Limited Role of Murine ATM in Oncogene-Induced Senescence and p53-Dependent Tumor Suppression
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{"title"=>"Limited role of murine ATM in oncogene-induced senescence and p53-dependent tumor suppression", "type"=>"journal", "authors"=>[{"first_name"=>"Alejo", "last_name"=>"Efeyan", "scopus_author_id"=>"8699306200"}, {"first_name"=>"Matilde", "last_name"=>"Murga", "scopus_author_id"=>"6603951800"}, {"first_name"=>"Barbara", "last_name"=>"Martinez-Pastor", "scopus_author_id"=>"12647788400"}, {"first_name"=>"Ana", "last_name"=>"Ortega-Molina", "scopus_author_id"=>"18234075900"}, {"first_name"=>"Rebeca", "last_name"=>"Soria", "scopus_author_id"=>"22036254800"}, {"first_name"=>"Manuel", "last_name"=>"Collado", "scopus_author_id"=>"7004837907"}, {"first_name"=>"Oscar", "last_name"=>"Fernandez-Capetillo", "scopus_author_id"=>"57188738961"}, {"first_name"=>"Manuel", "last_name"=>"Serrano", "scopus_author_id"=>"7201394101"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"354579450", "sgr"=>"65549105965", "pmid"=>"19421407", "scopus"=>"2-s2.0-65549105965", "isbn"=>"2003002731", "doi"=>"10.1371/journal.pone.0005475", "issn"=>"19326203"}, "id"=>"d72d11ed-451e-3197-a495-8578781fe458", "abstract"=>"Recent studies in human fibroblasts have provided a new general paradigm of tumor suppression according to which oncogenic signaling produces DNA damage and this, in turn, results in ATM/p53-dependent cellular senescence. Here, we have tested this model in a variety of murine experimental systems. Overexpression of oncogenic Ras in murine fibroblasts efficiently induced senescence but this occurred in the absence of detectable DNA damage signaling, thus suggesting a fundamental difference between human and murine cells. Moreover, lung adenomas initiated by endogenous levels of oncogenic K-Ras presented abundant senescent cells, but undetectable DNA damage signaling. Accordingly, K-Ras-driven adenomas were also senescent in Atm-null mice, and the tumorigenic progression of these lesions was only modestly accelerated by Atm-deficiency. Finally, we have examined chemically-induced fibrosarcomas, which possess a persistently activated DNA damage response and are highly sensitive to the activity of p53. We found that the absence of Atm favored genomic instability in the resulting tumors, but did not affect the persistent DNA damage response and did not impair p53-dependent tumor suppression. All together, we conclude that oncogene-induced senescence in mice may occur in the absence of a detectable DNA damage response. Regarding murine Atm, our data suggest that it plays a minor role in oncogene-induced senescence or in p53-dependent tumor suppression, being its tumor suppressive activity probably limited to the maintenance of genomic stability.", "link"=>"http://www.mendeley.com/research/limited-role-murine-atm-oncogeneinduced-senescence-p53dependent-tumor-suppression", "reader_count"=>63, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>5, "Researcher"=>17, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>1, "Student > Master"=>8, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>5, "Researcher"=>17, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>1, "Student > Master"=>8, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>2, "Biochemistry, Genetics and Molecular Biology"=>13, "Agricultural and Biological Sciences"=>36, "Medicine and Dentistry"=>4, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>36}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Iran"=>1, "Japan"=>1, "France"=>1, "Germany"=>1, "Spain"=>2}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/898672"], "description"=>"<p>A. Mice of the indicated genotypes, wt (n = 15), <i>p53</i>-super (n = 16), <i>Atm</i>-null (n = 9), <i>p53</i>-super/<i>Atm</i>-null (n = 13) and <i>Arf</i>-null (n = 12), were injected intramuscularly with 3-methyl-cholanthrene (3MC) and tumour development was monitored. Kaplan-Meier tumour-free curves were obtained and statistical significant differences (logrank test) were found for wt vs. <i>p53</i>-super (<i>p</i><0.005), <i>Atm</i>-null vs. <i>p53</i>-super/<i>Atm</i>-null (<i>p</i><0.001) and <i>Arf</i>-null vs. wt (<i>p</i><0.0001). No significant differences were found for wt vs. <i>Atm</i>-null (<i>p</i> = 0.11), or <i>p53</i>-super vs. <i>p53</i>-super/<i>Atm</i>-null (<i>p</i> = 0.18). B. Quantification of the persistent DNA damage response (γH2AX), proliferation (Ki67), and apoptosis (activated caspase-3) in 3MC-fibrosarcomas generated in mice of the indicated genotypes. Quantifications are relative to the 3MC-fibrosarcomas in wild-type mice. Values correspond to the average and standard deviation (n = 5 per genotype). Examples of the immunostainings are shown in the panels at the right.</p>", "links"=>[], "tags"=>["atm", "p53-mediated", "suppression", "dna", "chemically-induced"], "article_id"=>569126, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005475.g004", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Limited_role_of_Atm_in_p53_mediated_tumor_suppression_and_DNA_damage_response_in_chemically_induced_fibrosarcomas_/569126", "title"=>"Limited role of Atm in p53-mediated tumor suppression and DNA damage response in chemically-induced fibrosarcomas.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-07 02:32:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/898334"], "description"=>"<p>A. Immunoblots illustrating the phosphorylation status of Atm, Chk1 and H2AX under different conditions: infection of early passage primary MEFs with an empty vector or with H-<i>Ras</i>V12 expressing retrovirus (analyzed 6 days post-selection when cells were morphologically senescent), activation of an endogenous K-<i>Ras</i>V12 allele with 4-hydroxy-tamoxifen (OHT), and finally controls of DNA damage by replicative stress using hydroxyurea (HU 1 mM, 3 hrs) and by DNA breaks using ionizing radiation (IR 3 Gy, 45 min). B. Quantitative immunofluorescence of γH2AX in single cells from the same populations analysed in part A using high-throughput microscopy. The average intensity of the population is indicated with a bar. Note that upon replicative stress (HU) only the fraction of cells in S-phase activate the DDR, while upon irradiation (IR) the entire population activates the DDR. C. Immunoblots of the indicated proteins 6 days after selection of cells retrovirally transduced with H-<i>Ras</i>V12.</p>", "links"=>[], "tags"=>["dna", "signaling", "atm", "ras-induced", "senescence", "murine"], "article_id"=>568785, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005475.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lack_of_evidence_for_DNA_damage_signaling_and_limited_role_of_Atm_in_Ras_induced_senescence_in_murine_fibroblasts_/568785", "title"=>"Lack of evidence for DNA damage signaling and limited role of Atm in Ras-induced senescence in murine fibroblasts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-07 02:26:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/898920"], "description"=>"a<p>The functional status of p53 in the fibrosarcoma cell lines was determined by examining the levels of p53 and p21 upon γIR, both by immunohistochemistry (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone-0005475-g005\" target=\"_blank\">Fig. 5A</a>) and immunoblotting (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone-0005475-g005\" target=\"_blank\">Fig. 5B</a>), as well as, by their susceptibility to cell cycle arrest upon treatment with nutlin (Supplementary <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone.0005475.s005\" target=\"_blank\">Fig. S5</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone.0005475.s006\" target=\"_blank\">S6</a>).</p>b<p>These <i>Atm</i>-null lines with functional p53 correspond to a minority of the 3MC-fibrosarcomas produced in <i>Atm</i>-null mice, which by large have mutant p53 (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone-0005475-t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone-0005475-g005\" target=\"_blank\">Fig. 5B</a>). Only two lines were obtained that retained functional p53 (Supplementary <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone.0005475.s006\" target=\"_blank\">Fig. S6</a>): one derived from an <i>Atm</i>-null;<i>p53</i>-super mouse and the other one from an <i>Atm</i>-null;<i>p53</i>-wt mouse.</p>c<p>Aneuploidies correspond to metaphasases with chromosome numbers different from 40±1 or 80±2.</p>d<p>Statistical comparison (t-test) between <i>Atm</i>-null(p53-functional) and <i>Arf</i>-null(p53-functional): metaphases with fusions, <i>p</i> = 0.04; aneuploid cell lines, <i>p</i> = 0.06.</p>", "links"=>[], "tags"=>["instability", "3mc-fibrosarcoma"], "article_id"=>569373, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005475.t002", "stats"=>{"downloads"=>3, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chromosomal_instability_in_3MC_fibrosarcoma_cell_lines_/569373", "title"=>"Chromosomal instability in 3MC-fibrosarcoma cell lines.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-05-07 02:36:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/898537"], "description"=>"<p>A. Representative stainings of senescence-associated β−galactosidase (SAβGal) in lung cryosections from K-<i>Ras</i>V12/Atm-wt and K-<i>Ras</i>V12/Atm-null mice. The grade of the tumor (G2 or G3) is indicated. See Supplementary <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone.0005475.s003\" target=\"_blank\">Fig. S3</a> for panoramic views, including adenocarcinomas (G4, which are negative for SAβGal). B. Examples of Ki67 stainings of lung adenomas from the indicated mouse genotypes and quantification (adenomas n = 4 for each genotype). Values correspond to the average and standard deviation. C. Lack of detectable γH2AX staining in K-<i>Ras</i>V12-driven lung adenomas. The bottom panel shows a positive control of the lung from an irradiated wildt-type mouse (5 Gy, 45 min post-IR). D. Expression of Arf during K-<i>Ras</i>V12-driven lung tumorigenesis is specifically associated to the pre-malignant stages (adenomas, top), but not to the malignant ones (adenocarcinomas, bottom). Note that some cells in the adenoma are Arf-positive and others are Arf-negative, consistent with the concept that not all the tumor cells of these lesions are senescent, and indeed a fraction of cells are proliferating, as shown in part B.</p>", "links"=>[], "tags"=>["dna", "signaling", "atm", "senescent", "murine"], "article_id"=>568988, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005475.g003", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lack_of_evidence_for_DNA_damage_signaling_and_limited_role_of_Atm_in_senescent_murine_lung_tumors_/568988", "title"=>"Lack of evidence for DNA damage signaling and limited role of Atm in senescent murine lung tumors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-07 02:29:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/898432"], "description"=>"<p>A. Kaplan-Meier survival curves of the indicated mice (n = 15 mice for each group). The inducible K-<i>Ras</i>V12 allele was activated with OHT when the mice were 1 month old. B. Quantification of the different grades of lesions found in the lungs of K-<i>Ras</i>V12/Atm-wt and K-<i>Ras</i>V12/Atm-null mice (15 mice per group, and a total of n = 121 and n = 108 lesions, respectively). Asterisks indicate statistical significance of the Fisher's test <i>p</i><0.05.</p>", "links"=>[], "tags"=>["atm", "ras-driven", "murine"], "article_id"=>568882, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005475.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Limited_role_of_Atm_in_Ras_driven_murine_lung_tumorigenesis_/568882", "title"=>"Limited role of Atm in Ras-driven murine lung tumorigenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-07 02:28:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/444999", "https://ndownloader.figshare.com/files/445033", "https://ndownloader.figshare.com/files/445058", "https://ndownloader.figshare.com/files/445093", "https://ndownloader.figshare.com/files/445114", "https://ndownloader.figshare.com/files/445140"], "description"=>"<div><p>Recent studies in human fibroblasts have provided a new general paradigm of tumor suppression according to which oncogenic signaling produces DNA damage and this, in turn, results in ATM/p53-dependent cellular senescence. Here, we have tested this model in a variety of murine experimental systems. Overexpression of oncogenic Ras in murine fibroblasts efficiently induced senescence but this occurred in the absence of detectable DNA damage signaling, thus suggesting a fundamental difference between human and murine cells. Moreover, lung adenomas initiated by endogenous levels of oncogenic K-Ras presented abundant senescent cells, but undetectable DNA damage signaling. Accordingly, K-Ras-driven adenomas were also senescent in <em>Atm</em>-null mice, and the tumorigenic progression of these lesions was only modestly accelerated by <em>Atm</em>-deficiency. Finally, we have examined chemically-induced fibrosarcomas, which possess a persistently activated DNA damage response and are highly sensitive to the activity of p53. We found that the absence of <em>Atm</em> favored genomic instability in the resulting tumors, but did not affect the persistent DNA damage response and did not impair p53-dependent tumor suppression. All together, we conclude that oncogene-induced senescence in mice may occur in the absence of a detectable DNA damage response. Regarding murine Atm, our data suggest that it plays a minor role in oncogene-induced senescence or in p53-dependent tumor suppression, being its tumor suppressive activity probably limited to the maintenance of genomic stability.</p></div>", "links"=>[], "tags"=>["murine", "atm", "oncogene-induced", "senescence", "p53-dependent", "suppression"], "article_id"=>147702, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0005475.s001", "https://dx.doi.org/10.1371/journal.pone.0005475.s002", "https://dx.doi.org/10.1371/journal.pone.0005475.s003", "https://dx.doi.org/10.1371/journal.pone.0005475.s004", "https://dx.doi.org/10.1371/journal.pone.0005475.s005", "https://dx.doi.org/10.1371/journal.pone.0005475.s006"], "stats"=>{"downloads"=>10, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Limited_Role_of_Murine_ATM_in_Oncogene_Induced_Senescence_and_p53_Dependent_Tumor_Suppression/147702", "title"=>"Limited Role of Murine ATM in Oncogene-Induced Senescence and p53-Dependent Tumor Suppression", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-05-07 02:08:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/898786"], "description"=>"<p>A. Representative images of 3MC-fibrosarcomas immunostained for Arf, p53 and p21 (see also <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone-0005475-t001\" target=\"_blank\">Table 1</a>). The upper and middle rows are representative of the large majority of fibrosarcomas developed in wild-type (upper) and <i>Atm</i>-null (middle) mice, which are consistent with a mutant p53 (<i>i.e.</i> strongly positive for p53 and negative for p21). The lower row is representative of the fibrosarcomas developed in <i>Arf</i>-null mice, which are consistent with a functional p53 (<i>i.e.</i> very weakly positive for p53 and positive for p21). B. Examples of cancer cell lines established from 3MC-fibrosarcomas (each line derives from an independent fibrosarcoma). The genotype of the mice where the 3MC-fibrosarcomas were generated is indicated, as well as, the status of p53 as determined by a nutlin-sensitivity assay (see Supplementary <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone.0005475.s005\" target=\"_blank\">Figures S5</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005475#pone.0005475.s006\" target=\"_blank\">S6</a>). Cell lines were exposed to 10 Gy and protein extracts were obtained 1h and 24h after irradiation. The levels of the indicated proteins were determined by immunoblotting using β-actin as loading control.</p>", "links"=>[], "tags"=>["atm", "selective", "inactivate", "p53"], "article_id"=>569234, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005475.g005", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Absence_of_Atm_does_not_relieve_the_selective_pressure_to_inactivate_p53_during_chemical_carcinogenesis_/569234", "title"=>"Absence of Atm does not relieve the selective pressure to inactivate p53 during chemical carcinogenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-07 02:33:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/898890"], "description"=>"a<p>Most tumors strongly positive for p53, lacked p21 expression (reflecting a non-functional mutant p53); and, tumors negative or weakly positive for p53, had detectable p21 (reflecting a functional p53)</p>b<p>The few tumors that lacked Arf were negative or weakly positive for p53 (reflecting a functional p53)</p>", "links"=>[], "tags"=>["cell biology/cellular death and stress responses", "genetics and genomics/cancer genetics", "molecular biology/dna repair"], "article_id"=>569343, "categories"=>["Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Alejo Efeyan", "Matilde Murga", "Barbara Martinez-Pastor", "Ana Ortega-Molina", "Rebeca Soria", "Manuel Collado", "Oscar Fernandez-Capetillo", "Manuel Serrano"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005475.t001", "stats"=>{"downloads"=>4, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunohistochemical_analysis_of_3MC_fibrosarcomas_/569343", "title"=>"Immunohistochemical analysis of 3MC-fibrosarcomas.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-05-07 02:35:43"}

PMC Usage Stats | Further Information

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Relative Metric

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