127
Views
6
CrossRef citations to date
0
Altmetric
Original Research

Thiol-Reactive Star Polymers Functionalized with Short Ethoxy-Containing Moieties Exhibit Enhanced Uptake in Acute Lymphoblastic Leukemia Cells

ORCID Icon, , , , , ORCID Icon, , , , ORCID Icon, ORCID Icon & show all
Pages 9795-9808 | Published online: 11 Dec 2019

References

  • Steliarova-Foucher E, Colombet M, Ries LAG, et al. International incidence of childhood cancer, 2001–10: a population-based registry study. Lancet Oncol. 2017;18(6):719–731.28410997
  • Ness KK, Armenian SH, Kadan-Lottick N, Gurney JG. Adverse effects of treatment in childhood acute lymphoblastic leukemia: general overview and implications for long-term cardiac health. Expert Rev Hematol. 2011;4(2):185–197.21495928
  • Richards DA, Maruani A, Chudasama V. Antibody fragments as nanoparticle targeting ligands: a step in the right direction. Chem Sci. 2017;8:63–77.28451149
  • Cheng Z, Al Zaki A, Hui JZ, Muzykantov VR, Tsourkas A. Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities. Science. 2012;338(6109):903–910.23161990
  • Torres AG, Gait MJ. Exploiting cell surface thiols to enhance cellular uptake. Trends Biotechnol. 2012;30(4):185–190.22260747
  • Zhang R, Qin X, Kong F, Chen P, Pan G. Improving cellular uptake of therapeutic entities through interaction with components of cell membrane. Drug Deliv. 2019;26(1):328–342.30905189
  • Aubry S, Burlina F, Dupont E, et al. Cell-surface thiols affect cell entry of disulfide-conjugated peptides. FASEB J. 2009;23(9):2956–2967.19403512
  • Kichler A, Remy JS, Boussif O, et al. Efficient gene delivery with neutral complexes of lipospermine and thiol-reactive phospholipids. Biochem Biophys Res Commun. 1995;209(2):444–450.7733911
  • Sahaf B, Heydari K, Herzenberg LA, Herzenberg LA. Lymphocyte surface thiol levels. Proc Natl Acad Sci USA. 2003;100(7):4001–4005.12642656
  • Lawrence DA, Song R, Weber P. Surface thiols of human lymphocytes and their changes after in vitro and in vivo activation. J Leukoc Biol. 1996;60(5):611–618.8929552
  • Ceccarelli J, Delfino L, Zappia E, et al. The redox state of the lung cancer microenvironment depends on the levels of thioredoxin expressed by tumor cells and affects tumor progression and response to prooxidants. Int J Cancer. 2008;123(8):1770–1778.18661523
  • Tager M, Kroning H, Thiel U, Ansorge S. Membrane-bound Protein Disulfide Isomerase (PDI) is involved in regulation of surface expression of thiols and drug sensitivity of B-CLL sells. Exp Hematol. 1997;25(7):601–607.9216735
  • Skalska J, Brookes PS, Nadtochiy SM, et al. Modulation of cell surface protein free thiols: a potential novel mechanism of action of the sesquiterpene lactone parthenolide. PLoS One. 2009;4(12):e8115.19956548
  • Deynoux M, Sunter N, Hérault O, Mazurier F. Hypoxia and hypoxia-inducible factors in leukemias. Front Oncol. 2016;6:41.26955619
  • Moreno-Merlo F, Nicklee T, Hedley DW. Association between tissue hypoxia and elevated non-protein sulphydryl concentrations in human cervical carcinoma xenografts. Br J Cancer. 1999;81(6):989–993.10576655
  • Ren JM, McKenzie TG, Fu Q, et al. Star polymers. Chem Rev. 2016;116(12):6743–6836.27299693
  • Hu J, Qiao R, Whittaker MR, Quinn JF, Davis TP. Synthesis of star polymers by RAFT polymerization as versatile nanoparticles for biomedical applications. Aust J Chem. 2017;70(11):1161–1170.
  • Syrett JA, Haddleton DM, Whittaker MR, Davis TP, Boyer C. functional star polymeric molecular carriers built from biodegradable microgel/nanogel cores. Chem Commun (Camb). 2011;47(5):1449–1451.21180748
  • Ferreira J, Syrett J, Whittaker M, Haddleton D, Davis TP, Boyer C. Optimizing the feneration of narrow polydispersity ‘arm-first’ star polymers made using RAFT polymerization. Polym Chem. 2011;2(8):1671–1677.
  • Liu J, Duong H, Whittaker MR, Davis TP, Boyer C. Synthesis of functional core star polymers via RAFT polymerization for drug delivery applications. Macromol Rapid Commun. 2012;33(9):760–766.22495770
  • Boyer C, Teo J, Phillips P, et al. Effective delivery of siRNA into cancer cells and tumors using well-defined biodegradable cationic star polymers. Mol Pharm. 2013;10(6):2435–2444.23611705
  • Teo J, McCarroll JA, Boyer C, et al. A rationally optimized nanoparticle system for the delivery of RNA interference therapeutics into pancreatic tumors in vivo. Biomacromolecules. 2016;17(7):2337–2351.27305597
  • Rosselgong J, Armes SP. Quantification of intramolecular cyclization in branched copolymers by 1H NMR spectroscopy. Macromolecules. 2012;45(6):2731–2737.
  • Li Y, Duong HT, Laurent S, et al. Nanoparticles based on star polymers as theranostic vectors: endosomal-triggered drug release combined with MRI sensitivity. Adv Healthc Mater. 2015;4(1):148–156.24985790
  • Khor SY, Hu J, McLeod VM, et al. The pharmacokinetics and biodistribution of a 64 kDa PolyPEG star polymer after subcutaneous and pulmonary administration to rats. J Pharm Sci. 2016;105(1):293–300.26852861
  • Glass JJ, Li Y, De Rose R, et al. Thiol-reactive star polymers display enhanced association with distinct human blood components. ACS Appl Mater Interfaces. 2017;9(14):12182–12194.28338321
  • van der Vlies AJ, O’Neil CP, Hasegawa U, Hammond N, Hubbell JA. Synthesis of pyridyl disulfide-functionalized nanoparticles for conjugating thiol-containing small molecules, peptides, and proteins. Bioconjug Chem. 2010;21(4):653–662.20369815
  • Boyer C, Whittaker MR, Luzon M, Davis TP. Design and synthesis of dual thermoresponsive and antifouling hybrid polymer/gold nanoparticles. Macromolecules. 2009;42(18):6917–6926.
  • Pui C-H, Robison LL, Look AT. Acute lymphoblastic leukaemia. Lancet. 2008;371(9617):1030–1043.18358930
  • Lock RB, Liem N, Farnsworth ML, et al. The nonobese diabetic/severe combined immunodeficient (NOD/SCID) mouse model of childhood acute lymphoblastic leukemia reveals intrinsic differences in biologic characteristics at diagnosis and relapse. Blood. 2002;99(11):4100–4108.12010813
  • Liem NLM, Papa RA, Milross CG, et al. Characterization of childhood acute lymphoblastic leukemia xenograft models for the preclinical evaluation of new therapies. Blood. 2004;103(10):3905–3914.14764536
  • Costa Verdera H, Gitz-Francois JJ, Schiffelers RM, Vader P. Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis. J Control Release. 2017;266:100–108.28919558
  • Vercauteren D, Piest M, van der Aa LJ, et al. Flotillin-dependent endocytosis and a phagocytosis-like mechanism for cellular internalization of disulfide-based poly(Amido Amine)/DNA polyplexes. Biomaterials. 2011;32(11):3072–3084.21262529
  • Ariotti N, Hall Thomas E, Rae J, et al. Modular detection of GFP-labeled proteins for rapid screening by electron microscopy in cells and organisms. Dev Cell. 2015;35(4):513–525.26585296
  • Liu J, Bulmus V, Barner-Kowollik C, Stenzel MH, Davis TP. Direct synthesis of pyridyl disulfide-terminated polymers by RAFT polymerization. Macromol Rapid Commun. 2007;28(3):305–314.
  • Mortensen BT, Jensen PO, Helledie N, et al. Changing bone marrow micro-environment during development of acute myeloid leukaemia in rats. Br J Haematol. 1998;102(2):458–464.9695960
  • Wucherpfennig T, Wilsch-Bräuninger M, González-Gaitán M. Role of drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol. 2003;161(3):609–624.12743108
  • Watanabe S, Boucrot E. Fast and ultrafast endocytosis. Curr Opin Cell Biol. 2017;47:64–71.28391090
  • Dutta D, Donaldson JG. Search for inhibitors of endocytosis: intended specificity and unintended consequences. Cell Logist. 2012;2(4):203–208.23538558
  • Harush-Frenkel O, Debotton N, Benita S, Altschuler Y. Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochem Biophys Res Commun. 2007;353(1):26–32.17184736
  • von Kleist L, Stahlschmidt W, Bulut H, et al. Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell. 2011;146(3):471–484.21816279
  • Harris J, Werling D, Koss M, Monaghan P, Taylor G, Howard CJ. Expression of caveolin by bovine lymphocytes and antigen-presenting cells. Immunology. 2002;105(2):190–195.11872094
  • Bandmann V, Müller JD, Köhler T, Homann U. Uptake of fluorescent nano beads into BY2-cells involves clathrin-dependent and clathrin-independent endocytosis. FEBS Lett. 2012;586(20):3626–3632.23046971
  • Ito E, Fujimoto M, Ebine K, Uemura T, Ueda T, Nakano A. Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging. Plant J. 2012;69(2):204–216.21910772
  • Koivusalo M, Welch C, Hayashi H, et al. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol. 2010;188(4):547–563.20156964
  • Pendyala L, Velagapudi S, Toth K, et al. Translational studies of glutathione in bladder cancer cell lines and human specimens. Clin Cancer Res. 1997;3(5):793–798.9815751
  • Cao Y, Gong Y, Liu L, et al. The use of human umbilical vein endothelial cells (HUVECs) as an in vitro model to assess the toxicity of nanoparticles to endothelium: a review. J Appl Toxicol. 2017;37(12):1359–1369.28383141
  • Loretz B, Bernkop-Schnürch A. In vitro cytotoxicity testing of non-thiolated and thiolated chitosan nanoparticles for oral gene delivery. Nanotoxicology. 2007;1(2):139–148.
  • Pellom ST, Michalek RD, Crump KE, Langston PK, Juneau DG, Grayson JM. Increased cell surface free thiols identify effector CD8+ T cells undergoing T cell receptor stimulation. PLoS One. 2013;8(11):e81134.24236211
  • Li X, Wang X, Zhang X, et al. Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proc Natl Acad Sci USA. 2013;110(52):21165–21170.24324172
  • Samadi Moghaddam M, Heiny M, Shastri VP. Enhanced cellular uptake of nanoparticles by increasing the hydrophobicity of Poly(Lactic Acid) through copolymerization with cell-membrane-lipid components. Chem Commun. 2015;51(78):14605–14608.
  • Zhang S, Gao H, Bao G. Physical principles of nanoparticle cellular endocytosis. ACS Nano. 2015;9(9):8655–8671.26256227
  • Song Y, Xue L, Du S, et al. Caveolin-1 knockdown is associated with the metastasis and proliferation of human lung cancer cell line NCI-H460. Biomed Pharmacother. 2012;66(6):439–447.22898083
  • Elkin SR, Bendris N, Reis CR, et al. A systematic analysis reveals heterogeneous changes in the endocytic activities of cancer cells. Cancer Res. 2015;75(21):4640–4650.26359453
  • Young A. Structural insights into the clathrin coat. Semin Cell Dev Biol. 2007;18(4):448–458.17702618
  • Eavarone DA, Yu X, Bellamkonda RV. Targeted drug delivery to C6 glioma by transferrin‐coupled liposomes. J Biomed Mater Res. 2000;51(1):10–14.10813739
  • Bareford LM, Swaan PW. Endocytic mechanisms for targeted drug delivery. Adv Drug Deliv Rev. 2007;59(8):748–758.17659804
  • Ferguson SM, De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol. 2012;13(2):75–88.22233676
  • Rejman J, Oberle V, Zuhorn IS, Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J. 2004;377(1):159–169.14505488
  • Perumal OP, Inapagolla R, Kannan S, Kannan RM. The effect of surface functionality on cellular trafficking of dendrimers. Biomaterials. 2008;29(24–25):3469–3476.18501424
  • Fra AM, Williamson E, Simons K, Parton RG. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J Biol Chem. 1994;269(49):30745–30748.7982998
  • Li T, Takeoka S. enhanced cellular uptake of maleimide-modified liposomes via thiol-mediated transport. Int J Nanomedicine. 2014;9:2849–2861.24940060