Synergistic antitumor activity of lapatinib and retinoids on a novel subtype of breast cancer with coamplification of ERBB2 and RARA

Oncogene

Volumn 31, Issue 29, 2012, Pages 3431-3443

  Paroni, G ^a   Fratelli, M ^a   Gardini, G ^b   Bassano, C ^b   Flora, M ^b   Zanetti, A ^a   Guarnaccia, V ^a   Ubezio, P ^a   Centritto, F ^a   Terao, M ^a   Garattini, E ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b S MARIA NUOVA HOSPITAL   (Italy)

Author keywords

apoptosis; differentiation; HER2 neu; lapatinib; retinoic acid; targeted therapy

Indexed keywords

CELL PROTEIN; LAPATINIB; PROTEIN BIRC5; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID; SMAD3 PROTEIN; TRANSCRIPTION FACTOR FKHRL1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER INHIBITION; CELL DIFFERENTIATION; DRUG POTENTIATION; EPIDERMAL GROWTH FACTOR RECEPTOR 2 GENE; GENE; GENE AMPLIFICATION; GENE EXPRESSION; GENE PRODUCT; GENETIC ANALYSIS; MOLECULAR DYNAMICS; PHOSPHORYLATION; PRIORITY JOURNAL; RETINOIC ACID RECEPTOR ALPHA GENE; SENSITIVITY ANALYSIS; UPREGULATION;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG SYNERGISM; FORKHEAD TRANSCRIPTION FACTORS; GENE AMPLIFICATION; HUMANS; PHOSPHORYLATION; QUINAZOLINES; RECEPTOR, ERBB-2; RECEPTORS, RETINOIC ACID; SMAD3 PROTEIN; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; TRETINOIN;

EID: 84864141638     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.506     Document Type: Article

References (56)

1. Abramson V, Arteaga CL. (2011). New strategies in HER2-overexpressing breast cancer: many combinations of targeted drugs available. Clin Cancer Res 17: 952-958.
2. Afonja O, Juste D, Das S, Matsuhashi S, Samuels HH. (2004). Induction of PDCD4 tumor suppressor gene expression by RAR agonists, antiestrogen and HER-2/neu antagonist in breast cancer cells. Evidence for a role in apoptosis. Oncogene 23: 8135-8145. (Pubitemid 39531854)
3. Aryee MJ, Gutierrez-Pabello JA, Kramnik I, Maiti T, Quackenbush J. (2009). An improved empirical bayes approach to estimating differential gene expression in microarray time-course data: BETR (Bayesian Estimation of Temporal Regulation). BMC Bioinformatics 10: 409.
4. Balmer JE, Blomhoff R. (2002). Gene expression regulation by retinoic acid. J Lipid Res 43: 1773-1808. (Pubitemid 35315797)
5. Balmer JE, Blomhoff R. (2005). A robust characterization of retinoic acid response elements based on a comparison of sites in three species. J Steroid Biochem Mol Biol 96: 347-354. (Pubitemid 41384136)
6. Barral PM, Sarkar D, Su ZZ, Barber GN, DeSalle R, Racaniello VR et al. (2009). Functions of the cytoplasmic RNA sensors RIG-I and MDA-5: key regulators of innate immunity. Pharmacol Ther 124: 219-234.
7. Baselga J. (2006). Targeting tyrosine kinases in cancer: the second wave. Science 312: 1175-1178. (Pubitemid 43801135)
8. Baselga J, Swain SM. (2009). Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 9: 463-475.
9. Buck MB, Knabbe C. (2006). TGF-beta signaling in breast cancer. Ann NY Acad Sci 1089: 119-126. (Pubitemid 47092079)
10. Chambon P. (1996). A decade of molecular biology of retinoic acid receptors. FASEB J 10: 940-954. (Pubitemid 26285969)
11. Colombo V, Lupi M, Falcetta F, Forestieri D, Incalci M, Ubezio P. (2011). Chemotherapeutic activity of silymarin combined with doxorubicin or paclitaxel in sensitive and multidrug-resistant colon cancer cells. Cancer Chemother Pharmacol 67: 369-379.
12. Danforth Jr DN. (2004). All trans-retinoic acid acts synergistically with hydroxytamoxifen and transforming-growth factor beta to stimulate apoptosis in MCF-7 breast cancer cells. J Endocrinol 183: 395-404. (Pubitemid 39562719)
13. Decensi A, Bonanni B, Guerrieri-Gonzaga A, Torrisi R, Manetti L, Robertson C et al. (2000). Chemoprevention of breast cancer: the Italian experience. J Cell Biochem Suppl 34: 84-96. (Pubitemid 30176738)
14. Dokmanovic M, Chang BD, Fang J, Roninson IB. (2002). Retinoidinduced growth arrest of breast carcinoma cells involves coactivation of multiple growth-inhibitory genes. Cancer Biol Ther 1: 24-27.
15. Dusek RL, Attardi LD. (2011). Desmosomes: new perpetrators in tumour suppression. Nat Rev Cancer 11: 317-323.
16. Esteva FJ, Yu D, Hung MC, Hortobagyi GN. (2010). Molecular predictors of response to trastuzumab and lapatinib in breast cancer. Nat Rev Clin Oncol 7: 98-107.
17. Fitzgerald P, Teng M, Chandraratna RA, Heyman RA, Allegretto EA. (1997). Retinoic acid receptor alpha expression correlates with retinoid-induced growth inhibition of human breast cancer cells regardless of estrogen receptor status. Cancer Res 57: 2642-2650. (Pubitemid 27283774)
18. Garattini E, Gianni M, Terao M. (2007). Retinoids as differentiating agents in oncology: a network of interactions with intracellular pathways as the basis for rational therapeutic combinations. Curr Pharm Des 13: 1375-1400. (Pubitemid 46758854)
19. Garattini E, Parrella E, Diomede L, Gianni M, Kalac Y, Merlini L et al. (2004). ST1926, a novel and orally active retinoid-related molecule inducing apoptosis in myeloid leukemia cells: modulation of intracellular calcium homeostasis. Blood 103: 194-207. (Pubitemid 38029939)
20. Gianni M, Boldetti A, Guarnaccia V, Rambaldi A, Parrella E, Raska Jr I et al. (2009). Inhibition of the peptidyl-prolyl-isomerase Pin1 enhances the responses of acute myeloid leukemia cells to retinoic acid via stabilization of RARalpha and PML-RARalpha. Cancer Res 69: 1016-1026.
21. Gianni M, Li Calzi M, Terao M, Guiso G, Caccia S, Barbui T et al. (1996a). AM580, a stable benzoic derivative of retinoic acid, has powerful and selective cyto-differentiating effects on acute promyelocytic leukemia cells. Blood 87: 1520-1531. (Pubitemid 26056917)
22. Gianni M, Terao M, Gambacorti-Passerini C, Rambaldi A, Garattini E. (1996b). Effects of 1,25-dihydroxy vitamin D3 on all-trans retinoic acid sensitive and resistant acute promyelocytic leukemia cells. Biochem Biophys Res Commun 224: 50-56. (Pubitemid 26252410)
23. Gianni M, Zanotta S, Terao M, Garattini S, Garattini E. (1993). Effects of synthetic retinoids and retinoic acid isomers on the expression of alkaline phosphatase in F9 teratocarcinoma cells. Biochem Biophys Res Commun 196: 252-259. (Pubitemid 23309501)
24. Guha M, Plescia J, Leav I, Li J, Languino LR, Altieri DC. (2009). Endogenous tumor suppression mediated by PTEN involves survivin gene silencing. Cancer Res 69: 4954-4958.
25. Huang SL, Shyu RY, Yeh MY, Jiang SY. (2000). Cloning and characterization of a novel retinoid-inducible gene 1 (RIG1) deriving from human gastric cancer cells. Mol Cell Endocrinol 159: 15-24.
26. Hudis CA. (2007). Trastuzumab-mechanism of action and use in clinical practice. N Engl J Med 357: 39-51. (Pubitemid 47026733)
27. Kastner P, Mark M, Chambon P. (1995). Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83: 859-869. (Pubitemid 26006528)
28. Koay DC, Zerillo C, Narayan M, Harris LN, DiGiovanna MP. (2010). Anti-tumor effects of retinoids combined with trastuzumab or tamoxifen in breast cancer cells: induction of apoptosis by retinoid/trastuzumab combinations. Breast Cancer Res 12: R62.
29. Lupi M, Matera G, Branduardi D, Incalci M, Ubezio P. (2004). Cytostatic and cytotoxic effects of topotecan decoded by a novel mathematical simulation approach. Cancer Res 64: 2825-2832. (Pubitemid 38500621)
30. Mariani G, Fasolo A, De Benedictis E, Gianni L. (2009). Trastuzumab as adjuvant systemic therapy for HER2-positive breast cancer. Nat Clin Pract Oncol 6: 93-104.
31. McEarchern JA, Kobie JJ, Mack V, Wu RS, Meade-Tollin L, Arteaga CL et al. (2001). Invasion and metastasis of a mammary tumor involves TGF-beta signaling. Int J Cancer 91: 76-82.
32. Moreira C, Kaklamani V. (2010). Lapatinib and breast cancer: current indications and outlook for the future. Expert Rev Anticancer Ther 10: 1171-1182.
33. Mucida D, Cheroutre H. (2007). TGFbeta and retinoic acid intersect in immune-regulation. Cell Adhes Migr 1: 142-144.
34. Mueller E, Sarraf P, Tontonoz P, Evans RM, Martin KJ, Zhang M et al. (1998). Terminal differentiation of human breast cancer through PPAR gamma. Mol Cell 1: 465-470. (Pubitemid 128378895)
35. Ou CC, Hsu SC, Hsieh YH, Tsou WL, Chuang TC, Liu JY et al. (2008). Downregulation of HER2 by RIG1 involves the PI3K/Akt pathway in ovarian cancer cells. Carcinogenesis 29: 299-306.
36. Paik J, Blaner WS, Sommer KM, Moe R, Swisshlem K. (2003). Retinoids, retinoic acid receptors and breast cancer. Cancer Invest 21: 304-312. (Pubitemid 36532175)
37. Paroni G, Brancolini C. (2011). Measurement of caspase activity: from cell populations to individual cells. Methods Mol Biol 740: 65-79.
38. Puntoni M, Decensi A. (2009). The rationale and potential of cancer chemoprevention with special emphasis on breast cancer. Eur J Cancer 45 (Suppl 1): 346-354.
39. Roman SD, Ormandy CJ, Manning DL, Blamey RW, Nicholson RI, Sutherland RL et al. (1993). Estradiol induction of retinoic acid receptors in human breast cancer cells. Cancer Res 53: 5940-5945. (Pubitemid 24006164)
40. Rubin I, Yarden Y. (2001). The basic biology of HER2. Ann Oncol 12 (Suppl 1): S3-S8. (Pubitemid 32750577)
41. Sheikh MS, Shao ZM, Chen JC, Hussain A, Jetten AM, Fontana JA. (1993). Estrogen receptor-negative breast cancer cells transfected with the estrogen receptor exhibit increased RAR alpha gene expression and sensitivity to growth inhibition by retinoic acid. J Cell Biochem 53: 394-404. (Pubitemid 24043038)
42. Shyu RY, Chang SC, Yu JC, Hsu SJ, Chou JM, Lee MS et al. (2005). Expression and regulation of retinoid-inducible gene 1 (RIG1) in breast cancer. Anticancer Res 25: 2453-2460.
43. Srinivas H, Xia D, Moore NL, Uray IP, Kim H, Ma L et al. (2006). Akt phosphorylates and suppresses the transactivation of retinoic acid receptor alpha. Biochem J 395: 653-662.
44. Sturniolo MT, Dashti SR, Deucher A, Rorke EA, Broome AM, Chandraratna RA et al. (2003). A novel tumor suppressor protein promotes keratinocyte terminal differentiation via activation of type I transglutaminase. J Biol Chem 278: 48066-48073. (Pubitemid 37523257)
45. Sun G, Porter W, Safe S. (1998). Estrogen-induced retinoic acid receptor alpha 1 gene expression: role of estrogen receptor-Sp1 complex. Mol Endocrinol 12: 882-890. (Pubitemid 30659061)
46. Tan AR, Alexe G, Reiss M. (2009). Transforming growth factor-beta signaling: emerging stem cell target in metastatic breast cancer? Breast Cancer Res Treat 115: 453-495.
47. Terao M, Fratelli M, Kurosaki M, Zanetti A, Guarnaccia V, Paroni G et al. (2011). Induction of miR-21 by retinoic acid in estrogen receptor-positive breast carcinoma cells: biological correlates and molecular targets. J Biol Chem 286: 4027-4042.
48. Tsai FM, Shyu RY, Jiang SY. (2007). RIG1 suppresses Ras activation and induces cellular apoptosis at the Golgi apparatus. Cell Signal 19: 989-999.
49. Tsai FM, Shyu RY, Lin SC, Wu CC, Jiang SY. (2009). Induction of apoptosis by the retinoid inducible growth regulator RIG1 depends on the NC motif in HtTA cervical cancer cells. BMC Cell Biol 10: 15.
50. Wang Y, He QY, Chen H, Chiu JF. (2007). Synergistic effects of retinoic acid and tamoxifen on human breast cancer cells: proteomic characterization. Exp Cell Res 313: 357-368. (Pubitemid 46048821)
51. + regulatory T cells and inhibits development of Th17 cells by enhancing TGF-beta-driven Smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J Immunol 181: 2277-2284.
52. Yang J, Song K, Krebs TL, Jackson MW, Danielpour D. (2008a). Rb/E2F4 and Smad2/3 link survivin to TGF-beta-induced apoptosis and tumor progression. Oncogene 27: 5326-5338.
53. Yang JY, HungMC. (2009). A new fork for clinical application: targeting forkhead transcription factors in cancer. Clin Cancer Res 15: 752-757.
54. Yang Q, Sakurai T, Kakudo K. (2002). Retinoid, retinoic acid receptor beta and breast cancer. Breast cancer Res Treat 76: 167-173. (Pubitemid 35252494)
55. + myeloid cells that promote metastasis. Cancer Cell 13: 23-35. (Pubitemid 350309741)
56. Zujewski J, Vaughn-Cooke A, Flanders KC, Eckhaus MA, Lubet RA, Wakefield LM. (2001). Transforming growth factors-beta are not good biomarkers of chemopreventive efficacy in a preclinical breast cancer model system. Breast Cancer Res 3: 66-75. (Pubitemid 32223656)