Viewing protein fitness landscapes through a next-gen lens

Genetics

Volumn 198, Issue 2, 2014, Pages 461-471

  Boucher, Jeffrey I ^a   Cote, Pamela ^a   Flynn, Julia ^a   Jiang, Li ^a   Laban, Aneth ^a   Mishra, Parul ^a   Roscoe, Benjamin P ^a   Bolon, Daniel N A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PROTEIN;

ARTICLE; BINDING AFFINITY; CELL FUNCTION; EVOLUTION; EXPERIMENTATION; GENE LIBRARY; GENE MUTATION; GENETIC DRIFT; GENETIC ENGINEERING; GENETIC SELECTION; GENETIC VARIABILITY; GENOME; HUMAN; MAMMAL CELL; MICROORGANISM; MUTATIONAL ANALYSIS; NONHUMAN; POPULATION GENETICS; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; VIRUS; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; MUTATION; PROTEIN CONFORMATION; PROTEIN STABILITY;

ANIMALS; GENETIC DRIFT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MODELS, GENETIC; MUTATION; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEINS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84908049845     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.168351     Document Type: Article

References (75)

1. Acevedo, A., L. Brodsky, and R. Andino, 2014 Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 505: 686–690.
2. Araya, C. L., D. M. Fowler, W. Chen, I. Muniez, J. W. Kelly et al., 2012 A fundamental protein property, thermodynamic stability, revealed solely from large-scale measurements of protein function. Proc. Natl. Acad. Sci. USA 109: 16858–16863.
3. Baase, W. A., L. Liu, D. E. Tronrud, and B. W. Matthews, 1997 Lessons from the lysozyme of phage T4. Protein Sci. 19: 631–641.
4. Baker, T. A., and R. T. Sauer, 2012 ClpXP, an ATP-powered unfolding and protein-degradation machine. Biochim. Biophys. Acta 1823: 15–28.
5. Bank, C., R. T. Hietpas, A. Wong, D. N. Bolon, and J. D. Jensen, 2014 A bayesian MCMC approach to assess the complete distribution of fitness effects of new mutations: uncovering the potential for adaptive walks in challenging environments. Genetics 196: 841–852.
6. Bentley, D. R., S. Balasubramanian, H. P. Swerdlow, G. P. Smith, J. Milton et al., 2008 Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53–59.
7. Bershtein, S, W. Mu, A. W. Serohijos, J. Zhou, and E. I. Shakhnovich, 2013 Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness. Mol. Cell 49: 133–144.
8. Bloom, J. D., and F. H. Arnold, 2009 In the light of directed evolution: pathways of adaptive protein evolution. Proc. Natl. Acad. Sci. USA 106(Suppl 1): 9995–10000.
9. Bloom, J. D., S. T. Labthavikul, C. R. Otey, and F. H. Arnold, 2006 Protein stability promotes evolvability. Proc. Natl. Acad. Sci. USA 103: 5869–5874.
10. Bowie, J. U., and R. T. Sauer, 1989 Identification of C-terminal extensions that protect proteins from intracellular proteolysis. J. Biol. Chem. 264: 7596–7602.
11. Breen, M. S., C. Kemena, P. K. Vlasov, C. Notredame, and F. A. Kondrashov, 2012 Epistasis as the primary factor in molecular evolution. Nature 490: 535–538.
12. Chien, C. T., P. L. Bartel, R. Sternglanz, and S. Fields, 1991 The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA 88: 9578–9582.
13. Cordes, M. H., A. R. Davidson, and R. T. Sauer, 1996 Sequence space, folding and protein design. Curr. Opin. Struct. Biol. 6: 3–10.
14. Cowen, L. E., and S. Lindquist, 2005 Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309: 2185–2189.
15. Cunningham, B. C., and J. A. Wells, 1989 High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244: 1081–1085.
16. Dill, K. A., 1990 Dominant forces in protein folding. Biochemistry 29: 7133–7155.
17. Domingo-Calap, P., J. M. Cuevas, and R. Sanjuan, 2009 The fitness effects of random mutations in single-stranded DNA and RNA bacteriophages. PLoS Genet. 5: e1000742.
18. Eid, J., A. Fehr, J. Gray, K. Luong, J. Lyle et al., 2009 Real-time DNA sequencing from single polymerase molecules. Science 323: 133–138.
19. Eisenmesser, E. Z., D. A. Bosco, M. Akke, and D. Kern, 2002 Enzyme dynamics during catalysis. Science 295: 1520–1523.
20. Fleishman, S. J., T. A. Whitehead, D. C. Ekiert, C. Dreyfus, J. E. Corn et al., 2011 Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332: 816–821.
21. Fowler, D. M., C. L. Araya, S. J. Fleishman, E. H. Kellogg, J. J. Stephany et al., 2010 High-resolution mapping of protein sequence-function relationships. Nat. Methods 7: 741–746.
22. Gong, L. I., and J. D. Bloom, 2014 Epistatically interacting substitutions are enriched during adaptive protein evolution. PLoS Genet. 10: e1004328.
23. Gong, L. I., M. A. Suchard, and J. D. Bloom, 2013 Stability-mediated epistasis constrains the evolution of an influenza protein. eLife 2: e00631.
24. Gore, J., H. Youk, and A. van Oudenaarden, 2009 Snowdrift game dynamics and facultative cheating in yeast. Nature 459: 253–256.
25. Harms, M. J., and J. W. Thornton, 2013 Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nat. Rev. Genet. 14: 559–571.
26. Hiatt, J. B., R. P. Patwardhan, E. H. Turner, C. Lee, and J. Shendure, 2010 Parallel, tag-directed assembly of locally derived short sequence reads. Nat. Methods 7: 119–122.
27. Hietpas, R., B. Roscoe, L. Jiang, and D. N. Bolon, 2013a Fitness analyses of all possible point mutations for regions of genes in yeast. Nat. Protoc. 7: 1382–1396.
28. Hietpas, R. T., J. D. Jensen, and D. N. Bolon, 2011 Experimental illumination of a fitness landscape. Proc. Natl. Acad. Sci. USA 108: 7896–7901.
29. Hietpas, R. T., C. Bank, J. D. Jensen, and D. N. Bolon, 2013b Shifting fitness landscapes in response to altered environments. Evolution 67: 3512–3522.
30. Hsu, H. J., K. H. Lee, J. W. Jian, H. J. Chang, C. M. Yu et al., 2014 Antibody variable domain interface and framework sequence requirements for stability and function by high-throughput experiments. Structure 22: 22–34.
31. Ingolia, N. T., S. Ghaemmaghami, J. R. Newman, and J. S. Weissman, 2009 Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218–223.
32. Jarosz, D. F., M. Taipale, and S. Lindquist, 2010 Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu. Rev. Genet. 44: 189–216.
33. Jiang, L., P. Mishra, R. T. Hietpas, K. B. Zeldovich, and D. N. Bolon, 2013 Latent effects of Hsp90 mutants revealed at reduced expression levels. PLoS Genet. 9: e1003600.
34. Kacser, H., and J. A. Burns, 1981 The molecular basis of dominance. Genetics 97: 639–666.
35. King, J. L., and T. H. Jukes, 1969 Non-Darwinian evolution. Science 164: 788–798.
36. Lee, S. Y., L. Pullen, D. J. Virgil, C. A. Castaneda, D. Abeykoon et al., 2014 Alanine scan of core positions in ubiquitin reveals links between dynamics, stability, and function. J. Mol. Biol. 426: 1377–1389.
37. Lunzer, M., S. P. Miller, R. Felsheim, and A. M. Dean, 2005 The biochemical architecture of an ancient adaptive landscape. Science 310: 499–501.
38. Lynch, M., 2010 Evolution of the mutation rate. Trends Genet. 26: 345–352.
39. Lynch, M., and J. S. Conery, 2003 The origins of genome complexity. Science 302: 1401–1404.
40. Lynch, M., L. M. Bobay, F. Catania, J. F. Gout, and M. Rho, 2011 The repatterning of eukaryotic genomes by random genetic drift. Annu. Rev. Genomics Hum. Genet. 12: 347–366.
41. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader et al., 2005 Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376–380.
42. McLaughlin, Jr., R. N., F. J. Poelwijk, A. Raman, W. S. Gosal, and R. Ranganathan, 2012 The spatial architecture of protein function and adaptation. Nature 491: 138–142.
43. Melamed, D., D. L. Young, C. E. Gamble, C. R. Miller, and S. Fields, 2013 Deep mutational scanning of an RRM domain of the Saccharomyces cerevisiae poly(A)-binding protein. RNA 19: 1537–1551.
44. Nagalakshmi, U., Z. Wang, K. Waern, C. Shou, D. Raha et al., 2008 The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344–1349.
45. Ohta, T., 1973 Slightly deleterious mutant substitutions in evolution. Nature 246: 96–98.
46. Oliphant, A. R., and K. Struhl, 1989 An efficient method for generating proteins with altered enzymatic properties: application to beta-lactamase. Proc. Natl. Acad. Sci. USA 86: 9094–9098.
47. Ortlund, E. A., J. T. Bridgham, M. R. Redinbo, and J. W. Thornton, 2007 Crystal structure of an ancient protein: evolution by conformational epistasis. Science 317: 1544–1548.
48. Palzkill, T., and D. Botstein, 1992 Probing beta-lactamase structure and function using random replacement mutagenesis. Proteins 14: 29–44.
49. Peschard, P., G. Kozlov, T. Lin, I. A. Mirza, A. M. Berghuis et al., 2007 Structural basis for ubiquitin-mediated dimerization andactivation of the ubiquitin protein ligase Cbl-b. Mol. Cell 27: 474–485.
50. Phillips, A. H., Y. Zhang, C. N. Cunningham, L. Zhou, W. F. Forrest et al., 2013 Conformational dynamics control ubiquitindeubiquitinase interactions and influence in vivo signaling. Proc. Natl. Acad. Sci. USA 110: 11379–11384.
51. Picard, D., B. Khursheed, M. J. Garabedian, M. G. Fortin, S. Lindquist et al., 1990 Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348: 166–168.
52. Powers, E. T., D. L. Powers, and L. M. Gierasch, 2012 FoldEco: a model for proteostasis in E. coli. Cell Reports 1: 265–276.
53. Rennell, D., S. E. Bouvier, L. W. Hardy, and A. R. Poteete, 1991 Systematic mutation of bacteriophage T4 lysozyme. J. Mol. Biol. 222: 67–88.
54. Roscoe, B. P., and D. N. Bolon, 2014 Systematic exploration of ubiquitin sequence, E1 activation efficiency, and experimental fitness in yeast. J. Mol. Biol. 426: 2854–2870.
55. Roscoe, B. P., K. M. Thayer, K. B. Zeldovich, D. Fushman, and D. N. Bolon, 2014 Analyses of the effects of all ubiquitin point mutants on yeast growth rate. J. Mol. Biol. 425: 1363–1377.
56. Rothberg, J. M., W. Hinz, T. M. Rearick, J. Schultz, W. Mileski et al., 2011 An integrated semiconductor device enabling non-optical genome sequencing. Nature 475: 348–352.
57. Sahni, N., S. Yi, Q. Zhong, N. Jailkhani, B. Charloteaux et al., 2013 Edgotype: a fundamental link between genotype and phenotype. Curr. Opin. Genet. Dev. 23: 649–657.
58. Sanjuan, R., A. Moya, and S. F. Elena, 2004 The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc. Natl. Acad. Sci. USA 101: 8396–8401.
59. Starita, L. M., J. N. Pruneda, R. S. Lo, D. M. Fowler, H. J. Kim et al., 2013 Activity-enhancing mutations in an E3 ubiquitin ligase identified by high-throughput mutagenesis. Proc. Natl. Acad. Sci. USA 110: E1263–E1272.
60. Thornton, J. W., E. Need, and D. Crews, 2003 Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301: 1714–1717.
61. Tokuriki, N., and D. S. Tawfik, 2009a Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459: 668–673.
62. Tokuriki, N., and D. S. Tawfik, 2009b Protein dynamism and evolvability. Science 324: 203–207.
63. Tokuriki, N., and D. S. Tawfik, 2009c Stability effects of mutations and protein evolvability. Curr. Opin. Struct. Biol. 19: 596–604.
64. Tsai, I. J., D. Bensasson, A. Burt, and V. Koufopanou, 2008 Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc. Natl. Acad. Sci. USA 105: 4957–4962.
65. Villali, J., and D. Kern, 2010 Choreographing an enzyme’s dance. Curr. Opin. Chem. Biol. 14: 636–643.
66. Wagenaar, T. R., L. Ma, B. Roscoe, S. M. Park, D. N. Bolon et al., 2014 Resistance to vemurafenib resulting from a novel mutation in the BRAFV600E kinase domain. Pigment Cell Melanoma Res 27: 124–133.
67. Walzthoeni, T., A. Leitner, F. Stengel, and R. Aebersold, 2013 Mass spectrometry supported determination of protein complex structure. Curr. Opin. Struct. Biol. 23: 252–260.
68. Wang, Z., M. Gerstein, and M. Snyder, 2009 RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10: 57–63.
69. Weinreich, D. M., N. F. Delaney, M. A. Depristo, and D. L. Hartl, 2006 Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111–114.
70. Whitehead, T. A., A. Chevalier, Y. Song, C. Dreyfus, S. J. Fleishman et al., 2012 Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing. Nat. Biotechnol. 30: 543–548.
71. Wintrode, P. L., G. I. Makhatadze, and P. L. Privalov, 1994 Thermodynamics of ubiquitin unfolding. Proteins 18: 246–253.
72. Wright, S., 1932 The roles of mutation, inbreeding, crossbreeding and selection in evolution, pp. 356–366 in Proceedings of the Sixth International Congress of Genetics, edited by D. Jones. Ithaca, NY.
73. Wylie, C. S., and E. I. Shakhnovich, 2011 A biophysical protein folding model accounts for most mutational fitness effects in viruses. Proc. Natl. Acad. Sci. USA 108: 9916–9921.
74. Yang, Z., 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Computer applications in the biosciences. CABIOS 13: 555–556.
75. Zuckerkandl, E., 1976 Evolutionary processes and evolutionary noise at the molecular level. I. Functional density in proteins. J. Mol. Evol. 7: 167–183.