An evolutionary perspective on protein moonlighting

Biochemical Society Transactions

Volumn 42, Issue 6, 2014, Pages 1684-1691

  Copley, Shelley D ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Adaptive conflict; Bifunctional protein; Evolution; Gene duplication; Moonlighting

Indexed keywords

MOONLIGHTING PROTEIN; PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; FITNESS; GENE CONTROL; GENE DUPLICATION; GENE EXPRESSION; GENE FREQUENCY; GENE STRUCTURE; GENETIC CODE; GENETIC DRIFT; GENETIC VARIABILITY; HUMAN; OUTCOME ASSESSMENT; POINT MUTATION; PROTEIN FUNCTION; GENETICS; MOLECULAR EVOLUTION; MUTATION; PHYSIOLOGY;

EVOLUTION, MOLECULAR; GENE DUPLICATION; MUTATION; PROTEINS;

EID: 84911930913     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140245     Document Type: Article

References (58)

1. Horowitz, N.H. (1995) One-gene-one-enzyme: remembering biochemical genetics. Protein Sci. 4, 1017-1019 CrossRef PubMed
2. Beadle, G.W. and Tatum, E.L. (1941) Genetic control of biochemical reactions in Neurospora. Proc. Natl. Acad. Sci. U.S.A. 27, 499-506 CrossRef PubMed
3. McGuffee, S.R. and Elcock, A.H. (2010) Diffusion, crowding and protein stability in a dynamic molecular model of the bacterial cytoplasm. PLoS Comput. Biol. 6, e1000694 CrossRef PubMed
4. Shultzaberger, R.K., Maerkl, S.J., Kirsch, J.F. and Eisen, M.B. (2012) Probing the informational and regulatory plasticity of a transcription factor DNA-binding domain. PLoS Genet. 8, e1002614 CrossRef PubMed
5. Sirover, M.A. (2011) On the functional diversity of glyceraldehyde-3-phosphate dehydrogenase: biochemical mechanisms and regulatory control. Biochim. Biophys. Acta 1810, 741-751 CrossRef PubMed
6. Gómez-Arreaza, A., Acosta, H., Quiñones, W., Concepción, J.L., Michels, P.A. and Avilán, L. (2014) Extracellular functions of glycolytic enzymes of parasites: unpredicted use of ancient proteins. Mol. Biochem. Parasitol. 193, 75-81 CrossRef PubMed
7. Tunio, S.A., Oldfield, N.J., Berry, A., Ala'Aldeen, D.A., Wooldridge, K.G. and Turner, D.P. (2010) The moonlighting protein fructose-1, 6-bisphosphate aldolase of Neisseria meningitidis: surface localization and role in host cell adhesion. Mol. Microbiol. 7, 605-615 CrossRef
8. Aseev, L.V. and Boni, I.V. (2011) Extraribosomal functions of bacterial ribosomal proteins. Mol. Biol. 45, 739-750 CrossRef
9. Bergthorsson, U., Andersson, D.I. and Roth, J.R. (2007) Ohno's dilemma: evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. U.S.A. 104, 17004-17009 CrossRef PubMed
10. Hughes, A.L. (1994) The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B 256, 119-124 CrossRef
11. Conrad, B. and Antonarakis, S.E. (2007) Gene duplication: a drive for phenotypic diversity and cause of human disease. Annu. Rev. Genomics Hum. Genet. 8, 17-35 CrossRef PubMed
12. Lynch, M., Sung, W., Morris, K., Coffey, N., Landry, C.R., Dopman, E.B., Dickinson, W.J., Okamoto, K., Kulkarni, S., Hartl, D.L. and Thomas, W.K. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl. Acad. Sci. U.S.A. 105, 9272-9277 CrossRef PubMed
13. Lipinski, K.J., Farslow, J.C., Fitzpatrick, K.A., Lynch, M., Katju, V. and Bergthorsson, U. (2011) High spontaneous rate of gene duplication in Caenorhabditis elegans. Curr. Biol. 21, 306-310 CrossRef PubMed
14. Anderson, P. and Roth, J. (1981) Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc. Natl. Acad. Sci. U.S.A. 78, 3113-3117 CrossRef PubMed
15. Brunschwig, H., Levi, L., Ben-David, E., Williams, R.W., Yakir, B. and Shifman, S. (2012) Fine-scale maps of recombination rates and hotspots in the mouse genome. Genetics 191, 757-764 CrossRef PubMed
16. Myers, S., Bottolo, L., Freeman, C., McVean, G. and Donnelly, P. (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310, 321-324 CrossRef PubMed
17. Bailey, J.A., Gu, Z., Clark, R.A., Reinert, K., Samonte, R.V., Schwartz, S., Adams, M.D., Myers, E.W., Li, P.W. and Eichler, E.E. (2002) Recent segmental duplications in the human genome. Science 297, 1003-1007 CrossRef PubMed
18. Reams, A.B. and Neidle, E.L. (2004) Gene amplification involves site-specific short homology-independent illegitimate recombination in Acinetobacter sp. strain ADP1. J. Mol. Biol. 338, 643-656 CrossRef PubMed
19. Devers, M., Rouard, N and Martin-Laurent, F. (2008) Fitness drift of an atrazine-degrading population under atrazine selection pressure. Environ. Microbiol. 10, 676-684 CrossRef PubMed
20. Näsvall, J., Sun, L., Roth, J.R. and Andersson, D.I. (2012) Real-time evolution of new genes by innovation, amplification, and divergence. Science 338, 384-387 CrossRef PubMed
21. Miller, S.R., Wood, A.M., Blankenship, R.E., Kim, M. and Ferriera, S. (2011) Dynamics of gene duplication in the genomes of chlorophyll d-producing cyanobacteria: implications for the ecological niche. Genome Biol. Evol. 3, 601-613 CrossRef PubMed
22. Lynch, M. and Conery, J.S. (2000) The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155 CrossRef PubMed
23. Lee, H., Popodi, E., Tang, H. and Foster, P.L. (2012) Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc. Natl. Acad. Sci. U.S.A. 109, E2774-E2783 CrossRef PubMed
24. Nachman, M.W. and Crowell, S.L. (2000) Estimate of the mutation rate per nucleotide in humans. Genetics 156, 297-304 PubMed
25. Sanjuán, R., Nebot, M.R., Chirico, N., Mansky, L.M. and Belshaw, R. (2010) Viral mutation rates. J. Virol. 84, 9733-9748 CrossRef PubMed
26. Martincorena, I., Seshasayee, A.S. and Luscombe, N.M. (2012) Evidence of non-random mutation rates suggests an evolutionary risk management strategy. Nature 485, 95-98 CrossRef PubMed
27. Tokuriki, N., Stricher, F., Schymkowitz, J., Serrano, L. and Tawfik, D.S. (2007) The stability effects of protein mutations appear to be universally distributed. J. Mol. Biol. 369, 1318-1332 CrossRef PubMed
28. Bloom, J.D., Silberg, J.J., Wilke, C.O., Drummond, D.A., Adami, C. and Arnold, F.H. (2005) Thermodynamic prediction of protein neutrality. Proc. Natl. Acad. Sci. U.S.A. 102, 606-611 CrossRef PubMed
29. Ehinger, S., Schubert, W.D., Bergmann, S., Hammerschmidt, S. and Heinz, D.W. (2004) Plasmin(ogen)-binding α-enolase from Streptococcus pneumoniae: crystal structure and evaluation of plasmin(ogen)-binding sites. J. Mol. Biol. 343, 997-1005 CrossRef PubMed
30. Parera, M. and Martinez, M.A. (2014) Strong epistatic interactions within a single protein. Mol. Biol. Evol. 31, 1546-1553 CrossRef PubMed
31. Weinreich, D.M., Delaney, N.F., Depristo, M.A. and Hartl, D.L. (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111-114 CrossRef PubMed
32. Parera, M., Perez-Alvarez, N., Clotet, B. and Martínez, M.A. (2009) Epistasis among deleterious mutations in the HIV-1 protease. J. Mol. Biol. 392, 243-250 CrossRef PubMed
33. Khanal, A., Yu McLoughlin, S., Kershner, J.P. and Copley, S.D. (2014) Differential effects of a mutation on the normal and promiscuous activities of orthologs: implications for natural and directed evolution. Mol. Biol. Evol., doi:10.1093/molbev/msu271 PubMed
34. Shultzaberger, R.K., Malashock, D.S., Kirsch, J.F. and Eisen, M.B. (2010) The fitness landscapes of cis-acting binding sites in different promoter and environmental contexts. PLoS Genet. 6, e1001042 CrossRef PubMed
35. Martínez-Núñez, M.A., Pérez-Rueda, E., Gutiérrez-Ríos, R.M. and Merino, E. (2010) New insights into the regulatory networks of paralogous genes in bacteria. Microbiology 156, 14-22 CrossRef PubMed
36. Dong, D., Yuan, Z. and Zhang, Z. (2011) Evidences for increased expression variation of duplicate genes in budding yeast: from cis-to trans-regulation effects. Nucleic Acids Res. 39, 837-847 CrossRef PubMed
37. Zhao, B., Lei, L., Vassylyev, D.G., Lin, X., Cane, D.E., Kelly, S.L., Yuan, H., Lamb, D.C. and Waterman, M.R. (2009) Crystal structure of albaflavenone monooxygenase containing a moonlighting terpene synthase active site. J. Biol. Chem. 284, 36711-36719 CrossRef PubMed
38. Jacobsen, A., Hendriksen, R.S., Aaresturp, F.M., Ussery, D.W. and Friis, C. (2011) The Salmonella enterica pan-genome. Microb. Ecol. 62, 487-504 CrossRef PubMed
39. Chirico, N., Vianelli, A. and Belshaw, R. (2010) Why genes overlap in viruses. Proc. Biol. Sci. 277, 3809-3817 CrossRef PubMed
40. Sabath, N., Wagner, A. and Karlin, D. (2012) Evolution of viral proteins originated de novo by overprinting. Mol. Biol. Evol. 29, 3767-3780 CrossRef PubMed
41. Stoltzfus, C.M. (2009) Chapter 1. Regulation of HIV-1 alternative RNA splicing and its role in virus replication. Adv. Virus Res. 74, 1-40 CrossRef PubMed
42. Barbeau, B. and Mesnard, J.M. (2011) Making sense out of anti-sense transcription in human T-cell lymphotrophic viruses (HTLVs). Viruses 3, 456-468 CrossRef PubMed
43. Jacks, T., Power, M.D., Masiarz, F.R., Luciw, P.A., Barr, P.J. and Varmus, H.E. (1998) Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 331, 280-283 CrossRef
44. Gomis-Rüth, F.X., Dessen, A., Timmins, J., Bracher, A., Kolesnikowa, L., Becker, S., Klenk, H.D. and Weissenhorn, W. (2003) The matrix protein VP40 from Ebola virus octamerizes into pore-like structures with specific RNA binding properties. Structure 11, 423-433 CrossRef PubMed
45. Bornholdt, Z.A., Noda, T., Abelson, D.M., Halfmann, P., Wood, M.R., Kawaoka, Y. and Saphire, E.O. (2013) Structural rearrangement of ebola virus VP40 begets multiple functions in the virus life cycle. Cell 154, 763-774 CrossRef PubMed
46. Agarwal, S., Kulshreshtha, P., Bambah, Mukku, D. and Bhatnagar, R. (2008) α-Enolase binds to human plasminogen on the surface of Bacillus anthracis. Biochim. Biophys. Acta 1784, 986-994 CrossRef PubMed
47. Knaust, A., Weber, MV., Hammerschmidt, S., Bergmann, S., Frosch, M. and Kurzai, O. (2007) Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J. Bacteriol. 189, 3246-3255 CrossRef PubMed
48. Capello, M., Ferri-Borgogno, S., Cappello, P. and Novelli, F. (2011) α-Enolase: a promising therapeutic and diagnostic tumor target. FEBS J. 278, 1064-1074 CrossRef PubMed
49. Lopez-Alemany, R., Longstaff, C., Hawley, S., Mirshahi, M., Fábregas, P., Jardí, M., Merton, E., Miles, L.A. and Félez, J. (2003) Inhibition of cell surface mediated plasminogen activation by a monoclonal antibody against α-enolase. Am. J. Hematol. 7, 234-242 CrossRef
50. Miles, L.A., Dahlberg, C.M., Plescia, J., Felez, J., Kato, K. and Plow, E.F. (1991) Role of cell-surface lysines in plasminogen binding to cells: identification of α-enolase as a candidate plasminogen receptor. Biochemistry 30, 1682-1691 CrossRef PubMed
51. Nakajima, K., Hamanoue, M., Takemoto, N., Hattori, T., Kato, K. and Kohsaka, S. (1994) Plasminogen binds specifically to α-enolase on rat neuronal plasma membrane. J. Neurochem. 63, 2048-2057 CrossRef PubMed
52. Diaz-Ramos, À., Roig-Borrellas, A., García-Melero, A., Llorens, A. and López-Alemany, R. (2012) Requirement of plasminogen binding to its cell-surface receptor α-enolase for efficient regeneration of normal and dystrophic skeletal muscle. PLoS ONE 7, e50477 CrossRef PubMed
53. Wygrecka, M., Marsh, L.M., Morty, R.E., Henneke, I., Guenther, A., Lohmeyer, J., Markart, P. and Preissner, KT. (2009) Enolase-1 promotes plasminogen-mediated recruitment of monocytes to the acutely inflamed lung. Blood 113, 5588-5598 CrossRef PubMed
54. Volz, K. (2008) The functional duality of iron regulatory protein 1. Curr. Opin. Struct. Biol. 18, 106-111 CrossRef PubMed
55. Gerlt, J.A., Babbitt, P.C., Jacobson, M.P. and Almo, S.C. (2012) Divergent evolution in enolase superfamily: strategies for assigning functions. J. Biol. Chem. 287, 29-34 CrossRef PubMed
56. Gerlt, J.A., Babbitt, P.C. and Rayment, I. (2005) Divergent evolution in the enolase superfamily: the interplay of mechanism and specificity. Arch. Biochem. Biophys. 433, 59-70 CrossRef PubMed
57. Katritch, V., Cherezov, V. and Stevens, R.C. (2013) Structure-function of the G protein-coupled receptor superfamily. Annu. Rev. Pharmacol. Toxicol. 53, 531-556 CrossRef PubMed
58. Guo, B., Yu, Y. and Leibold, E.A. (1994) Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J. Biol. Chem. 269, 24252-24260 PubMed