Autophagy in the fission yeast Schizosaccharomyces pombe

FEBS Letters

Volumn 584, Issue 7, 2010, Pages 1327-1334

  Mukaiyama, Hiroyuki ^a   Nakase, Mai ^a   Nakamura, Taro ^b   Kakinuma, Yoshimi ^c   Takegawa, Kaoru ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b Osaka Prefecture University   (Japan)

^c EHIME UNIVERSITY   (Japan)

Author keywords

Autophagy; Fission yeast; Meiosis; Sporulation; Starvation

Indexed keywords

AMINO ACID; CELL PROTEIN; GREEN FLUORESCENT PROTEIN; NITROGEN; PERMEASE; PROTEIN ATG8; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER;

AUTOPHAGY; CELL CYCLE; EUKARYOTE; FUNGAL CELL; FUNGAL GENOME; FUNGUS MUTANT; GENE SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; SCHIZOSACCHAROMYCES POMBE; SEX DIFFERENTIATION; SPOROGENESIS; STARVATION; CELL VACUOLE; CYTOLOGY; ENZYMOLOGY; FUNGUS SPORE; GENETICS; METABOLISM; PHYSIOLOGY; SCHIZOSACCHAROMYCES;

EUKARYOTA; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

AMINO ACID TRANSPORT SYSTEMS; AUTOPHAGY; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; SPORES, FUNGAL; VACUOLES;

EID: 77950501572     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.12.037     Document Type: Review

References (91)

1. Tucker K.A., Reggiori F., Dunn W.A., Klionsky D.J. Atg23 is essential for the cytoplasm to vacuole targeting pathway and efficient autophagy but not pexophagy. J. Biol. Chem. 2003, 278:48445-48452.
2. Tsukada M., Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 1993, 333:169-174.
3. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
4. Nakatogawa H., Suzuki K., Kamada Y., Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 2009, 10:458-467.
5. Ichimura Y., et al. A ubiquitin-like system mediates protein lipidation. Nature 2000, 408:488-492.
6. Kamada Y., Funakoshi T., Shintani T., Nagano K., Ohsumi M., Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 2000, 150:1507-1513.
7. Mizushima N., et al. A protein conjugation system essential for autophagy. Nature 1998, 395:395-398.
8. Klionsky D.J., Ohsumi Y. Vacuolar import of proteins and organelles from the cytoplasm. Annu. Rev. Cell Dev. Biol. 1999, 15:1-32.
9. Baba M., Osumi M., Scott S.V., Klionsky D.J., Ohsumi Y. Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J. Cell Biol. 1997, 139:1687-1695.
10. Oku M., Sakai Y. Pexophagy in Pichia pastoris. Methods Enzymol. 2008, 451:217-228.
11. Sakai Y., Koller A., Rangell L.K., Keller G.A., Subramani S. Peroxisome degradation by microautophagy in Pichia pastoris: identification of specific steps and morphological intermediates. J. Cell Biol. 1998, 141:625-636.
12. Sakai Y., Subramani S. Environmental response of yeast peroxisomes. Aspects of organelle assembly and degradation. Cell Biochem. Biophys. 2000, 32(Spring):51-61.
13. Oku M., Nishimura T., Hattori T., Ano Y., Yamashita S., Sakai Y. Role of Vac8 in formation of the vacuolar sequestering membrane during micropexophagy. Autophagy 2006, 2:272-279.
14. Yamashita S., Oku M., Sakai Y. Functions of PI4P and sterol glucoside are necessary for the synthesis of a nascent membrane structure during pexophagy. Autophagy 2007, 3:35-37.
15. Sakai Y., Oku M., van der Klei I.J., Kiel J.A. Pexophagy: autophagic degradation of peroxisomes. Biochim. Biophys. Acta 2006, 1763:1767-1775.
16. Mukaiyama H., Oku M., Baba M., Samizo T., Hammond A.T., Glick B.S., Kato N., Sakai Y. Paz2 and 13 other PAZ gene products regulate vacuolar engulfment of peroxisomes during micropexophagy. Genes Cells 2002, 7:75-90.
17. Oku M., Warnecke D., Noda T., Muller F., Heinz E., Mukaiyama H., Kato N., Sakai Y. Peroxisome degradation requires catalytically active sterol glucosyltransferase with a GRAM domain. EMBO J. 2003, 22:3231-3241.
18. Nazarko T.Y., Farre J.C., Subramani S. Peroxisome size provides insights into the function of autophagy-related proteins. Mol. Biol. Cell 2009, 20:3828-3839.
19. Farre J.C., Manjithaya R., Mathewson R.D., Subramani S. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev. Cell 2008, 14:365-376.
20. Kanki, T. and Klionsky, D.J. (2009) Atg32 is a tag for mitochondria degradation in yeast. Autophagy 5.
21. Kanki T., Wang K., Cao Y., Baba M., Klionsky D.J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 2009, 17:98-109.
22. Okamoto, K., Kondo-Okamoto, N. and Ohsumi, Y. (2009) A landmark protein essential for mitophagy: Atg32 recruits the autophagic machinery to mitochondria. Autophagy 5.
23. Okamoto K., Kondo-Okamoto N., Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 2009, 17:87-97.
24. Otsubo Y., Yamamato M. TOR signaling in fission yeast. Crit. Rev. Biochem. Mol. Biol. 2008, 43:277-283.
25. Weisman R., Roitburg I., Schonbrun M., Harari R., Kupiec M. Opposite effects of tor1 and tor2 on nitrogen starvation responses in fission yeast. Genetics 2007, 175:1153-1162.
26. Matsuo T., Otsubo Y., Urano J., Tamanoi F., Yamamoto M. Loss of the TOR kinase Tor2 mimics nitrogen starvation and activates the sexual development pathway in fission yeast. Mol. Cell Biol. 2007, 27:3154-3164.
27. Nakashima A., Hasegawa T., Mori S., Ueno M., Tanaka S., Ushimaru T., Sato S., Uritani M. A starvation-specific serine protease gene, isp6+, is involved in both autophagy and sexual development in Schizosaccharomyces pombe. Curr. Genet. 2006, 49:403-413.
28. Kohda T.A., Tanaka K., Konomi M., Sato M., Osumi M., Yamamoto M. Fission yeast autophagy induced by nitrogen starvation generates a nitrogen source that drives adaptation processes. Genes Cells 2007, 12:155-170.
29. Bone N., Millar J.B., Toda T., Armstrong J. Regulated vacuole fusion and fission in Schizosaccharomyces pombe: an osmotic response dependent on MAP kinases. Curr. Biol. 1998, 8:135-144.
30. Catlett N.L., Weisman L.S. Divide and multiply: organelle partitioning in yeast. Curr. Opin. Cell Biol. 2000, 12:509-516.
31. Takegawa K., DeWald D.B., Emr S.D. Schizosaccharomyces pombe Vps34p, a phosphatidylinositol-specific PI 3-kinase essential for normal cell growth and vacuole morphology. J. Cell Sci. 1995, 108:3745-3756.
32. Onishi M., et al. Role of phosphatidylinositol 3-phosphate in formation of forespore membrane in Schizosaccharomyces pombe. Yeast 2003, 20:193-206.
33. Morishita M., Morimoto F., Kitamura K., Koga T., Fukui Y., Maekawa H., Yamashita I., Shimoda C. Phosphatidylinositol 3-phosphate 5-kinase is required for the cellular response to nutritional starvation and mating pheromone signals in Schizosaccharomyces pombe. Genes Cells 2002, 7:199-215.
34. Morishita M., Shimoda C. Positioning of medial actin rings affected by eccentrically located nuclei in a fission yeast mutant having large vacuoles. FEMS Microbiol. Lett. 2000, 188:63-67.
35. Wickner W. Yeast vacuoles and membrane fusion pathways. EMBO J. 2002, 21:1241-1247.
36. Iwaki T., Tanaka N., Takagi H., Giga-Hama Y., Takegawa K. Characterization of end4+, a gene required for endocytosis in Schizosaccharomyces pombe. Yeast 2004, 21:867-881.
37. Kashiwazaki J., Iwaki T., Takegawa K., Shimoda C., Nakamura T. Two fission yeast rab7 homologs, ypt7 and ypt71, play antagonistic roles in the regulation of vacuolar morphology. Traffic 2009, 10:912-924.
38. Bowers K., Stevens T.H. Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 2005, 1744:438-454.
39. Bonangelino C.J., Chavez E.M., Bonifacino J.S. Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol. Biol. Cell 2002, 13:2486-2501.
40. Wood V., et al. The genome sequence of Schizosaccharomyces pombe. Nature 2002, 415:871-880.
41. Takegawa K., Iwaki T., Fujita Y., Morita T., Hosomi A., Tanaka N. Vesicle-mediated protein transport pathways to the vacuole in Schizosaccharomyces pombe. Cell Struct. Funct. 2003, 28:399-417.
42. Tabuchi M., Iwaihara O., Ohtani Y., Ohuchi N., Sakurai J., Morita T., Iwahara S., Takegawa K. Vacuolar protein sorting in fission yeast: cloning, biosynthesis, transport, and processing of carboxypeptidase Y from Schizosaccharomyces pombe. J. Bacteriol. 1997, 179:4179-4189.
43. Koga T., et al. Sorting nexin homologues are targets of phosphatidylinositol 3-phosphate in sporulation of Schizosaccharomyces pombe. Genes Cells 2004, 9:561-574.
44. Iwaki T., et al. Characterization of vps33+, a gene required for vacuolar biogenesis and protein sorting in Schizosaccharomyces pombe. Yeast 2003, 20:845-855.
45. Iwaki T., Onishi M., Ikeuchi M., Kita A., Sugiura R., Giga-Hama Y., Fukui Y., Takegawa K. Essential roles of class E Vps proteins for sorting into multivesicular bodies in Schizosaccharomyces pombe. Microbiology 2007, 153:2753-2764.
46. Rothlisberger S., Jourdain I., Johnson C., Takegawa K., Hyams J.S. The dynamin-related protein Vps1 regulates vacuole fission, fusion and tubulation in the fission yeast, Schizosaccharomyces pombe. Fungal Genet. Biol. 2009, 46:927-935.
47. Takegawa K., Hosomi A., Iwaki T., Fujita Y., Morita T., Tanaka N. Identification of a SNARE protein required for vacuolar protein transport in Schizosaccharomyces pombe. Biochem. Biophys. Res. Commun. 2003, 311:77-82.
48. Iwaki T., Goa T., Tanaka N., Takegawa K. Characterization of Schizosaccharomyces pombe mutants defective in vacuolar acidification and protein sorting. Mol. Genet. Genom. 2004, 271:197-207.
49. Iwaki T., Hosomi A., Tokudomi S., Kusunoki Y., Fujita Y., Giga-Hama Y., Tanaka N., Takegawa K. Vacuolar protein sorting receptor in Schizosaccharomyces pombe. Microbiology 2006, 152:1523-1532.
50. Stephan J.S., Herman P.K. The regulation of autophagy in eukaryotic cells: do all roads pass through Atg1?. Autophagy 2006, 2:146-148.
51. Obara K., Sekito T., 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 2006, 17:1527-1539.
52. Stromhaug P.E., Klionsky D.J. Approaching the molecular mechanism of autophagy. Traffic 2001, 2:524-531.
53. Yoshimori T., Noda T. Toward unraveling membrane biogenesis in mammalian autophagy. Curr. Opin. Cell Biol. 2008, 20:401-407.
54. Yang Y.P., Liang Z.Q., Gu Z.L., Qin Z.H. Molecular mechanism and regulation of autophagy. Acta Pharmacol. Sin. 2005, 26:1421-1434.
55. Yen W.L., Legakis J.E., Nair U., Klionsky D.J. Atg27 is required for autophagy-dependent cycling of Atg9. Mol. Biol. Cell 2007, 18:581-593.
56. Obara K., Noda T., Niimi K., Ohsumi Y. Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells 2008, 13:537-547.
57. Cheong H., Klionsky D.J. Biochemical methods to monitor autophagy-related processes in yeast. Methods Enzymol. 2008, 451:1-26.
58. Hosokawa N., Sasaki T., Iemura S., Natsume T., Hara T., Mizushima N. Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 2009, 5:973-979.
59. Mercer C.A., Kaliappan A., Dennis P.B. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 2009, 5:649-662.
60. Ohsumi, Y. (1999) Molecular mechanism of autophagy in yeast, Saccharomyces cerevisiae. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 1577-1580; discussion 1580-1571.
61. Geng J., Baba M., Nair U., Klionsky D.J. Quantitative analysis of autophagy-related protein stoichiometry by fluorescence microscopy. J. Cell Biol. 2008, 182:129-140.
62. Obara K., Sekito T., Niimi K., Ohsumi Y. The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J. Biol. Chem. 2008, 283:23972-23980.
63. Suzuki K., Kubota Y., Sekito T., Ohsumi Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 2007, 12:209-218.
64. Mukaiyama H., Kajiwara S., Hosomi A., Giga-Hama Y., Tanaka N., Nakamura T., Takegawa K. Autophagy-deficient Schizosaccharomyces pombe mutants undergo partial sporulation during nitrogen starvation. Microbiology 2009, 155:3816-3826.
65. Kirisako T., et al. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J. Cell Biol. 2000, 151:263-276.
66. Shintani T., Klionsky D.J. Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J. Biol. Chem. 2004, 279:29889-29894.
67. Klionsky D.J. Monitoring autophagy in yeast: the Pho8Delta60 assay. Methods Mol. Biol. 2007, 390:363-371.
68. Klionsky D.J., et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
69. Takeshige K., Baba M., Tsuboi S., Noda T., Ohsumi Y. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol. 1992, 119:301-311.
70. Maeda T., Mochizuki N., Yamamoto M. Adenylyl cyclase is dispensable for vegetative cell growth in the fission yeast Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 1990, 87:7814-7818.
71. Maeda T., Watanabe Y., Kunitomo H., Yamamoto M. Cloning of the pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. J. Biol. Chem. 1994, 269:9632-9637.
72. Isshiki T., Mochizuki N., Maeda T., Yamamoto M. Characterization of a fission yeast gene, gpa2, that encodes a G alpha subunit involved in the monitoring of nutrition. Genes Dev. 1992, 6:2455-2462.
73. Welton R.M., Hoffman C.S. Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. Genetics 2000, 156:513-521.
74. Noda T., Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 1998, 273:3963-3966.
75. Uritani M., Hidaka H., Hotta Y., Ueno M., Ushimaru T., Toda T. Fission yeast Tor2 links nitrogen signals to cell proliferation and acts downstream of the Rheb GTPase. Genes Cells 2006, 11:1367-1379.
76. Alvarez B., Moreno S. Fission yeast Tor2 promotes cell growth and represses cell differentiation. J. Cell Sci. 2006, 119:4475-4485.
77. Funakoshi T., Matsuura A., Noda T., Ohsumi Y. Analyses of APG13 gene involved in autophagy in yeast, Saccharomyces cerevisiae. Gene 1997, 192:207-213.
78. Nakamura T., Nakamura-Kubo M., Hirata A., Shimoda C. The Schizosaccharomyces pombe spo3+ gene is required for assembly of the forespore membrane and genetically interacts with psy1(+)-encoding syntaxin-like protein. Mol. Biol. Cell 2001, 12:3955-3972.
79. Nakamura T., Asakawa H., Nakase Y., Kashiwazaki J., Hiraoka Y., Shimoda C. Live observation of forespore membrane formation in fission yeast. Mol. Biol. Cell. 2008, 19:3544-3553.
80. Chu S., DeRisi J., Eisen M., Mulholland J., Botstein D., Brown P.O., Herskowitz I. The transcriptional program of sporulation in budding yeast. Science 1998, 282:699-705.
81. Mata J., Lyne R., Burns G., Bahler J. The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 2002, 32:143-147.
82. Primig M., Williams R.M., Winzeler E.A., Tevzadze G.G., Conway A.R., Hwang S.Y., Davis R.W., Esposito R.E. The core meiotic transcriptome in budding yeasts. Nat. Genet. 2000, 26:415-423.
83. Onodera J., Ohsumi Y. Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J. Biol. Chem. 2005, 280:31582-31586.
84. Kitamoto K., Yoshizawa K., Ohsumi Y., Anraku Y. Dynamic aspects of vacuolar and cytosolic amino acid pools of Saccharomyces cerevisiae. J. Bacteriol. 1988, 170:2683-2686.
85. Wiemken A., Durr M. Characterization of amino acid pools in the vacuolar compartment of Saccharomyces cerevisiae. Arch. Microbiol. 1974, 101:45-57.
86. Ohsumi Y., Anraku Y. Active transport of basic amino acids driven by a proton motive force in vacuolar membrane vesicles of Saccharomyces cerevisiae. J. Biol. Chem. 1981, 256:2079-2082.
87. Sekito T., Fujiki Y., Ohsumi Y., Kakinuma Y. Novel families of vacuolar amino acid transporters. IUBMB Life 2008, 60:519-525.
88. Shimazu M., Sekito T., Akiyama K., Ohsumi Y., Kakinuma Y. A family of basic amino acid transporters of the vacuolar membrane from Saccharomyces cerevisiae. J. Biol. Chem. 2005, 280:4851-4857.
89. Russnak R., Konczal D., McIntire S.L. A family of yeast proteins mediating bidirectional vacuolar amino acid transport. J. Biol. Chem. 2001, 276:23849-23857.
90. Yang Z., Huang J., Geng J., Nair U., Klionsky D.J. Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. Mol. Biol. Cell 2006, 17:5094-5104.
91. Chardwiriyapreecha S., Shimazu M., Morita T., Sekito T., Akiyama K., Takegawa K., Kakinuma Y. Identification of the fnx1+ and fnx2+ genes for vacuolar amino acid transporters in Schizosaccharomyces pombe. FEBS Lett. 2008, 582:2225-2230.