Proteome dynamics: Revisiting turnover with a global perspective

Molecular and Cellular Proteomics

Volumn 11, Issue 12, 2012, Pages 1551-1565

  Claydon, Amy J ^a   Beynon, Robert ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; STABLE ISOTOPE;

CELL ORGANELLE; CHICK; CIRCADIAN RHYTHM; EXPERIMENTAL DESIGN; GROWTH; ISOTOPE LABELING; NITROGEN AVAILABILITY; NONHUMAN; PALATABILITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN MODIFICATION; PROTEIN STABILITY; REVIEW; RHYTHM; SEX DIFFERENCE; SPERM COMPETITION; SPERMATOGENESIS; TURNOVER TIME;

ANIMALS; HUMANS; ISOTOPE LABELING; PROTEINS; PROTEOLYSIS; PROTEOME; PROTEOMICS; STAINING AND LABELING;

ANIMALIA;

EID: 84870676972     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.O112.022186     Document Type: Review

References (76)

1. Van Slyke, D. D. (1942) Physiology of the amino acids. Science 95, 259
2. Schoenheimer, R. (1942) The Dynamic State of Body Constituents, Harvard University Press, Boston
3. Hinkson, I. V., and Elias, J. E. (2011) The dynamic state of protein turnover: it's about time. Trends Cell Biol. 21, 293-303
4. Cookson, E. J., Flannery, A. V., Cidlowski, J. A., and Beynon, R. J. (1992) Immunological detection of degradation intermediates of skeletal-muscle glycogen phosphorylase in vitro and in vivo. Biochem. J. 288, 291-296
5. Yewdell, J. W., Lacsina, J. R., Rechsteiner, M. C., and Nicchitta, C. V. (2011) Out with the old, in with the new? Comparing methods for measuring protein degradation. Cell Biol. Int. 35, 457-462
6. Beynon, R. J., and Pratt, J. M. (2005) Metabolic labeling of proteins for proteomics. Mol. Cell. Proteomics 4, 857-872 (Pubitemid 41309145)
7. Beynon, R. J. (2005) The dynamics of the proteome: strategies for measuring protein turnover on a proteome-wide scale. Brief. Funct. Genomic. Proteomic. 3, 382-390
8. Beynon, R. J., and Pratt, J. M. (2006) Strategies for measuring dynamics: the temporal component of proteomics. Methods Biochem. Anal. 49, 15-25 (Pubitemid 44621306)
9. Doherty, M. K., and Beynon, R. J. (2006) Protein turnover on the scale of the proteome. Expert Rev. Proteomics 3, 97-110 (Pubitemid 43979395)
10. Doherty, M. K., and Whitfield, P. D. (2011) Proteomics moves from expression to turnover: update and future perspective. Expert Rev. Proteomics 8, 325-334
11. Waterlow, J. C., Garlick, P. J., and Millward, D. J. (1978) Protein Turnover in Mammalian Tissues and in the Whole Body, Elsevier/North-Holland Biomedical Press, Amsterdam, The Netherlands
12. Schwanhausser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
13. Berlin, C. M., and Schimke, R. T. (1965) Influence of turnover rates on the responses of enzymes to cortisone. Mol. Pharmacol. 1, 149-156
14. Schimke, R. T., Sweeney, E. W., and Berlin, C. M. (1964) An analysis of the kinetics of rat liver tryptophan pyrrolase induction: the significance of both enzyme synthesis and degradation. Biochem. Biophys. Res. Commun. 15, 214-219
15. Schimke, R. T., and Doyle, D. (1970) Control of enzyme levels in animal tissues. Annu. Rev. Biochem. 39, 929-976
16. Hawkins, A. J. S. (1991) Protein turnover: a functional appraisal. Funct. Ecol. 5, 222-233
17. Millward, D. J., and Garlick, P. J. (1972) The pattern of protein turnover in the whole animal and the effect of dietary variation. Biochem. J. 129, 2P-3P
18. Millward, D. J., and Garlick, P. J. (1976) The energy cost of growth. Proc. Nutr. Soc. 35, 339-349
19. Millward, D. J. (1978) The regulation of muscle-protein turnover in growth and development. Biochem. Soc. Trans. 6, 494-499
20. Millward, D. J., Bates, P. C., and Rosochacki, S. (1981) The extent and nature of protein degradation in the tissues during development. Reprod. Nutr. Dev. 21, 265-277 (Pubitemid 11119045)
21. MacLennan, P. A., and Edwards, R. H. (1990) Protein turnover is elevated in muscle of mdx mice in vivo. Biochem. J. 268, 795-797 (Pubitemid 20196971)
22. Claydon, A. J., Thom, M. D., Hurst, J. L., and Beynon, R. J. (2012) Protein turnover: measurement of proteome dynamics by whole animal metabolic labelling with stable isotope labelled amino acids. Proteomics 12, 1194-1206
23. Boisvert, F. M., Ahmad, Y., Gierlinski, M., Charriere, F., Lamont, D., Scott, M., Barton, G., and Lamond, A. I. (2012) A quantitative spatial proteomics analysis of proteome turnover in human cells. Mol. Cell. Proteomics 11, M111.011429
24. Doherty, M. K., Hammond, D. E., Clague, M. J., Gaskell, S. J., and Beynon, R. J. (2009) Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J. Proteome Res. 8, 104-112
25. Kim, T. Y., Wang, D., Kim, A. K., Lau, E., Lin, A. J., Liem, D. A., Zhang, J., Zong, N. C., Lam, M. P., and Ping, P. (2012) Metabolic labeling reveals proteome dynamics of mouse mitochondria. Mol. Cell. Proteomics 10.1074/mcp.M112.021162
26. Cambridge, S. B., Gnad, F., Nguyen, C., Bermejo, J. L., Kruger, M., and Mann, M. (2011) Systems-wide proteomic analysis in mammalian cells reveals conserved, functional protein turnover. J. Proteome Res. 10, 5275-5284
27. Alvarez-Castelao, B., Ruiz-Rivas, C., and Castano, J. (2012) A critical appraisal of quantitative studies of protein degradation in the framework of cellular proteostasis. Biochem. Res. Int. 2012, 10.1155/2012/823597
28. Keene, O. N. (1995) The log transformation is special. Stat. Med. 14, 811-819
29. Troetschel, C., Albaum, S. P., Wolff, D., Schroeder, S., Goesmann, A., Nattkemper, T. W., and Poetsch, A. (2012) Protein turnover quantification in a multi-labeling approach-from data calculation to evaluation. Mol. Cell. Proteomics 11, 512-526
30. Dice, J. F., and Goldberg, A. L. (1975) Relationship between in vivo degradative rates and isoelectric points of proteins. Proc. Natl. Acad. Sci. U.S.A. 72, 3893-3897
31. Savas, J. N., Toyama, B. H., Xu, T., Yates, J. R., and Hetzer, M. W. (2012) Extremely long-lived nuclear pore proteins in the rat brain. Science 335, 942
32. Waterlow, J. C. (1995) Whole-body protein turnover in humans - past, present, and future. Annu. Rev. Nutr. 15, 57-92
33. Guan, S., Price, J. C., Ghaemmaghami, S., Prusiner, S. B., and Burlingame, A. L. (2012) Compartment modeling for mammalian protein turnover studies by stable isotope metabolic labeling. Anal. Chem. 84, 4014-4021
34. Beynon, R. J., Leyland, D. M., Evershed, R. P., Edwards, R. H., and Coburn, S. P. (1996) Measurement of the turnover of glycogen phosphorylase by gc/ms using stable isotope derivatives of pyridoxine (vitamin b6). Biochem. J. 317, 613-619 (Pubitemid 26254003)
35. Busch, R., Kim, Y. K., Neese, R. A., Schade-Serin, V., Collins, M., Awada, M., Gardner, J. L., Beysen, C., Marino, M. E., Misell, L. M., and Hellerstein, M. K. (2006) Measurement of protein turnover rates by heavy water labeling of nonessential amino acids. Biochim. Biophys. Acta 1760, 730-744
36. Price, J. C., Holmes, W. E., Li, K. W., Floreani, N. A., Neese, R. A., Turner, S. M., and Hellerstein, M. K. (2012) Measurement of human plasma proteome dynamics with (2)h(2)o and liquid chromatography tandem mass spectrometry. Anal. Biochem. 420, 73-83
37. Rachdaoui, N., Austin, L., Kramer, E., Previs, M. J., Anderson, V. E., Kasumov, T., and Previs, S. F. (2009) Measuring proteome dynamics in vivo: as easy as adding water? Mol. Cell. Proteomics 8, 2653-2663
38. Kasumov, T., Ilchenko, S., Li, L., Rachdaoui, N., Sadygov, R. G., Willard, B., McCullough, A. J., and Previs, S. (2011) Measuring protein synthesis using metabolic (2)h labeling, high-resolution mass spectrometry, and an algorithm. Anal. Biochem. 412, 47-55
39. Pratt, J. M., Petty, J., Riba-Garcia, I., Robertson, D. H., Gaskell, S. J., Oliver, S. G., and Beynon, R. J. (2002) Dynamics of protein turnover, a missing dimension in proteomics. Mol. Cell. Proteomics 1, 579-591
40. Helbig, A. O., Daran-Lapujade, P., van Maris, A. J., de Hulster, E. A., de Ridder, D., Pronk, J. T., Heck, A. J., and Slijper, M. (2011) The diversity of protein turnover and abundance under nitrogen-limited steady-state conditions in saccharomyces cerevisiae. Mol. Biosyst. 7, 3316-3326
41. Lampert, F. M., Matt, P., Grapow, M., Lefkovits, I., Zerkowski, H. R., and Grussenmeyer, T. (2007) "Turnover proteome" of human atrial trabeculae. J. Proteome Res. 6, 4458-4468 (Pubitemid 350158521)
42. Doherty, M. K., Whitehead, C., McCormack, H., Gaskell, S. J., and Beynon, R. J. (2005) Proteome dynamics in complex organisms: using stable isotopes to monitor individual protein turnover rates. Proteomics 5, 522-533 (Pubitemid 40262069)
43. Price, J. C., Guan, S., Burlingame, A., Prusiner, S. B., and Ghaemmaghami, S. (2010) Analysis of proteome dynamics in the mouse brain. Proc. Natl. Acad. Sci. U.S.A. 107, 14508-14513
44. Zhang, Y., Reckow, S., Webhofer, C., Boehme, M., Gormanns, P., Egge-Jacobsen, W. M., and Turck, C. W. (2011) Proteome scale turnover analysis in live animals using stable isotope metabolic labeling. Anal. Chem. 83, 1665-1672
45. Westman-Brinkmalm, A., Abramsson, A., Pannee, J., Gang, C., Gustavsson, M. K., von Otter, M., Blennow, K., Brinkmalm, G., Heumann, H., and Zetterberg, H. (2011) SILAC zebrafish for quantitative analysis of protein turnover and tissue regeneration. J. Proteomics 75, 425-434
46. Chow, L. S., Albright, R. C., Bigelow, M. L., Toffolo, G., Cobelli, C., and Nair, K. S. (2006) Mechanism of insulin's anabolic effect on muscle: measurements of muscle protein synthesis and breakdown using aminoacyl-tRNA and other surrogate measures. Am. J. Physiol. Endocrinol. Metab. 291, E729-E736 (Pubitemid 44484914)
47. Watt, P. W., Lindsay, Y., Scrimgeour, C. M., Chien, P. A., Gibson, J. N., Taylor, D. J., and Rennie, M. J. (1991) Isolation of aminoacyl-tRNA and its labeling with stable-isotope tracers: use in studies of human tissue protein synthesis. Proc. Natl. Acad. Sci. U.S.A. 88, 5892-5896 (Pubitemid 21914852)
48. Airhart, J., Vidrich, A., and Khairallah, E. A. (1974) Compartmentation of free amino acids for protein synthesis in rat liver. Biochem. J. 140, 539-545
49. Khairallah, E. A., and Mortimore, G. E. (1976) Assessment of protein turnover in perfused rat liver. Evidence for amino acid compartmentation from differential labeling of free and tRNA-gound valine. J. Biol. Chem. 251, 1375-1384
50. Papageorgopoulos, C., Caldwell, K., Shackleton, C., Schweingrubber, H., and Hellerstein, M. K. (1999) Measuring protein synthesis by mass isotopomer distribution analysis (MIDA). Anal. Biochem. 267, 1-16 (Pubitemid 29061800)
51. Dietschy, J. M., and McGarry, J. D. (1974) Limitations of acetate as a substrate for measuring cholesterol synthesis in liver. J. Biol. Chem. 249, 52-58
52. Hellerstein, M. K., and Neese, R. A. (1992) Mass isotopomer distribution analysis: a technique for measuring biosynthesis and turnover of polymers. Am. J. Physiol. 263, E988-E1001
53. Hellerstein, M. K., and Neese, R. A. (1999) Mass isotopomer distribution analysis at eight years: theoretical, analytic, and experimental considerations. Am. J. Physiol. 276, E1146-E1170 (Pubitemid 29323432)
54. Papageorgopoulos, C., Caldwell, K., Schweingrubber, H., Neese, R. A., Shackleton, C. H., and Hellerstein, M. (2002) Measuring synthesis rates of muscle creatine kinase and myosin with stable isotopes and mass spectrometry. Anal. Biochem. 309, 1-10 (Pubitemid 35305783)
55. Beynon, R. J., and Hurst, J. L. (2003) Multiple roles of major urinary proteins in the house mouse, mus domesticus. Biochem. Soc. Trans. 31, 142-146 (Pubitemid 36241415)
56. Cheetham, S. A., Smith, A. L., Armstrong, S. D., Beynon, R. J., and Hurst, J. L. (2009) Limited variation in the major urinary proteins of laboratory mice. Physiol. Behav. 96, 253-261
57. Ramm, S. A., Oliver, P. L., Ponting, C. P., Stockley, P., and Emes, R. D. (2008) Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Mol. Biol. Evol. 25, 207-219
58. Ramm, S. A., McDonald, L., Hurst, J. L., Beynon, R. J., and Stockley, P. (2009) Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition. Mol. Biol. Evol. 26, 189-198
59. Simpson, R. J., Lim, J. W., Moritz, R. L., and Mathivanan, S. (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev. Proteomics 6, 267-283
60. Brownridge, P., Holman, S. W., Gaskell, S. J., Grant, C. M., Harman, V. M., Hubbard, S. J., Lanthaler, K., Lawless, C., O'Cualain, R., Sims, P., Watkins, R., and Beynon, R. J. (2011) Global absolute quantification of a proteome: challenges in the deployment of a QconCAT strategy. Proteomics 11, 2957-2970
61. Carroll, K. M., Simpson, D. M., Eyers, C. E., Knight, C. G., Brownridge, P., Dunn, W. B., Winder, C. L., Lanthaler, K., Pir, P., Malys, N., Kell, D. B., Oliver, S. G., Gaskell, S. J., and Beynon, R. J. (2011) Absolute quantification of the glycolytic pathway in yeast: deployment of a complete QconCAT approach. Mol. Cell. Proteomics 10, M111.007633
62. Lee, A. Y., Yates, N. A., Ichetovkin, M., Deyanova, E., Southwick, K., Fisher, T. S., Wang, W., Loderstedt, J., Walker, N., Zhou, H., Zhao, X., Sparrow, C. P., Hubbard, B. K., Rader, D. J., Sitlani, A., Millar, J. S., and Hendrickson, R. C. (2012) Measurement of fractional synthetic rates of multiple protein analytes by triple quadrupole mass spectrometry. Clin. Chem. 58, 619-627
63. McClatchy, D. B., Dong, M. Q., Wu, C. C., Venable, J. D., and Yates, J. R. (2007) 15n metabolic labeling of mammalian tissue with slow protein turnover. J. Proteome Res. 6, 2005-2010 (Pubitemid 46814521)
64. Wu, C. C., MacCoss, M. J., Howell, K. E., Matthews, D. E., and Yates, J. R. (2004) Metabolic labeling of mammalian organisms with stable isotopes for quantitative proteomic analysis. Anal. Chem. 76, 4951-4959 (Pubitemid 39180319)
65. Johnson, H. A., Baldwin, R. L., France, J., and Calvert, C. C. (1999) A model of whole-body protein turnover based on leucine kinetics in rodents. J. Nutr. 129, 728-739 (Pubitemid 29118059)
66. Vogt, J. A., Hunzinger, C., Schroer, K., Holzer, K., Bauer, A., Schrattenholz, A., Cahill, M. A., Schillo, S., Schwall, G., Stegmann, W., and Albuszies, G. (2005) Determination of fractional synthesis rates of mouse hepatic proteins via metabolic 13c-labeling, MALDI-TOF MS and analysis of relative isotopologue abundances using average masses. Anal. Chem. 77, 2034-2042 (Pubitemid 40463818)
67. Hsieh, E. J., Shulman, N. J., Dai, D. F., Vincow, E. S., Karunadharma, P. P., Pallanck, L., Rabinovitch, P. S., and Maccoss, M. J. (2012) Topograph, a software platform for precursor enrichment corrected global protein turnover measurements. Mol. Cell. Proteomics 11, 1468-1474.
68. Cargile, B. J., Bundy, J. L., Grunden, A. M., and Stephenson, J. L. J. (2004) Synthesis/degradation ratio mass spectrometry for measuring relative dynamic protein turnover. Anal. Chem. 76, 86-97 (Pubitemid 38040636)
69. Maier, T., Schmidt, A., Guell, M., Kuhner, S., Gavin, A. C., Aebersold, R., and Serrano, L. (2011) Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol. Syst. Biol. 7, 511
70. Rao, P. K., Roxas, B. A., and Li, Q. (2008) Determination of global protein turnover in stressed mycobacterium cells using hybrid-linear ion trap- Fourier transform mass spectrometry. Anal. Chem. 80, 396-406
71. Jayapal, K. P., Sui, S., Philp, R. J., Kok, Y. J., Yap, M. G., Griffin, T. J., and Hu, W. S. (2010) Multitagging proteomic strategy to estimate protein turnover rates in dynamic systems. J. Proteome Res. 9, 2087-2097
72. Martin, S. F., Munagapati, V. S., Salvo-Chirnside, E., Kerr, L. E., and Le Bihan, T. (2012) Proteome turnover in the green alga Ostreococcus tauri by time course 15n metabolic labeling mass spectrometry. J. Proteome Res. 11, 476-486
73. Schwanhausser, B., Gossen, M., Dittmar, G., and Selbach, M. (2009) Global analysis of cellular protein translation by pulsed SILAC. Proteomics 9, 205-209
74. Claydon, A. J., Ramm, S. A., Pennington, A., Hurst, J. L., Stockley, P., and Beynon, R. (2012) Heterogenous turnover of sperm and seminal vesicle proteins in the mouse revealed by dynamic metabolic labeling. Mol. Cell. Proteomics 11, M111.014993
75. Li, L., Willard, B., Rachdaoui, N., Kirwan, J. P., Sadygov, R. G., Stanley, W. C., Previs, S., McCullough, A. J., and Kasumov, T. (2012) Plasma proteome dynamics: analysis of lipoproteins and acute phase response proteins with 2h2o metabolic labeling. Mol. Cell. Proteomics 11, M111.014209
76. Doherty, M. K., Brownridge, P., Owen, M. A., Davies, S. J., Young, I. S., and Whitfield, P. D. (2012) A proteomics strategy for determining the synthesis and degradation rates of individual proteins in fish. J. Proteomics 19, 4471-4477