Functional and Physical Interactions of the ARF Tumor Suppressor with p53 and Mdm2
The INK4a-ARF locus encodes two proteins, p16INK4aand p19ARF, that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53....
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 95; no. 14; pp. 8292 - 8297 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences of the United States of America
07.07.1998
National Acad Sciences National Academy of Sciences The National Academy of Sciences |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The INK4a-ARF locus encodes two proteins, p16INK4aand p19ARF, that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53. Using insect cells infected with baculovirus vectors and NIH 3T3 fibroblasts infected with ARF retrovirus, we determined that mouse p19ARFcan interact directly with p53, as well as with the p53 regulator mdm2. ARF can bind p53-DNA complexes, and it depends upon functional p53 to transcriptionally induce mdm2 and the cyclin-dependent kinase inhibitor p21Cip1, and to arrest cell proliferation. Binding of p19ARFto p53 requires the ARF N-terminal domain (amino acids 1-62) that is necessary and sufficient to induce cell cycle arrest. Overexpression of p19ARFin wild type or ARF-null mouse embryo fibroblasts increases the half-life of p53 from 15 to ≈ 75 min, correlating with an increased p53-dependent transcriptional response and growth arrest. Surprisingly, when overexpressed at supra-physiologic levels after introduction into ARF-null NIH 3T3 cells or mouse embryo fibroblasts, the p53 protein is handicapped in inducing this checkpoint response. In this setting, reintroduction of p19ARFrestores p53's ability to induce p21Cip1and mdm2, implying that, in addition to stabilizing p53, ARF modulates p53-dependent function through an additional mechanism. |
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| AbstractList | The
INK4a-ARF
locus encodes two proteins, p16
INK4a
and p19
ARF
, that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53. Using insect cells infected with baculovirus vectors and NIH 3T3 fibroblasts infected with ARF retrovirus, we determined that mouse p19
ARF
can interact directly with p53, as well as with the p53 regulator mdm2. ARF can bind p53-DNA complexes, and it depends upon functional p53 to transcriptionally induce mdm2 and the cyclin-dependent kinase inhibitor p21
Cip1
, and to arrest cell proliferation. Binding of p19
ARF
to p53 requires the ARF N-terminal domain (amino acids 1–62) that is necessary and sufficient to induce cell cycle arrest. Overexpression of p19
ARF
in wild type or
ARF
-null mouse embryo fibroblasts increases the half-life of p53 from 15 to ≈75 min, correlating with an increased p53-dependent transcriptional response and growth arrest. Surprisingly, when overexpressed at supra-physiologic levels after introduction into
ARF
-null NIH 3T3 cells or mouse embryo fibroblasts, the p53 protein is handicapped in inducing this checkpoint response. In this setting, reintroduction of p19
ARF
restores p53’s ability to induce p21
Cip1
and mdm2, implying that, in addition to stabilizing p53, ARF modulates p53-dependent function through an additional mechanism. The INK4a-ARF locus encodes two proteins, p16(INK4a) and p19(ARF), that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53. Using insect cells infected with baculovirus vectors and NIH 3T3 fibroblasts infected with ARF retrovirus, we determined that mouse p19(ARF) can interact directly with p53, as well as with the p53 regulator mdm2. ARF can bind p53-DNA complexes, and it depends upon functional p53 to transcriptionally induce mdm2 and the cyclin-dependent kinase inhibitor p21(Cip1), and to arrest cell proliferation. Binding of p19(ARF) to p53 requires the ARF N-terminal domain (amino acids 1-62) that is necessary and sufficient to induce cell cycle arrest. Overexpression of p19(ARF) in wild type or ARF-null mouse embryo fibroblasts increases the half-life of p53 from 15 to approximately 75 min, correlating with an increased p53-dependent transcriptional response and growth arrest. Surprisingly, when overexpressed at supra-physiologic levels after introduction into ARF-null NIH 3T3 cells or mouse embryo fibroblasts, the p53 protein is handicapped in inducing this checkpoint response. In this setting, reintroduction of p19(ARF) restores p53's ability to induce p21(Cip1) and mdm2, implying that, in addition to stabilizing p53, ARF modulates p53-dependent function through an additional mechanism. The INK4a-ARF locus encodes two proteins, p16 INK4a and p19 ARF , that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53. Using insect cells infected with baculovirus vectors and NIH 3T3 fibroblasts infected with ARF retrovirus, we determined that mouse p19 ARF can interact directly with p53, as well as with the p53 regulator mdm2. ARF can bind p53-DNA complexes, and it depends upon functional p53 to transcriptionally induce mdm2 and the cyclin-dependent kinase inhibitor p21 Cip1 , and to arrest cell proliferation. Binding of p19 ARF to p53 requires the ARF N-terminal domain (amino acids 1–62) that is necessary and sufficient to induce cell cycle arrest. Overexpression of p19 ARF in wild type or ARF -null mouse embryo fibroblasts increases the half-life of p53 from 15 to ≈75 min, correlating with an increased p53-dependent transcriptional response and growth arrest. Surprisingly, when overexpressed at supra-physiologic levels after introduction into ARF -null NIH 3T3 cells or mouse embryo fibroblasts, the p53 protein is handicapped in inducing this checkpoint response. In this setting, reintroduction of p19 ARF restores p53’s ability to induce p21 Cip1 and mdm2, implying that, in addition to stabilizing p53, ARF modulates p53-dependent function through an additional mechanism. The INK4a-ARF locus encodes two proteins, p16INK4aand p19ARF, that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53. Using insect cells infected with baculovirus vectors and NIH 3T3 fibroblasts infected with ARF retrovirus, we determined that mouse p19ARFcan interact directly with p53, as well as with the p53 regulator mdm2. ARF can bind p53-DNA complexes, and it depends upon functional p53 to transcriptionally induce mdm2 and the cyclin-dependent kinase inhibitor p21Cip1, and to arrest cell proliferation. Binding of p19ARFto p53 requires the ARF N-terminal domain (amino acids 1-62) that is necessary and sufficient to induce cell cycle arrest. Overexpression of p19ARFin wild type or ARF-null mouse embryo fibroblasts increases the half-life of p53 from 15 to ≈ 75 min, correlating with an increased p53-dependent transcriptional response and growth arrest. Surprisingly, when overexpressed at supra-physiologic levels after introduction into ARF-null NIH 3T3 cells or mouse embryo fibroblasts, the p53 protein is handicapped in inducing this checkpoint response. In this setting, reintroduction of p19ARFrestores p53's ability to induce p21Cip1and mdm2, implying that, in addition to stabilizing p53, ARF modulates p53-dependent function through an additional mechanism. The INK4a-ARF locus encodes two proteins, p16INK4a and p19ARF, that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53. The INK4a-ARF locus encodes two proteins, p16 super(INK4a) and p19 super(ARF), that restrain cell growth by affecting the functions of the retinoblastoma protein and p53, respectively. Disruption of this locus by deletions or point mutations is a common event in human cancer, perhaps second only to the loss of p53. Using insect cells infected with baculovirus vectors and NIH 3T3 fibroblasts infected with ARF retrovirus, we determined that mouse p19 super(ARF) can interact directly with p53, as well as with the p53 regulator mdm2. ARF can bind p53-DNA complexes, and it depends upon functional p53 to transcriptionally induce mdm2 and the cyclin-dependent kinase inhibitor p21 super(Cip1), and to arrest cell proliferation. Binding of p19 super(ARF) to p53 requires the ARF N-terminal domain (amino acids 1-62) that is necessary and sufficient to induce cell cycle arrest. Overexpression of p19 super(ARF) in wild type or ARF-null mouse embryo fibroblasts increases the half-life of p53 from 15 to ~75 min, correlating with an increased p53-dependent transcriptional response and growth arrest. Surprisingly, when overexpressed at supra-physiologic levels after introduction into ARF-null NIH 3T3 cells or mouse embryo fibroblasts, the p53 protein is handicapped in inducing this checkpoint response. In this setting, reintroduction of p19 super(ARF) restores p53's ability to induce p21 super(Cip1) and mdm2, implying that, in addition to stabilizing p53, ARF modulates p53- dependent function through an additional mechanism. |
| Author | Weber, Jason D. Zindy, Frederique Kamijo, Takehiko Zambetti, Gerard Roussel, Martine F. Sherr, Charles J. |
| AuthorAffiliation | Howard Hughes Medical Institute and Departments of † Tumor Cell Biology and § Biochemistry, St. Jude Children’s Research Hospital, 332 North Lauderdale, Memphis, TN 38105 |
| AuthorAffiliation_xml | – name: Howard Hughes Medical Institute and Departments of † Tumor Cell Biology and § Biochemistry, St. Jude Children’s Research Hospital, 332 North Lauderdale, Memphis, TN 38105 |
| Author_xml | – sequence: 1 givenname: Takehiko surname: Kamijo fullname: Kamijo, Takehiko – sequence: 2 givenname: Jason D. surname: Weber fullname: Weber, Jason D. – sequence: 3 givenname: Gerard surname: Zambetti fullname: Zambetti, Gerard – sequence: 4 givenname: Frederique surname: Zindy fullname: Zindy, Frederique – sequence: 5 givenname: Martine F. surname: Roussel fullname: Roussel, Martine F. – sequence: 6 givenname: Charles J. surname: Sherr fullname: Sherr, Charles J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/9653180$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright 1993-1998 National Academy of Sciences Copyright National Academy of Sciences Jul 7, 1998 Copyright © 1998, The National Academy of Sciences 1998 |
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| DOI | 10.1073/pnas.95.14.8292 |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 ObjectType-Article-1 ObjectType-Feature-2 Contributed by Charles J. Sherr T.K. and J.D.W. contributed equally to this work. To whom reprint requests should be addressed. e-mail: sherr@stjude.org. |
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| Snippet | The INK4a-ARF locus encodes two proteins, p16INK4aand p19ARF, that restrain cell growth by affecting the functions of the retinoblastoma protein and p53,... The INK4a-ARF locus encodes two proteins, p16 INK4a and p19 ARF , that restrain cell growth by affecting the functions of the retinoblastoma protein and p53,... The INK4a-ARF locus encodes two proteins, p16(INK4a) and p19(ARF), that restrain cell growth by affecting the functions of the retinoblastoma protein and p53,... The INK4a-ARF locus encodes two proteins, p16 INK4a and p19 ARF , that restrain cell growth by affecting the functions of the retinoblastoma protein and p53,... The INK4a-ARF locus encodes two proteins, p16INK4a and p19ARF, that restrain cell growth by affecting the functions of the retinoblastoma protein and p53,... The INK4a-ARF locus encodes two proteins, p16 super(INK4a) and p19 super(ARF), that restrain cell growth by affecting the functions of the retinoblastoma... |
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| SubjectTerms | 3T3 Cells Animals Antibodies Biological Sciences Cancer Cell growth Deoxyribonucleic acid DNA Gene Expression Regulation, Neoplastic Genes Genes, Tumor Suppressor Humans Infections Mice Mutation Neoplasm Proteins - genetics Neoplasm Proteins - metabolism NIH 3T3 cells Nuclear Proteins Plasmids Proteins Proteins - genetics Proteins - metabolism Proto-Oncogene Proteins - genetics Proto-Oncogene Proteins - metabolism Proto-Oncogene Proteins c-mdm2 Retroviridae Transfection Tumor Suppressor Protein p14ARF Tumor Suppressor Protein p53 - genetics Tumor Suppressor Protein p53 - metabolism Tumors Viruses |
| Title | Functional and Physical Interactions of the ARF Tumor Suppressor with p53 and Mdm2 |
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