Ubiquitin-specific protease 19 regulates the stability of the E3 ubiquitin ligase MARCH6

Experimental Cell Research

Volumn 328, Issue 1, 2014, Pages 207-216

  Nakamura, Nobuhiro ^a   Harada, Kumi ^a   Kato, Masako ^a   Hirose, Shigehisa ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Deubiquitinating enzyme; E3 ubiquitin ligase; Endoproteolytic processing; ER associated degradation; Proteasomal degradation

Indexed keywords

MARCH6 PROTEIN; MUTANT PROTEIN; PROTEIN P97; PROTEINASE; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN SPECIFIC PROTEASE 19; UNCLASSIFIED DRUG; ABC TRANSPORTER; ABCB11 PROTEIN, HUMAN; MARCH6 PROTEIN, HUMAN; MEMBRANE PROTEIN; SMALL INTERFERING RNA; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; USP19 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOPLASM; ENZYME STABILITY; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION; ANIMAL; CELL CULTURE; CHEMISTRY; ENDOPLASMIC RETICULUM; GENETICS; HEK293 CELL LINE; IMMUNOPRECIPITATION; METABOLISM; WESTERN BLOTTING;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; CELLS, CULTURED; ENDOPEPTIDASES; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; RNA, SMALL INTERFERING; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84908028504     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.07.025     Document Type: Article

References (46)

1. Vembar S.S., Brodsky J.L. One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 2008, 9(12):944-957.
2. Hampton R.Y., Garza R.M. Protein quality control as a strategy for cellular regulation: lessons from ubiquitin-mediated regulation of the sterol pathway. Chem. Rev. 2009, 109(4):1561-1574.
3. Ye Y., Meyer H.H., Rapoport T.A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 2001, 414(6864):652-656.
4. Ye Y., Meyer H.H., Rapoport T.A. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 2003, 162(1):71-84.
5. Dai R.M., Li C.C. Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat. Cell Biol. 2001, 3(8):740-744.
6. Jarosch E., Taxis C., Volkwein C., Bordallo J., Finley D., Wolf D.H., Sommer T. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 2002, 4(2):134-139.
7. Rabinovich E., Kerem A., Frohlich K.U., Diamant N., Bar-Nun S. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell Biol. 2002, 22(2):626-634.
8. Pickart C.M., Eddins M.J. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 2004, 1695(1-3):55-72.
9. Hirsch C., Gauss R., Horn S.C., Neuber O., Sommer T. The ubiquitylation machinery of the endoplasmic reticulum. Nature 2009, 458(7237):453-460.
10. Vashist S., Ng D.T. Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J. Cell Biol. 2004, 165(1):41-52.
11. Carvalho P., Goder V., Rapoport T.A. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 2006, 126(2):361-373.
12. Denic V., Quan E.M., Weissman J.S. A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 2006, 126(2):349-359.
13. Hassink G., Kikkert M., van Voorden S., Lee S.J., Spaapen R., van Laar T., Coleman C.S., Bartee E., Fruh K., Chau V., Wiertz E. TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum. Biochem. J. 2005, 388(2):647-655.
14. Fang S., Ferrone M., Yang C., Jensen J.P., Tiwari S., Weissman A.M. The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 2001, 98(25):14422-14427.
15. Kikkert M., Doolman R., Dai M., Avner R., Hassink G., van Voorden S., Thanedar S., Roitelman J., Chau V., Wiertz E. Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J. Biol. Chem. 2004, 279(5):3525-3534.
16. Nadav E., Shmueli A., Barr H., Gonen H., Ciechanover A., Reiss Y. A novel mammalian endoplasmic reticulum ubiquitin ligase homologous to the yeast Hrd1. Biochem. Biophys. Res. Commun. 2003, 303(1):91-97.
17. Younger J.M., Chen L., Ren H.Y., Rosser M.F., Turnbull E.L., Fan C.Y., Patterson C., Cyr D.M. Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 2006, 126(3):571-582.
18. Lerner M., Corcoran M., Cepeda D., Nielsen M.L., Zubarev R., Ponten F., Uhlen M., Hober S., Grander D., Sangfelt O. The RBCC gene RFP2 (Leu5) encodes a novel transmembrane E3 ubiquitin ligase involved in ERAD. Mol. Biol. Cell 2007, 18(5):1670-1682.
19. Stagg H.R., Thomas M., van den Boomen D., Wiertz E.J., Drabkin H.A., Gemmill R.M., Lehner P.J. The TRC8 E3 ligase ubiquitinates MHC class I molecules before dislocation from the ER. J. Cell Biol. 2009, 186(5):685-692.
20. Kim H.M., Yu Y., Cheng Y. Structure characterization of the 26S proteasome. Biochim. Biophys. Acta 2011, 1809(2):67-79.
21. Wang Q., Li L., Ye Y. Inhibition of p97-dependent protein degradation by Eeyarestatin I. J. Biol. Chem. 2008, 283(12):7445-7454.
22. Wang Q., Li L., Ye Y. Regulation of retrotranslocation by p97-associated deubiquitinating enzyme ataxin-3. J. Cell Biol. 2006, 174(7):963-971.
23. Ernst R., Mueller B., Ploegh H.L., Schlieker C. The otubain YOD1 is a deubiquitinating enzyme that associates with p97 to facilitate protein dislocation from the ER. Mol. Cell 2009, 36(1):28-38.
24. Claessen J.H., Mueller B., Spooner E., Pivorunas V.L., Ploegh H.L. The transmembrane segment of a tail-anchored protein determines its degradative fate through dislocation from the endoplasmic reticulum. J. Biol. Chem. 2010, 285(27):20732-20739.
25. Blount J.R., Burr A.A., Denuc A., Marfany G., Todi S.V. Ubiquitin-specific protease 25 functions in endoplasmic reticulum-associated degradation. PLoS One 2012, 7(5):e36542.
26. Hassink G.C., Zhao B., Sompallae R., Altun M., Gastaldello S., Zinin N.V., Masucci M.G., Lindsten K. The ER-resident ubiquitin-specific protease 19 participates in the UPR and rescues ERAD substrates. EMBO Rep. 2009, 10(7):755-761.
27. Combaret L., Adegoke O.A., Bedard N., Baracos V., Attaix D., Wing S.S. USP19 is a ubiquitin-specific protease regulated in rat skeletal muscle during catabolic states. Am. J. Physiol. Endocrinol. Metab. 2005, 288(4):E693-E700.
28. Sundaram P., Pang Z., Miao M., Yu L., Wing S.S. USP19-deubiquitinating enzyme regulates levels of major myofibrillar proteins in L6 muscle cells. Am. J. Physiol. Endocrinol. Metab. 2009, 297(6):E1283-E1290.
29. Lu Y., Adegoke O.A., Nepveu A., Nakayama K.I., Bedard N., Cheng D., Peng J., Wing S.S. USP19 deubiquitinating enzyme supports cell proliferation by stabilizing KPC1, a ubiquitin ligase for p27Kip1. Mol. Cell Biol. 2009, 29(2):547-558.
30. Lu Y., Bedard N., Chevalier S., Wing S.S. Identification of distinctive patterns of USP19-mediated growth regulation in normal and malignant cells. PLoS One 2011, 6(1):e15936.
31. Ventii K.H., Wilkinson K.D. Protein partners of deubiquitinating enzymes. Biochem. J. 2008, 414(2):161-175.
32. Mei Y., Hahn A.A., Hu S., Yang X. The USP19 deubiquitinase regulates the stability of c-IAP1 and c-IAP2. J. Biol. Chem. 2011, 286(41):35380-35387.
33. Velasco K., Zhao B., Callegari S., Altun M., Liu H., Hassink G., Masucci M.G., Lindsten K. An N-terminal SIAH-interacting motif regulates the stability of the ubiquitin specific protease (USP)-19. Biochem. Biophys. Res. Commun. 2013, 433(4):390-395.
34. Nakamura N., Kimura Y., Tokuda M., Honda S., Hirose S. MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 2006, 7(10):1019-1022.
35. Schreiner P., Chen X., Husnjak K., Randles L., Zhang N., Elsasser S., Finley D., Dikic I., Walters K.J., Groll M. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 2008, 453(7194):548-552.
36. Husnjak K., Elsasser S., Zhang N., Chen X., Randles L., Shi Y., Hofmann K., Walters K.J., Finley D., Dikic I. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008, 453(7194):481-488.
37. Flierman D., Ye Y., Dai M., Chau V., Rapoport T.A. Polyubiquitin serves as a recognition signal, rather than a ratcheting molecule, during retrotranslocation of proteins across the endoplasmic reticulum membrane. J. Biol. Chem. 2003, 278(37):34774-34782.
38. Wang L., Dong H., Soroka C.J., Wei N., Boyer J.L., Hochstrasser M. Degradation of the bile salt export pump at endoplasmic reticulum in progressive familial intrahepatic cholestasis type II. Hepatology 2008, 48(5):1558-1569.
39. Altun M., Zhao B., Velasco K., Liu H., Hassink G., Paschke J., Pereira T., Lindsten K. Ubiquitin-specific protease 19 (USP19) regulates hypoxia-inducible factor 1alpha (HIF-1alpha) during hypoxia. J. Biol. Chem. 2012, 287(3):1962-1969.
40. Thrower J.S., Hoffman L., Rechsteiner M., Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19(1):94-102.
41. Bagola K., Mehnert M., Jarosch E., Sommer T. Protein dislocation from the ER. Biochim. Biophys. Acta 2011, 1808(3):925-936.
42. Huang T.T., Nijman S.M., Mirchandani K.D., Galardy P.J., Cohn M.A., Haas W., Gygi S.P., Ploegh H.L., Bernards R., D'Andrea A.D. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat. Cell. Biol. 2006, 8(4):339-347.
43. Komander D., Clague M.J., Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 2009, 10(8):550-563.
44. Zhu X., Menard R., Sulea T. High incidence of ubiquitin-like domains in human ubiquitin-specific proteases. Proteins 2007, 69(1):1-7.
45. Garcia-Ranea J.A., Mirey G., Camonis J., Valencia A. p23 and HSP20/alpha-crystallin proteins define a conserved sequence domain present in other eukaryotic protein families. FEBS Lett. 2002, 529(2-3):162-167.
46. Vugmeyster Y., Borodovsky A., Maurice M.M., Maehr R., Furman M.H., Ploegh H.L. The ubiquitin-proteasome pathway in thymocyte apoptosis: caspase-dependent processing of the deubiquitinating enzyme USP7 (HAUSP). Mol. Immunol. 2002, 39(7-8):431-441.