Development and characterization of a preclinical ovarian carcinoma model to investigate the mechanism of acquired resistance to trastuzumab

International Journal of Oncology

Volumn 41, Issue 2, 2012, Pages 639-651

  Luistro, Leopoldo L ^a   Rosinski, James A ^a   Bian, Hongjin ^a   Bishayee, Subal ^b   Rameshwar, Pranela ^b   Ponzio, Nicholas M ^b   Ritland, Steve R ^a,c  

^a HOFFMANN LA ROCHE INC   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c CELGENE CORPORATION   (United States)

Author keywords

Acquired resistance; Herceptin; Human epidermal growth factor receptor 2; Microarray expression profiling; Mucin1; Ovarian cancer; Trastuzumab

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; MUCIN 1; TRASTUZUMAB;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MOUSE; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CARCINOMA; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; MUCIN-1; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARIAN NEOPLASMS; PROTEIN BINDING; RECEPTOR, ERBB-2; SEQUENCE ANALYSIS, DNA; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84863580775     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1463     Document Type: Article

References (47)

1. Alroy I and Yarden Y: The ErbB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. FEBS Lett 410: 83-86, 1997. (Pubitemid 27283389)
2. Olayioye MA, Neve RM, Lane HA and Hynes NE: The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J 19: 3159-3167, 2000. (Pubitemid 30428195)
3. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A, et al: Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancers. Science 244: 707-712, 1989. (Pubitemid 19147683)
4. Ross JS, Slodkowska EA, Symmans WF, Pusztai L, Ravdin PM and Hortobagyi GN: The HER-2 receptor and breast cancer: ten years of targeted anti-HER-2 therapy and personalized medicine. Oncologist 14: 320-368, 2009.
5. Dawood S, Broglio K, Buzdar AU, Hortobagyi GN and Giordano SH: Prognosis of women with metastatic breast cancer by HER2 status and trastuzumab treatment: an institutional-based review. J Clin Oncol 28: 92-98, 2010.
6. Bookman MA, Darcy KM, Clarke-Pearson D, Boothby RA and Horowitz IR: Evaluation of monoclonal anti-HER2 antibody, trastuzumab, in patients with recurrent or refractory ovarian or primary peritoneal carcinoma with overexpression of HER2: a phase II trial of the Gynecologic Oncology Group. J Clin Oncol 21: 283-290, 2003. (Pubitemid 46606157)
7. McAlpine JN, Wiegand KC, Vang R, Ronnett BM, Adamiak A, Köbel M, Kalloger SE, Swenerton KD, Huntsman DG, Gilks CB and Miller DM: HER2 overexpression and amplification is present in a subset of ovarian mucinous carcinomas and can be targeted with trastuzumab therapy. BMC Cancer 9: 433, 2009.
8. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M, Baselga J and Norton L: Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344: 783-792, 2001. (Pubitemid 32222155)
9. Cobleigh MA, Vogel CL, Tripathy D, Robert NJ, Scholl S, Fehrenbacher L, Wolter JM, Paton V, Shak S, Lieberman G and Slamon DJ: Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J Clin Oncol 17: 2639-2648, 1999. (Pubitemid 29415219)
10. Romond EH, Perez EA, Bryant J Suman VJ, Geyer CE Jr, Davidson NE, Tan-Chiu E, Martino S, Paik S, Kaufman PA, Swain SM, Pisansky TM, Fehrenbacher L, Kutteh LA, Vogel VG, Visscher DW, Yothers G, Jenkins RB, Brown AM, Dakhil SR, Mamounas EP, Lingle WL, Klein PM, Ingle JN and Wolmark N: Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med 353: 1673-1684, 2005.
11. Perez EA, Romond EH, Suman VJ, Jeong JH, Davidson NE, Geyer CE Jr, Martino S, Mamounas EP, Kaufman PA and Wolmark N: Four-year follow-up of trastuzumab plus adjuvant chemotherapy for operable human epidermal growth factor receptor 2-positive breast cancer: joint analysis of data from NCCTG N9831 and NSABP B-31. J Clin Oncol 29: 3366-3373, 2011.
12. Smith I, Procter M, Gelber RD, Guillaume S, Feyereislova A, Dowsett M, Goldhirsch A, Untch M, Mariani G, Baselga J, Kaufmann M, Cameron D, Bell R, Bergh J, Coleman R, Wardley A, Harbeck N, Lopez RI, Mallmann P, Gelmon K, Wilcken N, Wist E, Sánchez Rovira P and Piccart-Gebhart MJ: 2-year follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer: a randomised controlled trial. Lancet 369: 29-36, 2007. (Pubitemid 46039831)
13. Slamon D, Eiermann W, Robert N, Pienkowski T, Martin M, Press M, Mackey J, Glaspy J, Chan A, Pawlicki M, Pinter T, Valero V, Liu MC, Sauter G, von Minckwitz G, Visco F, Bee V, Buyse M, Bendahmane B, Tabah-Fisch I, Lindsay MA, Riva A and Crown J: Adjuvant trastuzumab in HER2-positive breast cancer. N Engl J Med 365: 1273-1283, 2011.
14. Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, Lordick F, Ohtsu A, Omuro Y, Satoh T, Aprile G, Kulikov E, Hill J, Lehle M, Rüschoff J and Kang YK: 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. Lancet 376: 687-697, 2010.
15. Spector NL and Blackwell KL: Understanding the mechanisms behind trastuzumab therapy for human epidermal growth factor receptor 2-positive breast cancer. J Clin Oncol 27: 5838-5847, 2009.
16. Albanell J and Baselga J: Unraveling resistance to trastuzumab (Herceptin): insulin-like growth factor-I receptor, a new suspect. J Natl Cancer Inst 93: 1830-1832, 2001. (Pubitemid 34048643)
17. Nahta R, Takahashi T, Ueno NT, Hung MC and Esteva FJ: p27Kip1 down-regulation is associated with trastuzumab resistance in breast cancer cells. Cancer Res 64: 3981-3986, 2004. (Pubitemid 38697313)
18. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA, Klos KS, Li P, Monia BP, Nguyen NT, Hortobagyi GN, Hung MC and Yu D: PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6: 117-127, 2004. (Pubitemid 39485684)
19. Nagy P, Friedländer E, Tanner M, Kapanen AI, Carraway KL, Isola J and Jovin TM: Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a Herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 65: 473-482, 2005.
20. Dhillon J, Astanehe A, Lee C, Fotovati A, Hu K and Dunn SE: The expression of activated Y-box binding protein-1 serine 102 mediates trastuzumab resistance in breast cancer cells by increasing CD44+ cells. Oncogene 29: 6294-6300, 2010.
21. Zhang S, Huang WC, Li P, Guo H, Poh SB, Brady SW, Xiong Y, Tseng LM, Li SH, Ding Z, Sahin AA, Esteva FJ, Hortobagyi GN and Yu D: Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat Med 17: 461-469, 2011.
22. Fernandes H, Cohen S and Bishayee S: Glycosylation-induced conformational modification positively regulates receptor-receptor association: a study with an aberrant epidermal growth factor receptor (EGFRvIII/DeltaEGFR) expressed in cancer cells. J Biol Chem 276: 5375-5383, 2001.
23. Meric F, Lee WP, Sahin A, Zhang H, Kung HJ and Hung MC: Expression profile of tyrosine kinases in breast cancer. Clin Cancer Res 8: 361-367, 2002. (Pubitemid 34193951)
24. Unger MA, Rishi M, Clemmer VB, Hartman JL, Keiper EA, Greshock JD, Chodosh LA, Liebman MN and Weber BL: Characterization of adjacent breast tumors using oligonucleotide microarrays. Breast Cancer Res 3: 336-341, 2001. (Pubitemid 32851165)
25. Raponi M, Belly RT, Karp JE, Lancet JE, Atkins D and Wang Y: Microarray analysis reveals genetic pathways modulated by tipifarnib in acute myeloid leukemia. BMC Cancer 4: 56, 2004.
26. Sliwkowski MX, Lofgren JA, Lewis GD, Hotaling TE, Fendly BM and Fox JA: Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin). Semin Oncol 26 (Suppl): 60-70, 1999. (Pubitemid 29411434)
27. Schroeder JA, Thompson MC, Gardner MM and Gendler SJ: Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J Biol Chem 276: 13057-13064, 2001.
28. Nielsen DL, Andersson M and Kamby C: HER2-targeted therapy in breast cancer. Monoclonal antibodies and tyrosine kinase inhibitors. Cancer Treat Rev 35: 121-136, 2009.
29. du Manoir JM, Francia G, Man S, Mossoba M, Medin JA, Viloria-Petit A, Hicklin DJ, Emmenegger U and Kerbel RS: Strategies for delaying or treating in vivo acquired resistance to trastuzumab in human breast cancer xenografts. Clin Cancer Res 12: 904-916, 2006. (Pubitemid 43259873)
30. Fessler SP, Wotkowicz MT, Mahanta SK and Bamdad C: MUC1*is a determinant of trastuzumab (Herceptin) resistance in breast cancer cells. Breast Cancer Res Treat 118: 113-124, 2009.
31. Valabrega G, Capellero S, Cavalloni G, Zaccarello G, Petrelli A, Migliardi G, Milani A, Peraldo-Neia C, Gammaitoni L, Sapino A, Pecchioni C, Moggio A, Giordano S, Aglietta M and Montemurro F: HER2-positive breast cancer cells resistant to trastuzumab and lapatinib lose reliance upon HER2 and are sensitive to the multitargeted kinase inhibitor sorafenib. Breast Cancer Res Treat 130: 29-40, 2011.
32. Ramanathan RK, Hwang JJ, Zamboni WC, Sinicrope FA, Safran H, Wong MK, Earle M, Brufsky A, Evans T, Troetschel M, Walko C, Day R, Chen HX and Finkelstein S: Low overexpression of HER-2/neu in advanced colorectal cancer limits the usefulness of trastuzumab (Herceptin) and irinotecan as therapy. A phase II trial. Cancer Invest 22: 858-865, 2004. (Pubitemid 39665350)
33. Pietras RJ, Fendly BM, Chazin VR, Pegram MD, Howell SB and Slamon DJ: Antibody to HER-2/neu receptor blocks DNA repair after cisplatin in human breast and ovarian cells. Oncogene 9: 1829-1838, 1994. (Pubitemid 24194147)
34. Ritter CA, Bianco R, Dugger T, Forbes J, Qu S, Rinehart C, King W and Arteaga CL: Mechanisms of resistance development against trastuzumab (Herceptin) in an in vivo breast cancer model. Int J Clin Pharmacol Ther 42: 642-643, 2004.
35. O'Brien NA, Browne BC, Chow L, Wang Y, Ginther C, Arboleda J, Duffy MJ, Crown J, O'Donovan N and Slamon DJ: Activated phosphoinositide 3-kinase/AKT signaling confers resistance to trastuzumab but not lapatinib. Mol Cancer Ther 9: 1489-1502, 2010.
36. Scheuer W, Freiss T, Burtscher H, Bossenmaier B, Endl J and Hasmann M: Strongly enhanced antitumor activity of trastuzumab and pertuzumab combination treatment on HER2-positive human xenograft tumor models. Cancer Res 69: 9330-9336, 2009.
37. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, Slamon DJ, Murphy M, Novotny WF, Burchmore M, Shak S, Stewart SJ and Press M: Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 20: 719-726, 2002. (Pubitemid 34111379)
38. low breast cancer stem cells. Cancer Res 69: 8058-8066, 2009.
39. Packer LM, Williams SJ, Callaghan S, Gotley DC and McGuckin MA: Expression of the cell surface mucin gene family in adenocarcinomas. Int J Oncol 25: 1119-1126, 2004.
40. Scibetta AG, Albanese I, Morris J, Cooper L, Downward J, Rowe P and Taylor-Papadimitriou J: Regulation of MUC1 expression in human mammary cell lines by the c-ErbB2 and ras signaling pathways. DNA Cell Biol 20: 265-274, 2001. (Pubitemid 32692444)
41. Hollingsworth MA and Swanson BJ: Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 4: 45-60, 2004. (Pubitemid 38082153)
42. Li Y, Kuwahara H, Ren J, Wen G and Kufe D: The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3 beta and beta-catenin. J Biol Chem 276: 6061-6064, 2001.
43. Baselga J, Gelmon KA, Verma S, Wardley A, Conte P, Miles D, Bianchi G, Cortes J, McNally VA, Ross GA, Fumoleau P and Gianni L: Phase II trial of pertuzumab and trastuzumab in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer that progressed during prior trastuzumab therapy. J Clin Oncol 28: 1138-1144, 2010.
44. Krop IE, LoRusso O, Miller KD, Modi S, Yardley D, Rodriguez G, Lu M, Burrington B, Agresta S and Rugo H: A phase 2 study of the HER2 antibody-drug conjugate trastuzumab-DM1 (TDM-1) in patients (PTS) with HER2-positive metastatic breast cancer (MBC) previously treated with trastuzumab, lapatinib, and chemotherapy [abstract 2770]. Ann Oncol 21 (Suppl 8): viii97, 2010.
45. Burris HA III, Rugo HS, Vukelja SJ, Vogel CL, Borson RA, Limentani S, Tan-Chiu E, Krop IE, Michaelson RA, Girish S, Amler L, Zheng M, Chu YW, Klencke B and O'Shaughnessy JA: Phase II study of the antibody drug conjugate trastuzumab-DM1 for the treatment of human epidermal growth factor receptor 2 (HER2)-positive breast cancer after prior HER2-directed therapy. J Clin Oncol 29: 398-405, 2011.
46. Konecny GE, Pegram MD, Venkatesan N, Finn R, Yang G, Rahmeh M, Untch M, Rusnak DW, Spehar G, Mullin RJ, Keith BR, Gilmer TM, Berger M, Podratz KC, Slamon DJ: Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer Res 66: 1630-1639, 2006. (Pubitemid 43259947)
47. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, Jagiello-Gruszfeld A, Crown J, Chan A, Kaufman B, Skarlos D, Campone M, Davidson N, Berger M, Oliva C, Rubin SD, Stein S and Cameron D: Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 355: 2733-2743, 2006. (Pubitemid 46021510)