Somatic mutations in RET exons 12 and 15 in sporadic medullary thyroid carcinomas: Different spectrum of mutations in sporadic type from hereditary type

Japanese Journal of Cancer Research

Volumn 90, Issue 11, 1999, Pages 1231-1237

  Uchino, Shinya ^a   Noguchi, Shiro ^a   Yamashita, Hiroto ^a   Sato, Mari ^a   Adachi, Mitsuo ^a   Yamashita, Hiroyuki ^a   Watanabe, Shin ^a   Ohshima, Akira ^a   Mitsuyama, Shoshu ^b   Iwashita, Toshihide ^c   Takahashi, Masahide ^c  

^a Noguchi Thyroid Clin/Hosp Found   (Japan)

^b KITAKYUSHU MUNICIPAL MEDICAL CENTER   (Japan)

^c NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Multiple endocrine neoplasia; Point mutation; RET gene; Sporadic medullary thyroid carcinoma; Tyrosine kinase domain

Indexed keywords

DNA; FORMALDEHYDE;

ARTICLE; CANCER RECURRENCE; CLINICAL ARTICLE; CODON; DNA SEQUENCE; EXON; GENE DELETION; GENE MUTATION; GERM LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; LEUKOCYTE; MULTIPLE ENDOCRINE ADENOMATOSIS; POINT MUTATION; PRIORITY JOURNAL; PROGNOSIS; PROTO ONCOGENE; SOMATIC MUTATION; THYROID GLAND; THYROID MEDULLARY CARCINOMA;

EID: 0032762050     PISSN: 09105050     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1349-7006.1999.tb00701.x     Document Type: Article

References (49)

1. Mulligan, L. M., Kwok, J. B. J., Healey, C. S., Elsdon, M. J., Eng, C., Gardner, E., Love, D. R., Mole, S. E., Moore, J. K., Papi, L., Ponder, M. A., Telenius, H., Tunnacliffe, A. and Ponder, B. A. J. Germ-line mutations of the RET proto-oncogene in multiple endocrine neoplasia type 2A. Nature, 363, 458-460 (1993).
2. Goodfellow, P. J. and Wells, S. A., Jr. RET gene and its implications for cancer. J. Natl. Cancer Inst., 87, 1515-1523 (1995).
3. Takahashi, M., Ritz, J. and Cooper, G. M. Activation of a novel human transforming gene. RET, by DNA rearrangement. Cell, 42, 581-588 (1985).
4. Pierotti, M. A., Santoro, M., Jenkins, R. B., Sozzi, G., Bongarzon, I., Grieco, M., Monzini, N., Miozzo, M., Herrmann, M. A., Fusco, A., Hay, I. D., Delia Porta, G. and Vecchio, G. Characterization of an inversion on the long arm of chromosome 10 juxtaposing D10S170 and RET and creating the oncogenic sequence RET/PTC. Proc. Natl. Acad. Sci. USA, 89, 1616-1620 (1992).
5. Bongarzone, I., Monzini, N., Borrello, M. G., Carcano, C., Ferraresi, G., Arighi, E., Mondellini, P., Della Porta, G. and Pierotti, M. A. Molecular characterization of a thyroid tumor-specific transforming sequence formed by the fusion of RET tyrosine kinase and the regulatory subunit R1α of cyclic AMP-dependent protein kinase A. Mol. Cell. Biol., 13, 358-366 (1993).
6. Bongarzone, I., Butti, M. G., Coronelli, S., Borrello, M. G., Santoro, M., Mondellini, P., Pilotti, S., Fusco, A., Della Porta, G. and Pierotti, M. A. Frequent activation of RET protooncogene by fusion with a new activating gene in papillary thyroid carcinomas. Cancer Res., 54, 2979-2985 (1994).
7. Jhiang, S. M., Smanik, P. A. and Mazzaferri, E. L. Development of a single-step duplex RT-PCR detecting different forms of RET activation, and identification of the third form of in vivo RET activation in human papillary thyroid carcinoma. Cancer Lett., 78, 69-76 (1994).
8. Fugazzola, L., Pierotti, M. A., Vigano, E., Pacini, F., Vorontsova, T. V. and Bongarzone, I. Molecular and biochemical analysis of RET/PTC4, a novel oncogenic rearrangement between RET and ELEI genes, in a post-Chernobyl papillary thyroid cancer. Oncogene, 13, 1093-1097 (1996).
9. Klugbauer, S., Demidchik, E. P., Lengfelder, E. and Rabes, H. M. Detection of a novel type of RET rearrangement (PTC5) in thyroid carcinomas after Chernobyl and analysis of the involved RET-fused gene RFG5. Cancer Res., 58, 198-203 (1998).
10. Eng, C., Clayton, D., Schuffenecker, I., Lenoir, G., Cote, G., Gagel, R. F., van Amstel, H. K. P., Lips, C. J. M., Nishisho, I., Takai, S., Marsh, D. J., Robinson, B. G., Frank-Raue, K., Raue, F., Xue, F., Noll, W. W., Romei, C., Pacini, F., Fink, M., Niederle, B., Zedenius, J., Nordenskjöld, M., Komminoth, P., Hendy, G. N., Gharib, H., Thibodeau, S. N., Lacroix, A., Frilling, A., Ponder, B. A. J. and Mulligan, L. M. The relationship between specific RET proto-oncogene mutations and disease phenotype in multiple endocrine neoplasia type 2. International RET mutation consortium analysis. JAMA, 276, 1575-1579 (1996).
11. Berndt, I., Reuter, M., Saller, B., Frank-Raue, K., Groth, P., Grubendorf, M., Raue, F., Ritter, M. M. and Höppner, W. A new hot spot for mutations in the ret protooncogene causing familial medullary thyroid carcinoma and multiple endocrine neoplasia type 2A. J. Clin. Endocrinol. Metab., 83, 770-774 (1998).
12. Hofstra, R. M. W., Landsvater, R. M., Ceccherini, I., Stulp, R. P., Stelwagen, T., Luo, Y., Pasini, B., Höppener, J. W. M., van Amstel, H. K. P., Romeo, G., Lips, C. J. M. and Buys, C. H. C. M. A mutation in the RET proto-oncogene associated with multiple endocrine neoplasia type 2B and sporadic medullary thyroid carcinoma. Nature, 367, 375-376 (1994).
13. Carlson, K. M., Dou, S., Chi, D., Scavarda, N., Toshima, K., Jackson, C. E., Wells, S. A., Jr., Goodfellow, P. J. and Donis-Keller, H. Single missense mutation in the tyrosine kinase catalytic domain of the RET protooncogene is associated with multiple endocrine neoplasia type 2B. Proc. Natl. Acad. Sci. USA, 91, 1579-1583 (1994).
14. Blaugrund, J. E., Johns, M. J., Eby, Y. J., Ball, D. W., Baylin, S. B., Hruban, R. H. and Sidransky, D. RET proto-oncogene mutations in inherited and sporadic medullary thyroid cancer. Hum. Mol. Genet., 3, 1895-1897 (1994).
15. Gimm, O., Marsh, D. J., Andrew, S. D., Frilling, A., Dahia, P. L., Mulligan, L. M., Zajac, J. D., Robinson, B. G. and Eng, C. Germline dinucleotide mutation in codon 883 of the RET proto-oncogene in multiple endocrine neoplasia type 2B without codon 918 mutation. J. Clin. Endocrinol. Metab., 82, 3902-3904 (1997).
16. Smith, D. P., Houghton, C. and Ponder, B. A. J. Germline mutation of RET codon 883 in two cases of de novo MEN 2B. Oncogene, 15, 1213-1217 (1997).
17. Miyauchi, A., Futami, H., Hai, N., Yokozawa, T., Kuma, K., Aoki, N., Kosugi, S., Sugano, K. and Yamaguchi, K. Two germline missense mutations at codons 804 and 806 of the RET proto-oncogene in the same allele in a patient with multiple endocrine neoplasia type 2B without codon 918 mutation. Jpn. J. Cancer Res., 90, 1-5 (1999).
18. Komminoth, P., Kunz, E. K., Matias-Guiu, X., Hiort, O., Christiansen, G., Colomer, A., Roth, J. and Heitz, P. U. Analysis of RET protooncogene point mutations distinguishes heritable from nonheritable medullary thyroid carcinomas. Cancer, 76, 479-489 (1995).
19. Kitamura, Y., Goodfellow, P. J., Shimizu, K., Nagahama, M., Ito, K., Kitagawa, W., Akasu, H., Takami, H., Tanaka, S. and Wells, S. A., Jr. Novel germline RET proto-oncogene mutations associated with medullary thyroid carcinoma (MTC): mutation analysis in Japanese patients with MTC. Oncogene, 14, 3103-3106 (1997).
20. Eng, C., Smith, D. P., Mulligan, L. M., Healey, C. S., Zvelebil, M. J., Stonehouse, T. J., Ponder, M. A., Jackson, C. E., Waterfield, M. D. and Ponder, B. A. J. A novel point mutation in the tyrosine kinase domain of the RET proto-oncogene in sporadic medullary thyroid carcinoma and in a family with FMTC. Oncogene, 10, 509-513 (1995).
21. Bolino, A., Schuffenecker, I., Luo, Y., Seri, M., Silengo, M., Tocco, T., Chabrier, G., Houdent, C., Murat, A., Schlumberger, M., Tourniaire, J., Lenoir, G. M. and Romeo, G. RET mutations in exons 13 and 14 of FMTC patients. Oncogene, 10, 2415-2419 (1995).
22. Fink, M., Weinhäusel, A., Niederle, B. and Haas, O. A. Distinction between sporadic and hereditary medullary thyroid carcinoma (MTC) by mutation analysis of the RET proto-oncogene. Int. J. Cancer, 69, 312-316 (1996).
23. Hofstra, B. M. W., Fattoruso, O., Quadro, L., Wu, Y., Libroia, A., Verga, U., Colantuoni, V. and Buys, C. H. C. M. A novel point mutation in the intracellular domain of the ret protooncogene in a family with medullary thyroid carcinoma. J. Clin. Endocrinol. Metab., 82, 4176-4178 (1997).
24. Bugalho, M. J., Frade, J. P., Santos, J. R., Limbert, E. and Sobrinho, L. Molecular analysis of the RET proto-oncogene in patients with sporadic medullary thyroid carcinoma: a novel point mutation in the extracellular cysteine-rich domain. Eur. J. Endocrinol., 136, 423-426 (1997).
25. Romei, C., Elisei, R., Pinchera, A., Ceccherini, I., Molinaro, E., Mancusi, F., Martino, E., Romeo, G. and Pacini, F. Somatic mutations of the RET protooncogene in sporadic medullary thyroid carcinoma are not restricted to exon 16 and are associated with tumor recurrence. J. Clin. Endocrinol. Metab., 81, 1619-1622 (1996).
26. Donis-Keller, H., Dou, S., Chi, D., Carlson, K. M., Toshima, K., Lairmore, T. C., Howe, J. R., Moley, J. F., Goodfellow, P. and Wells, S. A., Jr. Mutations in the RET proto-oncogene are associated with MEN 2A and FMTC. Hum. Mol. Genet., 2, 851-856 (1993).
27. Hofstra, R. M. W., Stelwagen, T., Stulp, R. P., de Jong, D., Hulsbeek, M., Kamsteeg, E. J., van den Berg, A., Landsvater, R. M., Vermey, A., Molenaar, W. M., Lips, C. J. M. and Buys, C. H. C. M. Extensive mutation scanning of RET in sporadic medullary thyroid carcinoma and of RET and VHL in sporadic pheochromocytoma reveals involvement of these genes in only a minority of cases. J. Clin. Endocrinol. Metab., 81, 2881-2884 (1996).
28. Ceecherini, I., Pacini, B., Pucini, F., Gullo, M. Bongarzone, I., Romei, C., Santamaria, G., Matera, I., Mondellini, P., Scopsi, L., Pinchera, A., Pierotti, M. A. and Romeo, G. Somatic in-frame deletions not involving juxtamembranous cysteine residues strongly activate the RET proto-oncogene. Oncogene, 14, 2609-2612 (1997).
29. Alemi, M., Lucas, S. D., Sällström, J. F., Bergholm, U., Åkerström, G. and Wilander, E. A complex nine base pair deletion in RET exon 11 common in sporadic medullary thyroid carcinoma. Oncogene, 14, 2041-2045 (1997).
30. Marsh, D. J., Learoyd, D. L., Andrew, S. D., Krishnan, L., Pojer, R., Richardson, A. L., Delbridge, L., Eng, C. and Robinson, B. G. Somatic mutations in the RET proto-oncogene in sporadic medullary thyroid carcinoma. Clin. Endocrinol. (Oxf), 44, 249-257 (1996).
31. Eng, C., Mulligan, L. M., Smith, D. P., Healey, C. S., Frilling, A., Raue, F., Neumann, H. P. H., Pfragner, R., Behmel, A., Lorenzo, M. J., Stonehouse, T. J., Ponder, M. A. and Ponder, B. A. J. Mutation of the RET protooncogene in sporadic medullary thyroid carcinoma. Genes Chromosom. Cancer, 12, 209-212 (1995).
32. Marsh, D. J., Andrew, S. D., Eng, C., Learoyd, D. L., Capes, A. G., Pojer, R., Richardson, A. L., Houghton, C., Mulligan, L. M., Ponder, B. A. J. and Robinson, B. G. Germline and somatic mutations in an oncogene: RET mutations in inherited medullary thyroid carcinoma. Cancer Res., 56, 1241-1243 (1996).
33. Zedenius, J., Larsson, C., Bergholm, U., Bovee, J., Svensson, A., Hallengren, B., Grimelius, L., Backdahl, M., Weber, G. and Wallin, G. Mutations of codon 918 in the RET proto-oncogene correlate to poor prognosis in sporadic medullary thyroid carcinomas. J. Clin. Endocrinol. Metab. 80, 3088-3090 (1995).
34. Jhiang, S. M., Fithian, L., Weghorst, C. M., Clark, O. H., Falko, J. M., O'Dorisio, T. M. and Mazzaferri, E. L. RET mutation screening in MEN2 patients and discovery of a novel mutation in a sporadic medullary thyroid carcinoma. Thyroid, 6, 115-121 (1996).
35. Uchino, S., Noguchi, S., Adachi, M., Sato, M., Yamashita, H., Watanabe, S., Murakami, T., Toda, M., Murakami, N. and Yamashita, H. Novel point mutations and allele loss at the RET locus in sporadic medullary thyroid carcinomas. Jpn. J. Cancer Res. 89, 411-418 (1998).
36. Uchino, S., Noguchi, S., Sato, M., Adachi, M., Yamashita, H., Watanabe, S., Murakami, T., Toda, M., Murakami, N. and Yamashita, H. RET gene analysis of latent small medullary thyroid carcinoma associated with Graves' disease. Thyroidol. Clin. Exp., 10, 279-281 (1998).
37. Ceecherini, I., Hofstra, R. M. W., Luo, Y., Stulp, R. P., Barone, V., Stelwagen, T., Bocciardi, R., Nijveen, H., Bolino, A., Seri, M., Ronchetto, P., Pasini, B., Bozzano, M., Buys, C. H. C. M. and Romeo, G. DNA polymorphisms and conditions for SSCP analysis of the 20 exons of the RET proto-oncogene. Oncogene, 9, 3025-3029 (1994).
38. Komminoth, P., Roth, J., Muletta-Feurer, S., Saremaslani, P., Seelentag, W. K. F. and Heitz, P. U. RET proto-oncogene point mutations in sporadic neuroendocrine tumors. J. Clin. Endocrinol. Metab., 81, 2041-2046 (1996).
39. Santoro, M., Carlomagno, F., Romuno, A., Bottaro, D. P., Dathan, N. A., Grieco, M., Fusco, A., Vecchio, G., Matoskova, B., Kraus, M. H. and Di Fiore, P. P. Activation of RET as a dominant transforming gene by germline mutations of MEN2A and MEN2B. Science, 267, 381-383 (1995).
40. Xing, S., Smanik, P. A., Oglesbee, M. J., Trosko, J. E., Mazzaferri, E. L. and Jhiang, S. M. Characterization of RET oncogenic activation in MEN2 inherited cancer syndromes. Endocrinology, 137, 1512-1519 (1996).
41. Hanks, S. K., Quinn, A. M. and Hunter, T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science, 241, 42-52 (1988).
42. Eng, C. The RET proto-oncogene in multiple endocrine neoplasia type 2 and Hirschsprung's disease. N. Engl. J. Med., 335, 943-951 (1996).
43. Borrello, M. G., Smith, D. P., Pasini, B., Bongarzone, I., Greco, A., Lorenzo, M. J., Arighi, E., Miranda, C., Eng, C., Alberti, L., Bocciardi, R., Mondellini, P., Scopsi, E., Romeo, G., Ponder, B. A. J. and Pierotti, M. A. RET activation by germline MEN2A and MEN2B mutations. Oncogene, 11, 2419-2427 (1995).
44. Komminoth, P., Muletta-Feurer, S., Saremaslani, P., Kunz, E. K., Matias-Guiu, X., Hiort, O., Schroder, S., Seelentag, W. K. F., Roth, J. and Heitz, P. U. Molecular diagnosis of multiple endocrine neoplasia (MEN) in paraffin-embedded specimens. Endocr. Pathol., 6, 267-278 (1995).
45. Shan, L., Nakamura, M., Nakamura, Y., Utsunomiya, H., Shou, N., Jiang, X., Jing, X., Yokoi, T. and Kakudo, K. Somatic mutations in the RET protooncogene in Japanese and Chinese sporadic medullary thyroid carcinomas. Jpn. J. Cancer Res., 89, 883-886 (1998).
46. Maeda, S., Namba, H., Takamura, N., Tanigawa, K., Takahashi, M., Noguchi, S., Nagataki, S., Kanematsu, T. and Yamashita, S. A single missense mutation in codon 918 of the RET proto-oncogene in sporadic medullary thyroid carcinomas. Endocr. J., 42, 245-250 (1995).
47. Piao, X., Paulson, R., van der Geer, P., Pawson, T. and Bernstein, A. Oncogenic mutation in the Kit receptor tyrosine kinase alters substrate specificity and induces degradation of the protein tyrosine phosphatase SHP-1. Proc. Natl. Acad. Sci. USA, 93, 14665-14669 (1996).
48. Webster, M. K., d'Avis, P. Y., Robertson, S. C. and Donoghue, D. J. Profound ligand-independent kinase activation of fibroblast growth factor receptor 3 by the activation loop mutation responsible for a lethal skeletal dysplasia, thanatophoric dysplasia type II. Mol. Cell. Biol., 16, 4081-4087 (1996).
49. Iwashita, T., Kato, M., Murukumi, H., Asai, N., Ishiguro, Y., Ito, S., Iwata, Y., Kawai, K., Asai, M., Kurokawa, K., Kajita, H. and Takahashi, M. 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 (1999).