Enzyme promiscuity – A light on the “darker” side of enzyme specificity

References

• Abhinav N, Atkins WM. 2008. A quantitative index of substrate promiscuity. Biochem. 47(1):157–166.
   PubMed Web of Science ®Google Scholar
• Aharoni A, Gaidukov L, Khersonsky O, Mc QGS, Roodveldt C, Tawfik DS. 2005. The evolvability of promiscuous protein functions. Nat Genet. 37(1):73–76.
   PubMed Web of Science ®Google Scholar
• Andrianantoandro E, Basu S, Karig DK, Weiss R. 2006. Synthetic biology: new engineering rules for an emerging discipline. Mol Sys Biol. 2:28.
   Web of Science ®Google Scholar
• Arbildi P, Sonora C, Del Rio N, Marques JM, Hernandez A. 2018. Alternative RNA splicing of leucocyte tissue transglutaminase in coeliac disease. Scand J Immunol. 87(5):e12659.
   PubMed Web of Science ®Google Scholar
• Babbitt PC, Hasson MS, Wedekind JE, Palmer DRJ, Barrett WC, Reed GH, Rayment I, Ringe D, Kenyon GL, Gerlt JA. 1996. The enolase superfamily: a general strategy for enzyme-catalyzed abstraction of the α-protons of carboxylic acids. Biochem. 35(51):16489–16501.
   PubMed Web of Science ®Google Scholar
• Babtie A, Tokuriki N, Hollfelder F. 2010. What makes an enzyme promiscuous? Curr Opin Chem Biol. 14(2):200–207.
   PubMed Web of Science ®Google Scholar
• Bahekar SP, Sarode PB, Wadekar MP, Chandak HS. 2015. Simple and efficient synthesis of 3,4-dihydropyrimidin-2(1H)-thiones utilizing L-proline nitrate as a proficient, recyclable and eco-friendly catalyst. J Saudi Chem Soc. 2:1–5.
   Google Scholar
• Baier F, Chen J, Solomonson M, Strynadka NC, Tokuriki N. 2015. Distinct metal isoforms underlie promiscuous activity profiles of metalloenzymes. ACS Chem Biol. 10(7):1684–1693.
   PubMed Web of Science ®Google Scholar
• Barford D, Das AK, Egloff MP. 1998. The structure and mechanism of protein phosphatases: Insights into catalysis and regulation. Annu Rev Biophys Biomol Struct. 27(1):133–164.
   PubMedGoogle Scholar
• Bordes I, Recatala J, Swiderek K, Moliner V. 2015. Is promiscuous CALB a good scaffold for designing new epoxidases? Molecules. 20(10):7789–17806.
   Web of Science ®Google Scholar
• Bornadel A, Akerman CO, Adlercreutz P, Hatti-Kaul R, Borg N. 2013. Kinetic modeling of lipase-catalyzed esterification reaction between oleic acid and trimethylolpropane: a simplified model for multi-substrate multi-product ping-pong mechanisms. Biotechnol Progress. 29(6):1422–1429.
   PubMed Web of Science ®Google Scholar
• Boukouris AE, Zervopoulos SD, Michelakis ED. 2016. Metabolic enzymes moonlighting in the nucleus: metabolic regulation of gene transcription. Trends Biochem. 41(8):712–730.
   PubMed Web of Science ®Google Scholar
• Bugg T. 2004. Introduction to enzyme and coenzyme chemistry. 2nd ed. Oxford (UK): Blackwell publishing; p. 2, 4, 5.
   Google Scholar
• Carbonell P, Faulon JL. 2010. Molecular signatures-based prediction of enzyme promiscuity. Bioinfo. 26(16):2012–2019.
   Google Scholar
• Chen W, Yao J, Meng J, Han W, Tao Y, Chen Y, Guo Y, Shi G, He Y, Jin JM, et al. 2019. Promiscuous enzymatic activity-aided multiple-pathway network design for metabolic flux rearrangement in hydroxytyrosol biosynthesis. Nature Commun. 10. Article number: 960.
   Web of Science ®Google Scholar
• Cheng L, Leung KS. 2018. Identification and characterization of moonlighting long non-coding RNAs based on RNA and protein interactome. Bioinfo. 34(20):3519–3528.
   Google Scholar
• Cohen HM, Tawfik DS, Griffiths AD. 2002. Promiscuous methylation of non-canonical DNA sites by HaeIII methyltransferase. Nucleic Acids Res. 30(17):3880–3885.
   PubMed Web of Science ®Google Scholar
• Colin PY, Kintses B, Gielen F, Miton CM, Fischer G, Mohamed MF, Hyvonen M, Morgavi DP, Janssen DB, Hollfelder F. 2015. Ultrahigh-throughput discovery of promiscuous enzymes by picodroplet functional metagenomics. Nature Commun. 6:10008.
   PubMed Web of Science ®Google Scholar
• Copley SD. 2003. Enzymes with extra talents: moonlighting functions and catalytic promiscuity. Curr Opin Chem Biol. 7(2):265–272.
   PubMed Web of Science ®Google Scholar
• de Visser JA, Krug J. 2014. Empirical fitness landscapes and the predictability of evolution. Nat Rev Genet. 15(7):480–490.
   PubMed Web of Science ®Google Scholar
• Delmas J, Robin F, Carvalho F, Mongaret C, Bonnet R. 2006. Prediction of the evolution of ceftazidime resistance in extended-spectrum beta-lactamase CTX-M-9. Antimicrob Agents Chemother. 50(2):731–738.
   PubMed Web of Science ®Google Scholar
• Devries EJ, Janssen DB. 2003. Biocatalytic conversion of epoxides. Curr Opin Biotechnol. 14:414–420.
   PubMed Web of Science ®Google Scholar
• Duarte F, Amrein BA, Kamerlin S. 2013. Modeling catalytic promiscuity in the alkaline phosphatase superfamily. Phys Chem Chem Phys. 15(27):11160–11177.
   PubMed Web of Science ®Google Scholar
• Fan L, Arvai AS, Cooper PK, Iwai S, Hanaoka F, Tainer JA. 2006. Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair. Mol Cell. 22(1):27–37.
   PubMed Web of Science ®Google Scholar
• Fisher HF. 2013. The application of transient-state kinetic isotope effects to the resolution of mechanisms of enzyme-catalyzed reactions. Mol. 18(7):8230–8242.
   PubMed Web of Science ®Google Scholar
• Gancedo C, Flores CL. 2008. Moonlighting proteins in yeasts. Microb Mol Biol Rev. 72(1):197–210.
   PubMed Web of Science ®Google Scholar
• Gupta RD. 2016. Recent advances in enzyme promiscuity. Sustain Chem Process. 4(1):1–7.
   Google Scholar
• Guzman GI, Sandberg TE, LaCroix RA, Nyerges A, Papp H, de Raad M, King ZA, Hefner Y, Northen TR, Notebaart RA, et al. 2019. Enzyme promiscuity shapes adaptation to novel growth substrates. Mol Syst Biol. 15:e8462.
   PubMed Web of Science ®Google Scholar
• Hoffmeister D, Yang J, Liu L, Thorson JS. 2003. Creation of the first anomeric D/L-sugar kinase by means of directed evolution. Pro Nat Acad Sci U S A. 100(23):13184–13189.
   PubMed Web of Science ®Google Scholar
• Huberts DH, van der Klei IJ. 2010. Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta. 1803(4):520–525.
   PubMed Web of Science ®Google Scholar
• Hult K, Berglund P. 2007. Enzyme promiscuity: mechanism and applications. Trends Biotechnol. 25(5):231–238.
   PubMed Web of Science ®Google Scholar
• Humble MS, Berglund P. 2011. Biocatalytic promiscuity. Eur J Org Chem. 2011(19):3391–3401.
   Web of Science ®Google Scholar
• Jayakumar R, Vadivel R, Ananthi N. 2018. Role of chirality in drugs. OMCIJ. 5(3):1–6.
   Google Scholar
• Jeanguenin L, Lara NA, Pribat A, Mageroy MH, Gregory JF, Rice KC, de Crecy-Lagard V, Hanson AD. 2010. Moonlighting glutamate formiminotransferases can functionally replace 5-formyltetrahydrofolate cycloligase. J Biol Chem. 285(53):41557–41566.
   PubMed Web of Science ®Google Scholar
• Jeffery CJ. 2003. Multifunctional proteins: examples of gene sharing. Ann Med. 35(1):28–35.
   PubMed Web of Science ®Google Scholar
• Jeffery CJ. 2015. Why study moonlighting proteins? Front Genet. 6:211
   PubMed Web of Science ®Google Scholar
• Jensen RA. 1976. Enzyme recruitment in evolution of new function. Annu Rev Microbiol. 30(1):409–425.
   PubMedGoogle Scholar
• Jia B, Cheong GW, Zhang S. 2013. Multifunctional enzymes in archaea: promiscuity and moonlight. Extremophiles. 17(2):193–203.
   PubMed Web of Science ®Google Scholar
• Jia B, Lee S, Pham B, Cho Y, Yang JK, Byeon HS, Kim J, Cheong GW. 2010. An archaeal NADH oxidase causes damage to both proteins and nucleic acids under oxidative stress. Mol Cells. 29(4):363–371.
   PubMed Web of Science ®Google Scholar
• Jia B, Linh L, Lee S, Pham B, Liu J, Pan H, Zhang S, Cheong GW. 2011. Biochemical characterization of glyceraldehyde-3-phosphate dehydrogenase from Thermococcus kodakarensis KOD1. Extremophiles. 15(3):337–346.
   PubMed Web of Science ®Google Scholar
• Kazlauskas RJ. 2005. Enhancing catalytic promiscuity for biocatalysis. Curr Opin Chem Biol. 9(2):195–201.
   PubMed Web of Science ®Google Scholar
• Kellogg BA, Poulter CD. 1997. Chain elongation in the isoprenoid biosynthetic pathway. Curr Opin Chem Biol. 1(4):570–578.
   PubMed Web of Science ®Google Scholar
• Khandelwal A, Chandu D, Roe CM, Kopan R, Quatrano RS. 2007. Moonlighting activity of presenilin in plants is independent of gamma-secretase and evolutionarily conserved. Proc Nat Acad Sci U S A. 104(33):13337–13342.
   PubMed Web of Science ®Google Scholar
• Khersonsky O, Malitsky S, Rogachev I, Tawfik DS. 2011. Role of chemistry versus substrate binding in recruiting promiscuous enzyme functions. Biochemistry. 50(13):2683–2690.
   PubMed Web of Science ®Google Scholar
• Khersonsky O, Roodveldt C, Tawfik DS. 2006. Enzyme promiscuity: evolutionary and mechanistic aspects. Curr Opin Chem Biol. 10(5):498–508.
   PubMed Web of Science ®Google Scholar
• Khersonsky O, Tawfik DS. 2006. The histidine 115-histidine 134 dyad mediates the lactonase activity of mammalian serum paraoxonases. J Biol Chem. 281(11):7649–7656.
   PubMed Web of Science ®Google Scholar
• Kirschner M, Gerhart J. 1998. Evolvability. Proc Natl Acad Sci U S A. 95(15):8420–8427.
   PubMed Web of Science ®Google Scholar
• Kolmodin K, Aqvist J. 2001. The catalytic mechanism of protein tyrosine phosphatases revisited. FEBS Lett. 498(2–3):208–213.
   PubMed Web of Science ®Google Scholar
• Koval T, Lipovova P, Podzimek T, Matousek J, Duskova J, Skalova T, Stepankova A, Hasek J, Dohnalek J. 2013. Plant multifunctional nuclease TBN1 with unexpected phospholipase activity: structural study and reaction-mechanism analysis. Acta Crystallogr D Biol Crystallogr. 69(2):213–226.
   PubMedGoogle Scholar
• Le Breton M, Henneke G, Norais C, Flament D, Myllykallio H, Querellou J, Raffin JP. 2007. The heterodimeric primase from the euryarchaeon Pyrococcus abyssi: a multifunctional enzyme for initiation and repair? J Mol Biol. 374(5):1172–1185.
   PubMed Web of Science ®Google Scholar
• Lee S, Jia B, Pham B, Shao Y, Kwak J, Cheong GW. 2012. Architecture and characterization of sarcosine oxidase from Thermococcus kodakarensis KOD1. Extremophiles. 16(1):87–93.
   PubMed Web of Science ®Google Scholar
• Macho AP, Duran RL, Zipfel C. 2015. Tyrosine Importance of tyrosine phosphorylation in receptor kinase complexes. Trends Plant Sci. 20(5):269–272.
   PubMed Web of Science ®Google Scholar
• Martinez-Nunez MA, Perez-Rueda E. 2016. Do lifestyles influence the presence of promiscuous enzymes in bacteria and Archaea metabolism? Sustain Chem Process. 4:3.
   Google Scholar
• Martinez-Nunez MA, Poot-Hernandez AC, Rodriguez-Vazquez K, Perez-Rueda E. 2013. Increments and duplication events of enzymes and transcription factors influence metabolic and regulatory diversity in prokaryotes. Plos One. 8(7):69707.
   Web of Science ®Google Scholar
• Martinez-Nunez MA, Rodríguez-Escamilla Z, Rodriguez-Vazquez K, Perez-Rueda E. 2017. Tracing the repertoire of promiscuous enzymes along the metabolic pathways in archaeal organisms. Life (Basel). 7:30.
   Web of Science ®Google Scholar
• Miles ZD, Roberts SA, McCarty RM, Bandarian V. 2014. Biochemical and structural studies of 6-carboxy-5,6,7,8-tetrahydropterin synthase reveal the molecular basis of catalytic promiscuity within the tunnel-fold superfamily. J Biol Chem. 22(34):23641–23652.
   Google Scholar
• Mittag T, Kay LE, Forman-Kay JD. 2010. Protein dynamics and conformational disorder in molecular recognition. J Mol Recog. 23(2):105–116.
   PubMed Web of Science ®Google Scholar
• Moore BD. 2004. Bifunctional and moonlighting enzymes: lighting the way to regulatory control. Trends Plant Sci. 9(5):221–228.
   PubMed Web of Science ®Google Scholar
• Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science. 300(5617):332–336.
   PubMed Web of Science ®Google Scholar
• Nam H, Lewis NE, Lerman JA, Lee DH, Chang RL, Kim D, Palsson BO. 2012. Network context and selection in the evolution to enzyme specificity. Sci. 337(6098):1101–1104.
   PubMed Web of Science ®Google Scholar
• Nguyen LA, He H, Huy CP. 2006. Chiral drugs: an overview. Int J Biomed Sci. 2(2):85–100.
   PubMedGoogle Scholar
• Norrgard MA, Mannervik B. 2011. Engineering GST M2-2 for high activity with indene 1,2-oxide and indication of an H-site residue sustaining catalytic promiscuity. J Mol Biol. 412(1):111–120.
   PubMed Web of Science ®Google Scholar
• O’Brien PJ, Herschlag D. 2001. Functional interrelationships in the alkaline phosphatase superfamily: phosphodiesterase activity of Escherichia coli alkaline phosphatase. Biochemistry. 40(19):5691–5699.
   PubMed Web of Science ®Google Scholar
• Pandey RP. 2017. Diversifying natural products with promiscuous glycosyltransferase enzymes via a sustainable microbial fermentation approach. Front Chem. 5(110):1–4.
   PubMedGoogle Scholar
• Pandya C, Dunaway-Mariano D, Xia Y, Allen KN. 2014. Structure-guided approach for detecting large domain inserts in protein sequences as illustrated using the haloacid dehalogenase superfamily. Proteins. 82(9):1896–1906.
   PubMed Web of Science ®Google Scholar
• Piedrafita G, Keller MA, Ralser M. 2015. The impact of non-enzymatic reactions and enzyme promiscuity on cellular metabolism during (oxidative) stress conditions. Biomolecules. 5(3):2101–2122.
   PubMed Web of Science ®Google Scholar
• Poelarends GJ, Veetil VP, Whitman CP. 2008. The chemical versatility of the β–α–β fold: Catalytic promiscuity and divergent evolution in the tautomerase superfamily. Cell Mol Life Sci. 65(22):3606–3618.
   PubMed Web of Science ®Google Scholar
• Pordea A. 2015. Metal-binding promiscuity in artificial metalloenzyme design. Curr Opin Chem Biol. 25:124–132.
   PubMed Web of Science ®Google Scholar
• Ramos LM, Ponce de Leon y Tobio AY, dos Santos MR, de Oliveira HC, Gomes AF, Gozzo FC, de Oliveira AL, Neto BA. 2012. Mechanistic studies on Lewis acid catalyzed Biginelli reactions in ionic liquids: evidence for the reactive intermediates and the role of the reagents. J Org Chem. 77(22):10184–10193.
   PubMed Web of Science ®Google Scholar
• Renata H, Wang ZJ, Arnold FH. 2015. Expanding the enzyme universe: accessing non-natural reactions by mechanism-guided directed evolution. Angew Chem Int Ed Engl. 54(11):3351–3367.
   PubMed Web of Science ®Google Scholar
• Rivera PC, Nyati P, Noriega FG. 2015. A corpora allata farnesyl diphosphate synthase in mosquitoes displaying a metal ion dependent substrate specificity. Insect Mol Biol. 64:44–50.
   Web of Science ®Google Scholar
• Ronimus R, Morgan H. 2003. Distribution and phylogenies of enzymes of the Embden–Meyerhof–Parnas pathway from archaea and hyperthermophilic bacteria support a gluconeogenic origin of metabolism. Archaea. 1(3):199–221.
   PubMedGoogle Scholar
• Rowe LA, Geddie ML, Alexander OB, Matsumura I. 2003. A comparison of directed evolution approaches using the beta-glucuronidase model system. J Mol Biol. 332(4):851–860.
   PubMed Web of Science ®Google Scholar
• Royer SF, Haslett L, Crennell SJ, Hough DW, Danson MJ, Bull SD. 2010. CentreStructurally informed site-directed mutagenesis of a stereochemically promiscuous aldolase to afford stereochemically complementary biocatalysts. J Am Chem Soc. 132(33):11753–11758.
   PubMed Web of Science ®Google Scholar
• Schiraldi C, Giuliano M, De Rosa M. 2002. Perspectives on biotechnological applications of archaea. Archaea. 1(2):75–86.
   PubMedGoogle Scholar
• Soskine M, Tawfik D. 2010. Mutational effects and the evolution of new protein functions. Nat Rev Genet. 11(8):572–582.
   PubMed Web of Science ®Google Scholar
• Srinivasan B, Marks H, Mitra S, Smalley DM, Skolnick J. 2016. Catalytic and substrate promiscuity: Distinct multiple chemistries catalyzed by the phosphatase domain of receptor protein tyrosine phosphatase. Biochem J. 473(14):2165–2177.
   PubMedGoogle Scholar
• Timar E, Groma G, Kiss A, Venetianer P. 2004. Changing the recognition specificity of a DNA-methyltransferase by in vitro evolution. Nucleic Acids Res. 32(13):3898–3903.
   PubMed Web of Science ®Google Scholar
• Ulusu NN. 2015. Curious cases of the enzymes. J Med Biochem. 34(3):271–281.
   PubMed Web of Science ®Google Scholar
• Wienkers LC, Rock B. 2014. Multienzyme kinetics and sequential metabolism. Methods Mol Biol. 1113:93–118.
   PubMedGoogle Scholar
• Woo EJ, Lee S, Cha H, Park JT, Yoon SM, Song HN, Park KH. 2008. Structural insight into the bifunctional mechanism of the glycogen-debranching enzyme TreX from the archaeon Sulfolobus solfataricus. J Biol Chem. 283(42):28641–22864.
   PubMed Web of Science ®Google Scholar
• Xiong D, Lu S, Wu J, Liang C, Wang W, Wang W, Jin JM, Tang SY. 2017. Improving key enzyme activity in phenylpropanoid pathway with a designed biosensor. Metab Eng. 40:115–123.
   PubMed Web of Science ®Google Scholar
• Yang K, Metcalf WW. 2004. A new activity for an old enzyme: Escherichia coli bacterial alkaline phosphatase is a phosphitedependent hydrogenase. Pro Nat Acad Sci USA. 101(21):7919–7924.
   PubMed Web of Science ®Google Scholar
• Yoshikuni Y, Ferrin TE, Keasling JD. 2006. Designed divergent evolution of enzyme function. Nature. 440(7087):1078–1082.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Akutsu J, Kawarabayasi Y. 2010. Identification of novel acetyltransferase activity on the thermostable protein ST0452 from Sulfolobus tokodaii strain 7. J Bacteriol. 192(13):3287–3293.
   PubMed Web of Science ®Google Scholar
• Zheng H, Mei YJ, Du K, Shi QY, Zhang PF. 2013. Trypsin catalysed one-pot multicomponent synthesis of 4-thiazolidinones. Catal Lett. 143(3):298–301.
   Web of Science ®Google Scholar