p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells

<p dir="ltr">The restoration of p53 has been suggested as a therapeutic approach in tumors. However, the timing of p53 restoration in relation to its efficacy during tumor progression still is unclear. We now show that the restoration of p53 in murine premalignant proliferating pinea...

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Main Author: Mohamad Harajly (18810850) (author)
Other Authors: Hasan Zalzali (18810853) (author), Zafar Nawaz (96166) (author), Sandra E. Ghayad (7353428) (author), Farah Ghamloush (9449144) (author), Hussein Basma (18810856) (author), Samiha Zainedin (18810859) (author), Wissam Rabeh (18810862) (author), Mark Jabbour (631068) (author), Ayman Tawil (6442628) (author), Danielle A. Badro (9155014) (author), Gerard I. Evan (13984602) (author), Raya Saab (7353425) (author)
Published: 2023
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author Mohamad Harajly (18810850)
author2 Hasan Zalzali (18810853)
Zafar Nawaz (96166)
Sandra E. Ghayad (7353428)
Farah Ghamloush (9449144)
Hussein Basma (18810856)
Samiha Zainedin (18810859)
Wissam Rabeh (18810862)
Mark Jabbour (631068)
Ayman Tawil (6442628)
Danielle A. Badro (9155014)
Gerard I. Evan (13984602)
Raya Saab (7353425)
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author_facet Mohamad Harajly (18810850)
Hasan Zalzali (18810853)
Zafar Nawaz (96166)
Sandra E. Ghayad (7353428)
Farah Ghamloush (9449144)
Hussein Basma (18810856)
Samiha Zainedin (18810859)
Wissam Rabeh (18810862)
Mark Jabbour (631068)
Ayman Tawil (6442628)
Danielle A. Badro (9155014)
Gerard I. Evan (13984602)
Raya Saab (7353425)
author_role author
dc.creator.none.fl_str_mv Mohamad Harajly (18810850)
Hasan Zalzali (18810853)
Zafar Nawaz (96166)
Sandra E. Ghayad (7353428)
Farah Ghamloush (9449144)
Hussein Basma (18810856)
Samiha Zainedin (18810859)
Wissam Rabeh (18810862)
Mark Jabbour (631068)
Ayman Tawil (6442628)
Danielle A. Badro (9155014)
Gerard I. Evan (13984602)
Raya Saab (7353425)
dc.date.none.fl_str_mv 2023-03-17T06:00:00Z
dc.identifier.none.fl_str_mv 10.1128/mcb.00747-15
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/p53_Restoration_in_Induction_and_Maintenance_of_Senescence_Differential_Effects_in_Premalignant_and_Malignant_Tumor_Cells/26021512
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Oncology and carcinogenesis
Tumor suppression
Tumor progression
Premalignant tumors
Invasive tumors
Tumor reentry
Neuroectodermal tumors
DNA-damaging therapy
dc.title.none.fl_str_mv p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <p dir="ltr">The restoration of p53 has been suggested as a therapeutic approach in tumors. However, the timing of p53 restoration in relation to its efficacy during tumor progression still is unclear. We now show that the restoration of p53 in murine premalignant proliferating pineal lesions resulted in cellular senescence, while p53 restoration in invasive pineal tumors did not. The effectiveness of p53 restoration was not dependent on p19Arf expression but showed an inverse correlation with Mdm2 expression. In tumor cells, p53 restoration became effective when paired with either DNA-damaging therapy or with nutlin, an inhibitor of p53-Mdm2 interaction. Interestingly, the inactivation of p53 after senescence resulted in reentry into the cell cycle and rapid tumor progression. The evaluation of a panel of human supratentorial primitive neuroectodermal tumors (sPNET) showed low activity of the p53 pathway. Together, these data suggest that the restoration of the p53 pathway has different effects in premalignant versus invasive pineal tumors, and that p53 activation needs to be continually sustained, as reversion from senescence occurs rapidly with aggressive tumor growth when p53 is lost again. Finally, p53 restoration approaches may be worth exploring in sPNET, where the p53 gene is intact but the pathway is inactive in the majority of examined tumors.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular and Cellular Biology<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1128/mcb.00747-15" target="_blank">https://dx.doi.org/10.1128/mcb.00747-15</a></p>
eu_rights_str_mv openAccess
id Manara2_8a3a02703f2e1c54746899f80f00a901
identifier_str_mv 10.1128/mcb.00747-15
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/26021512
publishDate 2023
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rights_invalid_str_mv CC BY 4.0
spelling p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor CellsMohamad Harajly (18810850)Hasan Zalzali (18810853)Zafar Nawaz (96166)Sandra E. Ghayad (7353428)Farah Ghamloush (9449144)Hussein Basma (18810856)Samiha Zainedin (18810859)Wissam Rabeh (18810862)Mark Jabbour (631068)Ayman Tawil (6442628)Danielle A. Badro (9155014)Gerard I. Evan (13984602)Raya Saab (7353425)Biological sciencesBiochemistry and cell biologyBiomedical and clinical sciencesOncology and carcinogenesisTumor suppressionTumor progressionPremalignant tumorsInvasive tumorsTumor reentryNeuroectodermal tumorsDNA-damaging therapy<p dir="ltr">The restoration of p53 has been suggested as a therapeutic approach in tumors. However, the timing of p53 restoration in relation to its efficacy during tumor progression still is unclear. We now show that the restoration of p53 in murine premalignant proliferating pineal lesions resulted in cellular senescence, while p53 restoration in invasive pineal tumors did not. The effectiveness of p53 restoration was not dependent on p19Arf expression but showed an inverse correlation with Mdm2 expression. In tumor cells, p53 restoration became effective when paired with either DNA-damaging therapy or with nutlin, an inhibitor of p53-Mdm2 interaction. Interestingly, the inactivation of p53 after senescence resulted in reentry into the cell cycle and rapid tumor progression. The evaluation of a panel of human supratentorial primitive neuroectodermal tumors (sPNET) showed low activity of the p53 pathway. Together, these data suggest that the restoration of the p53 pathway has different effects in premalignant versus invasive pineal tumors, and that p53 activation needs to be continually sustained, as reversion from senescence occurs rapidly with aggressive tumor growth when p53 is lost again. Finally, p53 restoration approaches may be worth exploring in sPNET, where the p53 gene is intact but the pathway is inactive in the majority of examined tumors.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular and Cellular Biology<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1128/mcb.00747-15" target="_blank">https://dx.doi.org/10.1128/mcb.00747-15</a></p>2023-03-17T06:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1128/mcb.00747-15https://figshare.com/articles/journal_contribution/p53_Restoration_in_Induction_and_Maintenance_of_Senescence_Differential_Effects_in_Premalignant_and_Malignant_Tumor_Cells/26021512CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/260215122023-03-17T06:00:00Z
spellingShingle p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
Mohamad Harajly (18810850)
Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Oncology and carcinogenesis
Tumor suppression
Tumor progression
Premalignant tumors
Invasive tumors
Tumor reentry
Neuroectodermal tumors
DNA-damaging therapy
status_str publishedVersion
title p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
title_full p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
title_fullStr p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
title_full_unstemmed p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
title_short p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
title_sort p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells
topic Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Oncology and carcinogenesis
Tumor suppression
Tumor progression
Premalignant tumors
Invasive tumors
Tumor reentry
Neuroectodermal tumors
DNA-damaging therapy