Kinetic Analysis of Protein Stability Reveals Age-Dependent Degradation

Cell

Volumn 167, Issue 3, 2016, Pages 803-815.e21

  McShane, Erik ^a   Sin, Celine ^b   Zauber, Henrik ^a   Wells, Jonathan N ^c   Donnelly, Neysan ^d   Wang, Xi ^a   Hou, Jingyi ^a   Chen, Wei ^a   Storchova, Zuzana ^d,e   Marsh, Joseph A ^c   Valleriani, Angelo ^b   Selbach, Matthias ^a,f  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^e University of Koblenz Landau   (Germany)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

aneuploidy; bioorthogonal amino acid tagging; gene copy number alterations; metabolic labeling; posttranslational control; protein complex assembly; protein degradation; proteomics; pulse chase experiment; trisomy

Indexed keywords

CD147 ANTIGEN; CELL PROTEIN; MULTIPROTEIN COMPLEX; ALANINE; AZIDOHOMOALANINE; PROTEASOME; PROTEIN; PROTEOME; UBIQUITIN;

ANEUPLOIDY; ARTICLE; ATTENUATION; CLICK CHEMISTRY; GENE AMPLIFICATION; IMMUNOPRECIPITATION; KINETICS; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN STABILITY; STOCHASTIC MODEL; STOICHIOMETRY; ANALOGS AND DERIVATIVES; CELL LINE; CHEMISTRY; GENETICS; HUMAN; MARKOV CHAIN; METABOLISM; PROTEIN SYNTHESIS;

ALANINE; ANEUPLOIDY; CELL LINE; CLICK CHEMISTRY; GENE AMPLIFICATION; HUMANS; KINETICS; MARKOV CHAINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; PROTEIN STABILITY; PROTEINS; PROTEOLYSIS; PROTEOME; UBIQUITIN;

EID: 84992386893     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.09.015     Document Type: Article

References (72)

1. Aalen, O.O., Effects of frailty in survival analysis. Stat. Methods Med. Res. 3 (1994), 227–243.
2. Aalen, O.O., Gjessing, H.K., Understanding the shape of the hazard rate: a process point of view (With comments and a rejoinder by the authors). Stat. Sci. 16 (2001), 1–22.
3. Akaike, H., A new look at the statistical model identification. IEEE Transactions Autom. Control 19 (1974), 716–723.
4. Andersen, J.S., Lam, Y.W., Leung, A.K., Ong, S.E., Lyon, C.E., Lamond, A.I., Mann, M., Nucleolar proteome dynamics. Nature 433 (2005), 77–83.
5. Battle, A., Khan, Z., Wang, S.H., Mitrano, A., Ford, M.J., Pritchard, J.K., Gilad, Y., Genomic variation. Impact of regulatory variation from RNA to protein. Science 347 (2015), 664–667.
6. Blikstad, I., Nelson, W.J., Moon, R.T., Lazarides, E., Synthesis and assembly of spectrin during avian erythropoiesis: stoichiometric assembly but unequal synthesis of alpha and beta spectrin. Cell 32 (1983), 1081–1091.
7. Bourdetsky, D., Schmelzer, C.E., Admon, A., The nature and extent of contributions by defective ribosome products to the HLA peptidome. Proc Natl Acad Sci USA 111 (2014), 1591–1599.
8. Burnham, K.P., Anderson, D.R., Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2002, Springer-Verlag.
9. Chew, G.L., Pauli, A., Rinn, J.L., Regev, A., Schier, A.F., Valen, E., Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs. Development 140 (2013), 2828–2834.
10. Ciechanover, A., Aaron Ciechanover - Nobel Lecture: Intracellular Protein Degradation, The Nobel Prizes 2004. 2005, Science History Publications/Watson Publishing.
11. Cohen, L.D., Zuchman, R., Sorokina, O., Müller, A., Dieterich, D.C., Armstrong, J.D., Ziv, T., Ziv, N.E., Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance. PLoS ONE, 8, 2013, e63191.
12. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26 (2008), 1367–1372.
13. de Lichtenberg, U., Jensen, L.J., Brunak, S., Bork, P., Dynamic complex formation during the yeast cell cycle. Science 307 (2005), 724–727.
14. Deneke, C., Lipowsky, R., Valleriani, A., Complex degradation processes lead to non-exponential decay patterns and age-dependent decay rates of messenger RNA. PLoS ONE, 8, 2013, e55442.
15. Dephoure, N., Hwang, S., O'Sullivan, C., Dodgson, S.E., Gygi, S.P., Amon, A., Torres, E.M., Quantitative proteomic analysis reveals posttranslational responses to aneuploidy in yeast. eLife, 3, 2014, e03023.
16. Dieterich, D.C., Link, A.J., Graumann, J., Tirrell, D.A., Schuman, E.M., Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc. Natl. Acad. Sci. USA 103 (2006), 9482–9487.
17. Doherty, M.K., Hammond, D.E., Clague, M.J., Gaskell, S.J., Beynon, R.J., Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J. Proteome Res. 8 (2009), 104–112.
18. Duttler, S., Pechmann, S., Frydman, J., Principles of cotranslational ubiquitination and quality control at the ribosome. Mol. Cell 50 (2013), 379–393.
19. Eichelbaum, K., Krijgsveld, J., Rapid temporal dynamics of transcription, protein synthesis, and secretion during macrophage activation. Mol. Cell. Proteomics 13 (2014), 792–810.
20. Eichelbaum, K., Winter, M., Berriel Diaz, M., Herzig, S., Krijgsveld, J., Selective enrichment of newly synthesized proteins for quantitative secretome analysis. Nat. Biotechnol. 30 (2012), 984–990.
21. Eravci, M., Sommer, C., Selbach, M., IPG strip-based peptide fractionation for shotgun proteomics. Methods Mol. Biol. 1156 (2014), 67–77.
22. Geiger, T., Cox, J., Mann, M., Proteomic changes resulting from gene copy number variations in cancer cells. PLoS Genet., 6, 2010, e1001090.
23. Goldberg, A.L., Protein degradation and protection against misfolded or damaged proteins. Nature 426 (2003), 895–899.
24. Goldberg, A.L., Dice, J.F., Intracellular protein degradation in mammalian and bacterial cells. Annu. Rev. Biochem. 43 (1974), 835–869.
25. Hinkson, I.V., Elias, J.E., The dynamic state of protein turnover: It's about time. Trends Cell Biol. 21 (2011), 293–303.
26. Hou, J., Wang, X., McShane, E., Zauber, H., Sun, W., Selbach, M., Chen, W., Extensive allele-specific translational regulation in hybrid mice. Mol. Syst. Biol., 11, 2015, 825.
27. Howden, A.J.M., Geoghegan, V., Katsch, K., Efstathiou, G., Bhushan, B., Boutureira, O., Thomas, B., Trudgian, D.C., Kessler, B.M., Dieterich, D.C., et al. QuaNCAT: quantitating proteome dynamics in primary cells. Nat. Methods 10 (2013), 343–346.
28. Jovanovic, M., Rooney, M.S., Mertins, P., Przybylski, D., Chevrier, N., Satija, R., Rodriguez, E.H., Fields, A.P., Schwartz, S., Raychowdhury, R., et al. Immunogenetics. Dynamic profiling of the protein life cycle in response to pathogens. Science, 347, 2015, 1259038.
29. Kiick, K.L., Saxon, E., Tirrell, D.A., Bertozzi, C.R., Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation. Proc. Natl. Acad. Sci. USA 99 (2002), 19–24.
30. Kim, W., Bennett, E.J., Huttlin, E.L., Guo, A., Li, J., Possemato, A., Sowa, M.E., Rad, R., Rush, J., Comb, M.J., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44 (2011), 325–340.
31. Kristensen, A.R., Gsponer, J., Foster, L.J., Protein synthesis rate is the predominant regulator of protein expression during differentiation. Mol. Syst. Biol., 9, 2013, 689.
32. Kulak, N.A., Pichler, G., Paron, I., Nagaraj, N., Mann, M., Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat. Methods 11 (2014), 319–324.
33. Lam, Y.W., Lamond, A.I., Mann, M., Andersen, J.S., Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 17 (2007), 749–760.
34. Larance, M., Ahmad, Y., Kirkwood, K.J., Ly, T., Lamond, A.I., Global subcellular characterization of protein degradation using quantitative proteomics. Mol. Cell. Proteomics 12 (2013), 638–650.
35. Leibiger, C., Kosyakova, N., Mkrtchyan, H., Glei, M., Trifonov, V., Liehr, T., First molecular cytogenetic high resolution characterization of the NIH 3T3 cell line by murine multicolor banding. J. Histochem. Cytochem. 61 (2013), 306–312.
36. Li, G.W., Burkhardt, D., Gross, C., Weissman, J.S., Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157 (2014), 624–635.
37. Liao, L., Park, S.K., Xu, T., Vanderklish, P., Yates, J.R. 3rd, Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice. Proc. Natl. Acad. Sci. USA 105 (2008), 15281–15286.
38. Liu, B., Han, Y., Qian, S.B., Cotranslational response to proteotoxic stress by elongation pausing of ribosomes. Mol. Cell 49 (2013), 453–463.
39. Marsh, J.A., Hernández, H., Hall, Z., Ahnert, S.E., Perica, T., Robinson, C.V., Teichmann, S.A., Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 153 (2013), 461–470.
40. Matalon, O., Horovitz, A., Levy, E.D., Different subunits belonging to the same protein complex often exhibit discordant expression levels and evolutionary properties. Curr. Opin. Struct. Biol. 26 (2014), 113–120.
41. Motoyama, A., Xu, T., Ruse, C.I., Wohlschlegel, J.A., Yates, J.R. 3rd, Anion and cation mixed-bed ion exchange for enhanced multidimensional separations of peptides and phosphopeptides. Anal. Chem. 79 (2007), 3623–3634.
42. Nedialkova, D.D., Leidel, S.A., Optimization of Codon Translation Rates via tRNA Modifications Maintains Proteome Integrity. Cell 161 (2015), 1606–1618.
43. Okamura, Y., Aoki, Y., Obayashi, T., Tadaka, S., Ito, S., Narise, T., Kinoshita, K., COXPRESdb in 2015: coexpression database for animal species by DNA-microarray and RNAseq-based expression data with multiple quality assessment systems. Nucleic Acids Res. 43 (2015), D82–D86.
44. Ong, S.E., Blagoev, B., Kratchmarova, I., Kristensen, D.B., Steen, H., Pandey, A., Mann, M., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1 (2002), 376–386.
45. Ori, A., Iskar, M., Buczak, K., Kastritis, P., Parca, L., Andrés-Pons, A., Singer, S., Bork, P., Beck, M., Spatiotemporal variation of mammalian protein complex stoichiometries. Genome Biol., 17, 2016, 47.
46. Puchades, M., Westman, A., Blennow, K., Davidsson, P., Removal of sodium dodecyl sulfate from protein samples prior to matrix-assisted laser desorption/ionization mass spectrometry. Rapid Commun. Mass Spectrom. 13 (1999), 344–349.
47. Rappsilber, J., Ishihama, Y., Mann, M., Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75 (2003), 663–670.
48. Ruepp, A., Brauner, B., Dunger-Kaltenbach, I., Frishman, G., Montrone, C., Stransky, M., Waegele, B., Schmidt, T., Doudieu, O.N., Stümpflen, V., Mewes, H.W., CORUM: the comprehensive resource of mammalian protein complexes. Nucleic Acids Res. 36 (2008), D646–D650.
49. Santaguida, S., Amon, A., Short- and long-term effects of chromosome mis-segregation and aneuploidy. Nat. Rev. Mol. Cell Biol. 16 (2015), 473–485.
50. Schimke, R.T., Doyle, D., Control of enzyme levels in animal tissues. Annu. Rev. Biochem. 39 (1970), 929–976.
51. Schoenheimer, R., The Dynamic State of Body Constituents. 1942, Harvard University Press.
52. Schubert, U., Antón, L.C., Gibbs, J., Norbury, C.C., Yewdell, J.W., Bennink, J.R., Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404 (2000), 770–774.
53. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., Selbach, M., Global quantification of mammalian gene expression control. Nature 473 (2011), 337–342.
54. Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R., Rajewsky, N., Widespread changes in protein synthesis induced by microRNAs. Nature 455 (2008), 58–63.
55. Shalgi, R., Hurt, J.A., Krykbaeva, I., Taipale, M., Lindquist, S., Burge, C.B., Widespread regulation of translation by elongation pausing in heat shock. Mol. Cell 49 (2013), 439–452.
56. Sheean, M.E., McShane, E., Cheret, C., Walcher, J., Müller, T., Wulf-Goldenberg, A., Hoelper, S., Garratt, A.N., Krüger, M., Rajewsky, K., et al. Activation of MAPK overrides the termination of myelin growth and replaces Nrg1/ErbB3 signals during Schwann cell development and myelination. Genes Dev. 28 (2014), 290–303.
57. Sin, C., Chiarugi, D., Valleriani, A., Degradation parameters from pulse-chase experiments. PLoS ONE, 11, 2016, e0155028.
58. Sormanni, P., Camilloni, C., Fariselli, P., Vendruscolo, M., The s2D method: simultaneous sequence-based prediction of the statistical populations of ordered and disordered regions in proteins. J. Mol. Biol. 427 (2015), 982–996.
59. Stingele, S., Stoehr, G., Peplowska, K., Cox, J., Mann, M., Storchova, Z., Global analysis of genome, transcriptome and proteome reveals the response to aneuploidy in human cells. Mol. Syst. Biol., 8, 2012, 608.
60. Subtelny, A.O., Eichhorn, S.W., Chen, G.R., Sive, H., Bartel, D.P., Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 508 (2014), 66–71.
61. Sury, M.D., McShane, E., Hernandez-Miranda, L.R., Birchmeier, C., Selbach, M., Quantitative proteomics reveals dynamic interaction of c-Jun N-terminal kinase (JNK) with RNA transport granule proteins splicing factor proline- and glutamine-rich (Sfpq) and non-POU domain-containing octamer-binding protein (Nono) during neuronal differentiation. Mol. Cell. Proteomics 14 (2015), 50–65.
62. tom Dieck, S., Kochen, L., Hanus, C., Heumüller, M., Bartnik, I., Nassim-Assir, B., Merk, K., Mosler, T., Garg, S., Bunse, S., et al. Direct visualization of newly synthesized target proteins in situ. Nat. Methods 12 (2015), 411–414.
63. Toyama, B.H., Savas, J.N., Park, S.K., Harris, M.S., Ingolia, N.T., Yates, J.R. 3rd, Hetzer, M.W., Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154 (2013), 971–982.
64. Tyler, R.E., Pearce, M.M.P., Shaler, T.A., Olzmann, J.A., Greenblatt, E.J., Kopito, R.R., Unassembled CD147 is an endogenous endoplasmic reticulum-associated degradation substrate. Mol. Biol. Cell 23 (2012), 4668–4678.
65. Vabulas, R.M., Hartl, F.U., Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310 (2005), 1960–1963.
66. Vavouri, T., Semple, J.I., Garcia-Verdugo, R., Lehner, B., Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138 (2009), 198–208.
67. Ward, C.L., Kopito, R.R., Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J. Biol. Chem. 269 (1994), 25710–25718.
68. Wells, J.N., Bergendahl, L.T., Marsh, J.A., Operon gene order is optimized for ordered protein complex assembly. Cell Rep. 14 (2016), 679–685.
69. Wheatley, D.N., Giddings, M.R., Inglis, M.S., Kinetics of degradation of “short-” and “long-lived” proteins in cultured mammalian cells. Cell Biol. Int. Rep. 4 (1980), 1081–1090.
70. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G., McCoy, A., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 235–242.
71. Wiśniewski, J.R., Zougman, A., Mann, M., Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J. Proteome Res. 8 (2009), 5674–5678.
72. Xie, S.Q., Nie, P., Wang, Y., Wang, H., Li, H., Yang, Z., Liu, Y., Ren, J., Xie, Z., RPFdb: a database for genome wide information of translated mRNA generated from ribosome profiling. Nucleic Acids Res. 44:D1 (2016), D254–D258.