271
Views
32
CrossRef citations to date
0
Altmetric
Original Research

Co-delivery of a RanGTP inhibitory peptide and doxorubicin using dual-loaded liposomal carriers to combat chemotherapeutic resistance in breast cancer cells

, , , ORCID Icon, , & show all
Pages 1655-1669 | Received 19 May 2020, Accepted 19 Aug 2020, Published online: 15 Sep 2020

References

  • Merlo LM, Pepper JW, Reid BJ, et al. Cancer as an evolutionary and ecological process. Nat Rev Cancer. 2006 Dec;6(12):924–935.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019 Jan;69(1):7–34.
  • Atkins MB, Tannir NM. Current and emerging therapies for first-line treatment of metastatic clear cell renal cell carcinoma. Cancer Treat Rev. 2018 Nov;70:127–137.
  • Haffty BG, Yang Q, Reiss M, et al. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol. 2006 Dec 20;24(36):5652–5657.
  • Dawar S, Singh N, Kanwar RK, et al. Multifunctional and multitargeted nanoparticles for drug delivery to overcome barriers of drug resistance in human cancers. Drug Discov Today. 2013 Dec;18(23–24):1292–1300.
  • Coley HM. Mechanisms and strategies to overcome chemotherapy resistance in metastatic breast cancer. Cancer Treat Rev. 2008 Jun;34(4):378–390.
  • Szakacs G, Hall MD, Gottesman MM, et al. Targeting the Achilles heel of multidrug-resistant cancer by exploiting the fitness cost of resistance. Chem Rev. 2014 Jun 11;114(11):5753–5774.
  • Markman JL, Rekechenetskiy A, Holler E, et al. Nanomedicine therapeutic approaches to overcome cancer drug resistance. Adv. Drug Delivery Rev. 2013 Nov;65(13–14):1866–1879.
  • Minotti G, Menna P, Salvatorelli E, et al. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev. 2004 Jun;56(2):185–229.
  • Minotti G, Recalcati S, Menna P, et al. Doxorubicin cardiotoxicity and the control of iron metabolism: quinone-dependent and independent mechanisms. Methods Enzymol. 2004;378:340–361.
  • Capelôa T, Benyahia Z, Zampieri LX, et al. Metabolic and non-metabolic pathways that control cancer resistance to anthracyclines. Semin Cell Dev Biol. 2020;98:181–191.
  • Aas T, Børresen A-L, Geisler S, et al. Specific P53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nat Med. 1996 July 01;2(7):811–814.
  • Loi S, Pommey S, Haibe-Kains B, et al. CD73 promotes anthracycline resistance and poor prognosis in triple negative breast cancer. Proc Natl Acad Sci U S A. 2013 Jul 2;110(27):11091–11096.
  • Shen J, He Q, Gao Y, et al. Mesoporous silica nanoparticles loading doxorubicin reverse multidrug resistance: performance and mechanism. Nanoscale. 2011 Oct 5;3(10):4314–4322.
  • Iyer AK, Singh A, Ganta S, et al. Role of integrated cancer nanomedicine in overcoming drug resistance. Adv. Drug Delivery Rev. 2013 Nov;65(13–14):1784–1802.
  • Turner JG, Dawson J, Sullivan DM. Nuclear export of proteins and drug resistance in cancer. Biochem Pharmacol. 2012;83(8):1021–1032.
  • Nielsen D, Maare C, Poulsen F, et al. The relationship between resistance, P-glycoprotein content, and steady state accumulation in five series of Ehrlich ascites tumor cell lines selected for resistance to daunorubicin. Cell Pharmacol. 1994;1:127–135.
  • Zununi Vahed S, Salehi R, Davaran S, et al. Liposome-based drug co-delivery systems in cancer cells. Mater Sci Eng C. 2017 Feb 01;71:1327–1341.
  • Torchilin V, Weissig V. Liposomes: a practical approach. Oxford (UK): Oxford University Press; 2003. p. 264.
  • Bulbake U, Doppalapudi S, Kommineni N, et al. Liposomal formulations in clinical use: an updated review. Pharmaceutics. 2017;9(2):12.
  • Chen X, Wang X, Wang Y, et al. Improved tumor-targeting drug delivery and therapeutic efficacy by cationic liposome modified with truncated bFGF peptide. J Control Release. 2010 Jul 1;145(1):17–25.
  • Sercombe L, Veerati T, Moheimani F, et al. Advances and challenges of liposome assisted drug delivery. Front Pharmacol. 2015;6:286.
  • Haggag YA, Matchett KB, Falconer RA, et al. Novel Ran-RCC1 inhibitory peptide-loaded nanoparticles have anti-cancer efficacy in vitro and in vivo. Cancers. 2019 Feb 14;11:2.
  • Kurisetty VV, Johnston PG, Johnston N, et al. RAN GTPase is an effector of the invasive/metastatic phenotype induced by osteopontin. Oncogene. 2008 Dec 04;27(57):7139–7149.
  • Yuen HF, Chan KK, Grills C, et al. Ran is a potential therapeutic target for cancer cells with molecular changes associated with activation of the PI3K/Akt/mTORC1 and Ras/MEK/ERK pathways. Clin Cancer Res. 2012 Jan 15;18(2):380–391.
  • Clarke PR, Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat Rev Mol Cell Biol. 2008 Jun;9(6):464–477.
  • Yuen H-F, Chan -K-K, Platt-Higgins A, et al. Ran GTPase promotes cancer progression via Met receptormediated downstream signaling. 2016. (2016).
  • Yuen HF, Gunasekharan VK, Chan KK, et al. RanGTPase: a candidate for Myc-mediated cancer progression. J Natl Cancer Inst. 2013 Apr 3;105(7):475–488.
  • Cekan P, Hasegawa K, Pan Y, et al. RCC1-dependent activation of Ran accelerates cell cycle and DNA repair, inhibiting DNA damage-induced cell senescence. Mol Biol Cell. 2016 Apr 15;27(8):1346–1357.
  • Cekan P, Hasegawa K, Pan Y, et al. RCC1-dependent activation of Ran accelerates cell cycle and DNA repair, inhibiting DNA damage-induced cell senescence. Mol Biol Cell. 2016;27(8):1346–1357.
  • Haggag YA, Matchett KB, Dakir EH, et al. Nano-encapsulation of a novel anti-Ran-GTPase peptide for blockade of regulator of chromosome condensation 1 (RCC1) function in MDA-MB-231 breast cancer cells. Int J Pharm. 2017 Apr 15;521(1–2):40–53.
  • Lei M, Ma G, Sha S, et al. Dual-functionalized liposome by co-delivery of paclitaxel with sorafenib for synergistic antitumor efficacy and reversion of multidrug resistance. Drug Deliv. 2019;26(1):262–272.
  • Zhang Y, Zhai M, Chen Z, et al. Dual-modified liposome codelivery of doxorubicin and vincristine improve targeting and therapeutic efficacy of glioma. Drug Deliv. 2017 Jan 01;24(1):1045–1055.
  • Lakkadwala S, Dos Santos Rodrigues B, Sun C, et al. Dual functionalized liposomes for efficient co-delivery of anti-cancer chemotherapeutics for the treatment of glioblastoma. J Control Release. 2019 Aug 10;307:247–260.
  • Ierano C, Portella L, Lusa S, et al. CXCR4-antagonist Peptide R-liposomes for combined therapy against lung metastasis. Nanoscale. 2016 Apr 14;8(14):7562–7571.
  • Roy B, Guha P, Bhattarai R, et al. Influence of lipid composition, pH, and temperature on physicochemical properties of liposomes with curcumin as model drug. J Oleo Sci. 2016;65(5):399–411.
  • Dharmalingam SR, Ramamurthy S, Chidambaram K, et al. A simple HPLC bioanalytical method for the determination of doxorubicin hydrochloride in rat plasma: application to pharmacokinetic studies. Trop J Pharm Res. 2014;13(3):409–415.
  • Haggag YA, Ibrahim RR, Hafiz AA. Design, formulation and in vivo evaluation of novel honokiol-loaded PEGylated PLGA nanocapsules for treatment of breast cancer. Int J Nanomed. 2020;15:1625–1642.
  • Haggag Y, Elshikh M, El-Tanani M, et al. Nanoencapsulation of sophorolipids in PEGylated poly(lactide-co-glycolide) as a novel approach to target colon carcinoma in the murine model. Drug Deliv Transl Res. 2020 Apr 1;10:1353–1366.
  • Yuen HF, Chan KK, Platt-Higgins A, et al. Ran GTPase promotes cancer progression via Met receptormediated downstream signaling. Oncotarget. 2016 Oct 03;7(46):75854–75864.
  • Haggag YA, Osman MA, El-Gizawy SA, et al. Polymeric nano-encapsulation of 5-fluorouracil enhances anti-cancer activity and ameliorates side effects in solid Ehrlich Carcinoma-bearing mice. Biomed Pharmacother. 2018;105:215–224.
  • Papadopoulos D, Kimler BF, Estes NC, et al. Growth delay effect of combined interstitial hyperthermia and brachytherapy in a rat solid tumor model. Anticancer Res. 1989 Jan-Feb;9(1):45–47.
  • Yoshioka T, Kawada K, Shimada T, et al. Lipid peroxidation in maternal and cord blood and protective mechanism against activated-oxygen toxicity in the blood. Am J Obstet Gynecol. 1979 Oct 1;135(3):372–376.
  • Buhl SN, Jackson KY. Optimal conditions and comparison of lactate dehydrogenase catalysis of the lactate-to-pyruvate and pyruvate-to-lactate reactions in human serum at 25, 30, and 37 degrees C. Clin Chem. 1978 May;24(5):828–831.
  • Rosalki SB. An improved procedure for serum creatine phosphokinase determination. J Lab Clin Med. 1967;69(4):696–705.
  • Zhang H. Thin-film hydration followed by extrusion method for liposome preparation. Methods Mol Biol (Clifton, NJ). 2017;1522:17–22.
  • Ai X, Zhong L, Niu H, et al. Thin-film hydration preparation method and stability test of DOX-loaded disulfide-linked polyethylene glycol 5000-lysine-di-tocopherol succinate nanomicelles. Asian J Pharm Sci. 2014 Oct 01;9(5):244–250.
  • Garidel P, Johann C, Mennicke L, et al. The mixing behavior of pseudobinary phosphatidylcholine-phosphatidylglycerol mixtures as a function of pH and chain length. Eur Biophys J. 1997;26(6):447–459.
  • Sułkowski W, Pentak D, Nowak K, et al. The influence of temperature, cholesterol content and pH on liposome stability. J Mol Struct. 2005;744:737–747.
  • Brgles M, Jurasin D, Sikiric MD, et al. Entrapment of ovalbumin into liposomes–factors affecting entrapment efficiency, liposome size, and zeta potential. J Liposome Res. 2008;18(3):235–248.
  • Chountoulesi M, Naziris N, Pippa N, et al. The significance of drug-to-lipid ratio to the development of optimized liposomal formulation. J Liposome Res. 2018 Sep;28(3):249–258.
  • Johnston MJ, Edwards K, Karlsson G, et al. Influence of drug-to-lipid ratio on drug release properties and liposome integrity in liposomal doxorubicin formulations. J Liposome Res. 2008;18(2):145–157.
  • Tefas LR, Sylvester B, Tomuta I, et al. Development of antiproliferative long-circulating liposomes co-encapsulating doxorubicin and curcumin, through the use of a quality-by-design approach. Drug Des Dev Ther. 2017;11:1605.
  • Li J, Wang X, Zhang T, et al. A review on phospholipids and their main applications in drug delivery systems. Asian J Pharm Sci. 2015 Mar 01;10(2):81–98.
  • Marinello PC, Panis C, Silva TNX, et al. Metformin prevention of doxorubicin resistance in MCF-7 and MDA-MB-231 involves oxidative stress generation and modulation of cell adaptation genes. Sci Rep. 2019 Mar 10;9(1):5864.
  • Xu L, Li H, Wang Y, et al. Enhanced activity of doxorubicin in drug resistant A549 tumor cells by encapsulation of P-glycoprotein inhibitor in PLGA-based nanovectors. Oncol Lett. 2014;7(2):387–392.
  • Lao J, Madani J, Pu, et al. Liposomal doxorubicin in the treatment of breast cancer patients: a review. J Drug Deliv. 2013;2013:12.
  • Mishra S, Tamta AK, Sarikhani M, et al. Subcutaneous ehrlich ascites carcinoma mice model for studying cancer-induced cardiomyopathy. Sci Rep. 2018;8(1):5599.
  • Nielsen D, Maare C, Eriksen J, et al. Characterisation of multidrug-resistant Ehrlich ascites tumour cells selected in vivo for resistance to etoposide. Biochem Pharmacol. 2000 Aug 1;60(3):353–361.
  • Nielsen D, Eriksen J, Maare C, et al. P-glycoprotein expression in Ehrlich ascites tumour cells after in vitro and in vivo selection with daunorubicin. Br J Cancer. 1998 Nov;78(9):1175–1180.
  • Nielsen D, Eriksen J, Maare C, et al. Characterisation of non-P-glycoprotein multidrug-resistant Ehrlich ascites tumour cells selected for resistance to mitoxantrone. Biochem Pharmacol. 2000 Aug 1;60(3):363–370.
  • Volm M, Mattern J, Pommerenke E. Time course of MDR gene amplification during in vivo selection for doxorubicin-resistance and during reversal in murine leukemia L 1210. Anticancer Res. 1991;11(2):579.
  • Chevillard S, Vielh P, Bastian G, et al. A single 24h contact time with adriamycin provokes the emergence of resistant cells expressing the Gp 170 protein. Anticancer Res. 1992;12(2):495–499.
  • Landen CN, Merritt WM, Mangala LS, et al. Intraperitoneal delivery of liposomal siRNA for therapy of advanced ovarian cancer. Cancer Biol Ther. 2006;5(12):1708–1713.
  • Sadzuka Y, Hirama R, Sonobe T. Effects of intraperitoneal administration of liposomes and methods of preparing liposomes for local therapy. Toxicol Lett. 2002 Jan 25;126(2):83–90.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.