mTORC2 Is Involved in the Induction of RSK Phosphorylation by Serum or Nutrient Starvation.
Identifieur interne : 000005 ( Main/Exploration ); précédent : 000004; suivant : 000006mTORC2 Is Involved in the Induction of RSK Phosphorylation by Serum or Nutrient Starvation.
Auteurs : Po-Chien Chou [États-Unis] ; Swati Rajput [États-Unis] ; Xiaoyun Zhao [République populaire de Chine] ; Chadni Patel [États-Unis] ; Danielle Albaciete [États-Unis] ; Won Jun Oh [États-Unis] ; Heineken Queen Daguplo [États-Unis] ; Nikhil Patel [États-Unis] ; Bing Su [République populaire de Chine] ; Guy Werlen [États-Unis] ; Estela Jacinto [États-Unis]Source :
- Cells [ 2073-4409 ] ; 2020.
Abstract
Cells adjust to nutrient fluctuations to restore metabolic homeostasis. The mechanistic target of rapamycin (mTOR) complex 2 responds to nutrient levels and growth signals to phosphorylate protein kinases belonging to the AGC (Protein Kinases A,G,C) family such as Akt and PKC. Phosphorylation of these AGC kinases at their conserved hydrophobic motif (HM) site by mTORC2 enhances their activation and mediates the functions of mTORC2 in cell growth and metabolism. Another AGC kinase family member that is known to undergo increased phosphorylation at the homologous HM site (Ser380) is the p90 ribosomal S6 kinase (RSK). Phosphorylation at Ser380 is facilitated by the activation of the mitogen-activated protein kinase/extracellular signal regulated kinase (MAPK/ERK) in response to growth factor stimulation. Here, we demonstrate that optimal phosphorylation of RSK at this site requires an intact mTORC2. We also found that RSK is robustly phosphorylated at Ser380 upon nutrient withdrawal or inhibition of glycolysis, conditions that increase mTORC2 activation. However, pharmacological inhibition of mTOR did not abolish RSK phosphorylation at Ser380, indicating that mTOR catalytic activity is not required for this phosphorylation. Since RSK and SIN1β colocalize at the membrane during serum restimulation and acute glutamine withdrawal, mTORC2 could act as a scaffold to enhance RSK HM site phosphorylation. Among the known RSK substrates, the CCTβ subunit of the chaperonin containing TCP-1 (CCT) complex had defective phosphorylation in the absence of mTORC2. Our findings indicate that the mTORC2-mediated phosphorylation of the RSK HM site could confer RSK substrate specificity and reveal that RSK responds to nutrient fluctuations.
DOI: 10.3390/cells9071567
PubMed: 32605013
PubMed Central: PMC7408474
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08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Rajput, Swati" sort="Rajput, Swati" uniqKey="Rajput S" first="Swati" last="Rajput">Swati Rajput</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Zhao, Xiaoyun" sort="Zhao, Xiaoyun" uniqKey="Zhao X" first="Xiaoyun" last="Zhao">Xiaoyun Zhao</name><affiliation wicri:level="1"><nlm:affiliation>Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai 200240, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai 200240</wicri:regionArea><wicri:noRegion>Shanghai 200240</wicri:noRegion></affiliation></author><author><name sortKey="Patel, Chadni" sort="Patel, Chadni" uniqKey="Patel C" first="Chadni" last="Patel">Chadni Patel</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Albaciete, Danielle" sort="Albaciete, Danielle" uniqKey="Albaciete D" first="Danielle" last="Albaciete">Danielle Albaciete</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Oh, Won Jun" sort="Oh, Won Jun" uniqKey="Oh W" first="Won Jun" last="Oh">Won Jun Oh</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Daguplo, Heineken Queen" sort="Daguplo, Heineken Queen" uniqKey="Daguplo H" first="Heineken Queen" last="Daguplo">Heineken Queen Daguplo</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Patel, Nikhil" sort="Patel, Nikhil" uniqKey="Patel N" first="Nikhil" last="Patel">Nikhil Patel</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Su, Bing" sort="Su, Bing" uniqKey="Su B" first="Bing" last="Su">Bing Su</name><affiliation wicri:level="1"><nlm:affiliation>Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai 200240, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai 200240</wicri:regionArea><wicri:noRegion>Shanghai 200240</wicri:noRegion></affiliation></author><author><name sortKey="Werlen, Guy" sort="Werlen, Guy" uniqKey="Werlen G" first="Guy" last="Werlen">Guy Werlen</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Jacinto, Estela" sort="Jacinto, Estela" uniqKey="Jacinto E" first="Estela" last="Jacinto">Estela Jacinto</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author></analytic><series><title level="j">Cells</title><idno type="eISSN">2073-4409</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Cells adjust to nutrient fluctuations to restore metabolic homeostasis. The mechanistic target of rapamycin (mTOR) complex 2 responds to nutrient levels and growth signals to phosphorylate protein kinases belonging to the AGC (Protein Kinases A,G,C) family such as Akt and PKC. Phosphorylation of these AGC kinases at their conserved hydrophobic motif (HM) site by mTORC2 enhances their activation and mediates the functions of mTORC2 in cell growth and metabolism. Another AGC kinase family member that is known to undergo increased phosphorylation at the homologous HM site (Ser380) is the p90 ribosomal S6 kinase (RSK). Phosphorylation at Ser380 is facilitated by the activation of the mitogen-activated protein kinase/extracellular signal regulated kinase (MAPK/ERK) in response to growth factor stimulation. Here, we demonstrate that optimal phosphorylation of RSK at this site requires an intact mTORC2. We also found that RSK is robustly phosphorylated at Ser380 upon nutrient withdrawal or inhibition of glycolysis, conditions that increase mTORC2 activation. However, pharmacological inhibition of mTOR did not abolish RSK phosphorylation at Ser380, indicating that mTOR catalytic activity is not required for this phosphorylation. Since RSK and SIN1β colocalize at the membrane during serum restimulation and acute glutamine withdrawal, mTORC2 could act as a scaffold to enhance RSK HM site phosphorylation. Among the known RSK substrates, the CCTβ subunit of the chaperonin containing TCP-1 (CCT) complex had defective phosphorylation in the absence of mTORC2. Our findings indicate that the mTORC2-mediated phosphorylation of the RSK HM site could confer RSK substrate specificity and reveal that RSK responds to nutrient fluctuations.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32605013</PMID><DateRevised><Year>2020</Year><Month>08</Month><Day>14</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2073-4409</ISSN><JournalIssue CitedMedium="Internet"><Volume>9</Volume><Issue>7</Issue><PubDate><Year>2020</Year><Month>Jun</Month><Day>27</Day></PubDate></JournalIssue><Title>Cells</Title><ISOAbbreviation>Cells</ISOAbbreviation></Journal><ArticleTitle>mTORC2 Is Involved in the Induction of RSK Phosphorylation by Serum or Nutrient Starvation.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E1567</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/cells9071567</ELocationID><Abstract><AbstractText>Cells adjust to nutrient fluctuations to restore metabolic homeostasis. The mechanistic target of rapamycin (mTOR) complex 2 responds to nutrient levels and growth signals to phosphorylate protein kinases belonging to the AGC (Protein Kinases A,G,C) family such as Akt and PKC. Phosphorylation of these AGC kinases at their conserved hydrophobic motif (HM) site by mTORC2 enhances their activation and mediates the functions of mTORC2 in cell growth and metabolism. Another AGC kinase family member that is known to undergo increased phosphorylation at the homologous HM site (Ser380) is the p90 ribosomal S6 kinase (RSK). Phosphorylation at Ser380 is facilitated by the activation of the mitogen-activated protein kinase/extracellular signal regulated kinase (MAPK/ERK) in response to growth factor stimulation. Here, we demonstrate that optimal phosphorylation of RSK at this site requires an intact mTORC2. We also found that RSK is robustly phosphorylated at Ser380 upon nutrient withdrawal or inhibition of glycolysis, conditions that increase mTORC2 activation. However, pharmacological inhibition of mTOR did not abolish RSK phosphorylation at Ser380, indicating that mTOR catalytic activity is not required for this phosphorylation. Since RSK and SIN1β colocalize at the membrane during serum restimulation and acute glutamine withdrawal, mTORC2 could act as a scaffold to enhance RSK HM site phosphorylation. Among the known RSK substrates, the CCTβ subunit of the chaperonin containing TCP-1 (CCT) complex had defective phosphorylation in the absence of mTORC2. Our findings indicate that the mTORC2-mediated phosphorylation of the RSK HM site could confer RSK substrate specificity and reveal that RSK responds to nutrient fluctuations.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chou</LastName><ForeName>Po-Chien</ForeName><Initials>PC</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rajput</LastName><ForeName>Swati</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0001-8794-4300</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Xiaoyun</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai 200240, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Patel</LastName><ForeName>Chadni</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Albaciete</LastName><ForeName>Danielle</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oh</LastName><ForeName>Won Jun</ForeName><Initials>WJ</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Daguplo</LastName><ForeName>Heineken Queen</ForeName><Initials>HQ</Initials><Identifier Source="ORCID">0000-0002-3669-1144</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Patel</LastName><ForeName>Nikhil</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Su</LastName><ForeName>Bing</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai 200240, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Werlen</LastName><ForeName>Guy</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jacinto</LastName><ForeName>Estela</ForeName><Initials>E</Initials><Identifier Source="ORCID">0000-0001-7118-1759</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>GM079176</GrantID><Acronym>NH</Acronym><Agency>NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>CA154674</GrantID><Acronym>NH</Acronym><Agency>NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>GM137493</GrantID><Acronym>NH</Acronym><Agency>NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>DFHS18CRF008</GrantID><Agency>New Jersey Commission on Cancer Research</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>27</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Cells</MedlineTA><NlmUniqueID>101600052</NlmUniqueID><ISSNLinking>2073-4409</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">AGC kinases</Keyword><Keyword MajorTopicYN="N">CCT/TRiC</Keyword><Keyword MajorTopicYN="N">CCTβ</Keyword><Keyword MajorTopicYN="N">MAPK/ERK</Keyword><Keyword MajorTopicYN="N">RSK</Keyword><Keyword MajorTopicYN="N">chaperonin</Keyword><Keyword MajorTopicYN="N">mTORC2</Keyword><Keyword MajorTopicYN="N">metabolism</Keyword><Keyword MajorTopicYN="N">nutrients</Keyword><Keyword MajorTopicYN="N">p90 ribosomal s6 kinase</Keyword><Keyword MajorTopicYN="N">starvation</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>05</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>06</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>23</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>7</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>7</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>7</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId 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