Interorganelle interactions and inheritance patterns of nuclei and vacuoles in budding yeast meiosis

Autophagy

Volumn 10, Issue 2, 2014, Pages 285-295

  Tsai, I Ting ^a,b   Lin, Jyun Liang ^b   Chiang, Yi Hsuan ^a,b   Chuang, Yu Chien ^b,c   Liang, Shu Shan ^b,d   Chuang, Chi Ning ^b   Huang, Tzyy Nan ^b   Wang, Ting Fang ^a,b,c,d  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^c ACADEMIA SINICA   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Bouquet formation; Meiosis; Nuclear envelope; Nucleus vacuole junction; Piecemeal microautophagy of the nucleus; Rapid prophase movements; Vacuoles

Indexed keywords

CELL PROTEIN; FUNGAL PROTEIN; NVJ1 PROTEIN; PROTEIN MPS3; UNCLASSIFIED DRUG; VAC8 PROTEIN;

ARTICLE; BUDDING YEAST; CELL NUCLEUS MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; DIFFUSION; FUNGUS MUTANT; FUNGUS SPORE; INHERITANCE; MEIOSIS; NONHUMAN; NUCLEAR PORE COMPLEX; PHENOTYPE; TELOMERE; TONOPLAST; YEAST;

BOUQUET FORMATION; MEIOSIS; NUCLEAR ENVELOPE; NUCLEUS-VACUOLE JUNCTION; PIECEMEAL MICROAUTOPHAGY OF THE NUCLEUS; RAPID PROPHASE MOVEMENTS; VACUOLES;

ANIMALS; AUTOPHAGY; CELL CYCLE PROTEINS; CELL NUCLEUS; INHERITANCE PATTERNS; MEIOSIS; NUCLEAR ENVELOPE; SACCHAROMYCETALES; VACUOLES;

EID: 84894482437     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.27192     Document Type: Article

References (49)

1. Parvinen M, Söderström KO. Chromosome rotation and formation of synapsis. Nature 1976; 260:534-5; PMID:1264213; http://dx.doi.org/10.1038/ 260534a0
2. Ding DQ, Chikashige Y, Haraguchi T, Hiraoka Y. Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J Cell Sci 1998; 111:701-12; PMID:9471999
3. Scherthan H. Telomere attachment and clustering during meiosis. Cell Mol Life Sci 2007; 64:117-24; PMID:17219025; http://dx.doi.org/10.1007/s00018-006- 6463-2
4. Conrad MN, Lee CY, Wilkerson JL, Dresser ME. MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2007; 104:8863-8; PMID:17495028; http://dx.doi.org/10.1073/pnas.0606165104
5. Conrad MN, Lee CY, Chao G, Shinohara M, Kosaka H, Shinohara A, Conchello JA, Dresser ME. Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 2008; 133:1175-87; PMID:18585352; http://dx.doi.org/10.1016/j.cell.2008.04.047
6. Kosaka H, Shinohara M, Shinohara A. Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet 2008; 4:e1000196; PMID:18818742; http://dx.doi.org/10.1371/journal.pgen.1000196
7. Koszul R, Kim KP, Prentiss M, Kleckner N, Kameoka S. Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 2008; 133:1188-201; PMID:18585353; http://dx.doi.org/10. 1016/j.cell.2008.04.050
8. Wanat JJ, Kim KP, Koszul R, Zanders S, Weiner B, Kleckner N, Alani E. Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet 2008; 4:e1000188; PMID:18818741; http://dx.doi.org/10.1371/journal.pgen.1000188
9. Sonntag Brown M, Zanders S, Alani E. Sustained and rapid chromosome movements are critical for chromosome pairing and meiotic progression in budding yeast. Genetics 2011; 188:21-32; PMID:21339478; http://dx.doi.org/10.1534/ genetics.110.125575
10. Bhalla N, Dernburg AF. Prelude to a division. Annu Rev Cell Dev Biol 2008; 24:397-424; PMID:18597662; http://dx.doi.org/10.1146/annurev.cellbio.23. 090506.123245
11. Loidl J, Lukaszewicz A, Howard-Till RA, Koestler T. The Tetrahymena meiotic chromosome bouquet is organized by centromeres and promotes interhomolog recombination. J Cell Sci 2012; 125:5873-80; PMID:22976299; http://dx.doi.org/10.1242/jcs.112664
12. Wynne DJ, Rog O, Carlton PM, Dernburg AF. Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol 2012; 196:47-64; PMID:22232701; http://dx.doi.org/10.1083/jcb.201106022
13. Koszul R, Kleckner N. Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 2009; 19:716-24; PMID:19854056; http://dx.doi.org/10.1016/j.tcb.2009.09.007
14. Chua PR, Roeder GS. Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 1997; 11:1786-800; PMID:9242487; http://dx.doi.org/10.1101/gad.11.14.1786
15. Conrad MN, Dominguez AM, Dresser ME. Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 1997; 276:1252-5; PMID:9157883; http://dx.doi.org/10.1126/science.276.5316.1252
16. Trelles-Sticken E, Dresser ME, Scherthan H. Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 2000; 151:95-106; PMID:11018056; http://dx.doi.org/10.1083/jcb.151.1.95
17. Jaspersen SL, Giddings TH Jr., Winey M. Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J Cell Biol 2002; 159:945-56; PMID:12486115; http://dx.doi.org/10.1083/jcb. 200208169
18. Beilharz T, Egan B, Silver PA, Hofmann K, Lithgow T. Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J Biol Chem 2003; 278:8219-23; PMID:12514182; http://dx.doi.org/10.1074/jbc.M212725200
19. Burri L, Lithgow T. A complete set of SNAREs in yeast. Traffic 2004; 5:45-52; PMID:14675424; http://dx.doi.org/10.1046/j.1600-0854.2003.00151.x
20. Rabitsch KP, Tóth A, Gálová M, Schleiffer A, Schaffner G, Aigner E, Rupp C, Penkner AM, Moreno-Borchart AC, Primig M, et al. A screen for genes required for meiosis and spore formation based on whole-genome expression. Curr Biol 2001; 11:1001-9; PMID:11470404; http://dx.doi.org/10.1016/S0960-9822(01)00274-3
21. Kvam E, Goldfarb DS. Nucleus-vacuole junctions and piecemeal microautophagy of the nucleus in S. cerevisiae. Autophagy 2007; 3:85-92; PMID:17204844
22. Wang YX, Catlett NL, Weisman LS. Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole. J Cell Biol 1998; 140:1063-74; PMID:9490720; http://dx.doi.org/10.1083/jcb.140.5.1063
23. Pan X, Roberts P, Chen Y, Kvam E, Shulga N, Huang K, Lemmon S, Goldfarb DS. Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p. Mol Biol Cell 2000; 11:2445-57; PMID:10888680; http://dx.doi.org/10.1091/mbc.11.7.2445
24. Roberts P, Moshitch-Moshkovitz S, Kvam E, O'Toole E, Winey M, Goldfarb DS. Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol Biol Cell 2003; 14:129-41; PMID:12529432; http://dx.doi.org/10.1091/mbc.E02-08-0483
25. Severs NJ, Jordan EG, Williamson DH. Nuclear pore absence from areas of close association between nucleus and vacuole in synchronous yeast cultures. J Ultrastruct Res 1976; 54:374-87; PMID:176417; http://dx.doi.org/10.1016/S0022- 5320(76)80023-8
26. Dawaliby R, Mayer A. Microautophagy of the nucleus coincides with a vacuolar diffusion barrier at nuclear-vacuolar junctions. Mol Biol Cell 2010; 21:4173-83; PMID:20943953; http://dx.doi.org/10.1091/mbc.E09-09-0782
27. Lai YJ, Lin FM, Chuang MJ, Shen HJ, Wang TF. Genetic requirements and meiotic function of phosphorylation of the yeast axial element protein Red1. Mol Cell Biol 2011; 31:912-23; PMID:21173162; http://dx.doi.org/10.1128/MCB.00895- 10
28. Lin FM, Lai YJ, Shen HJ, Cheng YH, Wang TF. Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis. EMBO J 2010; 29:586-96; PMID:19959993; http://dx.doi.org/ 10.1038/emboj.2009.362
29. Zubenko GS, Jones EW. Protein degradation, meiosis and sporulation in proteinase-deficient mutants of Saccharomyces cerevisiae. Genetics 1981; 97:45-64; PMID:7021321
30. Nelson H, Mandiyan S, Nelson N. A conserved gene encoding the 57-kDa subunit of the yeast vacuolar H+-ATPase. J Biol Chem 1989; 264:1775-8; PMID:2521486
31. Sheff MA, Thorn KS. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 2004; 21:661-70; PMID:15197731; http://dx.doi.org/10.1002/yea.1130
32. Sym M, Engebrecht JA, Roeder GS. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 1993; 72:365-78; PMID:7916652; http://dx.doi.org/10.1016/0092-8674(93)90114-6
33. Fuchs J, Loidl J. Behaviour of nucleolus organizing regions (NORs) and nucleoli during mitotic and meiotic divisions in budding yeast. Chromosome Res 2004; 12:427-38; PMID:15252239; http://dx.doi.org/10.1023/B:CHRO.0000034726. 05374.db
34. Kobayashi T, Horiuchi T. A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1996; 1:465-74; PMID:9078378; http://dx.doi.org/10.1046/j.1365-2443.1996. d01-256.x
35. Moreno-Borchart AC, Knop M. Prospore membrane formation: how budding yeast gets shaped in meiosis. Microbiol Res 2003; 158:83-90; PMID:12906380; http://dx.doi.org/10.1078/0944-5013-00194
36. Neiman AM. Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 2011; 189:737-65; PMID:22084423; http://dx.doi.org/10.1534/genetics. 111.127126
37. Roeder AD, Shaw JM. Vacuole partitioning during meiotic division in yeast. Genetics 1996; 144:445-58; PMID:8889511
38. Suda Y, Nakanishi H, Mathieson EM, Neiman AM. Alternative modes of organellar segregation during sporulation in Saccharomyces cerevisiae. Eukaryot Cell 2007; 6:2009-17; PMID:17905927; http://dx.doi.org/10.1128/EC.00238-07
39. Clyne RK, Katis VL, Jessop L, Benjamin KR, Herskowitz I, Lichten M, Nasmyth K. Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 2003; 5:480-5; PMID:12717442; http://dx.doi.org/10.1038/ncb977
40. Rose MD, Misra LM, Vogel JP. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 1989; 57:1211-21; PMID:2661018; http://dx.doi.org/10.1016/0092-8674(89)90058-5
41. Unal E, Kinde B, Amon A. Gametogenesis eliminates age-induced cellular damage and resets life span in yeast. Science 2011; 332:1554-7; PMID:21700873; http://dx.doi.org/10.1126/science.1204349
42. Lee CY, Conrad MN, Dresser ME. Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 2012; 8:e1002730; PMID:22654677; http://dx.doi.org/10.1371/journal.pgen.1002730
43. Rockmill B, Roeder GS. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proc Natl Acad Sci U S A 1988; 85:6057-61; PMID:3413075; http://dx.doi.org/10.1073/pnas.85.16.6057
44. Klionsky DJ. The molecular machinery of autophagy: unanswered questions. J Cell Sci 2005; 118:7-18; PMID:15615779; http://dx.doi.org/10.1242/jcs.01620
45. Van Den Hazel HB, Kielland-Brandt MC, Winther JR. Review: biosynthesis and function of yeast vacuolar proteases. Yeast 1996; 12:1-16; PMID:8789256; http://dx.doi.org/10.1002/(SICI)1097-0061(199601)12:1〈1::AID-YEA902〉3. 0.CO;2-N
46. Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I. The transcriptional program of sporulation in budding yeast. Science 1998; 282:699-705; PMID:9784122; http://dx.doi.org/10.1126/science.282.5389.699
47. Betz H, Weiser U. Protein degradation during yeast sporulation. Enzyme and cytochrome patterns. Eur J Biochem 1976; 70:385-95; PMID:188644; http://dx.doi.org/10.1111/j.1432-1033.1976.tb11028.x
48. Zubenko GS, Park FJ, Jones EW. Genetic properties of mutations at the PEP4 locus in Saccharomyces cerevisiae. Genetics 1982; 102:679-90; PMID:6764902
49. Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, Yeh CH, Huang HY, Wang TF. SUMO modifications control assembly of synaptonemal complex and poly-complex in meiosis of Saccharomyces cerevisiae. Genes Dev 2006; 20:2067-81; PMID:16847351; http://dx.doi.org/10.1101/gad.1430406