Inosine-5'-monophosphate dehydrogenase is a rate-determining factor for p53-dependent growth regulation

Molecular Biology of the Cell

Volumn 9, Issue 1, 1998, Pages 15-28

  Liu, Yuan ^a   Bohn, Shirley A ^a   Sherley, James L ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; GUANINE NUCLEOTIDE; GUANOSINE TRIPHOSPHATE; INOSINATE DEHYDROGENASE; MYCOPHENOLIC ACID; PROTEIN BAX; PROTEIN P53; PURINE; PUROMYCIN; RIBONUCLEOTIDE; ZINC CHLORIDE;

ANIMAL CELL; ARTICLE; CELL GROWTH; CONTROLLED STUDY; DNA DAMAGE; EPISTASIS; GENE EXPRESSION; GENE TRANSFER; GROWTH REGULATION; NONHUMAN; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0031910134     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.1.15     Document Type: Article

References (120)

1. Aaronson, S.A. (1991). Growth factors and cancer. Science 254, 1146-1152.
2. Allison, A.C., Kowalski, W.J., Muller, C.D., Eugui, E.M. (1993). Mechanisms of action of mycophenolic acid. Ann. NY Acad. Sci. 696, 63-87.
3. Antoniades, H.N., Galanopoulos, T., Neville-Golden, J., Kiritsy, C.P., and Lynch, S.E. (1994). p53 expression during normal tissue regeneration in response to acute cutaneous injury in swine. J. Clin. Invest. 93, 2206-2214.
4. Attardi, L.D., Lowe, S.W., Brugarolas, J., and Jacks, T. (1996). Transcriptional activation by p53, but not induction of the p21 gene, is essential for oncogene-mediated apoptosis. EMBO J. 15, 3693-3701.
5. Balzarini, J., Karlsson, A., Wang, L., Bohman, C., Horská, K., Votruba, I., Fridland, A., Aerschot, A.V., Herdewijn, P., and De-Clercq, E.D. (1993). Eicar (5-ethynyl-1-β-D-ribofuranosylimidazaole-4-carboxamide): A novel potent inhibitor of inosinate dehydrogenase activity and guanylate biosynthesis. J. Biol. Chem. 268, 24591-24598.
6. Barak, Y., Juven, T., Haffner, R., and Oren, M. (1993). Mdm2 expression is induced by wild-type p53 activity. EMBO J. 12, 461-468.
7. Bourne, H.R., Sanders, D.A., and McCormick, F. (1990). The GTPase superfamily: Conserved switch for diverse cell functions. Nature 348, 125-131.
8. Bourne, H.R., Sanders, D.A., and McCormick, F. (1991). The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117-127.
9. Brady, H.J., Salomons, G.S., Bobeldijk, R.C., and Berns, A.J. M. (1996). T cells from baxα transgenic mice show accelerated apoptosis in response to stimuli but do not show restored DNA damage-induced cell death in the absence of p53. EMBO J. 15, 1221-1230.
10. Brugarolas, J., Chandrasekaran, C., Gordon, J.I., Beach, D., Jacks, T., Hannon, G.J. (1995). Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377, 552-557.
11. Cantley, L.C., Auger, K.R., Carpenter, C., Duckworth, B., Graziani, A., Kapeller, R., and Soltoff, S. (1991). Oncogenes and signal transduction. Cell 64, 281-302.
12. Carter, S.B., Franklin, T.J., Jones, D.F., Leonard, B.J., Mills, S.D., Turner, R.W., and Turner, W.B. (1969). Mycophenolic acid: an anticancer compound with unusual properties. Nature 223, 848-850.
13. Chant J., and Stowers, L. (1995). GTPase cascades choreographing cellular behavior: movement, morphogenesis, and more. Cell 81, 1-4.
14. Chen C.-Y., Oliner, J.D., Zhan, Q., Fornace, A.J., Jr., Vogelstein, B., and Kastan, M.B. (1994). Interactions between p53 and MDM2 in a mammalian cell cycle checkpoint pathway. Proc Natl. Acad. Sci. USA 91, 2684-2688.
15. Chen X., Ko, L.J., Jayaraman, L., and Prives, C. (1996). p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev. 10, 2438-2451.
16. Chiou, S.-K., Rao, L., and White, E. (1994). Bcl-2 blocks p53-dependent apoptosis. Mol. Cell. Biol. 14, 2556-2563.
17. Clarke, P.R., Klebe, C., Wittinghofer, A., and Karsenti, E. (1995). Regulation of Cdc2/cyclin B activation by Ran, a Ras-related GTPase. J. Cell Sci., 208, 1217-1225.
18. Cochet, C., Job, D., Pirollet, F., and Chambaz, E.M. (1981). Cyclic nucleotide independent casein kinase (G type) in bovine adrenal cortex. Purification and properties of two molecular forms. Biochim. Biophys. Acta 658, 191-201.
19. Cocker, J.H., Platti, S., Santocanale, C., Nasmyth, K., and Diffley, J.F. X. (1996). An essential role for the Cdc6 protein in forming the pre-replicative complexes of budding yeast. Nature 379, 180-182.
20. Cohen, M.B. and Sadée, W. (1983). Contributions of the depletions of guanine and adenine nucleotides to the toxicity of purine starvation in the mouse T lymphoma cell line. Cancer Res. 43, 1587-1591.
21. Cohen, M.B., Maybaum, J., and Sadée, W. (1981). Guanine nucleotide depletion and toxicity in mouse T lymphoma (S-49) cells. J. Biol. Chem. 256, 8713-8717.
22. Colacino, J.M., Birch, G.M., and Tang, J.C. (1993). Cellular metabolism and anti-influenza activity of 1,3,4-thiadiazol-2-yl-cyanamide (LY217896). Antiviral Chem. Chemother. 4, 271-280.
23. Collart, F.R. and Huberman, E. (1987). Amplification of the IMP dehydrogenase gene in Chinese hamster cells resistant to mycophenolic acid. Mol. Cell. Biol. 7, 3328-3331.
24. Collart, F.R. and Huberman, E. (1988). Cloning and sequence analysis of the human and Chinese hamster inosine-5′-monophosphate dehydrogenase cDNAs. J. Biol. Chem. 263, 15769-15772.
25. Collart, F.R., Chubb, C.B., Mirkin, B.L., and Huberman, E. (1992). Increased inosine-5′-phosphate dehydrogenase gene expression in solid tumor tissues and tumor cell lines. Cancer Res. 52, 5826-5828.
26. Crabtree, G.W. and Henderson, J.F. (1971). Rate-limiting steps in the interconversion of purine ribonucleotides in Ehrlich ascites tumor cells in vitro. Cancer. Res. 31, 985-991.
27. Criss W.E., and Pradhan, T.K. (1976). Regulation of tumor cell metabolism by the adenylate and guanylate energy charges. In: Control Mechanisms in Cancer, ed. W.E. Criss, Ono, T., and J.R. Sabine, New York: Raven Press, 401-410.
28. 1 checkpoint control. Cell 82, 675-684.
29. Donehower, L.A., and Bradley, A. (1993). The tumor suppressor p53. Biochim. Biophys. Acta 1155, 181-205.
30. 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. (1993). WAF1, a potential mediator of p53 tumor suppression. Cell 75, 817-825.
31. Elasser, S., Lou, F., Wang, B., Campbell, J.L., and Jong, A. (1996). Interaction between yeast Cdc6 protein and B-type cyclin/Cdc28 kinases. Mol. Biol. Cell 7, 1723-1735.
32. Finlay, C.A. (1993). The mdm-2 oncogene can overcome wild-type p53 suppression of transformed cell growth. Mol. Cell. Biol. 13, 301-306.
33. Finlay, C.A., Hinds, P.W., and Levine, A.J. (1989). The p53 protooncogene can act as a suppressor of transformation. Cell 57, 1083-1093.
34. Franklin, T.J., and Twose, P.A. (1977). Reduction in β-adrenergic response of cultured glioma cells following depletion of intracellular GTP. Eur. J. Biochem. 77, 113-117.
35. Gibbs, J.B., and Marshall, M.S. (1989). The ras oncogene - an important regulatory element in lower eucaryotic organisms. Microbiol. Rev. 53, 171-185.
36. Glesne, D.A., Collart, F.R., and Huberman, E. (1991). Regulation of IMP dehydrogenase gene expression by its end products, guanine nucleotides. Mol. Cell. Biol. 11, 5417-5425.
37. Gottlieb, T.M., and Oren, M. (1996). p53 in growth control and neoplasia. Biochim. Biophys. Acta 1287, 77-102.
38. Gruber, H.E., Jansen, I., Willis, R.C., and Seegmiller, J.E. (1985). Alterations of inosinate branchpoint enzymes in cultured human lymphoblasts. Biochim. Biophys. Acta 846, 135-144.
39. 1 arrest. Blood 85, 2691-2698.
40. Hall, A. (1992). Signal transduction through small GTPases - a tale of two GAPs. Cell 69, 389-391.
41. Hermeking, H., and Eick, D. (1994). Mediation of c-myc-induced apoptosis by p53. Science 265, 2091-2093.
42. Hide, G., Graham, T., Buchanan, N., Tait, A., and Keith, K. (1994). Trypanosoma brucei: characterization of protein kinases that are capable of autophosphorylation in vitro. Parasitology 108, 161-166.
43. 1 to S phase in growth-stimulated rat FRTL-5 cells. J. Biol. Chem. 272, 13-16.
44. Hochhauser, S.J., Stein, J.L., and Stein, G.S. (1981). Gene expression and cell cycle regulation. Int. Rev. Cytol. 71, 95-243.
45. Hodges, S.D., Fung, E., McKay, D.J., Renaux, B.S., and Synder, F.F. (1989). Increased activity, amount, and altered kinetic properties of IMP dehydrogenase from mycophenolic acid-resistant neuroblastoma cells. J. Biol. Chem. 264, 18137-18141.
46. Hollstein, M., Sidransky, D., Vogelstein, B., and Harris, C.C. (1991). p53 mutations in human cancers. Science 253, 49-53.
47. Hunter, T. (1995). Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80, 225-236.
48. Jackson, R.C., Morris, H.P., and Weber, G. (1977). Partial purification, properties and regulation of inosine-5′-phosphate dehydrogenase in normal and malignant rat tissues. Biochem. J. 166, 1-10.
49. Jackson, R.C., Weber, G., and Morris, H.P. (1975). IMP dehydrogenase, an enzyme linked with proliferation and malignancy. Nature 256, 331-333.
50. Jayaram, H.N., Zhen, W., and Gharehbaghi, K. (1993). Biochemical consequences of resistance to tiazofurin in human myelogenous leukemic K562 cells. Cancer Res. 53, 2344-2348.
51. Kessis, T.D., Slebos, R.J., Nelson, W.G., Kastan, M.B., Plunkett, B.S., Han, S.M., Lorincz, A.T., Hedrick, L., and Cho, K.R. (1993). Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 90, 3988-3992.
52. Kharbanda, S.M., Sherman, M.L., and Kufe, D.W. (1990). Effects of tiazofurin on guanine nucleotide binding regulatory proteins in HL-60 cells. Blood 75, 583-588.
53. Kiguchi, K., Collart, F.R., Henning-Chubb, C., and Huberman, E. (1990). Induction of cell differentiation in melanoma cells by inhibitors of IMPD dehydrogenase: altered patterns of IMPD dehydrogenase expression and activity. Cell Growth & Differ. 1, 259-270.
54. Kinzler, K.W., and Vogelstein, B. (1996). Life (and death) in a malignant tumour. Nature 379, 19-20.
55. Knudson, C.M., Tung, K.S. K., Tourtellotte, W.G., Brown, G.A. J., and Korsmeyer, S.J. (1995). Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270, 96-99.
56. Ko, L.J., and Prives, C. (1996). p53: puzzle and paradigm. Genes Dev., 10, 1054-1072.
57. Konno, Y., Natsumeda, Y., Nagai, M., Yamaji, Y., Ohno, S., Suzuki, K., and Weber, G. (1991). Expression of human IMP dehydrogenase types I and II in Escherichia coli and distribution in human normal lymphocytes and leukemic cell lines. J. Biol. Chem. 266, 506-509.
58. Latham, K.M., Eastman, S.W., Wong, A., and Hinds, P.W. (1996). Inhibition of p53-mediated growth arrest by overexpression of cyclin-dependent kinases. Mol. Cell. Biol. 16, 4445-4455.
59. Lee, H.-J., Pawlak, K., Nguyen, B.T., Robins, R.K., and Sadée, W. (1985). Biochemical differences among four inosinate dehydrogenase inhibitors, mycophenolic acid, ribavirin, tiazofurin, and selenazofurin, studied in mouse lymphoma cell culture. Cancer Res. 45, 5512-5520.
60. Lehninger, A.L. (1973). Bioenergetics, 2nd ed., Menlo Park, CA: W.A. Benjamin.
61. Lehninger, A.L. (1975). Biochemistry, 2nd ed., New York: Worth Publishers.
62. Levine, A.J., and Momand, J. (1990). Tumor suppressor genes: the p53 and retinoblastoma sensitivity genes and gene products. Biochim. Biophys. Acta 1032, 119-136.
63. Liang, C., Weinreich, M., and Stillman, B. (1995). ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell 81, 667-676.
64. Lightfoot, T., and Snyder, F.F. (1994). Gene amplification and dual point mutations of mouse IMP dehydrogenase associated with cellular resistance to mycophenolic acid. Biochim. Biophys. Acta 1217, 156-162.
65. 1 arrest. Proc. Natl. Acad. Sci. USA 91, 10079-10083.
66. Lin, H.J., Eviner, V., Prendergast, G.C., and White, E. (1995). Activated H-ras rescues E1A-induced apoptosis and cooperates with E1A to overcome p53-dependent growth arrest. Mol. Cell. Biol. 15, 4536-4544.
67. 1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10, 934-947.
68. Livingstone, L.R., White, A., Sprouse, J., Livanos, E., Jacks, T., and Tlsty, T.D. (1992). Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell 70, 923-935.
69. Lui, M.S., Faderan, M.A, Liepnieks, J.J., Natsumeda, Y., Olah, E., Jayaram, H.N., and Weber, G. (1984). Modulation of IMP dehydrogenase activity and guanylate metabolism by tiazofurin (2-β-D-ribofuranosylthiazole-4-carboxamide). J. Biol. Chem. 259, 5078-5082.
70. Michael-Michalovitz, D., Yehiely, F., Gottlieb, E., and Oren, M. (1991). Simian virus 40 can overcome the antiproliferative effect of wild-type p53 in the absence of stable large T antigen-p53 binding. J. Virol. 65, 4160-4168.
71. Miyashita, T., and Reed, J.C. (1995). Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299.
72. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H.G., Lin, H.K., Lieberman, D.A., Hoffman, B., and Reed, J.C. (1994). Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9, 1799-1805.
73. Miyazaki, M., Uritani, M., and Kagiyama, H. (1988). The yeast peptide elongation factor 3 (EF-3) carries an active site for ATP hydrolysis which can interact with various nucleoside triphosphates in the absence of ribosomes. J. Biochem. 104, 445-450.
74. Murphy, M., Hinman, A., and Levine, A.J. (1996). Wild-type p53 negatively regulates the expression of a microtubule-associated protein. Genes Dev. 10, 2971-2980.
75. Nagai, M., Natsumeda, Y., and Weber, G. (1992). Proliferation-linked regulation of type II IMP dehydrogenase gene in human normal lymphocytes and HL-60 leukemic cells. Cancer Res. 52, 258-261.
76. Natsumeda, Y., and Carr, S.F. (1993). Human type I and II IMP dehydrogenases as drug targets. Ann. NY Acad. Sci. 696, 88-93.
77. Nelson, J.A., Rose, L.M., and Bennett, L.L., Jr. (1976). Effects of 2-amino-1,3,4,-thiadiazole on ribonucleotide pools of leukemia L1210 cells. Cancer Res. 36, 1375-1378.
78. Nelson, J.A., Rose, L.M., and Bennett, L.L., Jr. (1977). Mechanism of action of 2-amino-1,3,4,-thiadiazole (NSC 4728). Cancer Res. 37, 182-187.
79. Okayama, H., and Berg, P. (1983). A cDNA cloning vector that permits expression of cDNA inserts in mammalian cells. Mol. Cell. Biol. 3, 280-289.
80. Oltvai, Z.N., Milliman, C.L., and Korsmeyer, S.J. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609-619.
81. Onozawa, T., Danjoh, I., and Fujiyama, A. (1995). Biochemical similarity of Schizosaccharomyces pombe ras1 protein with RAS2 protein of Saccharomyces cervisiae. Yeast 11, 801-808.
82. Pall, M.L. (1985). GTP: A central regulator of cellular anabolism. Curr. Top. Cell. Regul. 25, 1-20.
83. Pall, M.L., and Robertson, C.K. (1988). Growth regulation by GTP. J. Biol. Chem. 263, 11168-11174.
84. Peeper, D.S., Upton, T.M., Ladha, M.H., Neuman, E., Zalvide, J., Bernards, R., DeCaprio, J.A., and Ewen, M.E. (1997). Ras signalling linked to the cell-cycle machinery by the retinoblastoma protein. Nature 386, 177-181.
85. Pelech, S.L., Meijer, L., and Krebs, E.G. (1987). Characterization of maturation-activated histone H1 and ribosomal S6 kinases in sea star oocytes. Biochemistry 26, 7960-7968.
86. Proffitt, R.T., Pathak, V.K., Villacorte, D.G., and Presant, C.A. (1983). Sensitive radiochemical assay for inosine-5′-monophosphate dehydrogenase and determination of activity in murine tumor tissue extracts. Cancer Res. 43, 1620-1623.
87. Putnam-Evans, C.L., Harmon, A.C., and Cormier, M.J. (1990). Purification and characterization of a novel calcium-dependent protein kinase from soybean. Biochemistry 29, 2488-2489.
88. Quartin, R.S., Cole, C.N., Pipas, J.M., and Levine, A.J. (1994). The amino-terminal functions of the simian virus 40 large T antigen are required to overcome wild-type p53-mediated growth arrest of cells. J. Virol. 68, 1334-1342.
89. Reed, R.R. (1990). G protein diversity and the regulation of signaling pathways. New Biol. 2, 957-960.
90. Rizzo, M.T., Tricot G., Hoffman, R., Jayaram, H.N., Weber, G., Garcia, J.G. N., and English, D. (1990). Inosine monophosphate dehydrogenase inhibitors. Probes for investigations of the functions of guanine nucleotide binding proteins in intact cells. Cell. Signal. 2, 509-519.
91. Robins, R.K., Srivastava, P.C., Narayanan, V.L., Plowman, J., Paull, K.D. (1982). 2-β-D-ribofuranosylthiazole-4-carboxamide, a novel potential antitumor agent for lung tumors and metastases. J. Med. Chem. 25, 107-108.
92. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning, A Laboratory Manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
93. Segawa, K., Minowa, A., Sugasawa, K., Takano, T., and Hanaoka, F. (1993). Abrogation of p53-mediated transactivation by SV40 large T antigen. Oncogene 8, 543-548.
94. Selvakumaran, M., Lin, H.-K., Miyashita, T., Wang, H.G., Krajewski, S., Reed, J.C., Hoffman, B., Lieberman, D. (1994). Immediate early up-regulation of bax expression by p53 but not TGFβ1: a paradigm for distinct apoptotic pathways. Oncogene 9, 1791-1798.
95. Shen, Y., and Shenk, T. (1994). Relief of p53-mediated transcriptional repression by the adenovirus E1B 19-kDa protein or the cellular Bcl-2 protein. Proc. Natl. Acad. Sci. USA, 91, 8940-8944.
96. Sherley, J.L. (1991). Guanine nucleotide biosynthesis is regulated by the cellular p53 concentration. J. Biol. Chem. 266, 24815-24828.
97. Sherley, J.L. (1996). The p53 rumor suppressor gene as regulator of somatic stem cell renewal division. Cope 12, 9-10.
98. Sherley, J.L., and Kelly, T.J. (1988). Regulation of human thymidine kinase during the cell cycle. J. Biol. Chem. 263, 8350-8358.
99. Sherley, J.L., Stadler, P.B., and Johnson, D.R. (1995a). The p53 antioncogene induces guanine nucleotide-dependent stem cell division kinetics. Proc. Natl. Acad. Sci. USA 92, 136-140.
100. Sherley, J.L., Stadler, P.B., and Stadler, J.S. (1995b). A quantitative method for the analysis of mammalian cell proliferation in culture in terms of dividing and non-dividing cells. Cell Proliferation 28, 137-144.
101. Sibley, D.R., Benovic, J.L., Caron, M.G., and Lefkowitz, R.J. (1987). Regulation of transmembrane signaling by receptor phosphorylation. Cell 48, 913-922.
102. Simon, M.I., Strathmann, M.P., and Gautam, N. (1992). Diversity of G proteins in signal transduction. Science 252, 802-808.
103. Spitovsky, D., Aengeneyndt, F., Braspenning, J., and Doeberitz, M. v.K. (1996). p53-independent growth regulation of cervical cancer cells by the papillomavirus E6 oncogene. Oncogene 13, 1027-1035.
104. Stadler, P.B., Pennacchi, J., and Sherley, J.L. (1994). Inosine-5′-monophosphate dehydrogenase activity is maintained in immortalized murine cells growth-arrested by serum deprivation. Adv. Enzyme Regul. 34, 91-106.
105. Stoehr, S.J., and Smolen, J.E. (1990). Human neutrophils contain a protein kinase C-like enzyme that utilizes guanosine triphosphate as a phosphate donor. Cofactor requirements, kinetics, and endogenous acceptor proteins. Blood 75, 479-487.
106. Streeter, D.G., Witkowski, J.T., Khare, G.P., Sidwell, R.W., Bauer, R.J., Robins, R.K., and Simon, L.N. (1973). Mechanism of action of 1-β-D-ribofuranosyl-1,2,4-triazole-3carboxamide (Virazole), a new broad-spectrum antiviral agent. Proc. Natl. Acad. Sci. USA 70, 1174-1178.
107. Szekeres, T., Fritzer, M., Pillwein, K., Felzmaim, T., and Chiba, P. (1992). Cell cycle dependent regulation of IMP dehydrogenase activity and effect of tiazofurin. Life Sci. 51, 1309-1315.
108. Tricot, G.J., Jayaram, H.N., Lapis, E., Natusmeda, Y., Nichols, C.R., Kneebone, P., Heerema, N., Weber, G., and Hoffman, R. (1989). Biochemically directed therapy of leukemia with tiazofurin, a selective blocker of inosine 5′-phosphate dehydrogenase activity. Cancer Res. 49, 3696-3701.
109. Turka, L.A., Dayton, J., Sinclair, G., Thompson, C.B., Mitchell, B.S. (1991). Guanine ribonucleotide depletion inhibits T cell activation: Mechanism of action of the immunosuppressive drug mizoribine. J. Clin. Invest. 87, 940-948.
110. Ullman, B. (1983). Characterization of mutant murine lymphoma cells with altered inosinate dehydrogenase activities. J. Biol. Chem. 258, 523-528.
111. Uritani, M., and Miyazaki, M. (1988). Characterization of the ATPase and GTPase activities of elongation factor 3 (EF-3) purified from yeasts. J. Biochem. 103, 522-530.
112. Vogelstein, B., and Kinzler, K.W. (1992). p53 function and dysfunction. Cell 70, 523-526.
113. Vousden, K.H., Vojtesek, B., Fisher, C., and Lane, D. (1993). HPV-16 E7 or adenovirus E1A can overcome the growth arrest of cells immortalized with a temperature-sensitive p53. Oncogene 8, 697-702.
114. Wang, Y., Okan, I., Szekely, L., Klein, G., and Wiman, K.G. (1995). Bcl-2 inhibits wild-type p53-triggered apoptosis but not G1 cell cycle arrest and transactivation of WAF1 and bax. Cell Growth & Differ. 6, 1071-1075.
115. Weber, G., Nakamura, H., Natsumeda, Y., Szekeres, T., and Nagai, M. (1992). Regulation of GTP biosynthesis. Advan. Enzyme Regul. 32, 57-69.
116. Williams, R.S., Shohet, R.V., and Stillman, B. (1997). A human protein related to yeast Cdc6p. Proc. Natl. Acad. Sci. USA 94, 142-147.
117. Yamashita, M., Fukada, S., Yoshikuni, M., Bulet, P., Hirai, T., Yamaguchi, A., Yasuda, H., Ohba, Y., and Nagahama, Y. (1992). M-phase-specific histone H1 kinase in fish oocytes: Purification, components, and biochemical properties. Eur. J. Biochem. 205, 537-543.
118. Yin, Y., Tainsky, M.A., Bischoff, F.Z., Strong, L.C., and Wahl, G.M. (1992). Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell 70, 937-948.
119. Zhen, W., Jayaram, H.N., and Weber, G. (1992). Antitumor activity of tiazofurin in human colon carcinoma HT-29. Cancer Invest. 10, 505-511.
120. Zwerschke, W., Rottjakob, H.-W., and Kuntzel, H. (1994). The Saccharomyces cerevisiae CDC6 gene is transcribed at late mitosis and encodes a ATP/GTPase controlling S phase initiation. J. Biol. Chem. 269, 23351-23356.