Apg10p, a novel protein-conjugating enzyme essential for autophagy in yeast

EMBO Journal

Volumn 18, Issue 19, 1999, Pages 5234-5241

  Shintani, Takahiro ^a   Mizushima, Noboru ^a   Ogawa, Yoko ^a,b   Matsuura, Akira ^a,c   Noda, Takeshi ^a   Ohsumi, Yoshinori ^a  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Autophagy; Protein conjugating enzyme; Protein conjugation; Saccharomyces cerevisiae

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINOPEPTIDASE I; ENZYME; FUNGAL PROTEIN; UBIQUITIN;

ARTICLE; AUTOPHAGY; CONJUGATION; CONTROLLED STUDY; DRUG HYDROLYSIS; GENE SEQUENCE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST CELL;

AMINO ACID SEQUENCE; AUTOPHAGY; BASE SEQUENCE; CLONING, MOLECULAR; CYSTEINE; DNA PRIMERS; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 0033214582     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.19.5234     Document Type: Article

References (58)

1. Adams, A., Gottschling, D.E., Kaiser, C.A. and Stearns, T. (1998) Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Baba, M., Takeshige, K., Baba, N. and Ohsumi, Y. (1994) Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J. Cell Biol., 124, 903-913.
3. Baba, M., Osumi, M. and Ohsumi, Y. (1995) Analysis of the membrane structures involved in autophagy in yeast by freeze-replica method. Cell Struct. Funct., 20, 465-471.
4. Baba, M., Osumi, M., Scott, S.V., Klionsky, D.J. and Ohsumi, Y. (1997) Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J. Cell Biol., 139, 1687-1695.
5. Bonifacino, J.S. and Weissman, AM. (1998) Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu. Rev. Cell Dev. Biol., 14, 19-57.
6. Ciechanover, A. (1998) The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J., 17, 7151-7160.
7. Desterro, J.M., Rodriguez, M.S. and Hay, R.T. (1998) SUMO-1 modification of 1κBα inhibits NF-κB activation. Mol. Cell, 2, 233-239.
8. Desterro, J.M., Rodriguez, M.S., Kemp, G.D. and Hay, R.T. (1999) Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem., 274, 10618-10624.
9. Duprez, E. et al. (1999) SUMO-1 modification of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation. J. Cell Sci., 112, 381-393.
10. Funakoshi, T., Matsuura, A., Noda, T. and Ohsumi, Y. (1997) Analyses of APG13 gene involved in autophagy in yeast, Saccharomyces cerevisiae. Gene, 192, 207-213.
11. Gong, L. and Yeh, E.T.H. (1999) Identification of the activating and conjugating enzymes of the NEDD8 conjugation pathway. J. Biol. Chem., 274, 12036-12042.
12. Gong, L., Kamitani, T., Fujise, K., Caskey, L.S. and Yeh, E.T.H. (1997) Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J. Biol. Chem., 272, 28198-28201.
13. Gong, L., Li, B., Millas, S. and Yeh, E.T.H. (1999) Molecular cloning and characterization of human AOS1 and UBA2, components of the sentrin-activating enzyme complex. FEBS Lett., 448, 185-189.
14. Haas, A.L. and Siepmann, T.J. (1997) Pathways of ubiquitin conjugation. FASEB J., 11, 1257-1268.
15. Harding, T.M., Hefner-Gravink, A., Thumm, M. and Klionsky, D.J. (1996) Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J. Biol. Chem., 271, 17621-17624.
16. Hershko, A. and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem., 67, 425-479.
17. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene, 77, 51-59.
18. Hochstrasser, M. (1998) There's the Rub: a novel ubiquitin-like modification linked to cell cycle regulation. Genes Dev., 12, 901-907.
19. Irie, K., Takase, M., Lee, K.S., Levin, D.E., Araki, H., Matsumoto, K. and Oshima, Y. (1993) MKK1 and MKK2, which encode Saccharomyces cerevisiae mitogen-activated protein kinase-kinase homologs, function in the pathway mediated by protein kinase C. Mol. Cell. Biol., 13, 3076-3083.
20. James, P., Halladay, J. and Craig, E.A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics, 144, 1425-1436.
21. Johnson, E.S. and Blobel, G. (1997) Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem., 272, 26799-26802.
22. Johnson, E.S., Schwienhorst, I., Dohmen, R.J. and Blobel, G. (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J., 16, 5509-5519.
23. Johnson, P.R. and Hochstrasser, M. (1997) SUMO-1: ubiquitin gains weight. Trends Cell Biol., 7, 408-413.
24. Jones, J.S. and Prakash, L. (1990) Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast, 6, 363-366.
25. Kametaka, S., Okano, T., Ohsumi, M. and Ohsumi, Y. (1998) Apg14p and Apg6/Vps30p form a protein complex essential for autophagy in the yeast, Saccharomyces cerevisiae. J. Biol. Chem., 273, 22284-22291.
26. Kamitani, T., Kito, K., Nguyen, H.P. and Yeh, E.T.H. (1997) Characterization of NEDD8, a developmentally down-regulated ubiquitin-like protein. J. Biol. Chem., 272, 28557-28562.
27. Kamitani, T., Nguyen, H.P., Kito, K., Fukuda-Kamitani, T. and Yeh, E.T.H. (1998) Covalent modification of PML by the sentrin family of ubiquitin-like proteins. J. Biol. Chem., 273, 3117-3120.
28. Kim, J., Dalton, V.M., Eggerton, K.P., Scott, S.V. and Klionsky, D.J. (1999) Apg7p/Cvt2p is required for the cytoplasm-to-vacuole targeting, macroautophagy and peroxisome degradation pathways. Mol. Biol. Cell, 10, 1337-1351.
29. Cdc4 complex. Genes Dev., 12, 914-926.
30. Lee, G.W., Melchior, F., Matunis, M.J., Mahajan, R., Tian, Q. and Anderson, P. (1998) Modification of Ran GTPase-activating protein by the small ubiquitin-related modifier SUMO-1 requires Ubc9, an E2-type ubiquitin-conjugating enzyme homologue. J. Biol. Chem., 273, 6503-6507.
31. Li, S.J. and Hochstrasser, M. (1999) A new protease required for cell-cycle progression in yeast. Nature, 398, 246-251.
32. Liakopoulos, D., Doenges, G., Matuschewski, K. and Jentsch, S. (1998) A novel protein modification pathway related to the ubiquitin system. EMBO J., 17, 2208-2214.
33. Mahajan, R., Delphin, C., Guan, T. Gerace, L. and Melchior, F. (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell, 88, 97-107.
34. Mahajan, R., Gerace, L. and Melchior, F. (1998) Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol., 140, 259-270.
35. Matunis, M.J., Coutavas, E. and Blobel, G. (1996) A novel ubiquirin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol., 135, 1457-1470.
36. Matunis, M.J., Wu, J. and Blobel, G. (1998) SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol., 140, 499-509.
37. Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y, Ishii, T., George, M.D., Klionsky, D.J., Ohsumi, M. and Ohsumi, Y. (1998a) A protein conjugation system essential for autophagy Nature, 395, 395-398.
38. Mizushima, N., Sugita, H., Yoshimori, T. and Ohsumi, Y. (1998b) A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J. Biol. Chem., 273, 33889-33892.
39. Mizushima, N., Noda, T. and Ohsumi, Y. (1999) Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J., 18, 3888-3896.
40. Müller, S. and Dejean, A. (1999) Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol., 73, 5139-5143.
41. Müller, S., Matunis, M.J. and Dejean, A. (1998) Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J., 17, 61-70.
42. Noda, T. and Ohsumi, Y. (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem., 273, 3963-3966.
43. Noda, T., Matsuura, A., Wada, Y. and Ohsumi, Y. (1995) Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun., 210, 126-132.
44. Okuma, T., Honda, R., Ichikawa, G., Tsumagari, N. and Yasuda, H. (1999) In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem. Biophys. Res. Commun., 254, 693-698.
45. Osaka, F., Kawasaki, H., Aida, N., Saeki, M., Chiba, T., Kawashima, S., Tanaka, K. and Kato, S. (1998) A new NEDD8-ligating system for cullin-4A. Genes Dev., 12, 2263-2268.
46. Saitoh, H., Pu, R.T. and Dasso, M. (1997) SUMO-1: wrestling with a new ubiquitin-related modifier. Trends Biochem. Sci., 22, 374-376.
47. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Schwarz, S.E., Matuschewski, K., Liakopoulos, D., Scheffner, M. and Jentsch, S. (1998) The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme. Proc. Natl Acad. Sci. USA, 95, 560-564.
49. Scott, S.V., Hefner-Gravink, A., Morano, K.A., Noda, T., Ohsumi, Y. and Klionsky, D.J. (1996) Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl Acad. Sci. USA, 93, 12304-12308.
50. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
51. Sternsdorf, T., Jensen, K. and Will, H. (1997) Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/SUMO-1. J. Cell Biol., 139, 1621-1634.
52. Sternsdorf, T., Jensen, K., Reich, B. and Will, H. (1999) The nuclear dot protein sp100, characterization of domains necessary for dimerization, subcellular localization and modification by small ubiquitin-like modifiers. J. Biol. Chem., 274, 12555-12566.
53. Takeshige, K., Baba, M., Tsuboi, S., Noda, T. and Ohsumi, Y. (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol., 119, 301-311.
54. Tanida, I., Mizushima, N., Kiyooka, M., Ohsumi, M., Ueno, T., Ohsumi, Y. and Kominami, E. (1999) Apg7p/Cvt2p: a novel protein-activating enzyme essential for autophagy. Mol. Biol. Cell, 10, 1367-1379.
55. Thumm, M, Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenhuis, M. and Wolf, D.H. (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett., 349, 275-280.
56. Tsukada, M. and Ohsumi, Y. (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett., 333, 169-174.
57. Varshavsky, A. (1997) The ubiquitin system. Trends Biochem. Sd., 22, 383-387.
58. Yuan,W., Stromhaug,P.E. and Dunn.W.A.Jr (1999) Glucose-induced autophagy of peroxisomes in Pichia pasioris requires a unique El-like protein. MoI. biol. Cell, 10, 1353-1366.