Control of mTORC1 signaling by the Opitz syndrome protein MID1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 21, 2011, Pages 8680-8685

  Liu, Enbo ^a   Knutzen, Christine A ^a   Krauss, Sybille ^b,c   Schweiger, Susann ^b,d   Chiang, Gary G ^a  

^a BURNHAM INSTITUTE   (United States)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Proteasome mediated degradation; Ubiquitin ligase

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; NEU DIFFERENTIATION FACTOR; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEASOME; PROTEIN MID1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL SIZE; DOWN REGULATION; ENZYME DEGRADATION; GENE MUTATION; OPITZ SYNDROME; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

CELL SIZE; CELLS, CULTURED; ESOPHAGUS; HUMANS; HYPERTELORISM; HYPOSPADIAS; MICROTUBULE PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; PROTEINS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 79957722643     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1100131108     Document Type: Article

References (55)

1. Schweiger S, Schneider R (2003) The MID1/PP2A complex: A key to the pathogenesis of Opitz BBB/G syndrome. Bioessays 25:356-366. (Pubitemid 36433182)
2. Meroni G, Diez-Roux G (2005) TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. Bioessays 27:1147-1157.
3. Trockenbacher A, et al. (2001) MID1, mutated in Opitz syndrome, encodes an ubiquitin ligase that targets phosphatase 2A for degradation. Nat Genet 29:287-294. (Pubitemid 33096453)
4. Cainarca S, Messali S, Ballabio A, Meroni G (1999) Functional characterization of the Opitz syndrome gene product (midin): Evidence for homodimerization and association with microtubules throughout the cell cycle. Hum Mol Genet 8:1387-1396. (Pubitemid 29374071)
5. Bork P, Holm L, Sander C (1994) The immunoglobulin fold. Structural classification, sequence patterns and common core. J Mol Biol 242:309-320.
6. Woo JS, Suh HY, Park SY, Oh BH (2006) Structural basis for protein recognition by B30.2/SPRY domains. Mol Cell 24:967-976.
7. Schweiger S, et al. (1999) The Opitz syndrome gene product, MID1, associates with microtubules. Proc Natl Acad Sci USA 96:2794-2799. (Pubitemid 29148797)
8. Liu J, Prickett TD, Elliott E, Meroni G, Brautigan DL (2001) Phosphorylation and microtubule association of the Opitz syndrome protein mid-1 is regulated by protein phosphatase 2A via binding to the regulatory subunit alpha 4. Proc Natl Acad Sci USA 98:6650-6655. (Pubitemid 32538271)
9. Aranda-Orgillés B, et al. (2008) The Opitz syndrome gene product MID1 assembles a microtubule-associated ribonucleoprotein complex. Hum Genet 123:163-176.
10. Chiang GG, Abraham RT (2007) Targeting the mTOR signaling network in cancer. Trends Mol Med 13:433-442. (Pubitemid 47570021)
11. Zoncu R, Efeyan A, Sabatini DM (2011) mTOR: From growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12:21-35.
12. Kapahi P, et al. (2010) With TOR, less is more: A key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab 11:453-465.
13. Nojima H, et al. (2003) The mammalian target of rapamycin (mTOR) partner, raptor, binds the mTOR substrates p70 S6 kinase and 4E-BP1 through their TOR signaling (TOS) motif. J Biol Chem 278:15461-15464. (Pubitemid 36799651)
14. Schalm SS, Fingar DC, Sabatini DM, Blenis J (2003) TOS motif-mediated raptor binding regulates 4E-BP1 multisite phosphorylation and function. Curr Biol 13:797-806. (Pubitemid 36573247)
15. Katiyar S, et al. (2009) REDD1, an inhibitor of mTOR signalling, is regulated by the CUL4A-DDB1 ubiquitin ligase. EMBO Rep 10:866-872.
16. Hu J, et al. (2008) WD40 protein FBW5 promotes ubiquitination of tumor suppressor TSC2 by DDB1-CUL4-ROC1 ligase. Genes Dev 22:866-871. (Pubitemid 351482839)
17. DeYoung MP, Horak P, Sofer A, Sgroi D, Ellisen LW (2008) Hypoxia regulates TSC1/2-mTOR signaling and tumor suppression through REDD1-mediated 14-3-3 shuttling. Genes Dev 22:239-251.
18. Leicht M, Simm A, Bertsch G, Hoppe J (1996) Okadaic acid induces cellular hypertrophy in AKR-2B fibroblasts: Involvement of the p70S6 kinase in the onset of protein and rRNA synthesis. Cell Growth Differ 7:1199-1209. (Pubitemid 26360700)
19. Lin TA, Lawrence JC, Jr. (1997) Control of PHAS-I phosphorylation in 3T3-L1 adipocytes: Effects of inhibiting protein phosphatases and the p70S6K signalling pathway. Diabetologia 40(Suppl 2):S18-S24.
20. Hara K, et al. (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. (Pubitemid 28319170)
21. Peterson RT, Desai BN, Hardwick JS, Schreiber SL (1999) Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycinassociated protein. Proc Natl Acad Sci USA 96:4438-4442. (Pubitemid 29190354)
22. Krause U, Bertrand L, Hue L (2002) Control of p70 ribosomal protein S6 kinase and acetyl-CoA carboxylase by AMP-activated protein kinase and protein phosphatases in isolated hepatocytes. Eur J Biochem 269:3751-3759. (Pubitemid 34989124)
23. Eichhorn PJ, Creyghton MP, Bernards R (2009) Protein phosphatase 2A regulatory subunits and cancer. Biochim Biophys Acta 1795:1-15.
24. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J (2002) Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 16:1472-1487. (Pubitemid 34686329)
25. Urano J, et al. (2007) Point mutations in TOR confer Rheb-independent growth in fission yeast and nutrient-independent mammalian TOR signaling in mammalian cells. Proc Natl Acad Sci USA 104:3514-3519. (Pubitemid 46364190)
26. Cheatham L, Monfar M, Chou MM, Blenis J (1995) Structural and functional analysis of pp70S6k. Proc Natl Acad Sci USA 92:11696-11700.
27. Dowling RJ, et al. (2010) mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328:1172-1176.
28. Wang X, et al. (2007) NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 128:129-139. (Pubitemid 46048884)
29. Suizu F, et al. (2009) The E3 ligase TTC3 facilitates ubiquitination and degradation of phosphorylated Akt. Dev Cell 17:800-810.
30. Chong-Kopera H, et al. (2006) TSC1 stabilizes TSC2 by inhibiting the interaction between TSC2 and the HERC1 ubiquitin ligase. J Biol Chem 281:8313-8316. (Pubitemid 43847930)
31. Panasyuk G, Nemazanyy I, Filonenko V, Gout I (2008) Ribosomal protein S6 kinase 1 interacts with and is ubiquitinated by ubiquitin ligase ROC1. Biochem Biophys Res Commun 369:339-343.
32. Mao JH, et al. (2008) FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression. Science 321:1499-1502.
33. Di Como CJ, Arndt KT (1996) Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev 10:1904-1916. (Pubitemid 26281685)
34. Schmidt A, Beck T, Koller A, Kunz J, Hall MN (1998) The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J 17:6924-6931. (Pubitemid 28550286)
35. Beck T, Schmidt A, Hall MN (1999) Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J Cell Biol 146:1227-1238.
36. Jacinto E, Guo B, Arndt KT, Schmelzle T, Hall MN (2001) TIP41 interacts with TAP42 and negatively regulates the TOR signaling pathway. Mol Cell 8:1017-1026.
37. Smetana JH, Zanchin NI (2007) Interaction analysis of the heterotrimer formed by the phosphatase 2A catalytic subunit, alpha4 and the mammalian ortholog of yeast Tip41 (TIPRL). FEBS J 274:5891-5904. (Pubitemid 350064027)
38. McConnell JL, Gomez RJ, McCorvey LR, Law BK, Wadzinski BE (2007) Identification of a PP2A-interacting protein that functions as a negative regulator of phosphatase activity in the ATM/ATR signaling pathway. Oncogene 26:6021-6030. (Pubitemid 47373801)
39. Yoo SJ, et al. (2008) The alpha4-containing form of protein phosphatase 2A in liver and hepatic cells. J Cell Biochem 105:290-300.
40. Hahn K, et al. (2010) PP2A regulatory subunit PP2A-B′ counteracts S6K phosphorylation. Cell Metab 11:438-444.
41. Grinthal A, Adamovic I, Weiner B, Karplus M, Kleckner N (2010) PR65, the HEAT-repeat scaffold of phosphatase PP2A, is an elastic connector that links force and catalysis. Proc Natl Acad Sci USA 107:2467-2472.
42. Xu Y, Chen Y, Zhang P, Jeffrey PD, Shi Y (2008) Structure of a protein phosphatase 2A holoenzyme: Insights into B55-mediated Tau dephosphorylation. Mol Cell 31:873-885.
43. Panasyuk G, et al. (2009) mTORbeta splicing isoform promotes cell proliferation and tumorigenesis. J Biol Chem 284:30807-30814.
44. Chiang GG, Abraham RT (2005) Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J Biol Chem 280:25485-25490. (Pubitemid 40962253)
45. Wang L, Lawrence JC, Jr., Sturgill TW, Harris TE (2009) Mammalian target of rapamycin complex 1 (mTORC1) activity is associated with phosphorylation of raptor by mTOR. J Biol Chem 284:14693-14697.
46. Foster KG, et al. (2010) Regulation of mTOR complex 1 (mTORC1) by raptor Ser863 and multisite phosphorylation. J Biol Chem 285:80-94.
47. Acosta-Jaquez HA, et al. (2009) Site-specific mTOR phosphorylation promotes mTORC1-mediated signaling and cell growth. Mol Cell Biol 29:4308-4324.
48. Gwinn DM, Asara JM, Shaw RJ (2010) Raptor is phosphorylated by cdc2 during mitosis. PLoS ONE 5:e9197.
49. Yip CK, Murata K, Walz T, Sabatini DM, Kang SA (2010) Structure of the human mTOR complex I and its implications for rapamycin inhibition. Mol Cell 38:768-774.
50. Carracedo A, Baselga J, Pandolfi PP (2008) Deconstructing feedback-signaling networks to improve anticancer therapy with mTORC1 inhibitors. Cell Cycle 7:3805-3809.
51. Kladney RD, et al. (2010) Tuberous sclerosis complex 1: An epithelial tumor suppressor essential to prevent spontaneous prostate cancer in aged mice. Cancer Res 70:8937-8947.
52. Liu L, et al. (2010) Rapamycin inhibits cytoskeleton reorganization and cell motility by suppressing RhoA expression and activity. J Biol Chem 285:38362-38373.
53. Gulhati P, et al. (2011) mTORC1 and mTORC2 regulate EMT, motility and metastasis of colorectal cancer via RhoA and Rac1 signaling pathways. Cancer Res, 10.1158/0008-5472.
54. Chiang GG, Abraham RT (2004) Determination of the catalytic activities of mTOR and other members of the phosphoinositide-3-kinase-related kinase family. Methods Mol Biol 281:125-141.
55. Kalejta RF, Brideau AD, Banfield BW, Beavis AJ (1999) An integral membrane green fluorescent protein marker, Us9-GFP, is quantitatively retained in cells during propidium iodide-based cell cycle analysis by flow cytometry. Exp Cell Res 248:322-328. (Pubitemid 29393954)