Ret inhibition decreases growth and metastatic potential of estrogen receptor positive breast cancer cells

EMBO Molecular Medicine

Volumn 5, Issue 9, 2013, Pages 1335-1350

  Gattelli, Albana ^a   Nalvarte, Ivan ^a   Boulay, Anne ^a,h   Roloff, Tim C ^a   Schreiber, Martin ^b   Carragher, Neil ^c   Macleod, Kenneth K ^c   Schlederer, Michaela ^d   Lienhard, Susanne ^a   Kenner, Lukas ^d,e   Torres Arzayus, Maria I ^f   Hynes, Nancy E ^a,g  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIV KLIN FÜR FRAUENHEILKUNDE   (Austria)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d Ludwig Boltzmann Institute for Cancer Research (LBI CR)   (Australia)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

^f DANA FARBER CANCER INSTITUTE   (United States)

^g UNIVERSITY OF BASEL   (Switzerland)

^h F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Endocrine therapy; Fak; IL6; Metastasis; Ret

Indexed keywords

ANTINEOPLASTIC AGENT; ESTROGEN RECEPTOR; FULVESTRANT; INTERLEUKIN 6; NVP AST 487; PROTEIN RET; TAMOXIFEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST METASTASIS; CANCER CELL; CANCER HORMONE THERAPY; CANCER INHIBITION; CELL MIGRATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

ENDOCRINE-THERAPY; FAK; IL6; METASTASIS; RET;

ANIMALS; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INTERLEUKIN-6; MICE; MICROARRAY ANALYSIS; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS C-RET; RECEPTORS, ESTROGEN; SURVIVAL ANALYSIS;

EID: 84883375310     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201302625     Document Type: Article

References (36)

1. Akeno-Stuart N, Croyle M, Knauf JA, Malaguarnera R, Vitagliano D, Santoro M, Stephan C, Grosios K, Wartmann M, Cozens R, et al (2007) The RET kinase inhibitor NVP-AST487 blocks growth and calcitonin gene expression through distinct mechanisms in medullary thyroid cancer cells. Cancer Res 67: 6956-6964
2. Badache A, Hynes NE (2001) Interleukin 6 inhibits proliferation and, in cooperation with an epidermal growth factor receptor autocrine loop, increases migration of T47D breast cancer cells. Cancer Res 61: 383-391
3. Boulay A, Breuleux M, Stephan C, Fux C, Brisken C, Fiche M, Wartmann M, Stumm M, Lane HA, Hynes NE (2008) The Ret receptor tyrosine kinase pathway functionally interacts with the ERalpha pathway in breast cancer. Cancer Res 68: 3743-3751
4. Boulay A, Rudloff J, Ye J, Zumstein-Mecker S, O'Reilly T, Evans DB, Chen S, Lane HA (2005) Dual inhibition of mTOR and estrogen receptor signaling in vitro induces cell death in models of breast cancer. Clin Cancer Res 11: 5319-5328
5. de Groot JW, Links TP, Plukker JT, Lips CJ, Hofstra RM (2006) RET as a diagnostic and therapeutic target in sporadic and hereditary endocrine tumors. Endocr Rev 27: 535-560
6. Esseghir S, Todd SK, Hunt T, Poulsom R, Plaza-Menacho I, Reis-Filho JS, Isacke CM (2007) A role for glial cell derived neurotrophic factor induced expression by inflammatory cytokines and RET/GFR alpha 1 receptor up-regulation in breast cancer. Cancer Res 67: 11732-11741
7. Forbes JF, Cuzick J, Buzdar A, Howell A, Tobias JS, Baum M (2008) Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial. Lancet Oncol 9: 45-53
8. Frame MC, Patel H, Serrels B, Lietha D, Eck MJ (2010) The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol 11: 802-814
9. Frasor J, Stossi F, Danes JM, Komm B, Lyttle CR, Katzenellenbogen BS (2004) Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Res 64: 1522-1533
10. Gianni L, Dafni U, Gelber RD, Azambuja E, Muehlbauer S, Goldhirsch A, Untch M, Smith I, Baselga J, Jackisch C, et al (2011) Treatment with trastuzumab for 1 year after adjuvant chemotherapy in patients with HER2-positive early breast cancer: a 4-year follow-up of a randomised controlled trial. Lancet Oncol 12: 236-244
11. Ichihara M, Murakumo Y, Takahashi M (2004) RET and neuroendocrine tumors. Cancer Lett 204: 197-211
12. Ito Y, Okada Y, Sato M, Sawai H, Funahashi H, Murase T, Hayakawa T, Manabe T (2005) Expression of glial cell line-derived neurotrophic factor family members and their receptors in pancreatic cancers. Surgery 138: 788-794
13. Jan R, Huang M, Lewis-Wambi J (2012) Loss of pigment epithelium-derived factor: A novel mechanism for the development of endocrine resistance in breast cancer. Breast Cancer Res 14: R146
14. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM, Yue P, Haverty PM, Bourgon R, Zheng J, et al (2010) Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466: 869-873
15. Kang J, Qian PX, Pandey V, Perry JK, Miller LD, Liu ET, Zhu T, Liu DX, Lobie PE (2010) Artemin is estrogen regulated and mediates antiestrogen resistance in mammary carcinoma. Oncogene 29: 3228-3240
16. Kohno T, Ichikawa H, Totoki Y, Yasuda K, Hiramoto M, Nammo T, Sakamoto H, Tsuta K, Furuta K, Shimada Y, et al (2012) KIF5B-RET fusions in lung adenocarcinoma. Nat Med 18: 375-377
17. Kothari V, Wei I, Shankar S, Kalyana-Sundaram S, Wang L, Ma LW, Vats P, Grasso CS, Robinson DR, Wu YM, et al (2013) Outlier kinase expression by RNA sequencing as targets for precision therapy. Cancer Discov 3: 280-293
18. Kurebayashi S, Miyashita Y, Hirose T, Kasayama S, Akira S, Kishimoto T (1997) Characterization of mechanisms of interleukin-6 gene repression by estrogen receptor. J Steroid Biochem Mol Biol 60: 11-17
19. Li H, Gomes PJ, Chen JD (1997) RAC3, a steroid/nuclear receptor-associated coactivator that is related to SRC-1 and TIF2. Proc Natl Acad Sci U S A 94: 8479-8484
20. Morandi A, Martin LA, Gao Q, Pancholi S, Mackay A, Robertson D, Zvelebil M, Dowsett M, Plaza-Menacho I, Isacke CM (2013) GDNF-RET signaling in ER-positive breast cancers is a key determinant of response and resistance to aromatase inhibitors. Cancer Res 73: 3787-3795
21. Morandi A, Plaza-Menacho I, Isacke CM (2011) RET in breast cancer: Functional and therapeutic implications. Trends Mol Med 17: 149-157
22. Nikolsky Y, Sviridov E, Yao J, Dosymbekov D, Ustyansky V, Kaznacheev V, Dezso Z, Mulvey L, Macconaill LE, Winckler W, et al (2008) Genome-wide functional synergy between amplified and mutated genes in human breast cancer. Cancer Res 68: 9532-9540
23. Plaza-Menacho I, Morandi A, Mologni L, Boender P, Gambacorti-Passerini C, Magee AI, Hofstra RM, Knowles P, McDonald NQ, Isacke CM (2011) Focal adhesion kinase (FAK) binds RET kinase via its FERM domain, priming a direct and reciprocal RET-FAK transactivation mechanism. J Biol Chem 286: 17292-17302
24. Plaza-Menacho I, Morandi A, Robertson D, Pancholi S, Drury S, Dowsett M, Martin LA, Isacke CM (2010) Targeting the receptor tyrosine kinase RET sensitizes breast cancer cells to tamoxifen treatment and reveals a role for RET in endocrine resistance. Oncogene 29: 4648-4657
25. Sandilands E, Serrels B, Wilkinson S, Frame MC (2012) Src-dependent autophagic degradation of Ret in FAK-signalling-defective cancer cells. EMBO Rep 13: 733-740
26. Sariola H, Saarma M (2003) Novel functions and signalling pathways for GDNF. J Cell Sci 116: 3855-3862
27. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367: 380-383
28. Suehara Y, Arcila M, Wang L, Hasanovic A, Ang D, Ito T, Kimura Y, Drilon A, Guha U, Rusch V, et al (2012) Identification of KIF5B-RET and GOPC-ROS1 Fusions in Lung Adenocarcinomas through a Comprehensive mRNA-Based Screen for Tyrosine Kinase Fusions. Clin Cancer Res 18: 6599-6608
29. Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, Asaka R, Hamanaka W, Ninomiya H, Uehara H, et al (2012) RET, ROS1 and ALK fusions in lung cancer. Nat Med 18: 378-381
30. Torres-Arzayus MI, Yuan J, DellaGatta JL, Lane H, Kung AL, Brown M (2006) Targeting the AIB1 oncogene through mammalian target of rapamycin inhibition in the mammary gland. Cancer Res 66: 11381-11388
31. Torres-Arzayus MI, Zhao J, Bronson R, Brown M (2010) Estrogen-dependent and estrogen-independent mechanisms contribute to AIB1-mediated tumor formation. Cancer Res 70: 4102-4111
32. Tozlu S, Girault I, Vacher S, Vendrell J, Andrieu C, Spyratos F, Cohen P, Lidereau R, Bieche I (2006) Identification of novel genes that co-cluster with estrogen receptor alpha in breast tumor biopsy specimens, using a large-scale real-time reverse transcription-PCR approach. Endocr Relat Cancer 13: 1109-1120
33. Unger K, Wienberg J, Riches A, Hieber L, Walch A, Brown A, O'Brien PC, Briscoe C, Gray L, Rodriguez E, et al (2010) Novel gene rearrangements in transformed breast cells identified by high-resolution breakpoint analysis of chromosomal aberrations. Endocr Relat Cancer 17: 87-98
34. van Oostrum J, Calonder C, Rechsteiner D, Ehrat M, Mestan J, Fabbro D, Voshol H (2009) Tracing pathway activities with kinase inhibitors and reverse phase protein arrays. Proteomics Clin Appl 3: 412-422
35. Vinatzer U, Dampier B, Streubel B, Pacher M, Seewald MJ, Stratowa C, Kaserer K, Schreiber M (2005) Expression of HER2 and the coamplified genes GRB7 and MLN64 in human breast cancer: quantitative real-time reverse transcription-PCR as a diagnostic alternative to immunohistochemistry and fluorescence in situ hybridization. Clin Cancer Res 11: 8348-8357
36. Waerner T, Alacakaptan M, Tamir I, Oberauer R, Gal A, Brabletz T, Schreiber M, Jechlinger M, Beug H (2006) ILEI: A cytokine essential for EMT, tumor formation, and late events in metastasis in epithelial cells. Cancer Cell 10: 227-239