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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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V. Zabrouskov, Y. Ge, J. Schwartz, and J. W. Walker
Unraveling Molecular Complexity of Phosphorylated Human Cardiac Troponin I by Top Down Electron Capture Dissociation/Electron Transfer Dissociation Mass Spectrometry
Mol. Cell. Proteomics, October 1, 2008; 7(10): 1838 - 1849.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
C.-L. Han, C.-W. Chien, W.-C. Chen, Y.-R. Chen, C.-P. Wu, H. Li, and Y.-J. Chen
A Multiplexed Quantitative Strategy for Membrane Proteomics: Opportunities for Mining Therapeutic Targets for Autosomal Dominant Polycystic Kidney Disease
Mol. Cell. Proteomics, October 1, 2008; 7(10): 1983 - 1997.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
A. Doucet, G. S. Butler, D. Rodriguez, A. Prudova, and C. M. Overall
Metadegradomics: Toward in Vivo Quantitative Degradomics of Proteolytic Post-translational Modifications of the Cancer Proteome
Mol. Cell. Proteomics, October 1, 2008; 7(10): 1925 - 1951.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
U. Kruse, M. Bantscheff, G. Drewes, and C. Hopf
Chemical and Pathway Proteomics: Powerful Tools for Oncology Drug Discovery and Personalized Health Care
Mol. Cell. Proteomics, October 1, 2008; 7(10): 1887 - 1901.
[Abstract] [Full Text] [PDF]

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 GENES CELLSHome page
K. Ota, K. Kito, S. Okada, and T. Ito
A proteomic screen reveals the mitochondrial outer membrane protein Mdm34p as an essential target of the F-box protein Mdm30p
Genes Cells, October 1, 2008; 13(10): 1075 - 1085.
[Abstract] [Full Text] [PDF]

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 Brief Funct Genomic ProteomicHome page
G. W. Becker
Stable isotopic labeling of proteins for quantitative proteomic applications
Brief Funct Genomic Proteomic, September 1, 2008; 7(5): 371 - 382.
[Abstract] [Full Text] [PDF]

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 Nucleic Acids ResHome page
A. Lebreton, J.-C. Rousselle, P. Lenormand, A. Namane, A. Jacquier, M. Fromont-Racine, and C. Saveanu
60S ribosomal subunit assembly dynamics defined by semi-quantitative mass spectrometry of purified complexes
Nucleic Acids Res., September 1, 2008; 36(15): 4988 - 4999.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
S. C. Bendall, C. Hughes, M. H. Stewart, B. Doble, M. Bhatia, and G. A. Lajoie
Prevention of Amino Acid Conversion in SILAC Experiments with Embryonic Stem Cells
Mol. Cell. Proteomics, September 1, 2008; 7(9): 1587 - 1597.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
M. Bantscheff, M. Boesche, D. Eberhard, T. Matthieson, G. Sweetman, and B. Kuster
Robust and Sensitive iTRAQ Quantification on an LTQ Orbitrap Mass Spectrometer
Mol. Cell. Proteomics, September 1, 2008; 7(9): 1702 - 1713.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
P. Mertins, H. C. Eberl, J. Renkawitz, J. V. Olsen, M. L. Tremblay, M. Mann, A. Ullrich, and H. Daub
Investigation of Protein-tyrosine Phosphatase 1B Function by Quantitative Proteomics
Mol. Cell. Proteomics, September 1, 2008; 7(9): 1763 - 1777.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
R. Raijmakers, C. R. Berkers, A. de Jong, H. Ovaa, A. J. R. Heck, and S. Mohammed
Automated Online Sequential Isotope Labeling for Protein Quantitation Applied to Proteasome Tissue-specific Diversity
Mol. Cell. Proteomics, September 1, 2008; 7(9): 1755 - 1762.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Luo, Y. Li, J.-J. Mu, J. Zhang, T. Tonaka, Y. Hamamori, S. Y. Jung, Y. Wang, and J. Qin
Regulation of Intra-S Phase Checkpoint by Ionizing Radiation (IR)-dependent and IR-independent Phosphorylation of SMC3
J. Biol. Chem., July 11, 2008; 283(28): 19176 - 19183.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
C. P. Albuquerque, M. B. Smolka, S. H. Payne, V. Bafna, J. Eng, and H. Zhou
A Multidimensional Chromatography Technology for In-depth Phosphoproteome Analysis
Mol. Cell. Proteomics, July 1, 2008; 7(7): 1389 - 1396.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
D. S. Spellman, K. Deinhardt, C. C. Darie, M. V. Chao, and T. A. Neubert
Stable Isotopic Labeling by Amino Acids in Cultured Primary Neurons: Application to Brain-derived Neurotrophic Factor-dependent Phosphotyrosine-associated Signaling
Mol. Cell. Proteomics, June 1, 2008; 7(6): 1067 - 1076.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
F. Mousson, A. Kolkman, W. W. M. P. Pijnappel, H. Th. M. Timmers, and A. J. R. Heck
Quantitative Proteomics Reveals Regulation of Dynamic Components within TATA-binding Protein (TBP) Transcription Complexes
Mol. Cell. Proteomics, May 1, 2008; 7(5): 845 - 852.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
M. Colzani, F. Schutz, A. Potts, P. Waridel, and M. Quadroni
Relative Protein Quantification by Isobaric SILAC with Immonium Ion Splitting (ISIS)
Mol. Cell. Proteomics, May 1, 2008; 7(5): 927 - 937.
[Abstract] [Full Text] [PDF]

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 Brief Funct Genomic ProteomicHome page
C. M.R. Lacerda, L. Xin, I. Rogers, and K. F. Reardon
Analysis of iTRAQ data using Mascot and Peaks quantification algorithms
Brief Funct Genomic Proteomic, April 4, 2008; (2008) eln017v1.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. Graumann, N. C. Hubner, J. B. Kim, K. Ko, M. Moser, C. Kumar, J. Cox, H. Scholer, and M. Mann
Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) and Proteome Quantitation of Mouse Embryonic Stem Cells to a Depth of 5,111 Proteins
Mol. Cell. Proteomics, April 1, 2008; 7(4): 672 - 683.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
A. Panchaud, J. Hansson, M. Affolter, R. Bel Rhlid, S. Piu, P. Moreillon, and M. Kussmann
ANIBAL, Stable Isotope-based Quantitative Proteomics by Aniline and Benzoic Acid Labeling of Amino and Carboxylic Groups
Mol. Cell. Proteomics, April 1, 2008; 7(4): 800 - 812.
[Abstract] [Full Text] [PDF]

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 Brief BioinformHome page
J. W. H. Wong, M. J. Sullivan, and G. Cagney
Computational methods for the comparative quantification of proteins in label-free LCn-MS experiments
Brief Bioinform, March 1, 2008; 9(2): 156 - 165.
[Abstract] [Full Text] [PDF]

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 Brief BioinformHome page
D. A. Stead, N. W. Paton, P. Missier, S. M. Embury, C. Hedeler, B. Jin, A. J. P. Brown, and A. Preece
Information quality in proteomics
Brief Bioinform, March 1, 2008; 9(2): 174 - 188.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
G. G. Xiao, M. Garg, S. Lim, D. Wong, V. L. Go, and W.-N. P. Lee
Determination of protein synthesis in vivo using labeling from deuterated water and analysis of MALDI-TOF spectrum
J Appl Physiol, March 1, 2008; 104(3): 828 - 836.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. Villanueva, A. Nazarian, K. Lawlor, S. S. Yi, R. J. Robbins, and P. Tempst
A Sequence-specific Exopeptidase Activity Test (SSEAT) for "Functional" Biomarker Discovery
Mol. Cell. Proteomics, March 1, 2008; 7(3): 509 - 518.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. Kruger, I. Kratchmarova, B. Blagoev, Y.-H. Tseng, C. R. Kahn, and M. Mann
Dissection of the insulin signaling pathway via quantitative phosphoproteomics
PNAS, February 19, 2008; 105(7): 2451 - 2456.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
D. Nanavati, M. Gucek, J. L. S. Milne, S. Subramaniam, and S. P. Markey
Stoichiometry and Absolute Quantification of Proteins with Mass Spectrometry Using Fluorescent and Isotope-labeled Concatenated Peptide Standards
Mol. Cell. Proteomics, February 1, 2008; 7(2): 442 - 447.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
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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