Systems-Level Response to Point Mutations in a Core Metabolic Enzyme Modulates Genotype-Phenotype Relationship

Cell Reports

Volumn 11, Issue 4, 2015, Pages 645-656

  Bershtein, Shimon ^a,b   Choi, Jeong Mo ^a   Bhattacharyya, Sanchari ^a   Budnik, Bogdan ^c   Shakhnovich, Eugene ^a  

^a HARVARD UNIVERSITY   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROFOLATE REDUCTASE; ESCHERICHIA COLI PROTEIN; PROTEOME; TRANSCRIPTOME;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; ESCHERICHIA COLI; FOLA GENE; GENOTYPE PHENOTYPE CORRELATION; GROWTH RATE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; UPREGULATION; ENZYMOLOGY; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE; REPRODUCTIVE FITNESS;

BACTERIA (MICROORGANISMS);

ESCHERICHIA COLI; GENETIC FITNESS; GENOTYPE; PHENOTYPE; POINT MUTATION; PROTEOME; TETRAHYDROFOLATE DEHYDROGENASE;

EID: 84928581611     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.051     Document Type: Article

References (47)

1. Altelaar A.F., Frese C.K., Preisinger C., Hennrich M.L., Schram A.W., Timmers H.T., Heck A.J., Mohammed S. Benchmarking stable isotope labeling based quantitative proteomics. J.Proteomics 2013, 88:14-26.
2. Applebee M.K., Joyce A.R., Conrad T.M., Pettigrew D.W., Palsson B.O. Functional and metabolic effects of adaptive glycerol kinase (GLPK) mutants in Escherichia coli. J.Biol. Chem. 2011, 286:23150-23159.
3. Bernstein J.A., Lin P.H., Cohen S.N., Lin-Chao S. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl. Acad. Sci. USA 2004, 101:2758-2763.
4. Bershtein S., Segal M., Bekerman R., Tokuriki N., Tawfik D.S. Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 2006, 444:929-932.
5. Bershtein S., Mu W., Shakhnovich E.I. Soluble oligomerization provides a beneficial fitness effect on destabilizing mutations. Proc. Natl. Acad. Sci. USA 2012, 109:4857-4862.
6. Bershtein S., Mu W., Serohijos A.W., Zhou J., Shakhnovich E.I. Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness. Mol. Cell 2013, 49:133-144.
7. Bollenbach T., Quan S., Chait R., Kishony R. Nonoptimal microbial response to antibiotics underlies suppressive drug interactions. Cell 2009, 139:707-718.
8. Bornholdt S., Sneppen K. Robustness as an evolutionary principle. Proc. Biol. Sci. 2000, 267:2281-2286.
9. Brauer M.J., Huttenhower C., Airoldi E.M., Rosenstein R., Matese J.C., Gresham D., Boer V.M., Troyanskaya O.G., Botstein D. Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol. Biol. Cell 2008, 19:352-367.
10. de Godoy L.M., Olsen J.V., Cox J., Nielsen M.L., Hubner N.C., Fröhlich F., Walther T.C., Mann M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455:1251-1254.
11. Dean A.M., Dykhuizen D.E., Hartl D.L. Fitness as a function of beta-galactosidase activity in Escherichia coli. Genet. Res. 1986, 48:1-8.
12. Dobson C.M. Protein folding and disease: a view from the first Horizon Symposium. Nat. Rev. Drug Discov. 2003, 2:154-160.
13. Drummond D.A., Wilke C.O. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 2008, 134:341-352.
14. Ehrenberg M., Bremer H., Dennis P.P. Medium-dependent control of the bacterial growth rate. Biochimie 2013, 95:643-658.
15. Elowitz M.B., Levine A.J., Siggia E.D., Swain P.S. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
16. Firnberg E., Labonte J.W., Gray J.J., Ostermeier M. A comprehensive, high-resolution map of a gene's fitness landscape. Mol. Biol. Evol. 2014, 31:1581-1592.
17. Geiler-Samerotte K.A., Dion M.F., Budnik B.A., Wang S.M., Hartl D.L., Drummond D.A. Misfolded proteins impose a dosage-dependent fitness cost and trigger a cytosolic unfolded protein response in yeast. Proc. Natl. Acad. Sci. USA 2011, 108:680-685.
18. Geiler-Samerotte K.A., Hashimoto T., Dion M.F., Budnik B.A., Airoldi E.M., Drummond D.A. Quantifying condition-dependent intracellular protein levels enables high-precision fitness estimates. PLoS ONE 2013, 8:e75320.
19. Käll L., Canterbury J.D., Weston J., Noble W.S., MacCoss M.J. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 2007, 4:923-925.
20. Klumpp S., Zhang Z., Hwa T. Growth rate-dependent global effects on gene expression in bacteria. Cell 2009, 139:1366-1375.
21. Kwon Y.K., Lu W., Melamud E., Khanam N., Bognar A., Rabinowitz J.D. A domino effect in antifolate drug action in Escherichia coli. Nat. Chem. Biol. 2008, 4:602-608.
22. Kwon Y.K., Higgins M.B., Rabinowitz J.D. Antifolate-induced depletion of intracellular glycine and purines inhibits thymineless death in E. coli. ACS Chem. Biol. 2010, 5:787-795.
23. Lee M.V., Topper S.E., Hubler S.L., Hose J., Wenger C.D., Coon J.J., Gasch A.P. A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Mol. Syst. Biol. 2011, 7:514.
24. Lehner B. Genotype to phenotype: lessons from model organisms for human genetics. Nat. Rev. Genet. 2013, 14:168-178.
25. Lynch M. Evolutionary diversification of the multimeric states of proteins. Proc. Natl. Acad. Sci. USA 2013, 110:E2821-E2828.
26. Ma J., Ward C.C., Jungreis I., Slavoff S.A., Schwaid A.G., Neveu J., Budnik B.A., Kellis M., Saghatelian A. Discovery of human sORF-encoded polypeptides (SEPs) in cell lines and tissue. J.Proteome Res. 2014, 13:1757-1765.
27. Maier T., Schmidt A., Güell M., Kühner S., Gavin A.C., Aebersold R., Serrano L. Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol. Syst. Biol. 2011, 7:511.
28. McClure R., Balasubramanian D., Sun Y., Bobrovskyy M., Sumby P., Genco C.A., Vanderpool C.K., Tjaden B. Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res. 2013, 41:e140.
29. Mika F., Hengge R. A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. Genes Dev. 2005, 19:2770-2781.
30. Sangurdekar D.P., Zhang Z., Khodursky A.B. The association of DNA damage response and nucleotide level modulation with the antibacterial mechanism of the anti-folate drug trimethoprim. BMC Genomics 2011, 12:583.
31. Schnell J.R., Dyson H.J., Wright P.E. Structure, dynamics, and catalytic function of dihydrofolate reductase. Annu. Rev. Biophys. Biomol. Struct. 2004, 33:119-140.
32. Singer S., Ferone R., Walton L., Elwell L. Isolation of a dihydrofolate reductase-deficient mutant of Escherichia coli. J.Bacteriol. 1985, 164:470-472.
33. Slavov N., Botstein D. Coupling among growth rate response, metabolic cycle, and cell division cycle in yeast. Mol. Biol. Cell 2011, 22:1997-2009.
34. Slavov N., Budnik B.A., Schwab D., Airoldi E.M., van Oudenaarden A. Constant growth rate can be supported by decreasing energy flux and increasing aerobic glycolysis. Cell Rep. 2014, 7:705-714.
35. Soskine M., Tawfik D.S. Mutational effects and the evolution of new protein functions. Nat. Rev. Genet. 2010, 11:572-582.
36. Taniguchi Y., Choi P.J., Li G.W., Chen H., Babu M., Hearn J., Emili A., Xie X.S. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 2010, 329:533-538.
37. Thompson A., Schäfer J., Kuhn K., Kienle S., Schwarz J., Schmidt G., Neumann T., Johnstone R., Mohammed A.K., Hamon C. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 2003, 75:1895-1904.
38. Toprak E., Veres A., Michel J.B., Chait R., Hartl D.L., Kishony R. Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat. Genet. 2012, 44:101-105.
39. Vogel C., Marcotte E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 2012, 13:227-232.
40. Wagner A., Wright J. Alternative routes and mutational robustness in complex regulatory networks. Biosystems 2007, 88:163-172.
41. Ward J.H. Hierarchical Grouping to Optimize an Objective Function. J.Am. Stat. Assoc. 1963, 58:236-244.
42. Wühr M., Haas W., McAlister G.C., Peshkin L., Rad R., Kirschner M.W., Gygi S.P. Accurate multiplexed proteomics at the MS2 level using the complement reporter ion cluster. Anal. Chem. 2012, 84:9214-9221.
43. Wylie C.S., Shakhnovich E.I. A biophysical protein folding model accounts for most mutational fitness effects in viruses. Proc. Natl. Acad. Sci. USA 2011, 108:9916-9921.
44. Zaslaver A., Bren A., Ronen M., Itzkovitz S., Kikoin I., Shavit S., Liebermeister W., Surette M.G., Alon U. A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat. Methods 2006, 3:623-628.
45. Zhang J., Maslov S., Shakhnovich E.I. Constraints imposed by non-functional protein-protein interactions on gene expression and proteome size. Mol. Syst. Biol. 2008, 4:210.
46. Zhou L., Zhang A.B., Wang R., Marcotte E.M., Vogel C. The proteomic response to mutants of the Escherichia coli RNA degradosome. Mol. Biosyst. 2013, 9:750-757.
47. Zwietering M.H., Jongenburger I., Rombouts F.M., van 't Riet K. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 1990, 56:1875-1881.