Turnover of organelles by autophagy in yeast

Current Opinion in Cell Biology

Volumn 21, Issue 4, 2009, Pages 522-530

  Farré, Jean Claude ^a   Krick, Roswitha ^b   Subramani, Suresh ^a   Thumm, Michael ^b  

^a SECTION OF MOLECULAR BIOLOGY   (United States)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY; CELL NUCLEUS; CELL ORGANELLE; CELL SURVIVAL; ENDOPLASMIC RETICULUM; EUKARYOTE; HOMEOSTASIS; MITOCHONDRION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; REVIEW; YEAST;

AUTOPHAGY; CELL NUCLEUS; FUNGI; HOMEOSTASIS; LIPIDS; MEMBRANE PROTEINS; MITOCHONDRIA; MODELS, BIOLOGICAL; ORGANELLES; PHAGOSOMES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 67949122010     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2009.04.015     Document Type: Review

References (69)

1. Mizushima N., Levine B., Cuervo A.M., and Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 451 (2008) 1069-1075
2. Levine B., and Kroemer G. Autophagy in the pathogenesis of disease. Cell 132 (2008) 27-42
3. Xie Z., and Klionsky D.J. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9 (2007) 1102-1109
4. Tsukada M., and Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333 (1993) 169-174
5. Thumm M., Egner R., Koch B., Schlumpberger M., Straub M., Veenhuis M., and Wolf D.H. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 349 (1994) 275-280
6. Klionsky D.J., Cregg J.M., Dunn W.A., Emr S.D., Sakai Y., Sandoval I.V., Sibirny A., Subramani S., Thumm M., Veenhuis M., et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell 5 (2003) 539-545
7. Ishihara N., Hamasaki M., Yokota S., Suzuki K., Kamada Y., Kihara A., Yoshimori T., Noda T., and Ohsumi Y. Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 12 (2001) 3690-3702
8. Reggiori F., Wang C.W., Nair U., Shintani T., Abeliovich H., and Klionsky D.J. Early stages of the secretory pathway, but not endosomes, are required for Cvt vesicle and autophagosome assembly in Saccharomyces cerevisiae. Mol Biol Cell 15 (2004) 2189-2204
9. Cheong H., Nair U., Geng J., and Klionsky D.J. The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol Biol Cell 19 (2008) 668-681
10. Kawamata T., Kamada Y., Kabeya Y., Sekito T., and Ohsumi Y. Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 19 (2008) 2039-2050
11. Suzuki K., Kubota Y., Sekito T., and Ohsumi Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12 (2007) 209-218
12. Cao Y., Cheong H., Song H., and Klionsky D.J. In vivo reconstitution of autophagy in Saccharomyces cerevisiae. J Cell Biol 182 (2008) 703-713. In a very elegant approach, 24 ATG-genes were consecutively deleted. This multiple knockout strain allowed the study of the assembly of defined Atg proteins at the PAS in the absence of the others.
13. Suzuki K., and Ohsumi Y. Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett 581 (2007) 2156-2161
14. Reggiori F., Tucker K.A., Stromhaug P.E., and Klionsky D.J. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 6 (2004) 79-90. The authors present for the first time the idea of a retrograde retrieval of the membrane protein, Atg9, from the PAS.
15. Reggiori F., Shintani T., Nair U., and Klionsky D.J. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 1 (2005) 101-109
16. He C., Baba M., Cao Y., and Klionsky D.J. Self-interaction is critical for Atg9 transport and function at the phagophore assembly site during autophagy. Mol Biol Cell 19 (2008) 5506-5516
17. Obara K., Sekito T., and Ohsumi Y. Assortment of phosphatidylinositol 3-kinase complexes-Atg14p directs association of complex I to the pre-autophagosomal structure in Saccharomyces cerevisiae. Mol Biol Cell 17 (2006) 1527-1539
18. Meiling-Wesse K., Barth H., Voss C., Eskelinen E.L., Epple U.D., and Thumm M. Atg21 is required for effective recruitment of Atg8 to the preautophagosomal structure during the Cvt pathway. J Biol Chem 279 (2004) 37741-37750
19. Stromhaug P.E., Reggiori F., Guan J., Wang C.W., and Klionsky D.J. Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol Biol Cell 15 (2004) 3553-3566
20. Krick R., Muehe Y., Prick T., Bremer S., Schlotterhose P., Eskelinen E.L., Millen J.I., Goldfarb D.S., and Thumm M. Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol Biol Cell 19 (2008) 4492-4505
21. Dove S.K., Piper R.C., McEwen R.K., Yu J.W., King M.C., Hughes D.C., Thuring J., Holmes A.B., Cooke F.T., Michell R.H., et al. Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J 23 (2004) 1922-1933
22. Krick R., Tolstrup J., Appelles A., Henke S., and Thumm M. The relevance of the phosphatidylinositolphosphat-binding motif FRRGT of Atg18 and Atg21 for the Cvt pathway and autophagy. FEBS Lett 580 (2006) 4632-4638
23. Obara K., Sekito T., Niimi K., and Ohsumi Y. The ATG18-ATG2 complex is recruited to autophagic membranes via PtdIns(3)P and exerts an essential function. J Biol Chem 282 (2008) 23972-23980
24. Krick R., Henke S., Tolstrup J., and Thumm M. Dissecting the localization and function of Atg18, Atg21 and Ygr223c. Autophagy 4 (2008) 896-905
25. Epple U.D., Eskelinen E.L., and Thumm M. Intravacuolar membrane lysis in Saccharomyces cerevisiae. Does vacuolar targeting of Cvt17/Aut5p affect its function?. J Biol Chem 278 (2003) 7810-7821
26. Efe J.A., Botelho R.J., and Emr S.D. Atg18 regulates organelle morphology and Fab1 kinase activity independent of its membrane recruitment by phosphatidylinositol 3,5-bisphosphate. Mol Biol Cell 18 (2007) 4232-4244
27. Mizushima N., Noda T., Yoshimori T., Tanaka Y., Ishii T., George M.D., Klionsky D.J., Ohsumi M., and Ohsumi Y. A protein conjugation system essential for autophagy. Nature 395 (1998) 395-398. This hallmark paper reports the formation of the Atg12-Atg5 conjugate by a ubiquitin-related system.
28. Geng J., and Klionsky D.J. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep 9 (2008) 859-864
29. Geng J., Baba M., Nair U., and Klionsky D.J. Quantitative analysis of autophagy-related protein stoichiometry by fluorescence microscopy. J Cell Biol 182 (2008) 129-140
30. Ichimura Y., Kirisako T., Takao T., Satomi Y., Shimonishi Y., Ishihara N., Mizushima N., Tanida I., Kominami E., Ohsumi M., et al. A ubiquitin-like system mediates protein lipidation. Nature 408 (2000) 488-492. Here conjugation of Atg8 to phosphatidylethanolamine by a ubiquitin-related system is uncovered.
31. Nakatogawa H., Ichimura Y., and Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130 (2007) 165-178. In vitro reconstitution of Atg8 lipidation points to a function of the conjugate in membrane tethering and fusion.
32. Xie Z., Nair U., and Klionsky D.J. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19 (2008) 3290-3298. This paper describes a relationship between the size of autophagosomes and the expression level of Atg8.
33. Hanada T., Noda N.N., Satomi Y., Ichimura Y., Fujioka Y., Takao T., Inagaki F., and Ohsumi Y. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 282 (2007) 37298-37302
34. Fujita N., Itoh T., Omori H., Fukuda M., Noda T., and Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 19 (2008) 2092-2100
35. Young A.R., Chan E.Y., Hu X., Kochl R., Crawshaw S.G., High S., Hailey D.W., Lippincott-Schwartz J., and Tooze S.A. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 119 (2006) 3888-3900
36. Hutchins M.U., Veenhuis M., and Klionsky D.J. Peroxisome degradation in Saccharomyces cerevisiae is dependent on machinery of macroautophagy and the Cvt pathway. J Cell Sci 112 (1999) 4079-4087
37. Sakai Y., Koller A., Rangell L.K., Keller G.A., and Subramani S. Peroxisome degradation by microautophagy in Pichia pastoris: identification of specific steps and morphological intermediates. J Cell Biol 141 (1998) 625-636
38. Veenhuis M., Douma A., Harder W., and Osumi M. Degradation and turnover of peroxisomes in the yeast Hansenula polymorpha induced by selective inactivation of peroxisomal enzymes. Arch Microbiol 134 (1983) 193-203
39. Dunn W.A., Cregg J.M., Kiel J.A., van der Klei I.J., Oku M., Sakai Y., Sibirny A.A., Stasyk O.V., and Veenhuis M. Pexophagy: the selective autophagy of peroxisomes. Autophagy 1 (2005) 75-83
40. Mukaiyama H., Baba M., Osumi M., Aoyagi S., Kato N., Ohsumi Y., and Sakai Y. Modification of a ubiquitin-like protein Paz2 conducted micropexophagy through formation of a novel membrane structure. Mol Biol Cell 15 (2004) 58-70. The authors detected by fluorescence microscopy the isolation membranes (MIPA and pexophagosome) during pexophagy, using Atg8 as a marker and studied its behaviour in this pathway.
41. Nazarko T.Y., Polupanov A.S., Manjithaya R.R., Subramani S., and Sibirny A.A. The requirement of sterol glucoside for pexophagy in yeast is dependent on the species and nature of peroxisome inducers. Mol Biol Cell 18 (2007) 106-118
42. Farré J.C., Manjithaya R., Mathewson R.D., and Subramani S. PpAtg30 tags peroxisomes for turnover by selective autophagy. Developmental Cell 14 (2008) 365-376. Represents the first description, and mechanistic insight into the role, of an organelle-specific receptor that delivers an organelle, the peroxisome, to the autophagic machinery for turnover.
43. Ano Y., Hattori T., Kato N., and Sakai Y. Intracellular ATP correlates with mode of pexophagy in Pichia pastoris. Biosci Biotechnol Biochem 69 (2005) 1527-1533
44. Kim J., Kamada Y., Stromhaug P.E., Guan J., Hefner-Gravink A., Baba M., Scott S.V., Ohsumi Y., Dunn W.A., and Klionsky D.J. Cvt9/Gsa9 functions in sequestering selective cytosolic cargo destined for the vacuole. J Cell Biol 153 (2001) 381-396
45. Ano Y., Hattori T., Oku M., Mukaiyama H., Baba M., Ohsumi Y., Kato N., and Sakai Y. A sorting nexin PpAtg24 regulates vacuolar membrane dynamics during pexophagy via binding to phosphatidylinositol-3-phosphate. Mol Biol Cell 16 (2005) 446-457
46. Monastyrska I., Kiel J.A., Krikken A.M., Komduur J.A., Veenhuis M., and van der Klei I.J. The Hansenula polymorpha ATG25 gene encodes a novel coiled-coil protein that is required for macropexophagy. Autophagy 1 (2005) 92-100
47. Schroder L.A., and Dunn W.A. PpAtg9 trafficking during micropexophagy in Pichia pastoris. Autophagy 2 (2006) 52-54
48. Stasyk O.V., Stasyk O.G., Mathewson R.D., Farre J.C., Nazarko V.Y., Krasovska O.S., Subramani S., Cregg J.M., and Sibirny A.A. Atg28, a novel coiled-coil protein involved in autophagic degradation of peroxisomes in the methylotrophic yeast Pichia pastoris. Autophagy 2 (2006) 30-38
49. Yamashita S., Oku M., Wasada Y., Ano Y., and Sakai Y. PI4P-signaling pathway for the synthesis of a nascent membrane structure in selective autophagy. J Cell Biol 173 (2006) 709-717. Describes a novel role for PtdIns4P and Pik1 in pexophagy of methanol-induced peroxisomes in P. pastoris.
50. Oku M., Warnecke D., Noda T., Muller F., Heinz E., Mukaiyama H., Kato N., and Sakai Y. Peroxisome degradation requires catalytically active sterol glucosyltransferase with a GRAM domain. EMBO J 22 (2003) 3231-3241
51. Mukaiyama H., Oku M., Baba M., Samizo T., Hammond A.T., Glick B.S., Kato N., and Sakai Y. Paz2 and 13 other PAZ gene products regulate vacuolar engulfment of peroxisomes during micropexophagy. Genes Cells 7 (2002) 75-90. Together with reference [37], this study describes the morphological steps of two different forms of pexophagy: macropexophagy and micropexophagy and the first comprehensive analysis of genes required for pexophagy.
52. Chang T., Schroder L.A., Thomson J.M., Klocman A.S., Tomasini A.J., Stromhaug P.E., and Dunn W.A. PpATG9 encodes a novel membrane protein that traffics to vacuolar membranes, which sequester peroxisomes during pexophagy in Pichia pastoris. Mol Biol Cell 16 (2005) 4941-4953
53. Fry M.R., Thomson J.M., Tomasini A.J., and Dunn W.A. Early and late molecular events of glucose-induced pexophagy in Pichia pastoris require Vac8. Autophagy 2 (2006) 280-288
54. Schroder L.A., Ortiz M.V., and Dunn W.A. The membrane dynamics of pexophagy are influenced by Sar1p in Pichia pastoris. Mol Biol Cell 19 (2008) 4888-4899. This study suggests retrograde trafficking from the pexophagosome to the ER and the participation of Sar1 in this process.
55. Roberts P., Moshitch-Moshkovitz S., Kvam E., O'Toole E., Winey M., and Goldfarb D.S. Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol Biol Cell 14 (2003) 129-141
56. Kvam E., and Goldfarb D.S. Nucleus-vacuole junctions and piecemeal microautophagy of the nucleus in S. cerevisiae. Autophagy 3 (2007) 85-92
57. Zhang Y., Qi H., Taylor R., Xu W., Liu L.F., and Jin S. The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3 (2007) 337-346
58. Priault M., Salin B., Schaeffer J., Vallette F.M., di Rago J.P., and Martinou J.C. Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ 12 (2005) 1613-1621
59. Nowikovsky K., Reipert S., Devenish R.J., and Schweyen R.J. Mdm38 protein depletion causes loss of mitochondrial K+/H+ exchange activity, osmotic swelling and mitophagy. Cell Death Differ 14 (2007) 1647-1656
60. Campbell C.L., and Thorsness P.E. Escape of mitochondrial DNA to the nucleus in yme1 yeast is mediated by vacuolar-dependent turnover of abnormal mitochondrial compartments. J Cell Sci 111 (1998) 2455-2464
61. Kanki T., and Klionsky D.J. Mitophagy in yeast occurs through a selective mechanism. J Biol Chem 283 (2008) 32386-32393
62. Kissova I., Salin B., Schaeffer J., Bhatia S., Manon S., and Camougrand N. Selective and non-selective autophagic degradation of mitochondria in yeast. Autophagy 3 (2007) 329-336
63. Tal R., Winter G., Ecker N., Klionsky D.J., and Abeliovich H. Aup1p, a yeast mitochondrial protein phosphatase homolog, is required for efficient stationary phase mitophagy and cell survival. J Biol Chem 282 (2007) 5617-5624
64. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27 (2008) 433-446
65. Narendra D., Tanaka A., Suen D.F., and Youle R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183 (2008) 795-803. Parkin is a mammalian ubiquitin ligase, whose defect leads to early onset of Parkinson's disease. After the addition of the mitochondrial uncoupler CCCP, Parkin was selectively recruited to mitochondria with low membrane potential. These mitochondria were subsequently degraded via mitophagy in an Atg5-dependent manner.
66. Kim I., Rodriguez-Enriquez S., and Lemasters J.J. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462 (2007) 245-253
67. Bernales S., McDonald K.L., and Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4 (2006) e423
68. Kruse K.B., Brodsky J.L., and McCracken A.A. 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 (2006) 203-212
69. Yorimitsu T., Nair U., Yang Z., and Klionsky D.J. Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281 (2006) 30299-30304