Selective inhibition of RET mediated cell proliferation in vitro by the kinase inhibitor SPP86

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Alao, John P ^a   Michlikova, Sona ^a   Dinér, Peter ^a,b   Grøtli, Morten ^a   Sunnerhagen, Per ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Breast cancer; Estrogen receptor; FAK; Kinase inhibitor; RET; Thyroid cancer

Indexed keywords

ANTINEOPLASTIC AGENT; ESTROGEN RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE INHIBITOR; PROTEIN RET;

ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; ESTROGEN RECEPTOR ALPHA; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-RET;

EID: 84940023717     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-853     Document Type: Article

References (62)

1. Mulligan LM: RET revisited: expanding the oncogenic portfolio. Nat Rev 2014, 14(3):173-186.
2. Plaza-Menacho I, Burzynski GM, de Groot JW, Eggen BJ, Hofstra RM: Current concepts in RET-related genetics, signaling and therapeutics. Trends Genet 2006, 22(11):627-636.
3. Cassinelli G, Favini E, Degl'Innocenti D, Salvi A, De Petro G, Pierotti MA, Zunino F, Borrello MG, Lanzi C: RET/PTC1-driven neoplastic transformation and proinvasive phenotype of human thyrocytes involve Met induction and beta-catenin nuclear translocation. Neoplasia 2009, 11(1):10-21.
4. Croyle M, Akeno N, Knauf JA, Fabbro D, Chen X, Baumgartner JE, Lane HA, Fagin JA: RET/PTC-induced cell growth is mediated in part by epidermal growth factor receptor (EGFR) activation: evidence for molecular and functional interactions between RET and EGFR. Cancer Res 2008, 68(11):4183-4191.
5. Plaza-Menacho I, Morandi A, Robertson D, Pancholi S, Drury S, Dowsett M, Martin LA, Isacke CM: Targeting the receptor tyrosine kinase RET sensitizes breast cancer cells to tamoxifen treatment and reveals a role for RET in endocrine resistance. Oncogene 2010, 29(33):4648-4657.
6. Wang C, Mayer JA, Mazumdar A, Brown PH: The rearranged during transfection/papillary thyroid carcinoma tyrosine kinase is an estrogen-dependent gene required for the growth of estrogen receptor positive breast cancer cells. Breast Cancer Res Treat 2011, 133(2):487-500.
7. Kohno T, Ichikawa H, Totoki Y, Yasuda K, Hiramoto M, Nammo T, Sakamoto H, Tsuta K, Furuta K, Shimada Y, Iwakawa R, Ogiwara H, Oike T, Enari M, Schetter AJ, Okayama H, Haugen A, Skaug V, Chiku S, Yamanaka I, Arai Y, Watanabe S, Sekine I, Ogawa S, Harris CC, Tsuda H, Yoshida T, Yokota J, Shibata T: KIF5B-RET fusions in lung adenocarcinoma. Nat Med 2012, 18(3):375-377.
8. Lipson D, Capelletti M, Yelensky R, Otto G, Parker A, Jarosz M, Curran JA, Balasubramanian S, Bloom T, Brennan KW, Donahue A, Downing SR, Frampton GM, Garcia L, Juhn F, Mitchell KC, White E, White J, Zwirko Z, Peretz T, Nechushtan H, Soussan-Gutman L, Kim J, Sasaki H, Kim HR, Park SI, Ercan D, Sheehan CE, Ross JS, Cronin MT, et al: Identification of new ALK and RET gene fusions from colorectal and lung cancer biopsies. Nat Med 2012, 18(3):382-384.
9. Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, Asaka R, Hamanaka W, Ninomiya H, Uehara H, Lim Choi Y, Satoh Y, Okumura S, Nakagawa K, Mano H, Ishikawa Y: RET, ROS1 and ALK fusions in lung cancer. Nat Med 2012, 18(3):378-381.
10. Moelling K, Schad K, Bosse M, Zimmermann S, Schweneker M: Regulation of Raf-Akt Cross-talk. J Biol Chem 2002, 277(34):31099-31106.
11. Wimmer R, Baccarini M: Partner exchange: protein-protein interactions in the Raf pathway. Trends Biochem Sci 2010, 35(12):660-668.
12. Poulikakos PI, Zhang C, Bollag G, Shokat KM, Rosen N: RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 2010, 464(7287):427-430.
13. Cohen P: Guidelines for the effective use of chemical inhibitors of protein function to understand their roles in cell regulation. Biochem J 2010, 425(1):53-54.
14. Putyrski M, Schultz C: Protein translocation as a tool: The current rapamycin story. FEBS Lett 2012, 586(15):2097-2105.
15. Chappell WH, Steelman LS, Long JM, Kempf RC, Abrams SL, Franklin RA, Bäsecke J, Stivala F, Donia M, Fagone P, Malaponte G, Mazzarino MC, Nicoletti F, Libra M, Maksimovic-Ivanic D, Mijatovic S, Montalto G, Cervello M, Laidler P, Milella M, Tafuri A, Bonati A, Evangelisti C, Cocco L, Martelli AM, McCubrey JA: Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR inhibitors: rationale and importance to inhibiting these pathways in human health. Oncotarget 2011, 2(3):135-164.
16. McCubrey JA, Steelman LS, ChappellWH, Abrams SL, Franklin RA, Montalto G, Cervello M, Libra M, Candido S, Malaponte G, Mazzarino MC, Fagone P, Nicoletti F, Bäsecke J, Mijatovic S, Maksimovic-Ivanic D, Milella M, Tafuri A, Chiarini F, Evangelisti C, Cocco L, Martelli AM: Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascade inhibitors: how mutations can result in therapy resistance and how to overcome resistance. Oncotarget 2012, 3(10):1068-1111.
17. Borrello MG, Ardini E, Locati LD, Greco A, Licitra L, Pierotti MA: RET inhibition: implications in cancer therapy. Expert Opin Ther Targets 2013, 17(4):403-419.
18. Mologni L: Development of RET kinase inhibitors for targeted cancer therapy. Curr Med Chem 2011, 18(2):162-175.
19. Phay JE, Shah MH: Targeting RET receptor tyrosine kinase activation in cancer. Clin Cancer Res 2010, 16(24):5936-5941.
20. Bain J, McLauchlan H, Elliott M, Cohen P: The specificities of protein kinase inhibitors: an update. Biochem J 2003, 371(Pt 1):199-204.
21. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P: The selectivity of protein kinase inhibitors: a further update. Biochem J 2007, 408(3):297-315.
22. Caccia D, Micciche F, Cassinelli G, Mondellini P, Casalini P, Bongarzone I: Dasatinib reduces FAK phosphorylation increasing the effects of RPI-1 inhibition in a RET/PTC1-expressing cell line. Mol Cancer 2010, 9:278.
23. Murakami H, Iwashita T, Asai N, Iwata Y, Narumiya S, Takahashi M: Rho-dependent and-independent tyrosine phosphorylation of focal adhesion kinase, paxillin and p130Cas mediated by Ret kinase. Oncogene 1999, 18(11):1975-1982.
24. Plaza-Menacho I, Morandi A, Mologni L, Boender P, Gambacorti-Passerini C, Magee AI, Hofstra RM, Knowles P, McDonald NQ, Isacke CM: Focal adhesion kinase (FAK) binds RET kinase via its FERM domain, priming a direct and reciprocal RET-FAK transactivation mechanism. J Biol Chem 2011, 286(19):17292-17302.
25. Brandt W, Mologni L, Preu L, Lemcke T, Gambacorti-Passerini C, Kunick C: Inhibitors of the RET tyrosine kinase based on a 2-(alkylsulfanyl)-4-(3-thienyl) nicotinonitrile scaffold. Eur J Med Chem 2010, 45(7):2919-2927.
26. Carlomagno F, Vitagliano D, Guida T, Napolitano M, Vecchio G, Fusco A, Gazit A, Levitzki A, Santoro M: The kinase inhibitor PP1 blocks tumorigenesis induced by RET oncogenes. Cancer Res 2002, 62(4):1077-1082.
27. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA: Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck-and FynT-dependent T cell activation. J Biol Chem 1996, 271(2):695-701.
28. Lanzi C, Cassinelli G, Cuccuru G, Zaffaroni N, Supino R, Vignati S, Zanchi C, Yamamoto M, Zunino F: Inactivation of Ret/Ptc1 oncoprotein and inhibition of papillary thyroid carcinoma cell proliferation by indolinone RPI-1. Cell Mol Life Sci 2003, 60(7):1449-1459.
29. Cassinelli G, Lanzi C, Petrangolini G, Tortoreto M, Pratesi G, Cuccuru G, Laccabue D, Supino R, Belluco S, Favini E, Poletti A, Zunino F: Inhibition of c-Met and prevention of spontaneous metastatic spreading by the 2-indolinone RPI-1. Mol Cancer Ther 2006, 5(9):2388-2397.
30. Lanzi C, Cassinelli G, Pensa T, Cassinis M, Gambetta RA, Borrello MG, Menta E, Pierotti MA, Zunino F: Inhibition of transforming activity of the ret/ptc1 oncoprotein by a 2-indolinone derivative. Int J Cancer 2000, 85(3):384-390.
31. Meulenbeld HJ, Mathijssen RH, Verweij J, de Wit R, de Jonge MJ: Danusertib, an aurora kinase inhibitor. Expert Opin Investig Drugs 2012, 21(3):383-393.
32. Pardanani A, Hood J, Lasho T, Levine RL, Martin MB, Noronha G, Finke C, Mak CC, Mesa R, Zhu H, Soll R, Gilliland DG, Tefferi A: TG101209, a small molecule JAK2-selective kinase inhibitor potently inhibits myeloproliferative disorder-associated JAK2V617F and MPLW515L/K mutations. Leukemia 2007, 21(8):1658-1668.
33. Arora A, Scholar EM: Role of tyrosine kinase inhibitors in cancer therapy. J Pharmacol Exp Ther 2005, 315(3):971-979.
34. Mendel DB, Schreck RE, West DC, Li G, Strawn LM, Tanciongco SS, Vasile S, Shawver LK, Cherrington JM: The angiogenesis inhibitor SU5416 has long-lasting effects on vascular endothelial growth factor receptor phosphorylation and function. Clin Cancer Res 2000, 6(12):4848-4858.
35. Kim A, Balis FM, Widemann BC: Sorafenib and sunitinib. Oncologist 2009, 14(8):800-805.
36. Yakes FM, Chen J, Tan J, Yamaguchi K, Shi Y, Yu P, Qian F, Chu F, Bentzien F, Cancilla B, Orf J, You A, Laird AD, Engst S, Lee L, Lesch J, Chou YC, Joly AH: Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther 2011, 10(12):2298-2308.
37. Wilhelm S, Carter C, Lynch M, Lowinger T, Dumas J, Smith RA, Schwartz B, Simantov R, Kelley S: Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat Rev Drug Discov 2006, 5(10):835-844.
38. Carlomagno F, Vitagliano D, Guida T, Ciardiello F, Tortora G, Vecchio G, Ryan AJ, Fontanini G, Fusco A, Santoro M: ZD6474, an orally available inhibitor of KDR tyrosine kinase activity, efficiently blocks oncogenic RET kinases. Cancer Res 2002, 62(24):7284-7290.
39. Ciardiello F, Tortora G: A novel approach in the treatment of cancer: targeting the epidermal growth factor receptor. Clin Cancer Res 2001, 7(10):2958-2970.
40. Mologni L, Redaelli S, Morandi A, Plaza-Menacho I, Gambacorti-Passerini C: Ponatinib is a potent inhibitor of wild-type and drug-resistant gatekeeper mutant RET kinase. Mol Cell Endocrinol 2013, 377(1-2):1-6.
41. O'Hare T, Shakespeare WC, Zhu X, Eide CA, Rivera VM, Wang F, Adrian LT, Zhou T, Huang WS, Xu Q, Metcalf CA 3rd, Tyner JW, Loriaux MM, Corbin AS, Wardwell S, Ning Y, Keats JA, Wang Y, Sundaramoorthi R, Thomas M, Zhou D, Snodgrass J, Commodore L, Sawyer TK, Dalgarno DC, Deininger MW, Druker BJ, Clackson T: AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutation-based resistance. Cancer Cell 2009, 16(5):401-412.
42. Akeno-Stuart N, Croyle M, Knauf JA, Malaguarnera R, Vitagliano D, Santoro M, Stephan C, Grosios K, Wartmann M, Cozens R, Caravatti G, Fabbro D, Lane HA, Fagin JA: The RET kinase inhibitor NVP-AST487 blocks growth and calcitonin gene expression through distinct mechanisms in medullary thyroid cancer cells. Cancer Res 2007, 67(14):6956-6964.
43. Morandi A, Martin LA, Gao Q, Pancholi S, Mackay A, Robertson D, Zvelebil M, Dowsett M, Plaza-Menacho I, Isacke CM: GDNF-RET signaling in ER-positive breast cancers is a key determinant of response and resistance to aromatase inhibitors. Cancer Res 2013, 73(12):3783-3795.
44. Lucet IS, Fantino E, Styles M, Bamert R, Patel O, Broughton SE, Walter M, Burns CJ, Treutlein H, Wilks AF, Rossjohn J: The structural basis of Janus kinase 2 inhibition by a potent and specific pan-Janus kinase inhibitor. Blood 2006, 107(1):176-183.
45. Diner P, Alao JP, Soderlund J, Sunnerhagen P, Grotli M: Preparation of 3-Substituted-1-Isopropyl-1H-pyrazolo[3, 4-d]pyrimidin-4-amines as RET Kinase Inhibitors. J Med Chem 2012, 55(10):4872-4876.
46. Jiang J, Wei Y, Shen J, Liu D, Chen X, Zhou J, Zong H, Yun X, Kong X, Zhang S, Yang Y, Gu J: Functional interaction of E1AF and Sp1 in glioma invasion. Mol Cell Biol 2007, 27(24):8770-8782.
47. Pilli T, Prasad KV, Jayarama S, Pacini F, Prabhakar BS: Potential utility and limitations of thyroid cancer cell lines as models for studying thyroid cancer. Thyroid 2009, 19(12):1333-1342.
48. Saiselet M, Floor S, Tarabichi M, Dom G, Hebrant A, van Staveren WC, Maenhaut C: Thyroid cancer cell lines: an overview. Front Endocrinol 2012, 3:133.
49. Preto A, Gonçalves J, Rebocho AP, Figueiredo J, Meireles AM, Rocha AS, Vasconcelos HM, Seca H, Seruca R, Soares P, Sobrinho-Simões M: Proliferation and survival molecules implicated in the inhibition of BRAF pathway in thyroid cancer cells harbouring different genetic mutations. BMC Cancer 2009, 9:387.
50. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, Luzzio MJ, Cooper B, Kath JC, Roberts WG, Parsons JT: Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem2007, 282(20):14845-14852.
51. Boulay A, Breuleux M, Stephan C, Fux C, Brisken C, Fiche M, Wartmann M, Stumm M, Lane HA, Hynes NE: The Ret receptor tyrosine kinase pathway functionally interacts with the ERalpha pathway in breast cancer. Cancer Res 2008, 68(10):3743-3751.
52. Gattelli A, Nalvarte I, Boulay A, Roloff TC, Schreiber M, Carragher N, Macleod KK, Schlederer M, Lienhard S, Kenner L, Torres-Arzayus MI, Hynes NE: Ret inhibition decreases growth and metastatic potential of estrogen receptor positive breast cancer cells. EMBO Mol Med 2013, 5(9):1335-1350.
53. St Bernard R, Zheng L, Liu W, Winer D, Asa SL, Ezzat S: Fibroblast growth factor receptors as molecular targets in thyroid carcinoma. Endocrinology 2005, 146(3):1145-1153.
54. Kim DW, Hwang JH, Suh JM, Kim H, Song JH, Hwang ES, Hwang IY, Park KC, Chung HK, Kim JM, Park J, Hemmings BA, Shong M: RET/PTC (rearranged in transformation/papillary thyroid carcinomas) tyrosine kinase phosphorylates and activates phosphoinositide-dependent kinase 1 (PDK1): an alternative phosphatidylinositol 3-kinase-independent pathway to activate PDK1. Mol Endocrinol 2003, 17(7):1382-1394.
55. Knauf JA, Kuroda H, Basu S, Fagin JA: RET/PTC-induced dedifferentiation of thyroid cells is mediated through Y1062 signaling through SHC-RAS-MAP kinase. Oncogene 2003, 22(28):4406-4412.
56. Murphy LC, Seekallu SV, Watson PH: Clinical significance of estrogen receptor phosphorylation. Endocr Relat Cancer 2011, 18(1):R1-R14.
57. Yamnik RL, Holz MK: mTOR/S6K1 and MAPK/RSK signaling pathways coordinately regulate estrogen receptor alpha serine 167 phosphorylation. FEBS Lett 2010, 584(1):124-128.
58. Gonzalez L, Agullo-Ortuno MT, Garcia-Martinez JM, Calcabrini A, Gamallo C, Palacios J, Aranda A, Martin-Perez J: Role of c-Src in human MCF7 breast cancer cell tumorigenesis. J Biol Chem 2006, 281(30):20851-20864.
59. Alao JP: The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Mol Cancer 2007, 6:24.
60. Alao JP, Lam EW, Ali S, Buluwela L, Bordogna W, Lockey P, Varshochi R, Stavropoulou AV, Coombes RC, Vigushin DM: Histone deacetylase inhibitor trichostatin A represses estrogen receptor alpha-dependent transcription and promotes proteasomal degradation of cyclin D1 in human breast carcinoma cell lines. Clin Cancer Res 2004, 10(23):8094-8104.
61. Fox BP, Kandpal RP: Invasiveness of breast carcinoma cells and transcript profile: Eph receptors and ephrin ligands as molecular markers of potential diagnostic and prognostic application. Biochem Biophys Res Commun 2004, 318(4):882-892.
62. Simiantonaki N, Jayasinghe C, Michel-Schmidt R, Peters K, Hermanns MI, Kirkpatrick CJ: Hypoxia-induced epithelial VEGF-C/VEGFR-3 upregulation in carcinoma cell lines. Int J Oncol 2008, 32(3):585-592.