The UHRF family: Oncogenes that are drugable targets for cancer therapy in the near future?

Pharmacology and Therapeutics

Volumn 115, Issue 3, 2007, Pages 419-434

  Bronner, Christian ^a   Achour, Mayada ^a   Arima, Yoshimi ^b   Chataigneau, Thierry ^a   Saya, Hideyuki ^b   Schini Kerth, Valérie B ^a  

^a CNRS   (France)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Cancer; E3 ligases; ICBP90; Np95; Oncogenes; UHRF

Indexed keywords

BORTEZOMIB; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLINE; DNA METHYLTRANSFERASE 1; DOUBLE STRANDED RNA; HISTONE; HISTONE H1; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; HOMEODOMAIN PROTEIN; HYDROXYUREA; MESSENGER RNA; NPI 0052; PROTEASOME; PROTEIN MDM2; PROTEIN P130; PROTEIN P14; PROTEIN P16INK4A; PROTEIN P21; PROTEIN P53; TRANSCRIPTION FACTOR E2F4; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; UNINDEXED DRUG;

CANCER CELL; CANCER THERAPY; CARCINOGENESIS; CELL PROLIFERATION; DRUG TARGETING; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EPIGENETICS; FEEDBACK SYSTEM; HUMAN; INHERITANCE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; ONCOGENE UHRF; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; REVIEW; TUMOR SUPPRESSOR GENE; UHRF1 GENE; UHRF2 GENE;

ANIMALS; ANTINEOPLASTIC AGENTS; CCAAT-ENHANCER-BINDING PROTEINS; CELL PROLIFERATION; DRUG DELIVERY SYSTEMS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; MICE; NEOPLASMS; NUCLEAR PROTEINS; ONCOGENES; UBIQUITIN-PROTEIN LIGASES;

EID: 34548451241     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2007.06.003     Document Type: Review

References (122)

1. Anderson K.C. Targeted therapy of multiple myeloma based upon tumor-microenvironmental interactions. Exp Hematol 35 (2007) 155-162
2. 1/S transition. Genes Cells 9 (2004) 131-142
3. Attwood J.T., Yung R.L., and Richardson B.C. DNA methylation and the regulation of gene transcription. Cell Mol Life Sci 59 (2002) 241-257
4. Bachman K.E., Park B.H., Rhee I., Rajagopalan H., Herman J.G., Baylin S.B., et al. Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 3 (2003) 89-95
5. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 (2001) 120-124
6. Baumbusch L.O., Thorstensen T., Krauss V., Fischer A., Naumann K., Assalkhou R., et al. The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res 29 (2001) 4319-4333
7. Bonapace I.M., Latella L., Papait R., Nicassio F., Sacco A., Muto M., et al. Np95 is regulated by E1A during mitotic reactivation of terminally differentiated cells and is essential for S phase entry. J Cell Biol 157 (2002) 909-914
8. Brady M.E., Ozanne D.M., Gaughan L., Waite I., Cook S., Neal D.E., et al. Tip60 is a nuclear hormone receptor coactivator. J Biol Chem 274 (1999) 17599-17604
9. Bronner C., Hopfner R., and Mousli M. Transcriptional regulation of the topoisomerase IIalpha gene. Anticancer Res 22 (2002) 605-612
10. Bronner C., Trotzier M.A., Filhol O., Cochet C., Rochette-Egly C., Scholler-Guinard M., et al. The antiapoptotic protein ICBP90 is a target for protein kinase 2. Ann N Y Acad Sci 1030 (2004) 355-360
11. Bronner C., Chataigneau T., and Schini-Kerth V.B. Chapter III. Epigenetic control of gene transcription. In: Giordano A. (Ed). From the control of cell growth to cancer (2007), Wiley and Sons publisher, Chichester
12. Buffart T.E., Carvalho B., Hopmans E., Brehm V., Kranenbarg E.K., Schaaij-Visser T.B., et al. Gastric cancers in young and elderly patients show different genomic profiles. J Pathol 211 (2007) 45-51
13. Cameron E.E., Bachman K.E., Myohanen S., Herman J.G., and Baylin S.B. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 21 (1999) 103-107
14. Chan H.M., Smith L., and La Thangue N.B. Role of LXCXE motif-dependent interactions in the activity of the retinoblastoma protein. Oncogene 20 (2001) 6152-6163
15. Chauhan D., Hideshima T., and Anderson K.C. A novel proteasome inhibitor NPI-0052 as an anticancer therapy. Br J Cancer 95 (2006) 961-965
16. *BARD1 RING ubiquitin ligase. J Biol Chem 277 (2002) 22085-22092
17. Chen C., Seth A.K., and Aplin A.E. Genetic and expression aberrations of E3 ubiquitin ligases in human breast cancer. Mol Cancer Res 4 (2006) 695-707
18. Chen I.T., Smith M.L., O'Connor P.M., and Fornace Jr. A.J. Direct interaction of Gadd45 with PCNA and evidence for competitive interaction of Gadd45 and p21Waf1/Cip1 with PCNA. Oncogene 11 (1995) 1931-1937
19. 2/M cell cycle arrest. Virology 305 (2003) 371-377
20. Citterio E., Papait R., Nicassio F., Vecchi M., Gomiero P., Mantovani R., et al. Np95 is a histone-binding protein endowed with ubiquitin ligase activity. Mol Cell Biol 24 (2004) 2526-2535
21. Cress W.D., and Seto E. Histone deacetylases, transcriptional control, and cancer. J Cell Physiol 184 (2000) 1-16
22. Crnogorac-Jurcevic T., Gangeswaran R., Bhakta V., Capurso G., Lattimore S., Akada M., et al. Proteomic analysis of chronic pancreatitis and pancreatic adenocarcinoma. Gastroenterology 129 (2005) 1454-1463
23. Dehal P., Satou Y., Campbell R.K., Chapman J., Degnan B., De Tomaso A., et al. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298 (2002) 2157-2167
24. Dugas J.C., Tai Y.C., Speed T.P., Ngai J., and Barres B.A. Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26 (2006) 10967-10983
25. Ezhkova E., and Tansey W.P. Proteasomal ATPases link ubiquitylation of histone H2B to methylation of histone H3. Mol Cell 13 (2004) 435-442
26. Fan S., Yuan R., Ma Y.X., Xiong J., Meng Q., Erdos M., et al. Disruption of BRCA1 LXCXE motif alters BRCA1 functional activity and regulation of RB family but not RB protein binding. Oncogene 20 (2001) 4827-4841
27. Fang J., Chen T., Chadwick B., Li E., and Zhang Y. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J Biol Chem 279 (2004) 52812-52815
28. Feldman N., Gerson A., Fang J., Li E., Zhang Y., Shinkai Y., et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat Cell Biol 8 (2006) 188-194
29. Fujimori A., Matsuda Y., Takemoto Y., Hashimoto Y., Kubo E., Araki R., et al. Cloning and mapping of Np95 gene which encodes a novel nuclear protein associated with cell proliferation. Mamm Genome 12 (1998) 1032-1035
30. Gius D., Bradbury C.M., Sun L., Awwad R.T., Huang L., Smart D.D., et al. The epigenome as a molecular marker and target. Cancer 104 (2005) 1789-1793
31. Glinsky G.V., Berezovska O., and Glinskii A.B. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest 115 (2005) 1503-1521
32. Gong T.W., Karolyi I.J., Macdonald J., Beyer L., Raphael Y., Kohrman D.C., et al. Age-related changes in cochlear gene expression in normal and shaker 2 mice. J Assoc Res Otolaryngol 7 (2006) 317-328
33. Gross J.M., Perkins B.D., Amsterdam A., Egana A., Darland T., Matsui J.I., Sciascia S., et al. Identification of zebrafish insertional mutants with defects in visual system development and function. Genetics 170 (2005) 245-261
34. Hartwell L.H., and Kastan M.B. Cell cycle control and cancer. Science 266 (1994) 1821-1828
35. Heir R., Ablasou C., Dumontier E., Elliott M., Fagotto-Kaufmann C., and Bedford F.K. The UBL domain of PLIC-1 regulates aggresome formation. EMBO Rep 7 (2006) 1252-1258
36. Hopfner R., Mousli M., Garnier J.M., Redon R., du Manoir S., Chatton B., et al. Genomic structure and chromosomal mapping of the gene coding for ICBP90, a protein involved in the regulation of the topoisomerase IIα gene expression. Gene 266 (2001) 15-23
37. Hopfner R., Mousli M., Jeltsch J.M., Voulgaris A., Lutz Y., Marin C., et al. ICBP90, a novel human CCAAT binding protein, involved in the regulation of topoisomerase IIα expression. Cancer Res 60 (2000) 121-128
38. Hopfner R., Mousli M., Oudet P., and Bronner C. Overexpression of ICBP90, a novel CCAAT-binding protein, overcomes cell contact inhibition by forcing topoisomerase IIα expression. Anticancer Res 22 (2002) 3165-3170
39. Hunter T. Oncoprotein networks. Cell 88 (1997) 333-346
40. Iida T., Suetake I., Tajima S., Morioka H., Ohta S., Obuse C., et al. PCNA clamp facilitates action of DNA cytosine methyltransferase 1 on hemimethylated DNA. Genes Cells 7 (2002) 997-1007
41. Inaba K., Padma P., Satouh Y., Shin-I T., Kohara Y., Satoh N., et al. ST analysis of gene expression in testis of the ascidian Ciona intestinalis. Mol Reprod Dev 62 (2002) 431-445
42. Issaeva N., Bozko P., Enge M., Protopopova M., Verhoef L.G., Masucci M., et al. Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors. Nat Med 10 (2004) 1321-1328
43. Ito A., Kawaguchi Y., Lai C.H., Kovacs J.J., Higashimoto Y., Appella E., et al. MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J 21 (2002) 6236-6245
44. Jaenisch R., and Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 (2003) 245-254
45. 1/S transition during the cell cycle. Oncogene 24 (2005) 7337-7345
46. Jenkins Y., Markovtsov V., Lang W., Sharma P., Pearsall D., Warner J., et al. Critical role of the ubiquitin ligase activity of UHRF1, a nuclear RING finger protein, in tumor cell growth. Mol Biol Cell 16 (2005) 5621-5629
47. Jenuwein T., and Allis C.D. Translating the histone code. Science 293 (2001) 1074-1080
48. Joazeiro C.A., and Weissman A.M. RING finger proteins: mediators of ubiquitin ligase activity. Cell 102 (2000) 549-552
49. Jones P.A. Effects of 5-azacytidine and its 2′-deoxyderivative on cell differentiation and DNA methylation. Pharmacol Ther 28 (1985) 17-27
50. Jones P.A., and Baylin S.B. The fundamental role of epigenetic events in cancer. Nat Rev Genet 3 (2002) 415-428
51. Kerscher O., Felberbaum R., and Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22 (2006) 159-180
52. Kinross K.M., Clark A.J., Iazzolino R.M., and Humbert P.O. E2f4 regulates fetal erythropoiesis through the promotion of cellular proliferation. Blood 108 (2006) 886-895
53. Klose R.J., and Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31 (2006) 89-97
54. Lachner M., and Jenuwein T. The many faces of histone lysine methylation. Curr Opin Cell Biol 14 (2002) 286-298
55. Laird P.W. The power and the promise of DNA methylation markers. Nat Rev Cancer 3 (2003) 253-266
56. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 3 (2002) 662-673
57. Li L.C., Okino S.T., Zhao H., Pookot D., Place R.F., Urakami S., et al. Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci U S A 103 (2006) 17337-17342
58. 1 arrest and associates with Cdk2. Biochem Biophys Res Commun 319 (2004) 464-468
59. Locker J., Tian J., Carver R., Concas D., Cossu C., Ledda-Columbano G.M., et al. A common set of immediate-early response genes in liver regeneration and hyperplasia. Hepatology 38 (2003) 314-325
60. Lorenzato M., Caudroy S., Bronner C., Evrard G., Simon M., Durlach A., et al. Cell cycle and/or proliferation markers: what is the best method to discriminate cervical high-grade lesions?. Hum Pathol 36 (2005) 1101-1107
61. Lorick K.L., Jensen J.P., Fang S., Ong A.M., Hatakeyama S., and Weissman A.M. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci U S A 96 (1999) 11364-11369
62. Luo Y., Hurwitz J., and Massague J. Cell-cycle inhibition by independent CDK and PCNA binding domains in p21Cip1. Nature 375 (1995) 159-161
63. Lou Z., Minter-Dykhouse K., and Chen J. BRCA1 participates in DNA decatenation. Nat Struct Mol Biol 12 (2005) 589-593
64. Macaluso M., Cinti C., Russo G., Russo A., and Giordano A. pRb2/p130-E2F4/5-HDAC1-SUV39H1-p300 and pRb2/p130-E2F4/5-HDAC1-SUV39H1-DNMT1 multimolecular complexes mediate the transcription of estrogen receptor-alpha in breast cancer. Oncogene 22 (2003) 3511-3517
65. Mallery D.L., Vandenberg C.J., and Hiom K. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J 21 (2002) 6755-6762
66. McGarrity T.J., and Amos C. Peutz-Jeghers syndrome: clinicopathology and molecular alterations. Cell Mol Life Sci 63 (2006) 2135-2144
67. Mellor J. It takes a PHD to read the histone code. Cell 126 (2006) 22-24
68. Mikkers H., and Berns A. Retroviral insertional mutagenesis: tagging cancer pathways. Adv Cancer Res 88 (2003) 53-99
69. Miura M., Watanabe H., Sasaki T., Tatsumi K., and Muto M. Dynamic changes in subnuclear NP95 location during the cell cycle and its spatial relationship with DNA replication foci. Exp Cell Res 263 (2001) 202-208
70. Momand J., Zambetti G.P., Olson D.C., George D., and Levine A.J. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69 (1992) 1237-1245
71. Momparler R.L. Cancer epigenetics. Oncogene 22 (2003) 6479-6483
72. Mori T., Li Y., Hata H., and Kochi H. NIRF is a ubiquitin ligase that is capable of ubiquitinating PCNP, a PEST-containing nuclear protein. FEBS Lett 557 (2004) 209-214
73. Mori T., Li Y., Hata H., Ono K., and Kochi H. NIRF, a novel RING finger protein, is involved in cell-cycle regulation. Biochem Biophys Res Commun 296 (2002) 530-536
74. Mortusewicz O., Schermelleh L., Walter J., Cardoso M.C., and Leonhardt H. Recruitment of DNA methyltransferase I to DNA repair sites. Proc Natl Acad Sci USA 102 (2005) 8905-8909
75. Mousli M., Hopfner R., Abbady A.Q., Monte D., Jeanblanc M., Oudet P., et al. ICBP90 belongs to a new family of proteins with an expression that is deregulated in cancer cells. Br J Cancer 89 (2003) 120-127
76. Muto M., Fujimori A., Nenoi M., Daino K., Matsuda Y., Kuroiwa A., et al. Isolation and Characterization of a Novel Human Radiosusceptibility Gene, NP95. Radiat Res 166 (2006) 723-733
77. Muto M., Kanari Y., Kubo E., Takabe T., Kurihara T., Fujimori A., et al. Targeted disruption of Np95 gene renders murine embryonic stem cells hypersensitive to DNA damaging agents and DNA replication blocks. J Biol Chem 277 (2002) 34549-34555
78. Muto M., Utsuyama M., Horiguchi T., Kubo E., Sado T., and Hirokawa K. The characterization of the monoclonal antibody Th-10a, specific for a nuclear protein appearing in the S phase of the cell cycle in normal thymocytes and its unregulated expression in lymphoma cell lines. Cell Prolif 28 (1995) 645-657
79. Naumann K., Fischer A., Hofmann I., Krauss V., Phalke S., Irmler K., et al. Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24 (2005) 1418-1429
80. Nicolas E., Ait-Si-Ali S., and Trouche D. The histone deacetylase HDAC3 targets RbAp48 to the retinoblastoma protein. Nucleic Acids Res 29 (2001) 3131-3136
81. Oba-Shinjo S.M., Bengtson M.H., Winnischofer S.M., Colin C., Vedoy C.G., de Mendonca Z., et al. Identification of novel differentially expressed genes in human astrocytomas by cDNA representational difference analysis. Brain Res Mol Brain Res 140 (2005) 25-33
82. Ogawa K., Solt D.B., and Farber E. Phenotypic diversity as an early property of putative preneoplastic hepatocyte populations in liver carcinogenesis. Cancer Res 40 (1980) 725-733
83. Papait R., Pistore C., Negri D., Pecoraro D., Cantarini L., and Bonapace I.M. Np95 Is Implicated in Pericentromeric Heterochromatin Replication and in Major Satellite Silencing. Mol Biol Cell 18 (2007) 1098-1106
84. Paull T.T., Cortez D., Bowers B., Elledge S.J., and Gellert M. Direct DNA binding by Brca1. Proc Natl Acad Sci U S A 98 (2001) 6086-6091
85. 2. Nature 442 (2006) 100-103
86. Pound A.W., and McGuire L.J. Repeated partial hepatectomy as a promoting stimulus for carcinogenic response of liver to nitrosamines in rats. Br J Cancer 37 (1978) 585-594
87. Qian Y.W., Wang Y.C., Hollingsworth R., Jones D., Ling N., and Lee E.A. A retinoblastoma-binding protein related to a negative regulator of Ras in yeast. Nature 364 (1993) 648-652
88. Rechsteiner M., and Rogers S.W. PEST sequences and regulation by proteolysis. Trends Biochem Sci 21 (1996) 267-271
89. Robertson K.D. DNA methylation and human disease. Nat Rev Genet 6 (2005) 597-610
90. Roccaro A.M., Hideshima T., Richardson P.G., Russo D., Ribatti D., Vacca A., et al. Bortezomib as an antitumor agent. Curr Pharm Biotechnol 7 (2006) 441-448
91. Sadler K.C., Krahn K.N., Gaur N.A., and Ukomadu C. Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1. Proc Natl Acad Sci U S A 104 (2007) 1570-1575
92. Sakai A., Kikuchi Y., Muroi M., Masui T., Furihata C., Uchida E., et al. Overexpression of NP95 mRNA by tumor promoters in the promotion phase of a two-stage BALB/3T3 cell transformation assay. Biol Pharm Bull 26 (2003) 347-351
93. Schaaf G.J., Ruijter J.M., van Ruissen F., Zwijnenburg D.A., Waaijer R., Valentijn L.J., et al. Full transcriptome analysis of rhabdomyosarcoma, normal, and fetal skeletal muscle: statistical comparison of multiple SAGE libraries. FASEB J 19 (2005) 404-406
94. Shen W.H. NtSET1, a member of a newly identified subgroup of plant SET-domain-containing proteins, is chromatin-associated and its ectopic overexpression inhibits tobacco plant growth. Plant J 28 (2001) 371-383
95. 1 cyclin-dependent kinases. Genes Dev 9 (1995) 1149-1163
96. 2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442 (2006) 96-99
97. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75 (2006) 243-269
98. Starita L.M., and Parvin J.D. The multiple nuclear functions of BRCA1: transcription, ubiquitination and DNA repair. Curr Opin Cell Biol 15 (2003) 345-350
99. St-Arnaud R., and Quelo I. Transcriptional coactivators potentiating AP-1 function in bone. Front Biosci 3 (1998) D838-D848
100. Strahl B.D., and Allis C.D. The language of covalent histone modifications. Nature 403 (2000) 41-45
101. Sun Y. Targeting E3 ubiquitin ligases for cancer therapy. Cancer Biol Ther 2 (2003) 623-629
102. Sun Y. E3 ubiquitin ligases as cancer targets and biomarkers. Neoplasia 8 (2006) 645-654
103. Sun Z.W., and Allis C.D. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418 (2002) 104-108
104. Trotzier M.A., Bronner C., Bathami K., Mathieu E., Abbady A.Q., Jeanblanc M., et al. Phosphorylation of ICBP90 by protein kinase A enhances topoisomerase IIalpha expression. Biochem Biophys Res Commun 319 (2004) 590-595
105. Uchida C., Miwa S., Isobe T., Kitagawa K., Hattori T., Oda T., et al. Effects of MdmX on Mdm2-mediated downregulation of pRB. FEBS Lett 580 (2006) 1753-1758
106. Uemura T., Kubo E., Kanari Y., Ikemura T., Tatsumi K., and Muto M. Temporal and spatial localization of novel nuclear protein NP95 in mitotic and meiotic cells. Cell Struct Funct 25 (2000) 149-159
107. Un F., Oi C., Prosser M., Wang N., Zhou B., Bronner C., et al. Modulating ICBP90 to suppress human ribonucleotide reductase M2 induction restores sensitivity to hydroxyurea cytotoxicity. Anticancer Res 26 (2006) 2761-2767
108. Unoki M., Nishidate T., and Nakamura Y. ICBP90, an E2F-1 target, recruits HDAC1 and binds to methyl-CpG through its SRA domain. Oncogene 23 (2004) 7601-7610
109. Varmus H., Pao W., Politi K., Podsypanina K., and Du Y.C. Oncogenes come of age. Cold Spring Harb Symp Quant Biol 70 (2005) 1-9
110. Vassilev L.T., Vu B.T., Graves B., Carvajal D., Podlaski F., Filipovic Z., et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303 (2004) 844-848
111. Vazquez N., Greenwell-Wild T., Marinos N.J., Swaim W.D., Nares S., Ott D.E., et al. Human immunodeficiency virus type 1-induced macrophage gene expression includes the p21 gene, a target for viral regulation. J Virol 79 (2005) 4479-4491
112. Ventura A., Kirsch D.G., McLaughlin M.E., Tuveson D.A., Grimm J., Lintault L., et al. Restoration of p53 function leads to tumour regression in vivo. Nature 445 (2007) 661-665
113. Waga S., Hannon G.J., Beach D., and Stillman B. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369 (1994) 574-578
114. Wang H., Zhai L., Xu J., Joo H.Y., Jackson S., Erdjument-Bromage H., et al. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 22 (2006) 383-394
115. Wang Q.T., Piotrowska K., Ciemerych M.A., Milenkovic L., Scott M.P., Davis R.W., et al. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6 (2004) 133-144
116. Wei J., Zhai L., Xu J., and Wang H. Role of Bmi1 in H2A ubiquitylation and Hox gene silencing. J Biol Chem 281 (2006) 22537-22544
117. Wiltshire T., Senft J., Wang Y., Konat G.W., Wenger S.L., Reed E., et al. BRCA1 contributes to cell cycle arrest and chemoresistance in response to anticancer agent, irofulven. Mol Pharmacol 71 (2007) 1051-1060
118. Woo H.R., Pontes O., Pikaard C.S., and Richards E.J. VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev 21 (2007) 267-277
119. WAF1/CIP1-induced apoptosis in human ovarian cancer cells. J Biol Chem 277 (2002) 36329-36337
120. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442 (2006) 86-90
121. Xie Y., and Varshavsky A. UFD4 lacking the proteasome-binding region catalyses ubiquitination but is impaired in proteolysis. Nat Cell Biol 12 (2002) 1003-1007
122. Yoshizuka N., Yoshizuka-Chadani Y., Krishnan V., and Zeichner S.L. Human immunodeficiency virus type 1 Vpr-dependent cell cycle arrest through a mitogen-activated protein kinase signal transduction pathway. J Virol 79 (2005) 11366-11381