A genetic engineering solution to the "arginine conversion problem" in stable isotope labeling by amino acids in cell culture (SILAC)

Molecular and Cellular Proteomics

Volumn 9, Issue 7, 2010, Pages 1567-1577

  Bicho, Claudia C ^a   Alves, Flavia De Lima ^a   Chen, Zhuo A ^a   Rappsilber, Juri ^a   Sawin, Kenneth E ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGINASE; ARGININE; GLUTAMIC ACID; GLUTAMINE; ORNITHINE OXOACID AMINOTRANSFERASE; PROLINE; STABLE ISOTOPE; FUNGAL PROTEIN; HYBRID PROTEIN;

ARTICLE; CATABOLISM; CELL DIVISION; CELL LABELING; CULTURE MEDIUM; DOWN REGULATION; GENE DELETION; GENETIC ENGINEERING; GENETIC MANIPULATION; ISOTOPE LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; SCHIZOSACCHAROMYCES POMBE; STABLE ISOTOPE LABELING BY AMINO ACIDS IN CELL CULTURE; UPREGULATION; AMINO ACID SEQUENCE; CELL CULTURE; CHEMISTRY; CULTURE TECHNIQUE; DEVICES; GENETICS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; PROCEDURES; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

AMINO ACID SEQUENCE; AMINO ACIDS; ARGININE; CELL CULTURE TECHNIQUES; CELLS, CULTURED; FUNGAL PROTEINS; GENETIC ENGINEERING; ISOTOPE LABELING; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PROTEOMICS; RECOMBINANT FUSION PROTEINS; SCHIZOSACCHAROMYCES;

EID: 77954695928     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.000208     Document Type: Article

References (61)

1. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
2. Ong, S. E., and Mann, M. (2005) Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262
3. de Godoy, L. M., Olsen, J. V., Cox, J., Nielsen, M. L., Hubner, N. C., Fröhlich, F., Walther, T. C., and Mann, M. (2008) Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455, 1251-1254
4. Krüger, M., Moser, M., Ussar, S., Thievessen, I., Luber, C. A., Forner, F., Schmidt, S., Zanivan, S., Fässler, R., and Mann, M. (2008) SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell 134, 353-364 (Pubitemid 352010327)
5. Ong, S. E., Kratchmarova, I., and Mann, M. (2003) Properties of 13C-substituted arginine in stable isotope labeling by amino acids in cell culture (SILAC). J. Proteome Res. 2, 173-181 (Pubitemid 37099053)
6. Blagoev, B., and Mann, M. (2006) Quantitative proteomics to study mitogen-activated protein kinases. Methods 40, 243-250 (Pubitemid 44635297)
7. Van Hoof, D., Pinkse, M. W., Oostwaard, D. W., Mummery, C. L., Heck, A. J., and Krijgsveld, J. (2007) An experimental correction for arginine-to-proline conversion artifacts in SILAC-based quantitative proteomics. Nat. Methods 4, 677-678 (Pubitemid 47338150)
8. Schmidt, F., Strozynski, M., Salus, S. S., Nilsen, H., and Thiede, B. (2007) Rapid determination of amino acid incorporation by stable isotope labeling with amino acids in cell culture (SILAC). Rapid Commun. Mass Spectrom. 21, 3919-3926 (Pubitemid 350220701)
9. Bendall, S. C., Hughes, C., Stewart, M. H., Doble, B., Bhatia, M., and Lajoie, G. A. (2008) Prevention of amino acid conversion in SILAC experiments with embryonic stem cells. Mol. Cell. Proteomics 7, 1587-1597
10. Liao, L., Park, S. K., Xu, T., Vanderklish, P., and Yates, J. R., 3rd (2008) Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice. Proc. Natl. Acad. Sci. U.S.A. 105, 15281-15286
11. Park, S. K., Liao, L., Kim, J. Y., and Yates, J. R., 3rd (2009) A computational approach to correct arginine-to-proline conversion in quantitative proteomics. Nat. Methods 6, 184-185
12. Gruhler, A., Olsen, J. V., Mohammed, S., Mortensen, P., Faergeman, N. J., Mann, M., and Jensen, O. N. (2005) Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell. Proteomics 4, 310-327
13. Soufi, B., Kelstrup, C. D., Stoehr, G., Fröhlich, F., Walther, T. C., and Olsen, J. V. (2009) Global analysis of the yeast osmotic stress response by quantitative proteomics. Mol. Biosyst. 5, 1337-1346
14. Ong, S. E., and Mann, M. (2006) A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1, 2650-2660
15. Graumann, J., Hubner, N. C., Kim, J. B., Ko, K., Moser, M., Kumar, C., Cox, J., Schöler, H., and Mann, M. (2008) 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 7, 672-683
16. Prokhorova, T. A., Rigbolt, K. T., Johansen, P. T., Henningsen, J., Kratchmarova, I., Kassem, M., and Blagoev, B. (2009) Stable isotope labeling by amino acids in cell culture (SILAC) and quantitative comparison of the membrane proteomes of self-renewing and differentiating human embryonic stem cells. Mol. Cell. Proteomics 8, 959-970
17. Hwang, S. I., Lundgren, D. H., Mayya, V., Rezaul, K., Cowan, A. E., Eng, J. K., and Han, D. K. (2006) Systematic characterization of nuclear proteome during apoptosis: a quantitative proteomic study by differential extraction and stable isotope labeling. Mol. Cell. Proteomics 5, 1131-1145
18. Mousson, F., Kolkman, A., Pijnappel, W. W., Timmers, H. T., and Heck, A. J. (2008) Quantitative proteomics reveals regulation of dynamic components within TATA-binding protein (TBP) transcription complexes. Mol. Cell. Proteomics 7, 845-852
19. Moreno, S., Klar, A., and Nurse, P. (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823
20. Bähler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., 3rd, Steever, A. B., Wach, A., Philippsen, P., and Pringle, J. R. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951 (Pubitemid 28328000)
21. Sawin, K. E., Lourenco, P. C., and Snaith, H. A. (2004) Microtubule nucleation at non-spindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr. Biol. 14, 763-775
22. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
23. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670
24. Rappsilber, J., Mann, M., and Ishihama, Y. (2007) Protocol for micropurification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906
25. Ishihama, Y., Rappsilber, J., Andersen, J. S., and Mann, M. (2002) Microcolumns with self-assembled particle frits for proteomics. J. Chromatogr. A 979, 233-239 (Pubitemid 35341547)
26. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
27. Jones, E. W., and Fink, G. R. (1982) The regulation of amino acid and nucleotide biosynthesis in yeast, in The Molecular Biology of the Yeast Saccharomyces: Vol. II. Metabolism and Gene Expression (Strathern, J. N., Jones, E. W., and Broach, J. R., eds) pp. 181-299, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
28. Davis, R. H. (1986) Compartmental and regulatory mechanisms in the arginine pathways of Neurospora crassa and Saccharomyces cerevisiae. Microbiol. Rev. 50, 280-313
29. Xu, H., Andi, B., Qian, J., West, A. H., and Cook, P. F. (2006) The alpha-aminoadipate pathway for lysine biosynthesis in fungi. Cell Biochem. Biophys. 46, 43-64
30. Van Huffel, C., Dubois, E., and Messenguy, F. (1994) Cloning and sequencing of Schizosaccharomyces pombe car1 gene encoding arginase. Expression of the arginine anabolic and catabolic genes in response to arginine and related metabolites. Yeast 10, 923-933
31. Fantes, P. A., and Creanor, J. (1984) Canavanine resistance and the mechanism of arginine uptake in the fission yeast Schizosaccharomyces pombe. J. Gen. Microbiol. 130, 3265-3273
32. Moreno, S., Hayles, J., and Nurse, P. (1989) Regulation of p34cdc2 protein kinase during mitosis. Cell 58, 361-372 (Pubitemid 19191417)
33. Lyne, R., Burns, G., Mata, J., Penkett, C. J., Rustici, G., Chen, D., Langford, C., Vetrie, D., and Bähler, J. (2003) Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4, 27
34. Wilhelm, B. T., Marguerat, S., Watt, S., Schubert, F., Wood, V., Goodhead, I., Penkett, C. J., Rogers, J., and Bähler, J. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453, 1239-1243
35. Schmidt, M. W., Houseman, A., Ivanov, A. R., and Wolf, D. A. (2007) Comparative proteomic and transcriptomic profiling of the fission yeast Schizosaccharomyces pombe. Mol. Syst. Biol. 3, 79
36. Booher, R. N., Alfa, C. E., Hyams, J. S., and Beach, D. H. (1989) The fission yeast cdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization. Cell 58, 485-497
37. Yamano, H., Gannon, J., and Hunt, T. (1996) The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe. EMBO J. 15, 5268-5279
38. Tanaka, K., Petersen, J., MacIver, F., Mulvihill, D. P., Glover, D. M., and Hagan, I. M. (2001) The role of Plo1 kinase in mitotic commitment and septation in Schizosaccharomyces pombe. EMBO J. 20, 1259-1270
39. Birkenbihl, R. P., and Subramani, S. (1995) The rad21 gene product of Schizosaccharomyces pombe is a nuclear, cell cycle-regulated phosphoprotein. J. Biol. Chem. 270, 7703-7711
40. Buck, V., Ng, S. S., Ruiz-Garcia, A. B., Papadopoulou, K., Bhatti, S., Samuel, J. M., Anderson, M., Millar, J. B., and McInerny, C. J. (2004) Fkh2p and Sep1p regulate mitotic gene transcription in fission yeast. J. Cell Sci. 117, 5623-5632
41. Martín-Cuadrado, A. B., Dueñas, E., Sipiczki, M., Vázquez de Aldana, C. R., and del Rey, F. (2003) The endo-beta-1,3- glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe. J. Cell Sci. 116, 1689-1698
42. Pinar, M., Coll, P. M., Rincón, S. A., and Pérez, P. (2008) Schizosaccharomyces pombe Pxl1 is a paxillin homologue that modulates Rho1 activity and participates in cytokinesis. Mol. Biol. Cell 19, 1727-1738
43. Tasto, J. J., Morrell, J. L., and Gould, K. L. (2003) An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J. Cell Biol. 160, 1093-1103
44. Rustici, G., Mata, J., Kivinen, K., Lió, P., Penkett, C. J., Burns, G., Hayles, J., Brazma, A., Nurse, P., and Bähler, J. (2004) Periodic gene expression program of the fission yeast cell cycle. Nat. Genet. 36, 809-817
45. Oliva, A., Rosebrock, A., Ferrezuelo, F., Pyne, S., Chen, H., Skiena, S., Futcher, B., and Leatherwood, J. (2005) The cell cycle-regulated genes of Schizosaccharomyces pombe. PLoS Biol. 3, e225
46. Peng, X., Karuturi, R. K., Miller, L. D., Lin, K., Jia, Y., Kondu, P., Wang, L., Wong, L. S., Liu, E. T., Balasubramanian, M. K., and Liu, J. (2005) Identification of cell cycle-regulated genes in fission yeast. Mol. Biol. Cell 16, 1026-1042
47. Marguerat, S., Jensen, T. S., de Lichtenberg, U., Wilhelm, B. T., Jensen, L. J., and Bähler, J. (2006) The more the merrier: comparative analysis of microarray studies on cell cycle-regulated genes in fission yeast. Yeast 23, 261-277
48. Gauthier, N. P., Jensen, L. J., Wernersson, R., Brunak, S., and Jensen, T. S. (2010) Cyclebase.org: version 2.0, an updated comprehensive, multispecies repository of cell cycle experiments and derived analysis results. Nucleic Acids Res. 38, D699-D702
49. Nurse, P. M. (2002) Nobel Lecture. Cyclin dependent kinases and cell cycle control. Biosci. Rep. 22, 487-499
50. Wilson-Grady, J. T., Villén, J., and Gygi, S. P. (2008) Phosphoproteome analysis of fission yeast. J. Proteome Res. 7, 1088-1097
51. Brill, L. M., Motamedchaboki, K., Wu, S., and Wolf, D. A. (2009) Comprehensive proteomic analysis of Schizosaccharomyces pombe by two-dimensional HPLC-tandem mass spectrometry. Methods 48, 311-319
52. Wheatley, D. N., Scott, L., Lamb, J., and Smith, S. (2000) Single amino acid (arginine) restriction: growth and death of cultured HeLa and human diploid fibroblasts. Cell Physiol. Biochem. 10, 37-55
53. Funabiki, H., Yamano, H., Kumada, K., Nagao, K., Hunt, T., and Yanagida, M. (1996) Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature 381, 438-441 (Pubitemid 26162735)
54. Yamada, H. Y., Matsumoto, S., and Matsumoto, T. (2000) High dosage expression of a zinc finger protein, Grt1, suppresses a mutant of fission yeast slp1(+), a homolog of CDC20/p55CDC/Fizzy. J. Cell Sci. 113, 3989-3999 (Pubitemid 32194524)
55. Juang, Y. L., Huang, J., Peters, J. M., McLaughlin, M. E., Tai, C. Y., and Pellman, D. (1997) APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle. Science 275, 1311-1314 (Pubitemid 27114160)
56. Yamashita, A., Sato, M., Fujita, A., Yamamoto, M., and Toda, T. (2005) The roles of fission yeast ase1 in mitotic cell division, meiotic nuclear oscillation, and cytokinesis checkpoint signaling. Mol. Biol. Cell 16, 1378-1395
57. Loïodice, I., Staub, J., Setty, T. G., Nguyen, N. P., Paoletti, A., and Tran, P. T. (2005) Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol. Biol. Cell 16, 1756-1768
58. Picotti, P., Bodenmiller, B., Mueller, L. N., Domon, B., and Aebersold, R. (2009) Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 138, 795-806
59. Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Véronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., André, B., Arkin, A. P., Astromoff, A., El-Bakkoury, M., Bangham, R., Benito, R., Brachat, S., Campanaro, S., Curtiss, M., Davis, K., Deutschbauer, A., Entian, K. D., Flaherty, P., Foury, F., Garfinkel, D. J., Gerstein, M., Gotte, D., Güldener, U., Hegemann, J. H., Hempel, S., Herman, Z., Jaramillo, D. F., Kelly, D. E.., Kelly, S. L., Kötter, P., LaBonte, D., Lamb, D. C., Lan, N., Liang, H., Liao, H., Liu, L., Luo, C., Lussier, M., Mao, R., Menard, P., Ooi, S. L., Revuelta, J. L., Roberts, C. J., Rose, M., Ross-Macdonald, P., Scherens, B., Schimmack, G., Shafer, B., Shoemaker, D. D., Sookhai-Mahadeo, S., Storms, R. K., Strathern, J. N., Valle, G., Voet, M., Volckaert, G., Wang, C. Y., Ward, T. R., Wilhelmy, J., Winzeler, E. A., Yang, Y., Yen, G., Youngman, E., Yu, K., Bussey, H., Boeke, J. D., Snyder, M., Philippsen, P., Davis, R. W., and Johnston, M. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391
60. Ishihama, Y., Sato, T., Tabata, T., Miyamoto, N., Sagane, K., Nagasu, T., and Oda, Y. (2005) Quantitative mouse brain proteomics using culture-derived isotope tags as internal standards. Nat. Biotechnol. 23, 617-621
61. Geiger, T., Cox, J., Ostasiewicz, P., Wisniewski, J. R., and Mann, M. (2010) Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat. Methods 7, 383-385