1,311
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Neurodegenerative disease-associated inclusion bodies are cleared by selective autophagy in budding yeast

, , , &
Article: 2236407 | Received 10 Feb 2023, Accepted 06 Jul 2023, Published online: 07 Aug 2023

References

  • Davies SW, Turmaine M, Cozens BA, et al. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell. 1997;90(3):537–26.
  • Higgins R, Kabbaj MH, Sherwin D, et al. The Cdc48 complex alleviates the cytotoxicity of misfolded proteins by regulating ubiquitin homeostasis. Cell Rep. 2020;32(2):107898. Epub 2020/07/16. PubMed PMID: 32668237; PubMed Central PMCID: PMCPMC7392062.
  • Kim YE, Hosp F, Frottin F, et al. Soluble oligomers of PolyQ-expanded huntingtin target a multiplicity of key cellular factors. Mol Cell. 2016;63(6):951–964. Epub 2016/08/30. PubMed PMID: 27570076.
  • Folger A, Wang Y. The cytotoxicity and clearance of mutant huntingtin and other misfolded proteins. Cells. 2021;10:2835. Epub 2021/11/28. PubMed PMID: 34831058; PubMed Central PMCID: PMCPMC8616338. doi: 10.3390/cells10112835.
  • Ross CA, Poirier MA. Protein aggregation and neurodegenerative disease. Nat Med. 2004;10:S10–S17. Epub 2004/07/24. PubMed PMID: 15272267. doi: 10.1038/nm1066.
  • Carra S, Seguin SJ, Landry J. HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy. 2008;4:237–239. Epub 2007/12/21. PubMed PMID: 18094623. doi: 10.4161/auto.5407.
  • Lu K, den Brave F, Jentsch S. Receptor oligomerization guides pathway choice between proteasomal and autophagic degradation. Nat Cell Biol. 2017;19(6):732–739. PubMed PMID: 28504708
  • Demand J, Alberti S, Patterson C, et al. Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr Biol. 2001;11(20):1569–1577. PubMed PMID: 11676916
  • McColgan P, Tabrizi SJ. Huntington’s disease: a clinical review. Eur J Neurol. 2018;25:24–34. Epub 2017/08/18. PubMed PMID: 28817209. doi: 10.1111/ene.13413.
  • Ross CA, Tabrizi SJ. Huntington’s disease: from molecular pathogenesis to clinical treatment. Lancet Neurol. 2011;10:83–98. Epub 2010/12/18. PubMed PMID: 21163446. doi: 10.1016/S1474-4422(10)70245-3.
  • Sathasivam K, Neueder A, Gipson TA, et al. Aberrant splicing of HTT generates the pathogenic exon 1 protein in Huntington disease. Proc Natl Acad Sci U S A. 2013;110(6):2366–2370. Epub 2013/01/24. PubMed PMID: 23341618; PubMed Central PMCID: PMCPMC3568346.
  • Mangiarini L, Sathasivam K, Seller M, et al. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 1996;87(3):493–506.
  • Peskett TR, Rau F, O’Driscoll J, et al. A liquid to solid phase transition underlying pathological huntingtin exon1 aggregation. Mol Cell. 2018;70:588–601 e6. Epub 2018/05/15. PubMed PMID: 29754822; PubMed Central PMCID: PMCPMC5971205. doi: 10.1016/j.molcel.2018.04.007.
  • Bauerlein FJB, Saha I, Mishra A, et al. In situ architecture and cellular interactions of polyQ inclusions. Cell. 2017;171(1):179–87 e10.
  • Gruber A, Hornburg D, Antonin M, et al. Molecular and structural architecture of polyQ aggregates in yeast. Proc Natl Acad Sci U S A. 2018;115(15):E3446–E53. Epub 2018/03/28. PubMed PMID: 29581260; PubMed Central PMCID: PMCPMC5899447.
  • Riguet N, Mahul-Mellier AL, Maharjan N, et al. Nuclear and cytoplasmic huntingtin inclusions exhibit distinct biochemical composition, interactome and ultrastructural properties. Nat Commun. 2021;12(1):6579. Epub 2021/11/14. PubMed PMID: 34772920; PubMed Central PMCID: PMCPMC8589980 neurodegenerative diseases, including from Merck Serono, UCB, and Abbvie. These companies had no specific role in the conceptualization, preparation, and decision to publish this work. H.A.L is also the co-founder and Chief Scientific Officer of ND BioSciences SA, a company that develops diagnostics and treatments for neurodegenerative diseases based on platforms that reproduce the complexity and diversity of proteins implicated in neurodegenerative diseases and their pathologies. All other authors declare no competing interests.
  • Leitman J, Ulrich Hartl F, Lederkremer GZ. Soluble forms of polyQ-expanded huntingtin rather than large aggregates cause endoplasmic reticulum stress. Nat Commun. 2013;4:2753. Epub 2013/11/13. PubMed PMID: 24217578. doi: 10.1038/ncomms3753.
  • Nakatogawa H, Suzuki K, Kamada Y, et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–467. Epub 2009/06/06. PubMed PMID: 19491929. doi: 10.1038/nrm2708.
  • Wen X, Klionsky DJ. An overview of macroautophagy in yeast. J Mol Biol. 2016;428:1681–1699. Epub 2016/02/26. PubMed PMID: 26908221; PubMed Central PMCID: PMCPMC4846508. doi: 10.1016/j.jmb.2016.02.021.
  • Farre JC, Subramani S. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat Rev Mol Cell Biol. 2016;17(9):537–552. PubMed PMID: 27381245
  • Hara T, Nakamura K, Matsui M, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006;441(7095):885–889. Epub 2006/04/21. PubMed PMID: 16625204.
  • Komatsu M, Waguri S, Chiba T, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006;441(7095):880–884. Epub 2006/04/21. PubMed PMID: 16625205.
  • Shen WC, Li HY, Chen GC, et al. Mutations in the ubiquitin-binding domain of OPTN/optineurin interfere with autophagy-mediated degradation of misfolded proteins by a dominant-negative mechanism. Autophagy. 2015;11:685–700. Epub 2014/12/09. PubMed PMID: 25484089; PubMed Central PMCID: PMCPMC4502753. doi: 10.4161/auto.36098.
  • Filimonenko M, Isakson P, Finley KD, et al. The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol Cell. 2010;38(2):265–279. Epub 2010/04/27. PubMed PMID: 20417604; PubMed Central PMCID: PMCPMC2867245.
  • Park H, Kang JH, Lee S. Autophagy in neurodegenerative diseases: a hunter for aggregates. Int J Mol Sci. 2020;21(9): Epub 2020/05/14. PubMed PMID: 32397599; PubMed Central PMCID: PMCPMC7247013. doi: 10.3390/ijms21093369.
  • Lu K, Psakhye I, Jentsch S. Autophagic clearance of polyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell. 2014;158:549–563. Epub 2014/07/22. PubMed PMID: 25042851. doi: 10.1016/j.cell.2014.05.048.
  • LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer’s disease. Nat Rev Neurosci. 2007;8:499–509. Epub 2007/06/07. PubMed PMID: 17551515. doi: 10.1038/nrn2168.
  • Villar-Pique A, Ventura S. Protein aggregation propensity is a crucial determinant of intracellular inclusion formation and quality control degradation. Biochim Biophys Acta. 2013;1833:2714–2724. Epub 2013/07/17. PubMed PMID: 23856334. doi: 10.1016/j.bbamcr.2013.06.023.
  • Ring J, Tadic J, Ristic S, et al. The HSP40 chaperone Ydj1 drives amyloid beta 42 toxicity. EMBO Mol Med. 2022;14(5):e13952. Epub 2022/04/05. PubMed PMID: 35373908; PubMed Central PMCID: PMCPMC9081910.
  • Park SK, Pegan SD, Mesecar AD, et al. Development and validation of a yeast high-throughput screen for inhibitors of Abeta(4)(2) oligomerization. Dis Model Mech. 2011;4:822–831. Epub 2011/08/04. PubMed PMID: 21810907; PubMed Central PMCID: PMCPMC3209651. doi: 10.1242/dmm.007963.
  • Treusch S, Hamamichi S, Goodman JL, et al. Functional links between Abeta toxicity, endocytic trafficking, and Alzheimer’s disease risk factors in yeast. Science. 2011;334(6060):1241–1245. Epub 2011/10/29. PubMed PMID: 22033521; PubMed Central PMCID: PMCPMC3281757.
  • Perrino G, Wilson C, Santorelli M, et al. Quantitative characterization of alpha-synuclein aggregation in living cells through automated microfluidics feedback control. Cell Rep. 2019;27:916–27 e5. Epub 2019/04/18. PubMed PMID: 30995486; PubMed Central PMCID: PMCPMC6484782. doi: 10.1016/j.celrep.2019.03.081.
  • Ocampo A, Liu J, Barrientos A. NAD+ salvage pathway proteins suppress proteotoxicity in yeast models of neurodegeneration by promoting the clearance of misfolded/oligomerized proteins. Hum Mol Genet. 2013;22:1699–1708. Epub 2013/01/22. PubMed PMID: 23335597; PubMed Central PMCID: PMCPMC3657478. doi: 10.1093/hmg/ddt016.
  • Chuang KH, Liang F, Higgins R, et al. Ubiquilin/Dsk2 promotes inclusion body formation and vacuole (lysosome)-mediated disposal of mutated huntingtin. Mol Biol Cell. 2016;27(13):2025–2036. PubMed PMID: 27170182
  • Higgins R, Kabbaj MH, Hatcher A, et al. The absence of specific yeast heat-shock proteins leads to abnormal aggregation and compromised autophagic clearance of mutant Huntingtin proteins. PLoS One. 2018;13(1):e0191490. PubMed PMID: 29346421
  • Iwata A, Christianson JC, Bucci M, et al. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc Natl Acad Sci U S A. 2005;102(37):13135–13140. Epub 2005/09/06. PubMed PMID: 16141322; PubMed Central PMCID: PMCPMC1201602.
  • Lu K, Psakhye I, Jentsch S. A new class of ubiquitin-Atg8 receptors involved in selective autophagy and polyQ protein clearance. Autophagy. 2014;10:2381–2382. Epub 2014/12/04. PubMed PMID: 25470352; PubMed Central PMCID: PMCPMC4502744. doi: 10.4161/15548627.2014.981919.
  • Xie Z, Nair U, Klionsky DJ. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell. 2008;19:3290–3298. Epub 2008/05/30. PubMed PMID: 18508918; PubMed Central PMCID: PMC2488302. doi: 10.1091/mbc.E07-12-1292.
  • Ammerer G, Hunter CP, Rothman JH, et al. PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol Cell Biol. 1986;6(7): 2490–2499. PubMed PMID: 3023936; PubMed Central PMCID: PMCPMC367803.
  • Toulmay A, Prinz WA. Direct imaging reveals stable, micrometer-scale lipid domains that segregate proteins in live cells. J Cell Biol. 2013;202(1):35–44. PubMed PMID: 23836928; PubMed Central PMCID: PMCPMC3704982
  • Duennwald ML, Jagadish S, Muchowski PJ, et al. Flanking sequences profoundly alter polyglutamine toxicity in yeast. Proc Natl Acad Sci U S A. 2006;103:11045–11050. Epub 2006/07/13. 0604547103 [pii]. PubMed PMID: 16832050. doi: 10.1073/pnas.0604547103.
  • Glover JR, Lindquist S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell. 1998;94(1): 73–82. PubMed PMID: 9674429.
  • Nair U, Cao Y, Xie Z, et al. Roles of the lipid-binding motifs of Atg18 and Atg21 in the cytoplasm to vacuole targeting pathway and autophagy. J Biol Chem. 2010;285:11476–11488. Epub 2010/02/16. PubMed PMID: 20154084; PubMed Central PMCID: PMCPMC2857026. doi: 10.1074/jbc.M109.080374.
  • Epple UD, Suriapranata I, Eskelinen EL, et al. Aut5/Cvt17p, a putative lipase essential for disintegration of autophagic bodies inside the vacuole. J Bacteriol. 2001;183:5942–5955. Epub 2001/09/22. PubMed PMID: 11566994; PubMed Central PMCID: PMCPMC99673.doi: 10.1128/JB.183.20.5942-5955.2001.
  • Teter SA, Eggerton KP, Scott SV, et al. Degradation of lipid vesicles in the yeast vacuole requires function of Cvt17, a putative lipase. J Biol Chem. 2001;276:2083–2087. Epub 2000/11/22. PubMed PMID: 11085977; PubMed Central PMCID: PMCPMC2749705. doi: 10.1074/jbc.C000739200.
  • Hirata E, Shirai K, Kawaoka T, et al. Atg15 in Saccharomyces cerevisiae consists of two functionally distinct domains. Mol Biol Cell. 2021;32:645–663. Epub 2021/02/25. PubMed PMID: 33625870; PubMed Central PMCID: PMCPMC8108511. doi: 10.1091/mbc.E20-07-0500.
  • Kawamata T, Makino S, Kagohashi Y, et al. A method for the isolation and characterization of autophagic bodies from yeast provides a key tool to investigate cargos of autophagy. J Biol Chem. 2022;298:102641. Epub 2022/10/29. PubMed PMID: 36306824; PubMed Central PMCID: PMCPMC9700044. doi: 10.1016/j.jbc.2022.102641.
  • Buchan JR, Kolaitis RM, Taylor JP, et al. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell. 2013;153(7):1461–1474. PubMed PMID: 23791177; PubMed Central PMCID: PMCPMC3760148
  • Boutouja F, Stiehm CM, Mastalski T, et al. Vps10-mediated targeting of Pep4 determines the activity of the vacuole in a substrate-dependent manner. Sci Rep. 2019;9(1):10557. Epub 2019/07/25. PubMed PMID: 31332264; PubMed Central PMCID: PMCPMC6646403.
  • Zhang A, Meng Y, Li Q, et al. The endosomal sorting complex required for transport complex negatively regulates Erg6 degradation under specific glucose restriction conditions. Traffic. 2020;21:488–502. Epub 2020/05/08. PubMed PMID: 32378292. doi: 10.1111/tra.12732.
  • Suzuki K, Kondo C, Morimoto M, et al. Selective transport of alpha-mannosidase by autophagic pathways: identification of a novel receptor, Atg34p. J Biol Chem. 2010;285:30019–30025. Epub 2010/07/20. PubMed PMID: 20639194; PubMed Central PMCID: PMCPMC2943286. doi: 10.1074/jbc.M110.143511.
  • Motley AM, Nuttall JM, Hettema EH. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 2012;31:2852–2868. Epub 2012/05/31. PubMed PMID: 22643220; PubMed Central PMCID: PMCPMC3395097. doi: 10.1038/emboj.2012.151.
  • Kanki T, Wang K, Cao Y, et al. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell. 2009;17:98–109. Epub 2009/07/22. PubMed PMID: 19619495; PubMed Central PMCID: PMCPMC2746076. doi: 10.1016/j.devcel.2009.06.014.
  • Mochida K, Oikawa Y, Kimura Y, et al. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature. 2015;522(7556):359–362. Epub 2015/06/05. PubMed PMID: 26040717.
  • Shintani T, Huang WP, Stromhaug PE, et al. Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev Cell. 2002;3:825–837. Epub 2002/12/14. PubMed PMID: 12479808; PubMed Central PMCID: PMCPMC2737732. doi: 10.1016/s1534-5807(02)00373-8.
  • Matscheko N, Mayrhofer P, Rao Y, et al. Atg11 tethers Atg9 vesicles to initiate selective autophagy. PLoS Biol. 2019;17:e3000377. Epub 2019/07/30. PubMed PMID: 31356628; PubMed Central PMCID: PMCPMC6687201. doi: 10.1371/journal.pbio.3000377.
  • Kamber RA, Shoemaker CJ, Denic V. Receptor-bound targets of selective autophagy use a scaffold protein to activate the Atg1 kinase. Mol Cell. 2015;59:372–381. Epub 2015/07/15. PubMed PMID: 26166702; PubMed Central PMCID: PMCPMC5602610. doi: 10.1016/j.molcel.2015.06.009.
  • Ragusa MJ, Stanley RE, Hurley JH. Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell. 2012;151:1501–1512. Epub 2012/12/12. PubMed PMID: 23219485; PubMed Central PMCID: PMCPMC3806636. doi: 10.1016/j.cell.2012.11.028.
  • Krick R, Muehe Y, Prick T, et al. Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol Biol Cell. 2008;19(10):4492–4505. Epub 2008/08/15. PubMed PMID: 18701704; PubMed Central PMCID: PMCPMC2555948.
  • Cheong H, Yorimitsu T, Reggiori F, et al. Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell. 2005;16:3438–3453. Epub 2005/05/20. PubMed PMID: 15901835; PubMed Central PMCID: PMCPMC1165424. doi: 10.1091/mbc.e04-10-0894.
  • Kanki T, Wang K, Baba M, et al. A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol Biol Cell. 2009;20(22):4730–4738. Epub 2009/10/02. PubMed PMID: 19793921; PubMed Central PMCID: PMCPMC2777103.
  • Sekito T, Kawamata T, Ichikawa R, et al. Atg17 recruits Atg9 to organize the pre-autophagosomal structure. Genes Cells. 2009;14:525–538. Epub 2009/04/18. PubMed PMID: 19371383. doi: 10.1111/j.1365-2443.2009.01299.x.
  • Rao Y, Perna MG, Hofmann B, et al. The Atg1-kinase complex tethers Atg9-vesicles to initiate autophagy. Nat Commun. 2016;7:10338. Epub 2016/01/13. PubMed PMID: 26753620; PubMed Central PMCID: PMCPMC4729957. doi: 10.1038/ncomms10338.
  • Mochida K, Yamasaki A, Matoba K, et al. Super-assembly of ER-phagy receptor Atg40 induces local ER remodeling at contacts with forming autophagosomal membranes. Nat Commun. 2020;11:3306. Epub 2020/07/06. PubMed PMID: 32620754; PubMed Central PMCID: PMCPMC7335187. doi: 10.1038/s41467-020-17163-y.
  • Farre JC, Burkenroad A, Burnett SF, et al. Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11. EMBO Rep. 2013;14:441–449. Epub 2013/04/06. PubMed PMID: 23559066; PubMed Central PMCID: PMCPMC3642380. doi: 10.1038/embor.2013.40.
  • Marshall RS, Hua Z, Mali S, et al. ATG8-binding UIM proteins define a new class of autophagy adaptors and receptors. Cell. 2019;177:766–81 e24. Epub 2019/04/09. PubMed PMID: 30955882. doi: 10.1016/j.cell.2019.02.009.
  • Zhou F, Wu Z, Zhao M, et al. Rab5-dependent autophagosome closure by ESCRT. J Cell Biol. 2019;218(6):1908–1927. Epub 2019/04/24. PubMed PMID: 31010855; PubMed Central PMCID: PMCPMC6548130.
  • Schafer JA, Schessner JP, Bircham PW, et al. ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast. EMBO J. 2020;39(2):e102586. Epub 2019/12/06. PubMed PMID: 31802527; PubMed Central PMCID: PMCPMC6960443.
  • Shen K, Calamini B, Fauerbach JA, et al. Control of the structural landscape and neuronal proteotoxicity of mutant Huntingtin by domains flanking the polyQ tract. Elife. 2016;5. PubMed PMID: 27751235; PubMed Central PMCID: PMCPMC5135392. doi: 10.7554/eLife.18065
  • Meguro S, Zhuang X, Kirisako H, et al. Pex3 confines pexophagy receptor activity of Atg36 to peroxisomes by regulating Hrr25-mediated phosphorylation and proteasomal degradation. J Biol Chem. 2020;295:16292–16298. Epub 2020/09/23. PubMed PMID: 32958557; PubMed Central PMCID: PMCPMC7705307. doi: 10.1074/jbc.RA120.013565.
  • Chen S, Desai T, McNew JA, et al. Lunapark stabilizes nascent three-way junctions in the endoplasmic reticulum. Proc Natl Acad Sci U S A. 2015;112:418–423. Epub 2014/12/31. PubMed PMID: 25548161; PubMed Central PMCID: PMCPMC4299238. doi: 10.1073/pnas.1423026112.
  • Anandhan A, Rodriguez-Rocha H, Bohovych I, et al. Overexpression of alpha-synuclein at non-toxic levels increases dopaminergic cell death induced by copper exposure via modulation of protein degradation pathways. Neurobiol Dis. 2015;81:76–92. Epub 2014/12/17. PubMed PMID: 25497688; PubMed Central PMCID: PMCPMC4459946. doi: 10.1016/j.nbd.2014.11.018.
  • Hyttinen JM, Amadio M, Viiri J, et al. Clearance of misfolded and aggregated proteins by aggrephagy and implications for aggregation diseases. Ageing Res Rev. 2014;18:16–28. Epub 2014/07/27. PubMed PMID: 25062811. doi: 10.4161/auto.36098.
  • Lamark T, Johansen T. Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int J Cell Biol. 2012;2012:736905. Epub 2012/04/21. PubMed PMID: 22518139; PubMed Central PMCID: PMC3320095. doi: 10.1128/mcb.6.7.2490-2499.1986.
  • Kabeya Y, Noda NN, Fujioka Y, et al. Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvation-induced autophagy in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 2009;389:612–615. Epub 2009/09/17. PubMed PMID: 19755117. doi: 10.1016/j.bbrc.2009.09.034.
  • Deosaran E, Larsen KB, Hua R, et al. NBR1 acts as an autophagy receptor for peroxisomes. J Cell Sci. 2013;126(Pt 4):939–952. Epub 2012/12/15. PubMed PMID: 23239026.
  • Yamashita S, Abe K, Tatemichi Y, et al. The membrane peroxin PEX3 induces peroxisome-ubiquitination-linked pexophagy. Autophagy. 2014;10:1549–1564. Epub 2014/07/10. PubMed PMID: 25007327; PubMed Central PMCID: PMCPMC4206534. doi: 10.4161/auto.29329.
  • Longtine MS, McKenzie A 3rd, Demarini DJ, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 1998;14(10):953–961.
  • Tanaka C, Tan LJ, Mochida K, et al. Hrr25 triggers selective autophagy-related pathways by phosphorylating receptor proteins. J Cell Biol. 2014;207(1):91–105. Epub 2014/10/08. PubMed PMID: 25287303; PubMed Central PMCID: PMCPMC4195827.
  • Tong AH, Evangelista M, Parsons AB, et al. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science. 2001;294(5550):2364–2368.
  • Daniel JA, Yoo J, Bettinger BT, et al. Eliminating gene conversion improves high-throughput genetics in Saccharomyces cerevisiae. Genetics. 2006;172(1):709–711. PubMed PMID: 16157664; PubMed Central PMCID: PMCPMC1456194