Thermosensitivity of growth is determined by chaperone-mediated proteome reallocation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 43, 2017, Pages 11548-11553

  Chen, Ke ^a   Gao, Ye ^b   Mih, Nathan ^a,c   O'Brien, Edward J ^a   Yang, Laurence ^a   Palsson, Bernhard O ^a,d,e  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e Chalmers University of Technology   (Denmark)

Author keywords

Bacterial growth law; Genome scale model; Molecular chaperones; Proteome allocation; Thermoadaptation

Indexed keywords

CHAPERONE; PROTEOME; ESCHERICHIA COLI PROTEIN; HEAT SHOCK PROTEIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; COMPUTER MODEL; CONTROLLED STUDY; ESCHERICHIA COLI K 12; GROWTH RATE; HEAT SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SYNTHESIS; SIMULATION; TEMPERATURE; THERMOSTABILITY; CHEMICAL MODEL; COMPUTER SIMULATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; HEAT; HUMAN; METABOLISM; PHYSIOLOGY;

COMPUTER SIMULATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK PROTEINS; HOT TEMPERATURE; HUMANS; MODELS, CHEMICAL; PROTEIN FOLDING; PROTEOME;

EID: 85032175673     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1705524114     Document Type: Article

References (61)

1. Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: Sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1-43.
2. Nguyen V, et al. (2017) Evolutionary drivers of thermoadaptation in enzyme catalysis. Science 355:289-294.
3. Bennett AF, Lenski RE (2007) An experimental test of evolutionary trade-offs during temperature adaptation. Proc Natl Acad Sci USA 104:8649-8654.
4. Tenaillon O, et al. (2012) The molecular diversity of adaptive convergence. Science 335:457-461.
5. Sandberg TE, et al. (2014) Evolution of Escherichia coli to 42 °C and subsequent genetic engineering reveals adaptive mechanisms and novel mutations. Mol Biol Evol 31:2647-2662.
6. Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125:443-451.
7. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324-332.
8. Saibil H (2013) Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol 14:630-642.
9. Genevaux P, Georgopoulos C, Kelley WL (2007) The Hsp70 chaperone machines of Escherichia coli: A paradigm for the repartition of chaperone functions. Mol Microbiol 66:840-857.
10. Horwich AL, Farr GW, Fenton WA (2006) GroEL-GroES-mediated protein folding. Chem Rev 106:1917-1930.
11. Hu B, Mayer MP, Tomita M (2006) Modeling Hsp70-mediated protein folding. Biophys J 91:496-507.
12. Tehver R, Thirumalai D (2008) Kinetic model for the coupling between allosteric transitions in GroEL and substrate protein folding and aggregation. J Mol Biol 377: 1279-1295.
13. Hingorani KS, Gierasch LM (2014) Comparing protein folding in vitro and in vivo: Foldability meets the fitness challenge. Curr Opin Struct Biol 24:81-90.
14. Powers ET, Powers DL, Gierasch LM (2012) FoldEco: A model for proteostasis in E. coli. Cell Rep 1:265-276.
15. Cho Y, et al. (2015) Individual and collective contributions of chaperoning and degradation to protein homeostasis in E. coli. Cell Rep 11:321-333.
16. Deuerling E, et al. (2003) Trigger factor and DnaK possess overlapping substrate pools and binding specificities. Mol Microbiol 47:1317-1328.
17. Kerner MJ, et al. (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122:209-220.
18. Calloni G, et al. (2012) Dnak functions as a central hub in the E. coli chaperone network. Cell Rep 1:251-264.
19. Corkrey R, et al. (2014) Protein thermodynamics can be predicted directly from biological growth rates. PLoS One 9:e96100.
20. Chen P, Shakhnovich EI (2010) Thermal adaptation of viruses and bacteria. Biophys J 98:1109-1118.
21. Dill KA, Ghosh K, Schmit JD (2011) Physical limits of cells and proteomes. Proc Natl Acad Sci USA 108:17876-17882.
22. Lerman JA, et al. (2012) In silico method for modelling metabolism and gene product expression at genome scale. Nat Commun 3:929.
23. Thiele I, et al. (2012) Multiscale modeling of metabolism and macromolecular synthesis in E. coli and its application to the evolution of codon usage. PLoS One 7:e45635.
24. O'Brien EJ, Lerman JA, Chang RL, Hyduke DR, Palsson BØ (2013) Genome-scale models of metabolism and gene expression extend and refine growth phenotype prediction. Mol Syst Biol 9:693.
25. Scott M, Gunderson CW, Mateescu EM, Zhang Z, Hwa T (2010) Interdependence of cell growth and gene expression: Origins and consequences. Science 330:1099-1102.
26. Chang RL, et al. (2013) Structural systems biology evaluation of metabolic thermotolerance in Escherichia coli. Science 340:1220-1223.
27. Brunk E, et al. (2016) Systems biology of the structural proteome. BMC Syst Biol 10:26.
28. Mayer M, Bukau B (2005) Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci 62:670-684.
29. Pierpaoli EV, et al. (1997) The power stroke of the DnaK/DnaJ/GrpE molecular chaperone system. J Mol Biol 269:757-768.
30. Jewett A, Shea JE (2008) Do chaperonins boost protein yields by accelerating folding or preventing aggregation? Biophys J 94:2987-2993.
31. Schröder H, Langer T, Hartl F, Bukau B (1993) DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J 12:4137-4144.
32. Weissman JS, Kashi Y, Fenton WA, Horwich AL (1994) GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78: 693-702.
33. Santra M, Farrell DW, Dill KA (2017) Bacterial proteostasis balances energy and chaperone utilization efficiently. Proc Natl Acad Sci USA 114:E2654-E2661.
34. Herendeen SL, Vanbogelen RA, Neidhardt FC (1979) Levels of major proteins of Escherichia coli during growth at different temperatures. J Bacteriol 139:185-194.
35. Seyer K, Lessard M, Piette G, Lacroix M, Saucier L (2003) Escherichia coli heat shock protein DnaK: Production and consequences in terms of monitoring cooking. Appl Environ Microbiol 69:3231-3237.
36. Rudolph B, Gebendorfer KM, Buchner J, Winter J (2010) Evolution of Escherichia coli for growth at high temperatures. J Biol Chem 285:19029-19034.
37. Yang L, et al. (2015) Systems biology definition of the core proteome of metabolism and expression is consistent with high-throughput data. Proc Natl Acad Sci USA 112:10810-10815.
38. Scott M, Klumpp S, Mateescu EM, Hwa T (2014) Emergence of robust growth laws from optimal regulation of ribosome synthesis. Mol Syst Biol 10:747.
39. Maitra A, Dill KA (2015) Bacterial growth laws reflect the evolutionary importance of energy efficiency. Proc Natl Acad Sci USA 112:406-411.
40. Bershtein S, Choi JM, Bhattacharyya S, Budnik B, Shakhnovich E (2015) Systemslevel response to point mutations in a core metabolic enzyme modulates genotypephenotype relationship. Cell Rep 11:645-656.
41. Bershtein S, Mu W, Serohijos AW, Zhou J, Shakhnovich EI (2013) Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness. Mol Cell 49:133-144.
42. Gromiha MM (2005) A statistical model for predicting protein folding rates from amino acid sequence with structural class information. J Chem Inf Model 45:494-501.
43. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
44. Bakan A, Meireles LM, Bahar I (2011) Prody: Protein dynamics inferred from theory and experiments. Bioinformatics 27:1575-1577.
45. Scalley ML, Baker D (1997) Protein folding kinetics exhibit an Arrhenius temperature dependence when corrected for the temperature dependence of protein stability. Proc Natl Acad Sci USA 94:10636-10640.
46. Oobatake M, Ooi T (1993) Hydration and heat stability effects on protein unfolding. Prog Biophys Mol Biol 59:237-284.
47. Oldfield CJ, et al. (2005) Comparing and combining predictors of mostly disordered proteins. Biochemistry 44:1989-2000.
48. Rousseau F, Serrano L, Schymkowitz JW (2006) How evolutionary pressure against protein aggregation shaped chaperone specificity. J Mol Biol 355:1037-1047.
49. Tsolis AC, Papandreou NC, Iconomidou VA, Hamodrakas SJ (2013) A consensus method for the prediction of 'aggregation-prone' peptides in globular proteins. PLoS One 8:e54175.
50. Blaby IK, et al. (2012) Experimental evolution of a facultative thermophile from a mesophilic ancestor. Appl Environ Microbiol 78:144-155.
51. Cooper VS, Bennett AF, Lenski RE (2001) Evolution of thermal dependence of growth rate of Escherichia coli populations during 20,000 generations in a constant environment. Evolution 55:889-896.
52. Bershtein S, Mu W, Shakhnovich EI (2012) Soluble oligomerization provides a beneficial fitness effect on destabilizing mutations. Proc Natl Acad Sci USA 109:4857-4862.
53. Galperin MY, Makarova KS, Wolf YI, Koonin EV (2014) Expanded microbial genome coverage and improved protein family annotation in the cog database. Nucleic Acids Res 43:D261-D269.
54. Bar-Even A, et al. (2011) The moderately efficient enzyme: Evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50:4402-4410.
55. Davidi D, et al. (2016) Global characterization of in vivo enzyme catalytic rates and their correspondence to in vitro kcat measurements. Proc Natl Acad Sci USA 113: 3401-3406.
56. Ebrahim A, et al. (2016) Multi-omic data integration enables discovery of hidden biological regularities. Nat Commun 7:13091.
57. Leuenberger P, et al. (2017) Cell-wide analysis of protein thermal unfolding reveals determinants of thermostability. Science 355:eaai7825.
58. Ouyang Z, Liang J (2008) Predicting protein folding rates from geometric contact and amino acid sequence. Protein Sci 17:1256-1263.
59. LaCroix RA, et al. (2014) Discovery of key mutations enabling rapid growth of Escherichia coli K-12 MG1655 on glucose minimal media using adaptive laboratory evolution. Appl Environ Microbiol 83:02246-14.
60. Bremer H, Dennis P (1996) Modulation of Chemical Composition and Other Parameters of the Cell at Different Exponential Growth Rates in Escherichia Coli and Salmonella, ed Neidhardt FC (ASM, Washington, DC).
61. Forchhammer J, Lindahl L (1971) Growth rate of polypeptide chains as a function of the cell growth rate in a mutant of Escherichia coli 15. J Mol Biol 55:563-568.