Myc Supports Self-Renewal of Basal Cells in the Esophageal Epithelium
It is widely believed that cellular senescence plays a critical role in both aging and cancer, and that senescence is a fundamental, permanent growth arrest that somatic cells cannot avoid. Here we show that Myc plays an important role in self-renewal of esophageal epithelial cells, contributing to...
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| Published in | Frontiers in cell and developmental biology Vol. 10; p. 786031 |
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| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Frontiers Media S.A
04.03.2022
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| Abstract | It is widely believed that cellular senescence plays a critical role in both aging and cancer, and that senescence is a fundamental, permanent growth arrest that somatic cells cannot avoid. Here we show that Myc plays an important role in self-renewal of esophageal epithelial cells, contributing to their resistance to cellular senescence. Myc is homogeneously expressed in basal cells of the esophageal epithelium and Myc positively regulates their self-renewal by maintaining their undifferentiated state. Indeed, Myc knockout induced a loss of the undifferentiated state of esophageal epithelial cells resulting in cellular senescence while forced MYC expression promoted oncogenic cell proliferation. A superoxide scavenger counteracted Myc knockout-induced senescence, therefore suggesting that a mitochondrial superoxide takes part in inducing senescence. Taken together, these analyses reveal extremely low levels of cellular senescence and senescence-associated phenotypes in the esophageal epithelium, as well as a critical role for Myc in self-renewal of basal cells in this organ. This provides new avenues for studying and understanding the links between stemness and resistance to cellular senescence. |
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| AbstractList | It is widely believed that cellular senescence plays a critical role in both aging and cancer, and that senescence is a fundamental, permanent growth arrest that somatic cells cannot avoid. Here we show that Myc plays an important role in self-renewal of esophageal epithelial cells, contributing to their resistance to cellular senescence. Myc is homogeneously expressed in basal cells of the esophageal epithelium and Myc positively regulates their self-renewal by maintaining their undifferentiated state. Indeed, Myc knockout induced a loss of the undifferentiated state of esophageal epithelial cells resulting in cellular senescence while forced MYC expression promoted oncogenic cell proliferation. A superoxide scavenger counteracted Myc knockout-induced senescence, therefore suggesting that a mitochondrial superoxide takes part in inducing senescence. Taken together, these analyses reveal extremely low levels of cellular senescence and senescence-associated phenotypes in the esophageal epithelium, as well as a critical role for Myc in self-renewal of basal cells in this organ. This provides new avenues for studying and understanding the links between stemness and resistance to cellular senescence.It is widely believed that cellular senescence plays a critical role in both aging and cancer, and that senescence is a fundamental, permanent growth arrest that somatic cells cannot avoid. Here we show that Myc plays an important role in self-renewal of esophageal epithelial cells, contributing to their resistance to cellular senescence. Myc is homogeneously expressed in basal cells of the esophageal epithelium and Myc positively regulates their self-renewal by maintaining their undifferentiated state. Indeed, Myc knockout induced a loss of the undifferentiated state of esophageal epithelial cells resulting in cellular senescence while forced MYC expression promoted oncogenic cell proliferation. A superoxide scavenger counteracted Myc knockout-induced senescence, therefore suggesting that a mitochondrial superoxide takes part in inducing senescence. Taken together, these analyses reveal extremely low levels of cellular senescence and senescence-associated phenotypes in the esophageal epithelium, as well as a critical role for Myc in self-renewal of basal cells in this organ. This provides new avenues for studying and understanding the links between stemness and resistance to cellular senescence. It is widely believed that cellular senescence plays a critical role in both aging and cancer, and that senescence is a fundamental, permanent growth arrest that somatic cells cannot avoid. Here we show that Myc plays an important role in self-renewal of esophageal epithelial cells, contributing to their resistance to cellular senescence. Myc is homogeneously expressed in basal cells of the esophageal epithelium and Myc positively regulates their self-renewal by maintaining their undifferentiated state. Indeed, Myc knockout induced a loss of the undifferentiated state of esophageal epithelial cells resulting in cellular senescence while forced MYC expression promoted oncogenic cell proliferation. A superoxide scavenger counteracted Myc knockout-induced senescence, therefore suggesting that a mitochondrial superoxide takes part in inducing senescence. Taken together, these analyses reveal extremely low levels of cellular senescence and senescence-associated phenotypes in the esophageal epithelium, as well as a critical role for Myc in self-renewal of basal cells in this organ. This provides new avenues for studying and understanding the links between stemness and resistance to cellular senescence. |
| Author | Rodriguez Esteban, Concepcion Castells, Antoni Yoshida, Kei Nuñez Delicado, Estrella Izpisua Belmonte, Juan Carlos Prieto, Javier Hishida, Tomoaki Reddy, Pradeep O’Keefe, David D. Kato, Ryuji Hishida-Nozaki, Yuriko Takahashi, Yuta Nakagawa, Hiroshi Vazquez-Ferrer, Eric Sahu, Sanjeeb Kumar Takemoto, Yuto Hatanaka, Fumiyuki Knoepfler, Paul S. Campistol, Josep M. |
| AuthorAffiliation | 4 Department of Cell Biology and Human Anatomy , University of California, Davis , Davis , CA , United States 1 Gene Expression Laboratory , Salk Institute for Biological Studies , La Jolla , CA , United States 5 Universidad Católica San Antonio de Murcia (UCAM) , Campus de los Jerónimos , Murcia , Spain 2 Laboratory of Biological Chemistry , School of Pharmaceutical Sciences , Wakayama Medical University , Wakayama , Japan 3 Department of Basic Medical Sciences , Graduate School of Pharmaceutical Sciences , Nagoya University , Nagoya , Japan 6 Gastroenterology Department , Hospital Clinic , CIBEREHD , IDIBAPS , University of Barcelona , Barcelona , Spain 8 Abramson Cancer Center , University of Pennsylvania , Philadelphia , PA , United States 7 Division of Gastroenterology , Department of Medicine , Perelman School of Medicine , Philadelphia , PA , United States |
| AuthorAffiliation_xml | – name: 5 Universidad Católica San Antonio de Murcia (UCAM) , Campus de los Jerónimos , Murcia , Spain – name: 6 Gastroenterology Department , Hospital Clinic , CIBEREHD , IDIBAPS , University of Barcelona , Barcelona , Spain – name: 2 Laboratory of Biological Chemistry , School of Pharmaceutical Sciences , Wakayama Medical University , Wakayama , Japan – name: 1 Gene Expression Laboratory , Salk Institute for Biological Studies , La Jolla , CA , United States – name: 7 Division of Gastroenterology , Department of Medicine , Perelman School of Medicine , Philadelphia , PA , United States – name: 3 Department of Basic Medical Sciences , Graduate School of Pharmaceutical Sciences , Nagoya University , Nagoya , Japan – name: 4 Department of Cell Biology and Human Anatomy , University of California, Davis , Davis , CA , United States – name: 8 Abramson Cancer Center , University of Pennsylvania , Philadelphia , PA , United States |
| Author_xml | – sequence: 1 givenname: Tomoaki surname: Hishida fullname: Hishida, Tomoaki – sequence: 2 givenname: Eric surname: Vazquez-Ferrer fullname: Vazquez-Ferrer, Eric – sequence: 3 givenname: Yuriko surname: Hishida-Nozaki fullname: Hishida-Nozaki, Yuriko – sequence: 4 givenname: Yuto surname: Takemoto fullname: Takemoto, Yuto – sequence: 5 givenname: Fumiyuki surname: Hatanaka fullname: Hatanaka, Fumiyuki – sequence: 6 givenname: Kei surname: Yoshida fullname: Yoshida, Kei – sequence: 7 givenname: Javier surname: Prieto fullname: Prieto, Javier – sequence: 8 givenname: Sanjeeb Kumar surname: Sahu fullname: Sahu, Sanjeeb Kumar – sequence: 9 givenname: Yuta surname: Takahashi fullname: Takahashi, Yuta – sequence: 10 givenname: Pradeep surname: Reddy fullname: Reddy, Pradeep – sequence: 11 givenname: David D. surname: O’Keefe fullname: O’Keefe, David D. – sequence: 12 givenname: Concepcion surname: Rodriguez Esteban fullname: Rodriguez Esteban, Concepcion – sequence: 13 givenname: Paul S. surname: Knoepfler fullname: Knoepfler, Paul S. – sequence: 14 givenname: Estrella surname: Nuñez Delicado fullname: Nuñez Delicado, Estrella – sequence: 15 givenname: Antoni surname: Castells fullname: Castells, Antoni – sequence: 16 givenname: Josep M. surname: Campistol fullname: Campistol, Josep M. – sequence: 17 givenname: Ryuji surname: Kato fullname: Kato, Ryuji – sequence: 18 givenname: Hiroshi surname: Nakagawa fullname: Nakagawa, Hiroshi – sequence: 19 givenname: Juan Carlos surname: Izpisua Belmonte fullname: Izpisua Belmonte, Juan Carlos |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35309931$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_3389_fcell_2024_1357589 crossref_primary_10_3390_pathophysiology30030027 |
| Cites_doi | 10.1016/j.stem.2010.06.023 10.1016/j.diff.2010.05.001 10.1073/pnas.0701953104 10.1038/nprot.2009.191 10.1126/science.1056782 10.1002/stem.1384 10.1126/scitranslmed.3002847 10.1007/s13238-019-0630-3 10.1126/science.1260419 10.1126/science.1112125 10.1111/j.1474-9726.2007.00318.x 10.1126/science.aau3879 10.1182/blood.v97.1.324 10.1158/2159-8290.CD-21-1059 10.1002/ijc.31873 10.1101/sqb.1991.056.01.015 10.1016/j.celrep.2014.09.027 10.1016/j.stem.2011.04.020 10.1038/sj.onc.1207923 10.1016/j.tibs.2016.01.005 10.1016/j.cell.2013.05.039 10.1007/s11357-999-0011-6 10.1126/scisignal.2004088 10.1016/j.stem.2016.05.012 10.1093/nar/gni051 10.1038/ncomms5226 10.1042/BJ20070797 10.1002/eji.200737972 10.1016/j.stem.2013.01.007 10.1172/JCI35012 10.1101/gad.1971610 10.1038/sj.onc.1203630 10.1158/0008-5472.CAN-13-3234 10.1158/2159-8290.CD-12-0095 10.1038/s41586-018-0811-x 10.1101/gad.192294.112 10.1016/s1097-2765(00)80367-6 10.1016/j.stem.2011.09.001 |
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| Copyright | Copyright © 2022 Hishida, Vazquez-Ferrer, Hishida-Nozaki, Takemoto, Hatanaka, Yoshida, Prieto, Sahu, Takahashi, Reddy, O’Keefe, Rodriguez Esteban, Knoepfler, Nuñez Delicado, Castells, Campistol, Kato, Nakagawa and Izpisua Belmonte. Copyright © 2022 Hishida, Vazquez-Ferrer, Hishida-Nozaki, Takemoto, Hatanaka, Yoshida, Prieto, Sahu, Takahashi, Reddy, O’Keefe, Rodriguez Esteban, Knoepfler, Nuñez Delicado, Castells, Campistol, Kato, Nakagawa and Izpisua Belmonte. 2022 Hishida, Vazquez-Ferrer, Hishida-Nozaki, Takemoto, Hatanaka, Yoshida, Prieto, Sahu, Takahashi, Reddy, O’Keefe, Rodriguez Esteban, Knoepfler, Nuñez Delicado, Castells, Campistol, Kato, Nakagawa and Izpisua Belmonte |
| Copyright_xml | – notice: Copyright © 2022 Hishida, Vazquez-Ferrer, Hishida-Nozaki, Takemoto, Hatanaka, Yoshida, Prieto, Sahu, Takahashi, Reddy, O’Keefe, Rodriguez Esteban, Knoepfler, Nuñez Delicado, Castells, Campistol, Kato, Nakagawa and Izpisua Belmonte. – notice: Copyright © 2022 Hishida, Vazquez-Ferrer, Hishida-Nozaki, Takemoto, Hatanaka, Yoshida, Prieto, Sahu, Takahashi, Reddy, O’Keefe, Rodriguez Esteban, Knoepfler, Nuñez Delicado, Castells, Campistol, Kato, Nakagawa and Izpisua Belmonte. 2022 Hishida, Vazquez-Ferrer, Hishida-Nozaki, Takemoto, Hatanaka, Yoshida, Prieto, Sahu, Takahashi, Reddy, O’Keefe, Rodriguez Esteban, Knoepfler, Nuñez Delicado, Castells, Campistol, Kato, Nakagawa and Izpisua Belmonte |
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| Keywords | senescence cancer aging MYC mitochondria highlights |
| Language | English |
| License | Copyright © 2022 Hishida, Vazquez-Ferrer, Hishida-Nozaki, Takemoto, Hatanaka, Yoshida, Prieto, Sahu, Takahashi, Reddy, O’Keefe, Rodriguez Esteban, Knoepfler, Nuñez Delicado, Castells, Campistol, Kato, Nakagawa and Izpisua Belmonte. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Viacheslav Senichkin, Lomonosov Moscow State University, Russia Demitrios Vynios, University of Patras, Greece Edited by: Gelina Kopeina, Lomonosov Moscow State University, Russia Takafumi Suzuki, Tohoku University, Japan Present Address: Sanjeeb Kumar Sahu, Altos Labs, San Diego, CA Juan Carlos Izpisua Belmonte, Altos Labs, San Diego, CA This article was submitted to Molecular and Cellular Oncology, a section of the journal Frontiers in Cell and Developmental Biology |
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| SubjectTerms | aging cancer Cell and Developmental Biology mitochondria highlights MYC senescence |
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| Title | Myc Supports Self-Renewal of Basal Cells in the Esophageal Epithelium |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/35309931 https://www.proquest.com/docview/2641504342 https://pubmed.ncbi.nlm.nih.gov/PMC8931341 https://doaj.org/article/31205045cd044c04b4a97467e784b2c0 |
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