MXI1, a putative tumor suppressor gene, suppresses growth of human glioblastoma cells

Cancer Research

Volumn 57, Issue 21, 1997, Pages 4905-4912

  Wechsler, Daniel S ^a,c   Shelly, Candace A ^a   Petroff, Christy A ^a   Dang, Chi V ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSATELLITE DNA;

ARTICLE; ASTROCYTE; BRAIN TUMOR; CANCER GROWTH; CELL CYCLE; CELL PROLIFERATION; CHROMOSOME 10Q; EXON; GENE MAPPING; GLIOBLASTOMA; GROWTH INHIBITION; HUMAN; HUMAN CELL; ONCOGENE C MYC; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TUMOR SUPPRESSOR GENE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIVISION; CHROMOSOMES, HUMAN, PAIR 10; DEXAMETHASONE; DNA-BINDING PROTEINS; G2 PHASE; GENE DELETION; GENES, TUMOR SUPPRESSOR; GENETIC VECTORS; GLIOBLASTOMA; GLUCOCORTICOIDS; HUMANS; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 0030784940     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Dang, C. V., and Lee, L. A. c-MYC Function in Neoplasia, p. 196. Austin, TX: R. G. Landes Company, 1995.
2. Henriksson, M., and Lüscher, B. Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv. Cancer Res., 68: 109-182, 1996.
3. Blackwood, E. M., and Eisenman, R. N. Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science (Washington DC), 251: 1211-1217, 1991.
4. Prendergast, G. C., Lawe, D., and Ziff, E. B. Association of Myn, the murine homolog of max, with c-Myc stimulates methylation-sensitive DNA binding and ras cotransformation. Cell, 65: 395-407, 1991.
5. Kato, G. J., Lee, W. M., Chen, L. L., and Dang, C. V. Max: functional domains and interaction with c-Myc. Genes Dev., 6: 81-92, 1992.
6. Blackwood, E. M., Lüscher, B., and Eisenman, R. N. Myc and Max associate in vivo. Genes Dev., 6: 71-80, 1992.
7. Eilers, M., Schirm, S., and Bishop, J. M. The MYC protein activates transcription of the alpha-prothymosin gene. EMBO J., 10: 133-141, 1991.
8. Bello-Fernandez, C., and Cleveland, J. L. c-myc transactivates the ornithine decarhoxylase gene. Curr. Top. Microbiol. Immunol., 782: 445-452, 1992.
9. Bello-Fernandez, C., Packham, G., and Cleveland, J. L. The ornithine decarboxylase gene is a transcriptional target of c-Myc. Proc. Natl. Acad. Sci. USA, 90: 7804-7808, 1993.
10. Jansen-Durr, P., Meichle, A., Steiner, P., Pagano, M., Finke, K., Botz, J., Wessbecher, J., Draetta, G., and Eilers, M. Differential modulation of cyclin gene expression by MYC. Proc. Natl. Acad. Sci. USA, 90: 3685-3689, 1993.
11. Hoang, A. T., Cohen, K. J., Barrett, J. F., Bergstrom, D. A., and Dang, C. V. Participation of cyclin A in Myc-induced apoptosis. Proc. Natl. Acad. Sci. USA, 91: 6875-6879, 1994.
12. Galaktionov, K., Chen, X., and Beach, D. Cdc25 cell-cycle phosphatase as a target of c-myc. Nature (Lond.), 382: 511-517, 1996.
13. Zervos, A. S., Gyuris, J., and Brent, R. Mxil, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell, 72: 223-232, 1993.
14. Ayer, D. E., Kretzner, L., and Eisenman, R. N. Mad: a heterodimeric partner for Max that antagonizes Myc transcriptional activity. Cell, 72: 211-222, 1993.
15. Hurlin, P. J., Queva, C., Koskinen, P. J., Steingrimsson, E., Ayer, D. E., Copeland, N. G., Jenkins, N. A., and Eisenman, R. N. Mad3 and Mad4: novel Max-interacting transcriptional repressors that suppress c-myc dependent transformation and are expressed during neural and epidermal differentiation. EMBO J., 14: 5646-5659, 1995.
16. Zervos, A. S., Gyuris, J., and Brent, R. Mxi1. a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell, 79: 389, 1994.
17. Albarosa, R., DiDonato, S., and Finocchiaro, G. Redefinition of the coding sequence of the MXI1 gene and identification of a polymorphic repeat in the 3′ non-coding region that allows the detection of loss of heterozygosity of chromosome 10q25 in glioblastomas. Hum. Genet., 95: 709-711, 1995.
18. Schreiber-Agus, N., Chin, L., Chen, K., Torres, R., Rao, G., Guida, P., Skoultchi, A. I., and DePinho, R. A. An amino-terminal domain of Mxi1 mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN3. Cell, 80: 777-786, 1995.
19. Lahoz, E. G., Xu, L., Schreiber-Agus, N., and DePinho, R. A. Suppression of Myc, but not E1a, transformation activity by Max-associated proteins, Mad and Mxil. Proc. Natl. Acad. Sci. USA, 91: 5503-5507, 1994.
20. Schreiber-Agus, N., Chin, L., Chen, K., Torres, R., Thomson, C. T., Sacchettini, J. C., and DePinho, R. A. Evolutionary relationships and functional conservation among vertebrate Max-associated proteins: the zebra fish homolog of Mxi1. Oncogene, 9: 3167-3177, 1994.
21. Cerni, C., Bousset, K., Seelos, C. Burkhardt, H., Henriksson, M., and Lüscher, B. Differential effects by Mad and Max on transformation by cellular and viral oncoproteins. Oncogene, 11: 587-596, 1995.
22. Chin, L., Schreiber-Agus, N., Pellicer, I., Chen, K., Lee, H. W., Dudast, M., Cordon Cardo, C., and DePinho, R. A. Contrasting roles for Myc and Mad proteins in cellular growth and differentiation. Proc. Natl. Acad. Sci. USA, 92: 8488-8492, 1995.
23. Koskinen, P. J., Ayer, D. E., and Eisenman, R. N. Repression of Myc-Ras cotransformation by Mad is mediated by multiple protein-protein interactions. Cell Growth Differ., 6: 623-629, 1995.
24. Vastrik, I., Kaipainen, A., Penttila, T. L., Lymboussakis, A., Alitalo, R., Parvinen, M., and Alitalo, K. Expression of the mad gene during cell differentiation inM vivo and its inhibition of cell growth in vitro. J. Cell Biol., 128: 1197-1208, 1995.
25. Larsson, L. G., Pettersson, M., Oberg, F., Nilsson, K., and Luscher, B. Expression of mad, mxil, max and c-myc during induced differentiation of hematopoietic cells: opposite regulation of mad and c-myc. Oncogene, 9: 1247-1252, 1994.
26. Delgado, M. D., Lerga, A., Canelles, M., Gomez Casares, M. T., and Leon, J. Differential regulation of Max and role of c-Myc during erythroid and myelomonocytic differentiation of K562 cells. Oncogene, 10: 1659-1665, 1995.
27. Gandarillas, A., and Watt, F. M. Changes in expression of members of the fos and jun families and myc network during terminal differentiation of human keratinocytes. Oncogene, 11: 1403-1407, 1995.
28. Meinhardt, G., and Hass, R. Differential expression of c-myc, max and mxi1 in human myeloid leukemia cells during retrodifferentiation and cell death. Leuk. Res., 19: 699-705, 1995.
29. Ayer, D. E., Lawrence, Q. A., and Eisenman, R. N. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell, 80: 767-776, 1995.
30. Rao, G., Alland, L., Guida, P., Schreiber-Agus, N., Chen, K., Chin, L., Rochelle, J. M., Seldin, M. F., Skoultchi, A. I., and DePinho, R. A. Mouse Sin3A interacts with and can functionally substitute for the amino-terminal repression of the Myc antagonist Mxil. Oncogene, 12: 1165-1172, 1996.
31. Harper, S. E., Qiu, Y., and Sharp, P. A. Sin3 corepressor function in Myc-induced transcription and transformation. Proc. Natl. Acad. Sci. USA, 93: 8536-8540, 1996.
32. Alland, L., Muhle, R., Hou, H. J., Potes, J., Chin, L., Schreiber-Agus, N., and DePinho, R. Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature (Lond.), 387: 49-55, 1997.
33. Heinzel, T., Lavinsky, R. M., Mullen, T. M., Soderstrom, M., Laherty, C. D., Torchia, J., Yang, W. M., Brard, G., Ngo, S. D., Davie, J. R., Seto, E., Eisenman, R. N., Rose, D. W., Glass, C. K., and Rosenfeld, M. G. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature (Lond.), 387: 43-48, 1997.
34. Hassig, C. A., Fleischer, T. C. Billin, A. N., Schreiber, S. L., and Ayer, D. E. Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell, 89: 341-347, 1997.
35. Laherty, C. D., Yang, W. M., Sun, J. M., Davie, J. R., Seto, E., and Eisenman, R. N. Histone deacelylases associated with the mSin3 corepressor mediate Mad transcriptional repression. Cell, 89: 349-356, 1997.
36. Wechsler, D. S., Hawkins, A. L., Li, X., Jabs, E. W., Griffin, C. A., and Dang, C. V. Localization of the human Mxi1 transcription factor gene (MXI1) to chromosome 10q24-q25. Genomics, 21: 669-672, 1994.
37. Edelhoff, S., Ayer, D. E., Zervos, A. S., Steingrimsson, E., Jenkins, N. A., Copeland, N. G., Eisenman, R. N., Brent, R., and Disteche, C. M. Mapping of two genes encoding members of a distinct subfamily of MAX interacting proteins: MAD to human chromosome 2 and mouse chromosome 6, and MXI 1 to human chromosome 10 and mouse chromosome 19. Oncogene, 9: 665-668, 1994.
38. Shapiro, D. N., Valentine, V., Eagle, L., Yin, X., Morris, S. W., and Prochownik, E. V. Assignment of the human MAD and MXI1 genes to chromosomes 2p12-p13 and 10q24-q25. Genomics, 23: 282-285, 1994.
39. Fujimoto, M., Fults, D. W., Thomas, G. A., Nakamura, Y., Heilbrun, M. P., White, R., Story, J. L., Naylor, S. L., Kagan-Hallet, K. S., and Sheridan, P. J. Loss of heterozygosity on chromosome 10 in human glioblastoma multiforme. Genomics, 4: 210-214, 1989.
40. Rasheed, B. K. A., Fuller, G. N., Friedman, A. H., Bigner, D. D., and Bigner, S. H. Loss of heterozygosity for 10q loci in human gliomas. Genes Chromosomes Cancer, 5: 75-82, 1992.
41. Ransom, D. T., Ritland, S. R., Moertel, C. A., Dahl, R. J., O'Fallon, J. R., Scheithauer, B. W., Kimmel, D. W., Kelly, P. J., Olopade, O. I., Diaz, M. O., and Jenkin, R. B. Correlation of cytogenetic analysis and loss of heterozygosity studies in human diffuse astrocytomas and mixed oligo-astrocytomas. Genes Chromosomes Cancer, 5: 357-374, 1992.
42. Fults, D., and Pedone, C. Deletion mapping of the long arm of chromosome 10 in glioblastoma multiforme. Genes Chromosomes Cancer, 7: 173-177, 1993.
43. Rasheed, B. K. A., McLendon, R. E., Friedman, H. S., Friedman, A. H., Fuchs, H. E., Bigner, D. D., and Bigner, S. H. Chromosome 10 deletion mapping in human gliomas: a common deletion region in 10q25. Oncogene, 10: 2243-2246, 1995.
44. Carter, B. S., Ewing, C. M., Ward, W. S., Treiger, B. F., Aalders, T. W., Schalken, J. A., Epstein, J. I., and Isaacs, W. B. Allelic loss of chromosomes 16q and 10q in human prostate cancer. Proc. Natl. Acad. Sci. USA, 87: 8751-8755, 1990.
45. Lundgren, R., Mandahl, N., Heim, S., Limon, J., Henrikson, H., and Mitelman, F. Cytogenetic analysis of 57 primary prostatic adenocarcinomas. Genes Chromosomes Cancer, 4: 16-24, 1992.
46. Eagle, L. R., Yin, X., Brothman, A. R., Williams, B. J., Atkin, N. B., and Prochownik, E. V. Mutation of the MXI1 gene in prostate cancer. Nat. Genet., 9: 249-255, 1995.
47. Gray, I. C., Phillips, S. M., Lee, S. J., Neoptolemos, J. P., Weissenbach, I., and Spurr, N. K. Loss of the chromosomal region 10q23-25 in prostate cancer. Cancer Res., 55: 4800-4803, 1995.
48. Kawamata, N., Park, D., Wilczynski, S., Yokota, J., and Koeffler, H. P. Point mutations of the Mxi1 gene are rare in prostate cancers. Prostate, 29: 191-193, 1996.
49. Weinberg, R. A. Tumor suppressor genes. Science (Washington DC), 254: 1138-1146, 1991.
50. Levine, A. J. The tumor suppressor genes. Annu. Rev. Biochem., 62: 623-651, 1993.
51. Fearon, E. R. DCC. Is there a connection between tumorigenesis and cell guidance molecules? Biochem. Biophys. Acta, 1288: M17-M23, 1996.
52. Engelhard, H. H., Butler, A. B., and Bauer, K. D. Quantification of the c-myc oncoprotein in human glioblastoma cells and tumor tissue. J. Neurosurg., 71: 224-232, 1989.
53. Shindo, H., Tani, E., Matsumoto, T., Hashimoto, T., and Furuyama, J. Stabilization of c-myc protein in human glioma cells. Acta Neuropathol., 86: 345-352, 1993.
54. Chattopadhyay, P., Banerjee, M., Sarkar, C., Mathur, M., Mohapatra, A. K., and Sinha, S. Infrequent alteration of the c-myc gene in human glial tumors associated with increased numbers of c-myc positive cells. Oncogene, 11: 2711-2714, 1995.
55. Banerjee, M., Dinda, A. K., Sinha, S., Sarkar, C., and Mathur, M. c-myc oncogene expression and cell proliferation in mixed oligo-astrocytoma. Int. J. Cancer, 65: 730-733, 1996.
56. Wechsler, D. S., Shelly, C. A., and Dang, C. V. Genomic structure of human MXI1, a putative tumor suppressor gene. Genomics, 32: 466-470, 1996.
57. McCombie, W. R., Heiner, C., Kelly, J. M., Fitzgerald, M. G., and Gocayne, J. D. Rapid and reliable fluorescent cycle sequencing of double stranded templates. DNA Sequence, 2: 289-296, 1992.
58. Smith, L. M., Sander, J. Z., Kaiser, R. J., Hughes, P., Dodd, C., Connel, C. R., Heiner, C., Kent, S. B., and Hood, L. E. Fluorescence detection in automated DNA sequence analysis. Nature (Lond.), 321: 674-679, 1986.
59. Mader, S., and White, J. H. A steroid-inducible promoter for the controlled overexpression of cloned genes in eukaryotic cells. Proc. Natl. Acad. Sci. USA, 90: 5603-5607, 1993.
60. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F., and Ricardi, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods, 139: 271-279, 1991.
61. Roy, B., and Reisman, D. Inducible expression of Mad accelerates growth arrest of serum deprived human glioblastoma cells. Cell Biol. Int., 19: 307-313, 1995.
62. Mohapatra, G., Kim, G. H., and Feurstein, B. G. Detection of multiple gains and losses of genetic material in ten glioma cell lines by comparative genomic hybridization. Genes Chromosomes Cancer, 13: 86-93, 1995.
63. LaRocca, R. V. Patterns of proto-oncogene expression in human glioma cell lines. J. Neurosci. Res., 24: 97-106, 1989.
64. James, C. D., Carlbom, E., Dumanski, J. P., Hansen, M., Nordenskjold, M., Collins, V. P., and Cavenee, W. K. Clonal genomic alterations in glioma malignancy stages. Cancer Res., 48: 5546-5551, 1988.
65. James, C. D., Mikkelsen, T., Cavenee, W. K., and Collins, V. P. Molecular genetic aspects of glial tumour evolution. Cancer Surv., 9: 631-644, 1990.
66. Mikkelsen, T., Cairncross, J. G., and Cavenee, W. K. Genetics of the malignant progression of astrocytoma. J. Cell Biochem., 46: 3-8, 1991.
67. Louis, D. N., and Gusella, J. F. A tiger behind many doors: multiple genetic pathways to malignant glioma. Trends Genet., 11: 412-415, 1995.
68. Li, J., Yen, C., Liaw, D., Podsypanina, K., Bose, S., Wang, S. L. Puc, J., Miliaresis, C., Rodgers, L., McCombie, R., Bigner, S. H., Giovanella, R. C., Ittimann, M., Tycko, B., Hibshoosh, H., Wigler, M. H., and Parsons, R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science (Washington DC), 275: 1943-1947, 1997.
69. Steck, P. A., Pershouse, M. A., Jasser, S. A., Yung, W. K., Lin, H., Ligon, A. H., Langford, L. A., Baumgard, M. L., Hattier, T., Davis, T., Frye, C., Hu, R., Swedlund, B., Teng, D. H., and Tavtigian, S. V. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet., 15: 356-362, 1997.
70. Bartsch, D., Peiffer, S. L., Kaleem, Z., Wells, S. A. J., and Goodfellow, P. J. Mxi1 tumor suppressor gene is not mutated in primary pancreatic adenocarcinoma. Cancer Lett., 102: 73-76, 1996.
71. 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 tumour suppressor pi6/CDKN2/MTS1 in human cancers. Nat. Med., 1: 686-692, 1995.
72. Herman, J. G., Merlo, A., Mao, L., Lapidus, R. G., Issa, J. P., Davidson, N. E., Sidransky, D., and Baylin, S. B. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res., 55: 4525-4530, 1995.
73. Herman, J. G., Latif, F., Weng, Y., Lerman, M. I., Zbar, B., Liu, S., Samid, D., Duan, D. S., Gnarra, J. R., Linehan, W. M., and Baylin, S. B. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc. Natl. Acad. Sci. USA, 91: 9700-9704, 1994.
74. Herman, J. G., Jen, J., Merlo, A., and Baylin, S. B. Hypermethylation-associated inactivation indicates a tumor suppressor role for p15INK4B. Cancer Res., 56: 722-727, 1996.
75. Chen, J., Willingham, T., Margraf, L. R., Schreiber Agus, N., DePinho, R. A., and Nisen, P. D. Effects of the MYC oncogene antagonist, MAD, on proliferation, cell cycling and the malignant phenotype of human brain tumour cells. Nat. Med., 1: 638-643, 1995.
76. Evan, G. I., Wyllie, A. H., Gilbert, C. S., Littlewood, T. D., Land, H., Brooks, M., Waters, C. M., Penn, L. Z., and Hancock, D. C. Induction of apoptosis in fibroblasts by c-myc protein. Cell, 69: 119-128, 1992.
77. Harrington, E. A., Fanidi, A., and Evan, G. I. Oncogenes and cell death. Curr. Opin. Genet. Dev., 4: 120-129, 1994.
78. Wu, M., Arsur, M., Bellas, R., FitzGerald, M. J., Lee, H., Schauer, S. L., Sherr, D. H., and Sonnenshein, G. E. Inhibition of c-myc expression induces apoptosis of WEHI 231 murine B cells. Mol. Cell. Biol., 16: 5015-5025, 1996.
79. Parker, S. L., Tong, T., Bolden, S., and Wingo, P. A. Cancer Statistics. CA-Cancer J. Clin., 46: 5-27, 1996.