Abstract
In fission yeast, the rad3 gene product plays a critical role in sensing DNA structure defects and activating damage response pathways. A structural homologue of rad3 in humans (ATR) has been identified based on sequence similarity in the protein kinase domain. General information regarding ATR expression, protein kinase activity, and cellular localization is known, but its function in human cells remains undetermined. In the current study, the ATR protein was examined by gel filtration of protein extracts and was found to exist predominantly as part of a large protein complex. A kinase-inactivated form of the ATR gene was prepared by site-directed mutagenesis and was used in transfection experiments to probe the function of this complex. Introduction of this kinase-dead ATR into a normal fibroblast cell line, an ATM-deficient fibroblast line derived from a patient with ataxia-telangiectasia, or a p53 mutant cell line all resulted in significant losses in cell viability. Clones expressing the kinase-dead ATR displayed increased sensitivity to x-rays and UV and a loss of checkpoint control. We conclude that ATR functions as a critical part of a protein complex that mediates responses to ionizing and UV radiation in human cells. These responses include effects on cell viability and cell cycle checkpoint control.
MeSH Terms
Ataxia Telangiectasia Mutated Proteins
Cell Cycle/genetics,radiation effects
Cell Cycle Proteins/genetics,physiology
Cell Line
Humans
Mutagenesis, Site-Directed
Mutation
Protein Kinases/genetics
Protein Serine-Threonine Kinases
Radiation Tolerance/genetics
Schizosaccharomyces
Transfection
Tumor Suppressor Protein p53/genetics,physiology
Ultraviolet Rays
Chemicals
Cell Cycle Proteins
Tumor Suppressor Protein p53
Protein Kinases
ATR protein, human
Ataxia Telangiectasia Mutated Proteins
Protein Serine-Threonine Kinases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Wright J A
Virginia Mason Research Center, 1000 Seneca Street, Seattle, WA 98101 and Department of Immunology, University of Washington School of Medicine, Seattle, WA 98195, USA.
Keegan K S
Herendeen D R
Bentley N J
Carr A M
Hoekstra M F
Concannon P
References (21)
21 references, click to expand
-
The cellular responses to DNA damage.
Trends Cell Biol. 1995 Jan;5(1):32-40
PMID: 14731431
-
Ataxia-telangiectasia: an interdisciplinary approach to pathogenesis.
Medicine (Baltimore). 1991 Mar;70(2):99-117
PMID: 2005780
-
Human, mouse, and rat calnexin cDNA cloning: identification of potential calcium binding motifs and gene localization to human chromosome 5.
Biochemistry. 1994 Mar 22;33(11):3229-36
PMID: 8136357
-
Radiosensitivity in ataxia-telangiectasia: anomalies in radiation-induced cell cycle delay.
Int J Radiat Biol. 1994 Feb;65(2):175-84
PMID: 7907115
-
Establishment and characterization of a permanent pSV ori--transformed ataxia-telangiectasia cell line.
Exp Cell Res. 1985 May;158(1):119-26
PMID: 2987007
-
PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints.
Science. 1995 Oct 6;270(5233):50-1
PMID: 7569949
-
The Schizosaccharomyces pombe rad3 checkpoint gene.
EMBO J. 1996 Dec 2;15(23):6641-51
PMID: 8978690
-
A single ataxia telangiectasia gene with a product similar to PI-3 kinase.
Science. 1995 Jun 23;268(5218):1749-53
PMID: 7792600
-
Isolation and characterization of the Schizosaccharomyces pombe rad3 gene, involved in the DNA damage and DNA synthesis checkpoints.
Gene. 1992 Sep 21;119(1):83-9
PMID: 1398093
-
Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair.
Genes Dev. 1994 Mar 15;8(6):652-65
PMID: 7926756
-
p53 point mutation in HPV negative human cervical carcinoma cell lines.
Oncogene. 1991 May;6(5):873-5
PMID: 1646990
-
A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage.
Cell. 1995 Sep 8;82(5):841-7
PMID: 7671311
-
Checkpoints: controls that ensure the order of cell cycle events.
Science. 1989 Nov 3;246(4930):629-34
PMID: 2683079
-
Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints.
EMBO J. 1998 Jan 2;17(1):159-69
PMID: 9427750
-
An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae.
Nucleic Acids Res. 1994 Aug 11;22(15):3104-12
PMID: 8065923
-
TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene.
Cell. 1995 Sep 8;82(5):823-9
PMID: 7671310
-
cDNA cloning and gene mapping of a candidate human cell cycle checkpoint protein.
Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2850-5
PMID: 8610130
-
Ataxia-telangiectasia and cellular responses to DNA damage.
Cancer Res. 1995 Dec 15;55(24):5991-6001
PMID: 8521380
-
Control of cell cycle arrest by the Mec1sc/Rad3sp DNA structure checkpoint pathway.
Curr Opin Genet Dev. 1997 Feb;7(1):93-8
PMID: 9024628
-
The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes.
Genes Dev. 1996 Oct 1;10(19):2423-37
PMID: 8843195
-
TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1.
Cell. 1995 Sep 8;82(5):831-40
PMID: 7545545