Inactivation of Ret/Ptc1 oncoprotein and inhibition of papillary thyroid carcinoma cell proliferation by indolinone RPI-1

Cellular and Molecular Life Sciences

Volumn 60, Issue 7, 2003, Pages 1449-1459

  Lanzi, C ^a   Cassinelli, G ^a   Cuccuru, G ^a   Zaffaroni, N ^a   Supino, R ^a   Vignati, S ^a   Zanchi, C ^a   Yamamoto, M ^b   Zunino, F ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

2 indolinone; AKT; C Jun N terminal kinase; Oncoprotein; Receptor tyrosine kinase Ret; Telomerase; Thyroid neoplasms

Indexed keywords

1,3 DIHYDRO 5,6 DIMETHOXY 3 (4 HYDROXYPHENYL)METHYLENE 1H INDOL 2 ONE; INDOLE DERIVATIVE; ONCOPROTEIN; OXINDOLE; PHOSPHOLIPASE C; PROTEIN KINASE B; PROTEIN RET; PROTEIN TYROSINE KINASE; RPI 1; STRESS ACTIVATED PROTEIN KINASE; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G2 PHASE; CELL PROLIFERATION; GENE INACTIVATION; GENE MUTATION; GENE REARRANGEMENT; GROWTH INHIBITION; HUMAN; HUMAN CELL; ONCOGENE RET; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TARGET CELL; THYROID MEDULLARY CARCINOMA; THYROID PAPILLARY CARCINOMA; TUMOR GROWTH;

ANIMALS; CARCINOMA, PAPILLARY; CELL CYCLE; CELL DIVISION; DNA, NEOPLASM; HUMANS; INDOLES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KINETICS; MEMBRANE PROTEINS; MICE; ONCOGENE PROTEINS; ONCOGENE PROTEINS, FUSION; PROTEIN-TYROSINE KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS C-RET; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TELOMERASE; THYROID NEOPLASMS; TUMOR CELLS, CULTURED;

MURINAE;

EID: 0041867947     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-003-2381-8     Document Type: Article

References (49)

1. Schuchardt A., D'Agati V., Larsson-Blomberg L., Costantini F. and Pachni V. (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367: 319-320
2. Pasini B., Borrello M. G., Greco A., Bongarzone I., Luo Y., Mondellini P. et al. (1995) Loss of function effect of RET mutations causing Hirschsprung disease. Nat. Genet. 10: 35-40
3. Jhiang S. M. (2000) The RET proto-oncogene in human cancers. Oncogene 19: 5590-5597
4. Tallini G. and Asa S. L. (2001) REToncogene activation in papillary thyroid carcinoma. Adv. Anat. Pathol. 8: 345-354
5. Takahashi M. (2001) The GDNF/Ret signaling pathway and human diseases. Cytokine Growth Factor Rev. 12: 361-373
6. Grieco M., Santoro M., Berlingieri M. T., Melillo R. M., Donghi R., Bongarzone I. et al. (1990) PTC is a novel rearranged form of the ret proto-oncogene and is frequently detected in vivo in human thyroid papillary carcinomas. Cell 60: 557-563
7. Ito S., Iwashita T., Asai N., Murakami H., Iwata Y., Sobue G. et al. (1997) Biological properties of Ret with cysteine mutations correlate with multiple endocrine neoplasia type 2A, familial medullary thyroid carcinoma, and Hirschsprung's disease phenotype. Cancer Res. 57: 2870-2872
8. Iwashita T., Kato M., Murakami H., Asai N., Ishiguro Y., Ito S. et al. (1999) Biological and biochemical properties of Ret with kinase domain mutations identified in multiple endocrine neoplasia type 2B and familial medullary thyroid carcinoma. Oncogene 18: 3919-3922
9. Santoro M., Chiappetta G., Cerrato A., Salvatore D., Zhang L., Manzo G. et al. (1996) Development of thyroid papillary carcinomas secondary to tissue-specific expression of the RET/PTC1 oncogene in transgenic mice. Oncogene 12: 1821-1826
10. Cho J.-Y., Sagartz J. E., Capen C. C., Mazzaferri E. L. and Jhiang S. M (1999) Early cellular abnormalities induced by RET/PTC1 oncogene in thyroid-targeted transgenic mice. Oncogene 18: 3659-3665
11. Michiels F.-M., Chappuis S., Caillou B., Pasini A., Talbot M., Monier R. et al. (1997) Development of medullary thyroid carcinoma in transgenic mice expressing the RET protooncogene altered by a multiple endocrine neoplasia type 2A mutation. Proc. Natl. Acad. Sci. USA 94: 3330-3335
12. Acton D. S., Velthuyzen D., Lips C. J. and Hoppener J. W. (2000) Multiple endocrine neoplasia type 2B mutation in human RET oncogene induces medullary thyroid carcinoma in transgenic mice. Oncogene 19: 3121-3125
13. Schlessinger J. (2000) Cell signaling by receptor tyrosine kinases. Cell 103: 211-225
14. Shawver L. K., Slamon D. and Ullrich A. (2002) Smart drugs: tyrosine kinase inhibitors in cancer therapy. Cancer Cell 1: 117-123
15. Lanzi C., Cassinelli G., Pensa T., Cassinis M., Gambetta R. A., Borrello M. G. et al. (2000) Inhibition of transforming activity of the ret/ptc1 oncoprotein by a 2-indolinone derivative. Int. J. Cancer 85: 384-390
16. Borrello M. G., Alberti L., Arighi E., Bongarzone I., Battistini C., Bardel A. et al. (1996) The full oncogenic activity of Ret/ptc2 depends on tyrosine 539, a docking site for phospholipase Cγ. Mol. Cell. Biol. 16: 2151-2163
17. Yamamoto M., Li M., Mitsuma N., Ito S., Kato M., Takahashi M. et al. (2001) Preserved phosphorylation of Ret receptor protein in spinal motor neurons of patients with amyotrophic lateral sclerosis: an immunohistochemical study by a phosphorylation- specific antibody at tyrosine 1062. Brain Res. 912: 89-94
18. Skehan P., Storeng R., Scudiero D., Monks A., McMahon J., Vistica D. et al. (1990) New colorimetric cytotoxicity assay for anti-cancer-drug screening. J. Natl. Cancer Inst. 82: 1107-1112
19. Villa R., Zaffaroni N., Folini M., Martelli G., De Palo G., Daidone M. G. et al. (1998) Telomerase activity in benign and malignant breast lesions: a pilot prospective study on fine-needle aspirates. J. Natl. Cancer Inst. 90: 537-539
20. Kim N. W., Piatyszek M. A., Prowse K. R., Harley C. B., West M. D., Ho P. L. et al. (1995) Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011-2015
21. Villa R., Della Porta C., Folini M., Daidone M. G. and Zaffaroni N. (2001) Possible regulation of telomerase activity by transcription and alternative splicing of telomerase reverse transcriptase in human melanoma. J. Invest. Dermatol. 116: 867-873
22. Cerutti J., Trapasso F., Battaglia C., Zhang L., Martelli M. L., Visconti R. et al. (1996) Block of c-myc expression by antisense oligonucleotides inhibits proliferation of human thyroid carcinoma cell lines. Clin. Cancer Res. 2: 119-126
23. Borrello M. G., Pelicci G., Arighi E., De Filippis L., Greco A., Bongarzone I. et al. (1994) The oncogenic versions of the Ret and Trk tyrosine kinases bind Shc and Grb2 adaptor proteins. Oncogene 9: 1661-1668
24. Van Weering D. H. J. and Bos J. L. (1997) Glial cell line-derived neurotrophic factor induces Ret-mediated lamellipodia formation. J. Biol. Chem. 272: 249-254
25. Lorenzo M. J., Gish G. D., Houghton C., Stonehouse T. J., Pawson T., Ponder B. A. et al. (1997) RET alternate splicing influences the interaction of activated Ret with the SH2 and PTB domains of Shc, and the SH2 domain of Grb2. Oncogene 14: 763-771
26. Asai N., Murakami H., Iwashita T. and Takahashi M. (1996) A mutation at tyrosine 1062 in MEN2A-Ret and MEN2B-Ret impairs their transforming activity and association with shc adaptor proteins. J. Biol. Chem. 271: 17644-17649
27. Arighi E., Alberti L., Torriti F., Ghizzoni S, Rizzetti M. G., Pelicci G. et al. (1997) Identification of Shc docking site on Ret tyrosine kinase. Oncogene 14: 773-782
28. Mercalli E., Ghizzoni S., Arighi E., Alberti L., Sangregorio R., Radice M. T. et al. (2001) Key role of Shc signaling in the transforming pathway triggered by Ret/ptc2 oncoprotein. Oncogene 20: 3475-3485
29. 2-terminal kinase by growth factors influences survival but not apoptosis of human thyrocytes. Thyroid 11: 629-636
30. Toker A. (2000) Protein kinases as mediators of phosphoinositide 3-kinase signaling. Mol. Pharmacol. 57: 652-658
31. Elenitoba-Johnson K. S. J. (2001) Complex regulation of telomerase activity: implications for cancer therapy. Am. J. Pathol. 159: 405-410
32. Holt S. E., Aisner D. L., Shay J. W. and Wright W. E. (1997) Lack of cell cycle regulation of telomerase activity in human cells. Proc. Natl. Acad. Sci. USA 94: 10687-10692
33. Ishizaka Y., Itoh F., Tahira T., Ikeda I., Ogura T., Sugimura T. et al. (1989) Presence of aberrant transcripts of ret proto-oncogene in a human papillary thyroid carcinoma cell line. Jpn. J. Cancer Res. 80: 1149-1152
34. Jossart G. H., Greulich K. M., Siperstein A. E., Duh Q., Clark O. H. and Weier H. U. (1995) Molecular and cytogenetic characterization of a t(1;10;21) translocation in the human papillary thyroid cancer cell line TPC-1 expressing the RET/H4 chimeric transcript. Surgery 118: 1018-1023
35. Basolo F., Giannini R., Toniolo A., Casalone R., Nikiforova M., Pacini F. et al. (2002) Establishment of a non-tumorigenic papillary thyroid cell line (FB-2) carrying the RET/PTC1 rearrangement. Int. J. Cancer 97: 608-614
36. WAFI/CipI: more than a break to the cell cycle? Biochim. Biophys. Acta 1471: 430-56
37. 2-terminal protein kinases (JNKs): evidence for a divergence of the ERKs and JNKs pathways induced by Ret. Oncogene 16: 2435-2445
38. Marshall G. M., Peaston A. E., Hocker J. E., Smith S. A., Hansford L. M., Tobias V. et al. (1997) Expression of multiple endocrine neoplasia 2B RET in neuroblastoma cells alters cell adhesion in vitro, enhances metastatic behavior in vivo, and activates Jun kinase. Cancer Res. 57: 5399-5405
39. Xing S., Furminger T. L., Tong Q. and Jhiang S. M. (1998) Signal transduction pathways activated by Ret oncoproteins in PC12 pheochromocytoma cells. J. Biol. Chem. 273: 4909-4914
40. Hayashi H., Ichihara M., Iwashita T., Murakami H., Shimono Y., Kawai K. et al. (2000) Characterization of intracellular signals via tyrosine 1062 in Ret activated by glial cell line-derived neurotrophic factor. Oncogene 19: 4469-4475
41. Salvatore D., Barone M. V., Salvatore G., Melillo R. M., Chiappetta G., Mineo A. et al. (2000) Tyrosines 1015 and 1062 are in vivo autophosphorylation sites in Ret and Ret-derived oncoproteins. J. Clin. Endocrinol. Metab. 85: 3898-3907
42. Ravichandran K. S. (2001) Signaling via Shc family adapter proteins. Oncogene 20: 6322-6330
43. shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402: 309-313
44. WAFI gene expression. Mol. Carcinog. 21: 26-36
45. Kang S. S., Kwon T., Kwon D. Y. and Do S. I. (1999) Akt protein kinase enhances human telomerase activity through phosphorylation of telomerase reverse transcriptase subunit. J. Biol. Chem. 274: 13085-13090
46. Li H., Zhao L., Yang Z., Funder J. W. and Liu J. P. (1998) Telomerase is controlled by protein kinase Cα in human breast cancer cells. J. Biol. Chem. 273: 33436-33442
47. Cheng A. J., Lin J. D., Chang T. and Wang T. C. (1998) Telomerase activity in benign and malignant human thyroid tissues. Br. J. Cancer 77: 2177-2180
48. Matthews P., Jones C. J., Skinner J., Haughton M., Micco C. de and Wynford-Thomas D. (2001) Telomerase activity and telomere length in thyroid neoplasia: biological and clinical implications. J. Pathol. 194: 183-193
49. Carlomagno F., Vitagliano D., Guida T., Napolitano M., Vecchio G., Fusco A. et al. (2002) The kinase inhibitor PP1 blocks tumorigenesis induced by RET oncogenes. Cancer Res. 62: 1077-1082