Quantitative phosphoproteomics reveals involvement of multiple signaling pathways in early phagocytosis by the retinal pigmented epithelium.
Identifieur interne : 000768 ( Main/Exploration ); précédent : 000767; suivant : 000769Quantitative phosphoproteomics reveals involvement of multiple signaling pathways in early phagocytosis by the retinal pigmented epithelium.
Auteurs : Cheng-Kang Chiang [Canada, Taïwan] ; Aleksander Tworak ; Brian M. Kevany ; Bo Xu [Canada] ; Janice Mayne [Canada] ; Zhibin Ning [Canada] ; Daniel Figeys [Canada] ; Krzysztof Palczewski [États-Unis]Source :
- The Journal of biological chemistry [ 1083-351X ] ; 2017.
Descripteurs français
- KwdFr :
- Animaux (MeSH), Lignée cellulaire (MeSH), Phagocytose (MeSH), Phosphatidylinositol 3-kinases (métabolisme), Phosphoprotéines (métabolisme), Protein kinases (métabolisme), Protéomique (MeSH), Souris (MeSH), Sérine-thréonine kinases TOR (métabolisme), Transcriptome (MeSH), Transduction du signal (MeSH), Épithélium pigmentaire de la rétine (cytologie), Épithélium pigmentaire de la rétine (métabolisme).
- MESH :
English descriptors
- KwdEn :
- Animals (MeSH), Cell Line (MeSH), Mice (MeSH), Phagocytosis (MeSH), Phosphatidylinositol 3-Kinases (metabolism), Phosphoproteins (metabolism), Protein Kinases (metabolism), Proteomics (MeSH), Retinal Pigment Epithelium (cytology), Retinal Pigment Epithelium (metabolism), Signal Transduction (MeSH), TOR Serine-Threonine Kinases (metabolism), Transcriptome (MeSH).
- MESH :
- chemical , metabolism : Phosphatidylinositol 3-Kinases, Phosphoproteins, Protein Kinases, TOR Serine-Threonine Kinases.
- cytology : Retinal Pigment Epithelium.
- metabolism : Retinal Pigment Epithelium.
- Animals, Cell Line, Mice, Phagocytosis, Proteomics, Signal Transduction, Transcriptome.
Abstract
One of the major biological functions of the retinal pigmented epithelium (RPE) is the clearance of shed photoreceptor outer segments (POS) through a multistep process resembling phagocytosis. RPE phagocytosis helps maintain the viability of photoreceptors that otherwise could succumb to the high metabolic flux and photo-oxidative stress associated with visual processing. The regulatory mechanisms underlying phagocytosis in the RPE are not fully understood, although dysfunction of this process contributes to the pathogenesis of multiple human retinal degenerative disorders, including age-related macular degeneration. Here, we present an integrated transcriptomic, proteomic, and phosphoproteomic analysis of phagocytosing RPE cells, utilizing three different experimental models: the human-derived RPE-like cell line ARPE-19, cultured murine primary RPE cells, and RPE samples from live mice. Our combined results indicated that early stages of phagocytosis in the RPE are mainly characterized by pronounced changes in the protein phosphorylation level. Global phosphoprotein enrichment analysis revealed involvement of PI3K/Akt, mechanistic target of rapamycin (mTOR), and MEK/ERK pathways in the regulation of RPE phagocytosis, confirmed by immunoblot analyses and in vitro phagocytosis assays. Most strikingly, phagocytosis of POS by cultured RPE cells was almost completely blocked by pharmacological inhibition of phosphorylation of Akt. Our findings, along with those of previous studies, indicate that these phosphorylation events allow the RPE to integrate multiple signals instigated by shed POS at different stages of the phagocytic process.
DOI: 10.1074/jbc.M117.812677
PubMed: 28978645
PubMed Central: PMC5712622
Affiliations:
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when="2017">2017</date><idno type="RBID">pubmed:28978645</idno><idno type="pmid">28978645</idno><idno type="doi">10.1074/jbc.M117.812677</idno><idno type="pmc">PMC5712622</idno><idno type="wicri:Area/Main/Corpus">000711</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000711</idno><idno type="wicri:Area/Main/Curation">000711</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000711</idno><idno type="wicri:Area/Main/Exploration">000711</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Quantitative phosphoproteomics reveals involvement of multiple signaling pathways in early phagocytosis by the retinal pigmented epithelium.</title><author><name sortKey="Chiang, Cheng Kang" sort="Chiang, Cheng Kang" uniqKey="Chiang C" first="Cheng-Kang" last="Chiang">Cheng-Kang Chiang</name><affiliation wicri:level="1"><nlm:affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5</wicri:regionArea><wicri:noRegion>Ontario K1H 8M5</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>the Department of Chemistry, National Dong Hwa University, No. 1 Sec. 2 Da Hsueh Road, Shoufeng, Hualien 97401, Taiwan.</nlm:affiliation><country xml:lang="fr">Taïwan</country><wicri:regionArea>the Department of Chemistry, National Dong Hwa University, No. 1 Sec. 2 Da Hsueh Road, Shoufeng, Hualien 97401</wicri:regionArea><wicri:noRegion>Hualien 97401</wicri:noRegion></affiliation></author><author><name sortKey="Tworak, Aleksander" sort="Tworak, Aleksander" uniqKey="Tworak A" first="Aleksander" last="Tworak">Aleksander Tworak</name><affiliation><nlm:affiliation>the Department of Pharmacology and.</nlm:affiliation><wicri:noCountry code="no comma">the Department of Pharmacology and.</wicri:noCountry></affiliation></author><author><name sortKey="Kevany, Brian M" sort="Kevany, Brian M" uniqKey="Kevany B" first="Brian M" last="Kevany">Brian M. Kevany</name><affiliation><nlm:affiliation>the Department of Pharmacology and.</nlm:affiliation><wicri:noCountry code="no comma">the Department of Pharmacology and.</wicri:noCountry></affiliation></author><author><name sortKey="Xu, Bo" sort="Xu, Bo" uniqKey="Xu B" first="Bo" last="Xu">Bo Xu</name><affiliation wicri:level="1"><nlm:affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5</wicri:regionArea><wicri:noRegion>Ontario K1H 8M5</wicri:noRegion></affiliation></author><author><name sortKey="Mayne, Janice" sort="Mayne, Janice" uniqKey="Mayne J" first="Janice" last="Mayne">Janice Mayne</name><affiliation wicri:level="1"><nlm:affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5</wicri:regionArea><wicri:noRegion>Ontario K1H 8M5</wicri:noRegion></affiliation></author><author><name sortKey="Ning, Zhibin" sort="Ning, Zhibin" uniqKey="Ning Z" first="Zhibin" last="Ning">Zhibin Ning</name><affiliation wicri:level="1"><nlm:affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5</wicri:regionArea><wicri:noRegion>Ontario K1H 8M5</wicri:noRegion></affiliation></author><author><name sortKey="Figeys, Daniel" sort="Figeys, Daniel" uniqKey="Figeys D" first="Daniel" last="Figeys">Daniel Figeys</name><affiliation wicri:level="1"><nlm:affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada, dfigeys@uottawa.ca.</nlm:affiliation><country wicri:rule="url">Canada</country><wicri:regionArea>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada</wicri:regionArea><wicri:noRegion>Canada</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>the Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>the Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8</wicri:regionArea><wicri:noRegion>Ontario M5G 1Z8</wicri:noRegion></affiliation></author><author><name sortKey="Palczewski, Krzysztof" sort="Palczewski, Krzysztof" uniqKey="Palczewski K" first="Krzysztof" last="Palczewski">Krzysztof Palczewski</name><affiliation wicri:level="1"><nlm:affiliation>the Department of Pharmacology and kxp65@case.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country></affiliation><affiliation><nlm:affiliation>the Cleveland Center for Membrane and Structural Biology, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation></author></analytic><series><title level="j">The Journal of biological chemistry</title><idno type="eISSN">1083-351X</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term><term>Cell Line (MeSH)</term><term>Mice (MeSH)</term><term>Phagocytosis (MeSH)</term><term>Phosphatidylinositol 3-Kinases (metabolism)</term><term>Phosphoproteins (metabolism)</term><term>Protein Kinases (metabolism)</term><term>Proteomics (MeSH)</term><term>Retinal Pigment Epithelium (cytology)</term><term>Retinal Pigment Epithelium (metabolism)</term><term>Signal Transduction (MeSH)</term><term>TOR Serine-Threonine Kinases (metabolism)</term><term>Transcriptome (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux (MeSH)</term><term>Lignée cellulaire (MeSH)</term><term>Phagocytose (MeSH)</term><term>Phosphatidylinositol 3-kinases (métabolisme)</term><term>Phosphoprotéines (métabolisme)</term><term>Protein kinases (métabolisme)</term><term>Protéomique (MeSH)</term><term>Souris (MeSH)</term><term>Sérine-thréonine kinases TOR (métabolisme)</term><term>Transcriptome (MeSH)</term><term>Transduction du signal (MeSH)</term><term>Épithélium pigmentaire de la rétine (cytologie)</term><term>Épithélium pigmentaire de la rétine (métabolisme)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Phosphatidylinositol 3-Kinases</term><term>Phosphoproteins</term><term>Protein Kinases</term><term>TOR Serine-Threonine Kinases</term></keywords><keywords scheme="MESH" qualifier="cytologie" xml:lang="fr"><term>Épithélium pigmentaire de la rétine</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Retinal Pigment Epithelium</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Retinal Pigment Epithelium</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Phosphatidylinositol 3-kinases</term><term>Phosphoprotéines</term><term>Protein kinases</term><term>Sérine-thréonine kinases TOR</term><term>Épithélium pigmentaire de la rétine</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cell Line</term><term>Mice</term><term>Phagocytosis</term><term>Proteomics</term><term>Signal Transduction</term><term>Transcriptome</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Lignée cellulaire</term><term>Phagocytose</term><term>Protéomique</term><term>Souris</term><term>Transcriptome</term><term>Transduction du signal</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">One of the major biological functions of the retinal pigmented epithelium (RPE) is the clearance of shed photoreceptor outer segments (POS) through a multistep process resembling phagocytosis. RPE phagocytosis helps maintain the viability of photoreceptors that otherwise could succumb to the high metabolic flux and photo-oxidative stress associated with visual processing. The regulatory mechanisms underlying phagocytosis in the RPE are not fully understood, although dysfunction of this process contributes to the pathogenesis of multiple human retinal degenerative disorders, including age-related macular degeneration. Here, we present an integrated transcriptomic, proteomic, and phosphoproteomic analysis of phagocytosing RPE cells, utilizing three different experimental models: the human-derived RPE-like cell line ARPE-19, cultured murine primary RPE cells, and RPE samples from live mice. Our combined results indicated that early stages of phagocytosis in the RPE are mainly characterized by pronounced changes in the protein phosphorylation level. Global phosphoprotein enrichment analysis revealed involvement of PI3K/Akt, mechanistic target of rapamycin (mTOR), and MEK/ERK pathways in the regulation of RPE phagocytosis, confirmed by immunoblot analyses and <i>in vitro</i> phagocytosis assays. Most strikingly, phagocytosis of POS by cultured RPE cells was almost completely blocked by pharmacological inhibition of phosphorylation of Akt. Our findings, along with those of previous studies, indicate that these phosphorylation events allow the RPE to integrate multiple signals instigated by shed POS at different stages of the phagocytic process.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">28978645</PMID><DateCompleted><Year>2018</Year><Month>01</Month><Day>16</Day></DateCompleted><DateRevised><Year>2018</Year><Month>12</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1083-351X</ISSN><JournalIssue CitedMedium="Internet"><Volume>292</Volume><Issue>48</Issue><PubDate><Year>2017</Year><Month>12</Month><Day>01</Day></PubDate></JournalIssue><Title>The Journal of biological chemistry</Title><ISOAbbreviation>J Biol Chem</ISOAbbreviation></Journal><ArticleTitle>Quantitative phosphoproteomics reveals involvement of multiple signaling pathways in early phagocytosis by the retinal pigmented epithelium.</ArticleTitle><Pagination><MedlinePgn>19826-19839</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1074/jbc.M117.812677</ELocationID><Abstract><AbstractText>One of the major biological functions of the retinal pigmented epithelium (RPE) is the clearance of shed photoreceptor outer segments (POS) through a multistep process resembling phagocytosis. RPE phagocytosis helps maintain the viability of photoreceptors that otherwise could succumb to the high metabolic flux and photo-oxidative stress associated with visual processing. The regulatory mechanisms underlying phagocytosis in the RPE are not fully understood, although dysfunction of this process contributes to the pathogenesis of multiple human retinal degenerative disorders, including age-related macular degeneration. Here, we present an integrated transcriptomic, proteomic, and phosphoproteomic analysis of phagocytosing RPE cells, utilizing three different experimental models: the human-derived RPE-like cell line ARPE-19, cultured murine primary RPE cells, and RPE samples from live mice. Our combined results indicated that early stages of phagocytosis in the RPE are mainly characterized by pronounced changes in the protein phosphorylation level. Global phosphoprotein enrichment analysis revealed involvement of PI3K/Akt, mechanistic target of rapamycin (mTOR), and MEK/ERK pathways in the regulation of RPE phagocytosis, confirmed by immunoblot analyses and <i>in vitro</i> phagocytosis assays. Most strikingly, phagocytosis of POS by cultured RPE cells was almost completely blocked by pharmacological inhibition of phosphorylation of Akt. Our findings, along with those of previous studies, indicate that these phosphorylation events allow the RPE to integrate multiple signals instigated by shed POS at different stages of the phagocytic process.</AbstractText><CopyrightInformation>© 2017 by The American Society for Biochemistry and Molecular Biology, Inc.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chiang</LastName><ForeName>Cheng-Kang</ForeName><Initials>CK</Initials><AffiliationInfo><Affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>the Department of Chemistry, National Dong Hwa University, No. 1 Sec. 2 Da Hsueh Road, Shoufeng, Hualien 97401, Taiwan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tworak</LastName><ForeName>Aleksander</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>the Department of Pharmacology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kevany</LastName><ForeName>Brian M</ForeName><Initials>BM</Initials><AffiliationInfo><Affiliation>the Department of Pharmacology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xu</LastName><ForeName>Bo</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mayne</LastName><ForeName>Janice</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ning</LastName><ForeName>Zhibin</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Figeys</LastName><ForeName>Daniel</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>From the Ottawa Institute of Systems Biology and Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada, dfigeys@uottawa.ca.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>the Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Palczewski</LastName><ForeName>Krzysztof</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0002-0788-545X</Identifier><AffiliationInfo><Affiliation>the Department of Pharmacology and kxp65@case.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>the Cleveland Center for Membrane and Structural Biology, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106, and.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>P30 EY011373</GrantID><Acronym>EY</Acronym><Agency>NEI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 EY009339</GrantID><Acronym>EY</Acronym><Agency>NEI NIH HHS</Agency><Country>United States</Country></Grant><Grant><Agency>CIHR</Agency><Country>Canada</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2017</Year><Month>10</Month><Day>04</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Biol Chem</MedlineTA><NlmUniqueID>2985121R</NlmUniqueID><ISSNLinking>0021-9258</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010750">Phosphoproteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.7.-</RegistryNumber><NameOfSubstance UI="D011494">Protein Kinases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.7.1.-</RegistryNumber><NameOfSubstance UI="D019869">Phosphatidylinositol 3-Kinases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.7.1.1</RegistryNumber><NameOfSubstance UI="D058570">TOR Serine-Threonine Kinases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 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