Autophagy and unfolded protein response (UPR) regulate mammary gland involution by restraining apoptosis-driven irreversible changes.
Identifieur interne : 000079 ( PubMed/Curation ); précédent : 000078; suivant : 000080Autophagy and unfolded protein response (UPR) regulate mammary gland involution by restraining apoptosis-driven irreversible changes.
Auteurs : Anni W Rri [États-Unis] ; Katherine L. Cook [États-Unis] ; Rong Hu [États-Unis] ; Lu Jin [États-Unis] ; Alan Zwart [États-Unis] ; David R. Soto-Pantoja [États-Unis] ; Jie Liu [États-Unis] ; Toren Finkel [États-Unis] ; Robert Clarke [États-Unis]Source :
- Cell death discovery [ 2058-7716 ] ; 2018.
Abstract
The postnatal mammary gland undergoes repeated cycles of proliferation and cell death, most notably when the fully differentiated (lactating) gland dedifferentiates to a prelactation state. Accumulation of milk proteins in the secretory epithelium creates the stress signal that triggers this process (involution). How this stress is perceived, and the cellular processes that are subsequently activated, remain unclear. We now report that Unfolded Protein Response (UPR), autophagy, and apoptosis related genes cluster separately during lactation and involution in the mouse mammary gland. Time-course experiments in rodents show that autophagy and UPR signaling are tightly co-regulated at the transition from reversible to irreversible involution. Inhibition of autophagy by chloroquine or genetic deletion of one ATG7 allele enhanced progression of mammary involution into the irreversible phase, as characterized by an early/precocious induction of apoptosis. These are the first preclinical in vivo data in support of a clinical trial testing an autophagy inhibitor for prevention of intraductal breast malignancy progression to invasive breast cancer. In marked contrast, stimulation of autophagy by low dose tunicamycin treatment reduced apoptosis and extended the reversible phase of involution by sustaining the secretory epithelium. Autophagy stimulators could be used short-term to promote lactation in women experiencing difficulties or irregularities in nursing. Taken together, these data indicate that UPR and autophagy play a key role in regulating the balance between cell survival and apoptosis during normal mammary gland regression.
DOI: 10.1038/s41420-018-0105-y
PubMed: 30345078
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Cook</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">District de Columbia</region></placeName><wicri:cityArea>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington</wicri:cityArea></affiliation></author><author><name sortKey="Hu, Rong" sort="Hu, Rong" uniqKey="Hu R" first="Rong" last="Hu">Rong Hu</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">District de Columbia</region></placeName><wicri:cityArea>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington</wicri:cityArea></affiliation></author><author><name sortKey="Jin, Lu" sort="Jin, Lu" uniqKey="Jin L" first="Lu" last="Jin">Lu Jin</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">District de Columbia</region></placeName><wicri:cityArea>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington</wicri:cityArea></affiliation></author><author><name sortKey="Zwart, Alan" sort="Zwart, Alan" uniqKey="Zwart A" first="Alan" last="Zwart">Alan Zwart</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">District de Columbia</region></placeName><wicri:cityArea>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington</wicri:cityArea></affiliation></author><author><name sortKey="Soto Pantoja, David R" sort="Soto Pantoja, David R" uniqKey="Soto Pantoja D" first="David R" last="Soto-Pantoja">David R. Soto-Pantoja</name><affiliation wicri:level="2"><nlm:affiliation>3Department of Surgery and Comprehensive Cancer Center, Wake Forest University, Winston Salem, NC 27157 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>3Department of Surgery and Comprehensive Cancer Center, Wake Forest University, Winston Salem</wicri:cityArea></affiliation></author><author><name sortKey="Liu, Jie" sort="Liu, Jie" uniqKey="Liu J" first="Jie" last="Liu">Jie Liu</name><affiliation wicri:level="2"><nlm:affiliation>4National Heart Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>4National Heart Lung and Blood Institute, National Institutes of Health, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="Finkel, Toren" sort="Finkel, Toren" uniqKey="Finkel T" first="Toren" last="Finkel">Toren Finkel</name><affiliation wicri:level="2"><nlm:affiliation>4National Heart Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>4National Heart Lung and Blood Institute, National Institutes of Health, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="Clarke, Robert" sort="Clarke, Robert" uniqKey="Clarke R" first="Robert" last="Clarke">Robert Clarke</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">District de Columbia</region></placeName><wicri:cityArea>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington</wicri:cityArea></affiliation></author></analytic><series><title level="j">Cell death discovery</title><idno type="ISSN">2058-7716</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The postnatal mammary gland undergoes repeated cycles of proliferation and cell death, most notably when the fully differentiated (lactating) gland dedifferentiates to a prelactation state. Accumulation of milk proteins in the secretory epithelium creates the stress signal that triggers this process (involution). How this stress is perceived, and the cellular processes that are subsequently activated, remain unclear. We now report that Unfolded Protein Response (UPR), autophagy, and apoptosis related genes cluster separately during lactation and involution in the mouse mammary gland. Time-course experiments in rodents show that autophagy and UPR signaling are tightly co-regulated at the transition from reversible to irreversible involution. Inhibition of autophagy by chloroquine or genetic deletion of one ATG7 allele enhanced progression of mammary involution into the irreversible phase, as characterized by an early/precocious induction of apoptosis. These are the first preclinical in vivo data in support of a clinical trial testing an autophagy inhibitor for prevention of intraductal breast malignancy progression to invasive breast cancer. In marked contrast, stimulation of autophagy by low dose tunicamycin treatment reduced apoptosis and extended the reversible phase of involution by sustaining the secretory epithelium. Autophagy stimulators could be used short-term to promote lactation in women experiencing difficulties or irregularities in nursing. Taken together, these data indicate that UPR and autophagy play a key role in regulating the balance between cell survival and apoptosis during normal mammary gland regression.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">30345078</PMID><DateRevised><Year>2019</Year><Month>11</Month><Day>20</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">2058-7716</ISSN><JournalIssue CitedMedium="Print"><Volume>4</Volume><PubDate><Year>2018</Year></PubDate></JournalIssue><Title>Cell death discovery</Title><ISOAbbreviation>Cell Death Discov</ISOAbbreviation></Journal><ArticleTitle>Autophagy and unfolded protein response (UPR) regulate mammary gland involution by restraining apoptosis-driven irreversible changes.</ArticleTitle><Pagination><MedlinePgn>40</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41420-018-0105-y</ELocationID><Abstract><AbstractText>The postnatal mammary gland undergoes repeated cycles of proliferation and cell death, most notably when the fully differentiated (lactating) gland dedifferentiates to a prelactation state. Accumulation of milk proteins in the secretory epithelium creates the stress signal that triggers this process (involution). How this stress is perceived, and the cellular processes that are subsequently activated, remain unclear. We now report that Unfolded Protein Response (UPR), autophagy, and apoptosis related genes cluster separately during lactation and involution in the mouse mammary gland. Time-course experiments in rodents show that autophagy and UPR signaling are tightly co-regulated at the transition from reversible to irreversible involution. Inhibition of autophagy by chloroquine or genetic deletion of one ATG7 allele enhanced progression of mammary involution into the irreversible phase, as characterized by an early/precocious induction of apoptosis. These are the first preclinical in vivo data in support of a clinical trial testing an autophagy inhibitor for prevention of intraductal breast malignancy progression to invasive breast cancer. In marked contrast, stimulation of autophagy by low dose tunicamycin treatment reduced apoptosis and extended the reversible phase of involution by sustaining the secretory epithelium. Autophagy stimulators could be used short-term to promote lactation in women experiencing difficulties or irregularities in nursing. Taken together, these data indicate that UPR and autophagy play a key role in regulating the balance between cell survival and apoptosis during normal mammary gland regression.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y" EqualContrib="Y"><LastName>Wärri</LastName><ForeName>Anni</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>2Institute of Biomedicine, University of Turku Medical Faculty, Turku, 20014 Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y" EqualContrib="Y"><LastName>Cook</LastName><ForeName>Katherine L</ForeName><Initials>KL</Initials><AffiliationInfo><Affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>3Department of Surgery and Comprehensive Cancer Center, Wake Forest University, Winston Salem, NC 27157 USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hu</LastName><ForeName>Rong</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jin</LastName><ForeName>Lu</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zwart</LastName><ForeName>Alan</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Soto-Pantoja</LastName><ForeName>David R</ForeName><Initials>DR</Initials><AffiliationInfo><Affiliation>3Department of Surgery and Comprehensive Cancer Center, Wake Forest University, Winston Salem, NC 27157 USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Jie</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>4National Heart Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>5University of Pittsburgh, UPMC Aging Institute, Pittsburgh, PA 15213 USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Finkel</LastName><ForeName>Toren</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>4National Heart Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>5University of Pittsburgh, UPMC Aging Institute, Pittsburgh, PA 15213 USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Clarke</LastName><ForeName>Robert</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>1Department of Oncology and Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057 USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>P30 CA051008</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>U01 CA184902</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>U54 CA149147</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>10</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Cell Death Discov</MedlineTA><NlmUniqueID>101665035</NlmUniqueID><ISSNLinking>2058-7716</ISSNLinking></MedlineJournalInfo><CommentsCorrectionsList><CommentsCorrections RefType="ErratumIn"><RefSource>Cell Death Discov. 2019 Jul 10;5:116</RefSource><PMID Version="1">31312525</PMID></CommentsCorrections></CommentsCorrectionsList><CoiStatement>Compliance with ethical standardsThe authors declare that they have no conflict of interest.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>01</Month><Day>31</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2018</Year><Month>08</Month><Day>01</Day></PubMedPubDate><PubMedPubDate 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