Multiple Mechanisms of p16INK4A Inactivation in Non-Small Cell Lung Cancer Cell Lines

Cancer Research

Volumn 55, Issue 24, 1995, Pages 6200-6209

  Shapiro, Geoffrey I ^a   Park, Julie E ^a   Edwards, Christian D ^a   Mao, Li ^b   Merlo, Adrian ^b   Sidransky, David ^b   Ewen, Mark E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CDK4 PROTEIN, HUMAN; CDK6 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; DNA; MESSENGER RNA; ONCOPROTEIN; PROTEIN P16INK4A; PROTEIN SERINE THREONINE KINASE; RETINOBLASTOMA PROTEIN; RNA; SPHINGOLIPID ACTIVATOR PROTEIN 2;

ARTICLE; CELL CULTURE; CELL CYCLE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LUNG NON SMALL CELL CANCER; LUNG TUMOR; METABOLISM; METHYLATION; PATHOLOGY; TUMOR SUPPRESSOR GENE; ENZYME INACTIVATION; ENZYME INHIBITION; GENE LOCUS; GENE REARRANGEMENT; GROWTH INHIBITION; HUMAN CELL; INTRON; POINT MUTATION; PRIORITY JOURNAL;

CARCINOMA, NON-SMALL-CELL LUNG; CARRIER PROTEINS; CELL CYCLE; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE 6; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASES; DNA, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; LUNG NEOPLASMS; METHYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RETINOBLASTOMA PROTEIN; RNA, MESSENGER; RNA, NEOPLASM; SEQUENCE DELETION; TUMOR CELLS, CULTURED;

EID: 0028971961     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Sherr, C. J. G1 phase progression: cycling on cue. Cell, 79: 551–555, 1994.
2. Morgan, D. O. Principles of CDK regulation. Nature (Lond.), 374: 131–134, 1995.
3. Hirama, T., and Koeffler, H. P. Role of the cyclin-dependent kinase inhibitors in the development of cancer. Blood, 86: 841–854, 1995.
4. 1 cyclin-dependent kinases. Genes Dev., 9: 1149–1163, 1995.
5. El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817–825, 1993.
6. 1 cyclin-dependent kinases. Cell, 75: 805–816, 1993.
7. Xiong, Y., Harmon, G. J., Zhang, H., Casso, D., Kobayashi, R. and Beach, D. p21 is a universal inhibitor of cyclin kinases. Nature (Lond.), 366: 701–704, 1993.
8. INK4B/ MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Dev., 8: 2939–2952, 1994.
9. INK4. Mol. Cell. Biol., 15: 2682–2688, 1995.
10. Hirai, H., Roussel, M. F., Kato, J., Ashmun, R. A., and Sherr, C. J. Novel INK4 proteins, p18 and p19, are specific inhibitors of cyclin D-dependent kinases CDK4 and CDK6. Mol. Cell. Biol., 15: 2672–2681, 1995.
11. INK4B is a potential effector of TGF-β-induced cell cycle arrest. Nature (Lond.), 371: 257–261, 1994.
12. Serrano, M., Hannon, G. J., and Beach, D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature (Lond.), 366: 704–707, 1993.
13. Jiang, W., Kahn, S. M., Tomita, N., Zhang, Y., Lu, S., and Weinstein, I. B. Amplification and expression of the human cyclin D gene in esophageal cancer. Cancer Res., 52: 1980–1983, 1992.
14. Seto, M., Yamamoto, K., Iida, S., Akao, Y., Utsumi, K. R., Kubonishi, I., Miyoshi, I., Ohtsuki, T., Yawata, Y., and Namba, M. Gene rearrangement and overexpression of PRAD1 in lymphoid malignancy with t(11;140(q13;q32) translocation. Oncogene, 7: 1401–1406, 1992.
15. Faust, J. B., and Meeker, T. C. Amplification and expression of the bcl-1 gene in human solid tumor cell lines. Cancer Res., 52: 2460–2463, 1992.
16. Gillett, C., Fantl, V., Smith, R., Fisher, C., Bartek, J., Dickson, C., Barnes, D., and Peters, G. Amplification and overexpression of cyclin D1 in breast cancer detected by immunohistochemical staining. Cancer Res., 54: 1812–1817, 1994.
17. Hunter, T., and Pines, J. Cyclins and cancer II: cyclin D and cdk inhibitors come of age. Cell, 79: 573–582, 1994.
18. Motokura, T., Bloom, T., Kim, H. G., Juppner, H., Ruderman, J. V., Kronenberg, H. M., and Arnold, A. A novel cyclin encoded by a bcl/-linked candidate oncogene. Nature (Lond.), 350: 512–515, 1991.
19. Hinds, P. W., Dowdy, S. F., Eaton, E. N., Arnold, A., and Weinberg, R. A. Function of a human cyclin gene as an oncogene. Proc. Natl. Acad. Sci. USA, 91: 709–713, 1994.
20. Wang, T. C., Cardiff, R. D., Zukerberg, L., Lees, E., Arnold, A., and Schmidt, E. V. Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature (Lond.), 369: 669–671, 1994.
21. He, J., Allen, J. R., Collins, V. P., Allalunis-Turner, M. J., Godbout, R., Day, R. S., III, and James, C. D. CDK4 amplification is an alternative mechanism to pl6 gene homozygous deletion in glioma cell lines. Cancer Res., 54: 5804–5807, 1994.
22. Schmidt, E. E., Ichimura, K., Reifenberger, G., and Collins, V. P. CDKN2 (p16/MTS1) gene deletion or CDK4 amplification occurs in the majority of glioblastomas. Cancer Res., 54: 6321–6324, 1994.
23. INK4 expression is frequent in high grade gliomas. Cancer Res., 55: 1941–1945, 1995.
24. INK4A as a human tumor suppressor. BBA Rev. Cancer, in press, 1995.
25. Kamb, A. Cell-cycle regulators and cancer. Trends Genet., 11: 136–140, 1995.
26. Nobori, T., Miura, K., Wu, D. J., Lois, A., Takabayashi, K., and Carson, D. A. Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature (Lond.), 368: 753–756, 1994.
27. Kamb, A., Gruis, N. A., Weaver-Feldhaus, J., Liu, Q., Harshman, K., Tavtigian, S. V., Stocjert, E., Day, R. S. I., Johnson, B. E., and Skolnick, M. H. A cell cycle regulator potentially involved in genesis of many tumor types. Science (Washington DC), 264: 436–440, 1994.
28. Moulton, T., Samara, G., Chung, W. Y., Yuan, L., Desai, R., Sisti, M., Bruce, J., and Tycko, B. MTS1/p16/CDKN2 lesions in primary glioblastoma multiforme. Am. J. Pathol., 146: 613–619, 1995.
29. Walker, D. G., Duan, W., Popvic, E. A., Kaye, A. H., Tomlinson, F. H., and Lavin, M. Homozygous deletions of the multiple tumor suppressor gene 1 in progression of human astrocytomas. Cancer Res., 55: 20–23, 1995.
30. Giani, C., and Finocchiaro, G. Mutation rate of the CDKN2 gene in malignant gliomas. Cancer Res., 54: 6338–6339, 1994.
31. Ueki, K., Rubio, M. P., Ramesh, V., Correa, K. M., Rutter, J. L., von, D. A., Buckler, A. J., Gusella, J. F., and Louis, D. N. MTS1/CDKN2 gene mutations are rare in primary human astrocytomas with allelic loss of chromosome 9p. Hum. Mol. Genet., 3: 1841–1845, 1994.
32. Dreyling, M. H., Bohlander, S. K., Adeyanju, M. O., and Olopade, O. I. Detection of CDKN2 deletions in tumor cell lines and primary glioma by interphase fluorescence in situ hybridization. Cancer Res., 55: 984–988, 1995.
33. INK4B) display frequent homozygous deletions in primary cells from T- but not from B-cell lineage acute lymphoblastic leukemias. Blood, 84: 4038–4044, 1994.
34. INK4b/MTS2 in pediatric acute lymphoblastic leukemia. Blood, 85: 2321–2330, 1995.
35. Quesnel, B., Preudhomme, C., Philippe, N., Vanrumbeke, M., Dervite, I., Lai, J. L., Bauters, F., Wattel, E., and Fenaux, P. pl6 gene homozygous deletions in acute lymphoblastic leukemia. Blood, 85: 657–663, 1995.
36. Sill, H., Goldman, J. M., and Cross, N. C. Homozygous deletions of the pi6 tumor-suppressor gene are associated with lymphoid transformation of chronic myeloid leukemia. Blood, 85: 2013–2016, 1995.
37. Stranks, G., Height, S. E., Mitchell, P., Jadayel, D., Yuille, M. A., De, L. C., Clutterbuck, R. D., Treleaven, J. G., Powles, R. L., Nacheva, E., Oscier, D. G., Karpas, A., Lenoir, G. M., Smith, S. D., Millar, J. L., Catovsky, D., and Dyer, M. J. S. Deletions and rearrangement of CDKN2 in lymphoid malignancy. Blood, 85: 893– 901, 1995.
38. INK4B/MTS2 in human leukemias and lymphomas. Cancer Res., 55: 1436–1440, 1995.
39. Hatta, Y., Hirama, T., Miller, C. W., Yamada, Y., Tomonaga, M., and Koeffler, H. P. Homozygous deletions of the p15 (MTS2) and p16 (CDKN2/MTS1) genes in adult T-cell leukemia. Blood, 85: 2699–2704, 1995.
40. Hussussian, C. J., Struewing, J. P., Goldstein, A. M., Higgins, P. A., Ally, D. S., Sheahan, M. D., Clark, W. J., Tucker, M. A., and Dracopoli, N. C. Germline p16 mutations in familial melanoma. Nat. Genet., 8: 15–21, 1994.
41. INK4 function. Nat. Genet., 10: 114–116, 1995.
42. Kamb, A., Shattuck-Eidens, D., Eeles, R., Liu, Q., Gruis. N. A., Ding, W., Hussey, C., Tran, T., Miki, Y., Weaver-Feldhaus, J., McClure, M., Aitken, J. F., Anderson, D. E., Bergman, W., Frants, R., Goldgar, D. E., Green, A., MacLennan, R., Martin, N. G., Meyer, L. J., Youl, P., Zone, J. J., Skolnick, M. H., and Cannon-Albright, L. A. Analysis of the p16 gene (CDKN2) as a candidate for the chromosome 9p melanoma susceptibility locus. Nat. Genet., 8: 22–26, 1994.
43. Caldas, C., Hahn, S. A., da Costa, L. T., Redston, M. S., Schutte, M., Seymour, A. B., Weinstein, C. L., Hrubam, R. H., Yeo, C. J., and Kern, S. E. Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat. Genetics, 8: 27–32, 1994.
44. Zhou, X., Tarmin, L., Yin, J., Jiang, H. Y., Suzuki, H., Rhyu, M. G., Abraham, J. M., and Meltzer, S. J. The MTS1 gene is frequently mutated in primary human esophageal tumors. Oncogene, 9: 3737–3741, 1994.
45. Mori, T., Miura, K., Aoki, T., Nishihira, T., Mori, S., and Nakamura, Y. Frequent somatic mutation of the MTS1/CDK41 (multiple tumor suppressor/cyclin-dependent kinase 4 inhibitor) gene in esophageal squamous cell carcinoma. Cancer Res., 54: 3396–3397, 1994.
46. INK4 gene mediated by an adenovirus vector. Cancer Res., 55: 3250–3253, 1995.
47. ink4 requires functional retinoblastoma protein. Proc. Natl. Acad. Sci. USA, 92: 6289–6293, 1995.
48. Arap, W., Nishikawa, R., Furnari, F. B., Cavenee, W. K., and Huang, H. J. S. Replacement of the p16/CDKN2 gene suppresses human glioma cell growth. Cancer Res., 55: 1351–1354, 1995.
49. INK4. Science (Washington DC), 267: 249–252, 1995.
50. Koh, J., Enders, G. H., Dynlacht, B. D., and Harlow, E. Tumor-derived p16 alleles encoding proteins defective in cell-cycle inhibition. Nature (Lond.), 375: 506–510, 1995.
51. Lukas, J., Parry, D., Aagaard, L., Mann, D. J., Bartkova, J., Strauss, M., Peters, G., and Bartek, J. Retinoblastoma-protein-dependent cell cycle inhibition by the tumor suppressor pi6. Nature (Lond.), 375: 503–506, 1995.
52. INK4 expression in primary lung cancers and cell lines. Cancer Res., 55: 505–509, 1995.
53. INK4 protein is restricted to the subset of lung cancer lines that retains wildtype RB. Oncogene, 9: 3375–3378, 1994.
54. Okamoto, A., Demetrick, D. J., Spillare, E. A., Hagiwara, K., Hussain, S. P., Bennett, W. P., Forrester. K., Gerwin, B., Serrano, M., Beach, D. H., and Harris, C. C Mutations and altered expression of pI6INK4 in human cancer. Proc. Natl. Acad. Sci. USA, 91: 11045–11049, 1994.
55. Cairns, P., Polascik, T. J., Eby, Y., Tokino, K., Califano, J., Merlo, A., Mao, L., Herath, J., Jenkins. R., Westra, W., Rutter, J. L., Buckler, A., Gabrielson, E., Tockman, M., Cho, K. R., Hedrick, L., Bova, G. S., Isaacs, W., Schwab, D., and Sidransky, D. Frequency of homozygous deletion at p16/CDKN2 in primary human tumors. Nat. Genet., 11: 210–212, 1995.
56. Liu, Q., Neuhausen, S., McClure, M., Frye, C., Weaver-Feldhaus, J., Gruis, N. A., Eddington, K., Allalunis-Turner, M. J., Skolnick, M. H., Fujimura, F. K., and Kamb, A. CDKN2 (MTS1) tumor suppressor gene mutations in human tumor cell lines. Oncogene, 10: 1061–1067, 1995.
57. Hayashi, N., Sugimoto, Y., Tsuchiya, E., Ogawa, M., and Nakamura, Y. Somatic mutations of the MTS (multiple tumor suppressor) 1/CDK41 (cyclin-dependent kinase-4 inhibitor) gene in human primary non-small cell lung carcinomas. Biochem. Biophys. Res. Commun., 202: 1426–1430, 1994.
58. Merlo, A., Herman, J. G., Mao, L., Lee, D. J., Gabrielson, E., Burger, P. C., Baylin, S. B., and Sidransky, D. 5′ CpG island methylation is associated with transcriptional silencing of the tumor suppressor p16/CDKN2/MTSl in human cancers. Nat. Med., 7: 686–692, 1995.
59. Mao, L., Merlo, A., Bedi, G., Shapiro, G. I., Edwards, C. D., Rollins, B. J., and Sidransky, D. A novel pl6,NK4A transcript. Cancer Res., 55: 2995–2997, 1995.
60. Stone, S. S., Jiang, P., Dyananth, P., Tavtigian, S. V., Katcher, H., Parry, D., Peters, G., and Kamb, A. Complex structure and regulation of the p16 (MTS1) locus. Cancer Res., 55: 2988–2994, 1995.
61. Ohta, M., Nagai, H., Shimizu, M., Rasio, D., Berd, D., Mastrangelo, M., Singh, A. D., Shields, J. A., Shields, C. L., Croce, C. M., and Huebner, K. Rarity of somatic and germline mutations of the cyclin-dependent kinase 4 inhibitor gene, CDK41, in melanoma. Cancer Res., 54: 5269–5272, 1994.
62. Vairo, G., Livingston, D. M., and Ginsberg, D. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev., 9: 869–881, 1995.
63. Morgenstern, J. P., and Land, H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res., 18: 3587–3596, 1990.
64. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (eds.) Current Protocols in Molecular Biology, pp. 2.03–2.14.3. New York: John Wiley & Sons, 1993.
65. INK4B/ MTS2, and p18 genes in primary and metastatic lung cancer. Cancer Res., 55: 1448–1451, 1995.
66. Washimi, O., Nagatake, M., Osada, H., Ueda, R., Koshikawa, T., Seki, T., Takahashi, T., and Takahashi, T. In vivo occurrence of p16 (MTS1) and p15 (MTS2) alterations preferentially in non-small cell lung cancer. Cancer Res., 55: 514–517, 1995.
67. Xiao, S., Li, D., Corson, J. M., Vijg, J., and Fletcher, J. A. Codeletion of p15 and pi6 genes in primary non-small cell lung carcinoma. Cancer Res., 55: 2968–2971, 1995.
68. Zhang, S. Y., Klein-Szanto, A. J. P., Sauter, E. R., Shafarenko, M., Mitsunaga, S., Nobori, T., Carson, D. A., Ridge, J. A., and Goodrow, T. Higher frequency of alterations in the p16/CDKN2 gene in squamous cell carcinoma lines that in primary tumors of the head and neck. Cancer Res., 54: 5151–5153, 1994.
69. INK4a tumor suppressor protein. Cancer Res., 55: 2503–2506, 1995.