Abstract
Early cellular events associated with tumorigenesis often include loss of cell cycle checkpoints or alteration in growth signaling pathways. Identification of novel genes involved in cellular proliferation may lead to new classes of cancer therapeutics. By screening a tetracycline-inducible cDNA library in A549 cells for genes that interfere with proliferation, we have identified a fragment of UHRF1 (ubiquitin-like protein containing PHD and RING domains 1), a nuclear RING finger protein, that acts as a dominant negative effector of cell growth. Reduction of UHRF1 levels using an UHRF1-specific shRNA decreased growth rates in several tumor cell lines. In addition, treatment of A549 cells with agents that activated different cell cycle checkpoints resulted in down-regulation of UHRF1. The primary sequence of UHRF1 contains a PHD and a RING motif, both of which are structural hallmarks of ubiquitin E3 ligases. We have confirmed using an in vitro autoubiquitination assay that UHRF1 displays RING-dependent E3 ligase activity. Overexpression of a GFP-fused UHRF1 RING mutant that lacks ligase activity sensitizes cells to treatment with various chemotherapeutics. Taken together, our results suggest a general requirement for UHRF1 in tumor cell proliferation and implicate the RING domain of UHRF1 as a functional determinant of growth regulation.
MeSH Terms
Binding Sites
CCAAT-Enhancer-Binding Proteins/chemistry,genetics,metabolism
Cell Division/physiology
Cell Line, Tumor
Cloning, Molecular
HeLa Cells
Humans
Kinetics
Neoplasms/enzymology
Oligonucleotides, Antisense
Recombinant Proteins/metabolism
Retroviridae/genetics
Transcription, Genetic
Ubiquitin-Protein Ligases
Chemicals
CCAAT-Enhancer-Binding Proteins
Oligonucleotides, Antisense
Recombinant Proteins
UHRF1 protein, human
Ubiquitin-Protein Ligases
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Jenkins Yonchu
Rigel Pharmaceuticals, South San Francisco, CA 94080, USA. yjenkins@rigel.com
Markovtsov Vadim
Lang Wayne
Sharma Poonam
Pearsall Denise
Warner Justin
Franci Christian
Huang Betty
Huang Jianing
Yam George C
Vistan Joseph P
Pali Erlina
Vialard Jorge
Janicot Michel
Lorens James B
Payan Donald G
Hitoshi Yasumichi
References (31)
31 references, click to expand
-
ICBP90, a novel human CCAAT binding protein, involved in the regulation of topoisomerase IIalpha expression.
Cancer Res. 2000 Jan 1;60(1):121-8
PMID: 10646863
-
ICBP90 belongs to a new family of proteins with an expression that is deregulated in cancer cells.
Br J Cancer. 2003 Jul 7;89(1):120-7
PMID: 12838312
-
Optimization of regulated LTR-mediated expression.
Virology. 2000 Jun 20;272(1):7-15
PMID: 10873744
-
The APC11 RING-H2 finger mediates E2-dependent ubiquitination.
Mol Biol Cell. 2000 Jul;11(7):2315-25
PMID: 10888670
-
The RING-H2 finger protein APC11 and the E2 enzyme UBC4 are sufficient to ubiquitinate substrates of the anaphase-promoting complex.
Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8973-8
PMID: 10922056
-
The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases.
Trends Cell Biol. 2000 Oct;10(10):429-39
PMID: 10998601
-
Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.
Nature. 2001 May 24;411(6836):494-8
PMID: 11373684
-
Mechanisms underlying ubiquitination.
Annu Rev Biochem. 2001;70:503-33
PMID: 11395416
-
Np95 is regulated by E1A during mitotic reactivation of terminally differentiated cells and is essential for S phase entry.
J Cell Biol. 2002 Jun 10;157(6):909-14
PMID: 12058012
-
NIRF, a novel RING finger protein, is involved in cell-cycle regulation.
Biochem Biophys Res Commun. 2002 Aug 23;296(3):530-6
PMID: 12176013
-
Targeted disruption of Np95 gene renders murine embryonic stem cells hypersensitive to DNA damaging agents and DNA replication blocks.
J Biol Chem. 2002 Sep 13;277(37):34549-55
PMID: 12084726
-
Cellular localization and antiproliferative effect of peptides discovered from a functional screen of a retrovirally delivered random peptide library.
Chem Biol. 2003 Oct;10(10):975-87
PMID: 14583264
-
Transcriptional regulation by histone ubiquitination and deubiquitination.
Genes Dev. 2003 Nov 15;17(22):2733-40
PMID: 14630937
-
Targeting E3 ubiquitin ligases for cancer therapy.
Cancer Biol Ther. 2003 Nov-Dec;2(6):623-9
PMID: 14688465
-
NIRF is a ubiquitin ligase that is capable of ubiquitinating PCNP, a PEST-containing nuclear protein.
FEBS Lett. 2004 Jan 16;557(1-3):209-14
PMID: 14741369
-
Np95 is a histone-binding protein endowed with ubiquitin ligase activity.
Mol Cell Biol. 2004 Mar;24(6):2526-35
PMID: 14993289
-
Down-regulation of nuclear protein ICBP90 by p53/p21Cip1/WAF1-dependent DNA-damage checkpoint signals contributes to cell cycle arrest at G1/S transition.
Genes Cells. 2004 Feb;9(2):131-42
PMID: 15009091
-
Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases.
Oncogene. 2004 Mar 15;23(11):2057-70
PMID: 15021893
-
The novel functions of ubiquitination in signaling.
Curr Opin Cell Biol. 2004 Apr;16(2):119-26
PMID: 15196553
-
Ubiquitin signalling: what's in a chain?
Nat Cell Biol. 2004 Jul;6(7):571-2
PMID: 15232583
-
Molecular biology: what ubiquitin can do for transcription.
Curr Biol. 2004 Aug 10;14(15):R622-4
PMID: 15296779
-
ICBP90, an E2F-1 target, recruits HDAC1 and binds to methyl-CpG through its SRA domain.
Oncogene. 2004 Oct 7;23(46):7601-10
PMID: 15361834
-
Integration of murine leukemia virus DNA depends on mitosis.
EMBO J. 1993 May;12(5):2099-108
PMID: 8491198
-
The ubiquitin system.
Annu Rev Biochem. 1998;67:425-79
PMID: 9759494
-
Cloning and mapping of Np95 gene which encodes a novel nuclear protein associated with cell proliferation.
Mamm Genome. 1998 Dec;9(12):1032-5
PMID: 9880673
-
Multiple roles for the receptor tyrosine kinase axl in tumor formation.
Cancer Res. 2005 Oct 15;65(20):9294-303
PMID: 16230391
-
PHD domains and E3 ubiquitin ligases: viruses make the connection.
Trends Cell Biol. 2003 Jan;13(1):7-12
PMID: 12480335
-
Overexpression of ICBP90, a novel CCAAT-binding protein, overcomes cell contact inhibition by forcing topoisomerase II alpha expression.
Anticancer Res. 2002 Nov-Dec;22(6A):3165-70
PMID: 12530060
-
A conserved RING finger protein required for histone H2B monoubiquitination and cell size control.
Mol Cell. 2003 Jan;11(1):261-6
PMID: 12535538
-
Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter.
Mol Cell. 2003 Jan;11(1):267-74
PMID: 12535539
-
RING for destruction?
Curr Biol. 2000 Jan 27;10(2):R84-7
PMID: 10662664