Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response

PLoS Biology

Volumn 4, Issue 12, 2006, Pages 2311-2324

  Bernales, Sebastián ^a   McDonald, Kent L ^b   Walter, Peter ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE; ATG8 PROTEIN, S CEREVISIAE; GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CELL SURVIVAL; CELL VACUOLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FLUORESCENCE MICROSCOPY; MITOCHONDRION; NONHUMAN; PEROXISOME; STEADY STATE; YEAST CELL; METABOLISM; PHAGOSOME; PHYSIOLOGY; PROTEIN FOLDING; STRESS; TISSUE DISTRIBUTION; ULTRASTRUCTURE; YEAST;

AUTOPHAGY; CELL SURVIVAL; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; PHAGOSOMES; PROTEIN FOLDING; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS; TISSUE DISTRIBUTION; YEASTS;

EID: 33845480131     PISSN: 15457885     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0040423     Document Type: Article

References (82)

1. Wickner W, Schekman R (2005) Protein translocation across biological membranes. Science 310: 1452-1456.
2. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191.
3. McCracken AA, Brodsky JL (2005) Recognition and delivery of ERAD substrates to the proteasome and alternative paths for cell survival. Curr Top Microbiol Immunol 300: 17-40.
4. Ron D (2002) Translational control in the endoplasmic reticulum stress response. J Clin Invest 110: 1383-1388.
5. van Anken E, Braakman I (2005) Versatility of the endoplasmic reticulum protein folding factory. Crit Rev Biochem Mol Biol 40: 191-228.
6. Bernales S, Papa FR, Walter P (2006) Intracellular signaling by the unfolded protein response. Annu Rev Cell Dev Biol 22 : 487-508.
7. Cox JS, Shamu CE, Walter P (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73: 1197-1206.
8. Mori K, Ma W, Gething MJ, Sambrook J (1993) A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74: 743-756.
9. Credle JJ, Finer-Moore JS, Papa FR, Stroud RM, Walter P (2005) On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc Natl Acad Sci U S A 102: 18773-18784.
10. Shamu CE, Walter P (1996) Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J 15: 3028-3039.
11. Sidrauski C, Walter P (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90: 1031-1039.
12. Kawahara T, Yanagi H, Yura T, Mori K (1997) Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol Biol Cell 8: 1845-1862.
13. Cox JS, Walter P (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391-404.
14. Mori K, Kawahara T, Yoshida H, Yanagi H, Yura T (1996) Signalling from endoplasmic reticulum to nucleus: Transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1: 803-817.
15. Shen X, Ellis RE, Lee K, Liu CY, Yang K, et al. (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107: 893-903.
16. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
17. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96.
18. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, et al. (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258.
19. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, et al. (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6: 1355-1364.
20. Yoshida H, Haze K, Yanagi H, Yura T, Mori K (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 273: 33741-33749.
21. Li M, Baumeister P, Roy B, Phan T, Foti D, et al. (2000) ATF6 as a transcription activator of the endoplasmic reticulum stress element: Thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol Cell Biol 20: 5096-5106.
22. Kokame K, Kato H, Miyata T (2001) Identification of ERSE-II, a new cis-acting element responsible for the ATF6-dependent mammalian unfolded protein response. J Biol Chem 276: 9199-9205.
23. Okada T, Yoshida H, Akazawa R, Negishi M, Mori K (2002) Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 366: 585-594.
24. Leber JH, Bernales S, Walter P (2004) IRE1-independent gain control of the unfolded protein response. PLoS Biol 2: E235. DOI: 10.1371/journal.pbio. 0020235
25. Meusser B, Hirsch C, Jarosch E, Sommer T (2005) ERAD: The long road to destruction. Nat Cell Biol 7: 766-772.
26. Romisch K (2005) Endoplasmic reticulum-associated degradation. Annu Rev Cell Dev Biol 21: 435-456.
27. Yorimitsu T, Klionsky DJ (2005) Autophagy: Molecular machinery for self-eating. Cell Death Differ 12: 1542-1552.
28. Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333: 169-174.
29. Thumm M, Egner R, Koch B, Schlumpberger M, Straub M, et al. (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 349: 275-280.
30. Harding TM, Morano KA, Scott SV, Klionsky DJ (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 131: 591-602.
31. Yuan W, Tuttle DL, Shi YJ, Ralph GS, Dunn WA Jr. (1997) Glucose-induced microautophagy in Pichia pastoris requires the alpha-subunit of phosphofructokinase. J Cell Sci 110 (Pt 16): 1935-1945.
32. Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 119: 301-311.
33. Leao-Helder AN, Krikken AM, Gellissen G, van der Klei IJ, Veenhuis M, et al. (2004) Atg21p is essential for macropexophagy and microautophagy in the yeast Hansenula polymorpha. FEBS Lett 577: 491-495.
34. Hamasaki M, Noda T, Baba M, Ohsumi Y (2005) Starvation triggers the delivery of the endoplasmic reticulum to the vacuole via autophagy in yeast. Traffic 6: 56-65.
35. Cuervo AM (2004) Autophagy: In sickness and in health. Trends Cell Biol 14: 70-77.
36. Hamasaki M, Noda T, Ohsumi Y (2003) The early secretory pathway contributes to autophagy in yeast. Cell Struct Funct 28: 49-54.
37. Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, et al. (2001) Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 12: 3690-3702.
38. Reggiori F, Wang CW, Nair U, Shintani T, Abeliovich H, et al. (2004) Early stages of the secretory pathway, but not endosomes, are required for Cvt vesicle and autophagosome assembly in Saccharomyces cerevisiae. Mol Biol Cell 15: 2189-2204.
39. Dunn WA Jr., Cregg JM, Kiel JA, van der Klei IJ, Oku M, et al. (2005) Pexophagy: The selective autophagy of peroxisomes. Autophagy 1: 75-83.
40. Kundu M, Thompson CB (2005) Macroautophagy versus mitochondrial autophagy: A question of fate? Cell Death Differ 12: 1484-1489.
41. Harding TM, Hefner-Gravink A, Thumm M, Klionsky DJ (1996) Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J Biol Chem 271: 17621-17624.
42. Scott SV, Hefner-Gravink A, Morano KA, Noda T, Ohsumi Y, et al. (1996) Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc Natl Acad Sci U S A 93: 12304-12308.
43. Baba M, Osumi M, Scott SV, Klionsky DJ, Ohsumi Y (1997) Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J Cell Biol 139: 1687-1695.
44. Scott SV, Baba M, Ohsumi Y, Klionsky DJ (1997) Aminopeptidase I is targeted to the vacuole by a nonclassical vesicular mechanism. J Cell Biol 138: 37-44.
45. McDonald K (1999) High-pressure freezing for preservation of high resolution fine structure and antigenicity for immunolabeling. Methods Mol Biol 117: 77-97.
46. Baba M, Osumi M, Ohsumi Y (1995) Analysis of the membrane structures involved in autophagy in yeast by freeze-replica method. Cell Struct Funct 20: 465-471.
47. Baba M, Takeshige K, Baba N, Ohsumi Y (1994) Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J Cell Biol 124: 903-913.
48. Walther P, Ziegler A (2002) Freeze substitution of high-pressure frozen samples: The visibility of biological membranes is improved when the substitution medium contains water. J Microsc 208: 3-10.
49. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
50. Niwa M, Patil CK, DeRisi J, Walter P (2005) Genome-scale approaches for discovering novel nonconventional splicing substrates of the Ire1 nuclease. Genome Biol 6: R3.
51. Papa FR, Zhang C, Shokat K, Walter P (2003) Bypassing a kinase activity with an ATP-competitive drug. Science 302: 1533-1537.
52. Huang WP, Scott SV, Kim J, Klionsky DJ (2000) The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J Biol Chem 275: 5845-5851.
53. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, et al. (1999) Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 147: 435-446.
54. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, et al. (2000) A ubiquitin-like system mediates protein lipidation. Nature 408: 488-492.
55. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, et al. (2000) The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 151: 263-276.
56. Reggiori F, Tucker KA, Stromhaug PE, Klionsky DJ (2004) The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 6: 79-90.
57. Suzuki K, Kamada Y, Ohsumi Y (2002) Studies of cargo delivery to the vacuole mediated by autophagosomes in Saccharomyces cerevisiae. Dev Cell 3: 815-824.
58. Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, et al. (2001) The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J 20: 5971-5981.
59. Kim J, Huang WP, Klionsky DJ (2001) Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J Cell Biol 152: 51-64.
60. Shintani T, Klionsky DJ (2004) Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J Biol Chem 279: 29889-29894.
61. Schroder M, Chang JS, Kaufman RJ (2000) The unfolded protein response represses nitrogen-starvation induced developmental differentiation in yeast. Genes Dev 14: 2962-2975.
62. Suzuki K, Noda T, Ohsumi Y (2004) Interrelationships among Atg proteins during autophagy in Saccharomyces cerevisiae. Yeast 21: 1057-1065.
63. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, et al. (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150: 1507-1513.
64. Lang T, Reiche S, Straub M, Bredschneider M, Thumm M (2000) Autophagy and the cvt pathway both depend on AUT9. J Bacteriol 182: 2125-2133.
65. Mizushima N, Noda T, Ohsumi Y (1999) Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J 18: 3888-3896.
66. Yorimitsu T, Klionsky DJ (2005) Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol Biol Cell 16: 1593-1605.
67. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee AH, Qian SB, et al. (2004) XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21: 81-93.
68. Sriburi R, Jackowski S, Mori K, Brewer JW (2004) XBP1: A link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J Cell Biol 167: 35-41.
69. Kruse KB, Brodsky JL, McCracken AA (2006) Characterization of an ERAD gene as VPS30/ATG6 reveals two alternative and functionally distinct protein quality control pathways: One for soluble Z variant of human alpha-1 proteinase inhibitor (A1PiZ) and another for aggregates of A1PiZ. Mol Biol Cell 17: 203-212.
70. Feldman D, Swarm RL, Becker J (1980) Elimination of excess smooth endoplasmic reticulum after phenobarbital administration. J Histochem Cytochem 28: 997-1006.
71. Chin DJ, Luskey KL, Anderson RG, Faust JR, Goldstein JL, et al. (1982) Appearance of crystalloid endoplasmic reticulum in compactin-resistant Chinese hamster cells with a 500-fold increase in 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Proc Natl Acad Sci U S A 79: 1185-1189.
72. Orci L, Brown MS, Goldstein JL, Garcia-Segura LM, Anderson RG (1984) Increase in membrane cholesterol: A possible trigger for degradation of HMG CoA reductase and crystalloid endoplasmic reticulum in UT-1 cells. Cell 36: 835-845.
73. Farre JC, Subramani S (2004) Peroxisome turnover by micropexophagy: An autophagy-related process. Trends Cell Biol 14: 515-523.
74. Mijaljica D, Prescott M, Devenish RJ (2007) Different fates of mitochondria: Alternative ways for degradation? Autophagy 3. Online ISSN: 1554-8635
75. Bellu AR, Kiel JA (2003) Selective degradation of peroxisomes in yeasts. Microsc Res Tech 61: 161-170.
76. Ng DT, Spear ED, Walter P (2000) The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J Cell Biol 150: 77-88.
77. Juhasz G, Neufeld TP (2006) Autophagy: A forty-year search for a missing membrane source. PLoS Biol 4: e36. DOI: 10.1371/journal.pbio.0040036
78. Teichert U, Mechler B, Muller H, Wolf DH (1989) Lysosomal (vacuolar) proteinases of yeast are essential catalysts for protein degradation, differentiation, and cell survival. J Biol Chem 264: 16037-16045.
79. Yorimitsu T, Nair U, Yang Z, Klionsky DJ (2006) Endoplasmic Reticulum stress triggers autophagy. J Biol Chem 281: 30299-30304.
80. Ogata M, Hino SI, Saito A, Morikawa K, Kondo S, et al. (2006) Autophagy is activated for cell survival after ER stress. Mol Cell Biol. E-pub 9 October 2006.
81. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
82. Heiman MG, Walter P (2000) Prm1p, a pheromone-regulated multi-spanning membrane protein, facilitates plasma membrane fusion during yeast mating. J Cell Biol 151: 719-730.