MCG10, a novel p53 target gene that encodes a KH domain RNA-binding protein, is capable of inducing apoptosis and cell cycle arrest in G2-M

Molecular and Cellular Biology

Volumn 20, Issue 15, 2000, Pages 5602-5618

  Zhu, Jianhui ^a   Chen, Xinbin ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; RNA BINDING PROTEIN;

APOPTOSIS; ARTICLE; HUMAN; HUMAN CELL; MITOSIS INHIBITION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA BINDING; SEQUENCE HOMOLOGY; TUMOR SUPPRESSOR GENE;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; APOPTOSIS; CELL CYCLE; CELL LINE; CHROMOSOMES, HUMAN, PAIR 3; DNA DAMAGE; G2 PHASE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MITOSIS; MOLECULAR SEQUENCE DATA; MUTATION; POLY C; RESPONSE ELEMENTS; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 0033928264     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.15.5602-5618.2000     Document Type: Article

References (110)

1. Agarwal, M. L., W. R. Taylor, M. V. Chernov, O. B. Chernova, and G. R. Stark. 1998. The p53 network. J. Biol. Chem. 273:1-4.
2. Almog, N., and V. Rotter. 1997. Involvement of p53 in cell differentiation and development. Biochim. Biophys. Acta 1333:F1-F27.
3. Attardi, L. D., S. W. Lowe, J. Brugarolas, and T. Jacks. 1996. Transcriptional activation by p53, but not induction of the p21 gene, is essential for oncogene-mediated apoptosis. EMBO J. 15:3693-3701.
4. Barlat, I., F. Maurier, M. Duchesne, E. Guitard, B. Tocque, and F. Schweighoffer. 1997. A role for Sam68 in cell cycle progression antagonized by a spliced variant within the KH domain. J. Biol. Chem. 272:3129-3132.
5. Bennett, M., K. Macdonald, S. W. Chan, J. P. Luzio, R. Simari, and P. Weissberg. 1998. Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. Science 282:290-293.
6. Braga, E., E. Pugacheva, I. Bazov, V. Ermilova, T. Kazubskaya, N. Mazurenko, F. Kisseljov, J. Liu, R. Garkavtseva, E. Zabarovsky, and L. Kisselev. 1999. Comparative allelotyping of the short arm of human chromosome 3 in epithelial tumors of four different types. FEBS Lett. 454:215-219.
7. Brugarolas, J., C. Chandrasekaran, J. I. Gordon, D. Beach, T. Jacks, and G. J. Hannon. 1995. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377:552-557.
8. Bunz, F., A. Dutriaux, C. Lengauer, T. Waldman, S. Zhou, J. P. Brown, J. M. Sedivy, K. W. Kinzler, and B. Vogelstein. 1998. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282:1497-1501.
9. Burd, C. G., and G. Dreyfuss. 1994. Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615-621.
10. Bustelo, X. R., K. L. Suen, W. M. Michael, G. Dreyfuss, and M. Barbacid. 1995. Association of the vav proto-oncogene product with poly(rC)-specific RNA-binding proteins. Mol. Cell. Biol. 15:1324-1332.
11. Carrier, F., A. Gatignol, M. C. Hollander, K. T. Jeang, and A. J. Fornace, Jr. 1994. Induction of RNA-binding proteins in mammalian cells by DNA-damaging agents. Proc. Natl. Acad. Sci. USA 91:1554-1558.
12. Chan, T. A., H. Hermeking, C. Lengauer, K. W. Kinzler, and B. Vogelstein. 1999. 14-3-3Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 401:616-620.
13. Chen, X. 1999. The p53 family: same response, different signals? Mol. Med. Today 5:387-392.
14. Chen, X., J. Bargonetti, and C. Prives. 1995. p53, through p21 (WAF1/ CIP1), induces cyclin D1 synthesis. Cancer Res. 55:4257-4263.
15. Chen, X., L. J. Ko, L. Jayaraman, and C. Prives. 1996. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev. 10:2438-2451.
16. Chin, L., S. E. Artandi, Q. Shen, A. Tam, S. L. Lee, G. J. Gottlieb, C. W. Greider, and R. A. DePinho. 1999. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97:527-538.
17. Clurman, B., and M. Groudine. 1997. Tumour-suppressor genes. Killer in search of a motive? Nature 389:122-123.
18. Cohen, G. B., R. Ren, and D. Baltimore. 1995. Modular binding domains in signal transduction proteins. Cell 80:237-248.
19. Colgin, L. M., and R. R. Reddel. 1999. Telomere maintenance mechanisms and cellular immortalization. Curr. Opin. Genet. Dev. 9:97-103. (Erratum, 9:247.)
20. Deng, C., P. Zhang, J. W. Harper, S. J. Elledge, and P. Leder. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82:675-684.
21. Di Como, C. J., C. Gaiddon, and C. Prives. 1999. p73 function is inhibited by tumor-derived p53 mutants in mammalian cells. Mol. Cell. Biol. 19:1438-1449.
22. Dietrich, W. F., E. H. Radany, J. S. Smith, J. M. Bishop, D. Hanahan, and E. S. Lander. 1994. Genome-wide search for loss of heterozygosity in transgenic mouse tumors reveals candidate tumor suppressor genes on chromosomes 9 and 16. Proc. Natl. Acad. Sci. USA 91:9451-9455.
23. Dreyfuss, G., M. J. Matunis, S. Pinol-Roma, and C. G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
24. Driouch, K., M. Briffod, I. Bieche, M. H. Champeme, and R. Lidereau. 1998. Location of several putative genes possibly involved in human breast cancer progression. Cancer Res. 58:2081-2086.
25. Druck, T., K. Kastury, P. Hadaczek, J. Podolski, A. Toloczko, A. Sikorski, M. Ohta, S. LaForgia, J. Lasota, P. McCue, et al. 1995. Loss of heterozygosity at the familial RCC t(3;8) locus in most clear cell renal carcinomas. Cancer Res. 55:5348-5353.
26. Du, Q., I. N. Melnikova, and P. D. Gardner. 1998. Differential effects of heterogeneous nuclear ribonucleoprotein K on Sp1-and Sp3-mediated transcriptional activation of a neuronal nicotinic acetylcholine receptor promoter. J. Biol. Chem. 273:19877-19883.
27. el-Deiry, W. S. 1998. Regulation of p53 downstream genes. Semin. Cancer Biol. 8:345-357.
28. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
29. Elkeles, A., T. Juven-Gershon, D. Israeli, S. Wilder, A. Zalcenstein, and M. Oren. 1999. The c-fos proto-oncogene is a target for transactivation by the p53 tumor suppressor. Mol. Cell. Biol. 19:2594-2600.
30. Friedlander, P., Y. Haupt, C. Prives, and M. Oren. 1996. A mutant p53 that discriminates between p53-responsive genes cannot induce apoptosis. Mol. Cell. Biol. 16:4961-4971.
31. Fullwood, P., S. Marchini, J. S. Rader, A. Martinez, D. Macartney, M. Broggini, C. Morelli, G. Barbanti-Brodano, E. R. Maher, and F. Latif. 1999. Detailed genetic and physical mapping of tumor suppressor loci on chromosome 3p in ovarian cancer. Cancer Res. 59:4662-4667.
32. Giaccia, A. J., and M. B. Kastan. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12:2973-2983.
33. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells hy tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
34. Gottlieb, T. M., and M. Oren. 1996. p53 in growth control and neoplasia. Biochim. Biophys. Acta 1287:77-102.
35. Hermeking, H., C. Lengauer, K. Polyak, T.-C. He, L. Zhang, S. Thiagalingam, K. W. Kinzler, and B. Vogelstein. 1997. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1:3-11.
36. Hobert, O., B. Jallal, J. Schlessinger, and A. Ullrich. 1994. Novel signaling pathway suggested by SH3 domain-mediated p95vav/heterogeneous ribonucleoprotein K interaction. J. Biol. Chem. 269:20225-20228.
37. Hwang, B. J., J. M. Ford, P. C. Hanawalt, and G. Chu. 1999. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. USA 96:424-428.
38. Imreh, S., M. Kost-Alimova, I. Kholodnyuk, Y. Yang, A. Szeles, H. Kiss, Y. Liu, K. Foster, E. Zabarovsky, E. Stanbridge, and G. Klein. 1997. Differential elimination of 3p and retention of 3q segments in human/mouse microcell hybrids during tumor growth. Genes Chromosomes Cancer 20:224-233.
39. Israeli, D., E. Tessler, Y. Haupt, A. Elkeles, S. Wilder, R. Amson, A. Telerman, and M. Oren. 1997. A novel p53-inducible gene, PAG608, encodes a nuclear zinc finger protein whose overexpression promotes apoptosis. EMBO J. 16:4384-4392.
40. Jackman, J., I. Alamo, Jr., and A. J. Fornace, Jr. 1994. Genotoxic stress confers preferential and coordinate messenger RNA stability on the five gadd genes. Cancer Res. 54:5656-5662.
41. Johansen, F. E., and R. Prywes. 1994. Two pathways for serum regulation of the c-fos serum response element require specific sequence elements and a minimal domain of serum response factor. Mol. Cell. Biol. 14:5920-5928.
42. Kastan, M. B., Q. Zhan, W. S. el-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, and A. J. Fornace, Jr. 1992. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxiatelangiectasia. Cell 71:587-597.
43. Kern, S. E., K. W. Kinzler, A. Bruskin, D. Jarosz, P. Friedman, C. Prives, and B. Vogelstein. 1991. Identification of p53 as a sequence-specific DNA-binding protein. Science 252:1708-1711.
44. Kholodnyuk, I., M. Kost-Alimova, V. Kashuba, R. Gizatulin, A. Szeles, E. J. Stanbridge, E. R. Zabarovsky, G. Klein, and S. Imreh. 1997. A 3p21.3 region is preferentially eliminated from human chromosome 3/mouse microcell hybrids during tumor growth in SCID mice. Genes Chromosomes Cancer 18:200-211.
45. Kiledjian, M., X. Wang, and S. A. Liebhaber. 1995. Identification of two KH domain proteins in the alpha-globin mRNP stability complex. EMBO J. 14:4357-4364.
46. Ko, L. J., and C. Prives. 1996. p53: puzzle and paradigm. Genes Dev. 10:1054-1072.
47. Ko, L. J., S. Y. Shieh, X. Chen, L. Jayararaan, K. Tamai, Y. Taya, C. Prives, and Z. Q. Pan. 1997. p53 is phosphorylated by CDK7-cyclin H in a p36MATI-dependent manner. Mol. Cell. Biol. 17:7220-7229.
48. Krecic, A. M., and M. S. Swanson. 1999. hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11:363-371.
49. Kusumoto, M., T. Ogawa, K. Mizumoto, H. Ueno, H. Niiyama, N. Sato, M. Nakamura, and M. Tanaka. 1999. Adenovirus-mediated p53 gene transduction inhibits telomerase activity independent of its effects on cell cycle arrest and apoptosis in human pancreatic cancer cells. Clin. Cancer Res. 5:2140-2147.
50. Lee, C. W., and N. B. La Thangue. 1999. Promoter specificity and stability control of the p53-related protein p73. Oncogene 18:4171-4181.
51. Lengauer, C., K. W. Kinzler, and B. Vogelstein. 1998. Genetic instabilities in human cancers. Nature 396:643-649.
52. Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
53. Lin, Q., S. J. Taylor, and D. Shalloway. 1997. Specificity and determinants of Sam68 RNA binding: implications for the biological function of K homology domains. J. Biol. Chem. 272:27274-27280.
54. Lingner, J., and T. R. Cech. 1998. Telomerase and chromosome end maintenance. Curr. Opin. Genet. Dev. 8:226-232.
55. Loughran, O., L. J. Clark, J. Bond, A. Baker, I. J. Berry, K. G. Edington, I. S. Ly, R. Simmons, R. Haw, D. M. Black, R. F. Newbold, and E. K. Parkinson. 1997. Evidence for the inactivation of multiple replicative lifespan genes in immortal human squamous cell carcinoma keratinocytes. Oncogene 14:1955-1964.
56. Mashimo, T., M. Watabe, S. Hirota, S. Hosobe, K. Miura, P. J. Tegtmeyer, C. W. Rinker-Shaeffer, and K. Watabe. 1998. The expression of the KAI1 gene, a tumor metastasis suppressor, is directly activated by p53. Proc. Natl. Acad. Sci. USA 95:11307-11311.
57. Matsuzawa, S., S. Takayama, B. A. Froesch, J. M. Zapata, and J. C. Reed. 1998. p53-inducible human homologue of Drosophila seven in absentia (Siah) inhibits cell growth: suppression by BAG-I. EMBO J. 17:2736-2747.
58. Mehle, C., A. Lindblom, B. Ljungberg, R. Stenling, and G. Roos. 1998. Loss of heterozygosity at chromosome 3p correlates with telomerase activity in renal cell carcinoma. Int. J. Oncol. 13:289-295.
59. Michelotti, E. F., G. A. Michelotti, A. I. Aronsohn, and D. Levens. 1996. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol. Cell. Biol. 16:2350-2360.
60. Michelotti, G. A., E. F. Michelotti, A. Pullner, R. C. Duncan, D. Eick, and D. Levens. 1996. Multiple single-stranded cis elements are associated with activated chromatin of the human c-myc gene in vivo. Mol. Cell. Biol. 16:2656-2669.
61. Mitelman, F., F. Mertens, and B. Johansson. 1997. A breakpoint map of recurrent chromosomal rearrangements in human neoplasia. Nat. Genet. 15(Spec. No.):417-474.
62. Miyashita, T., S. Krajewski, M. Krajewska, H. G. Wang, H. K. Lin, D. A. Liebermann, B. Hoffman, and J. C. Reed. 1994. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799-1805.
63. Mori, T., A. Yanagisawa, Y. Kato, K. Miura, T. Nishihira, S. Mori, and Y. Nakamura. 1994. Accumulation of genetic alterations during esophageal carcinogenesis. Hum. Mol. Genet. 3:1969-1971.
64. Muller, M., S. Wilder, D. Bannasch, D. Israeli, K. Lehlbach, M. Li-Weber, S. L. Friedman, P. R. Galle, W. Stremmel, M. Oren, and P. H. Krammer. 1998. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J. Exp. Med. 188:2033-2045.
65. Munger, K., W. C. Phelps, V. Bubb, P. M. Howley, and R. Schlegel. 1989. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 63:4417-4421.
66. Musco, G., G. Stier, C. Joseph, M. A. Castiglione Morelli, M. Nilges, T. J. Gibson, and A. Pastore. 1996. Three-dimensional structure and stability of the KH domain: molecular insights into the fragile X syndrome. Cell 85: 237-245.
67. Nagata, S. 2000. Apoptotic DNA fragmentation. Exp. Cell Res. 256:12-18.
68. Nelson, W. G., and M. B. Kastan. 1994. DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol. 14:1815-1823.
69. 2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol. Cell. Biol. 18:629-643.
70. Nikiforova, M. N., Y. E. Nikiforov, P. Biddinger, D. R. Gnepp, L. A. Grosembacher, B. L. Wajchenberg, J. A. Fagin, and R. M. Cohen. 1999. Frequent loss of heterozygosity at chromosome 3p14.2-3p21 in human pancreatic islet cell tumours. Clin. Endocrinol. (Oxford) 51:27-33.
71. Oberhammer, F., J. W. Wilson, C. Dive, I. D. Morris, J. A. Hickman, A. E. Wakeling, P. R. Walker, and M. Sikorska. 1993. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J. 12:3679-3684.
72. Ogasawara, S., C. Maesawa, G. Tamura, and R. Satodate. 1995. Frequent microsatellite alterations on chromosome 3p in esophageal squamous cell carcinoma. Cancer Res. 55:891-894.
73. Ostareck, D. H., A. Ostareck-Lederer, M. Wilm, B. J. Thiele, M. Mann, and M. W. Hentze. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89:597-606.
74. Ostareck-Lederer, A., D. H. Ostareck, and M. W. Hentze. 1998. Cytoplasmic regulatory functions of the KH-domain proteins hnRNPs K and E1/E2. Trends Biochem. Sci. 23:409-411.
75. Partridge, M., G. Emilion, and J. D. Langdon. 1996. LOH at 3p correlates with a poor survival in oral squamous cell carcinoma. Br. J. Cancer 73:366-371.
76. Pietenpol, J. A., T. Tokino, S. Thiagalingam, W. S. el-Deiry, K. W. Kinzler, and B. Vogelstein. 1994. Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl. Acad. Sci. USA 91:1998-2002.
77. Pinol-Roma, S., Y. D. Choi, M. J. Matunis, and G. Dreyfuss. 1988. Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins. Genes Dev. 2:215-227. (Erratum, 2:190.)
78. Roperch, J. P., F. Lethrone, S. Prieur, L. Piouffre, D. Israeli, M. Tuynder, M. Nemani, P. Pasturaud, M. C. Gendron, J. Dausset, M. Oren, R. B. Amson, and A. Telerman. 1999. SIAH-1 promotes apoptosis and tumor suppression through a network involving the regulation of protein folding, unfolding, and trafficking: identification of common effectors with p53 and p21 (Waf1). Proc. Natl. Acad. Sci. USA 96:8070-8073.
79. Rouault, J. P., N. Falette, F. Guehenneux, C. Guillot, R. Rimokh, Q. Wang, C. Berthet, C. Moyret-Lalle, P. Savatier, B. Pain, P. Shaw, R. Berger, J. Samarut, J. P. Magaud, M. Ozturk, C. Samarut, and A. Puisieux. 1996. Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat. Genet. 14:482-486.
80. Sakahira, H., M. Enari, Y. Ohsawa, Y. Uchiyama, and S. Nagata. 1999. Apoptotic nuclear morphological change without DNA fragmentation. Curr. Biol. 9:543-546.
81. Sheikh, M. S., F. Carrier, M. A. Papathanasiou, M. C. Hollander, Q. Zhan, K. Yu, and A. J. Fornace, Jr. 1997. Identification of several human homologs of hamster DNA damage-inducible transcripts: cloning and characterization of a novel UV-inducible cDNA that codes for a putative RNA-binding protein. J. Biol. Chem. 272:26720-26726.
82. Siomi, H., and G. Dreyfuss. 1997. RNA-binding proteins as regulators of gene expression. Curr. Opin. Genet. Dev. 7:345-353.
83. Siomi, H., M. C. Siomi, R. L. Nussbaum, and G. Dreyfuss. 1993. The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell 74:291-298.
84. Swanson, M. S., and G. Dreyfuss. 1988. Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol. Cell. Biol. 8:2237-2241.
85. Taylor, S. J., and D. Shalloway. 1994. An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature 368:867-871.
86. Todd, S., W. A. Franklin, M. Varella-Garcia, T. Kennedy, C. E. Hilliker, Jr., L. Hahner, M. Anderson, J. S. Wiest, H. A. Drabkin, and R. M. Gemmill. 1997. Homozygous deletions of human chromosome 3p in lung tumors. Cancer Res. 57:1344-1352.
87. Tomonaga, T., G. A. Michelotti, D. Libutti, A. Uy, B. Sauer, and D. Levens. 1998. Unrestraining genetic processes with a protein-DNA hinge. Mol. Cell 1:759-764.
88. Utrera, R., L. Collavin, D. Lazarevic, D. Delia, and C. Schneider. 1998. A novel p53-inducible gene coding for a microtubule-localized protein with G2-phase-specific expression. EMBO J. 17:5015-5025.
89. Van Seuningen, I., J. Ostrowski, X. R. Bustelo, P. R. Sleath, and K. Bomsztyk. 1995. The K protein domain that recruits the interleukin 1-responsive K protein kinase lies adjacent to a cluster of c-Src and Vav SH3-binding sites: implications that K protein acts as a docking platform. J. Biol. Chem. 270: 26976-26985.
90. Varmeh-Ziaie, S., I. Okan, Y. Wang, K. P. Magnusson, P. Warthoe, M. Strauss, and K. G. Wiman. 1997. Wig-1, a new p53-induced gene encoding a zinc finger protein. Oncogene 15:2699-2704.
91. Venot, C., M. Maratrat, C. Dureuil, E. Conseiller, L. Bracco, and L. Debussche. 1998. The requirement for the p53 proline-rich functional domain for mediation of apoptosis is correlated with specific PIG3 gene transactivation and with transcriptional repression. EMBO J. 17:4668-4679.
92. Venot, C., M. Maratrat, V. Sierra, E. Conseiller, and L. Debussche. 1999. Definition of a p53 transactivation function-deficient mutant and characterization of two independent p53 transactivation subdomains. Oncogene 18: 2405-2410.
93. Verkerk, A. J., B. B. deVries, M. F. Niermeijer, Y. H. Fu, D. L. Nelson, S. T. Warren, D. F. Majoor-Krakauer, D. J. Halley, and B. A. Oostra. 1992. Intragenic probe used for diagnostics in fragile X families. Am. J. Med. Genet. 43:192-196.
94. Waldman, T., C. Lengauer, K. W. Kinzler, and B. Vogelstein. 1996. Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 381:713-716.
95. Wang, X. W., Q. Zhan, J. D. Coursen, M. A. Khan, H. U. Kontny, L. Yu, M. C. Hollander, P. M. O'Connor, A. J. Fornace, Jr., and C. C. Harris. 1999. GADD45 induction of a G2/M cell cycle checkpoint. Proc. Natl. Acad. Sci. USA 96:3706-3711.
96. Warren, S. T., and D. L. Nelson. 1994. Advances in molecular analysis of fragile X syndrome. JAMA 271:536-542.
97. Weiss, I. M., and S. A. Liebhaber. 1994. Erythroid cell-specific determinants of alpha-globin mRNA stability. Mol. Cell. Biol. 14:8123-8132.
98. Weng, Z., S. M. Thomas, R. J. Rickles, J. A. Taylor, A. W. Brauer, C. Seidel-Dugan, W. M. Michael, G. Dreyfuss, and J. S. Brugge. 1994. Identification of Src, Fyn, and Lyn SH3-binding proteins: implications for a function of SH3 domains. Mol. Cell. Biol. 14:4509-4521.
99. Wieland, I., T. Ammermuller, M. Bohm, B. Totzeck, and M. F. Rajewsky. 1996. Microsatellite instability and loss of heterozygosity at the hMLH1 locus on chromosome 3p21 occur in a subset of nonsmall cell lung carcinomas. Oncol. Res. 8:1-5.
100. Wistuba, I. I., C. Behrens, S. Milchgrub, D. Bryant, J. Hung, J. D. Minna, and A. F. Gazdar. 1999. Sequential molecular abnormalities are involved in the multistage development of squamous cell lung carcinoma. Oncogene 18:643-650.
101. Wistuba, I. I., F. D. Montellano, S. Milchgrub, A. K. Virmani, C. Behrens, H. Chen, M. Ahmadian, J. A. Nowak, C. Muller, J. D. Minna, and A. F. Gazdar. 1997. Deletions of chromosome 3p are frequent and early events in the pathogenesis of uterine cervical carcinoma. Cancer Res. 57:3154-3158.
102. Wolf, B. B., M. Schuler, F. Echeverri, and D. R. Green. 1999. Caspase-3 is the primary activator of apoptotic DNA fragmentation via DNA fragmentation factor-45/inhibitor of caspase-activated DNase inactivation. J. Biol. Chem. 274:30651-30656.
103. Wu, G. S., T. F. Burns, E. R. McDonald, 3rd, W. Jiang, R. Meng, I. D. Krantz, G. Kao, D. D. Gan, J. Y. Zhou, R. Muschel, S. R. Hamilton, N. B. Spinner, S. Markowitz, G. Wu, and W. S. El-Deiry. 1997. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat. Genet. 17:141-143.
104. Wu, G. S., P. Saftig, C. Peters, and W. S. El-Deiry. 1998. Potential role for cathepsin D in p53-dependent tumor suppression and chemosensitivity. Oncogene 16:2177-2183.
105. Yin, Y., Y. Terauchi, G. G. Solomon, S. Aizawa, P. N. Rangarajan, Y. Yazaki, T. Kadowaki, and J. C. Barrett. 1998. Involvement of p85 in p53-dependent apoptotic response to oxidative stress. Nature 391:707-710.
106. Zhan, Q., I. Bae, M. B. Kastan, and A. J. Fornace, Jr. 1994. The p53-dependent gamma-ray response of GADD45. Cancer Res. 54:2755-2760.
107. Zhu, J., J. Jiang, W. Zhou, and X. Chen. 1998. The potential tumor suppressor p73 differentially regulates cellular p53 target genes. Cancer Res. 58:5061-5065.
108. Zhu, J., J. Jiang, W. Zhou, K. Zhu, and X. Chen. 1999. Differential regulation of cellular target genes by p53 devoid of the PXXP motifs with impaired apoptotic activity. Oncogene 18:2149-2155.
109. Zhu, J., W. Zhou, J. Jiang, and X. Chen. 1998. Identification of a novel p53 functional domain that is necessary for mediating apoptosis. J. Biol. Chem. 273:13030-13036.
110. Zhu, K., W. J., J. Zhu, J. Jiang, J. Shou, and X. Chen. 1999. p53 induces TAP1 and enhances the transport of MHC class I peptides. Oncogene 18:7740-7747.