Global Analysis of Fission Yeast Mating Genes Reveals New Autophagy Factors

PLoS Genetics

Volumn 9, Issue 8, 2013, Pages

  Sun, Ling Ling ^a   Li, Ming ^a   Suo, Fang ^a   Liu, Xiao Man ^a   Shen, En Zhi ^a   Yang, Bing ^a   Dong, Meng Qiu ^a   He, Wan Zhong ^a   Du, Li Lin ^a  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ATG10 PROTEIN; ATG12 PROTEIN; ATG13 PROTEIN; ATG14 PROTEIN; ATG15 PROTEIN; ATG16 PROTEIN; ATG18 PROTEIN; ATG18A PROTEIN; ATG18B PROTEIN; ATG18C PROTEIN; ATG2 PROTEIN; ATG4 PROTEIN; ATG9 PROTEIN; AUTOPHAGY PROTEIN 5; CTL1 PROTEIN; FSC1 PROTEIN; FUNGAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATG10 GENE; ATG12 GENE; ATG13 GENE; ATG14 GENE; ATG15 GENE; ATG16 GENE; ATG18A GENE; ATG18B GENE; ATG18C GENE; ATG2 GENE; ATG4 GENE; ATG5 GENE; ATG9 GENE; AUTOPHAGOSOME; CELL VACUOLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; FUNGAL GENE; FUNGAL GENOME; GENE DELETION; GENETIC ANALYSIS; GENETIC CODE; MACROAUTOPHAGY; MATING SYSTEM; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE;

AUTOPHAGY; CYTOPLASM; GENOME, FUNGAL; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; PEPTIDES; PHAGOSOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE DELETION; VACUOLES;

EID: 84884658187     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003715     Document Type: Article

References (88)

1. 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.
2. Tsukada M, Ohsumi Y, (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333: 169-174.
3. Kohda TA, Tanaka K, Konomi M, Sato M, Osumi M, et al. (2007) Fission yeast autophagy induced by nitrogen starvation generates a nitrogen source that drives adaptation processes. Genes Cells 12: 155-170 doi:10.1111/j.1365-2443.2007.01041.x.
4. Levine B, Kroemer G, (2008) Autophagy in the pathogenesis of disease. Cell 132: 27-42 doi:10.1016/j.cell.2007.12.018.
5. Mizushima N, Komatsu M, (2011) Autophagy: renovation of cells and tissues. Cell 147: 728-741 doi:10.1016/j.cell.2011.10.026.
6. Xie Z, Klionsky DJ, (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9: 1102-1109 doi:10.1038/ncb1007-1102.
7. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y, (2009) Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10: 458-467 doi:10.1038/nrm2708.
8. Mizushima N, Yoshimori T, Ohsumi Y, (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27: 107-132 doi:10.1146/annurev-cellbio-092910-154005.
9. Klionsky DJ, (2007) The importance of diversity. Autophagy 3: 83-84.
10. King JS, (2012) Autophagy across the eukaryotes: Is S. cerevisiae the odd one out? Autophagy 8: 1159-1162.
11. Berbee ML, Taylor JW, (2010) Dating the molecular clock in fungi - how close are we? Fungal Biology Reviews 24: 1-16 doi:10.1016/j.fbr.2010.03.001.
12. Mizushima N, (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22: 132-139 doi:10.1016/j.ceb.2009.12.004.
13. Mukaiyama H, Kajiwara S, Hosomi A, Giga-Hama Y, Tanaka N, et al. (2009) Autophagy-deficient Schizosaccharomyces pombe mutants undergo partial sporulation during nitrogen starvation. Microbiology 155: 3816-3826 doi:10.1099/mic.0.034389-0.
14. Yamamoto M, Imai Y, Watanabe Y (1997) Mating and Sporulation in Schizosaccharomyces pombe. The molecular and cellular biology of the yeast Saccharomyces: Cell cycle and cell biology. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. pp. 1037-1106.
15. Nielsen O (2004) Mating-Type Control and Differentiation. The molecular biology of Schizosaccharomyces pombe: genetics, genomics and beyond. Berlin: Springer Verlag. pp. 281-296.
16. Leupold U, Sipiczki M, (1991) Sterile UGA nonsense mutants of fission yeast. Curr Genet 20: 67-73.
17. Wood V, Harris MA, McDowall MD, Rutherford K, Vaughan BW, et al. (2012) PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res 40: D695-699 doi:10.1093/nar/gkr853.
18. Kim D-U, Hayles J, Kim D, Wood V, Park H-O, et al. (2010) Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat Biotech 28: 617-623 doi:10.1038/nbt.1628.
19. Han TX, Xu X-Y, Zhang M-J, Peng X, Du L-L, (2010) Global fitness profiling of fission yeast deletion strains by barcode sequencing. Genome Biol 11: R60 doi:10.1186/gb-2010-11-6-r60.
20. Forsburg SL, Rhind N, (2006) Basic methods for fission yeast. Yeast 23: 173-183 doi:10.1002/yea.1347.
21. Mukaiyama H, Nakase M, Nakamura T, Kakinuma Y, Takegawa K, (2010) Autophagy in the fission yeast Schizosaccharomyces pombe. FEBS Lett 584: 1327-1334 doi:10.1016/j.febslet.2009.12.037.
22. 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 doi:10.1074/jbc.M404399200.
23. Cheong H, Klionsky DJ, (2008) Biochemical methods to monitor autophagy-related processes in yeast. Meth Enzymol 451: 1-26 doi:10.1016/S0076-6879(08)03201-1.
24. Meijer WH, van der Klei IJ, Veenhuis M, Kiel JAKW, (2007) ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes. Autophagy 3: 106-116.
25. 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 doi:10.1093/emboj/18.14.3888.
26. Matsunaga K, Morita E, Saitoh T, Akira S, Ktistakis NT, et al. (2010) Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J Cell Biol 190: 511-521 doi:10.1083/jcb.200911141.
27. Itakura E, Kishi C, Inoue K, Mizushima N, (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19: 5360-5372 doi:10.1091/mbc.E08-01-0080.
28. Kihara A, Noda T, Ishihara N, Ohsumi Y, (2001) Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152: 519-530.
29. 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 doi:10.1093/emboj/20.21.5971.
30. Kim J, Huang W-P, Stromhaug PE, Klionsky DJ, (2002) Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J Biol Chem 277: 763-773 doi:10.1074/jbc.M109134200.
31. Suzuki K, Kubota Y, Sekito T, Ohsumi Y, (2007) Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12: 209-218 doi:10.1111/j.1365-2443.2007.01050.x.
32. Cheong H, Nair U, Geng J, Klionsky DJ, (2008) 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: 668-681 doi:10.1091/mbc.E07-08-0826.
33. Xie Z, Nair U, Klionsky DJ, (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19: 3290-3298 doi:10.1091/mbc.E07-12-1292.
34. Obara K, Sekito T, Niimi K, Ohsumi Y, (2008) The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J Biol Chem 283: 23972-23980 doi:10.1074/jbc.M803180200.
35. Nair U, Cao Y, Xie Z, Klionsky DJ, (2010) Roles of the lipid-binding motifs of Atg18 and Atg21 in the cytoplasm to vacuole targeting pathway and autophagy. J Biol Chem 285: 11476-11488 doi:10.1074/jbc.M109.080374.
36. Traiffort E, Ruat M, O'Regan S, Meunier FM, (2005) Molecular characterization of the family of choline transporter-like proteins and their splice variants. J Neurochem 92: 1116-1125 doi:10.1111/j.1471-4159.2004.02962.x.
37. O'Regan S, Traiffort E, Ruat M, Cha N, Compaore D, et al. (2000) An electric lobe suppressor for a yeast choline transport mutation belongs to a new family of transporter-like proteins. Proc Natl Acad Sci USA 97: 1835-1840 doi:10.1073/pnas.030339697.
38. Michel V, Bakovic M, (2009) The solute carrier 44A1 is a mitochondrial protein and mediates choline transport. FASEB J 23: 2749-2758 doi:10.1096/fj.08-121491.
39. Zufferey R, Santiago TC, Brachet V, Ben Mamoun C, (2004) Reexamining the role of choline transporter-like (Ctlp) proteins in choline transport. Neurochem Res 29: 461-467.
40. Mullen GP, Mathews EA, Vu MH, Hunter JW, Frisby DL, et al. (2007) Choline transport and de novo choline synthesis support acetylcholine biosynthesis in Caenorhabditis elegans cholinergic neurons. Genetics 177: 195-204 doi:10.1534/genetics.107.074120.
41. Morigasaki S, Shimada K, Ikner A, Yanagida M, Shiozaki K, (2008) Glycolytic enzyme GAPDH promotes peroxide stress signaling through multistep phosphorelay to a MAPK cascade. Mol Cell 30: 108-113 doi:10.1016/j.molcel.2008.01.017.
42. Mitsuzawa H, Kimura M, Kanda E, Ishihama A, (2005) Glyceraldehyde-3-phosphate dehydrogenase and actin associate with RNA polymerase II and interact with its Rpb7 subunit. FEBS Lett 579: 48-52 doi:10.1016/j.febslet.2004.11.045.
43. Tabuchi M, Iwaihara O, Ohtani Y, Ohuchi N, Sakurai J, et al. (1997) Vacuolar protein sorting in fission yeast: cloning, biosynthesis, transport, and processing of carboxypeptidase Y from Schizosaccharomyces pombe. J Bacteriol 179: 4179-4189.
44. Noda T, Kim J, Huang WP, Baba M, Tokunaga C, et al. (2000) Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 148: 465-480.
45. 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.
46. Yamamoto H, Kakuta S, Watanabe TM, Kitamura A, Sekito T, et al. (2012) Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 198: 219-233 doi:10.1083/jcb.201202061.
47. Vjestica A, Tang X-Z, Oliferenko S, (2008) The actomyosin ring recruits early secretory compartments to the division site in fission yeast. Mol Biol Cell 19: 1125-1138 doi:10.1091/mbc.E07-07-0663.
48. Kawamoto T, Noshiro M, Shen M, Nakamasu K, Hashimoto K, et al. (1998) Structural and phylogenetic analyses of RGD-CAP/beta ig-h3, a fasciclin-like adhesion protein expressed in chick chondrocytes. Biochim Biophys Acta 1395: 288-292.
49. Elkins T, Hortsch M, Bieber AJ, Snow PM, Goodman CS, (1990) Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting. J Cell Biol 110: 1825-1832.
50. Huber O, Sumper M, (1994) Algal-CAMs: isoforms of a cell adhesion molecule in embryos of the alga Volvox with homology to Drosophila fasciclin I. EMBO J 13: 4212-4222.
51. Zhang J, Gratchev A, Riabov V, Mamidi S, Schmuttermaier C, et al. (2009) A novel GGA-binding site is required for intracellular sorting mediated by stabilin-1. Mol Cell Biol 29: 6097-6105 doi:10.1128/MCB.00505-09.
52. Darsow T, Rieder SE, Emr SD, (1997) A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J Cell Biol 138: 517-529.
53. Wang C-W, Stromhaug PE, Shima J, Klionsky DJ, (2002) The Ccz1-Mon1 protein complex is required for the late step of multiple vacuole delivery pathways. J Biol Chem 277: 47917-47927 doi:10.1074/jbc.M208191200.
54. Wang C-W, Stromhaug PE, Kauffman EJ, Weisman LS, Klionsky DJ, (2003) Yeast homotypic vacuole fusion requires the Ccz1-Mon1 complex during the tethering/docking stage. J Cell Biol 163: 973-985 doi:10.1083/jcb.200308071.
55. Bone N, Millar JB, Toda T, Armstrong J, (1998) Regulated vacuole fusion and fission in Schizosaccharomyces pombe: an osmotic response dependent on MAP kinases. Curr Biol 8: 135-144.
56. Umekawa M, Klionsky DJ, (2012) The Cytoplasm-to-Vacuole Targeting Pathway: A Historical Perspective. Int J Cell Biol 2012: 142634 doi:10.1155/2012/142634.
57. Polson HEJ, de Lartigue J, Rigden DJ, Reedijk M, Urbé S, et al. (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6: 506-522.
58. Behrends C, Sowa ME, Gygi SP, Harper JW, (2010) Network organization of the human autophagy system. Nature 466: 68-76 doi:10.1038/nature09204.
59. Lu Q, Yang P, Huang X, Hu W, Guo B, et al. (2011) The WD40 repeat PtdIns(3)P-binding protein EPG-6 regulates progression of omegasomes to autophagosomes. Dev Cell 21: 343-357 doi:10.1016/j.devcel.2011.06.024.
60. Strømhaug PE, Reggiori F, Guan J, Wang C-W, Klionsky DJ, (2004) 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: 3553-3566 doi:10.1091/mbc.E04-02-0147.
61. Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691 doi:10.1038/nature02026.
62. Suzuki K, Akioka M, Kondo-Kakuta C, Yamamoto H, Ohsumi Y, (2013) Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J Cell Sci 126: 2534-2544 doi:10.1242/jcs.122960.
63. Klionsky DJ, (2005) The molecular machinery of autophagy: unanswered questions. J Cell Sci 118: 7-18 doi:10.1242/jcs.01620.
64. Ganley IG, Wong P-M, Gammoh N, Jiang X, (2011) Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 42: 731-743 doi:10.1016/j.molcel.2011.04.024.
65. Chen D, Fan W, Lu Y, Ding X, Chen S, et al. (2012) A mammalian autophagosome maturation mechanism mediated by TECPR1 and the Atg12-Atg5 conjugate. Mol Cell 45: 629-641 doi:10.1016/j.molcel.2011.12.036.
66. Itakura E, Kishi-Itakura C, Mizushima N, (2012) The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 151: 1256-1269 doi:10.1016/j.cell.2012.11.001.
67. Keeney JB, Boeke JD, (1994) Efficient targeted integration at leu1-32 and ura4-294 in Schizosaccharomyces pombe. Genetics 136: 849-856.
68. Bähler J, Wu JQ, Longtine MS, Shah NG, McKenzie A 3rd, et al. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14: 943-951. doi:10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y.
69. Yu Y, Ren J-Y, Zhang J-M, Suo F, Fang X-F, et al. (2013) A proteome-wide visual screen identifies fission yeast proteins localizing to DNA double-strand breaks. DNA Repair (Amst) 12: 433-443 doi:10.1016/j.dnarep.2013.04.001.
70. Matsuyama A, Arai R, Yashiroda Y, Shirai A, Kamata A, et al. (2006) ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24: 841-847 doi:10.1038/nbt1222.
71. Esposito RE, Dresser M, Breitenbach M, (1991) Identifying sporulation genes, visualizing synaptonemal complexes, and large-scale spore and spore wall purification. Meth Enzymol 194: 110-131.
72. Bullard JH, Purdom E, Hansen KD, Dudoit S, (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11: 94 doi:10.1186/1471-2105-11-94.
73. Strimmer K, (2008) fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24: 1461-1462 doi:10.1093/bioinformatics/btn209.
74. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, et al. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25: 288-289 doi:10.1093/bioinformatics/btn615.
75. Matsuo Y, Asakawa K, Toda T, Katayama S, (2006) A rapid method for protein extraction from fission yeast. Biosci Biotechnol Biochem 70: 1992-1994.
76. Kaiser CA, Schekman R, (1990) Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell 61: 723-733.
77. Ryuko S, Ma Y, Ma N, Sakaue M, Kuno T, (2012) Genome-wide screen reveals novel mechanisms for regulating cobalt uptake and detoxification in fission yeast. Mol Genet Genomics 287: 651-662 doi:10.1007/s00438-012-0705-9.
78. Yamaguchi M, Noda NN, Yamamoto H, Shima T, Kumeta H, et al. (2012) Structural insights into atg10-mediated formation of the autophagy-essential atg12-atg5 conjugate. Structure 20: 1244-1254 doi:10.1016/j.str.2012.04.018.
79. Matsushita M, Suzuki NN, Obara K, Fujioka Y, Ohsumi Y, et al. (2007) Structure of Atg5.Atg16, a complex essential for autophagy. J Biol Chem 282: 6763-6772 doi:10.1074/jbc.M609876200.
80. Fujioka Y, Noda NN, Nakatogawa H, Ohsumi Y, Inagaki F, (2010) Dimeric coiled-coil structure of Saccharomyces cerevisiae Atg16 and its functional significance in autophagy. J Biol Chem 285: 1508-1515 doi:10.1074/jbc.M109.053520.
81. Delorenzi M, Speed T, (2002) An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18: 617-625.
82. Biegert A, Mayer C, Remmert M, Söding J, Lupas AN, (2006) The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res 34: W335-339 doi:10.1093/nar/gkl217.
83. Katoh K, Misawa K, Kuma K, Miyata T, (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
84. Price MN, Dehal PS, Arkin AP, (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490 doi:10.1371/journal.pone.0009490.
85. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ, (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191 doi:10.1093/bioinformatics/btp033.
86. Gouet P, Courcelle E, Stuart DI, Métoz F, (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
87. Watanabe Y, Kobayashi T, Yamamoto H, Hoshida H, Akada R, et al. (2012) Structure-based analyses reveal distinct binding sites for Atg2 and phosphoinositides in Atg18. J Biol Chem 287: 31681-31690 doi:10.1074/jbc.M112.397570.
88. Rieter E, Vinke F, Bakula D, Cebollero E, Ungermann C, et al. (2013) Atg18 function in autophagy is regulated by specific sites within its β-propeller. J Cell Sci 126: 593-604 doi:10.1242/jcs.115725.