Synthesis and Evaluation of 198Au/PAMAM-MPEG-FA against Cancer Cells

Author(s): Reza Rezaei, Simin Janitabar Darzi*, Mahnaz Yazdani

Journal Name: Anti-Cancer Agents in Medicinal Chemistry
(Formerly Current Medicinal Chemistry - Anti-Cancer Agents)

Volume 20 , Issue 10 , 2020

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Graphical Abstract:


Abstract:

Background: There is a significant dearth of clinical biochemistry researches to evaluate the facility of exploitation of folate targeted radioactive gold-labeled anti-cancer drugs against various cancer cell lines.

Objective: The aim of this paper was to develop a gold-based compound with an efficient therapeutic potential against breast cancer. To this end, the synthesis of the 198Au/PAMAM-MPEG-FA composite was considered here.

Methods: The radioactive gold (198Au) nanoparticles were encapsulated into Folic acid (FA)-targeted Polyamidoamine dendrimer (PAMAM) modified with Maleimide-Polyethylene glycol Succinimidyl Carboxymethyl ester (MPEG). After that, anticancer assessments of the prepared 198Au/PAMAM-MPEG-FA hybrid mater against breast cancer were investigated.

Further studies were also devised to compare the anticancer capabilities of the 198Au/PAMAM-MPEG-FA composite with the synthesized P-MPEG, 197Au/P-MPEG, 197Au/P-MPEG-FA, 197Au/P-FA and 198Au/P-MPEG-FA conjugates. The prepared drugs were characterized by means of various analytical techniques. The radionuclidic purity of the 198Au/P-MPEG-FA solution was determined using High Purity Germanium (HPGe) spectroscopy and its stability in the presence of human serum was studied. The cell uptake and toxicity of the prepared drugs were evaluated in vitro, and some comparative studies of the toxicity of the drugs were conducted towards the MCF7 (Human breast cancer cell), 4T1 (Mice breast adenocarcinoma cell) and C2C12 (Mice muscle normal cell).

Results: The results showed that cell uptake of 198Au/P-MPEG-FA nanoparticles is high in the 4T1 cell line and the order of uptake is as 4T1> MCF7> C2C12. Moreover, of the tested compounds, 198Au/P-MPEG-FA had the highest toxicity towards the cancerous 4T1 and MCF7 in all concentrations after 24, 48 and 72h (P < 0.001). Furthermore, the cytotoxicity of the drugs was concentration-dependent.

Conclusion: On the basis of the present research, 198Au/P-MPEG-FA has been proposed as a good candidate for the induction of cell death in breast cancer, although further experimental and clinical investigations are required.

Keywords: Radioactive gold, PAMAM dendrimer, drug targeting, cellular uptake, toxicity, folate.

[1]
Dobrovolskaia, M.A.; Patri, A.K.; Zheng, J.; Clogston, J.D.; Ayub, N.; Aggarwal, P.; Neun, B.W.; Hall, J.B.; McNeil, S.E. Interaction of colloidal gold nanoparticles with human blood: Effects on particle size and analysis of plasma protein binding profiles. Nanomedicine (Lond.), 2009, 5(2), 106-117.
[http://dx.doi.org/10.1016/j.nano.2008.08.001] [PMID: 19071065]
[2]
Zhou, B.; Xiong, Z.; Wang, P.; Peng, C.; Shen, M.; Mignani, S.; Majoral, J.P.; Shi, X. Targeted tumor dual mode CT/MR imaging using multifunctional polyethylenimine-entrapped gold nanoparticles loaded with gadolinium. Drug Deliv., 2018, 25(1), 178-186.
[http://dx.doi.org/10.1080/10717544.2017.1422299] [PMID: 29301434]
[3]
Sztandera, K.; Gorzkiewicz, M.; Klajnert-Maculewicz, B. Gold nanoparticles in cancer treatment. Mol. Pharm., 2019, 16(1), 1-23.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00810] [PMID: 30452861]
[4]
Duncan, B.; Kim, C.; Rotello, V.M. Gold nanoparticle platforms as drug and biomacromolecule delivery systems. J. Control. Release, 2010, 148(1), 122-127.
[http://dx.doi.org/10.1016/j.jconrel.2010.06.004] [PMID: 20547192]
[5]
Gates, A.T.; Fakayode, S.O.; Lowry, M.; Ganea, G.M.; Murugeshu, A.; Robinson, J.W.; Strongin, R.M.; Warner, I.M. Gold nanoparticle sensor for homocysteine thiolactone-induced protein modification. Langmuir, 2008, 24(8), 4107-4113.
[http://dx.doi.org/10.1021/la7033142] [PMID: 18324853]
[6]
Haba, Y.; Kojima, C.; Harada, A.; Ura, T.; Horinaka, H.; Kono, K. Preparation of poly(ethylene glycol)-modified poly(amido amine) dendrimers encapsulating gold nanoparticles and their heat generating ability. Langmuir, 2007, 23(10), 5243-5246.
[http://dx.doi.org/10.1021/la0700826] [PMID: 17419657]
[7]
Chen, C.; Ke, J.; Zhou, X.E.; Yi, W.; Brunzelle, J.S.; Li, J.; Yong, E.L.; Xu, H.E.; Melcher, K. Structural basis for molecular recognition of folic acid by folate receptors. Nature, 2013, 500(7463), 486-489.
[http://dx.doi.org/10.1038/nature12327] [PMID: 23851396]
[8]
Li, Y.; He, H.; Lu, W.; Jia, X. A poly(amidoamine) dendrimer based drug carrier for delivering DOX to gliomas cells. RSC Advances, 2017, 7, 15475-15481.
[http://dx.doi.org/10.1039/C7RA00713B]
[9]
Wang, B.; Sun, Y.; Davis, T.P.; Ke, P.C.; Wu, Y.; Ding, F. Understanding effects of PAMAM dendrimer size and surface chemistry on serum protein binding with discrete molecular dynamics simulations. ACS Sustain. Chem. Eng., 2018, 6(9), 11704-11715.
[http://dx.doi.org/10.1021/acssuschemeng.8b01959] [PMID: 30881771]
[10]
Lu, Y.; Low, P.S. Folate-mediated delivery of macromolecular anticancer therapeutic agents. Adv. Drug Deliv. Rev., 2012, 64, 342-352.
[http://dx.doi.org/10.1016/j.addr.2012.09.020] [PMID: 12204598]
[11]
Biswal, B.K.; Kavitha, M.; Verma, R.S.; Prasad, E. Tumor cell imaging using the intrinsic emission from PAMAM dendrimer: A case study with HeLa cells. Cytotechnology, 2009, 61(1-2), 17-24.
[http://dx.doi.org/10.1007/s10616-009-9237-5] [PMID: 19908158]
[12]
Jevprasesphant, R.; Penny, J.; Jalal, R.; Attwood, D.; McKeown, N.B.; D’Emanuele, A. The influence of surface modification on the cytotoxicity of PAMAM dendrimers. Int. J. Pharm., 2003, 252(1-2), 263-266.
[http://dx.doi.org/10.1016/S0378-5173(02)00623-3] [PMID: 12550802]
[13]
Zhao, X.; Li, H.; Lee, R.J. Targeted drug delivery via folate receptors. Expert Opin. Drug Deliv., 2008, 5(3), 309-319.
[http://dx.doi.org/10.1517/17425247.5.3.309] [PMID: 18318652]
[14]
Wang, M.; Hu, H.; Sun, Y.; Qiu, L.; Zhang, J.; Guan, G.; Zhao, X.; Qiao, M.; Cheng, L.; Cheng, L.; Chen, D. A pH-sensitive gene delivery system based on folic acid-PEG-chitosan - PAMAM-plasmid DNA complexes for cancer cell targeting. Biomaterials, 2013, 34(38), 10120-10132.
[http://dx.doi.org/10.1016/j.biomaterials.2013.09.006] [PMID: 24094823]
[15]
Arruebo, M.; Vilaboa, N.; Sáez-Gutierrez, B.; Lambea, J.; Tres, A.; Valladares, M.; González-Fernández, A. Assessment of the evolution of cancer treatment therapies. Cancers (Basel), 2011, 3(3), 3279-3330.
[http://dx.doi.org/10.3390/cancers3033279] [PMID: 24212956]
[16]
Chanda, N.; Kan, P.; Watkinson, L.D.; Shukla, R.; Zambre, A.; Carmack, T.L.; Engelbrecht, H.; Lever, J.R.; Katti, K.; Fent, G.M.; Casteel, S.W.; Smith, C.J.; Miller, W.H.; Jurisson, S.; Boote, E.; Robertson, J.D.; Cutler, C.; Dobrovolskaia, M.; Kannan, R.; Katti, K.V. Radioactive gold nanoparticles in cancer therapy: therapeutic efficacy studies of GA-198AuNP nanoconstruct in prostate tumor bearing mice. Nanomedicine (Lond.), 2010, 6(2), 201-209.
[http://dx.doi.org/10.1016/j.nano.2009.11.001] [PMID: 19914401]
[17]
Cutler, C.S.; Chanda, N.; Shukla, R.; Sisay, N.; Cantorias, M.; Zambre, A.; McLaughlin, M.; Kelsey, J.; Upenandran, A.; Robertson, D.; Deutscher, S.; Kannan, R.; Katti, K. Nanoparticles and phage display selected peptides for imaging and therapy of cancer. Recent Results Cancer Res., 2013, 194, 133-147.
[http://dx.doi.org/10.1007/978-3-642-27994-2_8] [PMID: 22918758]
[18]
Flocks, R.H.; Kerr, H.D.; Elkins, H.B.; Culp, D.A. The treatment of carcinoma of the prostate by interstitial radiation with radioactive gold (Au198); A follow-up report. J. Urol., 1954, 71(5), 628-633.
[http://dx.doi.org/10.1016/S0022-5347(17)67835-2] [PMID: 13152893]
[19]
Kojima, C.; Kono, K.; Maruyama, K.; Takagishi, T. Synthesis of polyamidoamine dendrimers having poly(ethylene glycol) grafts and their ability to encapsulate anticancer drugs. Bioconjug. Chem., 2000, 11(6), 910-917.
[http://dx.doi.org/10.1021/bc0000583] [PMID: 11087341]
[20]
Khan, M.K.; Minc, L.D.; Nigavekar, S.S.; Kariapper, M.S.; Nair, B.M.; Schipper, M.; Cook, A.C.; Lesniak, W.G.; Balogh, L.P. Fabrication of 198Au0 radioactive composite nanodevices and their use for nanobrachytherapy. Nanomedicine (Lond.), 2008, 4(1), 57-69.
[http://dx.doi.org/10.1016/j.nano.2007.11.005] [PMID: 18249156]
[21]
Singh, P.; Pandit, S.; Mokkapati, V.R.S.S.; Garg, A.; Ravikumar, V.; Mijakovic, I. Gold nanoparticles in diagnostics and therapeutics for human cancer. Int. J. Mol. Sci., 2018, 19(7), 1979-1995.
[http://dx.doi.org/10.3390/ijms19071979] [PMID: 29986450]
[22]
Bobo, D.; Robinson, K.J.; Islam, J.; Thurecht, K.J.; Corrie, S.R. Nanoparticle-based medicines: A review of FDA-approved materials and clinical trials to date. Pharm. Res., 2016, 33(10), 2373-2387.
[http://dx.doi.org/10.1007/s11095-016-1958-5] [PMID: 27299311]
[23]
Zhang, M.; Zhu, J.; Zheng, Y.; Guo, R.; Wang, S.; Mignani, S.; Caminade, A.M.; Majoral, J.P.; Shi, X. Doxorubicin-conjugated PAMAM dendrimers for pH-responsive drug release and folic acid targeted cancer therapy. Pharmaceutics, 2018, 10(3), 162-174.
[http://dx.doi.org/10.3390/pharmaceutics10030162] [PMID: 30235881]
[24]
Yingchoncharoen, P.; Kalinowski, D.S.; Richardson, D.R. Lipid based drug delivery systems in cancer therapy: what is available and what is yet to come. Pharmacol. Rev., 2016, 68(3), 701-787.
[http://dx.doi.org/10.1124/pr.115.012070] [PMID: 27363439]
[25]
Beik, J.; Jafariyan, M.; Montazerabadi, A.; Ghadimi-Daresajini, A.; Tarighi, P.; Mahmoudabadi, A.; Ghaznavi, H.; Shakeri-Zadeh, A. The benefits of folic acid-modified gold nanoparticles in CT-based molecular imaging: Radiation dose reduction and image contrast enhancement. Artif. Cells Nanomed. Biotechnol., 2018, 46(8), 1993-2001.
[PMID: 29233015]
[26]
Krystofiak, E.S.; Matson, V.Z.; Steeber, D.A.; Oliver, J.A. Elimination of tumor cells using folate receptor targeting by antibody conjugated, gold-coated magnetite nanoparticles in a murine breast cancer model. J. Nanomater., 2012, 2012,Article ID 431012.
[27]
Garay, L.B.; Sanchez, S.C.M.; Ortega, F.M. Use in vitro of gold nanoparticles functionalized with folic acid as a photothermal agent on treatment of HeLa cells. J. Mex. Chem. Soc., 2018, 62, 1-10.
[28]
Zhu, D.; Wu, S.; Hu, C.; Chen, Z.; Wang, H.; Fan, F.; Qin, Y.; Wang, C.; Sun, H.; Leng, X.; Kong, D.; Zhang, L. Folate-targeted polymersomes loaded with both paclitaxel and doxorubicin for the combination chemotherapy of hepatocellular carcinoma. Acta Biomater., 2017, 58, 399-412.
[http://dx.doi.org/10.1016/j.actbio.2017.06.017] [PMID: 28627436]
[29]
Kukowska-Latallo, J.F.; Candido, K.A.; Cao, Z.; Nigavekar, S.S.; Majoros, I.J.; Thomas, T.P.; Balogh, L.P.; Khan, M.K.; Baker, J.R., Jr. Nanoparticle targeting of anticancer drug improves therapeutic response in animal model of human epithelial cancer. Cancer Res., 2005, 65(12), 5317-5324.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-3921] [PMID: 15958579]
[30]
Kelemen, L.E. The role of folate receptor alpha in cancer development, progression and treatment: Cause, consequence or innocent bystander? Int. J. Cancer, 2006, 119(2), 243-250.
[http://dx.doi.org/10.1002/ijc.21712] [PMID: 16453285]
[31]
Li, J.; Yao, S.; Wang, K.; Lu, Z.; Su, X.; Li, L.; Yuan, C.; Feng, J.; Yan, S.; Kong, B.; Song, K. Hypocrellin B-loaded, folate conjugated polymeric micelle for intraperitoneal targeting of ovarian cancer in vitro and in vivo. Cancer Sci., 2018, 109(6), 1958-1969.
[http://dx.doi.org/10.1111/cas.13605] [PMID: 29617063]
[32]
Sega, E.I.; Low, P.S. Tumor detection using folate receptor targeted imaging agents. Cancer Metastasis Rev., 2008, 27(4), 655-664.
[http://dx.doi.org/10.1007/s10555-008-9155-6] [PMID: 18523731]
[33]
Shen, J.; Hu, Y.; Putt, K.S.; Singhal, S.; Han, H.; Visscher, D.W.; Murphy, L.M.; Low, P.S. Assessment of folate receptor alpha and beta expression in selection of lung and pancreatic cancer patients for receptor targeted therapies. Oncotarget, 2017, 9(4), 4485-4495.
[PMID: 29435118]
[34]
Nikzad, S.; Hashemi, B.; Hasan, Z.S.; Mozdarani, H.; Baradaran- Ghahfarokhi, M.; Amini, P. The application of the linear quadratic model to compensate the effects of prolonged fraction delivery time on a Balb/C breast adenocarcinoma tumor: An in vivo study. Int. J. Radiat. Biol., 2016, 92(2), 80-86.
[http://dx.doi.org/10.3109/09553002.2016.1117677] [PMID: 26630280]
[35]
Pulaski, B.A.; Terman, D.S.; Khan, S.; Muller, E.; Ostrand- Rosenberg, S. Cooperativity of Staphylococcal aureus enterotoxin B superantigen, major histocompatibility complex class II, and CD80 for immunotherapy of advanced spontaneous metastases in a clinically relevant postoperative mouse breast cancer model. Cancer Res., 2000, 60(10), 2710-2715.
[PMID: 10825145]
[36]
Tao, K.; Fang, M.; Alroy, J.; Sahagian, G.G. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer, 2008, 8, 228-247.
[http://dx.doi.org/10.1186/1471-2407-8-228] [PMID: 18691423]
[37]
Geersing, A.; de Vries, R.H.; Jansen, G.; Rots, M.G.; Roelfes, G. Folic acid conjugates of a bleomycin mimic for selective targeting of folate receptor positive cancer cells. Bioorg. Med. Chem. Lett., 2019, 29(15), 1922-1927.
[http://dx.doi.org/10.1016/j.bmcl.2019.05.047] [PMID: 31155430]
[38]
Sun, C.; Veiseh, O.; Kohler, N.; Gunn, J.; Lee, D.; Sze, R.; Hallahan, A.; Zhang, M. Intracellular uptake of folate receptor targeted superparamagnetic nanoparticles for enhanced tumor detection by MRI. TechConnect Briefs, 2005, 1, 74-77.
[39]
Narmani, A.; Yavari, K.; Mohammadnejad, J. Imaging, biodistribution and in vitro study of smart 99mTc-PAMAM G4 dendrimer as novel nano-complex. Colloids Surf. B Biointerfaces, 2017, 159, 232-240.
[http://dx.doi.org/10.1016/j.colsurfb.2017.07.089] [PMID: 28800462]
[40]
Jhaveri, M.S.; Rait, A.S.; Chung, K.N.; Trepel, J.B.; Chang, E.H. Antisense oligonucleotides targeted to the human A folate receptor inhibit breast cancer cell growth and sensitize the cells to doxorubicin treatment. Mol. Cancer Ther., 2004, 3(12), 1505-1512.
[PMID: 15634643]
[41]
Yu, Y.; Wang, J.; Kaul, S.C.; Wadhwa, R.; Miyako, E. Folic acid receptor-mediated targeting enhances the cytotoxicity, efficacy, and selectivity of Withania somnifera leaf extract: In vitro and in vivo evidence. Front. Oncol., 2019, 9, 602.
[http://dx.doi.org/10.3389/fonc.2019.00602] [PMID: 31334122]
[42]
Deng, J.; Yao, M.; Gao, C. Cytotoxicity of gold nanoparticles with different structures and surface-anchored chiral polymers. Acta Biomater., 2017, 53, 610-618.
[http://dx.doi.org/10.1016/j.actbio.2017.01.082] [PMID: 28213095]
[43]
Sunoqrot, S.; Liu, Y.; Kim, D.H.; Hong, S. In vitro evaluation of dendrimer-polymer hybrid nanoparticles on their controlled cellular targeting kinetics. Mol. Pharm., 2013, 10(6), 2157-2166.
[http://dx.doi.org/10.1021/mp300560n] [PMID: 23234605]
[44]
Wang, H.; Zheng, L.; Peng, C.; Shen, M.; Shi, X.; Zhang, G. Folic acid-modified dendrimer-entrapped gold nanoparticles as nanoprobes for targeted CT imaging of human lung adencarcinoma. Biomaterials, 2013, 34(2), 470-480.
[http://dx.doi.org/10.1016/j.biomaterials.2012.09.054] [PMID: 23088841]
[45]
Nikzad, S.; Hashemi, B. MTT assay instead of the clonogenic assay in measuring the response of cells to ionizing radiation. J. Radiobiol., 2014, 1, 3-8.
[46]
Alizadeh-Navaei, R.; Rafiei, A.; Abedian-Kenari, S.; Asgarian- Omran, H.; Valadan, R.; Hedayatizadeh-Omran, A. Effect of first line gastric cancer chemotherapy regime on the AGS cell line - MTT assay results. Asian Pac. J. Cancer Prev., 2016, 17(1), 131-133.
[http://dx.doi.org/10.7314/APJCP.2016.17.1.131] [PMID: 26838197]
[47]
Shameli, K.; Ahmad, M.B.; Jazayeri, S.D.; Sedaghat, S.; Shabanzadeh, P.; Jahangirian, H.; Mahdavi, M.; Abdollahi, Y. Synthesis and characterization of polyethylene glycol mediated silver nanoparticles by the green method. Int. J. Mol. Sci., 2012, 13(6), 6639-6650.
[http://dx.doi.org/10.3390/ijms13066639] [PMID: 22837654]
[48]
Saxena, G. Synthesis and Characterization of Doxorubicin Carrying Cetuximab-pamam Dendrimer Bioconjugates., Master of Science Thesis, Virginia Commonwealth University. 2012.
[49]
Patil, Y.B.; Toti, U.S.; Khdair, A.; Ma, L.; Panyam, J. Single-step surface functionalization of polymeric nanoparticles for targeted drug delivery. Biomaterials, 2009, 30(5), 859-866.
[http://dx.doi.org/10.1016/j.biomaterials.2008.09.056] [PMID: 19019427]
[50]
Marchesano, V.; Hernandez, Y.; Salvenmoser, W.; Ambrosone, A.; Tino, A.; Hobmayer, B.; de la Fuente, J.M.; Tortiglione, C. Imaging inward and outward trafficking of gold nanoparticles in whole animals. ACS Nano, 2013, 7(3), 2431-2442.
[http://dx.doi.org/10.1021/nn305747e] [PMID: 23448235]
[51]
Bartczak, D.; Nitti, S.; Millar, T.M.; Kanaras, A.G. Exocytosis of peptide functionalized gold nanoparticles in endothelial cells. Nanoscale, 2012, 4(15), 4470-4472.
[http://dx.doi.org/10.1039/c2nr31064c] [PMID: 22743818]
[52]
Grohn, F.; Bauer, B.J.; Akpalu, Y.A.; Jackson, C.L.; Amis, E.J. Dendrimer templates for the formation of gold nanoclusters. Macromolecules, 2000, 33, 6042-6050.
[http://dx.doi.org/10.1021/ma000149v]
[53]
Hedden, R.C.; Bauer, B.J.; Smith, A.P.; Grohn, F.; Amis, E.J. Templating of inorganic nanoparticles by PAMAM/PEG dendrimer- star polymers. Polymer (Guildf.), 2002, 43, 5473-5481.
[http://dx.doi.org/10.1016/S0032-3861(02)00428-7]
[54]
Majoros, I.J.; Thomas, T.P.; Mehta, C.B.; Baker, J.R., Jr. Poly(amidoamine) dendrimer-based multifunctional engineered nanodevice for cancer therapy. J. Med. Chem., 2005, 48(19), 5892-5899.
[http://dx.doi.org/10.1021/jm0401863] [PMID: 16161993]
[55]
Eitenmiller, R.R.; Ye, L.; Landen, W. Vitamin Analysis for the Health and Food Sciences, 2nd ed; CRC press, Taylor & Francis: Boca Raton, 2016, p. 454.
[http://dx.doi.org/10.1201/9781420009750]
[56]
Off, M.K.; Steindal, A.E.; Porojnicu, A.C.; Juzeniene, A.; Vorobey, A.; Johnsson, A.; Moan, J. Ultraviolet photodegradation of folic acid. J. Photochem. Photobiol. B, 2005, 80(1), 47-55.
[http://dx.doi.org/10.1016/j.jphotobiol.2005.03.001] [PMID: 15963436]
[57]
Chanphai, P.; Tajmir-Riahi, H.A. Characterization of folic acid- PAMAM conjugates: Drug loading efficacy and dendrimer morphology. J. Biomol. Struct. Dyn., 2018, 36(7), 1918-1924.
[http://dx.doi.org/10.1080/07391102.2017.1341339] [PMID: 28605947]
[58]
Ghosh, S.K.; Pal, T. Interparticle coupling effect on the surface plasmon resonance of gold nanoparticles: From theory to applications. Chem. Rev., 2007, 107(11), 4797-4862.
[http://dx.doi.org/10.1021/cr0680282] [PMID: 17999554]
[59]
Prisner, L.; Bohn, N.; Hahn, U.; Mews, A. Size dependent targeted delivery of gold nanoparticles modified with the IL-6R-specific aptamer AIR-3A to IL-6R-carrying cells. Nanoscale, 2017, 9(38), 14486-14498.
[http://dx.doi.org/10.1039/C7NR02973J] [PMID: 28929152]
[60]
Neshatian, M.; Chung, S.; Yohan, D.; Yang, C.; Chithrania, D.B. Determining the size dependence of colloidal gold nanoparticle uptake in a tumor-like interface (Hypoxic). Colloid. Interface Sci., 2014, 1, 57-61.
[61]
Oh, E.; Delehanty, J.B.; Sapsford, K.E.; Susumu, K.; Goswami, R.; Blanco-Canosa, J.B.; Dawson, P.E.; Granek, J.; Shoff, M.; Zhang, Q.; Goering, P.L.; Huston, A.; Medintz, I.L. Cellular uptake and fate of PEGylated gold nanoparticles is dependent on both cell-penetration peptides and particle size. ACS Nano, 2011, 5(8), 6434-6448.
[http://dx.doi.org/10.1021/nn201624c] [PMID: 21774456]
[62]
Huang, K.; Ma, H.; Liu, J.; Huo, S.; Kumar, A.; Wei, T.; Zhang, X.; Jin, S.; Gan, Y.; Wang, P.C.; He, S.; Zhang, X.; Liang, X.J. Size-dependent localization and penetration of ultrasmall gold nanoparticles in cancer cells, multicellular spheroids, and tumors in vivo. ACS Nano, 2012, 6(5), 4483-4493.
[http://dx.doi.org/10.1021/nn301282m] [PMID: 22540892]
[63]
Chandrasekar, D.; Sistla, R.; Ahmad, F.J.; Khar, R.K.; Diwan, P.V. The development of folate-PAMAM dendrimer conjugates for targeted delivery of anti-arthritic drugs and their pharmacokinetics and biodistribution in arthritic rats. Biomaterials, 2007, 28(3), 504-512.
[http://dx.doi.org/10.1016/j.biomaterials.2006.07.046] [PMID: 16996126]
[64]
Stella, B.; Arpicco, S.; Peracchia, M.T.; Desmaele, D.; Hoebeke, J.; Renoir, M.; Angelo, J.D.; Cattel, L.; Couvreur, P. Design of folic acid‐conjugated nanoparticles for drug targeting. J. Pharm. Sci., 2000, 89, 1452-1464.
[65]
Thanh, L.D. Streaming potential and zeta potential measurements in porous rocks. GEP, 2018, 6, 89-100.
[66]
Sun, J.; Jiang, L.; Lin, Y.; Gerhard, E.M.; Jiang, X.; Li, L.; Yang, J.; Gu, Z. Enhanced anticancer efficacy of paclitaxel through multistage tumor-targeting liposomes modified with RGD and KLA peptides. Int. J. Nanomed., 2017, 12, 1517-1537.
[http://dx.doi.org/10.2147/IJN.S122859] [PMID: 28280323]
[67]
Sadeghi, M.; Jabal-Ameli, H.; Ahmadi, S.J.; Sadjadi, S.S.; Bakht, M.K. Production of cationic 198Au3+ and nonionic 198Au0 for radionuclide therapy applications via the nat Au (n, γ) 198Au reaction. J. Radioanal. Nucl. Chem., 2012, 293, 45-49.
[http://dx.doi.org/10.1007/s10967-012-1772-4]
[68]
Goel, S.; Chen, F.; Ehlerding, E.B.; Cai, W. Intrinsically radiolabeled nanoparticles: An emerging paradigm. Small, 2014, 10(19), 3825-3830.
[http://dx.doi.org/10.1002/smll.201401048] [PMID: 24978934]
[69]
Green, J.M.; Donohoe, M.E.; Foster, M.E.; Glajch, J.L. Thin layer chromatographic procedures for the characterization of technetlum•99m BLCISATE. J. Nucl. Med. Technol., 1994, 22, 21-26.
[70]
Bhattacharya, R.; Patra, C.R.; Earl, A.; Wang, S.; Katarya, A.; Beng, L.L.; Kizhakkedathu, J.N.; Yaszemski, M.J.; Greipp, P.R.; Mukhopadhyay, D.; Mukherjee, P. Attaching folic acid on gold nanoparticles using noncovalent interaction via different polyethylene glycol backbones and targeting of cancer cells. Nanomed. Nanotechnology, 2007, 3, 224-238.
[71]
Palmerston Mendes, L.; Pan, J.; Torchilin, V.P. Dendrimers as nanocarriers for nucleic acid and drug delivery in cancer therapy. Molecules, 2017, 22(9), 1401-1422.
[http://dx.doi.org/10.3390/molecules22091401] [PMID: 28832535]
[72]
Huang, M.; Yang, C.S.; Xin, Y.; Jiang, G. Epidermal growth factor receptor-targeted poly(amidoamine)-based dendrimer complexed oncolytic adenovirus: Is it safe totally? J. Thorac. Dis., 2017, 9(1), E89-E90.
[http://dx.doi.org/10.21037/jtd.2017.01.41] [PMID: 28203445]
[73]
Wang, W.; Xiong, W.; Zhu, Y.; Xu, H.; Yang, X. Protective effect of PEGylation against poly(amidoamine) dendrimer-induced hemolysis of human red blood cells. J. Biomed. Mater. Res. B Appl. Biomater., 2010, 93(1), 59-64.
[http://dx.doi.org/10.1002/jbm.b.31558] [PMID: 20186802]
[74]
Luo, D.; Haverstick, K.; Belcheva, N.; Han, E.; Saltzman, W.M. Poly(ethylene glycol)-conjugated PAMAM dendrimer for biocompatible, high-efficiency DNA delivery. Macromolecules, 2002, 359, 3456-3462.
[http://dx.doi.org/10.1021/ma0106346]
[75]
Janitabar-Darzi, S.; Rezaei, R.; Yavari, K. In vitro cytotoxicity effects of 197Au/PAMAMG4 and 198Au/PAMAMG4 nanocomposites against MCF7 and 4T1 breast cancer cell lines. Adv. Pharm. Bull., 2017, 7(1), 87-95.
[http://dx.doi.org/10.15171/apb.2017.011] [PMID: 28507941]


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VOLUME: 20
ISSUE: 10
Year: 2020
Page: [1250 - 1265]
Pages: 16
DOI: 10.2174/1871520620666200220113452
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