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GENE EXPRESSION

Correlation between Protein and mRNA Abundance in Yeast

Steven P. Gygi, Yvan Rochon, B. Robert Franza, Ruedi Aebersold
Steven P. Gygi
Department of Molecular Biotechnology, University of Washington, Seattle, Washington 98195-7730
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Yvan Rochon
Department of Molecular Biotechnology, University of Washington, Seattle, Washington 98195-7730
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B. Robert Franza
Department of Molecular Biotechnology, University of Washington, Seattle, Washington 98195-7730
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Ruedi Aebersold
Department of Molecular Biotechnology, University of Washington, Seattle, Washington 98195-7730
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DOI: 10.1128/MCB.19.3.1720
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  • Fig. 1.
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    Fig. 1.

    Schematic illustration of proteome analysis by 2DE and mass spectrometry. In part I, proteins are separated by 2DE, stained spots are excised and subjected to in-gel digestion with trypsin, and the resulting peptides are separated by on-line capillary high-performance liquid chromatography. In part II, a peptide is shown eluting from the column in part I. The peptide is ionized by electrospray ionization and enters the mass spectrometer. The mass of the ionized peptide is detected, and the first quadrupole mass filter allows only the specific mass-to-charge ratio of the selected peptide ion to pass into the collision cell. In the collision cell, the energized, ionized peptides collide with neutral argon gas molecules. Fragmentation of the peptide is essentially random but occurs mainly at the peptide bonds, resulting in smaller peptides of differing lengths (masses). These peptide fragments are detected as a tandem mass (MS/MS) spectrum in the third quadrupole mass filter where two ion series are recorded simultaneously, one each from sequencing inward from the N and C termini of the peptide, respectively. In part III, the MS/MS spectrum from the selected, ionized peptide is compared to predicted tandem mass spectra computer generated from a sequence database. Provided that the peptide sequence exists in the database, the peptide and, by association, the protein from which the peptide was derived can be identified. Unambiguous protein identification is attained in a single analysis because multiple peptides are identified as being derived from the same protein.

  • Fig. 2.
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    Fig. 2.

    2D silver-stained gel of the proteins in yeast total cell lysate. Proteins were separated in the first dimension (horizontal) by isoelectric focusing and then in the second dimension (vertical) by molecular weight sieving. Protein spots (156) were chosen to include the entire range of molecular weights, isoelectric focusing points, and staining intensities. Spots were excised, and the corresponding protein was identified by mass spectrometry and database searching. The spots are labeled on the gel and correspond to the data presented in Table 1. Molecular weights are given in thousands.

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    Fig. 3.

    Tandem mass (MS/MS) spectra resulting from analysis of a single spot on a 2D gel. The first quadrupole selected a single mass-to-charge ratio (m/z) of 687.2 (A) or 592.6 (B), while the collision cell was filled with argon gas, and a voltage which caused the peptide to undergo fragmentation by CID was applied. The third quadrupole scanned the mass range from 50 to 1,400 m/z. The computer program Sequest (8) was utilized to match MS/MS spectra to amino acid sequence by database searching. Both spectra matched peptides from the same protein, S57593 (yeast hypothetical protein YMR226C). Five other peptides from the same analysis were matched to the same protein.

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    Fig. 4.

    Current proteome analysis technology utilizing 2DE without preenrichment samples mainly highly expressed and long-lived proteins. Genes encoding highly expressed proteins generally have large codon bias values. (A) Distribution of the yeast genome (more than 6,000 genes) based on codon bias. The interval with the largest frequency of genes is 0.0 to 0.1, with more than 2,500 genes. (B) Distribution of the genes from identified proteins in this study based on codon bias. No genes with codon bias values less than 0.1 were detected in this study. (C) Distribution of identified proteins in this study based on predicted half-life (estimated by N-end rule).

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    Fig. 5.

    Correlation between protein and mRNA levels for 106 genes in yeast growing at log phase with glucose as a carbon source. mRNA and protein levels were calculated as described in Materials and Methods. The data represent a population of genes with protein expression levels visible by silver staining on a 2D gel chosen to include the entire range of molecular weights, isoelectric focusing points, and staining intensities. The inset shows the low-end portion of the main figure. It contains 69% of the original data set. The Pearson product moment correlation for the entire data set was 0.935. The correlation for the inset containing 73 proteins (69%) was only 0.356.

  • Fig. 6.
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    Fig. 6.

    Effect of highly abundant proteins on Pearson product moment correlation coefficient for mRNA and protein abundance in yeast. The set of 106 genes was ranked according to protein abundance, and the correlation value was calculated by including the 40 lowest-abundance genes and then progressively including the remaining 66 genes in order of abundance. The correlation value climbs as the final 11 highly abundant proteins are included.

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    Fig. 7.

    Relationship between codon bias and protein and mRNA levels in this study. Yeast mRNA and protein expression levels were calculated as described in Materials and Methods. The data represent the same 106 genes as in Fig. 5.

Tables

  • Figures
  • Table 1.

    Expressed genes identified from 2D gel in Fig. 2

    Mol wtpISpot no.YPD gene nameaProtein abundance (103copies/cell)mRNA abundance (copies/cell)Codon bias
    17,2596.75133CPR115.261.70.769
    18,7024.8083EGD220.15.20.724
    18,7264.44147YKL056C61.288.40.831
    18,9785.95135YER067W3.76.70.118
    19,1085.04130YLR109W94.49.70.680
    19,6819.08136ATP711.0NAb,c 0.246
    20,5056.07111GUK116.53.70.422
    21,4445.25148SAR15.410.40.455
    21,5834.9895TSA1110.640.10.845
    22,6024.3080EFB166.123.80.875
    23,0796.29112SOD212.62.20.351
    23,7435.44137HSP26NAd 0.70.434
    24,0335.9796ADK117.416.40.656
    24,0584.43143YKL117W29.210.40.339
    24,3536.30140TFS18.10.70.146
    24,6625.8599URA525.46.00.359
    24,8086.3397GSP126.35.20.735
    24,9088.73122RPS518.6NAc 0.899
    25,0814.6581MRP89.3NAc 0.241
    25,9606.06116RPE15.80.70.372
    26,3789.55127RPS396.8NAc 0.863
    26,4675.18100VMA410.53.70.427
    26,6615.8498TPI1NAd NAc 0.900
    27,1565.5693PRE86.90.70.129
    27,3346.13115YHR049W18.42.20.520
    27,4725.3392YNL010W31.63.70.421
    27,4808.95123GPM110.0169.40.902
    27,4808.95124GPM1231.4169.40.902
    27,4808.95125GPM17.5169.40.902
    27,8095.97139HOR25.70.70.381
    27,8744.4678YST113.652.80.805
    28,5954.5141PUP24.40.70.147
    29,1566.59114YMR226C14.52.20.283
    29,2448.40120DPM15.011.20.362
    29,4435.9148PRE43.43.70.162
    30,0126.39138PRB121.21.50.449
    30,0734.6377BMH114.728.20.454
    30,2967.94121OMP267.441.60.499
    30,4356.3489GPP170.211.20.703
    31,3325.5788ILV613.93.00.402
    32,1595.46113IPP163.13.70.752
    32,2636.00149HIS122.44.50.232
    33,3115.3584SPE315.16.70.468
    34,4655.60129ADE18.75.20.305
    34,7625.3285SEC1410.96.00.373
    34,7975.8542URA149.58.90.237
    34,7996.0490BEL1103.281.00.875
    35,5565.9743YDL124W6.44.50.206
    35,6198.4159TDH169.832.7c 0.940
    35,6505.4968CAR15.23.00.339
    35,7126.72117TDH249.6473.0c 0.982
    35,7126.72154TDH2863.5473.0c 0.982
    35,7126.72155TDH279.4473.0c 0.982
    36,2724.85128APA18.70.70.425
    36,3585.0575YJR105W17.617.10.522
    36,3585.0576YJR105W27.517.10.522
    36,5966.3779ADH258.9260.0c 0.711
    36,7146.30102ADH1746.1260.00.913
    36,7146.30103ADH117.6260.00.913
    36,7146.30104ADH161.4260.00.913
    36,7146.30105ADH152.7260.00.913
    37,0336.2344TAL144.83.70.701
    37,7967.3657IDH229.46.70.330
    37,8866.49106ILV576.04.50.892
    38,7007.8355BAT130.911.20.469
    38,7026.2446QCR2NAd 2.20.326
    39,4775.5886FBA117.8183.60.935
    39,4775.5887FBA1427.2183.60.935
    39,5406.50150HOM260.34.50.592
    39,5616.12156PSA196.427.50.718
    41,1586.0149YNL134C14.91.50.316
    41,6237.1858BAT219.08.90.250
    41,7287.29110ERG1024.14.50.543
    41,9005.4274TOM4022.32.20.375
    42,4026.2945CYS36.78.90.621
    42,8835.6367DYS115.85.20.526
    43,4096.31107SER110.51.50.292
    43,4215.5991ERG62.214.10.408
    44,1747.3256YBR025C13.16.00.684
    44,6824.9972TIF12.939.40.834
    44,7077.77108PGK123.7165.70.897
    44,7077.77109PGK1315.2165.70.897
    46,0806.7230CAR215.4NAc 0.495
    46,3838.5253IDP17.70.70.436
    46,5535.9847IDP232.4NAc 0.197
    46,6796.3950ENO135.40.70.930
    46,6796.3951ENO16.60.70.930
    46,6796.3952ENO12.20.70.930
    46,7735.8263ENO215.5289.10.960
    46,7735.8264ENO2635.5289.10.960
    46,7735.8265ENO293.0289.10.960
    46,7735.8266ENO231.0289.10.960
    47,4026.09126COR12.50.70.422
    47,6668.9854AAT211.76.00.338
    48,3645.2573WTM174.513.40.365
    48,5306.2061MET1738.129.00.576
    48,9045.1869LYS916.23.70.463
    48,9874.90153SUP4529.611.90.377
    49,7275.4770PRO213.65.20.297
    49,9129.2762TEF2558.5282.00.932
    50,4445.6735YDR190C4.82.20.228
    50,8376.1132YEL047C3.81.50.387
    50,8914.59151TUB211.27.40.404
    51,5476.8027LPD118.92.20.351
    52,2167.2529SHM219.77.40.722
    52,8595.5437YFR044C30.26.70.442
    53,7985.1971HXK226.57.40.756
    53,8036.05145GYP64.40.70.147
    54,4035.2939ALD637.72.20.664
    54,4035.2940ALD66.62.20.664
    54,5026.2031ADE136.31.50.417
    54,5437.7525PYK1225.3101.80.965
    54,5437.7526PYK139.8101.80.965
    55,2216.66146YEL071W16.33.00.244
    55,2954.35134PDI166.214.10.589
    55,3645.9824GLK122.66.00.237
    55,4817.97118ATP121.62.20.637
    55,8866.4728CYS422.2NAc 0.444
    56,1675.8333ARO814.33.00.324
    56,1675.8334ARO89.13.00.324
    56,5846.3620CYB218.9NAc 0.259
    57,3665.5360FRS22.30.70.451
    57,3835.98144ZWF15.60.70.215
    57,4645.4936THR421.43.70.508
    57,5125.507SRV26.5NAc 0.260
    57,7274.92152VMA233.78.90.546
    58,5736.4717ACH14.41.50.327
    58,5736.4718ACH15.41.50.327
    61,3535.8721PDC16.5200.70.962
    61,3535.8722PDC1303.2200.70.962
    61,3535.8723PDC116.3200.70.962
    61,6495.5438CCT82.21.50.271
    61,9026.21101PDC54.3NAc 0.828
    62,2666.1916ICL120.1NAc 0.327
    62,8628.0219ILV35.34.50.548
    63,0826.40119PGM22.23.00.402
    64,3355.775PAB130.41.50.616
    66,1205.428STI16.70.70.313
    66,1205.429STI16.40.70.313
    66,4505.29141SSB27.0NAc 0.880
    66,4505.29142SSB22.3NAc 0.880
    66,4565.2310SSB164.579.50.907
    66,4565.2311SSB159.079.50.907
    66,4565.2312SSB113.779.50.907
    68,3975.8282LEU43.13.00.407
    69,3134.9013SSA224.318.60.892
    69,3134.9014SSA277.118.60.892
    74,3788.4615YKL029C2.83.70.353
    75,3965.826GRS15.57.40.500
    85,7206.251MET62.0NAc 0.772
    85,7206.252MET610.9NAc 0.772
    85,7206.253MET61.4NAc 0.772
    93,2766.11131EFT117.941.60.890
    93,2766.11132EFT15.741.60.890
    102,064e 6.61e 94ADE34.85.20.423
    107,482e 5.33e 4MCM32.7NAc 0.240
    • ↵a YPD gene names are available from the YPD website (39).

    • ↵b NA, calculation could not be performed or was not available.

    • ↵c mRNA data inconclusive or NA.

    • ↵d No methionines in predicted ORF; therefore, protein concentration was not determined.

    • ↵e Measured molecular weight or pI did not match theoretical molecular weight or pI.

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Correlation between Protein and mRNA Abundance in Yeast
Steven P. Gygi, Yvan Rochon, B. Robert Franza, Ruedi Aebersold
Molecular and Cellular Biology Mar 1999, 19 (3) 1720-1730; DOI: 10.1128/MCB.19.3.1720

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Correlation between Protein and mRNA Abundance in Yeast
Steven P. Gygi, Yvan Rochon, B. Robert Franza, Ruedi Aebersold
Molecular and Cellular Biology Mar 1999, 19 (3) 1720-1730; DOI: 10.1128/MCB.19.3.1720
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