhao L, Gu Z, Liu X, Tian G, et al., Carbon, 57, 120 (2013)
Liu Z, Robinson JT, Sun XM, Dai HJ, J. Am. Chem. Soc., 130(33), 10876 (2008)
Le QV, Choi J, Oh YK, J. Pharm. Invest., 48, 527 (2018)
Wu X, Hu Z, Nizzero S, Zhang G, Ramirez MR, Shi C, et al., J. Control. Release, 268, 92 (2017)
Jasim DA, Moyon CM, Begin D, Bianco A, Kostarelos K, Chem. Sci., 6, 3952 (2015)
Li B, Zhang XY, Yang JZ, Zhang YJ, Li WX, Fan CH, et al., Int. J. Nanomed., 9, 4697 (2014)
Meyer JC, Geim AK, Katsnelson MI, Novoselov KS, Booth TJ, Roth S, Nature, 446, 60 (2007)
Patra N, Wang B, Kral P, Nano Lett., 9, 3766 (2009)
Yang K, Wan J, Zhang S, Zhang Y, Lee ST, Liu Z, ACS Nano., 5, 516 (2011)
Sato M, Grasser W, Endo N, Akins R, Simmons H, Thompson DD, et al., J. Clin. Invest., 88, 2095 (1991)
Chaudhari KR, Kumar A, Khandelwal VKM, Mishra AK, Monkkonen J, Murthy RSR, Adv. Funct. Mater., 22(19), 4101 (2012)

[Referenced By]

[1] Coleman RE, Clin. Cancer Res., 12, 6243 (2006)

[2] Coleman RE, Rubens RD, Br. J. Cancer, 55, 61 (1987)

[3] Coleman RE, Cancer Treat. Rev., 27, 165 (2001)

[4] Delea T, McKiernan J, Brandman J, Edelsberg J, Sung J, Raut M, et al., J. Support. Oncol., 4, 341 (2006)

[5] Costa L, Badia X, Chow E, Lipton A, Wardley A, Support. Care Cancer, 16, 879 (2008)

[6] Athanasiou KA, Zhu C, Lanctot DR, Agrawal CM, Wang X, Tissue Eng., 6, 361 (2000)

[7] Jiang T, Yu X, Carbone EJ, Nelson C, Kan HM, Lo KWH, Int. J. Pharm., 475, 547 (2014)

[8] Culpepper BK, Bonvallet PP, Reddy MS, Ponnazhagan S, Bellis SL, Biomaterials, 34, 1506 (2013)

[9] Culpepper BK, Morris DS, Prevelige PE, Bellis SL, Biomaterials, 34, 2455 (2013)

[10] Zhang G, Guo B, Wu H, Tang T, Zhang BT, Zheng L, et al., Nat. Med., 18, 307 (2012)

[11] Wang H, Liu J, Tao S, Chai G, Wang J, Hu FQ, et al., Int. J. Nanomed., 10, 5671 (2015)

[12] Neale JR, Richter NB, Merten KE, Taylor KG, Singh S, Waite LC, et al., Bioorg. Med. Chem. Lett., 19, 680 (2009)

[13] Xie Y, Tan X, Huang J, Huang H, Zou P, Hu J, Drug Deliv., 24, 1067 (2017)

[14] Chaudhari KR, Kumar A, Khandelwal VKM, Ukawala M, Manjappa AS, Mishra AK, et al., J. Control. Release, 158, 470 (2012)

[15] Ye WI, Zhao YP, Li HQ, Na R, Li F, Mei QB, et al., Sci. Rep., 5, 14614 (2015)

[16] Karacivi M, Bolu BS, Sanyal R, Mol. Pharm., 14, 1373 (2017)

[17] Swami A, Reagan MR, Basto P, Mishima Y, Kamaly N, Glavey S, et al., Proc. Natl. Acad. Sci. U. S. A., 111, 10287 (2014)

[18] Shane E, N. Engl. J. Med., 362, 1825 (2010)

[19] Goeckeler WF, Edwards B, Volkert WA, Holmes RA, Simon J, Wilson D, J. Nucl. Med., 28, 495 (1987)

[20] Bayouth JE, Macey DJ, Kasi LP, Fossella FV, J. Nucl. Med., 35, 63 (1994)

[21] Hirabayashi H, Sawamoto T, Fujisaki J, Tokunaga Y, Kimura S, Hata T, Pharm. Res., 18, 646 (2001)

[22] Yang X, Zhang X, Liu Z, Ma Y, Huang Y, Chen Y, J. Phys. Chem. C, 112, 17554 (2008)

[23] Tran TH, Thapa RK, Nguyen HT, Pham TT, Ramasamy T, Kim DS, et al., J. Pharm. Invest., 46, 505 (2016)

[24] Lee JS, Youn YH, Kwon IK, Ko NR, J. Pharm. Invest., 48, 209 (2018)

[25] Stankovich S, Piner RD, Nguyen ST, Ruoff RS, Carbon, 44, 3342 (2006)

[26] Ames BN, Assay of Inorganic Phosphate, Total Phosphate and Phosphatases. Methods in Enzymology, Academic Press, 1966.Methods in Enzymology, Academic Press, p.115 1966

[27] Wright LE, Ottewell PD, Rucci N, Peyruchaud O, Pagnotti GM, Chiechi A, et al., Bonekey Rep., 5, 804 (2016)

[28] Hummers WS, Offeman RE, J. Am. Chem. Soc., 80, 1339 (1958)

[29] Goncalves G, Vila M, Bdikin I, de Andres A, Emami N, Ferreira RAS, et al., Sci. Rep., 4, 6735 (2014)

[30] Szabo T, Tombacz E, Illes E, Dekany I, Carbon, 44, 537 (2006)

[31] Liu J, Cui L, Losic D, Acta Biomater., 9, 9243 (2013)

[32] Kingsley LA, Fournier PG, Chirgwin JM, Guise TA, Mol. Cancer Ther., 6, 2609 (2007)

[33] Baron R, Neff L, Louvard D, Courtoy PJ, J. Cell Boil., 101, 2210 (1985)

[34] Teitelbaum SL, Science, 289, 1504 (2000)

[35] Hong BJ, Compton OC, An Z, Eryazici I, Nguyen ST, ACS Nano., 6, 63 (2012)

[36] Yan L, Chang YN, Zhao L, Gu Z, Liu X, Tian G, et al., Carbon, 57, 120 (2013)

[37] Liu Z, Robinson JT, Sun XM, Dai HJ, J. Am. Chem. Soc., 130(33), 10876 (2008)

[38] Le QV, Choi J, Oh YK, J. Pharm. Invest., 48, 527 (2018)

[39] Wu X, Hu Z, Nizzero S, Zhang G, Ramirez MR, Shi C, et al., J. Control. Release, 268, 92 (2017)

[40] Jasim DA, Moyon CM, Begin D, Bianco A, Kostarelos K, Chem. Sci., 6, 3952 (2015)

[41] Li B, Zhang XY, Yang JZ, Zhang YJ, Li WX, Fan CH, et al., Int. J. Nanomed., 9, 4697 (2014)

[42] Meyer JC, Geim AK, Katsnelson MI, Novoselov KS, Booth TJ, Roth S, Nature, 446, 60 (2007)

[43] Patra N, Wang B, Kral P, Nano Lett., 9, 3766 (2009)

[44] Yang K, Wan J, Zhang S, Zhang Y, Lee ST, Liu Z, ACS Nano., 5, 516 (2011)

[45] Sato M, Grasser W, Endo N, Akins R, Simmons H, Thompson DD, et al., J. Clin. Invest., 88, 2095 (1991)

[46] Chaudhari KR, Kumar A, Khandelwal VKM, Mishra AK, Monkkonen J, Murthy RSR, Adv. Funct. Mater., 22(19), 4101 (2012)