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Originally published In Press as doi:10.1074/mcp.M200025-MCP200 on May 20, 2002.
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Molecular & Cellular Proteomics 1:376-386, 2002.
© 2002 by The American Society for Biochemistry and Molecular Biology, Inc.

Research

Stable Isotope Labeling by Amino Acids in Cell Culture, SILAC, as a Simple and Accurate Approach to Expression Proteomics*

Shao-En Ong{ddagger}, Blagoy Blagoev{ddagger}, Irina Kratchmarova{ddagger}, Dan Bach Kristensen§, Hanno Steen{ddagger},¶, Akhilesh Pandey{ddagger},|| and Matthias Mann{ddagger},**

{ddagger} Protein Interaction Laboratory, University of Southern Denmark
§ MDS-Proteomics A/S, Staermosegaardsvej 6, Odense M, DK-5230, Denmark

Quantitative proteomics has traditionally been performed by two-dimensional gel electrophoresis, but recently, mass spectrometric methods based on stable isotope quantitation have shown great promise for the simultaneous and automated identification and quantitation of complex protein mixtures. Here we describe a method, termed SILAC, for stable isotope labeling by amino acids in cell culture, for the in vivo incorporation of specific amino acids into all mammalian proteins. Mammalian cell lines are grown in media lacking a standard essential amino acid but supplemented with a non-radioactive, isotopically labeled form of that amino acid, in this case deuterated leucine (Leu-d3). We find that growth of cells maintained in these media is no different from growth in normal media as evidenced by cell morphology, doubling time, and ability to differentiate. Complete incorporation of Leu-d3 occurred after five doublings in the cell lines and proteins studied. Protein populations from experimental and control samples are mixed directly after harvesting, and mass spectrometric identification is straightforward as every leucine-containing peptide incorporates either all normal leucine or all Leu-d3. We have applied this technique to the relative quantitation of changes in protein expression during the process of muscle cell differentiation. Proteins that were found to be up-regulated during this process include glyceraldehyde-3-phosphate dehydrogenase, fibronectin, and pyruvate kinase M2. SILAC is a simple, inexpensive, and accurate procedure that can be used as a quantitative proteomic approach in any cell culture system.

** To whom correspondence may be addressed. Email: Mann{at}bmb.sdu.dk.


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A. Guo, J. Villen, J. Kornhauser, K. A. Lee, M. P. Stokes, K. Rikova, A. Possemato, J. Nardone, G. Innocenti, R. Wetzel, et al.
Signaling networks assembled by oncogenic EGFR and c-Met
PNAS, January 15, 2008; 105(2): 692 - 697.
[Abstract] [Full Text] [PDF]

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 Nucleic Acids ResHome page
F. Diella, C. M. Gould, C. Chica, A. Via, and T. J. Gibson
Phospho.ELM: a database of phosphorylation sites update 2008
Nucleic Acids Res., January 11, 2008; 36(suppl_1): D240 - D244.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
J. J. Pesavento, H. Yang, N. L. Kelleher, and C. A. Mizzen
Certain and Progressive Methylation of Histone H4 at Lysine 20 during the Cell Cycle
Mol. Cell. Biol., January 1, 2008; 28(1): 468 - 486.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
R. Hebeler, S. Oeljeklaus, K. A. Reidegeld, M. Eisenacher, C. Stephan, B. Sitek, K. Stuhler, H. E. Meyer, M. J. G. Sturre, P. P. Dijkwel, et al.
Study of Early Leaf Senescence in Arabidopsis thaliana by Quantitative Proteomics Using Reciprocal 14N/15N Labeling and Difference Gel Electrophoresis
Mol. Cell. Proteomics, January 1, 2008; 7(1): 108 - 120.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
M. L. Miller, S. Hanke, A. M. Hinsby, C. Friis, S. Brunak, M. Mann, and N. Blom
Motif Decomposition of the Phosphotyrosine Proteome Reveals a New N-terminal Binding Motif for SHIP2
Mol. Cell. Proteomics, January 1, 2008; 7(1): 181 - 192.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J.-W. Yang, H. Vacher, K.-S. Park, E. Clark, and J. S. Trimmer
Trafficking-dependent phosphorylation of Kv1.2 regulates voltage-gated potassium channel cell surface expression
PNAS, December 11, 2007; 104(50): 20055 - 20060.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. P. Stokes, J. Rush, J. MacNeill, J. M. Ren, K. Sprott, J. Nardone, V. Yang, S. A. Beausoleil, S. P. Gygi, M. Livingstone, et al.
Profiling of UV-induced ATM/ATR signaling pathways
PNAS, December 11, 2007; 104(50): 19855 - 19860.
[Abstract] [Full Text] [PDF]

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 PhysiologyHome page
T. Pisitkun, J. D. Hoffert, M.-J. Yu, and M. A. Knepper
Tandem Mass Spectrometry in Physiology
Physiology, December 1, 2007; 22(6): 390 - 400.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
H. Keshishian, T. Addona, M. Burgess, E. Kuhn, and S. A. Carr
Quantitative, Multiplexed Assays for Low Abundance Proteins in Plasma by Targeted Mass Spectrometry and Stable Isotope Dilution
Mol. Cell. Proteomics, December 1, 2007; 6(12): 2212 - 2229.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
D. Bonenfant, H. Towbin, M. Coulot, P. Schindler, D. R. Mueller, and J. van Oostrum
Analysis of Dynamic Changes in Post-translational Modifications of Human Histones during Cell Cycle by Mass Spectrometry
Mol. Cell. Proteomics, November 1, 2007; 6(11): 1917 - 1932.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
L.-Y. Tang, N. Deng, L.-S. Wang, J. Dai, Z.-L. Wang, X.-S. Jiang, S.-J. Li, L. Li, Q.-H. Sheng, D.-Q. Wu, et al.
Quantitative Phosphoproteome Profiling of Wnt3a-mediated Signaling Network: Indicating the Involvement of Ribonucleoside-diphosphate Reductase M2 Subunit Phosphorylation at Residue Serine 20 in Canonical Wnt Signal Transduction
Mol. Cell. Proteomics, November 1, 2007; 6(11): 1952 - 1967.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
P. A. Everley, C. A. Gartner, W. Haas, A. Saghatelian, J. E. Elias, B. F. Cravatt, B. R. Zetter, and S. P. Gygi
Assessing Enzyme Activities Using Stable Isotope Labeling and Mass Spectrometry
Mol. Cell. Proteomics, October 1, 2007; 6(10): 1771 - 1777.
[Abstract] [Full Text] [PDF]

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 Brief BioinformHome page
B.-J. M. Webb-Robertson and W. R. Cannon
Current trends in computational inference from mass spectrometry-based proteomics
Brief Bioinform, September 1, 2007; 8(5): 304 - 317.
[Abstract] [Full Text] [PDF]

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 Appl. Environ. Microbiol.Home page
Y. Coute, C. Hernandez, R. D. Appel, J.-C. Sanchez, and A. Margolles
Labeling of Bifidobacterium longum Cells with 13C-Substituted Leucine for Quantitative Proteomic Analyses
Appl. Envir. Microbiol., September 1, 2007; 73(17): 5653 - 5656.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
D. Bouyssie, A. G. de Peredo, E. Mouton, R. Albigot, L. Roussel, N. Ortega, C. Cayrol, O. Burlet-Schiltz, J.-P. Girard, and B. Monsarrat
Mascot File Parsing and Quantification (MFPaQ), a New Software to Parse, Validate, and Quantify Proteomics Data Generated by ICAT and SILAC Mass Spectrometric Analyses: Application To the Proteomics Study of Membrane Proteins from Primary Human Endothelial Cells
Mol. Cell. Proteomics, September 1, 2007; 6(9): 1621 - 1637.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
P. R. Cutillas and B. Vanhaesebroeck
Quantitative Profile of Five Murine Core Proteomes Using Label-free Functional Proteomics
Mol. Cell. Proteomics, September 1, 2007; 6(9): 1560 - 1573.
[Abstract] [Full Text] [PDF]

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 Genome ResHome page
D. B. McClatchy, L. Liao, S. K. Park, J. D. Venable, and J. R. Yates
Quantification of the synaptosomal proteome of the rat cerebellum during post-natal development
Genome Res., September 1, 2007; 17(9): 1378 - 1388.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. Rivers, D. M. Simpson, D. H. L. Robertson, S. J. Gaskell, and R. J. Beynon
Absolute Multiplexed Quantitative Analysis of Protein Expression during Muscle Development Using QconCAT
Mol. Cell. Proteomics, August 1, 2007; 6(8): 1416 - 1427.
[Abstract] [Full Text] [PDF]

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 BioinformaticsHome page
S. McIlwain, D. Page, E. L. Huttlin, and M. R. Sussman
Using dynamic programming to create isotopic distribution maps from mass spectra
Bioinformatics, July 1, 2007; 23(13): i328 - i336.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. J. Benschop, S. Mohammed, M. O'Flaherty, A. J. R. Heck, M. Slijper, and F. L. H. Menke
Quantitative Phosphoproteomics of Early Elicitor Signaling in Arabidopsis
Mol. Cell. Proteomics, July 1, 2007; 6(7): 1198 - 1214.
[Abstract] [Full Text] [PDF]

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 Microbiol. Mol. Biol. Rev.Home page
K. L. Maxwell and L. Frappier
Viral Proteomics
Microbiol. Mol. Biol. Rev., June 1, 2007; 71(2): 398 - 411.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
C. S. Lane, Y. Wang, R. Betts, W. J. Griffiths, and L. H. Patterson
Comparative Cytochrome P450 Proteomics in the Livers of Immunodeficient Mice Using 18O Stable Isotope Labeling
Mol. Cell. Proteomics, June 1, 2007; 6(6): 953 - 962.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. Jin, G. J. Li, J. Davis, D. Zhu, Y. Wang, C. Pan, and J. Zhang
Identification of Novel Proteins Associated with Both {alpha}-Synuclein and DJ-1
Mol. Cell. Proteomics, May 1, 2007; 6(5): 845 - 859.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. P. C. Vissers, J. I. Langridge, and J. M. F. G. Aerts
Analysis and Quantification of Diagnostic Serum Markers and Protein Signatures for Gaucher Disease
Mol. Cell. Proteomics, May 1, 2007; 6(5): 755 - 766.
[Abstract] [Full Text] [PDF]


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