Proteomic analysis reveals GIT1 as a novel mTOR complex component critical for mediating astrocyte survival

Genes and Development

Volumn 30, Issue 12, 2016, Pages 1383-1388

  Smithson, Laura J ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Brain; GIT1; MTOR

Indexed keywords

BINDING PROTEIN; CASPASE 3; G PROTEIN COUPLED RECEPTOR KINASE INTERACTING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; NEUROFIBROMIN; PROTEIN KINASE B; PROTEIN P53; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR 7; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; GIT1 PROTEIN, HUMAN; GIT1 PROTEIN, MOUSE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVATION; FIBROBLAST; MOUSE; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; ANIMAL; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ASTROCYTES; CELL CYCLE PROTEINS; CELL SURVIVAL; CELLS, CULTURED; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GTPASE-ACTIVATING PROTEINS; HEK293 CELLS; HUMANS; MICE; NEUROFIBROMIN 1; PROTEIN BINDING; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; TOR SERINE-THREONINE KINASES;

EID: 84975742278     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.279661.116     Document Type: Article

References (40)

1. Bagrodia S, Bailey D, Lenard Z, Hart M, Guan JL, Premont RT, Taylor SJ, Cerione RA. 1999. A tyrosine-phosphorylated protein that binds to an important regulatory region on the cool family of p21-activated kinase-binding proteins. J Biol Chem 274: 22393-22400.
2. Bajenaru ML, Zhu Y, Hedrick NM, Donahoe J, Parada LF, Gutmann DH. 2002. Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol Cell Biol 22: 5100-5113.
3. Banerjee S, Byrd JN, Gianino SM, Harpstrite SE, Rodriguez FJ, Tuskan RG, Reilly KM, Piwnica-Worms DR, Gutmann DH. 2010. The neurofibromatosis type 1 tumor suppressor controls cell growth by regulating signal transducer and activator of transcription-3 activity in vitro and in vivo. Cancer Res 70: 1356-1366.
4. Banerjee S, Crouse NR, Emnett RJ, Gianino SM, Gutmann DH. 2011. Neurofibromatosis-1 regulates mTOR-mediated astrocyte growth and glioma formation in a TSC/Rheb-independent manner. Proc Natl Acad Sci 108: 15996-16001.
5. Barbet NC, Schneider U, Helliwell SB, Stansfield I, Tuite MF, Hall MN. 1996. TOR controls translation initiation and early G1 progression in yeast. Mol Biol Cell 7: 25-42.
6. Chang JS, Su CY, Yu WH, Lee WJ, Liu YP, Lai TC, Jan YH, Yang YF, Shen CN, Shew JY, et al. 2015. GIT1 promotes lung cancer cell metastasis through modulating Rac1/Cdc42 activity and is associated with poor prognosis. Oncotarget 6: 36278-36291.
7. Claing A, Perry SJ, Achiriloaie M, Walker JK, Albanesi JP, Lefkowitz RJ, Premont RT. 2000. Multiple endocytic pathways of G protein-coupled receptors delineated by GIT1 sensitivity. Proc Natl Acad Sci 97: 1119-1124.
8. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. 2004. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 24: 200-216.
9. Fiuza M, Gonzalez-Gonzalez I, Perez-Otano I. 2013. GluN3A expression restricts spine maturation via inhibition of GIT1/Rac1 signaling. Proc Natl Acad Sci 110: 20807-20812.
10. Foster H, Coley HM, Goumenou A, Pados G, Harvey A, Karteris E. 2010. Differential expression of mTOR signalling components in drug resistance in ovarian cancer. Anticancer Res 30: 3529-3534.
11. Gingras AC, Kennedy SG, O’Leary MA, Sonenberg N, Hay N. 1998. 4EBP1, a repressor ofmRNAtranslation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev 12: 502-513.
12. Hara K, Yonezawa K, Weng QP, Kozlowski MT, Belham C, Avruch J. 1998. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem 273: 14484-14494.
13. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, Hall A, Hall MN. 2004. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6: 1122-1128.
14. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY, Huang Q, Qin J, Su B. 2006. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127: 125-137.
15. Kaul A, Toonen JA, Cimino PJ, Gianino SM, Gutmann DH. 2015. Akt-or MEK-mediated mTOR inhibition suppresses Nf1 optic glioma growth. Neuro Oncol 17: 843-853.
16. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110: 163-175.
17. Kim DH, Sarbassov DD, Ali SM, Latek RR, Guntur KV, Erdjument-Bromage H, Tempst P, Sabatini DM. 2003. GβL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol Cell 11: 895-904.
18. Lee da Y, Yeh TH, Emnett RJ, White CR, Gutmann DH. 2010. Neurofibromatosis-1 regulates neuroglial progenitor proliferation and glial differentiation in a brain region-specific manner. Genes Dev 24: 2317-2329.
19. Luo Y, Liu L, Wu Y, Singh K, Su B, Zhang N, Liu X, Shen Y, Huang S. 2015. Rapamycin inhibits mSin1 phosphorylation independently of mTORC1 and mTORC2. Oncotarget 6: 4286-4298.
20. Manabe R, Kovalenko M, Webb DJ, Horwitz AR. 2002. GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J Cell Sci 115: 1497-1510.
21. Mayer C, Zhao J, Yuan X, Grummt I. 2004. mTOR-dependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev 18: 423-434.
22. Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA, Li T, Miteva YV, Hauri S, Sardiu ME, Low TY, et al. 2013. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10: 730-736.
23. Miloslavski R, Cohen E, Avraham A, Iluz Y, Hayouka Z, Kasir J, Mudhasani R, Jones SN, Cybulski N, Ruegg MA, et al. 2014. Oxygen sufficiency controls TOP mRNA translation via the TSC-Rheb-mTOR pathway in a 4E-BP-independent manner. J Mol Cell Biol 6: 255-266.
24. Oshiro N, Takahashi R, Yoshino K, Tanimura K, Nakashima A, Eguchi S, Miyamoto T, Hara K, Takehana K, Avruch J, et al. 2007. The prolinerich Akt substrate of 40 kDa (PRAS40) is a physiological substrate of mammalian target of rapamycin complex 1. J Biol Chem 282: 20329-20339.
25. Paglin S, Lee NY, Nakar C, Fitzgerald M, Plotkin J, Deuel B, Hackett N, McMahill M, Sphicas E, Lampen N, et al. 2005. Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res 65: 11061-11070.
26. Pearce LR, Sommer EM, Sakamoto K, Wullschleger S, Alessi DR. 2011. Protor-1 is required for efficient mTORC2-mediated activation of SGK1 in the kidney. Biochem J 436: 169-179.
27. Peterson RT, Beal PA, Comb MJ, Schreiber SL. 2000. FKBP12-rapamycinassociated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J Biol Chem 275: 7416-7423.
28. Peterson TR, Laplante M, Thoreen CC, Sancak Y, Kang SA, Kuehl WM, Gray NS, Sabatini DM. 2009. DEPTORis anmTORinhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell 137: 873-886.
29. Premont RT, Claing A, Vitale N, Freeman JL, Pitcher JA, Patton WA, Moss J, Vaughan M, Lefkowitz RJ. 1998. β2-adrenergic receptor regulation by GIT1, aGprotein-coupled receptor kinase-associatedADPribosylation factor GTPase-activating protein. Proc Natl Acad Sci 95: 14082-14087.
30. Sandsmark DK, Zhang H, Hegedus B, Pelletier CL, Weber JD, Gutmann DH. 2007. Nucleophosmin mediates mammalian target of rapamycin-dependent actin cytoskeleton dynamics and proliferation in neurofibromin-deficient astrocytes. Cancer Res 67: 4790-4799.
31. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 14: 1296-1302.
32. Sekulic A, Hudson CC, Homme JL, Yin P, Otterness DM, Karnitz LM, Abraham RT. 2000. A direct linkage between the phosphoinositide 3-kinase-AKT signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells. Cancer Res 60: 3504-3513.
33. Uhlmann EJ, Li W, Scheidenhelm DK, Gau CL, Tamanoi F, Gutmann DH. 2004. Loss of tuberous sclerosis complex 1 (Tsc1) expression results in increased Rheb/S6K pathway signaling important for astrocyte cell size regulation. Glia 47: 180-188.
34. Vitale N, Patton WA, Moss J, Vaughan M, Lefkowitz RJ, Premont RT. 2000. GIT proteins, A novel family of phosphatidylinositol 3,4, 5-trisphosphate-stimulated GTPase-activating proteins for ARF6. J Biol Chem 275: 13901-13906.
35. Yin G, Haendeler J, Yan C, Berk BC. 2004. GIT1 functions as a scaffold for MEK1-extracellular signal-regulated kinase 1 and 2 activation by angiotensin II and epidermal growth factor. Mol Cell Biol 24: 875-885.
36. Yuan Y, Pan B, Sun H, Chen G, Su B, Huang Y. 2015. Characterization of Sin1 isoforms reveals an mTOR-dependent and independent function of Sin1γ. PLoS One 10: e0135017.
37. Za L, Albertinazzi C, Paris S, Gagliani M, Tacchetti C, de Curtis I. 2006. βPIX controls cell motility and neurite extension by regulating the distribution of GIT1. J Cell Sci 119: 2654-2666.
38. Zhang H, Webb DJ, Asmussen H, Niu S, Horwitz AF. 2005. A GIT1/PIX/ Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J Neurosci 25: 3379-3388.
39. Zhao ZS, Manser E, Loo TH, Lim L. 2000. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol Cell Biol 20: 6354-6363.
40. Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, Rushing EJ, Marth JD, Parada LF. 2001. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15: 859-876.