Modulation of macropinocytosis-mediated internalization decreases ocular toxicity of antibody–drug conjugates

Cancer Research

Volumn 78, Issue 8, 2018, Pages 2115-2126

  Zhao, Hui ^a   Atkinson, John ^a   Gulesserian, Sara ^a   Zeng, Zhilan ^a   Nater, Jenny ^a   Ou, Jimmy ^a   Yang, Peng ^a   Morrison, Karen ^a   Coleman, Jeffrey ^a   Malik, Faisal ^a   Challita Eid, Pia ^a   Karki, Sher ^a   Aviña, Hector ^a   Hubert, Rene ^a   Capo, Linnette ^a   Snyder, Josh ^a   Moon, Sung Ju ^a   Luethy, Roland ^a   Mendelsohn, Brian A ^a   Stover, David R ^a   Doñate, Fernando ^a   more..

^a Agensys Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGS 16C3F; ANTIBODY DRUG CONJUGATE; MACROGOL; POLYGLUTAMIC ACID; UNCLASSIFIED DRUG; ANTIBODY CONJUGATE;

ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CORNEA EPITHELIUM; DISEASE SEVERITY; EPITHELIUM CELL; EYE TOXICITY; FIBROBLAST; HUMAN; HUMAN CELL; HYDROPHOBICITY; IN VITRO STUDY; INTERNALIZATION; LEPORIDAE; MALE; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; TUMOR XENOGRAFT; UMBILICAL VEIN ENDOTHELIAL CELL; AMINO ACID SEQUENCE; ANIMAL; ANIMAL MODEL; CELL CULTURE; DRUG EFFECT; MACACA FASCICULARIS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; EPITHELIUM, CORNEAL; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOCONJUGATES; MACACA FASCICULARIS; MALE; MODELS, ANIMAL; PINOCYTOSIS; RABBITS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 85047867122     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-17-3202     Document Type: Article

References (32)

1. Beck A, Goetsch L, Dumontet C, Corvaia N. Strategies and challenges for the next generation of antibody-drug conjugates. Nat Rev Drug Discov 2017;16:315–37.
2. de Goeij BE, Lambert JM. New developments for antibody-drug conjugate-based therapeutic approaches. Curr Opin Immunol 2016; 40:14–23.
3. Donaghy H. Effects of antibody, drug and linker on the preclinical and clinical toxicities of antibody-drug conjugates. MAbs 2016;8:659–71.
4. Saber H, Leighton JK. An FDA oncology analysis of antibody-drug conjugates. Regul Toxicol Pharmacol 2015;71:444–52.
5. Zhao H, Gulesserian S, Malinao MC, Ganesan SK, Song J, Chang MS, et al. A Potential mechanism for ADC-induced neutropenia: role of neutrophils in their own demise. Mol Cancer Ther 2017;16:1866–76.
6. Zhao H, Gulesserian S, Ganesan SK, Ou J, Morrison K, Zeng Z, et al. Inhibition of megakaryocyte differentiation by antibody-drug conjugates (ADCs) is mediated by macropinocytosis: implications for ADC-induced thrombocytopenia. Mol Cancer Ther 2017;16:1877–86.
7. Eaton JS, Miller PE, Mannis MJ, Murphy CJ. Ocular adverse events associated with antibody-drug conjugates in human clinical trials. J Ocul Pharmacol Ther 2015;31:589–604.
8. Thompson JA, Motzer R, Molina AM, Choueiri TK, Heath EI, Kollmanns-berger CK, et al. Phase I studies of anti-ENPP3 antibody drug conjugates (ADCs) in advanced refractory renal cell carcinomas (RRCC). J Clin Oncol 33, 2015 (suppl; abstr 2503).
9. Ribrag V, Dupuis J, Tilly H, Morschhauser F, Laine F, Houot R, et al. A dose-escalation study of SAR3419, an anti-CD19 antibody maytansinoid conjugate, administered by intravenous infusion once weekly in patients with relapsed/refractory B-cell non-Hodgkin lymphoma. Clin Cancer Res 2014;20:213–20.
10. Tannir NM, Forero-Torres A, Ramchandren R, Pal SK, Ansell SM, Infante JR, et al. Phase I dose-escalation study of SGN-75 in patients with CD70-positive relapsed/refractory non-Hodgkin lymphoma or metastatic renal cell carcinoma. Invest New Drugs 2014;32:1246–57.
11. Tsuda M, Takano Y, Shigeyasu C, Imoto S, Yamada M. Abnormal corneal lesions induced by trastuzumab emtansine: an antibody-drug conjugate for breast cancer. Cornea 2016;35:1378–80.
12. Beeram M, Krop IE, Burris HA, Girish SR, Yu W, Lu MW, et al. A phase 1 study of weekly dosing of trastuzumab emtansine (T-DM1) in patients with advanced human epidermal growth factor 2-positive breast cancer. Cancer 2012;118:5733–40.
13. Hassan R, Thomas A, Alewine C, Le DT, Jaffee EM, Pastan I. Mesothelin immunotherapy for cancer: ready for prime time? J Clin Oncol 2016;34: 4171–9.
14. Moore KN, Martin LP, O'Malley DM, Matulonis UA, Konner JA, Perez RP, et al. Safety and activity of mirvetuximab soravtansine (IMGN853), a folate receptor alpha-targeting antibody-drug conjugate, in platinum-resistant ovarian, fallopian tube, or primary peritoneal cancer: a phase I expansion study. J Clin Oncol 2017;35:1112–8.
15. Shapiro GI, Vaishampayan UN, LoRusso P, Barton J, Hua S, Reich SD, et al. First-in-human trial of an anti-5T4 antibody-monomethylauristatin conjugate, PF-06263507, in patients with advanced solid tumors. Invest New Drugs 2017;35:315–23.
16. Liu Z, Carvajal M, Carraway CA, Carraway K, Pflugfelder SC. Expression of the receptor tyrosine kinases, epidermal growth factor receptor, ErbB2, and ErbB3, in human ocular surface epithelia. Cornea 2001;20:81–5.
17. Bialucha CU, Collins SD, Li X, Saxena P, Zhang X, Durr C, et al. Discovery and optimization of HKT288, a cadherin-6-targeting ADC for the treatment of ovarian and renal cancers. Cancer Discov 2017;7:1030–45.
18. Coveler AL, Ko AH, Catenacci DV, Von Hoff D, Becerra C, Whiting NC, et al. A phase 1 clinical trial of ASG-5ME, a novel drug-antibody conjugate targeting SLC44A4, in patients with advanced pancreatic and gastric cancers. Invest New Drugs 2016;34:319–28.
19. Secker GA, Daniels JT. Limbal epithelial stem cells of the cornea. In: Watt F, Gage F, editors. StemBook [monograph on the Internet]. Cambridge (MA): Harvard Stem Cell Institute; 2008. Published 2009 Jun 30. Available from: https://www.ncbi.nlm.nih.gov/books/NBK27054/.
20. Joe AW, Yeung SN. Concise review: identifying limbal stem cells: classical concepts and new challenges. Stem Cells Transl Med 2014;3:318–22.
21. Doñate F, Raitano A, Morrison K, An Z, Capo L, Avina H, et al. AGS16F is a novel antibody drug conjugate directed against ENPP3 for the treatment of renal cell carcinoma. Clin Cancer Res 2016;22:1989–99.
22. Challita-Eid PM, Satpayev D, Yang P, An Z, Morrison K, Shostak Y, et al. Enfortumab vedotin antibody-drug conjugate targeting nectin-4 is a highly potent therapeutic agent in multiple preclinical cancer models. Cancer Res 2016;76:3003–13.
23. Mattie M, Raitano A, Morrison K, Morrison K, An Z, Capo L, et al. The discovery and preclinical development of ASG-5ME, an antibody-drug conjugate targeting SLC44A4-positive epithelial tumors including pancreatic and prostate cancer. Mol Cancer Ther 2016;15:2679–87.
24. Commisso C, Davidson SM, Soydaner-Azeloglu RG, Parker SJ, Kamphorst JJ, Hackett S, et al. Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells. Nature 2013;497:633–7.
25. Lim JP, Gleeson PA. Macropinocytosis: an endocytic pathway for inter-nalising large gulps. Immunol Cell Biol 2011;89:836–43.
26. Lloyd JB. Cell physiology of the rat visceral yolk sac: a study of pinocytosis and lysosome function. Teratology 1990;41:383–93.
27. Hawe A, Sutter M, Jiskoot W. Extrinsic fluorescent dyes as tools for protein characterization. Pharm Res 2008;25:1487–99.
28. Turecek PL, Bossard MJ, Schoetens F, Ivens IA. PEGylation of biopharma-ceuticals: a review of chemistry and nonclinical safety information of approved drugs. J Pharm Sci 2016;105:460–75.
29. Lyon RP, Bovee TD, Doronina SO, Burke PJ, Hunter JH, Neff-LaFord HD, et al. Reducing hydrophobicity of homogeneous antibody-drug conjugates improves pharmacokinetics and therapeutic index. Nat Biotechnol 2015; 33:733–5.
30. King HD, Dubowchik GM, Mastalerz H, Willner D, Hofstead SJ, Firestone RA, et al. Monoclonal antibody conjugates of doxorubicin prepared with branched peptide linkers: inhibition of aggregation by methoxytriethyle-neglycol chains. J Med Chem 2002;45:4336–43.
31. Igawa T, Tsunoda H, Tachibana T, Maeda A, Mimoto F, Moriyama C, et al. Reduced elimination of IgG antibodies by engineering the variable region. Protein Eng Des Sel 2010;23:385–92.
32. Wilson SL, Ahearne M, Hopkinson A. An overview of current techniques for ocular toxicity testing. Toxicology 2015;327:32–46.