Single site suppressors of a fission yeast temperature-sensitive mutant in Cdc48 identified by whole genome sequencing

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Marinova, Irina N ^a   Engelbrecht, Jacob ^a   Ewald, Adrian ^a   Langholm, Lasse L ^a   Holmberg, Christian ^a   Kragelund, Birthe B ^a   Gordon, Colin ^b   Nielsen, Olaf ^a   Hartmann Petersen, Rasmus ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AURORA B KINASE; DNA; UBIQUITIN; CDC48 PROTEIN; CELL CYCLE PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; BUDDING; CELL DIVISION; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; DNA REPAIR; FUNGAL STRAIN; GENE MAPPING; GENE MUTATION; GENE SEQUENCE; MUTAGENESIS; NONHUMAN; PHENOTYPE; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; QUALITY CONTROL; SCHIZOSACCHAROMYCES; SINGLE NUCLEOTIDE POLYMORPHISM; STRUCTURE ANALYSIS; SUMOYLATION; TEMPERATURE SENSITIVITY; UBIQUITINATION; ULTRAVIOLET IRRADIATION; AMINO ACID SEQUENCE; CHEMISTRY; CLASSIFICATION; COLD; DNA SEQUENCE; FUNGAL GENOME; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MOLECULAR GENETICS; MOLECULAR MODEL; MUTATION; PROCEDURES; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; TEMPERATURE;

MAMMALIA; SCHIZOSACCHAROMYCETACEAE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; COLD TEMPERATURE; GENOME, FUNGAL; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE;

EID: 84922658139     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117779     Document Type: Article

References (45)

1. Stolz A, Hilt W, Buchberger A, Wolf DH (2011) Cdc48: a power machine in protein degradation. Trends Biochem Sci 36: 515-523. S0968-0004(11)00084-3 [pii]; doi: 10.1016/j.tibs.2011.06.001 PMID: 21741246
2. Bays NW, Wilhovsky SK, Goradia A, Hodgkiss-Harlow K, Hampton RY (2001) HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol Biol Cell 12: 4114-4128. PMID: 11739805
3. Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414: 652-656. 414652a [pii]. doi: 10.1038/414652a PMID: 11740563
4. Braun S, Matuschewski K, Rape M, Thoms S, Jentsch S (2002) Role of the ubiquitin-selective CDC48 (UFD1/NPL4) chaperone (segregase) in ERAD of OLE1 and other substrates. EMBO J 21: 615-621. PMID: 11847109
5. Sommer T, Jarosch E, Lenk U (2001) Compartment-specific functions of the ubiquitin-proteasome pathway. Rev Physiol Biochem Pharmacol 142: 97-160. PMID: 11190579
6. Rabinovich E, Kerem A, Frohlich KU, Diamant N, Bar-Nun S (2002) AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol Cell Biol 22: 626-634. PMID: 11756557
7. Schuberth C, Buchberger A (2008) UBX domain proteins: major regulators of the AAA ATPase Cdc48/ p97. Cell Mol Life Sci 65: 2360-2371. doi: 10.1007/s00018-008-8072-8 PMID: 18438607
8. Pye VE, Dreveny I, Briggs LC, Sands C, Beuron F, et al. (2006) Going through the motions: the ATPase cycle of p97. J Struct Biol 156: 12-28. S1047-8477(06)00073-6 [pii]; doi: 10.1016/j.jsb.2006.03.003 PMID: 16621604
9. Beuron F, Dreveny I, Yuan X, Pye VE, McKeown C, et al. (2006) Conformational changes in the AAA ATPase p97-p47 adaptor complex. EMBO J 25: 1967-1976. 7601055 [pii]; doi: 10.1038/sj.emboj. 7601055 PMID: 16601695
10. Jentsch S, Rumpf S (2007) Cdc48 (p97): a "molecular gearbox" in the ubiquitin pathway? Trends Biochem Sci 32: 6-11. S0968-0004(06)00322-7 [pii]; doi: 10.1016/j.tibs.2006.11.005 PMID: 17142044
11. Kondo H, Rabouille C, Newman R, Levine TP, Pappin D, et al. (1997) p47 is a cofactor for p97-mediated membrane fusion. Nature 388: 75-78. doi: 10.1038/40411 PMID: 9214505
12. Jarosch E, Taxis C, Volkwein C, Bordallo J, Finley D, et al. (2002) Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat Cell Biol 4: 134-139. ncb746 [pii]. doi: 10. 1038/ncb746 PMID: 11813000
13. Hartmann-Petersen R, Wallace M, Hofmann K, Koch G, Johnsen AH, et al. (2004) The Ubx2 and Ubx3 cofactors direct Cdc48 activity to proteolytic and nonproteolytic ubiquitin-dependent processes. Curr Biol 14: 824-828. S0960982204002994 [pii]. doi: 10.1016/j.cub.2004.04.029 PMID: 15120077
14. Mosbech A, Gibbs-Seymour I, Kagias K, Thorslund T, Beli P, et al. (2012) DVC1 (C1orf124) is a DNA damage-targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks. Nat Struct Mol Biol 19: 1084-1092. nsmb.2395 [pii]; doi: 10.1038/nsmb.2395 PMID: 23042605
15. Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, et al. (2000) Activation of a membranebound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102: 577-586. S0092-8674(00)00080-5 [pii]. PMID: 11007476
16. Stewart EV, Lloyd SJ, Burg JS, Nwosu CC, Lintner RE, et al. (2012) Yeast sterol regulatory elementbinding protein (SREBP) cleavage requires Cdc48 and Dsc5, a ubiquitin regulatory X domain-containing subunit of the Golgi Dsc E3 ligase. J Biol Chem 287: 672-681. M111.317370 [pii]; doi: 10.1074/jbc. M111.317370 PMID: 22086920
17. Renton AE, Chio A, Traynor BJ (2014) State of play in amyotrophic lateral sclerosis genetics. Nat Neurosci 17: 17-23. nn.3584 [pii]; doi: 10.1038/nn.3584 PMID: 24369373
18. Ju JS, Weihl CC (2010) Inclusion body myopathy, Paget's disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum Mol Genet 19: R38-R45. ddq157 [pii]; doi: 10.1093/hmg/ddq157 PMID: 20410287
19. Tang WK, Xia D (2013) Altered Intersubunit Communication Is the Molecular Basis for Functional Defects of Pathogenic p97 Mutants. J Biol Chem 288: 36624-36635. M113.488924 [pii]; doi: 10.1074/jbc. M113.488924 PMID: 24196964
20. Rape M, Hoppe T, Gorr I, Kalocay M, Richly H, et al. (2001) Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone. Cell 107: 667-677. S0092-8674(01)00595-5 [pii]. PMID: 11733065
21. Madsen L, Seeger M, Semple CA, Hartmann-Petersen R (2009) New ATPase regulators-p97 goes to the PUB. Int J Biochem Cell Biol 41: 2380-2388. S1357-2725(09)00173-3 [pii]; doi: 10.1016/j.biocel. 2009.05.017 PMID: 19497384
22. Alexandru G, Graumann J, Smith GT, Kolawa NJ, Fang R, et al. (2008) UBXD7 binds multiple ubiquitin ligases and implicates p97 in HIF1alpha turnover. Cell 134: 804-816. S0092-8674(08)00835-0 [pii]; doi: 10.1016/j.cell.2008.06.048 PMID: 18775313
23. Nie M, Aslanian A, Prudden J, Heideker J, Vashisht AA, et al. (2012) Dual recruitment of Cdc48 (p97)-Ufd1-Npl4 ubiquitin-selective segregase by small ubiquitin-like modifier protein (SUMO) and ubiquitin in SUMO-targeted ubiquitin ligase-mediated genome stability functions. J Biol Chem 287: 29610-29619. M112.379768 [pii]; doi: 10.1074/jbc.M112.379768 PMID: 22730331
24. Kohler JB, Jorgensen ML, Beinoraite G, Thorsen M, Thon G (2013) Concerted Action of the Ubiquitin-Fusion Degradation Protein 1 (Ufd1) and Sumo-Targeted Ubiquitin Ligases (STUbLs) in the DNA-Damage Response. PLoS One 8: e80442. PONE-D-13-25961 [pii]. doi: 10.1371/journal.pone.0080442 PMID: 24265825
25. Bergink S, Ammon T, Kern M, Schermelleh L, Leonhardt H, et al. (2013) Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51-Rad52 interaction. Nat Cell Biol 15: 526-532. ncb2729 [pii]; doi: 10.1038/ncb2729 PMID: 23624404
26. Dobrynin G, Popp O, Romer T, Bremer S, Schmitz MH, et al. (2011) Cdc48/p97-Ufd1-Npl4 antagonizes Aurora B during chromosome segregation in HeLa cells. J Cell Sci 124: 1571-1580. jcs.069500 [pii]; doi: 10.1242/jcs.069500 PMID: 21486945
27. Verma R, Oania RS, Kolawa NJ, Deshaies RJ (2013) Cdc48/p97 promotes degradation of aberrant nascent polypeptides bound to the ribosome. Elife 2: e00308. 00308 [pii]. doi: 10.7554/eLife.00308 PMID: 23358411
28. Ikai N, Yanagida M (2006) Cdc48 is required for the stability of Cut1/separase in mitotic anaphase. J Struct Biol 156: 50-61. S1047-8477(06)00128-6 [pii]; doi: 10.1016/j.jsb.2006.04.003 PMID: 16904908
29. Yuasa T, Hayashi T, Ikai N, Katayama T, Aoki K, et al. (2004) An interactive gene network for securinseparase, condensin, cohesin, Dis1/Mtc1 and histones constructed by mass transformation. Genes Cells 9: 1069-1082. GTC790 [pii]; doi: 10.1111/j.1365-2443.2004.00790.x PMID: 15507118
30. Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823. PMID: 2005825
31. Moir D, Stewart SE, Osmond BC, Botstein D (1982) Cold-sensitive cell-division-cycle mutants of yeast: isolation, properties, and pseudoreversion studies. Genetics 100: 547-563. PMID: 6749598
32. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415: 871-880. nature724 [pii]. doi: 10.1038/nature724 PMID: 11859360
33. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359. nmeth.1923 [pii]; doi: 10.1038/nmeth.1923 PMID: 22388286
34. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079. btp352 [pii]; doi: 10.1093/bioinformatics/btp352 PMID: 19505943
35. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297-1303. gr.107524.110 [pii]; doi: 10.1101/gr.107524.110 PMID: 20644199
36. Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, et al. (2009) VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 25: 2283-2285. btp373 [pii]; doi: 10.1093/bioinformatics/btp373 PMID: 19542151
37. Davies JM, Brunger AT, Weis WI (2008) Improved structures of full-length p97, an AAA ATPase: implications for mechanisms of nucleotide-dependent conformational change. Structure 16: 715-726. S0969-2126(08)00098-1 [pii]; doi: 10.1016/j.str.2008.02.010 PMID: 18462676
38. Li H, Robertson AD, Jensen JH (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins 61: 704-721. doi: 10.1002/prot.20660 PMID: 16231289
39. Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, et al. (2011) Comparative functional genomics of the fission yeasts. Science 332: 930-936. science.1203357 [pii]; doi: 10.1126/science.1203357 PMID: 21511999
40. Naula N, Hilti N, Schweingruber AM, Schweingruber ME (2003) Cordycepin in Schizosaccharomyces pombe: effects on the wild type and phenotypes of mutants resistant to the drug. Curr Genet 43: 400-406. doi: 10.1007/s00294-003-0413-4 PMID: 12827445
41. Hayles J, Wood V, Jeffery L, Hoe KL, Kim DU, et al. (2013) A genome-wide resource of cell cycle and cell shape genes of fission yeast. Open Biol 3: 130053. rsob.130053 [pii]; doi: 10.1098/rsob.130053 PMID: 23697806
42. Roguev A, Wiren M, Weissman JS, Krogan NJ (2007) High-throughput genetic interaction mapping in the fission yeast Schizosaccharomyces pombe. Nat Methods 4: 861-866. nmeth1098 [pii]; doi: 10. 1038/nmeth1098 PMID: 17893680
43. Kriegenburg F, Jakopec V, Poulsen EG, Nielsen SV, Roguev A, et al. (2014) A chaperone-assisted degradation pathway targets kinetochore proteins to ensure genome stability. PLoS Genet 10: e1004140. PGENETICS-D-13-02357 [pii]. doi: 10.1371/journal.pgen.1004140 PMID: 24497846
44. Bebeacua C, Forster A, McKeown C, Meyer HH, Zhang X, et al. (2012) Distinct conformations of the protein complex p97-Ufd1-Npl4 revealed by electron cryomicroscopy. Proc Natl Acad Sci U S A 109: 1098-1103. 1114341109 [pii]; doi: 10.1073/pnas.1114341109 PMID: 22232657
45. Park S, Isaacson R, Kim HT, Silver PA, Wagner G (2005) Ufd1 exhibits the AAA-ATPase fold with two distinct ubiquitin interaction sites. Structure 13: 995-1005. S0969- 2126(05)00178-4 [pii]; doi: 10. 1016/j.str.2005.04.013 PMID: 16004872