Reconstructing Ancient Proteins to Understand the Causes of Structure and Function

Annual Review of Biophysics

Volumn 46, Issue , 2017, Pages 247-269

  Hochberg, Georg K A ^a   Thornton, Joseph W ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Ancestral reconstruction; Epistasis; Evolutionary biochemistry; Historical contingency; Vertical analysis

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DIMER; PROTEIN; SERINE PROTEINASE; TETRAMER; TRANSCRIPTION FACTOR; OXIDOREDUCTASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; CHROMATOPHORE; COMPARATIVE STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; EPISTASIS; FLUORESCENCE; GENE DUPLICATION; GENE SEQUENCE; GENE SYNTHESIS; HUMAN; HYDROGEN BOND; INDEL MUTATION; LAST COMMON ANCESTOR; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; PURIFYING SELECTION; REVIEW; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY; ANIMAL; ANTHOZOA; APICOMPLEXA; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MUTATION; PROTEIN MULTIMERIZATION;

ANIMALS; ANTHOZOA; APICOMPLEXA; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; MUTATION; OXIDOREDUCTASES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEINS; PROTOZOAN PROTEINS; SUBSTRATE SPECIFICITY; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 85019699606     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-070816-033631     Document Type: Review

References (83)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21:2104-5
2. Agafonov RV, Wilson C, Otten R, Buosi V, Kern D. 2014. Energetic dissection of Gleevec's selectivity toward human tyrosine kinases. Nat. Struct. Mol. Biol. 21:848-53
3. Aharoni A, Gaidukov L, Khersonsky O, McQ Gould S, Roodveldt C, Tawfik DS. 2005. The 'evolvability' of promiscuous protein functions. Nat. Genet. 37:73-76
4. Ahnert SE, Marsh JA, Hernández H, Robinson CV, Teichmann SA. 2015. Principles of assembly reveal a periodic table of protein complexes. Science 350:aaa2245
5. Anderson DP, Whitney DS, Hanson-Smith V, Woznica A, Campodonico-Burnett W, et al. 2016. Evolution of an ancient protein function involved in organized multicellularity in animals. eLife 5:e10147
6. Anderson DW, McKeown AN, Thornton JW. 2015. Intermolecular epistasis shaped the function and evolution of an ancient transcription factor and its DNA binding sites. eLife 4:e07864
7. Baker CR, Hanson-Smith V, Johnson AD. 2013. Following gene duplication, paralog interference constrains transcriptional circuit evolution. Science 342:104-8
8. Baldwin AJ, Kay LE. 2009. NMR spectroscopy brings invisible protein states into focus. Nat. Chem. Biol. 5:8-14
9. Bloom JD, Gong LI, BaltimoreD. 2010. Permissive secondarymutations enable the evolution of influenza oseltamivir resistance. Science 328:1272-75
10. Bloom JD, Romero PA, Lu Z, Arnold FH. 2007. Neutral genetic drift can alter promiscuous protein functions, potentially aiding functional evolution. Biol. Direct 2:17
11. Boucher JI, Jacobowitz JR, Beckett BC, Classen S, Theobald DL. 2014. An atomic-resolution view of neofunctionalization in the evolution of apicomplexan lactate dehydrogenases. eLife 3:e02304
12. Bridgham JT, Carroll SM, Thornton JW. 2006. Evolution of hormone-receptor complexity bymolecular exploitation. Science 312:97-101
13. Bridgham JT, Ortlund EA, Thornton JW. 2009. An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461:515-19
14. Brown CJ, Johnson AK, DaughdrilGW.2010. Comparingmodels of evolution for ordered and disordered proteins. Mol. Biol. Evol. 27:609-21
15. Brown CJ, Takayama S, Campen AM, Vise P, Marshall TW, et al. 2002. Evolutionary rate heterogeneity in proteins with long disordered regions. J. Mol. Evol. 55:104-10
16. Clifton BE, Jackson CJ. 2016. Ancestral protein reconstruction yields insights into adaptive evolution of binding specificity in solute-binding proteins. Cell Chem. Biol. 2:236-45
17. Crick F. 1988. What Mad Pursuit: A Personal View of Scientific Discovery. New York: Basic Books
18. Cunningham BC, Jhurani P, Ng P, Wells JA. 1989. Receptor and antibody epitopes in human growth hormone identified by homolog-scanning mutagenesis. Science 243:1330-36
19. Danielsen M, Hinck L, Ringold GM. 1989. Two amino acids within the knuckle of the first zinc finger specify DNA response element activation by the glucocorticoid receptor. Cell 57:1131-38
20. Dawkins R. 1986. The Blind Watchmaker. New York: Norton
21. Devamani T, Rauwerdink AM, Lunzer M, Jones BJ. 2016. Catalytic promiscuity of ancestral esterases and hydroxynitrile lyases. J. Am. Chem. Soc. 138:1046-56
22. Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, et al. 1998. The structure of the potassium channel: Molecular basis of K+ conduction and selectivity. Science 280:69-77
23. Eick GN, Bridgham JT, Anderson DP, Harms MJ, Thornton JW. 2017. Robustness of reconstructed ancestral protein functions to statistical uncertainty. Mol. Biol. Evol. 34(2):247-61
24. Ekici OD, Paetzel M, Dalbey RE. 2008. Unconventional serine proteases: Variations on the catalytic Ser/His/Asp triad configuration. Protein Sci. 17:2023-37
25. Elleuche S, Fodor K, von der Heyde A, Klippel B, Wilmanns M, Antranikian G. 2014. Group III alcohol dehydrogenase from Pectobacterium atrosepticum: Insights into enzymatic activity and organization of the metal ion-containing region. Appl. Microbiol. Biotechnol. 98:4041-51
26. Felsenstein J. 2004. Inferring Phylogenies. Sunderland, Mass.: Sinauer Assoc.
27. Field SF, Bulina MY, Kelmanson IV, Bielawski JP, Matz MV. 2006. Adaptive evolution of multicolored fluorescent proteins in reef-building corals. J. Mol. Evol. 62:332-39
28. Field SF, Matz MV. 2010. Retracing evolution of red fluorescence in GFP-like proteins from Faviina corals. Mol. Biol. Evol. 27:225-33
29. Finnigan GC, Hanson-Smith V, Stevens TH, Thornton JW. 2012. Evolution of increased complexity in a molecular machine. Nature 481:360-64
30. Gaucher EA, Thomson JM, Burgan MF, Benner SA. 2003. Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature 425:285-88
31. Gerlt JA, Babbitt PC. 2009. Enzyme (re)design: Lessons from natural evolution and computation. Curr. Opin. Chem. Biol. 13:10-18
32. GoldsteinRA. 2011. The evolution and evolutionary consequences of marginal thermostability in proteins. Proteins 79:1396-407
33. Goodsell DS, Olson AJ. 2000. Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29:105-53
34. Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proc. R. Soc. Lond. B 205:581-98
35. Hanson-Smith V, Johnson A. 2016. PhyloBot: A web portal for automated phylogenetics, ancestral sequence reconstruction, exploration of mutational trajectories. PLOS Comput. Biol. 12:e1004976
36. Harms MJ, Eick GN, Goswami D, Colucci JK, Griffin PR, et al. 2013. Biophysical mechanisms for large-effect mutations in the evolution of steroid hormone receptors. PNAS 110:11475-80
37. Harms MJ, Thornton JW. 2013. Evolutionary biochemistry: Revealing the historical and physical causes of protein properties. Nat. Rev. Genet. 14:559-71
38. Harms MJ, Thornton JW. 2014. Historical contingency and its biophysical basis in glucocorticoid receptor evolution. Nature 512:203-7
39. Hart KM, Harms MJ, Schmidt BH, Elya C, Thornton JW, Marqusee S. 2014. Thermodynamic system drift in protein evolution. PLOS Biol. 12:e1001994
40. Hedstrom L, Farr-Jones S, Kettner CA, RutterWJ. 1994. Converting trypsin to chymotrypsin: Groundstate binding does not determine substrate specificity. Biochemistry 33:8764-69
41. Hung S-H, Hedstrom L. 1998. Converting trypsin to elastase: Substitution of the S1 site and adjacent loops reconstitutes esterase specificity but not amidase activity. Protein Eng. 11:669-73
42. Jacob F. 1977. Evolution and tinkering. Science 196:1161-66
43. Jones DT, Taylor WR, Thornton JM. 1994. A mutation data matrix for transmembrane proteins. FEBS Lett. 339:269-75
44. Khersonsky O, TawfikDS. 2010. Enzyme promiscuity: Amechanistic and evolutionary perspective. Annu. Rev. Biochem. 79:471-505
45. Kim H, Grunkemeyer TJ, Modi C, Chen L, Fromme R, et al. 2013. Acid-base catalysis and crystal structures of a least evolved ancestralGFP-like protein undergoing green-to-red photoconversion. Biochemistry 52:8048-59
46. Kim H, Zou T, Modi C, Dörner K, Grunkemeyer TJ, et al. 2015. A hinge migration mechanism unlocks the evolution of green-to-red photoconversion in GFP-like proteins. Structure 23:34-43
47. Kimura M. 1983. The Neutral Theory of Molecular Evolution. New York: Cambridge Univ. Press
48. Kobilka BK, Kobilka TS, Daniel K, Regan JW, Caron MG, Lefkowitz RJ. 1988. Chimeric alpha 2-, beta 2-adrenergic receptors: Delineation of domains involved in effector coupling and ligand binding specificity. Science 240:1310-16
49. Levy ED, Erba EB, Robinson CV, Teichmann SA. 2008. Assembly reflects evolution of protein complexes. Nature 453:1262-65
50. Li Y, Suino K, Daugherty J, Xu HE. 2005. Structural and biochemical mechanisms for the specificity of hormone binding and coactivator assembly by mineralocorticoid receptor. Mol. Cell. 19:367-80
51. Liljas A, Laurberg M. 2000. A wheel invented three times: The molecular structures of the three carbonic anhydrases. EMBO Rep. 1:16-17
52. Lunzer M, Golding GB, Dean AM. 2010. Pervasive cryptic epistasis in molecular evolution. PLOS Genet. 6:e1001162
53. Lynch M. 2012. The evolution of multimeric protein assemblages. Mol. Biol. Evol. 29:1353-66
54. Lynch M. 2013. Evolutionary diversification of the multimeric states of proteins. PNAS 110:E2821-28
55. Marsh JA, Teichmann SA. 2014. Protein flexibility facilitates quaternary structure assembly and evolution. PLOS Biol. 12:e1001870
56. Marsh JA, Teichmann SA. 2015. Structure, dynamics, assembly, evolution of protein complexes. Annu. Rev. Biochem. 84:551-75
57. McKeown AN, Bridgham JT, Anderson DW, Murphy MN, Ortlund EA, Thornton JW. 2014. Evolution of DNA specificity in a transcription factor family produced a new gene regulatory module. Cell 159:58-68
58. Nagar B, Hantschel O, Young MA, Scheffzek K, Veach D, et al. 2003. Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112:859-71
59. Ortlund EA, Bridgham JT, Redinbo MR, Thornton JW. 2007. Crystal structure of an ancient protein: Evolution by conformational epistasis. Science 317:1544-48
60. Pauling L, Zuckerkandl E. 1963. Chemical paleogenetics:Molecular "restoration studies" of extinct forms of life. Acta. Chem. Scand. 17:S9-16
61. Perica T, Chothia C, Teichmann SA. 2012. Evolution of oligomeric state through geometric coupling of protein interfaces. PNAS 109:8127-32
62. Perica T, Kondo Y, Tiwari SP, McLaughlin SH, Kemplen KR, et al. 2014. Evolution of oligomeric state through allosteric pathways that mimic ligand binding. Science 346:1254346
63. Perona JJ, Craik CS. 1997. Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J. Biol. Chem. 272:29987-90
64. Perutz M. 1983. Species adaptation in a protein molecule. Mol. Biol. Evol. 1:1-28
65. Schwabe JWR, Chapman L, Finch JT, Rhodes D. 1993. The crystal structure of the estrogen receptor DNA-binding domain bound to DNA: How receptors discriminate between their response elements. Cell 75:567-78
66. Seeliger MA, Nagar B, Frank F, Cao X, Henderson MN, Kuriyan J. 2007. c-Src binds to the cancer drug imatinib with an inactive Abl/c-Kit conformation and a distributed thermodynamic penalty. Structure 15:299-311
67. Siddiq MA, Loehlin DW, Montooth KL, Thornton JW. 2017. Experimental test and refutation of a classic case of molecular adaptation in Drosophila melanogaster. Nature Ecol. Evol. 1:0025
68. Stackhouse J, Presnell SR, McGeehan GM, Nambiar KP, Benner SA. 1990. The ribonuclease from an extinct bovid ruminant. FEBS Lett. 262:104-6
69. Starr TN, Thornton JW. 2016. Epistasis in protein evolution. Protein Sci. 25:1204-18
70. Thorne JL, Goldman N, Jones DT. 1996. Combining protein evolution and secondary structure. Mol. Biol. Evol. 13:666-73
71. Thornton JW. 2004. Resurrecting ancient genes: Experimental analysis of extinct molecules. Nat. Rev. Genet. 5:366-75
72. Thornton JW, Need E, Crews D. 2003. Resurrecting the ancestral steroid receptor: Ancient origin of estrogen signaling. Science 301:1714-17
73. Tokuriki N, Tawfik DS. 2009. Protein dynamism and evolvability. Science 324:203-7
74. Ugalde JA, Chang BS, Matz MV. 2004. Evolution of coral pigments recreated. Science 305:1433
75. Venekei I, Szilágyi L, Gráf L, RutterWJ. 1996. Attempts to convert chymotrypsin to trypsin. FEBS Lett. 379:143-47
76. Voordeckers K, Brown CA, Vanneste K, van der Zande E, Voet A, et al. 2012. Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication. PLOS Biol. 10:e1001446
77. Wheeler LC, Lim SA, Marqusee S, Harms MJ. 2016. The thermostability and specificity of ancient proteins. Curr. Opin. Struct. Biol. 38:37-43
78. Wilson C, Agafonov RV, Hoemberger M, Kutter S, Zorba A, et al. 2015. Using ancient protein kinases to unravel a modern cancer drug's mechanism. Science 347:882-86
79. Wouters MA, Liu K, Riek P, Husain A. 2003. A despecialization step underlying evolution of a family of serine proteases. Mol. Cell. 12:343-54
80. Yang Z. 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. J. Mol. Evol. 39:306-14
81. Yang Z. 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24:1586-91
82. Yang Z, Kumar S, Nei M. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641-50
83. Zuckerkandl E, Pauling L. 1965. Evolutionary divergence and convergence in proteins. Evol. Gen. Prot. 97:97-166