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Review

Implications of receptor-mediated endocytosis and intracellular trafficking dynamics in the development of antibody drug conjugates

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Pages 13-21 | Published online: 06 Dec 2012

References

  • Adams GP, Weiner LM. Monoclonal antibody therapy of cancer. Nat Biotechnol 2005; 23:1147 - 57; http://dx.doi.org/10.1038/nbt1137; PMID: 16151408
  • Beck A, Haeuw JF, Wurch T, Goetsch L, Bailly C, Corvaïa N. The next generation of antibody-drug conjugates comes of age. Discov Med 2010; 10:329 - 39; PMID: 21034674
  • Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007; 8:603 - 12; http://dx.doi.org/10.1038/nrm2216; PMID: 17609668
  • Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005; 6:112 - 26; http://dx.doi.org/10.1038/nrm1571; PMID: 15687999
  • Höning S, Ricotta D, Krauss M, Späte K, Spolaore B, Motley A, et al. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 2005; 18:519 - 31; http://dx.doi.org/10.1016/j.molcel.2005.04.019; PMID: 15916959
  • Owen DJ, Evans PR. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 1998; 282:1327 - 32; http://dx.doi.org/10.1126/science.282.5392.1327; PMID: 9812899
  • McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2011; 12:517 - 33; http://dx.doi.org/10.1038/nrm3151; PMID: 21779028
  • Wigge P, Köhler K, Vallis Y, Doyle CA, Owen D, Hunt SP, et al. Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol Biol Cell 1997; 8:2003 - 15; PMID: 9348539
  • Ferguson SM, Raimondi A, Paradise S, Shen H, Mesaki K, Ferguson A, et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell 2009; 17:811 - 22; http://dx.doi.org/10.1016/j.devcel.2009.11.005; PMID: 20059951
  • Sundborger A, Soderblom C, Vorontsova O, Evergren E, Hinshaw JE, Shupliakov O. An endophilin-dynamin complex promotes budding of clathrin-coated vesicles during synaptic vesicle recycling. J Cell Sci 2011; 124:133 - 43; http://dx.doi.org/10.1242/jcs.072686; PMID: 21172823
  • Roux A, Uyhazi K, Frost A, De Camilli P. GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 2006; 441:528 - 31; http://dx.doi.org/10.1038/nature04718; PMID: 16648839
  • Stowell MH, Marks B, Wigge P, McMahon HT. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat Cell Biol 1999; 1:27 - 32; http://dx.doi.org/10.1038/8997; PMID: 10559860
  • Sweitzer SM, Hinshaw JE. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 1998; 93:1021 - 9; http://dx.doi.org/10.1016/S0092-8674(00)81207-6; PMID: 9635431
  • Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009; 10:513 - 25; http://dx.doi.org/10.1038/nrm2728; PMID: 19603039
  • Helenius A, Marsh M. Endocytosis of enveloped animal viruses. Ciba Found Symp 1982; •••:59 - 76; PMID: 6129957
  • van Weering JR, Verkade P, Cullen PJ. SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic 2012; 13:94 - 107; http://dx.doi.org/10.1111/j.1600-0854.2011.01297.x; PMID: 21973056
  • Yamashiro DJ, Maxfield FR. Acidification of morphologically distinct endosomes in mutant and wild-type Chinese hamster ovary cells. J Cell Biol 1987; 105:2723 - 33; http://dx.doi.org/10.1083/jcb.105.6.2723; PMID: 2447098
  • Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004; 5:121 - 32; http://dx.doi.org/10.1038/nrm1315; PMID: 15040445
  • Choudhury A, Sharma DK, Marks DL, Pagano RE. Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit rab4 and perturb membrane recycling. Mol Biol Cell 2004; 15:4500 - 11; http://dx.doi.org/10.1091/mbc.E04-05-0432; PMID: 15292453
  • Radhakrishna H, Donaldson JG. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol 1997; 139:49 - 61; http://dx.doi.org/10.1083/jcb.139.1.49; PMID: 9314528
  • Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 2004; 15:3542 - 52; http://dx.doi.org/10.1091/mbc.E04-02-0151; PMID: 15146059
  • Naslavsky N, Weigert R, Donaldson JG. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 2003; 14:417 - 31; http://dx.doi.org/10.1091/mbc.02-04-0053; PMID: 12589044
  • Huotari J, Helenius A. Endosome maturation. EMBO J 2011; 30:3481 - 500; http://dx.doi.org/10.1038/emboj.2011.286; PMID: 21878991
  • Roederer M, Bowser R, Murphy RF. Kinetics and temperature dependence of exposure of endocytosed material to proteolytic enzymes and low pH: evidence for a maturation model for the formation of lysosomes. J Cell Physiol 1987; 131:200 - 9; http://dx.doi.org/10.1002/jcp.1041310209; PMID: 2438291
  • Russell MR, Nickerson DP, Odorizzi G. Molecular mechanisms of late endosome morphology, identity and sorting. Curr Opin Cell Biol 2006; 18:422 - 8; http://dx.doi.org/10.1016/j.ceb.2006.06.002; PMID: 16781134
  • Karin M, Mintz B. Receptor-mediated endocytosis of transferrin in developmentally totipotent mouse teratocarcinoma stem cells. J Biol Chem 1981; 256:3245 - 52; PMID: 6259157
  • Dautry-Varsat A, Ciechanover A, Lodish HF. pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci U S A 1983; 80:2258 - 62; http://dx.doi.org/10.1073/pnas.80.8.2258; PMID: 6300903
  • Trivedi RR, Bhattacharyya S. Constitutive internalization and recycling of metabotropic glutamate receptor 5 (mGluR5). Biochem Biophys Res Commun 2012; 427:185 - 90; http://dx.doi.org/10.1016/j.bbrc.2012.09.040; PMID: 22995293
  • Pellinen T, Ivaska J. Integrin traffic. J Cell Sci 2006; 119:3723 - 31; http://dx.doi.org/10.1242/jcs.03216; PMID: 16959902
  • Harari D, Yarden Y. Molecular mechanisms underlying ErbB2/HER2 action in breast cancer. Oncogene 2000; 19:6102 - 14; http://dx.doi.org/10.1038/sj.onc.1203973; PMID: 11156523
  • Harford J, Wolkoff AW, Ashwell G, Klausner RD. Monensin inhibits intracellular dissociation of asialoglycoproteins from their receptor. J Cell Biol 1983; 96:1824 - 8; http://dx.doi.org/10.1083/jcb.96.6.1824; PMID: 6304116
  • Harford J, Bridges K, Ashwell G, Klausner RD. Intracellular dissociation of receptor-bound asialoglycoproteins in cultured hepatocytes. A pH-mediated nonlysosomal event. J Biol Chem 1983; 258:3191 - 7; PMID: 6298227
  • Roepstorff K, Grandal MV, Henriksen L, Knudsen SL, Lerdrup M, Grøvdal L, et al. Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 2009; 10:1115 - 27; http://dx.doi.org/10.1111/j.1600-0854.2009.00943.x; PMID: 19531065
  • Ellinger I, Schwab M, Stefanescu A, Hunziker W, Fuchs R. IgG transport across trophoblast-derived BeWo cells: a model system to study IgG transport in the placenta. Eur J Immunol 1999; 29:733 - 44; http://dx.doi.org/10.1002/(SICI)1521-4141(199903)29:03<733::AID-IMMU733>3.0.CO;2-C; PMID: 10092075
  • Rocca A, Lamaze C, Subtil A, Dautry-Varsat A. Involvement of the ubiquitin/proteasome system in sorting of the interleukin 2 receptor beta chain to late endocytic compartments. Mol Biol Cell 2001; 12:1293 - 301; PMID: 11359922
  • Jones SM, Foreman SK, Shank BB, Kurten RC. EGF receptor downregulation depends on a trafficking motif in the distal tyrosine kinase domain. Am J Physiol Cell Physiol 2002; 282:C420 - 33; PMID: 11832327
  • Shenoy SK, McDonald PH, Kohout TA, Lefkowitz RJ. Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 2001; 294:1307 - 13; http://dx.doi.org/10.1126/science.1063866; PMID: 11588219
  • Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HE, Behrens J, et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol 2002; 4:222 - 31; http://dx.doi.org/10.1038/ncb758; PMID: 11836526
  • Ober RJ, Martinez C, Lai X, Zhou J, Ward ES. Exocytosis of IgG as mediated by the receptor, FcRn: an analysis at the single-molecule level. Proc Natl Acad Sci U S A 2004; 101:11076 - 81; http://dx.doi.org/10.1073/pnas.0402970101; PMID: 15258288
  • Mircic M, Kavanaugh A. The clinical efficacy of tocilizumab in rheumatoid arthritis. Drugs Today (Barc) 2009; 45:189 - 97; http://dx.doi.org/10.1358/dot.2009.45.3.1343794; PMID: 19436841
  • Igawa T, Ishii S, Tachibana T, Maeda A, Higuchi Y, Shimaoka S, et al. Antibody recycling by engineered pH-dependent antigen binding improves the duration of antigen neutralization. Nat Biotechnol 2010; 28:1203 - 7; http://dx.doi.org/10.1038/nbt.1691; PMID: 20953198
  • Chaparro-Riggers J, Liang H, DeVay RM, Bai L, Sutton JE, Chen W, et al. Increasing serum half-life and extending cholesterol lowering in vivo by engineering antibody with pH-sensitive binding to PCSK9. J Biol Chem 2012; 287:11090 - 7; http://dx.doi.org/10.1074/jbc.M111.319764; PMID: 22294692
  • Tettamanzi MC, Keeler C, Meshack S, Hodsdon ME. Analysis of site-specific histidine protonation in human prolactin. Biochemistry 2008; 47:8638 - 47; http://dx.doi.org/10.1021/bi800444t; PMID: 18652486
  • Keeler C, Jablonski EM, Albert YB, Taylor BD, Myszka DG, Clevenger CV, et al. The kinetics of binding human prolactin, but not growth hormone, to the prolactin receptor vary over a physiologic pH range. Biochemistry 2007; 46:2398 - 410; http://dx.doi.org/10.1021/bi061958v; PMID: 17279774
  • Kulkarni MV, Tettamanzi MC, Murphy JW, Keeler C, Myszka DG, Chayen NE, et al. Two independent histidines, one in human prolactin and one in its receptor, are critical for pH-dependent receptor recognition and activation. J Biol Chem 2010; 285:38524 - 33; http://dx.doi.org/10.1074/jbc.M110.172072; PMID: 20889499
  • Rudnick SI, Lou J, Shaller CC, Tang Y, Klein-Szanto AJ, Weiner LM, et al. Influence of affinity and antigen internalization on the uptake and penetration of Anti-HER2 antibodies in solid tumors. Cancer Res 2011; 71:2250 - 9; http://dx.doi.org/10.1158/0008-5472.CAN-10-2277; PMID: 21406401
  • Fujimori K, Covell DG, Fletcher JE, Weinstein JN. Modeling analysis of the global and microscopic distribution of immunoglobulin G, F(ab’)2, and Fab in tumors. Cancer Res 1989; 49:5656 - 63; PMID: 2790783
  • Weinstein JN, Eger RR, Covell DG, Black CD, Mulshine J, Carrasquillo JA, et al. The pharmacology of monoclonal antibodies. Ann N Y Acad Sci 1987; 507:199 - 210; http://dx.doi.org/10.1111/j.1749-6632.1987.tb45802.x; PMID: 3327413
  • Juweid M, Neumann R, Paik C, Perez-Bacete MJ, Sato J, van Osdol W, et al. Micropharmacology of monoclonal antibodies in solid tumors: direct experimental evidence for a binding site barrier. Cancer Res 1992; 52:5144 - 53; PMID: 1327501
  • Eger RR, Covell DG, Carrasquillo JA, Abrams PG, Foon KA, Reynolds JC, et al. Kinetic model for the biodistribution of an 111In-labeled monoclonal antibody in humans. Cancer Res 1987; 47:3328 - 36; PMID: 3581071
  • Ingle GS, Chan P, Elliott JM, Chang WS, Koeppen H, Stephan JP, et al. High CD21 expression inhibits internalization of anti-CD19 antibodies and cytotoxicity of an anti-CD19-drug conjugate. Br J Haematol 2008; 140:46 - 58; PMID: 17991300
  • Ackerman ME, Pawlowski D, Wittrup KD. Effect of antigen turnover rate and expression level on antibody penetration into tumor spheroids. Mol Cancer Ther 2008; 7:2233 - 40; http://dx.doi.org/10.1158/1535-7163.MCT-08-0067; PMID: 18645032
  • Thurber GM, Schmidt MM, Wittrup KD. Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance. Adv Drug Deliv Rev 2008; 60:1421 - 34; http://dx.doi.org/10.1016/j.addr.2008.04.012; PMID: 18541331
  • Reddy S, Shaller CC, Doss M, Shchaveleva I, Marks JD, Yu JQ, et al. Evaluation of the anti-HER2 C6.5 diabody as a PET radiotracer to monitor HER2 status and predict response to trastuzumab treatment. Clin Cancer Res 2011; 17:1509 - 20; http://dx.doi.org/10.1158/1078-0432.CCR-10-1654; PMID: 21177408
  • Schier R, Bye J, Apell G, McCall A, Adams GP, Malmqvist M, et al. Isolation of high-affinity monomeric human anti-c-erbB-2 single chain Fv using affinity-driven selection. J Mol Biol 1996; 255:28 - 43; http://dx.doi.org/10.1006/jmbi.1996.0004; PMID: 8568873
  • Schier R, McCall A, Adams GP, Marshall KW, Merritt H, Yim M, et al. Isolation of picomolar affinity anti-c-erbB-2 single-chain Fv by molecular evolution of the complementarity determining regions in the center of the antibody binding site. J Mol Biol 1996; 263:551 - 67; http://dx.doi.org/10.1006/jmbi.1996.0598; PMID: 8918938
  • Adams GP, Schier R, McCall AM, Simmons HH, Horak EM, Alpaugh RK, et al. High affinity restricts the localization and tumor penetration of single-chain fv antibody molecules. Cancer Res 2001; 61:4750 - 5; PMID: 11406547
  • Zahnd C, Kawe M, Stumpp MT, de Pasquale C, Tamaskovic R, Nagy-Davidescu G, et al. Efficient tumor targeting with high-affinity designed ankyrin repeat proteins: effects of affinity and molecular size. Cancer Res 2010; 70:1595 - 605; http://dx.doi.org/10.1158/0008-5472.CAN-09-2724; PMID: 20124480
  • Schmidt MM, Wittrup KD. A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol Cancer Ther 2009; 8:2861 - 71; http://dx.doi.org/10.1158/1535-7163.MCT-09-0195; PMID: 19825804
  • Polson AG, Calemine-Fenaux J, Chan P, Chang W, Christensen E, Clark S, et al. Antibody-drug conjugates for the treatment of non-Hodgkin’s lymphoma: target and linker-drug selection. Cancer Res 2009; 69:2358 - 64; http://dx.doi.org/10.1158/0008-5472.CAN-08-2250; PMID: 19258515
  • Doronina SO, Toki BE, Torgov MY, Mendelsohn BA, Cerveny CG, Chace DF, et al. Development of potent monoclonal antibody auristatin conjugates for cancer therapy. Nat Biotechnol 2003; 21:778 - 84; http://dx.doi.org/10.1038/nbt832; PMID: 12778055
  • Kovtun YV, Audette CA, Ye Y, Xie H, Ruberti MF, Phinney SJ, et al. Antibody-drug conjugates designed to eradicate tumors with homogeneous and heterogeneous expression of the target antigen. Cancer Res 2006; 66:3214 - 21; http://dx.doi.org/10.1158/0008-5472.CAN-05-3973; PMID: 16540673
  • Erickson HK, Park PU, Widdison WC, Kovtun YV, Garrett LM, Hoffman K, et al. Antibody-maytansinoid conjugates are activated in targeted cancer cells by lysosomal degradation and linker-dependent intracellular processing. Cancer Res 2006; 66:4426 - 33; http://dx.doi.org/10.1158/0008-5472.CAN-05-4489; PMID: 16618769
  • Tanaka M, Kano Y, Akutsu M, Tsunoda S, Izumi T, Yazawa Y, et al. The cytotoxic effects of gemtuzumab ozogamicin (mylotarg) in combination with conventional antileukemic agents by isobologram analysis in vitro. Anticancer Res 2009; 29:4589 - 96; PMID: 20032408
  • Lewis Phillips GD, Li G, Dugger DL, Crocker LM, Parsons KL, Mai E, et al. Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody-cytotoxic drug conjugate. Cancer Res 2008; 68:9280 - 90; http://dx.doi.org/10.1158/0008-5472.CAN-08-1776; PMID: 19010901
  • Erickson HK, Lewis Phillips GD, Leipold DD, Provenzano CA, Mai E, Johnson HA, et al. The effect of different linkers on target cell catabolism and pharmacokinetics/pharmacodynamics of trastuzumab maytansinoid conjugates. Mol Cancer Ther 2012; 11:1133 - 42; http://dx.doi.org/10.1158/1535-7163.MCT-11-0727; PMID: 22408268
  • Sievers EL, Senter PD. Antibody-Drug Conjugates in Cancer Therapy. [Epub ahead of print] Annu Rev Med 2012; http://dx.doi.org/10.1146/annurev-med-050311-201823; PMID: 23043493
  • Lambert JM. Drug-conjugated monoclonal antibodies for the treatment of cancer. Curr Opin Pharmacol 2005; 5:543 - 9; http://dx.doi.org/10.1016/j.coph.2005.04.017; PMID: 16087399
  • Haeuw JF, Caussanel V, Beck A. [Immunoconjugates, drug-armed antibodies to fight against cancer]. Med Sci (Paris) 2009; 25:1046 - 52; http://dx.doi.org/10.1051/medsci/200925121046; PMID: 20035677
  • LoRusso PM, Weiss D, Guardino E, Girish S, Sliwkowski MX. Trastuzumab emtansine: a unique antibody-drug conjugate in development for human epidermal growth factor receptor 2-positive cancer. Clin Cancer Res 2011; 17:6437 - 47; http://dx.doi.org/10.1158/1078-0432.CCR-11-0762; PMID: 22003071
  • Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, et al, EMILIA Study Group. Trastuzumab emtansine for HER2-positive advanced breast cancer. [Epub ahead of print] N Engl J Med 2012; 367:1783 - 91; http://dx.doi.org/10.1056/NEJMoa1209124; PMID: 23020162
  • Bross PF, Beitz J, Chen G, Chen XH, Duffy E, Kieffer L, et al. Approval summary: gemtuzumab ozogamicin in relapsed acute myeloid leukemia. Clin Cancer Res 2001; 7:1490 - 6; PMID: 11410481
  • Hamann PR, Hinman LM, Beyer CF, Lindh D, Upeslacis J, Flowers DA, et al. An anti-CD33 antibody-calicheamicin conjugate for treatment of acute myeloid leukemia. Choice of linker. Bioconjug Chem 2002; 13:40 - 6; http://dx.doi.org/10.1021/bc0100206; PMID: 11792177
  • Löwenberg B, Beck J, Graux C, van Putten W, Schouten HC, Verdonck LF, et al, Dutch-Belgian Hemato-Oncology Cooperative Group (HOVON), German Austrian AML Study Group (AMLSG), Swiss Group for Clinical Cancer Research Collaborative Group (SAKK). Gemtuzumab ozogamicin as postremission treatment in AML at 60 years of age or more: results of a multicenter phase 3 study. Blood 2010; 115:2586 - 91; http://dx.doi.org/10.1182/blood-2009-10-246470; PMID: 20103782