Stability of the endosomal scaffold protein lAMTOR3 depends on heterodimer assembly and proteasomal degradation

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 18228-18242

  De Araújo, Mariana E G ^a   Stasyk, Taras ^a   Taub, Nicole ^a   Ebner, Hannes L ^a   Fürst, Beatrix ^a   Filipek, Przemyslaw ^a   Weys, Sabine R ^a   Hess, Michael W ^a   Lindner, Herbert ^a   Kremser, Leopold ^a   Huber, Lukas A ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEX ASSEMBLY; ENDOSOMAL MEMBRANE; HETERO DIMERS; INTRACELLULAR PROTEINS; PROTEASOMAL DEGRADATION; PROTEASOMES; SCAFFOLD PROTEIN;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

HETERODIMER; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE; MULTIPROTEIN COMPLEX; PROTEASOME; PROTEIN LAMTOR1; PROTEIN LAMTOR2; PROTEIN LAMTOR3; PROTEIN LAMTOR4; PROTEIN LAMTOR5; RAGULATOR COMPLEX; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; EMBRYO; ENDOSOME; ENZYME DEGRADATION; HUMAN; HUMAN CELL; LYSOSOME; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; QUALITY CONTROL; SIGNAL TRANSDUCTION; UBIQUITINATION;

AND LAMTOR5 (HBXIP); LAMTOR1 (P18); LAMTOR2 (P14); LAMTOR3 (MP1); LAMTOR4 (C7ORF59); MAP KINASES (MAPKS); MTOR; PROTEIN DEGRADATION; SCAFFOLD PROTEINS; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; EMBRYO, MAMMALIAN; ENDOSOMES; FIBROBLASTS; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEINS; PROTEOLYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UBIQUITIN;

EID: 84880080614     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.349480     Document Type: Article

References (43)

1. Kolch, W. (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6, 827-837 (Pubitemid 41568732)
2. Levchenko, A., Bruck, J., and Sternberg, P. W. (2000) Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc. Natl. Acad. Sci. U.S.A. 97, 5818-5823 (Pubitemid 30367482)
3. McKay, M. M., and Morrison, D. K. (2007) Integrating signals from RTKs to ERK/MAPK. Oncogene 26, 3113-3121 (Pubitemid 46763008)
4. Brown, M. D., and Sacks, D. B. (2009) Protein scaffolds in MAP kinase signalling. Cell Signal. 21, 462-469
5. Salerno, M., Palmieri, D., Bouadis, A., Halverson, D., and Steeg, P. S. (2005) Nm23-H1 metastasis suppressor expression level influences the binding properties, stability, and function of the kinase suppressor of Ras1 (KSR1) Erk scaffold in breast carcinoma cells. Mol. Cell. Biol. 25, 1379-1388 (Pubitemid 40204915)
6. Schaeffer, H. J., Catling, A. D., Eblen, S. T., Collier, L. S., Krauss, A., and Weber, M. J. (1998) MP1. A MEK binding partner that enhances enzymatic activation of the MAP kinase cascade. Science 281, 1668-1671 (Pubitemid 28435581)
7. Teis, D., Wunderlich, W., and Huber, L. A. (2002) Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev. Cell 3, 803-814 (Pubitemid 35460781)
8. Teis, D., Taub, N., Kurzbauer, R., Hilber, D., de Araujo, M. E., Erlacher, M., Offterdinger, M., Villunger, A., Geley, S., Bohn, G., Klein, C., Hess, M. W., and Huber, L. A. (2006) p14-MP1-MEK1 signaling regulates endosomal traffic and cellular proliferation during tissue homeostasis. J. Cell Biol. 175, 861-868 (Pubitemid 44969192)
9. Bohn, G., Allroth, A., Brandes, G., Thiel, J., Glocker, E., Schäffer, A. A., Rathinam, C., Taub, N., Teis, D., Zeidler, C., Dewey, R. A., Geffers, R., Buer, J., Huber, L. A., Welte, K., Grimbacher, B., and Klein, C. (2007) A novel human primary immunodeficiency syndrome caused by deficiency of the endosomal adaptor protein p14. Nat. Med. 13, 38-45 (Pubitemid 46067384)
10. Taub, N., Nairz, M., Hilber, D., Hess, M. W., Weiss, G., and Huber, L. A. (2012) The late endosomal adaptor p14 is a macrophage host-defense factor against Salmonella infection. J. Cell Sci. 125, 2698-2708
11. Nada, S., Hondo, A., Kasai, A., Koike, M., Saito, K., Uchiyama, Y., and Okada, M. (2009) The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J. 28, 477-489
12. Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A. L., Nada, S., and Sabatini, D. M. (2010) Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290-303
13. Kurzbauer, R., Teis, D., de Araujo, M. E., Maurer-Stroh, S., Eisenhaber, F., and Clausen, T. (2004) Crystal structure of the p14/MP1 scaffolding complex. How a twin couple attaches mitogen-activated protein kinase signaling to late endosomes. Proc. Natl. Acad. Sci. U.S.A. 101, 10984-10989 (Pubitemid 38989571)
14. Bar-Peled, L., Schweitzer, L. D., Zoncu, R., and Sabatini, D. M. (2012) Ragulator is a GEF for the Rag GTPases that signal amino acid levels to mTORC1. Cell 150, 1196-1208
15. Wunderlich, W., Fialka, I., Teis, D., Alpi, A., Pfeifer, A., Parton, R. G., Lottspeich, F., and Huber, L. A. (2001) A novel 14-kilodalton protein interacts with the mitogen-activated protein kinase scaffold mp1 on a late endosomal/lysosomal compartment. J. Cell Biol. 152, 765-776 (Pubitemid 34280161)
16. Stasyk, T., Holzmann, J., Stumberger, S., Ebner, H. L., Hess, M. W., Bonn, G. K., Mechtler, K., and Huber, L. A. (2010) Proteomic analysis of endosomes from genetically modified p14/MP1 mouse embryonic fibroblasts. Proteomics 10, 4117-4127
17. Obexer, P., Geiger, K., Ambros, P. F., Meister, B., and Ausserlechner, M. J. (2007) FKHRL1-mediated expression of Noxa and Bim induces apoptosis via the mitochondria in neuroblastoma cells. Cell Death Differ. 14, 534-547
18. Glatter, T., Wepf, A., Aebersold, R., and Gstaiger, M. (2009) An integrated workflow for charting the human interaction proteome. Insights into the PP2A system. Mol. Syst. Biol. 5, 237
19. Ory, D. S., Neugeboren, B. A., and Mulligan, R. C. (1996) A stable humanderived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc. Natl. Acad. Sci. U.S.A. 93, 11400-11406 (Pubitemid 26347133)
20. Chowdary, D. R., Dermody, J. J., Jha, K. K., and Ozer, H. L. (1994) Accumulation of p53 in a mutant cell line defective in the ubiquitin pathway. Mol. Cell. Biol. 14, 1997-2003 (Pubitemid 24074596)
21. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
22. Gonzalez, L., Jr., and Scheller, R. H. (1999) Regulation of membrane trafficking. Structural insights from a Rab/effector complex. Cell 96, 755-758 (Pubitemid 29165078)
23. Connor, M. K., Kotchetkov, R., Cariou, S., Resch, A., Lupetti, R., Beniston, R. G., Melchior, F., Hengst, L., and Slingerland, J. M. (2003) CRM1/Ranmediated nuclear export of p27Kip1 involves a nuclear export signal and links p27 export and proteolysis. Mol. Biol. Cell 14, 201-213 (Pubitemid 36106030)
24. Hoshino, D., Koshikawa, N., and Seiki, M. (2011) A p27(kip1)-binding protein, p27RF-Rho, promotes cancer metastasis via activation of RhoA and RhoC. J. Biol. Chem. 286, 3139-3148
25. Thompson, W. C., Deanin, G. G., and Gordon, M. W. (1979) Intact microtubules are required for rapid turnover of carboxyl-terminal tyrosine of α-tubulin in cell cultures. Proc. Natl. Acad. Sci. U.S.A. 76, 1318-1322 (Pubitemid 9143731)
26. Bloom, J., Amador, V., Bartolini, F., DeMartino, G., and Pagano, M. (2003) Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell 115, 71-82 (Pubitemid 37255319)
27. Coulombe, P., Rodier, G., Bonneil, E., Thibault, P., and Meloche, S. (2004) N-terminal ubiquitination of extracellular signal-regulated kinase 3 and p21 directs their degradation by the proteasome. Mol. Cell. Biol. 24, 6140-6150 (Pubitemid 38891117)
28. Jin, Y., Lee, H., Zeng, S. X., Dai, M. S., and Lu, H. (2003) MDM2 promotes p21waf1/cip1 proteasomal turnover independently of ubiquitylation. EMBO J. 22, 6365-6377 (Pubitemid 37522593)
29. Touitou, R., Richardson, J., Bose, S., Nakanishi, M., Rivett, J., and Allday, M. J. (2001) A degradation signal located in the C-terminus of p21WAF1/ CIP1 is a binding site for the C8 alpha-subunit of the 20S proteasome. EMBO J. 20, 2367-2375 (Pubitemid 32452854)
30. Chen, X., Chi, Y., Bloecher, A., Aebersold, R., Clurman, B. E., and Roberts, J. M. (2004) N-Acetylation and ubiquitin-independent proteasomal degradation of p21Cip1. Mol. Cell 16, 839-847 (Pubitemid 39586541)
31. Sdek, P., Ying, H., Chang, D. L., Qiu, W., Zheng, H., Touitou, R., Allday, M. J., and Xiao, Z. X. (2005) MDM2 promotes proteasome-dependent ubiquitin-independent degradation of retinoblastoma protein. Mol. Cell 20, 699-708 (Pubitemid 41740692)
32. Wagner, S. A., Beli, P., Weinert, B. T., Nielsen, M. L., Cox, J., Mann, M., and Choudhary, C. (2011) Mol. Cell. Proteomics 10.1074/mcp.M111013284
33. Catling, A. D., Schaeffer, H. J., Reuter, C. W., Reddy, G. R., and Weber, M. J. (1995) A proline-rich sequence unique to MEK1 and MEK2 is required for raf binding and regulates MEK function. Mol. Cell. Biol. 15, 5214-5225
34. Brahma, A., and Dalby, K. N. (2007) Regulation of protein phosphorylation within the MKK1-ERK2 complex by MP1 and the MP1*P14 heterodimer. Arch. Biochem. Biophys. 460, 85-91 (Pubitemid 46482415)
35. Casar, B., Arozarena, I., Sanz-Moreno, V., Pinto, A., Agudo-Ibáñez, L., Marais, R., Lewis, R. E., Berciano, M. T., and Crespo, P. (2009) Ras subcellular localization defines extracellular signal-regulated kinase 1 and 2 substrate specificity through distinct utilization of scaffold proteins. Mol. Cell. Biol. 29, 1338-1353
36. Lunin, V. V., Munger, C., Wagner, J., Ye, Z., Cygler, M., and Sacher, M. (2004) The structure of the MAPK scaffold, MP1, bound to its partner, p14. A complex with a critical role in endosomal MAP kinase signaling. J. Biol. Chem. 279, 23422-23430 (Pubitemid 38685652)
37. Qian, C., Zhang, Q., Wang, X., Zeng, L., Farooq, A., and Zhou, M. M. (2005) Structure of the adaptor protein p14 reveals a profilin-like fold with distinct function. J. Mol. Biol. 347, 309-321 (Pubitemid 40312461)
38. Cui, Q., Sulea, T., Schrag, J. D., Munger, C., Hung, M. N., Naïm, M., Cygler, M., and Purisima, E. O. (2008) Molecular dynamics-solvated interaction energy studies of protein-protein interactions. The MP1-p14 scaffolding complex. J. Mol. Biol. 379, 787-802
39. Cyr, D. M., Höhfeld, J., and Patterson, C. (2002) Protein quality control. U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem. Sci. 27, 368-375 (Pubitemid 34756520)
40. Goldberg, A. L. (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895-899 (Pubitemid 38056882)
41. Hershko, A., and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (Pubitemid 28411135)
42. Wolf, D. H., and Hilt, W. (2004) The proteasome. A proteolytic nanomachine of cell regulation and waste disposal. Biochim. Biophys. Acta 1695, 19-31 (Pubitemid 39574965)
43. McClellan, A. J., Tam, S., Kaganovich, D., and Frydman, J. (2005) Protein quality control. Chaperones culling corrupt conformations. Nat. Cell Biol. 7, 736-741 (Pubitemid 41079041)