Merging molecular mechanism and evolution: Theory and computation at the interface of biophysics and evolutionary population genetics

Current Opinion in Structural Biology

Volumn 26, Issue 1, 2014, Pages 84-91

  Serohijos, Adrian WR ^a   Shakhnovich, Eugene I ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICS; EPISTASIS; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; POPULATION DYNAMICS; POPULATION GENETICS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STABILITY; REPRODUCTIVE FITNESS; REVIEW; THEORETICAL STUDY; ANIMAL; BIOLOGICAL MODEL; PROCEDURES;

ANIMALS; BIOPHYSICS; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; GENETICS, POPULATION; HUMANS; MODELS, BIOLOGICAL; PROTEIN FOLDING;

EID: 84902507257     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2014.05.005     Document Type: Review

References (85)

1. Gerrish P.J., Lenski R.E. The fate of competing beneficial mutations in an asexual population. Genetica 1998, 102-3:127-144.
2. Desai M.M., Fisher D.S. Beneficial mutation selection balance and the effect of linkage on positive selection. Genetics 2007, 176:1759-1798.
3. Todd M.J., Walke S., Lorimer G., Truscott K., Scopes R.K. The single-ring Thermoanaerobacter brockii chaperonin 60 (Tbr-EL7) dimerizes to Tbr-EL14.Tbr-ES7 under protein folding conditions. Biochemistry 1995, 34:14932-14941.
4. McDonald J.H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991, 351:652-654.
5. Smith N.G., Eyre-Walker A. Adaptive protein evolution in Drosophila. Nature 2002, 415:1022-1024.
6. Silander O.K., Tenaillon O., Chao L. Understanding the evolutionary fate of finite populations: the dynamics of mutational effects. PLoS Biol 2007, 5:e94.
7. Privalov P.L. Stability of proteins: small globular proteins. Adv Protein Chem 1979, 33:167-241.
8. Shakhnovich E.I., Finkelstein A.V. Theory of cooperative transitions in protein molecules I. Why denaturation of globular protein is a first-order phase transition. Biopolymers 1989, 28:1667-1680.
9. Zeldovich K.B., Chen P., Shakhnovich E.I. Protein stability imposes limits on organism complexity and speed of molecular evolution. Proc Natl Acad Sci U S A 2007, 104:16152-16157.
10. 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.
11. Wylie C.S., Shakhnovich E.I. A biophysical protein folding model accounts for most mutational fitness effects in viruses. Proc Natl Acad Sci U S A 2011, 108:9916-9921.
12. Goldstein R.A. The evolution and evolutionary consequences of marginal thermostability in proteins. Proteins 2011, 79:1396-1407.
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. Lobkovsky A.E., Wolf Y.I., Koonin E.V. Universal distribution of protein evolution rates as a consequence of protein folding physics. Proc Natl Acad Sci U S A 2010, 107:2983-2988.
15. Serohijos A.W., Rimas Z., Shakhnovich E.I. Protein biophysics explains why highly abundant proteins evolve slowly. Cell Rep 2012, 2:249-256.
16. Serohijos A.W., Shakhnovich E.I. Contribution of selection for protein folding stability in shaping the patterns of polymorphisms in coding regions. Mol Biol Evol 2014, 31:165-176.
17. Hartl D.L., Clark A.G. Principles of population genetics 2007, Sunderland, MA, Sinauer. 4th ed.
18. Privalov P.L., Khechinashvili N.N. A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study. J Mol Biol 1974, 86:665-684.
19. Taverna D.M., Goldstein R.A. Why are proteins marginally stable?. Proteins 2002, 46:105-109.
20. Bloom J.D., Raval A., Wilke C.O. Thermodynamics of neutral protein evolution. Genetics 2007, 175:255-266.
21. Kuhlman B., Dantas G., Ireton G.C., Varani G., Stoddard B.L., Baker D. Design of a novel globular protein fold with atomic-level accuracy. Science 2003, 302:1364-1368.
22. DePristo M.A., Weinreich D.M., Hartl D.L. Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet 2005, 6:678-687.
23. Hingorani K., Gierasch L.M. Comparing protein folding in vitro and in vivo: foldability meets the fitness challenge. Curr Opin Struct Biol 2014, 24:81-90.
24. Chen P., Shakhnovich E.I. Lethal mutagenesis in viruses and bacteria. Genetics 2009, 183:639-650.
25. Goldstein R.A. Population size dependence of fitness effect distribution and substitution rate probed by biophysical model of protein thermostability. Genome Biol Evol 2013, 5:1584-1593.
26. Serohijos A.W., Rimas Z., Shakhnovich E.I. Protein biophysics explains why highly abundant proteins evolve slowly. Cell Rep 2012, 2:249-256.
27. Kumar M.D., Bava K.A., Gromiha M.M., Prabakaran P., Kitajima K., Uedaira H., Sarai A. ProTherm and ProNIT: thermodynamic databases for proteins and protein-nucleic acid interactions. Nucleic Acids Res 2006, 34:D204-D206.
28. Tokuriki N., Stricher F., Schymkowitz J., Serrano L., Tawfik D.S. The stability effects of protein mutations appear to be universally distributed. J Mol Biol 2007, 369:1318-1332.
29. Renzette N., Caffrey D.R., Zeldovich K.B., Liu P., Gallagher G.R., Aiello D., Porter A.J., Kurt-Jones E.A., Bolon D.N., Poh Y.P., et al. Evolution of the influenza A virus genome during development of oseltamivir resistance in vitro. J Virol 2014, 88:272-281.
30. Sanjuan R., Moya A., Elena S,F. The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci U S A 2004, 101:8396-8401.
31. Eyre-Walker A., Keightley P.D. The distribution of fitness effects of new mutations. Nat Rev Genet 2007, 8:610-618.
32. Kryukov G.V., Shpunt A., Stamatoyannopoulos J.A., Sunyaev S.R. Power of deep, all-exon resequencing for discovery of human trait genes. Proc Natl Acad Sci U S A 2009, 106:3871-3876.
33. Sawyer S.A., Parsch J., Zhang Z., Hartl D.L. Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila. Proc Natl Acad Sci U S A 2007, 104:6504-6510.
34. Bustamante C.D., Fledel-Alon A., Williamson S., Nielsen R., Hubisz M.T., Glanowski S., Tanenbaum D.M., White T.J., Sninsky J.J., Hernandez R.D., et al. Natural selection on protein-coding genes in the human genome. Nature 2005, 437:1153-1157.
35. Eyre-Walker A., Woolfit M., Phelps T. The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 2006, 173:891-900.
36. Rospert S., Glick B.S., Jeno P., Schatz G., Todd M.J., Lorimer G.H., Viitanen P.V. Identification and functional analysis of chaperonin 10, the groES homolog from yeast mitochondria. Proc Natl Acad Sci U S A 1993, 90:10967-10971.
37. Loewe L., Charlesworth B., Bartolome C., Noel V. Estimating selection on nonsynonymous mutations. Genetics 2006, 172:1079-1092.
38. Ohta T. Slightly deleterious mutant substitutions in evolution. Nature 1973, 246:96-98.
39. Crow J.F., Kimura M. An Introduction to Population Genetics Theory 1970, Harper & Row, New York.
40. Serohijos A.W., Lee S.Y., Shakhnovich E.I. Highly abundant proteins favor more stable 3D structures in yeast. Biophys J 2013, 104:L1-L3.
41. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
42. Ishihama Y., Schmidt T., Rappsilber J., Mann M., Hartl F.U., Kerner M.J., Frishman D. Protein abundance profiling of the Escherichia coli cytosol. BMC Genomics 2008, 9:102.
43. Lynch M. The Origins of Genome Architecture 2007, Sinauer Associates, Sunderland, MA.
44. Cherry J.L. Highly expressed and slowly evolving proteins share compositional properties with thermophilic proteins. Mol Biol Evol 2010, 27:735-741.
45. Wylie C.S., Shakhnovich E.I. Mutation induced extinction in finite populations: lethal mutagenesis and lethal isolation. PLoS Comput Biol 2012, 8:e1002609.
46. Lynch M., Conery J.S. The origins of genome complexity. Science 2003, 302:1401-1404.
47. Tokuriki N., Oldfield C.J., Uversky V.N., Berezovsky I.N., Tawfik D.S. Do viral proteins possess unique biophysical features?. Trends Biochem Sci 2009, 34:53-59.
48. Mendez R., Fritsche M., Porto M., Bastolla U. Mutation bias favors protein folding stability in the evolution of small populations. PLoS Comput Biol 2010, 6:e1000767.
49. Dasmeh P., Serohijos A.W., Kepp K.P., Shakhnovich E.I. Positively selected sites in cetacean myoglobins contribute to protein stability. PLoS Comput Biol 2013, 9:e1002929.
50. Studer R.A., Christin P.A., Williams M.A., Orengo C.A. Stability-activity tradeoffs constrain the adaptive evolution of RubisCO. Proc Natl Acad Sci U S A 2014, 10. 1073/pnas.1310811111.
51. Goloubinoff P., Gatenby A.A., Lorimer G.H. GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature 1989, 337:44-47.
52. Chothia C. Proteins. One thousand families for the molecular biologist. Nature 1992, 357:543-544.
53. Koonin E.V., Wolf Y.I., Karev G.P. The structure of the protein universe and genome evolution. Nature 2002, 420:218-223.
54. Huynen M.A., van Nimwegen E. The frequency distribution of gene family sizes in complete genomes. Mol Biol Evol 1998, 15:583-589.
55. Qian J., Luscombe N.M., Gerstein M. Protein family and fold occurrence in genomes: power-law behaviour and evolutionary model. J Mol Biol 2001, 313:673-681.
56. Li H., Helling R., Tang C., Wingreen N. Emergence of preferred structures in a simple model of protein folding. Science 1996, 273:666-669.
57. England J.L., Shakhnovich E.I. Structural determinant of protein designability. Phys Rev Lett 2003, 90:218101.
58. Shakhnovich B.E., Deeds E., Delisi C., Shakhnovich E. Protein structure and evolutionary history determine sequence space topology. Genome Res 2005, 15:385-392.
59. Dixit P.D., Maslov S. Evolutionary capacitance and control of protein stability in protein-protein interaction networks. PLoS Comput Biol 2013, 9:e1003023.
60. Heo M., Maslov S., Shakhnovich E. Topology of protein interaction network shapes protein abundances and strengths of their functional and nonspecific interactions. Proc Natl Acad Sci U S A 2011, 108:4258-4263.
61. Debes C., Wang M., Caetano-Anolles G., Grater F. Evolutionary optimization of protein folding. PLoS Comput Biol 2013, 9:e1002861.
62. Dokholyan N.V., Shakhnovich B., Shakhnovich E.I. Expanding protein universe and its origin from the biological Big Bang. Proc Natl Acad Sci U S A 2002, 99:14132-14136.
63. Peterson G.J., Presse S., Peterson K.S., Dill K.A. Simulated evolution of protein-protein interaction networks with realistic topology. PLoS One 2012, 7:e39052.
64. Fernandez A., Lynch M. Non-adaptive origins of interactome complexity. Nature 2011, 474:502-505.
65. Zeldovich K.B., Shakhnovich E.I. Understanding protein evolution: from protein physics to Darwinian selection. Annu Rev Phys Chem 2008, 59:105-127.
66. Deeds E.J., Shakhnovich E.I. A structure-centric view of protein evolution, design, and adaptation. Advances in Enzymology and Related Areas of Molecular Biology Protein Evolution 2007, Vol. 75:133-191. Wiley.
67. Wilke C.O. Bringing molecules back into molecular evolution. PLoS Comput Biol 2012, 8:e1002572.
68. Zeldovich K.B., Chen P., Shakhnovich B.E., Shakhnovich E.I. A first-principles model of early evolution: emergence of gene families, species, and preferred protein folds. PLoS Comput Biol 2007, 3:e139.
69. Cuypers T.D., Hogeweg P. Virtual genomes in flux: an interplay of neutrality and adaptability explains genome expansion and streamlining. Genome Biol Evol 2012, 4:212-229.
70. van Nimwegen E. Scaling laws in the functional content of genomes. Trends Genet 2003, 19:479-484.
71. Maslov S., Krishna S., Pang T.Y., Sneppen K. Toolbox model of evolution of prokaryotic metabolic networks and their regulation. Proc Natl Acad Sci U S A 2009, 106:9743-9748.
72. Karr J.R., Sanghvi J.C., Macklin D.N., Gutschow M.V., Jacobs J.M., Bolival B., Assad-Garcia N., Glass J.I., Covert M.W. A whole-cell computational model predicts phenotype from genotype. Cell 2012, 150:389-401.
73. McFarland C.D., Korolev K.S., Kryukov G.V., Sunyaev S.R., Mirny L.A. Impact of deleterious passenger mutations on cancer progression. Proc Natl Acad Sci U S A 2013, 110:2910-2915.
74. Bershtein S., Mu W., Shakhnovich E.I. Soluble oligomerization provides a beneficial fitness effect on destabilizing mutations. Proc Natl Acad Sci U S A 2012, 109:4857-4862.
75. Jiang L., Mishra P., Hietpas R.T., Zeldovich K.B., Bolon D.N. Latent effects of Hsp90 mutants revealed at reduced expression levels. PLoS Genet 2013, 9:e600-e1003.
76. Roscoe B.P., Thayer K.M., Zeldovich K.B., Fushman D., Bolon D.N. Analyses of the effects of all ubiquitin point mutants on yeast growth rate. J Mol Biol 2013, 425:1363-1377.
77. Hietpas R.T., Bank C., Jensen J.D., Bolon D.N. Shifting fitness landscapes in response to altered environments. Evolution 2013, 67:3512-3522.
78. Adkar B.V., Tripathi A., Sahoo A., Bajaj K., Goswami D., Chakrabarti P., Swarnkar M.K., Gokhale R.S., Varadarajan R. Protein model discrimination using mutational sensitivity derived from deep sequencing. Structure 2012, 20:371-381.
79. Soskine M., Tawfik D.S. Mutational effects and the evolution of new protein functions. Nat Rev Genet 2010, 11:572-582.
80. Tokuriki N., Tawfik D.S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 2009, 459:668-673.
81. Queitsch C., Sangster T.A., Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002, 417:618-624.
82. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
83. Pollock D.D., Thiltgen G., Goldstein R.A. Amino acid coevolution induces an evolutionary Stokes shift. Proc Natl Acad Sci U S A 2012, 109:E1352-E1359.
84. Ashenberg O., Gong L.I., Bloom J.D. Mutational effects on stability are largely conserved during protein evolution. Proc Natl Acad Sci U S A 2013, 110:21071-21076.
85. Gong L.I., Suchard M.A., Bloom J.D. Stability-mediated epistasis constrains the evolution of an influenza protein. Elife 2013, 2:e00631.