Aberrant intracellular metabolism of T-DM1 confers T-DM1 resistance in human epidermal growth factor receptor 2-positive gastric cancer cells

Cancer Science

Volumn 108, Issue 7, 2017, Pages 1458-1468

  Wang, Hongbin ^a,b   Wang, Wenqian ^a   Xu, Yongping ^a   Yang, Yong ^a   Chen, Xiaoyan ^a   Quan, Haitian ^a   Lou, Liguang ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Antibody drug conjugate; drug resistance; HER2; T DM1; V ATPase

Indexed keywords

ANTINEOPLASTIC AGENT; BAFILOMYCIN A1; BETA ACTIN; BETA TUBULIN; DRUG METABOLITE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GELDANAMYCIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HERTUZUMAB VC MONOMETHYL AURISTATIN E; LAPATINIB; LYSINE MCC DM1; MERTANSINE; MONOCLONAL ANTIBODY; NERATINIB; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRASTUZUMAB; TRASTUZUMAB EMTANSINE; UNCLASSIFIED DRUG; VINORELBINE TARTRATE; ANTIBODY CONJUGATE; ERBB2 PROTEIN, HUMAN; MAYTANSINE;

ACIDIFICATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CELL TRANSPORT; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG METABOLISM; DRUG POTENCY; DRUG PROTEIN BINDING; ENDOCYTOSIS; ENZYME ACTIVITY; EXTERNALIZATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GASTRIC CANCER CELL LINE; HUMAN; IC50; IN VITRO STUDY; INTERNALIZATION; LYSOSOME; M PHASE CELL CYCLE CHECKPOINT; MICROTUBULE ASSEMBLY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH CANCER; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; DRUG RESISTANCE; DRUG SCREENING; FLUORESCENCE MICROSCOPY; METABOLISM; NUDE MOUSE; PHYSIOLOGY; STOMACH TUMOR; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; HUMANS; IMMUNOCONJUGATES; MAYTANSINE; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; RECEPTOR, ERBB-2; STOMACH NEOPLASMS; VACUOLAR PROTON-TRANSLOCATING ATPASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85019568716     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.13253     Document Type: Article

References (51)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. Ca-Cancer J Clin 2005; 55: 74–108.
2. Van Cutsem E, Sagaert X, Topal B, Haustermans K, Prenen H. Gastric cancer. The Lancet 2016; 388: 2654–64.
3. Szász AM, Lánczky A, Nagy Á et al. Cross-validation of survival associated biomarkers in gastric cancer using transcriptomic data of 1,065 patients. Oncotarget. 2016; 7: 49322–33.
4. Hofmann M, Stoss O, Shi D et al. Assessment of a HER2 scoring system for gastric cancer: results from a validation study. Histopathology 2008; 52: 797–805.
5. Bang Y-J, Van Cutsem E, Feyereislova A et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. The Lancet 2010; 376: 687–97.
6. Barok M, Joensuu H, Isola J. Trastuzumab emtansine: mechanisms of action and drug resistance. Breast Cancer Res 2014; 16: 209.
7. Nolting B. Linker technologies for antibody–drug conjugates. Antibody-Drug Conjugates 2013; 1045: 71–100.
8. Lewis Phillips GD, Li G, Dugger DL et al. Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody-cytotoxic drug conjugate. Cancer Res 2008; 68: 9280–90.
9. Erickson HK, Park PU, Widdison WC 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.
10. Polakis P. Antibody drug conjugates for cancer therapy. Pharmacol Rev 2016; 68: 3–19.
11. Saftig P. Lysosomes. New York: Landes Bioscience/Eurekah. Springer Science + Business Media, 2005.
12. Verma S, Miles D, Gianni L et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. New Engl J Med 2012; 367: 1783–91.
13. Hurvitz SA, Dirix L, Kocsis J et al. Phase II randomized study of trastuzumab emtansine versus trastuzumab plus docetaxel in patients with human epidermal growth factor receptor 2–positive metastatic breast cancer. J Clin Oncol 2013; 31: 2977.
14. Wildiers H, Kim S, Gonzalez-Martin A et al. T-DM1 for HER2-positive metastatic breast cancer (MBC): Primary results from TH3RESA, a phase 3 study of T-DM1 vs treatment of physician's choice. Eur J Cancer Elsevier Sci Ltd The Boulevard, Langford Lane, Kidlington, Oxford Ox5 1Gb, Oxon, England, 2013; S7–8.
15. Okines AF, Cunningham D. Trastuzumab in gastric cancer. Eur J Cancer 2010; 46: 1949–59.
16. Wang W, Liu Y, Zhao Z et al. Y-632 inhibits heat shock protein 90 (Hsp90) function by disrupting the interaction between Hsp90 and Hsp70/Hsp90 organizing protein, and exerts antitumor activity in vitro and in vivo. Cancer Sci 2016; 107: 782–90.
17. Wang Q, Quan H, Zhao J, Xie C, Wang L, Lou L. RON confers lapatinib resistance in HER2-positive breast cancer cells. Cancer Lett 2013; 340: 43–50.
18. Quan H, Liu H, Li C, Lou L. 1,4-Diamino-2,3-dicyano-1,4-bis (methylthio) butadiene (U0126) Enhances the Cytotoxicity of Combretastatin A4 Independently of Mitogen-Activated Protein Kinase Kinase. J Pharmacol Exp Ther 2009; 330: 326–33.
19. Austin CD, De Mazière AM, Pisacane PI et al. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin. Mol Biol Cell 2004; 15: 5268–82.
20. Oroudjev E, Lopus M, Wilson L et al. Maytansinoid-antibody conjugates induce mitotic arrest by suppressing microtubule dynamic instability. Mol Cancer Ther 2010; 9: 2700–13.
21. Erickson HK, Widdison WC, Mayo MF et al. Tumor delivery and in vivo processing of disulfide-linked and thioether-linked antibody-maytansinoid conjugates. Bioconjugate Chem 2010; 21: 84–92.
22. Erickson HK, Lewis Phillips GD, Leipold DD 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.
23. Rock BM, Tometsko ME, Patel SK, Hamblett KJ, Fanslow WC, Rock DA. Intracellular catabolism of an antibody drug conjugate with a noncleavable linker. Drug Metab Disps 2015; 43: 1341–4.
24. Zelenin A. Acridine orange as a probe for molecular and cell biology. Fluorescent and Luminescent Probes for Biological Activity. Academic Press, London, 1993, pp. 83–99.
25. Jiang J, Dong L, Wang L et al. HER2-targeted antibody drug conjugates for ovarian cancer therapy. Eur J Pharm Sci 2016; 93: 274–86.
26. Lin K, Tibbitts J, Shen BQ. Pharmacokinetics and ADME characterizations of antibody-drug conjugates. Methods Mol Biol 2013; 1045: 117–31.
27. Wakankar A, Chen Y, Gokarn Y, Jacobson FS. Analytical methods for physicochemical characterization of antibody drug conjugates. MAbs-Austin 2011; 3: 161–72.
28. Narayan M, Wilken JA, Harris LN, Baron AT, Kimbler K, Maihle NJ. Trastuzumab-Induced HER reprogramming in “Resistant” breast carcinoma cells. Cancer Res 2009; 69: 2191–4.
29. Xiao Z, Carrasco RA, Schifferli K et al. A potent HER3 monoclonal antibody that blocks both ligand-dependent and-independent activities: differential impacts of PTEN status on tumor response. Mol Cancer Ther 2016; 15: 689–701.
30. Wicki A, Mandalà M, Massi D et al. Acquired resistance to clinical cancer therapy: a twist in physiological signaling. Physiol Rev 2016; 96: 805–29.
31. Zhang L, Zhang S, Yao J et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature 2015; 527: 100–4.
32. Miekus K. The Met tyrosine kinase receptor as a therapeutic target and a potential cancer stem cell factor responsible for therapy resistance (Review). Oncol Rep 2017; 37: 647–56.
33. Ebbesen SH, Scaltriti M, Bialucha CU et al. Pten loss promotes MAPK pathway dependency in HER2/neu breast carcinomas. P Natl Acad Sci 2016; 113: 3030–5.
34. Chan CTO, Metz MZ, Kane SE. Differential sensitivities of trastuzumab (Herceptin)-resistant human breast cancer cells to phosphoinositide-3 kinase (PI-3K) and epidermal growth factor receptor (EGFR) kinase inhibitors. Breast Cancer Res Tr 2005; 91: 187–201.
35. Yakes FM, Chinratanalab W, Ritter CA, King W, Seelig SA, Arteaga CL. Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt is required for antibody-mediated effects on p27, Cyclin D1, and antitumor action. Cancer Res 2002; 62: 4132–41.
36. Le X, Claret F, Lammayot A et al. The role of cyclin-dependent kinase inhibitor p27Kip1 in anti-HER2 antibody-induced G1 cell cycle arrest and tumor growth inhibition. J Biol Chem 2003; 278: 23441–50.
37. Nahta R, Takahashi T, Ueno NT, Hung M, Esteva FJ. P27kip1 down-regulation is associated with trastuzumab resistance in breast cancer cells. Cancer Res 2004; 64: 3981–6.
38. Nagy P, Friedlander E, Tanner M et al. Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a Herceptin-Resistant, MUC4-Expressing breast cancer cell line. Cancer Res 2005; 65: 473–82.
39. Priceschiavi SA, Jepson S, Li P et al. Rat Muc4 (sialomucin complex) reduces binding of anti-ErbB2 antibodies to tumor cell surfaces, a potential mechanism for herceptin resistance. Int J Cancer 2002; 99: 783–91.
40. Osipo C, Patel P, Rizzo P et al. ErbB-2 inhibition activates Notch-1 and sensitizes breast cancer cells to a gamma-secretase inhibitor. Oncogene 2008; 27: 5019.
41. Yu S-F, Zheng B, Go M et al. A novel anti-CD22 anthracycline-based antibody–drug conjugate (ADC) that overcomes resistance to auristatin-based ADCs. Clin Cancer Res 2015; 21: 3298–306.
42. Stavrovskaya AA, Stromskaya TP. Transport proteins of the ABC family and multidrug resistance of tumor cells. Biochemistry-Us 2008; 73: 592–604.
43. Kovtun YV, Audette CA, Mayo MF et al. Antibody-maytansinoid conjugates designed to bypass multidrug resistance. Cancer Res 2010; 70: 2528–37.
44. Drukman S, Kavallaris M. Microtubule alterations and resistance to tubulin-binding agents (review). Int J Oncol 2002; 21: 621–8.
45. Rai A, Kapoor S, Naaz A, Santra MK, Panda D. Enhanced stability of microtubules contributes in the development of colchicine resistance in MCF-7 cells. Biochem Pharmacol 2017; 132: 38–47.
46. Sauveur J, Chettab A, Cleret A, Savina A, Dumontet C. Mechanisms of resistance to trastuzumab emtansine in gastric cancer. Cancer Res 2016; 76: 309.
47. Loganzo F, Tan X, Sung M et al. Tumor cells chronically treated with a Trastuzumab–Maytansinoid Antibody-Drug conjugate develop varied resistance mechanisms but respond to alternate treatments. Mol Cancer Ther 2015; 14: 952–63.
48. Lewis Phillips G. Mechanisms of acquired resistance to trastuzumab emtansine (T-DM1). Presented at: World ADC Summit 2011; San Francisco, CA: London, UK: HansonWade; 2011. Google Scholar
49. Sung MS, Tan X, Hosselet C et al. Caveolae-mediated endocytosis as a novel mechanism of resistance to T-DM1 ADC. Cancer Res 2016; 76: 2113.
50. Doronina SO, Mendelsohn BA, Bovee TD et al. Enhanced activity of monomethylauristatin F through monoclonal antibody delivery: effects of linker technology on efficacy and toxicity. Bioconjugate Chem 2006; 17: 114–24.
51. Zhitomirsky B, Assaraf YG. Lysosomes as mediators of drug resistance in cancer. Drug Resist Update 2016; 24: 23–33.