Application of chloroquine as an endosomal escape enhancing agent: new frontiers for an old drug

References

• Oh S, Shin JH, Jang EJ, et al. Anti-inflammatory activity of chloroquine and amodiaquine through p21-mediated suppression of T cell proliferation and Th1 cell differentiation. Biochem Biophys Res Commun. 2016;474(2):345–350. .
   PubMed Web of Science ®Google Scholar
• Al-Bari MAA. Chloroquine analogues in drug discovery: new directions of uses, mechanisms of actions and toxic manifestations from malaria to multifarious diseases. J Antimicrob Chemother. 2015;70(6):1608–1621.
   PubMed Web of Science ®Google Scholar
• Gostner JM, Schröcksnadel S, Becker K, et al. Antimalarial drug chloroquine counteracts activation of indoleamine (2, 3)-dioxygenase activity in human PBMC. FEBS Open Bio. 2012;2:241–245.
   PubMed Web of Science ®Google Scholar
• Baradaran Eftekhari R, Maghsoudnia N, Dorkoosh FA. Chloroquine: A brand-new scenario for an old drug. Taylor & Francis; 2020.
   Google Scholar
• Krafts K, Hempelmann E, Skórska-Stania A. From methylene blue to chloroquine: a brief review of the development of an antimalarial therapy. Parasitol Res. 2012;111(1):1–6.
   PubMed Web of Science ®Google Scholar
• CfD C. Prevention. The history of malaria, an ancient disease. Centers for Disease Control and Prevention. Atlanta, GA, USA; 2010. [cited 2021 Jan 13]. Available from https://www.cdc.gov/malaria/about/history/index.html
   Google Scholar
• Cooper R, Magwere T. Chloroquine: novel uses & manifestations. Indian J Med Res. 2008;127:4.
   PubMed Web of Science ®Google Scholar
• White NJ. The treatment of malaria. N Engl J Med. 1996;335(11):800–806.
   PubMed Web of Science ®Google Scholar
• Canfield C, Clyde D, Peters W. et al. Chemotherapy of Malaria. World Health Org Geneva. 1986; 99–100.
   Google Scholar
• Peters W, Ekong R, Robinson B, et al. Antihistaminic drugs that reverse chloroquine resistance in Plasmodium falciparum. Lancet. 1989;334(8658):334–335. .
   Google Scholar
• Pereira MR, Henrich PP, Johnson D, et al. In vivo and in vitro antimalarial properties of azithromycin-chloroquine combinations that include the resistance reversal agent amlodipine. Antimicrob Agents Chemother. 2011;55(7):3115–3124.
   PubMed Web of Science ®Google Scholar
• Petri M. Hydroxychloroquine use in the Baltimore Lupus Cohort: effects on lipids, glucose and thrombosis. Lupus. 1996;5(1_suppl):16–22.
   Google Scholar
• Leadbetter EA, Rifkin IR, Hohlbaum AM, et al. Chromatin–IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature. 2002;416(6881):603–607. .
   PubMed Web of Science ®Google Scholar
• Means TK, Latz E, Hayashi F, et al. Human lupus autoantibody–DNA complexes activate DCs through cooperation of CD32 and TLR9. J Clin Invest. 2011;55(7):407–417.
   Google Scholar
• Yao X, Ye F, Zhang M, et al. In vitro antiviral activity and projection of optimized dosing design of hydroxychloroquine for the treatment of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Clin Infect Dis. 2008;71(15):732–739.
   Google Scholar
• Group RC. Effect of hydroxychloroquine in hospitalized patients with Covid-19. N Engl J Med. 2020;383(21):2030–2040.
   Web of Science ®Google Scholar
• Kiley J NIH halts clinical trial of hydroxychloroquine. National Institutes of Health [online]. 2020. [cited 2020 Jun 13]. Available from https://wwwnihgov/news-events/news-releases/nih-halts-clinical-trial-hydroxychloroquine
   Google Scholar
• Tang W, Cao Z, Han M, et al. Hydroxychloroquine in patients with mainly mild to moderate coronavirus disease 2019: open label, randomised controlled trial. BMJ (Clinical Research Ed.). 2020;369:369.
   Google Scholar
• Verbaanderd C, Maes H, Schaaf MB, et al. Repurposing Drugs in Oncology (ReDO)-chloroquine and hydroxychloroquine as anti-cancer agents. ecancermedicalscience. 2003;11:11.
   Google Scholar
• Zhang Y, Wang Q, Ma A, et al. Functional expression of TLR9 in esophageal cancer. Oncol Rep. 2014;31(5):2298–2304.
   PubMed Web of Science ®Google Scholar
• Mohamed FE, Al‐Jehani RM, Minogue SS, et al. Effect of toll‐like receptor 7 and 9 targeted therapy to prevent the development of hepatocellular carcinoma. Liver Int. 2015;35(3):1063–1076.
   PubMed Web of Science ®Google Scholar
• Hulboy DL, Gautam S, Fingleton B, et al. The influence of matrix metalloproteinase-7 on early mammary tumorigenesis in the multiple intestinal neoplasia mouse. Oncol Rep. 2004;12(1):13–17.
   PubMed Web of Science ®Google Scholar
• Nunes BL, Jucá MJ, Gomes EG, et al. Metalloproteinase-1, metalloproteinase-7, and p53 immunoexpression and their correlation with clinicopathological prognostic factors in colorectal adenocarcinoma. Int J Biol Markers. 2009;24(3):156–164.
   PubMed Web of Science ®Google Scholar
• Dannenberg AJ, Altorki NK, Boyle JO, et al. Cyclo-oxygenase 2: a pharmacological target for the prevention of cancer. Lancet Oncol. 2001;2(9):544–551.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li Y, Li Y, et al. Chloroquine inhibits MGC803 gastric cancer cell migration via the Toll-like receptor 9/nuclear factor kappa B signaling pathway. Mol Med Rep. 2015;11(2):1366–1371.
   PubMed Web of Science ®Google Scholar
• Kužnik A, Benčina M, Švajger U, et al. Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J Immunol. 2011;186(8):4794–4804.
   PubMed Web of Science ®Google Scholar
• Sun X, Cheng G, Hao M, et al. CXCL12/CXCR4/CXCR7 chemokine axis and cancer progression. Cancer Metast Rev. 2010;29(4):709–722.
   PubMed Web of Science ®Google Scholar
• Yasumoto K, Koizumi K, Kawashima A, et al. Role of the CXCL12/CXCR4 axis in peritoneal carcinomatosis of gastric cancer. Cancer Res. 2006;66(4):2181–2187.
   PubMed Web of Science ®Google Scholar
• Singh S, Singh UP, Grizzle WE, et al. CXCL12–CXCR4 interactions modulate prostate cancer cell migration, metalloproteinase expression and invasion. Lab Invest. 2004;84(12):1666–1676.
   PubMed Web of Science ®Google Scholar
• Singh S, Srivastava S, Bhardwaj A, et al. CXCL12–CXCR4 signalling axis confers gemcitabine resistance to pancreatic cancer cells: a novel target for therapy. Br J Cancer. 2010;103(11):1671–1679.
   PubMed Web of Science ®Google Scholar
• Fukui H, Zhang X, Sun C, et al. IL-22 produced by cancer-associated fibroblasts promotes gastric cancer cell invasion via STAT3 and ERK signaling. Br J Cancer. 2014;111(4):763–771.
   PubMed Web of Science ®Google Scholar
• Fang Z, Tang Y, Fang J, et al. Simvastatin inhibits renal cancer cell growth and metastasis via AKT/mTOR, ERK and JAK2/STAT3 pathway. PLoS One. 2013;8:5.
   Google Scholar
• Balic A, Sørensen MD, Trabulo SM, et al. Chloroquine targets pancreatic cancer stem cells via inhibition of CXCR4 and hedgehog signaling. Mol Cancer Ther. 2014;13(7):1758–1771.
   PubMed Web of Science ®Google Scholar
• Kim EL, Wüstenberg R, Rübsam A, et al. Chloroquine activates the p53 pathway and induces apoptosis in human glioma cells. Neuro Oncol. 2010;12(4):389–400.
   PubMed Web of Science ®Google Scholar
• Burikhanov R, Hebbar N, Noothi SK, et al. Chloroquine-inducible par-4 secretion is essential for tumor cell apoptosis and inhibition of metastasis. Cell Rep. 2017;18(2):508–519.
   PubMed Web of Science ®Google Scholar
• Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer. 2014;14(5):359–370.
   PubMed Web of Science ®Google Scholar
• Zhou Q, McCracken MA, Strobl JS. Control of mammary tumor cell growth in vitro by novel cell differentiation and apoptosis agents. Breast Cancer Res Treat. 2002;75(2):107–117.
   PubMed Web of Science ®Google Scholar
• Maclean KH, Dorsey FC, Cleveland JL, et al. Targeting lysosomal degradation induces p53-dependent cell death and prevents cancer in mouse models of lymphomagenesis. J Clin Invest. 2008;118(1):79–88.
   PubMed Web of Science ®Google Scholar
• George P. p53 how crucial is its role in cancer. Int J Curr Pharm Res. 2011;3(2):19–25.
   Google Scholar
• Hwang JR, Kim WY, Cho Y-J, et al. Chloroquine reverses chemoresistance via upregulation of p21 WAF1/CIP1 and autophagy inhibition in ovarian cancer. Cell Death Dis. 2020;11(12):1–17.
   PubMed Web of Science ®Google Scholar
• Al‐Bari MAA. Co‐targeting of lysosome and mitophagy in cancer stem cells with chloroquine analogues and antibiotics. J Cell Mol Med. 2020;24(20):11667–11679.
   PubMed Web of Science ®Google Scholar
• Ganguli A, Choudhury D, Datta S, et al. Inhibition of autophagy by chloroquine potentiates synergistically anti-cancer property of artemisinin by promoting ROS dependent apoptosis. Biochimie. 2014;107:338–349.
   PubMed Web of Science ®Google Scholar
• Sasaki K, Tsuno NH, Sunami E, et al. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer. 2010;10(1):1–11.
   PubMedGoogle Scholar
• Liu F, Shang Y, Chen S-Z. Chloroquine potentiates the anti-cancer effect of lidamycin on non-small cell lung cancer cells in vitro. Acta Pharmacol Sin. 2014;35(5):645–652.
   PubMed Web of Science ®Google Scholar
• Peterse EF, Niessen B, Addie RD, et al. Targeting glutaminolysis in chondrosarcoma in context of the IDH1/2 mutation. Br J Cancer. 2018;118(8):1074–1083.
   PubMed Web of Science ®Google Scholar
• Jarzyna R, Kiersztan A, Lisowa O, et al. The inhibition of gluconeogenesis by chloroquine contributes to its hypoglycaemic action. Eur J Pharmacol. 2001;428(3):381–388.
   PubMed Web of Science ®Google Scholar
• Choi -M-M, Kim E-A, Choi S-Y, et al. Inhibitory properties of nerve-specific human glutamate dehydrogenase isozyme by chloroquine. BMB Rep. 2007;40(6):1077–1082.
   Google Scholar
• Yauch RL, Gould SE, Scales SJ, et al. A paracrine requirement for hedgehog signalling in cancer. Nature. 2008;455(7211):406–410.
   PubMed Web of Science ®Google Scholar
• Thongchot S, Loilome W, Yongvanit P, et al. Chloroquine exerts anti-metastatic activities under hypoxic conditions in cholangiocarcinoma cells. Asian Pac J Cancer Prev. 2015;16(5):2031–2035.
   PubMedGoogle Scholar
• Nagaraju GP, Mezina A, Shaib WL, et al. Targeting the Janus-activated kinase-2-STAT3 signalling pathway in pancreatic cancer using the HSP90 inhibitor ganetespib. Eur J Cancer. 2016;52:109–119.
   PubMed Web of Science ®Google Scholar
• Park BC, Park SH, Paek S-H, et al. Chloroquine-induced nitric oxide increase and cell death is dependent on cellular GSH depletion in A172 human glioblastoma cells. Toxicol Lett. 2008;178(1):52–60.
   PubMed Web of Science ®Google Scholar
• Sahay G, Alakhova DY, Kabanov AV. Endocytosis of nanomedicines. J Control Release. 2010;145(3):182–195.
   PubMed Web of Science ®Google Scholar
• Rothen-Rutishauser BM, Schürch S, Haenni B, et al. Interaction of fine particles and nanoparticles with red blood cells visualized with advanced microscopic techniques. Environ Sci Technol. 2006;40(14):4353–4359.
   PubMed Web of Science ®Google Scholar
• Kuhn DA, Vanhecke D, Michen B, et al. Different endocytotic uptake mechanisms for nanoparticles in epithelial cells and macrophages. Beilstein J Nanotechnol. 2014;5(1):1625–1636.
   PubMedGoogle Scholar
• Lim JP, Gleeson PA. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol. 2011;89(8):836–843.
   PubMed Web of Science ®Google Scholar
• Sorkin A, Puthenveedu MA. Clathrin-mediated endocytosis. In: Yarden Y, Tarcic G, editors. Vesicle Trafficking in Cancer. New York: Springer New York; 2013. p. 1–31.
   Google Scholar
• Kirkham M, Parton RG. Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta-Mol Cell Res. 2005;1745(3):273–286.
   Web of Science ®Google Scholar
• Sandvig K, Pust S, Skotland T, et al. Clathrin-independent endocytosis: mechanisms and function. Curr Opin Cell Biol. 2011;23(4):413–420.
   PubMed Web of Science ®Google Scholar
• Cobbold C, Coventry J, Ponnambalam S, et al. The Menkes disease ATPase (ATP7A) is internalized via a Rac1-regulated, clathrin-and caveolae-independent pathway. Hum Mol Genet. 2003;12(13):1523–1533.
   PubMed Web of Science ®Google Scholar
• Jones AT. Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med. 2007;11(4):670–684.
   PubMed Web of Science ®Google Scholar
• Kühn S, Lopez-Montero N, Chang -Y-Y, et al. Imaging macropinosomes during Shigella infections. Methods. 2017;127:12–22.
   PubMed Web of Science ®Google Scholar
• Zhao F, Zhao Y, Liu Y, et al. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. small. 2011;7(10):1322–1337.
   PubMed Web of Science ®Google Scholar
• Panariti A, Miserocchi G, Rivolta I. The effect of nanoparticle uptake on cellular behavior: disrupting or enabling functions? Nanotechnol Sci Appl. 2012;5:87.
   PubMedGoogle Scholar
• Rejman J, Oberle V, Zuhorn IS, et al. Size-dependent internalization of particles via the pathways of clathrin-and caveolae-mediated endocytosis. Biochem J. 2004;377(1):159–169.
   PubMedGoogle Scholar
• Chithrani BD, Chan WC. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett. 2007;7(6):1542–1550.
   PubMed Web of Science ®Google Scholar
• Jin H, Heller DA, Sharma R, et al. Size-dependent cellular uptake and expulsion of single-walled carbon nanotubes: single particle tracking and a generic uptake model for nanoparticles. ACS Nano. 2009;3(1):149–158.
   PubMed Web of Science ®Google Scholar
• Wang S-H, Lee C-W, Chiou A, et al. Size-dependent endocytosis of gold nanoparticles studied by three-dimensional mapping of plasmonic scattering images. J Nanobiotechnology. 2010;8(1):33.
   PubMedGoogle Scholar
• Wu M, Guo H, Liu L, et al. Size-dependent cellular uptake and localization profiles of silver nanoparticles. Int J Nanomed. 2019;14:4247.
   PubMed Web of Science ®Google Scholar
• Fröhlich E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomedicine. 2012;7:5577.
   PubMed Web of Science ®Google Scholar
• Mansouri S, Cuie Y, Winnik F, et al. Characterization of folate-chitosan-DNA nanoparticles for gene therapy. Biomaterials. 2006;27(9):2060–2065.
   PubMed Web of Science ®Google Scholar
• Lu H, Dai Y, Lv L, et al. Chitosan-graft-polyethylenimine/DNA nanoparticles as novel non-viral gene delivery vectors targeting osteoarthritis. Plos One. 2014;9(1):e84703.
   PubMed Web of Science ®Google Scholar
• Patil ML, Zhang M, Betigeri S, et al. Surface-modified and internally cationic polyamidoamine dendrimers for efficient siRNA delivery. Bioconjug Chem. 2008;19(7):1396–1403.
   PubMed Web of Science ®Google Scholar
• Lunnoo T, Assawakhajornsak J, Puangmali T. In silico study of gold nanoparticle uptake into a mammalian cell: interplay of size, shape, surface charge, and aggregation. J Phys Chem C. 2019;123(6):3801–3810.
   Web of Science ®Google Scholar
• Dausend J, Musyanovych A, Dass M, et al. Uptake mechanism of oppositely charged fluorescent nanoparticles in HeLa cells. Macromol Biosci. 2008;8(12):1135–1143.
   PubMed Web of Science ®Google Scholar
• Ding H-M, Ma Y-Q. Role of physicochemical properties of coating ligands in receptor-mediated endocytosis of nanoparticles. Biomaterials. 2012;33(23):5798–5802.
   PubMed Web of Science ®Google Scholar
• Sun S, Huang Y, Zhou C, et al. Effect of hydrophobicity on nano-bio interactions of zwitterionic luminescent gold nanoparticles at the cellular level. Bioconjug Chem. 2018;29(6):1841–1846.
   PubMed Web of Science ®Google Scholar
• Han S, Cheng Q, Wu Y, et al. Effects of hydrophobic core components in amphiphilic PDMAEMA nanoparticles on siRNA delivery. Biomaterials. 2015;48:45–55.
   PubMed Web of Science ®Google Scholar
• Li Y, Chen X, Gu N. Computational investigation of interaction between nanoparticles and membranes: hydrophobic/hydrophilic effect. J Phys Chem A. 2008;112(51):16647–16653.
   PubMed Web of Science ®Google Scholar
• Chen L, Wang H, Li X, et al. Highly hydrophilic carbon nanoparticles: uptake mechanism by mammalian and plant cells. RSC Adv. 2018;8(61):35246–35256.
   Web of Science ®Google Scholar
• Storm G, Belliot SO, Daemen T, et al. Surface modification of nanoparticles to oppose uptake by the mononuclear phagocyte system. Adv Drug Deliv Rev. 1995;17(1):31–48.
   Web of Science ®Google Scholar
• Verma A, Stellacci F. Effect of surface properties on nanoparticle–cell interactions. small. 2010;6(1):12–21.
   PubMed Web of Science ®Google Scholar
• Nativo P, Prior IA, Brust M. Uptake and intracellular fate of surface-modified gold nanoparticles. ACS Nano. 2008;2(8):1639–1644.
   PubMed Web of Science ®Google Scholar
• Dou T, Wang J, Han C, et al. Cellular uptake and transport characteristics of chitosan modified nanoparticles in Caco-2 cell monolayers. Int J Biol Macromol. 2019;138:791–799.
   PubMed Web of Science ®Google Scholar
• Sun X, Chen J, Chen H, et al. Polyethylenimine modified liposomes as potential carriers for antitumor drug delivery in vitro. Die Pharmazie- Int J Pharm Sci. 2012;67(5):426–431.
   Google Scholar
• Banerjee A, Qi J, Gogoi R, et al. Role of nanoparticle size, shape and surface chemistry in oral drug delivery. JControlled Release. 2016;238:176–185.
   PubMed Web of Science ®Google Scholar
• Nangia S, Sureshkumar R. Effects of nanoparticle charge and shape anisotropy on translocation through cell membranes. Langmuir. 2012;28(51):17666–17671.
   PubMed Web of Science ®Google Scholar
• Anselmo AC, Zhang M, Kumar S, et al. Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis, and targeting. ACS Nano. 2015;9(3):3169–3177.
   PubMed Web of Science ®Google Scholar
• Yi X, Shi X, Gao H. Cellular uptake of elastic nanoparticles. Phys Rev Lett. 2011;107(9):098101.
   PubMed Web of Science ®Google Scholar
• Tang H, Ye H, Zhang H, et al. Wrapping of nanoparticles by the cell membrane: the role of interactions between the nanoparticles. Soft Matter. 2015;11(44):8674–8683.
   PubMed Web of Science ®Google Scholar
• Yi X, Gao H. Kinetics of receptor-mediated endocytosis of elastic nanoparticles. Nanoscale. 2017;9(1):454–463.
   PubMed Web of Science ®Google Scholar
• Banquy X, Suarez F, Argaw A, et al. Effect of mechanical properties of hydrogel nanoparticles on macrophage cell uptake. Soft Matter. 2009;5(20):3984–3991.
   Web of Science ®Google Scholar
• Ambudkar SV, Kimchi-Sarfaty C, Sauna ZE, et al. P-glycoprotein: from genomics to mechanism. Oncogene. 2003;22(47):7468–7485.
   PubMed Web of Science ®Google Scholar
• Yamagishi T, Sahni S, Sharp DM, et al. P-glycoprotein mediates drug resistance via a novel mechanism involving lysosomal sequestration. J Biol Chem. 2013;288(44):31761–31771.
   PubMedGoogle Scholar
• Varkouhi AK, Scholte M, Storm G, et al. Endosomal escape pathways for delivery of biologicals. J Control Release. 2011;151(3):220–228.
   PubMed Web of Science ®Google Scholar
• Zhang B, Mallapragada S. The mechanism of selective transfection mediated by pentablock copolymers; Part II: nuclear entry and endosomal escape. Acta Biomater. 2011;7(4):1580–1587.
   PubMed Web of Science ®Google Scholar
• Xie Y, Yu F, Tang W, et al. Chloroquine-containing DMAEMA copolymers as efficient anti-miRNA delivery vectors with improved endosomal escape and anti-migratory activity in cancer cells. Macromol Biosci. 2018;18:1.
   Web of Science ®Google Scholar
• Boussif O, Lezoualc’h F, Zanta MA, et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Nat Acad Sci. 1995;92(16):7297–7301.
   PubMed Web of Science ®Google Scholar
• Hu Y, Wang H, Song H, et al. Peptide-grafted dextran vectors for efficient and high-loading gene delivery. Biomater Sci. 2019;7(4):1543–1553.
   PubMed Web of Science ®Google Scholar
• Cervia LD, Chang -C-C, Wang L, et al. Distinct effects of endosomal escape and inhibition of endosomal trafficking on gene delivery via electrotransfection. PLoS One. 2017;12:2.
   Web of Science ®Google Scholar
• Smith WS, Johnston DA, Holmes SE, et al. Augmentation of Saporin-based immunotoxins for human Leukaemia and lymphoma cells by triterpenoid Saponins: the modifying effects of small molecule pharmacological agents. Toxins (Basel). 2019;11(2):127. .
   Web of Science ®Google Scholar
• Du Rietz H, Hedlund H, Wilhelmson S, et al. Imaging small molecule-induced endosomal escape of siRNA. Nat Commun. 2020;11(1):1–17. .
   PubMed Web of Science ®Google Scholar
• Feldmann DP, Cheng Y, Kandil R, et al. In vitro and in vivo delivery of siRNA via VIPER polymer system to lung cells. JControlled Release. 2018;276:50–58.
   PubMed Web of Science ®Google Scholar
• Lönn P, Kacsinta AD, Cui X-S, et al. Enhancing endosomal escape for intracellular delivery of macromolecular biologic therapeutics. Sci Rep. 2016;6(1):1–9. .
   PubMedGoogle Scholar
• Ciftci K, Levy RJ. Enhanced plasmid DNA transfection with lysosomotropic agents in cultured fibroblasts. Int J Pharm. 2001;218(1–2):81–92.
   PubMedGoogle Scholar
• Zhou X, Huang L. DNA transfection mediated by cationic liposomes containing lipopolylysine: characterization and mechanism of action. Biochimica Et Biophysica Acta (BBA) - Biomembranes. 1994;1189(2):195–203.
   PubMed Web of Science ®Google Scholar
• Hyndman L, Lemoine JL, Huang L, et al. HIV-1 Tat protein transduction domain peptide facilitates gene transfer in combination with cationic liposomes. J Control Release. 2004;99(3):435–444. .
   PubMed Web of Science ®Google Scholar
• Erbacher P, Roche AC, Monsigny M, et al. Glycosylated polylysine/DNA complexes: gene transfer efficiency in relation with the size and the sugar substitution level of glycosylated polylysines and with the plasmid size. Bioconjug Chem. 1995;6(4):401–410. .
   PubMed Web of Science ®Google Scholar
• Erbacher P, Roche AC, Monsigny M, et al. Putative role of chloroquine in gene transfer into a human hepatoma cell line by DNA/lactosylated polylysine complexes. Exp Cell Res. 1996;225(1):186–194. .
   PubMed Web of Science ®Google Scholar
• Radaic A, De Jesus M. Solid lipid nanoparticles release DNA upon endosomal acidification in human embryonic kidney cells. Nanotechnology. 2018;29(31):315102.
   PubMed Web of Science ®Google Scholar
• El-Sayed A, Khalil IA, Kogure K, et al. Octaarginine-and octalysine-modified nanoparticles have different modes of endosomal escape. J Biol Chem. 2008;283(34):23450–23461.
   PubMed Web of Science ®Google Scholar
• Khalil IA, Kimura S, Sato Y, et al. Synergism between a cell penetrating peptide and a pH-sensitive cationic lipid in efficient gene delivery based on double-coated nanoparticles. JControlled Release. 2018;275:107–116.
   PubMed Web of Science ®Google Scholar
• Zhang X, Sawyer GJ, Dong X, et al. Thein vivo use of chloroquine to promote non-viral gene delivery to the liver via the portal vein and bile duct. J Gene Med cross‐disciplinary j res sci gene trans clin appl. 2003;5(3):209–218.
   Google Scholar
• Shao M, Zhu W, Lv X, et al. Encapsulation of chloroquine and doxorubicin by MPEG-PLA to enhance anticancer effects by lysosomes inhibition in ovarian cancer. Int J Nanomed. 2018;13:8231.
   PubMed Web of Science ®Google Scholar
• Ducharme J, Farinotti R. Clinical pharmacokinetics and metabolism of chloroquine. Focus on recent advancements. Clin pharmacokinetics. 1996;31(4):257–274.
   PubMed Web of Science ®Google Scholar