SH3BP4 Is a Negative Regulator of Amino Acid-Rag GTPase-mTORC1 Signaling

Molecular Cell

Volumn 46, Issue 6, 2012, Pages 833-846

  Kim, Young Mi ^a   Stone, Matthew ^a   Hwang, Tae Hyun ^b   Kim, Yeon Gil ^c   Dunlevy, Jane R ^d   Griffin, Timothy J ^a   Kim, Do Hyung ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c POSTECH   (South Korea)

^d UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MEMBRANE PROTEIN; RAG GUANOSINE TRIPHOSPHATASE; SH3 DOMAIN BINDING PROTEIN 4; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AMINO ACID ANALYSIS; ARTICLE; AUTOPHAGY; BINDING AFFINITY; BINDING KINETICS; CELL GROWTH; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; FLUORESCENCE ANALYSIS; HELA CELL; HUMAN; HUMAN CELL; INHIBITION KINETICS; LYSOSOME; NONHUMAN; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MALNUTRITION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACIDS; ANIMALS; AUTOPHAGY; BINDING SITES; CELL LINE; GUANOSINE; HEK293 CELLS; HUMANS; LYSOSOMES; MICE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TOR SERINE-THREONINE KINASES;

EID: 84863009605     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.04.007     Document Type: Article

References (39)

1. Binda M., Peli-Gulli M.P., Bonfils G., Panchaud N., Urban J., Sturgill T.W., Loewith R., De Virgilio C. The Vam6 GEF controls TORC1 by activating the EGO complex. Mol. Cell 2009, 35:563-573.
2. Bonfils G., Jaquenoud M., Bontron S., Ostrowicz C., Ungermann C., De Virgilio C. Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Mol. Cell 2012, 46:105-110.
3. Bryk B., Hahn K., Cohen S.M., Teleman A.A. MAP4K3 regulates body size and metabolism in Drosophila. Dev. Biol. 2010, 344:150-157.
4. Chen R.Q., Yang Q.K., Lu B.W., Yi W., Cantin G., Chen Y.L., Fearns C., Yates J.R., Lee J.D. CDC25B mediates rapamycin-induced oncogenic responses in cancer cells. Cancer Res. 2009, 69:2663-2668.
5. Chiba S., Tokuhara M., Morita E.H., Abe S. TTP at Ser245 phosphorylation by AKT is required for binding to 14-3-3. J. Biochem. 2009, 145:403-409.
6. Dubouloz F., Deloche O., Wanke V., Cameroni E., De Virgilio C. The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol. Cell 2005, 19:15-26.
7. Dunlevy J.R., Berryhill B.L., Vergnes J.P., SundarRaj N., Hassell J.R. Cloning, chromosomal localization, and characterization of cDNA from a novel gene, SH3BP4, expressed by human corneal fibroblasts. Genomics 1999, 62:519-524.
8. Duran A., Amanchy R., Linares J.F., Joshi J., Abu-Baker S., Porollo A., Hansen M., Moscat J., Diaz-Meco M.T. p62 is a key regulator of nutrient sensing in the mTORC1 pathway. Mol. Cell 2011, 44:134-146.
9. Erpel T., Superti-Furga G., Courtneidge S.A. Mutational analysis of the Src SH3 domain: the same residues of the ligand binding surface are important for intra- and intermolecular interactions. EMBO J. 1995, 14:963-975.
10. Findlay G.M., Yan L., Procter J., Mieulet V., Lamb R.F. A MAP4 kinase related to Ste20 is a nutrient-sensitive regulator of mTOR signalling. Biochem. J. 2007, 403:13-20.
11. Fingar D.C., Blenis J. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 2004, 23:3151-3171.
12. Gao M., Kaiser C.A. A conserved GTPase-containing complex is required for intracellular sorting of the general amino-acid permease in yeast. Nat. Cell Biol. 2006, 8:657-667.
13. Goberdhan D.C., Boyd C.A. mTOR: dissecting regulation and mechanism of action to understand human disease. Biochem. Soc. Trans. 2009, 37:213-216.
14. Han J.M., Jeong S.J., Park M.C., Kim G., Kwon N.H., Kim H.K., Ha S.H., Ryu S.H., Kim S. Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 2012, 149:410-424.
15. Hara K., Maruki Y., Long X., Yoshino K., Oshiro N., Hidayat S., Tokunaga C., Avruch J., Yonezawa K. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 2002, 110:177-189.
16. Harrison D.E., Strong R., Sharp Z.D., Nelson J.F., Astle C.M., Flurkey K., Nadon N.L., Wilkinson J.E., Frenkel K., Carter C.S., et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009, 460:392-395.
17. Hirose E., Nakashima N., Sekiguchi T., Nishimoto T. RagA is a functional homologue of S. cerevisiae Gtr1p involved in the Ran/Gsp1-GTPase pathway. J. Cell Sci. 1998, 111:11-21.
18. Hosokawa N., Hara T., Kaizuka T., Kishi C., Takamura A., Miura Y., Iemura S., Natsume T., Takehana K., Yamada N., et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 2009, 20:1981-1991.
19. Jung C.H., Jun C.B., Ro S.H., Kim Y.M., Otto N.M., Cao J., Kundu M., Kim D.H. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 2009, 20:1992-2003.
20. Jung C.H., Ro S.H., Cao J., Otto N.M., Kim D.H. mTOR regulation of autophagy. FEBS Lett. 2010, 584:1287-1295.
21. Kim D.H., Sarbassov D.D., Ali S.M., King J.E., Latek R.R., Erdjument-Bromage H., Tempst P., Sabatini D.M. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 2002, 110:163-175.
22. Kim E., Goraksha-Hicks P., Li L., Neufeld T.P., Guan K.L. Regulation of TORC1 by Rag GTPases in nutrient response. Nat. Cell Biol. 2008, 10:935-945.
23. Loewith R., Jacinto E., Wullschleger S., Lorberg A., Crespo J.L., Bonenfant D., Oppliger W., Jenoe P., Hall M.N. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 2002, 10:457-468.
24. Mizushima N., Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007, 3:542-545.
25. Musacchio A., Saraste M., Wilmanns M. High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat. Struct. Biol. 1994, 1:546-551.
26. Narita M., Young A.R., Arakawa S., Samarajiwa S.A., Nakashima T., Yoshida S., Hong S., Berry L.S., Reichelt S., Ferreira M., et al. Spatial coupling of mTOR and autophagy augments secretory phenotypes. Science 2011, 332:966-970.
27. Pan C., Gnad F., Olsen J.V., Mann M. Quantitative phosphoproteome analysis of a mouse liver cell line reveals specificity of phosphatase inhibitors. Proteomics 2008, 8:4534-4546.
28. Panchamoorthy G., Fukazawa T., Stolz L., Payne G., Reedquist K., Shoelson S., Songyang Z., Cantley L., Walsh C., Band H. Physical and functional interactions between SH2 and SH3 domains of the Src family protein tyrosine kinase p59fyn. Mol. Cell. Biol. 1994, 14:6372-6385.
29. Sancak Y., Peterson T.R., Shaul Y.D., Lindquist R.A., Thoreen C.C., Bar-Peled L., Sabatini D.M. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 2008, 320:1496-1501.
30. Sancak Y., Bar-Peled L., Zoncu R., Markhard A.L., Nada S., Sabatini D.M. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010, 141:290-303.
31. Sekiguchi T., Hirose E., Nakashima N., Ii M., Nishimoto T. Novel G proteins, Rag C and Rag D, interact with GTP-binding proteins, Rag A and Rag B. J. Biol. Chem. 2001, 276:7246-7257.
32. Selman C., Tullet J.M., Wieser D., Irvine E., Lingard S.J., Choudhury A.I., Claret M., Al-Qassab H., Carmignac D., Ramadani F., et al. Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 2009, 326:140-144.
33. Shamji A.F., Nghiem P., Schreiber S.L. Integration of growth factor and nutrient signaling: implications for cancer biology. Mol. Cell 2003, 12:271-280.
34. Tosoni D., Puri C., Confalonieri S., Salcini A.E., De Camilli P., Tacchetti C., Di Fiore P.P. TTP specifically regulates the internalization of the transferrin receptor. Cell 2005, 123:875-888.
35. Um S.H., Frigerio F., Watanabe M., Picard F., Joaquin M., Sticker M., Fumagalli S., Allegrini P.R., Kozma S.C., Auwerx J., Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 2004, 431:200-205.
36. Vander Haar E., Lee S.I., Bandhakavi S., Griffin T.J., Kim D.H. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 2007, 9:316-323.
37. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
38. Yan L., Mieulet V., Burgess D., Findlay G.M., Sully K., Procter J., Goris J., Janssens V., Morrice N.A., Lamb R.F. PP2A T61 epsilon is an inhibitor of MAP4K3 in nutrient signaling to mTOR. Mol. Cell 2010, 37:633-642.
39. Zoncu R., Bar-Peled L., Efeyan A., Wang S., Sancak Y., Sabatini D.M. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H-ATPase. Science 2011, 334:678-683.