The mTOR-Regulated Phosphoproteome Reveals a Mechanism of mTORC1-Mediated Inhibition of Growth Factor Signaling

The mammalian target of rapamycin (mTOR) protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse processes controlled by mTOR, few substrates are known. We defined the mTOR-regulated phosphoproteome by quantitative mass spectrometry and charact...

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Published in:	Science (American Association for the Advancement of Science) Vol. 332; no. 6035; pp. 1317 - 1322
Main Authors:	Hsu, Peggy P., Kang, Seong A., Rameseder, Jonathan, Zhang, Yi, Ottina, Kathleen A., Lim, Daniel, Peterson, Timothy R., Choi, Yongmun, Gray, Nathanael S., Yaffe, Michael B., Marto, Jarrod A., Sabatini, David M.
Format:	Journal Article
Language:	English
Published:	United States American Association for the Advancement of Science 10-06-2011 The American Association for the Advancement of Science
Subjects:	Amino acids Animals Cell Line Cellular biology Gene expression regulation GRB10 Adaptor Protein - metabolism Growth factors HeLa cells Humans Immunoblotting Inhibition Insulin Insulin - metabolism Intercellular Signaling Peptides and Proteins - metabolism Kinases Mass Spectrometry Mechanistic Target of Rapamycin Complex 1 Mice Multiprotein Complexes Naphthyridines - pharmacology Peptides Phosphoproteins - metabolism Phosphorylation Physiological regulation Proline Proteins Proteins - metabolism Proteome - metabolism Proteomics Receptors Signal Transduction Signaling Sirolimus - pharmacology TOR Serine-Threonine Kinases - metabolism Up regulation Vehicles
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Abstract	The mammalian target of rapamycin (mTOR) protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse processes controlled by mTOR, few substrates are known. We defined the mTOR-regulated phosphoproteome by quantitative mass spectrometry and characterized the primary sequence motif specificity of mTOR using positional scanning peptide libraries. We found that the phosphorylation response to insulin is largely mTOR dependent and that mTOR exhibits a unique preference for proline, hydrophobic, and aromatic residues at the +1 position. The adaptor protein Grb10 was identified as an mTORC1 substrate that mediates the inhibition of phosphoinositide 3-kinase typical of cells lacking tuberous sclerosis complex 2 (TSC2), a tumor suppressor and negative regulator of mTORC1. Our work clarifies how mTORC1 inhibits growth factor signaling and opens new areas of investigation in mTOR biology.
AbstractList	A search for substrates of a growth-promoting kinase revealed a regulatory feedback loop involved in tumor suppression. The mammalian target of rapamycin (mTOR) protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse processes controlled by mTOR, few substrates are known. We defined the mTOR-regulated phosphoproteome by quantitative mass spectrometry and characterized the primary sequence motif specificity of mTOR using positional scanning peptide libraries. We found that the phosphorylation response to insulin is largely mTOR dependent and that mTOR exhibits a unique preference for proline, hydrophobic, and aromatic residues at the +1 position. The adaptor protein Grb10 was identified as an mTORC1 substrate that mediates the inhibition of phosphoinositide 3-kinase typical of cells lacking tuberous sclerosis complex 2 (TSC2), a tumor suppressor and negative regulator of mTORC1. Our work clarifies how mTORC1 inhibits growth factor signaling and opens new areas of investigation in mTOR biology. The mTOR protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse processes controlled by mTOR, few substrates are known. We defined the mTOR-regulated phosphoproteome by quantitative mass spectrometry and characterized the primary sequence motif specificity of mTOR using positional scanning peptide libraries. We found that the phosphorylation response to insulin is largely mTOR-dependent and that mTOR exhibits a unique preference for proline, hydrophobic, and aromatic residues at the +1 position. The adaptor protein Grb10 was identified as an mTORC1 substrate that mediates the inhibition of PI3K typical of cells lacking TSC2, a tumor suppressor and negative regulator of mTORC1. Our work clarifies how mTORC1 inhibits growth factor signaling and opens new areas of investigation in mTOR biology. The mammalian target of rapamycin (mTOR) protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse processes controlled by mTOR, few substrates are known. We defined the mTOR-regulated phosphoproteome by quantitative mass spectrometry and characterized the primary sequence motif specificity of mTOR using positional scanning peptide libraries. We found that the phosphorylation response to insulin is largely mTOR dependent and that mTOR exhibits a unique preference for proline, hydrophobic, and aromatic residues at the +1 position. The adaptor protein Grb10 was identified as an mTORC1 substrate that mediates the inhibition of phosphoinositide 3-kinase typical of cells lacking tuberous sclerosis complex 2 (TSC2), a tumor suppressor and negative regulator of mTORC1. Our work clarifies how mTORC1 inhibits growth factor signaling and opens new areas of investigation in mTOR biology. The protein kinase mTOR functions in protein complexes (mTORC1 and mTORC2) that are activated in response to agents such as growth factors and insulin and has important roles in regulating many physiological responses, including cell growth, proliferation, metabolism, and cell survival (see the Perspective by Yea and Fruman ). Hsu et al. (p. 1317) and Yu et al. (p. 1322) conducted proteomic screens to identify substrates of mTORC1 and mTORC2 kinases. Numerous proteins that appear to be direct substrates were identified, including a new mTOR substrate, Grb10. Grb10 is an adaptor molecule that functions in the formation of signaling complexes associated with growth factor receptor tyrosine kinases. The mammalian target of rapamycin (mTOR) protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse processes controlled by mTOR, few substrates are known. We defined the mTOR-regulated phosphoproteome by quantitative mass spectrometry and characterized the primary sequence motif specificity of mTOR using positional scanning peptide libraries. We found that the phosphorylation response to insulin is largely mTOR dependent and that mTOR exhibits a unique preference for proline, hydrophobic, and aromatic residues at the +1 position. The adaptor protein Grb10 was identified as an mTORC1 substrate that mediates the inhibition of phosphoinositide 3-kinase typical of cells lacking tuberous sclerosis complex 2 (TSC2), a tumor suppressor and negative regulator of mTORC1. Our work clarifies how mTORC1 inhibits growth factor signaling and opens new areas of investigation in mTOR biology. [PUBLICATION ABSTRACT]
Author	Sabatini, David M. Ottina, Kathleen A. Rameseder, Jonathan Lim, Daniel Marto, Jarrod A. Gray, Nathanael S. Zhang, Yi Hsu, Peggy P. Yaffe, Michael B. Kang, Seong A. Choi, Yongmun Peterson, Timothy R.
AuthorAffiliation	4 David H. Koch Institute for Integrative Cancer Research at MIT, 77 Massachusetts Avenue, Cambridge, MA 02139, USA 5 Department of Cancer Biology, Dana Farber Cancer Institute (DFCI), 250 Longwood Avenue, Boston, MA 02115, USA 1 Whitehead Institute for Biomedical Research, Nine Cambridge Center, Cambridge, MA 02142, USA 2 Department of Biology, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA 8 Howard Hughes Medical Institute 7 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, 250 Longwood Avenue, Boston, MA 02115, USA 6 Blais Proteomics Center, DFCI, 250 Longwood Avenue, Boston, MA 02115, USA 3 Computational and Systems Biology Initiative, MIT, Cambridge, MA 02139, USA
AuthorAffiliation_xml	– name: 2 Department of Biology, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA – name: 7 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, 250 Longwood Avenue, Boston, MA 02115, USA – name: 8 Howard Hughes Medical Institute – name: 1 Whitehead Institute for Biomedical Research, Nine Cambridge Center, Cambridge, MA 02142, USA – name: 3 Computational and Systems Biology Initiative, MIT, Cambridge, MA 02139, USA – name: 4 David H. Koch Institute for Integrative Cancer Research at MIT, 77 Massachusetts Avenue, Cambridge, MA 02139, USA – name: 6 Blais Proteomics Center, DFCI, 250 Longwood Avenue, Boston, MA 02115, USA – name: 5 Department of Cancer Biology, Dana Farber Cancer Institute (DFCI), 250 Longwood Avenue, Boston, MA 02115, USA
Author_xml	– sequence: 1 givenname: Peggy P. surname: Hsu fullname: Hsu, Peggy P. – sequence: 2 givenname: Seong A. surname: Kang fullname: Kang, Seong A. – sequence: 3 givenname: Jonathan surname: Rameseder fullname: Rameseder, Jonathan – sequence: 4 givenname: Yi surname: Zhang fullname: Zhang, Yi – sequence: 5 givenname: Kathleen A. surname: Ottina fullname: Ottina, Kathleen A. – sequence: 6 givenname: Daniel surname: Lim fullname: Lim, Daniel – sequence: 7 givenname: Timothy R. surname: Peterson fullname: Peterson, Timothy R. – sequence: 8 givenname: Yongmun surname: Choi fullname: Choi, Yongmun – sequence: 9 givenname: Nathanael S. surname: Gray fullname: Gray, Nathanael S. – sequence: 10 givenname: Michael B. surname: Yaffe fullname: Yaffe, Michael B. – sequence: 11 givenname: Jarrod A. surname: Marto fullname: Marto, Jarrod A. – sequence: 12 givenname: David M. surname: Sabatini fullname: Sabatini, David M.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21659604$$D View this record in MEDLINE/PubMed
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Snippet	The mammalian target of rapamycin (mTOR) protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse... A search for substrates of a growth-promoting kinase revealed a regulatory feedback loop involved in tumor suppression. The mammalian target of rapamycin... The protein kinase mTOR functions in protein complexes (mTORC1 and mTORC2) that are activated in response to agents such as growth factors and insulin and has... The mTOR protein kinase is a master growth promoter that nucleates two complexes, mTORC1 and mTORC2. Despite the diverse processes controlled by mTOR, few...
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SubjectTerms	Amino acids Animals Cell Line Cellular biology Gene expression regulation GRB10 Adaptor Protein - metabolism Growth factors HeLa cells Humans Immunoblotting Inhibition Insulin Insulin - metabolism Intercellular Signaling Peptides and Proteins - metabolism Kinases Mass Spectrometry Mechanistic Target of Rapamycin Complex 1 Mice Multiprotein Complexes Naphthyridines - pharmacology Peptides Phosphoproteins - metabolism Phosphorylation Physiological regulation Proline Proteins Proteins - metabolism Proteome - metabolism Proteomics Receptors Signal Transduction Signaling Sirolimus - pharmacology TOR Serine-Threonine Kinases - metabolism Up regulation Vehicles
Title	The mTOR-Regulated Phosphoproteome Reveals a Mechanism of mTORC1-Mediated Inhibition of Growth Factor Signaling
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