Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica

BMC Genomics

Volumn 17, Issue 1, 2016, Pages

  Pomraning, Kyle R ^a   Kim, Young Mo ^a   Nicora, Carrie D ^a   Chu, Rosalie K ^a   Bredeweg, Erin L ^a   Purvine, Samuel O ^a   Hu, Dehong ^a   Metz, Thomas O ^a   Baker, Scott E ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Beta oxidation; Lipid; Metabolome; Nitrogen; Phosphoproteome; Phosphorylation; Proteome; Regulation; Ribosome biogenesis; Translation; Yarrowia lipolytica

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE CITRATE SYNTHASE; ALANINE; CITRIC ACID; DNA BINDING PROTEIN; FUMARIC ACID; LIPID; MALIC ACID; NITROGEN; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; PROTEOME; PUTRESCINE; SPERMIDINE; SUGAR ALCOHOL; TRANSCRIPTION FACTOR; UREA; ACETYL COENZYME A; FUNGAL DNA; FUNGAL PROTEIN;

ARTICLE; ASCOMYCETES; CITRIC ACID CYCLE; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; FATTY ACID OXIDATION; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; METABOLOME; NONHUMAN; PROTEIN PHOSPHORYLATION; STRUCTURAL GENE; UPREGULATION; YARROWIA LIPOLYTICA; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; YARROWIA;

ACETYL COENZYME A; CITRIC ACID; DNA, FUNGAL; FUNGAL PROTEINS; LIPID METABOLISM; METABOLOME; NITROGEN; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEOME; YARROWIA;

EID: 84959172287     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-016-2471-2     Document Type: Article

References (104)

1. Athenstaedt K, Jolivet P, Boulard C, Zivy M, Negroni L, Nicaud JM, et al. Lipid particle composition of the yeast Yarrowia lipolytica depends on the carbon source. Proteomics. 2006;6(5):1450-9. doi: 10.1002/pmic.200500339.
2. Beopoulos A, Chardot T, Nicaud JM. Yarrowia lipolytica: A model and a tool to understand the mechanisms implicated in lipid accumulation. Biochimie. 2009;91(6):692-6. doi: 10.1016/j.biochi.2009.02.004.
3. Ageitos JM, Vallejo JA, Veiga-Crespo P, Villa TG. Oily yeasts as oleaginous cell factories. Appl Microbiol Biotechnol. 2011;90(4):1219-27. doi: 10.1007/s00253-011-3200-z.
4. Morin N, Cescut J, Beopoulos A, Lelandais G, Le Berre V, Uribelarrea JL, et al. Transcriptomic Analyses during the Transition from Biomass Production to Lipid Accumulation in the Oleaginous Yeast Yarrowia lipolytica. Plos One. 2011;6(11):e27966. 10.1371/journal.pone.0027966.
5. Sitepu IR, Sestric R, Ignatia L, Levin D, German JB, Gillies LA, et al. Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Bioresour Technol. 2013;144:360-9. doi: 10.1016/j.biortech.2013.06.047.
6. Blazeck J, Hill A, Liu LQ, Knight R, Miller J, Pan A, et al. Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production. Nat Commun. 2014;5:3131. doi: 10.1038/Ncomms4131.
7. Cooper TG. Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiol Rev. 2002;26(3):223-38.
8. Gagiano M, Bauer FF, Pretorius IS. The sensing of nutritional status and the relationship to filamentous growth in Saccharomyces cerevisiae. Fems Yeast Res. 2002;2(4):433-70.
9. Magasanik B, Kaiser CA. Nitrogen regulation in Saccharomyces cerevisiae. Gene. 2002;290(1-2):1-18.
10. Wong KH, Hynes MJ, Davis MA. Recent advances in nitrogen regulation: a comparison between Saccharomyces cerevisiae and filamentous fungi. Eukaryot Cell. 2008;7(6):917-25. doi: 10.1128/EC.00076-08.
11. Zaman S, Lippman SI, Zhao X, Broach JR. How Saccharomyces responds to nutrients. Annu Rev Genet. 2008;42:27-81. doi: 10.1146/annurev.genet.41.110306.130206.
12. Conrad M, Schothorst J, Kankipati HN, Van Zeebroeck G, Rubio-Texeira M, Thevelein JM. Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev. 2014;38(2):254-99. doi: 10.1111/1574-6976.12065.
13. Rodkaer SV, Faergeman NJ. Glucose- and nitrogen sensing and regulatory mechanisms in Saccharomyces cerevisiae. Fems Yeast Res. 2014;14(5):683-96. doi: 10.1111/1567-1364.12157.
14. Marzluf GA. Genetic regulation of nitrogen metabolism in the fungi. Microbiol Mol Biol Rev. 1997;61(1):17-32.
15. Kulkarni AA, Abul-Hamd AT, Rai R, El Berry H, Cooper TG. Gln3p nuclear localization and interaction with Ure2p in Saccharomyces cerevisiae. J Biol Chem. 2001;276(34):32136-44. doi: 10.1074/jbc.M104580200.
16. Cox KH, Rai R, Distler M, Daugherty JR, Coffman JA, Cooper TG. Saccharomyces cerevisiae GATA sequences function as TATA elements during nitrogen catabolite repression and when Gln3p is excluded from the nucleus by overproduction of Ure2p. J Biol Chem. 2000;275(23):17611-8. doi: 10.1074/jbc.M001648200.
17. Beck T, Hall MN. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature. 1999;402(6762):689-92. doi: 10.1038/45287.
18. Cunningham TS, Andhare R, Cooper TG. Nitrogen catabolite repression of DAL80 expression depends on the relative levels of Gat1p and Ure2p production in Saccharomyces cerevisiae. J Biol Chem. 2000;275(19):14408-14.
19. Georis I, Feller A, Vierendeels F, Dubois E. The yeast GATA factor Gat1 occupies a central position in nitrogen catabolite repression-sensitive gene activation. Mol Cell Biol. 2009;29(13):3803-15. doi: 10.1128/MCB.00399-09.
20. Coffman JA, Rai R, Loprete DM, Cunningham T, Svetlov V, Cooper TG. Cross regulation of four GATA factors that control nitrogen catabolic gene expression in Saccharomyces cerevisiae. J Bacteriol. 1997;179(11):3416-29.
21. Mazurie A, Bottani S, Vergassola M. An evolutionary and functional assessment of regulatory network motifs. Genome Biol. 2005;6(4):R35. doi: 10.1186/gb-2005-6-4-r35.
22. Lavoie H, Hogues H, Whiteway M. Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi. Curr Opin Microbiol. 2009;12(6):655-63. doi: 10.1016/j.mib.2009.09.015.
23. Ratledge C. Fatty acid biosynthesis in microorganisms being used for Single Cell Oil production. Biochimie. 2004;86(11):807-15. doi: 10.1016/j.biochi.2004.09.017.
24. Garay LA, Boundy-Mills KL, German JB. Accumulation of high-value lipids in single-cell microorganisms: a mechanistic approach and future perspectives. J Agric Food Chem. 2014;62(13):2709-27. doi: 10.1021/jf4042134.
25. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, et al. Genome evolution in yeasts. Nature. 2004;430(6995):35-44. doi: 10.1038/nature02579.
26. Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, et al. A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun. 2012;3:1112. doi: 10.1038/ncomms2112.
27. Garreau de Loubresse N, Prokhorova I, Holtkamp W, Rodnina MV, Yusupova G, Yusupov M. Structural basis for the inhibition of the eukaryotic ribosome. Nature. 2014;513(7519):517-22. doi: 10.1038/nature13737.
28. Blinder D, Magasanik B. Recognition of nitrogen-responsive upstream activation sequences of Saccharomyces cerevisiae by the product of the GLN3 gene. J Bacteriol. 1995;177(14):4190-3.
29. Ravagnani A, Gorfinkiel L, Langdon T, Diallinas G, Adjadj E, Demais S, et al. Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter-specific recognition by the Aspergillus nidulans GATA factor AreA. EMBO J. 1997;16(13):3974-86. doi: 10.1093/emboj/16.13.3974.
30. Courchesne WE, Magasanik B. Regulation of nitrogen assimilation in Saccharomyces cerevisiae: roles of the URE2 and GLN3 genes. J Bacteriol. 1988;170(2):708-13.
31. Kudla B, Caddick MX, Langdon T, Martinez-Rossi NM, Bennett CF, Sibley S, et al. The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J. 1990;9(5):1355-64.
32. Arndt K, Fink GR. GCN4 protein, a positive transcription factor in yeast, binds general control promoters at all 5' TGACTC 3' sequences. Proc Natl Acad Sci USA. 1986;83(22):8516-20.
33. Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, et al. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol Cell Biol. 2001;21(13):4347-68. doi: 10.1128/MCB.21.13.4347-4368.2001.
34. MacIsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD, Fraenkel E. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics. 2006;7:113. doi: 10.1186/1471-2105-7-113.
35. Badis G, Chan ET, van Bakel H, Pena-Castillo L, Tillo D, Tsui K, et al. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol Cell. 2008;32(6):878-87. doi: 10.1016/j.molcel.2008.11.020.
36. Meimoun A, Holtzman T, Weissman Z, McBride HJ, Stillman DJ, Fink GR, et al. Degradation of the transcription factor Gcn4 requires the kinase Pho85 and the SCF(CDC4) ubiquitin-ligase complex. Mol Biol Cell. 2000;11(3):915-27.
37. Liko D, Slattery MG, Heideman W. Stb3 binds to ribosomal RNA processing element motifs that control transcriptional responses to growth in Saccharomyces cerevisiae. J Biol Chem. 2007;282(36):26623-8. doi: 10.1074/jbc.M704762200.
38. Liko D, Conway MK, Grunwald DS, Heideman W. Stb3 plays a role in the glucose-induced transition from quiescence to growth in Saccharomyces cerevisiae. Genetics. 2010;185(3):797-810. doi: 10.1534/genetics.110.116665.
39. Huber A, French SL, Tekotte H, Yerlikaya S, Stahl M, Perepelkina MP, et al. Sch9 regulates ribosome biogenesis via Stb3, Dot6 and Tod6 and the histone deacetylase complex RPD3L. EMBO J. 2011;30(15):3052-64. doi: 10.1038/emboj.2011.221.
40. Lundin M, Nehlin JO, Ronne H. Importance of a flanking AT-rich region in target site recognition by the GC box-binding zinc finger protein MIG1. Mol Cell Biol. 1994;14(3):1979-85.
41. Cubero B, Scazzocchio C. Two different, adjacent and divergent zinc finger binding sites are necessary for CREA-mediated carbon catabolite repression in the proline gene cluster of Aspergillus nidulans. EMBO J. 1994;13(2):407-15.
42. Wang ZP, Xu HM, Wang GY, Chi Z, Chi ZM. Disruption of the MIG1 gene enhances lipid biosynthesis in the oleaginous yeast Yarrowia lipolytica ACA-DC 50109. Biochim Biophys Acta. 2013;1831(4):675-82. doi: 10.1016/j.bbalip.2012.12.010.
43. Ephrussi A, Church GM, Tonegawa S, Gilbert W. B lineage--specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science. 1985;227(4683):134-40.
44. Newburger DE, Bulyk ML. UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res. 2009;37(Database issue):D77-82. doi: 10.1093/nar/gkn660.
45. Ratledge C. Regulation of lipid accumulation in oleaginous micro-organisms. Biochem Soc Trans. 2002;30(Pt 6):1047-50. doi:10.1042/.
46. Pomraning KR, Smith KM, Freitag M. Bulk segregant analysis followed by high-throughput sequencing reveals the Neurospora cell cycle gene, ndc-1, to be allelic with the gene for ornithine decarboxylase, spe-1. Eukaryot Cell. 2011;10(6):724-33. doi: 10.1128/EC.00016-11.
47. Serna L, Stadler D. Nuclear division cycle in germinating conidia of Neurospora crassa. J Bacteriol. 1978;136(1):341-51.
48. Evans CT, Ratledge C. Biochemical activities during lipid accumulation in Candida curvata. Lipids. 1983;18(9):630-5.
49. Ratledge C, Wynn JP. The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol. 2002;51:1-51.
50. Zhang H, Zhang L, Chen H, Chen YQ, Chen W, Song Y, et al. Enhanced lipid accumulation in the yeast Yarrowia lipolytica by over-expression of ATP:citrate lyase from Mus musculus. J Biotechnol. 2014;192(Pt A):78-84. doi: 10.1016/j.jbiotec.2014.10.004.
51. Qiao K, Imam Abidi SH, Liu H, Zhang H, Chakraborty S, Watson N, et al. Engineering lipid overproduction in the oleaginous yeast Yarrowia lipolytica. Metab Eng. 2015;29:56-65. doi: 10.1016/j.ymben.2015.02.005.
52. Tai M, Stephanopoulos G. Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab Eng. 2013;15:1-9. doi: 10.1016/j.ymben.2012.08.007.
53. Wagner PD, Vu ND. Phosphorylation of ATP-citrate lyase by nucleoside diphosphate kinase. J Biol Chem. 1995;270(37):21758-64.
54. Ramakrishna S, Benjamin WB. Rapid purification of enzymes of fatty acid biosynthesis from rat adipose tissue. Prep Biochem. 1983;13(5):475-88.
55. Swaney DL, Beltrao P, Starita L, Guo A, Rush J, Fields S, et al. Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat Methods. 2013;10(7):676-82. doi: 10.1038/nmeth.2519.
56. Shi S, Chen Y, Siewers V, Nielsen J. Improving production of malonyl coenzyme A-derived metabolites by abolishing Snf1-dependent regulation of Acc1. mBio. 2014;5(3):e01130-14. doi: 10.1128/mBio.01130-14.
57. Choi JW, Da Silva NA. Improving polyketide and fatty acid synthesis by engineering of the yeast acetyl-CoA carboxylase. J Biotechnol. 2014;187:56-9. doi: 10.1016/j.jbiotec.2014.07.430.
58. Wynn JP, Kendrick A, Hamid AA, Ratledge C. Malic enzyme: a lipogenic enzyme in fungi. Biochem Soc Trans. 1997;25(4):S669.
59. Shapiro BM, Stadtman ER. The regulation of glutamine synthesis in microorganisms. Annu Rev Microbiol. 1970;24:501-24. doi: 10.1146/annurev.mi.24.100170.002441.
60. Hummelt G, Mora J. NADH-dependent glutamate synthase and nitrogen metabolism in Neurospora crassa. Biochem Biophys Res Commun. 1980;92(1):127-33.
61. Dunn-Coleman NS, Robey EA, Tomsett AB, Garrett RH. Glutamate synthase levels in Neurospora crassa mutants altered with respect to nitrogen metabolism. Mol Cell Biol. 1981;1(2):158-64.
62. Middelhoven WJ. The Pathway of Arginine Breakdown in Saccharomyces Cerevisiae. Biochim Biophys Acta. 1964;93:650-2.
63. Magasanik B et al. Regulation of Nitrogen Utilization. In: Molecular and Cellular Biology of the Yeast Saccharomyces: Gene Expression. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1992. p. 283-317.
64. Oberholzer VG, Briddon A. 3-Amino-2-piperidone in the urine of patients with hyperornithinemia. Clin Chim Acta. 1978;87(3):411-5.
65. Camacho JA, Obie C, Biery B, Goodman BK, Hu CA, Almashanu S, et al. Hyperornithinaemia-hyperammonaemia-homocitrullinuria syndrome is caused by mutations in a gene encoding a mitochondrial ornithine transporter. Nat Genet. 1999;22(2):151-8. doi: 10.1038/9658.
66. Pitkin J, Davis RH. The genetics of polyamine synthesis in Neurospora crassa. Arch Biochem Biophys. 1990;278(2):386-91.
67. Pitkin J, Perriere M, Kanehl A, Ristow JL, Davis RH. Polyamine metabolism and growth of neurospora strains lacking Cis-acting control sites in the ornithine decarboxylase gene. Arch Biochem Biophys. 1994;315(1):153-60. doi: 10.1006/abbi.1994.1484.
68. Davis RH, Krasner GN, DiGangi JJ, Ristow JL. Distinct roles of putrescine and spermidine in the regulation of ornithine decarboxylase in Neurospora crassa. Proc Natl Acad Sci U S A. 1985;82(12):4105-9.
69. Sadowski I, Breitkreutz BJ, Stark C, Su TC, Dahabieh M, Raithatha S et al. The PhosphoGRID Saccharomyces cerevisiae protein phosphorylation site database: version 2.0 update. Database: the journal of biological databases and curation. 2013;2013:bat026. doi: 10.1093/database/bat026.
70. Jope RS, Yuskaitis CJ, Beurel E. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem Res. 2007;32(4-5):577-95. doi: 10.1007/s11064-006-9128-5.
71. Zhan XL, Hong Y, Zhu T, Mitchell AP, Deschenes RJ, Guan KL. Essential functions of protein tyrosine phosphatases PTP2 and PTP3 and RIM11 tyrosine phosphorylation in Saccharomyces cerevisiae meiosis and sporulation. Mol Biol Cell. 2000;11(2):663-76.
72. Kassis S, Melhuish T, Annan RS, Chen SL, Lee JC, Livi GP, et al. Saccharomyces cerevisiae Yak1p protein kinase autophosphorylates on tyrosine residues and phosphorylates myelin basic protein on a C-terminal serine residue. Biochem J. 2000;348(Pt 2):263-72.
73. Oliphant AR, Brandl CJ, Struhl K. Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Mol Cell Biol. 1989;9(7):2944-9.
74. Hassanshahian M, Tebyanian H, Cappello S. Isolation and characterization of two crude oil-degrading yeast strains, Yarrowia lipolytica PG-20 and PG-32, from the Persian Gulf. Mar Pollut Bull. 2012;64(7):1386-91. doi: 10.1016/j.marpolbul.2012.04.020.
75. Viljoen BC, Greyling T. Yeasts associated with Cheddar and Gouda making. Int J Food Microbiol. 1995;28(1):79-88.
76. Zinjarde SS, Pant AA. Hydrocarbon degraders from tropical marine environments. Mar Pollut Bull. 2002;44(2):118-21.
77. Barth G, Gaillardin C. Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol Rev. 1997;19(4):219-37.
78. Beopoulos A, Mrozova Z, Thevenieau F, Le Dall MT, Hapala I, Papanikolaou S, et al. Control of lipid accumulation in the yeast Yarrowia lipolytica. Appl Environ Microbiol. 2008;74(24):7779-89. doi: 10.1128/AEM.01412-08.
79. Papanikolaou S, Chevalot I, Komaitis M, Marc I, Aggelis G. Single cell oil production by Yarrowia lipolytica growing on an industrial derivative of animal fat in batch cultures. Appl Microbiol Biot. 2002;58(3):308-12. doi: 10.1007/s00253-001-0897-0.
80. Gietz RD and Woods RA. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 2002;350:87-96.
81. Madzak C, Treton B, Blanchin-Roland S. Strong hybrid promoters and integrative expression/secretion vectors for quasi-constitutive expression of heterologous proteins in the yeast Yarrowia lipolytica. J Mol Microbiol Biotechnol. 2000;2(2):207-16.
82. Pomraning KR, Wei S, Karagiosis SA, Kim YM, Dohnalkova AC, Arey BW, et al. Comprehensive Metabolomic, Lipidomic and Microscopic Profiling of Yarrowia lipolytica during Lipid Accumulation Identifies Targets for Increased Lipogenesis. Plos One. 2015;10(4):e0123188. doi: 10.1371/journal.pone.0123188.
83. Wolinski H, Kohlwein SD. Microscopic analysis of lipid droplet metabolism and dynamics in yeast. Methods Mol Biol. 2008;457:151-63.
84. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671-5.
85. Kamentsky L, Jones TR, Fraser A, Bray MA, Logan DJ, Madden KL, et al. Improved structure, function and compatibility for Cell Profiler: modular high-throughput image analysis software. Bioinformatics. 2011;27(8):1179-80. doi: 10.1093/bioinformatics/btr095.
86. Kim YM, Schmidt BJ, Kidwai AS, Jones MB, Kaiser BLD, Brewer HM, et al. Salmonella modulates metabolism during growth under conditions that induce expression of virulence genes. Mol Biosyst. 2013;9(6):1522-34. doi: 10.1039/C3mb25598k.
87. Hiller K, Hangebrauk J, Jager C, Spura J, Schreiber K, Schomburg D. MetaboliteDetector: comprehensive analysis tool for targeted and nontargeted GC/MS based metabolome analysis. Anal Chem. 2009;81(9):3429-39. doi: 10.1021/ac802689c.
88. Ficarro SB, Adelmant G, Tomar MN, Zhang Y, Cheng VJ, Marto JA. Magnetic bead processor for rapid evaluation and optimization of parameters for phosphopeptide enrichment. Anal Chem. 2009;81(11):4566-75. doi: 10.1021/ac9004452.
89. Yang F, Waters KM, Webb-Robertson BJ, Sowa MB, von Neubeck C, Aldrich JT, et al. Quantitative phosphoproteomics identifies filaggrin and other targets of ionizing radiation in a human skin model. Exp Dermatol. 2012;21(5):352-7. doi: 10.1111/j.1600-0625.2012.01470.x.
90. Mertins P, Yang F, Liu T, Mani DR, Petyuk VA, Gillette MA, et al. Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol Cell Proteomics. 2014;13(7):1690-704. doi: 10.1074/mcp.M113.036392.
91. Kelly RT, Page JS, Luo Q, Moore RJ, Orton DJ, Tang K, et al. Chemically etched open tubular and monolithic emitters for nanoelectrospray ionization mass spectrometry. Anal Chem. 2006;78(22):7796-801. doi: 10.1021/ac061133r.
92. Maiolica A, Borsotti D, Rappsilber J. Self-made frits for nanoscale columns in proteomics. Proteomics. 2005;5(15):3847-50. doi: 10.1002/pmic.200402010.
93. Petyuk VA, Mayampurath AM, Monroe ME, Polpitiya AD, Purvine SO, Anderson GA, et al. DtaRefinery, a software tool for elimination of systematic errors from parent ion mass measurements in tandem mass spectra data sets. Mol Cell Proteomics. 2010;9(3):486-96. doi: 10.1074/mcp.M900217-MCP200.
94. Kim S, Pevzner PA. MS-GF+ makes progress towards a universal database search tool for proteomics. Nat Commun. 2014;5:5277. doi: 10.1038/ncomms6277.
95. Monroe ME, Shaw JL, Daly DS, Adkins JN, Smith RD. MASIC: a software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC-MS(/MS) features. Comput Biol Chem. 2008;32(3):215-7. doi: 10.1016/j.compbiolchem.2008.02.006.
96. Elias JE, Gygi SP. Target-decoy search strategy for mass spectrometry-based proteomics. Methods Mol Biol. 2010;604:55-71. doi: 10.1007/978-1-60761-444-9_5.
97. Polpitiya AD, Qian WJ, Jaitly N, Petyuk VA, Adkins JN, Camp 2nd DG, et al. DAnTE: a statistical tool for quantitative analysis of -omics data. Bioinformatics. 2008;24(13):1556-8. doi: 10.1093/bioinformatics/btn217.
98. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674-6. doi: 10.1093/bioinformatics/bti610.
99. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, Chan ET, et al. Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 2012;40(Database issue):D700-5. doi: 10.1093/nar/gkr1029.
100. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42(Database issue):D199-205. doi: 10.1093/nar/gkt1076.
101. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25. doi: 10.1186/gb-2009-10-3-r25.
102. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078-9. doi: 10.1093/bioinformatics/btp352.
103. Bailey TL. DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics. 2011;27(12):1653-9. doi: 10.1093/bioinformatics/btr261.
104. Tanaka E, Bailey T, Grant CE, Noble WS, Keich U. Improved similarity scores for comparing motifs. Bioinformatics. 2011;27(12):1603-9. doi: 10.1093/bioinformatics/btr257.