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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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Temporal Perturbation of Tyrosine Phosphoproteome Dynamics Reveals the System-wide Regulatory Networks
Mol. Cell. Proteomics, February 1, 2009; 8(2): 226 - 231.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
P. Van Damme, S. Maurer-Stroh, K. Plasman, J. Van Durme, N. Colaert, E. Timmerman, P.-J. De Bock, M. Goethals, F. Rousseau, J. Schymkowitz, et al.
Analysis of Protein Processing by N-terminal Proteomics Reveals Novel Species-specific Substrate Determinants of Granzyme B Orthologs
Mol. Cell. Proteomics, February 1, 2009; 8(2): 258 - 272.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
H. Roelofsen, M. Dijkstra, D. Weening, M. P. de Vries, A. Hoek, and R. J. Vonk
Comparison of Isotope-labeled Amino Acid Incorporation Rates (CILAIR) Provides a Quantitative Method to Study Tissue Secretomes
Mol. Cell. Proteomics, February 1, 2009; 8(2): 316 - 324.
[Abstract] [Full Text] [PDF]

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 Genome ResHome page
G. Mittler, F. Butter, and M. Mann
A SILAC-based DNA protein interaction screen that identifies candidate binding proteins to functional DNA elements
Genome Res., February 1, 2009; 19(2): 284 - 293.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
S. Dhungana, B. A. Merrick, K. B. Tomer, and M. B. Fessler
Quantitative Proteomics Analysis of Macrophage Rafts Reveals Compartmentalized Activation of the Proteasome and of Proteasome-mediated ERK Activation in Response to Lipopolysaccharide
Mol. Cell. Proteomics, January 1, 2009; 8(1): 201 - 213.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
H. Choi, D. Fermin, and A. I. Nesvizhskii
Significance Analysis of Spectral Count Data in Label-free Shotgun Proteomics
Mol. Cell. Proteomics, December 1, 2008; 7(12): 2373 - 2385.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
E. Szajli, T. Feher, and K. F. Medzihradszky
Investigating the Quantitative Nature of MALDI-TOF MS
Mol. Cell. Proteomics, December 1, 2008; 7(12): 2410 - 2418.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
M. Lamkanfi, T.-D. Kanneganti, P. Van Damme, T. Vanden Berghe, I. Vanoverberghe, J. Vandekerckhove, P. Vandenabeele, K. Gevaert, and G. Nunez
Targeted Peptidecentric Proteomics Reveals Caspase-7 as a Substrate of the Caspase-1 Inflammasomes
Mol. Cell. Proteomics, December 1, 2008; 7(12): 2350 - 2363.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
A. R. Kristensen, S. Schandorff, M. Hoyer-Hansen, M. O. Nielsen, M. Jaattela, J. Dengjel, and J. S. Andersen
Ordered Organelle Degradation during Starvation-induced Autophagy
Mol. Cell. Proteomics, December 1, 2008; 7(12): 2419 - 2428.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. Mann and N. L. Kelleher
Mass Spectrometry Special Feature: Precision proteomics: The case for high resolution and high mass accuracy
PNAS, November 25, 2008; 105(47): 18132 - 18138.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
D. B. Martin, T. Holzman, D. May, A. Peterson, A. Eastham, J. Eng, and M. McIntosh
MRMer, an Interactive Open Source and Cross-platform System for Data Extraction and Visualization of Multiple Reaction Monitoring Experiments
Mol. Cell. Proteomics, November 1, 2008; 7(11): 2270 - 2278.
[Abstract] [Full Text] [PDF]

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 JCBHome page
L. Trinkle-Mulcahy, S. Boulon, Y. W. Lam, R. Urcia, F.-M. Boisvert, F. Vandermoere, N. A. Morrice, S. Swift, U. Rothbauer, H. Leonhardt, et al.
Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes
J. Cell Biol., October 20, 2008; 183(2): 223 - 239.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Song, W. Kong, N. Weatherspoon, G. Qin, W. Tyler, J. Turk, R. Curtiss III, and Y. Shi
Modulation of the Regulatory Activity of Bacterial Two-component Systems by SlyA
J. Biol. Chem., October 17, 2008; 283(42): 28158 - 28168.
[Abstract] [Full Text] [PDF]

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 Physiol. GenomicsHome page
S. P. Mirza and M. Olivier
Methods and approaches for the comprehensive characterization and quantification of cellular proteomes using mass spectrometry
Physiol Genomics, October 8, 2008; 33(1): 3 - 11.
[Abstract] [Full Text] [PDF]

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 Physiol. GenomicsHome page
E. W. Deutsch, H. Lam, and R. Aebersold
Data analysis and bioinformatics tools for tandem mass spectrometry in proteomics
Physiol Genomics, October 8, 2008; 33(1): 18 - 25.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
L. Liao, S. K. Park, T. Xu, P. Vanderklish, and J. R. Yates III
Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice
PNAS, October 7, 2008; 105(40): 15281 - 15286.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
M. Skiba, T. C. Mettenleiter, and A. Karger
Quantitative Whole-Cell Proteome Analysis of Pseudorabies Virus-Infected Cells
J. Virol., October 1, 2008; 82(19): 9689 - 9699.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
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
Briefings in Functional Genomics, 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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