Heterologous expression of MlcE in Saccharomyces cerevisiae provides resistance to natural and semi-synthetic statins

Metabolic Engineering Communications

Volumn 2, Issue , 2015, Pages 117-123

  Ley, Ana ^a   Coumou, Hilde Cornelijne ^a   Frandsen, Rasmus John Normand ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Cell factory; Polyketide; Resistance; Saccharomyces cerevisiae; Statins; Transport

Indexed keywords

COMPACTIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MEVINOLIN;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG SENSITIVITY; FLUORESCENCE MICROSCOPY; GENE; GENE EXPRESSION; GENOTYPE; MLCE GENE; NONHUMAN; PHYLOGENETIC TREE; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

EID: 84943273814     PISSN: None     EISSN: 22140301     Source Type: Journal    
DOI: 10.1016/j.meteno.2015.09.003     Document Type: Article

References (43)

1. Abe Y., Suzuki T., Ono C., Iwamoto K., Hosobuchi M., Yoshikawa H. Molecular cloning and characterization of an ML-236B (compactin) biosynthetic gene cluster in Penicillium citrinum. Mol. Genet. Genom. 2002, 267:636-646. 10.1007/s00438-002-0697-y.
2. Alberts A.W., Chen J., Kuron G., Hunt V., Huff J., Hoffman C., Rothrock J., Lopez M., Joshua H., Harris E., Patchett A., Monaghan R., Currie S., Stapley E., Albers-Schonberg G., Hensens O., Hirshfield J., Hoogsteen K., Liesch J., Springer J. Mevinolin: a highly potent competitive inhibitor of hydroxymethylglutaryl-coenzyme A reductase and a cholesterol-lowering agent. Proc. Natl. Acad. Sci. USA 1980, 77:3957-3961.
3. Barrios-González J., Miranda R.U. Biotechnological production and applications of statins. Appl. Microbiol. Biotechnol. 2010, 85:869-883. 10.1007/s00253-009-2239-6.
4. Bernsel A., Viklund H., Hennerdal A., Elofsson A. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 2009, 37:W465-W468. 10.1093/nar/gkp363.
5. Callahan T.M., Rose M.S., Meade M.J., Ehrenshaft M., Upchurch R.G. CFP, the putative cercosporin transporter of Cercospora kikuchii, is required for wild type cercosporin production, resistance, and virulence on soybean. Mol. Plant Microbe Interact. 1999, 12:901-910. 10.1094/MPMI.1999.12.10.901.
6. Chen Y.-P., Tseng C.-P., Liaw L.-L., Wang C.-L., Chen I.-C., Wu W.-J., Wu M.-D., Yuan G.-F. Cloning and characterization of monacolin K biosynthetic gene cluster from Monascus pilosus. J. Agric. Food Chem. 2008, 56:5639-5646. 10.1021/jf800595k.
7. Choi D., Cho K., Cha W., Ryu S. Effect of triton X-100 on compactin production from Penicillium citrinum. Biotechnol. Bioprocess Eng. 2004, 9:171-178. 10.1007/BF02942288.
8. Consortium T.U. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 2013, 41:D43-D47. 10.1093/nar/gks1068.
9. Dunlop M.J., Dossani Z.Y., Szmidt H.L., Chu H.C., Lee T.S., Keasling J.D., Hadi M.Z., Mukhopadhyay A. Engineering microbial biofuel tolerance and export using efflux pumps. Mol. Syst. Biol. 2011, 7:487. 10.1038/msb.2011.21.
10. Endo A. new hypocholesteroleic agent produced by a Monascus species. J. Antibiot. (Tokyo) 1979, 32:852-854.
11. Endo A., Kuroda M., Tanzawa K. Competitive inhibition of 3-hydroxy-3-methylglutaryl coenzyme A reductase by ML-236A and ML-236B fungal metabolites, having hypocholesterolemic activity. 1976. Atheroscler. Suppl. 1976, 5:39-42. 10.1016/j.atherosclerosissup.2004.08.021.
12. GBI Research Statins market to 2018-weak product pipeline and shift of focus towards combination therapies will lead to erosion of brand share. GBI Res. Glob. Bus. Intell. 2013, 20:18-20.
13. Gietz R.D., Schiestl R.H. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2007, 2:31-34.
14. Hutchinson C.R., Kennedy J., Park C., Kendrew S., Auclair K., Vederas J. Aspects of the biosynthesis of non-aromatic fungal polyketides by iterative polyketide synthases. Antonie Van Leeuwenhoek 2000, 78:287-295.
15. Jia Z., Zhang X., Zhao Y., Cao X. Enhancement of lovastatin production by supplementing polyketide antibiotics to the submerged culture of Aspergillus terreus. Appl. Biochem. Biotechnol. 2010, 160:2014-2025. 10.1007/s12010-009-8762-1.
16. Katoh K., Asimenos G., Toh H. Bioinformatics for DNA sequence analysis. Bioinformatics for DNA Sequence Analysis, Methods in Molecular Biology, Methods in Molecular Biology 2009, 39-64. Humana Press, Springer, Totowa, NJ. 10.1007/978-1-59745-251-9. D. Posada (Ed.).
17. Kennedy J., Auclair K., Kendrew S.G., Park C., Vederas J.C., Hutchinson C.R. Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis. Science 1999, 284:1368-1372. 10.1126/science.284.5418.1368.
18. Larkin M.a, Blackshields G., Brown N.P., Chenna R., McGettigan P.a, McWilliam H., Valentin F., Wallace I.M., Wilm a, Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. 10.1093/bioinformatics/btm404.
19. Lisby M., Mortensen U.H., Rothstein R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 2003, 5:572-577. 10.1038/ncb997.
20. Malla S., Niraula N.P., Liou K., Sohng J.K. Self-resistance mechanism in Streptomyces peucetius: overexpression of drrA, drrB and drrC for doxorubicin enhancement. Microbiol. Res. 2010, 165:259-267. 10.1016/j.micres.2009.04.002.
21. Manzoni M., Rollini M. Biosynthesis and biotechnological production of statins by filamentous fungi and application of these cholesterol-lowering drugs. Appl. Microbiol. Biotechnol. 2002, 58:555-564. 10.1007/s00253-002-0932-9.
22. Marger M.D., Saier M.H. A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci. 1993, 18:13-20.
23. Martín J.F., Casqueiro J., Liras P. Secretion systems for secondary metabolites: how producer cells send out messages of intercellular communication. Curr. Opin. Microbiol. 2005, 8:282-293. 10.1016/j.mib.2005.04.009.
24. Maury J., Asadollahi M.a, Møller K., Clark A., Nielsen J. Microbial isoprenoid production: an example of green chemistry through metabolic engineering. Adv. Biochem. Eng. Biotechnol. 2005, 100:19-51.
25. McWilliam H., Li W., Uludag M., Squizzato S., Park Y.M., Buso N., Cowley A.P., Lopez R. Analysis tool Web Services from the EMBL-EBI. Nucleic Acids Res. 2013, 41:W597-W600. 10.1093/nar/gkt376.
26. Mikkelsen M.D., Buron L.D., Salomonsen B., Olsen C.E., Hansen B.G., Mortensen U.H., Halkier B.A. Microbial production of indolylglucosinolate through engineering of a multi-gene pathway in a versatile yeast expression platform. Metab. Eng. 2012, 14:104-111. 10.1016/j.ymben.2012.01.006.
27. Morimoto K., Janssen W.J., Michael B., Mcphillips K.A., Borges V.M., Bowler P., Xiao Y., Kench J.A., Peter M., Vandivier R.W., Fessler M.B., Bowler R.P., Henson P.M. Lovastatin enhances clearance of apoptotic cells (efferocytosis) with implications for chronic obstructive pulmonary disease. J. Immunol. 2013, 7657-7665.
28. Nørholm M.H.H. A mutant Pfu DNA polymerase designed for advanced uracil-excision DNA engineering. BMC Biotechnol. 2010, 10:21. 10.1186/1472-6750-10-21.
29. Nour-Eldin H.H., Hansen B.G., Nørholm M.H.H., Jensen J.K., Halkier B.a Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res. 2006, 34:e122. 10.1093/nar/gkl635.
30. Pao S.S., Paulsen I.T., Saier M.H.J. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 1998, 62:1-34.
31. Partow S., Siewers V., Bjćrn S., Nielsen J., Maury J. Characterization of different promoters for designing a new expression vector in Saccharomyces cerevisiae. Yeast 2010, 27:955-964. 10.1002/yea.
32. Paulsen I.T., Brown M.H., Skurray R.a Proton-dependent multidrug efflux systems. Microbiol. Rev. 1996, 60:575-608.
33. Paulsen I.T., Skurray R.a Topology, structure and evolution of two families of proteins involved in antibiotic and antiseptic resistance in eukaryotes and prokaryotes-an analysis. Gene 1993, 124:1-11.
34. Pitkin J.W., Panaccione D.G., Walton J.D. A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum. Microbiology 1996, 142:1557-1565.
35. Pronk J.T. Auxotrophic yeast strains in fundamental and applied research. Appl. Environ. Microbiol. 2002, 68:2095-2100. 10.1128/AEM.68.5.2095-2100.2002.
36. Sherman F., Fink G.R., Hicks J.B., Laboratory C.S.H. Laboratory Course Manual for Methods in Yeast Genetics 1986, Cold Spring Harbor Laboratory, Cold Spring Harbor.
37. Singh S.K., Pandey A. Emerging approaches in fermentative production of statins. Appl. Biochem. Biotechnol. 2013, 171:927-938. 10.1007/s12010-013-0400-2.
38. Ullán R.V., Liu G., Casqueiro J., Gutiérrez S., Bañuelos O., Martín J.F. The cefT gene of Acremonium chrysogenum C10 encodes a putative multidrug efflux pump protein that significantly increases cephalosporin C production. Mol. Genet. Genom. 2002, 267:673-683. 10.1007/s00438-002-0702-5.
39. Verduyn C., Postma E., Scheffers W.A., Van Dijken J.P. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 1992, 8:501-517. 10.1002/yea.320080703.
40. Woodcock D.M., Ceowther P.J., Doherty J., Jefferson S., DeCruz E., Noyer-Weidner M., Smith S.S., Michael M.Z., Graham M.W. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation n plasmid and phage recombinants. Nucleic Acids Res. 1989, 17:3469-3478.
41. Xu W., Chooi Y.-H., Choi J.W., Li S., Vederas J.C., Da Silva N.a, Tang Y. LovG: the thioesterase required for dihydromonacolin L release and lovastatin nonaketide synthase turnover in lovastatin biosynthesis. Angew. Chem. Int. Ed. Engl. 2013, 52:6472-6475. 10.1002/anie.201302406.
42. Xu Y., Willems A., Au-Yeung C., Tahlan K., Nodwell J.R. A two-step mechanism for the activation of actinorhodin export and resistance in Streptomyces coelicolor. MBio 2012, 3. 10.1128/mBio.00191-12.
43. Yu C.-S., Chen Y.-C., Lu C.-H., Hwang J.-K. Prediction of protein subcellular localization. Proteins 2006, 64:643-651. 10.1002/prot.21018.