Carnosic Acid, Tangeretin, and Ginkgolide-B Anti-neoplastic Cytotoxicity in Dual Combination with Dexamethasone-[anti-EGFR] in Pulmonary Adenocarcinoma (A549)

Author(s): Cody P. Coyne* , Lakshmi Narayanan .

Journal Name: Anti-Cancer Agents in Medicinal Chemistry

Volume 19 , Issue 6 , 2019

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Graphical Abstract:


Abstract:

Background: Traditional chemotherapeutics of low-molecular weight diffuse passively across intact membrane structures of normal healthy cells found in tissues and organ systems in a non-specific unrestricted manner which largely accounts for the induction of most sequelae which restrict dosage, administration frequency, and duration of therapeutic intervention. Molecular strategies that offer enhanced levels of potency, greater efficacy and broader margins-of-safety include the discovery of alternative candidate therapeutics and development of methodologies capable of mediating properties of selective “targeted” delivery.

Materials and Methods: The covalent immunopharmaceutical, dexamethasone-(C21-phosphoramidate)-[anti- EGFR] was synthesized utilizing organic chemistry reactions that comprised a multi-stage synthesis regimen. Multiple forms of analysis were implemented to vadliate the successful synthesis (UV spectrophotometric absorbance), purity and molar-incorporation-index (UV spectrophotometric absorbance, chemical-based protein determination), absence of fragmentation/polymerization (SDS-PAGE/chemiluminescent autoradiography), retained selective binding-avidity of IgG-immunoglobulin (cell-ELISA); and selectively “targeted” antineoplastic cytotoxicity (biochemistry-based cell vitality/viability assay).

Results: The botanicals carnosic acid, ginkgolide-B and tangeretin, each individually exerted maximum antineoplastic cytotoxicity levels of 58.1%, 5.3%, and 41.1% respectively against pulmonary adenocarcinoma (A549) populations. Dexamethasone-(C21-phosphoramidate)-[anti-EGFR] formulated at corticosteroid/ glucocorticoid equivalent concentrations produced anti-neoplastic cytotoxicity at levels of 7.7% (10-9 M), 26.9% (10-8 M), 64.9% (10-7 M), 69.9% (10-6 M) and 73.0% (10-5 M). Ccarnosic acid, ginkgolide-B and tangeretin in simultaneous dual-combination with dexamethasone-(C21-phosphoramidate)-[anti-EGFR] exerted maximum anti-neoplastic cytotoxicity levels of 70.5%, 58.6%, and 69.7% respectively.

Discussion: Carnosic acid, ginkgolide-B and tangeretin botanicals exerted anti-neoplastic cytotoxicity against pulmonary adenocarcinoma (A549) which additively contributed to the anti-neoplastic cytotoxic potency of the covalent immunopharmaceutical, dexamethasone-(C21-phosphoramidate)-[anti-EGFR]. Carnosic acid and tangeretin were most potent in this regard both individually and in dual-combination with dexamethasone-(C21- phosphoramidate)-[anti-EGFR]. Advantages and attributes of carnosic acid and tangeretin as potential monotherapeutics are a wider margin-of-safety of conventional chemotherapeutics which would readily complement the selective “targeted” delivery properties of dexamethasone-(C21-phosphoramidate)-[anti-EGFR] and possibly other covalent immunopharmaceuticals in addition to providing opportunities for the discovery of combination therapies that provide heightened levels of anti-neoplastic efficacy.

Keywords: Carnosic acid, ginkgolide-B, tangeretin, covalent immunopharmaceuticals, dexamethasone, anti-EGFR, selective “targeted” delivery, anti-neoplastic cytotoxic potency.

[1]
Kirstein, M.N.; Hassan, I.; Guire, D.E.; Weller, D.R.; Dagit, J.W.; Fisher, J.E.; Remmel, R.P. High-performance liquid chromatographic method for the determination of gemcitabine and 2′,2′-difluorodeoxyuridine in plasma and tissue culture media. J. Chromatogr. B Biomed. Sci. Appl., 2006, 835(1-2), 136-142.
[2]
Honeywell, R.; Laan, A.C.; van Groeningen, C.J.; Strocchi, E.; Ruiter, R.; Giaccone, G.; Peters, G.J. The determination of gemcitabine and 2′-deoxycytidine in human plasma and tissue by APCI tandem mass spectrometry. J. Chrom. B, 2007, 847, 142-152.
[3]
Perello, L.; Demirdjian, S.; Dory, A.; Bourget, P. Application of high-performance, thin-layer chromatography to quality control of antimetabolite analogue infusion bags. J. AOAC Int., 2001, 84, 1296-1300.
[4]
Wang, L.Z.; Yong, W.P.; Soo, R.A.; Lee, S.C.; Soong, R.; Lee, H.S.; Goh, B.C. Rapid determination of gemcitabine and its metabolite in human plasma by LC-MSMS through micro protein precipitation with minimum matrix effect. J. Pharm. Sci. Res., 2009, 1, 23-32.
[5]
Limmer, S.; Hahn, J.; Schmidt, R.; Wachholz, K.; Zengerle, A.; Lechner, K.; Eibl, H.; Issels, R.D.; Hossann, M.; Lindner, L.H. Gemcitabine treatment of tat soft tissue sarcoma with phosphatidyldiglycerol-based thermosensitive liposomes. Pharm. Res., 2014, 31, 2276-2286.
[6]
Singh, R.; Shakya, A.K.; Naik, R.; Shalan, N. Stability-indicating HPLC determination of gemcitabine in pharmaceutical formulations. Int. J. Anal. Chem., 2015, 2015, 1-12.
[7]
Golf, S.W.; Graef, V.; Schiller, J.T.; Hischer, H.; Funk, W. Thin-layer chromatography--the forgotten alternative for the quantitative determination of steroids. Biomed. Chrom., 1987, 2, 189-192.
[8]
Paw, B.; Misztal, G.; Dzwonnik, K. Thin-layer chromatographic analysis of fludarabine and formycin A in human plasma. Acta Pol. Pharm., 2000, 57, 341-343.
[9]
Patel, H. A validated stability-indicating HPTLC method for the estimation of gemcitabine HCl in its dosage form. J. Planar Chromatogr. Mod. TLC, 2012, 25, 77-80.
[10]
Chang, C.C.; Hsieh, T.L.; Tiong, T.Y.; Hsiao, C.H.; Ji, A.T.; Hsu, W.T.; Lee, O.K.; Ho, J.H. Regulation of metastatic ability and drug resistance in pulmonary adenocarcinoma by matrix rigidity via activating c-Met and EGFR. Biomaterials, 2015, 60, 141-150.
[11]
Shicang, Y.; Guijun, H.; Guisheng, Q.; Yuying, L.; Guoming, W.; Ruiling, G. Efficacy of chemotherapeutic agents under hypoxic conditions in pulmonary adenocarcinoma multidrug resistant cell line. J. Chemother., 2007, 19, 203-211.
[12]
Salomon, D.S.; Brandt, R.; Ciardiello, F. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit. Rev. Oncol. Hematol., 1995, 19, 183-232.
[13]
Kim, Y.J.; Kim, J.S.; Seo, Y.R.; Park, J.H.; Choi, M.S.; Sung, M.K. Carnosic acid suppresses colon tumor formation in association with anti-adipogenic activity. Mol. Nutr. Food Res., 2014, 58, 2274-2285.
[14]
Min, K.J.; Jung, K.J.; Kwon, T.K. Carnosic acid induces apoptosis through reactive oxygen species-mediated endoplasmic reticulum stress induction in human renal carcinoma caki cells. J. Cancer Prev., 2014, 19, 170-178.
[15]
Xiang, Q.; Ma, Y.; Dong, J.; Shen, R. Carnosic acid induces apoptosis associated with mitochondrial dysfunction and Akt inactivation in HepG2 cells. Int. J. Food Sci. Nutr., 2014, 66(1), 1-9.
[16]
Gao, Q.; Liu, H.; Yao, Y.; Geng, L.; Zhang, X.; Jiang, L.; Shi, B.; Yang, F. Carnosic acid induces autophagic cell death through inhibition of the Akt/mTOR pathway in human hepatoma cells. J. Appl. Toxicol., 2014, 35(5), 485-492.
[17]
Park, S.Y.; Song, H.; Sung, M.K.; Kang, Y.H.; Lee, K.W.; Park, J.H. Carnosic acid inhibits the epithelial-mesenchymal transition in B16F10 melanoma cells: A possible mechanism for the inhibition of cell migration. Int. J. Mol. Sci., 2014, 15, 12698-12713.
[18]
Shin, H.B.; Choi, M.S.; Ryu, B.; Lee, N.R.; Kim, H.I.; Choi, H.E.; Chang, J.; Lee, K.T.; Jang, D.S.; Inn, K.S. Antiviral activity of carnosic acid against respiratory syncytial virus. Virol. J., 2013, 10, 303.
[19]
Yesil-Celiktas, O.; Sevimli, C.; Bedir, E.; Vardar-Sukan, F. Inhibitory effects of rosemary extracts, carnosic acid and rosmarinic acid on the growth of various human cancer cell lines. Plant Foods Hum. Nutr., 2010, 65, 158-163.
[20]
Visanji, J.M.; Thompson, D.G.; Padfield, P.J. Induction of G2/M phase cell cycle arrest by carnosol and carnosic acid is associated with alteration of cyclin A and cyclin B1 levels. Cancer Lett., 2008, 237, 130-136.
[21]
Jiang, W.; Qiu, W.; Wang, Y.; Cong, Q.; Edwards, D.; Ye, B.; Xu, C. Ginkgo may prevent genetic-associated ovarian cancer risk: multiple biomarkers and anticancer pathways induced by ginkgolide B in BRCA1-mutant ovarian epithelial cells. Eur. J. Cancer Prev., 2011, 20, 508-517.
[22]
Arivazhagan, L.; Sorimuthu, P.S. Tangeretin, a citrus pentamethoxyflavone, exerts cytostatic effect via p53/p21 up-regulation and suppresses metastasis in 7,12-dimethylbenz(á)anthracene-induced rat mammary carcinoma. J. Nutr. Biochem., 2014, 25, 1140-1153.
[23]
Periyasamy, K.; Baskaran, K.; Ilakkia, A.; Vanitha, K.; Selvaraj, S.; Sakthisekaran, D. Antitumor efficacy of tangeretin by targeting the oxidative stress mediated on 7,12-dimethylbenz(a) anthracene-induced proliferative breast cancer in Sprague-Dawley rats. Cancer Chemother. Pharmacol., 2014, 75(2), 263-272.
[24]
Wang, J.; Duan, Y.; Zhi, D.; Li, G.; Wang, L.; Zhang, H.; Gu, L.; Ruan, H.; Zhang, K.; Liu, Q.; Li, S.; Ho, C.T.; Zhao, H. Pro-apoptotic effects of the novel tangeretin derivate 5-acetyl-6,7,8,4′-tetramethylnortangeretin on MCF-7 breast cancer cells. Cell Biochem. Biophys., 2014, 70, 1255-1263.
[25]
Dong, Y.; Cao, A.; Shi, J.; Yin, P.; Wang, L.; Ji, G.; Xie, J.; Wu, D. Tangeretin, a citrus polymethoxyflavonoid, induces apoptosis of human gastric cancer AGS cells through extrinsic and intrinsic signaling pathways. Oncol. Rep., 2014, 31, 1788-1794.
[26]
Lakshmi, A.; Subramanian, S. Chemotherapeutic effect of tangeretin, a polymethoxylated flavone studied in 7, 12 dimethylbenz(a)anthracene induced mammary carcinoma in experimental rats. Biochimie, 2014, 99, 96-109.
[27]
Lust, S.; Vanhoecke, B.; Van Gele, M.; Philippé, J.; Bracke, M.; Offner, F. The flavonoid tangeretin activates the unfolded protein response and synergizes with imatinib in the erythroleukemia cell line K562. Mol. Nutr. Food Res., 2010, 54, 823-832.
[28]
Arafa, S.A.; Zhu, Q.; Barakat, B.M.; Wani, G.; Zhao, Q.; El-Mahdy, M.A.; Wani, A.A. Tangeretin sensitizes cisplatin-resistant human ovarian cancer cells through downregulation of phosphoinositide 3-kinase/Akt signaling pathway. Cancer Res., 2009, 69, 8910-8917.
[29]
Morley, K.L.; Ferguson, P.J.; Koropatnick, J. Tangeretin and nobiletin induce G1 cell cycle arrest but not apoptosis in human breast and colon cancer cells. Cancer Lett., 2007, 251, 168-178.
[30]
Chen, K.H.; Weng, M.S.; Lin, J.K. Tangeretin suppresses IL-1beta-induced cyclooxygenase (COX)-2 expression through inhibition of p38 MAPK, JNK, and AKT activation in human lung carcinoma cells. Biochem. Pharmacol., 2007, 73, 215-227.
[31]
Rao, J.R.; Mulla, T.S.; Yadav, S.S.; Rajput, M.P.; Bharekar, V.V. Validated HPTLC method for simultaneous estimation of ciprofloxacin hydrochloride and dexamethasone in bulk drug and formulation. Int. J. Chemtech Res., 2012, 4, 1589-1594.
[32]
Pan, M.H.; Chen, W.J.; Lin-Shiau, S.Y.; Ho, C.T.; Lin, J.K. Tangeretin induces cell-cycle G1 arrest through inhibiting cyclin-dependent kinases 2 and 4 activities as well as elevating Cdk inhibitors p21 and p27 in human colorectal carcinoma cells. Carcinogenesis, 2002, 23, 1677-1684.
[33]
Hirano, T.; Abe, K.; Gotoh, M.; Oka, K. Citrus flavone tangeretin inhibits leukaemic HL-60 cell growth partially through induction of apoptosis with less cytotoxicity on normal lymphocytes. Br. J. Cancer, 1995, 72, 1380-1388.
[34]
Depypere, H.T.; Bracke, M.E.; Boterberg, T.; Mareel, M.M.; Nuytinck, M.; Vennekens, K.; Serreyn, R. Inhibition of tamoxifen’s therapeutic benefit by tangeretin in mammary cancer. Eur. J. Cancer, 2000, 36, 73.
[35]
Rao, K.S.; Rani, S.U.; Charyulu, D.K.; Kumar, K.N.; Lee, B.K.; Lee, H.Y.; Kawai, T. A novel route for immobilization of oligonucleotides onto modified silica nanoparticles. Anal. Chim. Acta, 2006, 576, 177-183.
[36]
Coyne, C.P.; Narayanan, L. Fludarabine-(C2-methylhydroxyphosphoramide)-[anti-IGF-1R] synthesis and selectively “targeted” anti-neoplastic cytotoxicity against pulmonary adenocarcinoma (A549). J. Pharm. Drug Deliv. Res., 2015, 4, 129.
[37]
Beloglazova, N.G.; Epanchintsev, A.; Sil’nikov, V.N.; Zenkova, M.A.; Vlasov, V.V. Highly efficient site-directed RNA cleavage by imidazole-containing conjugates of antisense oligonucleotides. Mol. Biol. (Mosk.), 2002, 36, 731-739.
[38]
Hu, Q.; Deng, X.; Yu, X.; Kong, J.; Zhang, X. One-step conjugation of aminoferrocene to phosphate groups as electroactive probes for electrochemical detection of sequence-specific DNA. Biosens. Bioelectron., 2015, 65, 71-77.
[39]
Wang, P.; Giese, R.W. Phosphate-specific fluorescence labeling with BO-IMI: Reaction details. J. Chromatogr. A, 1998, 809, 211-218.
[40]
Wang, P.; Giese, R.W. Phosphate-specific fluorescence labeling of pepsin by BO-IMI. Anal. Biochem., 1995, 230, 329-332.
[41]
Coyne, C.P.; Narayanan, L. Dexamethasone-(C21-phosphoramide)-[anti-EGFR]: Molecular design, synthetic organic chemistry reactions and anti-neoplastic cytotoxic potency against pulmonary adenocarcinoma (A549). J. Drug Des. Develop. Ther., 2016, 10, 2575-2597.
[42]
Watson, E.; Dea, P.; Chan, K.K. Kinetics of phosphoramide mustard hydrolysis in aqueous solution. J. Pharm. Sci., 1985, 74, 1283-1292.
[43]
Surabhi, P. Synthesis and evaluation of phosphoramide mustard prodrugs for site-specific activation. Master Dissertation, Rutgers University, Medicinal Chemistry Graduate Program: New Brunswick, NJ, 2007.
[44]
Coyne, C.P.; Ross, M.; Bailey, J.; Jones, T. Dual potency anti-HER2/neu and anti-EGFR anthracycline-immunoconjugates in chemotherapeutic-resistant mammary carcinoma combined with cyclosporin-A and verapamil P-glycoprotein inhibition. J. Drug Target., 2009, 17, 474-489.
[45]
Coyne, C.P.; Jones, T.; Pharr, T. Synthesis of a covalent gemcitabine-(carbamate)-[anti-HER2/neu] immunochemotherapeutic and cytotoxic anti-neoplastic activity against chemotherapeutic-resistant SKBr-3 mammary carcinoma. Bioorg. Med. Chem., 2011, 19, 67-76.
[46]
Coyne, C.P.; Jones, T.; Sygula, A.; Bailey, J.; Pinchuk, L. Epirubicin-[anti-HER2/neu] synthesized with an epirubicin-(C13-imino)-EMCS analog: Anti-neoplastic activity against chemotherapeutic-resistant SKBr-3 mammary carcinoma in combination with organic selenium. J. Cancer Ther., 2011, 2(1), 22-39.
[47]
Coyne, C.P.; Jones, T.; Bear, R. Synthesis of epirubicin-(C3-amide)-[anti-HER2/neu] utilizing a UV-photoactivated epirubicin. Cancer Biother. Radiopharm., 2012, 27, 41-55.
[48]
Coyne, C.P.; Jones, T.; Bear, R. Synthesis of gemcitabine-(C4-amide)-[anti-HER2/neu] utilizing a UV-photoactivated gemcitabine intermediate: cytotoxic anti-neoplastic activity against chemotherapeutic-resistant mammary adenocarcinoma SKBr-3. J. Cancer Ther., 2012, 3, 689-711.
[49]
Beyer, U.; Rothen-Rutishauser, B.; Unger, C.; Wunderli-Allenspach, H.; Kratz, F. Difference in the intracellular distribution of acid-sensitive doxorubicin-protein conjugates in comparison to free and liposomal-formulated doxorubicin as shown by confocal microscopy. Pharmacol. Res., 2001, 18, 29-38.
[50]
Ulbrich, K.; Etrych, T.; Chytil, P.; Jelinkova, M.; Rihova, B. HPMA copolymers with pH-controlled release of doxorubicin: In vitro cytotoxicity and in vivo antitumor activity. J. Control. Release, 2003, 87, 33-47.
[51]
Di Stefano, G.; Lanza, M.; Kratz, F.; Merina, L.; Fiume, L. A novel method for coupling doxorubicin to lactosaminated human albumin by an acid sensitive hydrazone bond: Synthesis, characterization. and preliminary biological properties of the conjugate. Eur. J. Pharm. Sci., 2004, 23, 393-397.
[52]
Sinkule, J.A.; Rosen, S.T.; Radosevich, J.A. Monoclonal antibody 44-3A6 doxorubicin immunoconjugates: Comparative in vitro anti-tumor efficacy of different conjugation methods. Tumour Biol., 1991, 12(4), 198-206.
[53]
Conesa, M.C.; Ortega, V.; Gascón, Y.M.J.; Baños, A.M.; Jordana, C.M.; Benavente-García, O.; Castillo, J. Treatment of metastatic melanoma B16F10 by the flavonoids tangeretin, rutin, and diosmin. J. Agric. Food Chem., 2005, 53, 6791-6797.
[54]
Einbond, L.S.; Wu, H.A.; Kashiwazaki, R.; He, K.; Roller, M.; Su, T.; Wang, X.; Oldsberry, S. Carnosic acid inhibits the growth of ER-negative human breast cancer cells and synergizes with curcumin. Fitoterapia, 2012, 83, 1160-1168.
[55]
Park, K.M.; Kindu, J.; Chae, I.G.; Kim, D.H.; Yu, M.H.; Kundu, J.K.; Chen, K.S. Carsonol induces apoptosis through generation of ROS and inactivation of STAT3 signaling in human colon cancer HCT116 cells. Int. J. Oncol., 2014, 44(4), 1309-1315.
[56]
Kim, Y.J.; Kim, J.S.; Seo, Y.R.; Park, J.H.; Choi, M.S.; Sung, M.K. Carnosic acid suppresses colon tumor formation in association with anti-adipogenic activity. Mol. Nutr. Food Res., 2014, 58, 2274-2285.
[57]
Chae, I.G.; Yu, M.H. Im, N.K.; Jung, Y.T.; Lee, J.; Chun, K.S.; Lee, I.S. Effect of Rosemarinus officinalis L. on MMP-9, MCP-1 levels, and cell migration in RAW 264.7 and smooth muscle cells. J. Med. Food, 2012, 15, 879-886.
[58]
Zhi, Y.; Pan, J.; Shen, W.; He, P.; Zheng, J.; Zhou, X.; Lu, G.; Chen, Z.; Zhou, Z. Ginkgolide B inhibits human bladder cancer cell migration and invasion through MicroRNA-223-3p. Cell. Physiol. Biochem., 2016, 39, 1787-1794.
[59]
Jiang, W.; Cong, Q.; Wang, Y.; Ye, B.; Xu, C. Ginkgo may sensitize ovarian cancer cells to cisplatin: antiproliferative and apoptosis-inducing effects of ginkgolide B on ovarian cancer cells. Integr. Cancer Ther., 2014, 13, NP10-NP17.
[60]
Aponte, M.; Jiang, W.; Lakkis, M.; Li, M.J.; Edwards, D.; Albitar, L.; Vitonis, A.; Mok, S.C.; Cramer, D.W.; Ye, B. Activation of platelet-activating factor receptor and pleiotropic effects on tyrosine phospho-EGFR/Src/FAK/paxillin in ovarian cancer. Cancer Res., 2008, 68, 5839-5848.
[61]
Ghosh, S.; Dungdung, S.R.; Choudhury, S.T.; Chakraborty, S.; Das, N. Mitochondria protection with ginkgolide B-loaded polymeric nanocapsules prevents diethylnitrosamine-induced hepatocarcinoma in rats. Nanomedicine, 2014, 9, 441-456.
[62]
Ye, B.; Aponte, M.; Dai, Y.; Li, L.; Ho, M.C.; Vitonis, A.; Edwards, D.; Huang, T.N.; Cramer, D.W. Ginkgo biloba and ovarian cancer prevention: Epidemiological and biological evidence. Cancer Lett., 2007, 251, 43-52.
[63]
Sun, L.; He, Z.; Ke, J.; Li, S.; Wu, X.; Lian, L.; He, X.; He, X.; Hu, J.; Zou, Y.; Wu, X.; Lan, P. PAF receptor antagonist Ginkgolide B inhibits tumourigenesis and angiogenesis in colitis-associated cancer. Int. J. Clin. Exp. Pathol., 2015, 8, 432-440.
[64]
Wielckens, K.; Delfs, T.; Muth, A.; Freese, V.; Kleeberg, H.J. Glucocorticoid-induced lymphoma cell death: The good and the evil. J. Steroid Biochem., 1987, 27, 413-419.
[65]
Kanat, O.; Ozet, A.; Ataergin, S.; Arpaci, F.; Kuzhan, O.; Komurcu, S.; Ozturk, B.; Ozturk, M. Modified outpatient dexamethazone, cytarabine and cisplatin regimen may lead to high response rates and low toxicity in lymphoma. Med. Princ. Pract., 2010, 19, 344-347.
[66]
Lerza, R.; Botta, M.; Barsotti, B.; Schenone, E.; Mencoboni, M.; Bogliolo, G.; Pannacciulli, I.; Arboscello, E. Dexamethazone-induced acute tumor lysis syndrome in a T-cell malignant lymphoma. Leuk. Lymphoma, 2002, 43, 1129-1132.
[67]
Watanabe, N.; Takahashi, T.; Sugimoto, N.; Tanaka, Y.; Kurata, M.; Matsushita, A.; Maeda, A.; Nagai, K.; Nasu, K. Excellent response of chemotherapy-resistant B-cell-type chronic lymphocytic leukemia with meningeal involvement to rituximab. Int. J. Clin. Oncol., 2005, 10, 357-361.
[68]
Mao, Y.; Triantafillou, G.; Hertlein, E.; Towns, W.; Stefanovski, M.; Mo, X.; Jarjoura, D.; Phelps, M.; Marcucci, G.; Lee, L.J.; Goldenberg, D.M.; Lee, R.J.; Byrd, J.C.; Muthusamy, N. Milatuzumab-conjugated liposomes as targeted dexamethasone carriers for therapeutic delivery in CD74+ B-cell malignancies. Clin. Cancer Res., 2013, 19, 347-356.
[69]
Belz, K.; Schoeneberger, H.; Wehner, S.; Weigert, A.; Bönig, H.; Klingebiel, T.; Fichtner, I.; Fulda, S. Smac mimetic and glucocorticoids synergize to induce apoptosis in childhood ALL by promoting ripoptosome assembly. Blood, 2014, 124, 240-250.
[70]
Domenech, C.; Suciu, S.; De Moerloose, B.; Mazingue, F.; Plat, G.; Ferster, A.; Uyttebroeck, A.; Sirvent, N.; Lutz, P.; Yakouben, K.; Munzer, M.; Röhrlich, P.; Plantaz, D.; Millot, F.; Philippet, P.; Dastugue, N.; Girard, S.; Cavé, H.; Benoit, Y.; Bertrandfor, Y. Dexamethasone (6 mg/m2/day) and prednisolone (60 mg/m2/day) were equally effective as induction therapy for childhood acute lymphoblastic leukemia in the EORTC CLG 58951 randomized trial. Haematologica, 2014, 99, 1220-1227.
[71]
Wang, L.C.; Wei, W.H.; Zhang, X.W.; Liu, D.; Zeng, K.W.; Tu, P.F. An integrated proteomics and bioinformatics approach reveals the anti-inflammatory mechanism of carnosic acid. Front. Pharmacol., 2018, 9, 370377-370383.
[72]
Tran, T.V.; Park, S.J.; Shin, E.J.; Tran, H.Q.; Jeong, J.H.; Jang, C.G.; Lee, Y.J.; Nah, S.Y.; Nabeshima, T.; Kim, H.C. Blockade of platelet-activating factor receptor attenuates abnormal behaviors induced by phencyclidine in mice through down-regulation of NF-kB. Brain Res. Bull., 2018, 37, 71-78.
[73]
Xu, J.J.; Liu, Z.; Tang, W.; Wang, G.C.; Chung, H.Y.; Liu, Q.Y.; Zhuang, L.; Li, M.M.; Li, Y.L. Tangeretin from citrus reticulate inhibits respiratory syncytial virus replication and associated inflammation in vivo. J. Agric. Food Chem., 2015, 63, 9520-9527.
[74]
Shu, Z.; Yang, B.; Zhao, H.; Xu, B.; Jiao, W.; Wang, Q.; Wang, Z.; Kuang, H. Tangeretin exerts anti-neuroinflammatory effects via NF-êB modulation in lipopolysaccharide-stimulated microglial cells. Int. Immunopharmacol., 2014, 19, 275-282.
[75]
Liu, P.; Dong, J. Protective effects of carnosic acid against mitochondria-mediated injury in H9c2 cardiomyocytes induced by hypoxia/reoxygenation. Exp. Ther. Med., 2017, 14, 5629-5634.
[76]
Gao, J.; Chen, T.; Zhao, D.; Zheng, J.; Liu, Z. Ginkgolide B exerts cardioprotective properties against doxorubicin-induced cardiotoxicity by regulating reactive oxygen species, akt and calcium signaling pathways in vitro and in vivo. PLoS One, 2016, 11, e0168219-e0168235.
[77]
Wang, M.; Meng, D.; Zhang, P.; Wang, X.; Du, G.; Brennan, C.; Li, S.; Ho, C.T.; Zhao, H. Antioxidant protection of nobiletin, 5-demethylnobiletin, tangeretin, and 5-demethyltangeretin from citrus peel in saccharomyces cerevisiae. J. Agric. Food Chem., 2018, 66, 3155-3160.
[78]
Thummuri, D.; Naidu, V.G.M.; Chaudhari, P. Carnosic acid attenuates RANKL-induced oxidative stress and osteoclastogenesis via induction of NRF2 and suppression of NF-kB and MAPK signalling. J. Mol. Med., 2017, 95, 1065-1076.
[79]
Omar, H.A.; Mohamed, W.R.; Arab, H.H.; Arafa, S.A. Tangeretin alleviates cisplatin-induced acute hepatic injury in rats: Targeting MAPKs and apoptosis. PLoS One, 2016, 11, e0151649-e0151655.
[80]
Wu, J.; Zhao, Y.M.; Deng, Z.K. Tangeretin ameliorates renal failure via regulating oxidative stress, NF-kB-TNF-a/iNOS signalling and improves memory and cognitive deficits in 5/6 nephrectomized rats. Inflammopharmacology, 2018, 26, 119-132.
[81]
Zhou, T.; You, W.T.; Ma, Z.C.; Liang, Q.D.; Tan, H.L.; Xiao, C.R.; Tang, X.L.; Zhang, B.L.; Wang, Y.G.; Gao, Y. Ginkgolide B protects human umbilical vein endothelial cells against xenobiotic injuries via PXR activation. Acta Pharmacol. Sin., 2016, 37, 177-186.
[82]
Nabekura, T.; Yamaki, T.; Hiroi, T.; Ueno, K.; Kitagawa, S. Inhibition of anticancer drug efflux transporter P-glycoprotein by rosemary phytochemicals. Pharmacol. Res., 2010, 61, 259-263.
[83]
Plouzek, C.A.; Ciolino, H.P.; Yeh, G.C. Inhibition of P-glycoprotein activity and reversal of multidrug resistance in vitro by rosemary extract. Eur. J. Cancer, 1999, 35, 1541-1545.
[84]
Ishii, K.; Tanaka, S.; Kagami, K.; Henmi, K.; Toyoda, H.
Kaise, T.; Hirano, T. Effects of naturally occurring polymethyoxyflavonoids on cell growth, p-glycoprotein function, cell cycle, and apoptosis of daunorubicin-resistant T lymphoblastoid leukemia cells. Cancer Invest., 2010, 28, 220-229.
[85]
Wesolowska, O.; Wiœniewski, J.; Sroda-Pomianek, K.; Bielawska-Pohl, A.; Paprocka, M.; Duœ, D.; Duarte, N.; Ferreira, M.J.; Michalak, K. Multidrug resistance reversal and apoptosis induction in human colon cancer cells by some flavonoids present in citrus plants. J. Nat. Prod., 2012, 75, 1896-1902.
[86]
Berger, A.S.; Cheng, C.K.; Pearson, P.A.; Ashton, P.; Crooks, P.A.; Cynkowski, T.; Cynkowska, G.; Jaffe, G.J. Intravitreal sustained release corticosteroid-5-fluoruracil conjugate in the treatment of experimental proliferative vitreoretinopathy. Invest. Ophthalmol. Vis. Sci., 1996, 37, 2318-2325.
[87]
Basu, A.; Shrivastav, T.G.; Maitra, S.K. A direct antigen heterologous enzyme immunoassay for measuring progesterone in serum without using displacer. Steroids, 2006, 71, 222-230.
[88]
Hatzidakis, G.; Stefanakis, A.; Krambovitis, E. Comparison of different antibody-conjugate derivatives for the development of a sensitive and specific progesterone assay. J. Reprod. Fertil., 1993, 97, 557-561.
[89]
Khatun, S.; Nara, S.; Tripathi, V.; Rangari, K.; Chaube, S.K.; Kariya, K.P.; Kumar, S.; Shrivastav, T.G. Development of ELISA for measurement of progesterone employing 17-alpha-OH-P-HRP as enzyme label. J. Immunoassay Immunochem., 2009, 30, 186-196.
[90]
Shrivastav, T.G.; Chaube, S.K.; Kariya, K.P.; Prasad, P.K. Influence of different length spacers containing enzyme conjugate on functional parameters of progesterone ELISA. J. Immunoassay Immunochem., 2013, 34, 94-108.
[91]
Kobayashi, N.; Kato, Y.; Oyama, H.; Taga, S.; Niwa, T.; Sun, P.; Ohtoyo, M.; Goto, J. Anti-estradiol-17beta single-chain Fv fragments: Generation, characterization, gene randomization, and optimized phage display. Steroids, 2008, 73, 1485-1499.
[92]
Ogihara, T.; Miyal, K.; Nishi, K.; Ishibashi, K.; Kumahara, Y. Enzyme-labelled immunoassay for plasma cortisol. J. Clin. Endocrinol. Metab., 1977, 44, 91-95.
[93]
Nakao, T.; Tamamura, F.; Tsunoda, N.; Kawata, K. Double antibody enzyme immunoassay of cortisol in bovine plasma. Steroids, 1981, 38, 111-120.
[94]
Nakao, T. Practical procedure for enzyme immunoassay of progesterone in bovine serum. Acta Endocrinol., 1980, 93, 223-227.
[95]
Yamashita, K.; Takahashi, M.; Tsukamoto, S.; Numazawa, M.; Okuyama, M.; Honma, S. Use of novel picolinoyl derivatization for simultaneous quantification of six corticosteroids by liquid chromatography-electrospray ionization tandem mass spectrometry. J. Chromatogr. A, 2007, 1173, 120-128.
[96]
Melgert, B.N.; Olinga, P.; Jack, V.K.; Molema, G.; Meijer, D.K.; Poelstra, K. Dexamethasone coupled to albumin is selectively taken up by rat nonparenchymal liver cells and attenuates LPS-induced activation of hepatic cells. J. Hepatol., 2000, 32, 603-611.
[97]
Erlanger, B.E.; Borek, F.; Beiser, S.M.; Lieberman, S. Steroid-protein conjugates II. Preparation and characterization of conjugates of bovine serum albumin with progesterone, deoxycorticosterone, and estrone. J. Biol. Chem., 1959, 234, 1090-1094.
[98]
De Goeij, A.F.; van Zeeland, J.K.; Beek, C.J.; Bosman, F.T. Steroid-bovine serum albumin conjugates: molecular characterization and their interaction with androgen and estrogen receptors. J. Steroid Biochem., 1986, 24, 1017-1031.
[99]
Erlanger, B.E.; Borek, F.; Beiser, S.M.; Lieberman, S. Steroid-protein conjugates. I. Preparation and characterization of conjugates of bovine serum albumin with testosterone and with cortisone. J. Biol. Chem., 1957, 228, 713-727.
[100]
Ali, S.M.; Khan, A.R.; Ahmad, M.U.; Chen, P.; Sheikh, S.; Ahmad, I. Synthesis and biological evaluation of gemcitabine-lipid conjugate (NEO6002). Bioorg. Med. Chem. Lett., 2005, 15(10), 2571-2574.
[101]
Chen, P.; Chien, P.Y.; Khan, A.R.; Sheikh, S.; Ali, S.M.; Ahmad, M.U.; Ahmad, I. In vitro and in vivo anti-cancer activity of a novel gemcitabine-cardiolipin conjugate. Anticancer Drugs, 2006, 17(1), 53-61.
[102]
Onishi, H.; Matsuyama, M. Conjugate between chondroitin sulfate and prednisolone with a glycine linker: Preparation and in vitro conversion analysis. Chem. Pharm. Bull., 2013, 61, 902-912.
[103]
Chiu, M.L.; Tseng, T.T.C.; Monbouquette, H.G. A convenient homogeneous enzyme immunoassay for estradiol detection. Biotechnol. Appl. Biochem., 2011, 58, 75-82.
[104]
Bucki, R.; Leszczynska, K.; Byfield, F.J.; Fein, D.E.; Won, E.; Cruz, K.; Namiot, A.; Kulakowska, A.; Namiot, Z.; Savage, P.B.; Diamond, S.L.; Janmey, P.A. Combined antibacterial and anti-inflammatory activity of a cationic disubstituted dexamethasone-spermine conjugate. Antimicrob. Agents Chemother., 2010, 54, 2525-2533.
[105]
Funk, D.; Schrenk, H.H.; Frei, E. Development of a novel polyethylene glycol-corticosteroid-conjugate with an acid-cleavable linker. J. Drug Target., 2011, 19, 434-445.
[106]
He, X.K.; Yuan, Z.X.; Wu, X.J.; Xu, C.Q.; Li, W.Y. Low molecular weight hydroxyethyl chitosan-prednisolone conjugate for renal targeting therapy: Synthesis, characterization and in vivo studies. Theranostics, 2012, 2, 1054-1063.
[107]
Pang, Y.N.; Zhang, Y.; Zhang, Z.R. Synthesis of an enzyme-dependent prodrug and evaluation of its potential for colon targeting. World J. Gastroenterol., 2002, 8, 913-917.
[108]
Quan, L.D.; Purdue, P.E.; Liu, X.M.; Boska, M.D.; Lele, S.M.; Thiele, G.M.; Mikuls, T.R.; Dou, H.; Goldring, S.R.; Wang, D. Development of a macromolecular prodrug for the treatment of inflammatory arthritis: Mechanisms involved in arthrotropism and sustained therapeutic efficacy. Arthritis Res. Ther., 2010, 12, R170.
[109]
Kiew, L.V.; Cheong, S.K.; Sidik, K.; Chung, L.Y. Improved plasma stability and sustained release profile of gemcitabine via polypeptide conjugation. Int. J. Pharm., 2010, 391(1-2), 212-220.
[110]
Alexander, R.L.; Greene, B.T.; Torti, S.V.; Kucera, G.L. A novel phospholipid gemcitabine conjugate is able to bypass three drug-resistance mechanisms. Cancer Chemother. Pharmacol., 2005, 56(1), 15-21.
[111]
Alexander, R.L.; Morris-Natschke, S.L.; Ishaq, K.S.; Fleming, R.A.; Kucera, G.L. Synthesis of cytotoxic activity of two novel 1-dodecylthio-2-decyloxypropyl-3-phophatidic acid conjugates with gemcitabine and cytosine arabinoside. J. Med. Chem., 2003, 46, 4205-4208.
[112]
Alexander, R.L.; Kucera, G.L. Lipid nucleoside conjugates for the treatment of cancer. Curr. Pharm. Des., 2005, 11(9), 1079-1089.
[113]
Lammers, T.; Subr, V.; Ulbrich, K.; Peschke, P.; Huber, P.E.; Hennink, W.E.; Storm, G. Simultaneous delivery of doxorubicin and gemcitabine to tumors in vivo using prototypic polymeric drug carriers. Biomaterials, 2009, 30(20), 3466-3475.
[114]
Guo, P.; Ma, J.; Li, S.; Guo, Z.; Adams, A.L.; Gallo, J.M. Targeted delivery of a peripheral benzodiazepine receptor ligand-gemcitabine conjugate to brain tumors in a xenograft model. Cancer Chemother. Pharmacol., 2001, 48(2), 169-176.
[115]
Guo, Z.; Gallo, J.M. Selective protection of 2′,2′-difluorodexoycytidine (gemcitabine). J. Org. Chem., 1999, 64, 8319-8322.
[116]
Castelli, F.; Sarpietro, M.G.; Ceruti, M.; Rocco, F.; Cattel, L. Characterization of lipophilic gemcitabine prodrug-liposomal membrane interaction by differential scanning calorimetry. Mol. Pharm., 2006, 3(6), 737-744.
[117]
Lagisetty, P.; Vilekar, P.; Awasthi, V. Synthesis of radiolabeled cytarabine conjugates. Bioorg. Med. Chem. Lett., 2009, 19, 4764-4767.
[118]
Inapagolla, R.; Guru, B.R.; Kurtoglu, Y.E.; Gao, X.; Lieh-Lai, M.; Bassett, D.J.; Kannan, R.M. In vivo efficacy of dendrimer-methylprednisolone conjugate formulation for the treatment of lung inflammation. Int. J. Pharm., 2010, 399, 140-147.
[119]
Ratcliffe, K.E.; Fraser, H.M.; Sellar, R.; Rivier, J.; Millar, R.P. Bifunctional gonadotropin-releasing hormone antagonist-progesterone analogs with increased efficacy and duration of action. Endocrinology, 2006, 147, 571-579.
[120]
Everts, M.; Kok, R.J.; Asgeirsdóttir, S.A.; Melgert, B.N.; Moolenaar, T.J.; Koning, G.A.; van Luyn, M.J.; Meijer, D.K.; Molema, G. Selective intracellular delivery of dexamethasone into activated endothelial cells using an E-selectin-directed immunoconjugate. J. Immunol., 2002, 168, 883-889.
[121]
Granfeldt, A.; Hvas, C.L.; Graversen, J.H.; Christensen, P.A.; Petersen, M.D.; Anton, G.; Svendsen, P.; Sølling, C.; Etzerodt, A.; Tønnesen, E.; Moestrup, S.K.; Møller, H.J. Targeting dexamethasone to macrophages in a porcine endotoxemic model. Crit. Care Med., 2013, 41, e309-e318.
[122]
Li, Z.H.; Zhang, Q.; Wang, H.B.; Zhang, Y.N.; Ding, D.; Pan, L.Q.; Miao, D.; Xu, S.; Zhang, C.; Luo, P.H.; Naranmandura, H.; Chen, S.Q. Preclinical studies of targeted therapies for CD20-positive B lymphoid malignancies by Ofatumumab conjugated with auristatin. Invest. New Drugs, 2014, 32(1), 75-86.
[123]
Lapalombella, R.; Yu, B.; Triantafillou, G.; Liu, Q.; Butchar, J.P.; Lozanski, G.; Ramanunni, A.; Smith, L.L.; Blum, W.; Andritsos, L.; Wang, D.S.; Lehman, A.; Chen, C.S.; Johnson, A.J.; Marcucci, G.; Lee, R.J.; Lee, L.J.; Tridandapani, S.; Muthusamy, N.; Byrd, J.C. Lenalidomide down-regulates the CD20 antigen and antagonizes direct and antibody-dependent cellular cytotoxicity of rituximab on primary chronic lymphocytic leukemia cells. Blood, 2008, 112, 5180-5189.
[124]
Stanglmaier, M.; Reis, S.; Hallek, M. Rituximab and alemtuzumab induce a nonclassic, caspase-independent apoptotic pathway in B-lymphoid cell lines and in chronic lymphocytic leukemia cells. Ann. Hematol., 2004, 83, 634-645.
[125]
Weitzman, J.; Betancur, M.; Boissel, L.; Rabinowitz, A.P.; Klein, A.; Klingemann, H. Variable contribution of monoclonal antibodies to ADCC in patients with chronic lymphocytic leukemia. Leuk. Lymphoma, 2009, 50, 1361-1368.
[126]
Lv, M.; Lin, Z.; Qiao, C.; Gen, S.; Lang, X.; Li, Y.; Feng, J.; Shen, B. Novel anti-CD20 antibody TGLA with enhanced antibody-dependent cell-mediated cytotoxicity mediates potent anti-lymphoma activity. Cancer Lett., 2010, 294, 66-73.
[127]
Asgeirsdóttir, S.A.; Kok, R.J.; Everts, M.; Meijer, D.K.; Molema, G. Delivery of pharmacologically active dexamethasone into activated endothelial cells by dexamethasone-anti-E-selectin immunoconjugate. Biochem. Pharmacol., 2003, 65, 1729-1739.
[128]
Pietras, R.J.; Pegram, M.D.; Finn, R.S.; Maneval, D.A.; Slamon, D.J. Remission of human breast cancer xenografts on therapy with humanized monoclonal antibody to HER-2 receptor and DNA-reactive drugs. Oncogene, 1998, 17(17), 2235-2249.
[129]
Marches, R.; Uhr, J.W. Enhancement of the p27Kip1-mediated antiproliferative effect of trastuzumab (Herceptin) on HER2-overexpressing tumor cells. Int. J. Cancer, 2004, 112(3), 492-501.
[130]
Sliwkowski, M.X.; Lofgren, J.A.; Lewis, G.D.; Hotaling, T.E.; Fendly, B.M.; Fox, J.A. Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin). Semin. Oncol., 1999, 26(4)(Suppl. 12), 60-70.
[131]
Lin, N.U.; Carey, L.A.; Liu, M.C.; Younger, J.; Come, S.E.; Ewend, M.; Harris, G.J.; Bullitt, E.; Van den Abbeele, A.D.; Henson, J.W.; Li, X.; Gelman, R.; Burstein, H.J.; Kasparian, E.; Kirsch, D.G.; Crawford, A.; Hochberg, F.; Winer, E.P. Phase II trial of lapatinib for brain metastases in patients with human epidermal growth factor receptor 2-positive breast cancer. J. Clin. Oncol., 2008, 26(12), 1993-1999.
[132]
Cobleigh, M.A.; Vogel, C.L.; Tripathy, D.; Robert, N.J.; Scholl, S.; Fehrenbacher, L.; Wolter, J.M.; Paton, V.; Shak, S.; Lieberman, G.; Slamon, D.J. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HE+R2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J. Clin. Oncol., 1999, 17(9), 2639-2648.
[133]
Vogel, C.L.; Cobleigh, M.A.; Tripathy, D.; Gutheil, J.C.; Harris, L.N.; Fehrenbacher, L.; Slamon, D.J.; Murphy, M.; Novotny, W.F.; Burchmore, M.; Shak, S.; Stewart, S.J.; Press, M. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J. Clin. Oncol., 2002, 20(3), 719-726.
[134]
Lewis Phillips, G.D.; Li, G.; Dugger, D.L.; Crocker, L.M.; Parsons, K.L.; Mai, E.; Blättler, W.A.; Lambert, J.M.; Chari, R.V.; Lutz, R.J.; Wong, W.L.; Jacobson, F.S.; Koeppen, H.; Schwall, R.H.; Kenkare-Mitra, S.R.; Spencer, S.D.; Sliwkowski, M.X. Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody-cytotoxic drug conjugate. Cancer Res., 2008, 68(22), 9280-9290.
[135]
Kute, T.E.; Savage, L.; Sehle, J.R.; Kim-Shapiro, J.W.; Blanks, M.J.; Wood, J.; Vaughn, J.P. Breast tumor cells isolated from in vitro resistance to trastuzumab remain sensitive to trastuzumab anti-tumor effects in vivo and to ADCC killing. Cancer Immunol. Immunother., 2009, 58(11), 1887-1896.
[136]
Narayan, M.; Wilken, J.A.; Harris, L.N.; Baron, A.T.; Kimbler, K.D.; Maihle, N.J. Trastuzumab-induced HER reprogramming in “resistant” breast carcinoma cells. Cancer Res., 2009, 69(6), 2191-2194.
[137]
Chen, F.L.; Xia, W.; Spector, N.L. Acquired resistance to small molecule ErbB2 tyrosine kinase inhibitors. Clin. Cancer Res., 2008, 14(21), 6730-6734.
[138]
Ritter, C.A.; Perez-Torres, M.; Rinehart, C.; Guix, M.; Dugger, T.; Engelman, J.A.; Arteaga, C.L. Human breast cancer cells selected for resistance to trastuzumab in vivo overexpress epidermal growth factor receptor and ErbB ligands and remain dependent on the ErbB receptor network. Clin. Cancer Res., 2007, 13(16), 4909-4919.
[139]
Nanda, R. Targeting the human epidermal growth factor receptor 2 (HER2) in the treatment of breast cancer: Recent advances and future directions. Rev. Recent Clin. Trials, 2007, 2(2), 111-116.
[140]
Mitra, D.; Brumlik, M.J.; Okamgba, S.U.; Zhu, Y.; Duplessis, T.T.; Parvani, J.G.; Lesko, S.M.; Brogi, E.; Jones, F.E. An oncogenic isoform of HER2 associated with locally disseminated breast cancer and trastuzumab resistance. Mol. Cancer Ther., 2009, 8(8), 2152-2162.
[141]
Oliveras-Ferraros, C.; Vazquez-Martin, A.; Martin-Castilló, B.; Pérez-Martínez, M.C.; Cufí, S.; Del Barco, S.; Bernado, L.; Brunet, J.; López-Bonet, E.; Menendez, J.A. Pathway-focused proteomic signatures in HER2-overexpressing breast cancer with a basal-like phenotype: New insights into de novo resistance to trastuzumab (Herceptin). Int. J. Oncol., 2010, 37(3), 669-678.
[142]
Köninki, K.; Barok, M.; Tanner, M.; Staff, S.; Pitkänen, J.; Hemmilä, P.; Ilvesaro, J.; Isola, J. Multiple molecular mechanisms underlying trastuzumab and lapatinib resistance in JIMT-1 breast cancer cells. Cancer Lett., 2010, 294(2), 211-219.
[143]
Oliveras-Ferraros, C.; Vazquez-Martin, A.; Cufí, S.; Torres-Garcia, V.Z.; Sauri-Nadal, T.; Barco, S.D.; Lopez-Bonet, E.; Brunet, J.; Martin-Castillo, B.; Menendez, J.A. Inhibitor of Apoptosis (IAP) survivin is indispensable for survival of HER2 gene-amplified breast cancer cells with primary resistance to HER1/2-targeted therapies. Biochem. Biophys. Res. Commun., 2011, 407(2), 412-419.
[144]
Barok, M.; Tanner, M.; Köninki, K.; Isola, J. Trastuzumab-DM1 causes tumour growth inhibition by mitotic catastrophe in trastuzumab-resistant breast cancer cells in vivo. Breast Cancer Res., 2011, 13(2), R46.
[145]
Shih, L.B.; Goldenberg, D.M.; Xuan, H.; Lu, H.W.; Mattes, M.J.; Hall, T.C. Internalization of an intact doxorubicin immunoconjugate. Cancer Immunol. Immunother., 1994, 38(2), 92-98.
[146]
Stan, A.C.; Radu, D.L.; Casares, S.; Bona, C.A.; Brumeanu, T.D. Antineoplastic efficacy of doxorubicin enzymatically assembled on galactose residues of a monoclonal antibody specific for the carcinoembryonic antigen. Cancer Res., 1999, 59, 115-121.
[147]
Weaver, D.J.; Voss, E.W. Analysis of rates of receptor-mediated endocytosis and exocytosis of a fluorescent hapten-protein conjugate in murine macrophage: Implications for antigen processing. Biol. Cell, 1998, 90, 169-181.
[148]
Lim, S.H.; Vaughan, A.T.; Ashton-Key, M.; Williams, E.L.; Dixon, S.V.; Chan, H.T.; Beers, S.A.; French, R.R.; Cox, K.L.; Davies, A.J.; Potter, K.N.; Mockridge, C.I.; Oscier, D.G.; Johnson, P.W.; Cragg, M.S.; Glennie, M.J. Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy. Blood, 2011, 118, 2530-2540.
[149]
Beum, P.V.; Peek, E.M.; Lindorfer, M.A.; Beurskens, F.J.; Engelberts, P.J.; Parren, P.W.; van de Winkel, J.G.; Taylor, R.P. Loss of CD20 and bound CD20 antibody from opsonized B cells occurs more rapidly because of trogocytosis mediated by Fc receptor-expressing effector cells than direct internalization by the B cells. J. Immunol., 2011, 187, 3438-3447.
[150]
Pimm, M.V.; Paul, M.A.; Ogumuyiwa, T.; Baldwin, R.W. Biodistribution and tumour localization of a daunomycin-monoclonal antibody conjugate in nude mice and human tumour xenografts. Cancer Immunol. Immunother., 1988, 27(3), 267-271.
[151]
Bidwell, III, G.L.; Davis, A.N.; Fokt, I.; Priebe, W.; Raucher, D. A thermally targeted elastin-like polypeptide-doxorubicin conjugate overcomes drug resistance. Invest. New Drugs, 2007, 25, 313-326.
[152]
Minko, T.; Kopecková, P.; Pzharov, V.; Kopecek, J. HPMA copolymer bound adriamycin overcomes MDR1 gene encoded resistance in a human ovarian carcinoma cell line. J. Control. Release, 1998, 54, 223-233.
[153]
Guillemard, V.; Uri Saragovi, H. Prodrug chemotherapeutics bypass p-glycoprotein resistance and kill tumors in vivo with high efficacy and target-dependent selectivity. Oncogene, 2004, 23, 3613-3621.
[154]
Dubikovskaya, E.A.; Thorne, S.H.; Pillow, T.H.; Contag, C.H.; Wender, P.A. Overcoming multidrug resistance of small-molecule therapeutics through conjugation with releasable octaarginine transporters. Proc. Natl. Acad. Sci., 2008, 105(34), 12128-12133.
[155]
Wang, F.; Jiang, X.; Yang, D.C.; Elliott, R.L.; Head, J.F. Doxorubicin-gallium-transferrin conjugate overcomes multidrug resistance: Evidence for drug accumulation in the nucleus of drug resistant MCF-7/ADR cells. Anticancer Res., 2000, 20(2A), 799-808.
[156]
Régina, A.; Demeule, M.; Ché, C.; Lavallée, I.; Poirier, J.; Gabathuler, R.; Béliveau, R.; Castaigne, J.P. Antitumour activity of ANG1005, a conjugate between paclitaxel and the new brain delivery vector Angiopep-2. Br. J. Pharmacol., 2008, 155, 185-197.
[157]
Asakura, T.; Takahashi, N.; Takada, K.; Inoue, T.; Ohkawa, K. Drug conjugate of doxorubicin with glutathione is a potent reverser of multidrug resistance in rat hepatoma cells. Anticancer Drugs, 1997, 8, 199-203.
[158]
Mazel, M.; Clair, P.; Rousselle, C.; Vidal, P.; Scherrmann, J.M.; Mathieu, D.; Temsamani, J. Doxorubicin-peptide conjugates overcome multidrug resistance. Anticancer Drugs, 2001, 12, 107-116.
[159]
Lam, W.; Leung, C.H.; Chan, H.L.; Fong, W.F. Toxicity and DNA binding of dextran-doxorubicin conjugates in multidrug-resistant KB-V1 cells: Optimization of dextran size. Anticancer Drugs, 2000, 11, 377-384.
[160]
Dubikovskaya, E.A.; Thorne, S.H.; Pillow, T.H.; Contag, C.H.; Wender, P.A. Overcoming multidrug resistance of small-molecule therapeutics through conjugation with releasable octaarginine transporters. Proc. Natl. Acad. Sci., 2008, 105, 12128-12133.


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VOLUME: 19
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Year: 2019
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DOI: 10.2174/1871520619666181204100226
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