In Vitro Reconstitution and Optimization of the Entire Pathway to Convert Glucose into Fatty Acid

ACS Synthetic Biology

Volumn 6, Issue 4, 2017, Pages 701-709

  Liu, Zheng ^a   Zhang, Yuchen ^b   Jia, Xiaoge ^b   Hu, Mengzhu ^b   Deng, Zixin ^b   Xu, Yancheng ^a   Liu, Tiangang ^b  

^a ZHONGNAN HOSPITAL OF WUHAN UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

Author keywords

fatty acid biosynthesis; fatty acids; glucose; glycolysis; in vitro reconstitution; pyruvate dehydrogenase

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ADENOSINE TRIPHOSPHATE; DECANOIC ACID; FATTY ACID; FRUCTOSE 6 PHOSPHATE; GLUCOKINASE; GLUCOSE; GLUCOSE 6 PHOSPHATE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LAURIC ACID; MYRISTIC ACID; PALMITIC ACID; PENTOSE PHOSPHATE; PYRUVATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; ACETYL COENZYME A CARBOXYLASE; FATTY ACID SYNTHASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PYRUVATE DEHYDROGENASE COMPLEX;

ARTICLE; CITRIC ACID CYCLE; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; GLYCOLYSIS; IN VITRO STUDY; MASS FRAGMENTOGRAPHY; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; TITRIMETRY; GENETICS; METABOLISM; THIN LAYER CHROMATOGRAPHY;

ACETYL-COA CARBOXYLASE; CHROMATOGRAPHY, THIN LAYER; ESCHERICHIA COLI; FATTY ACID SYNTHASES; FATTY ACIDS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLUCOSE; GLYCOLYSIS; NADP; PENTOSE PHOSPHATE PATHWAY; PYRUVATE DEHYDROGENASE COMPLEX;

EID: 85018460890     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.6b00348     Document Type: Article

References (58)

1. Berg, J., Tymoczko, J., and Stryer, L. (2012) Biochemistry, 7 th ed., W.H. Freeman and Company, New York, NY.
2. Samuel, V. T., Petersen, K. F., and Shulman, G. I. (2010) Lipid-induced insulin resistance: unravelling the mechanism Lancet 375, 2267-2277 10.1016/S0140-6736(10)60408-4
3. Randle, P. J. (1998) Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years Diabetes/Metab. Rev. 14, 263-283 10.1002/(SICI)1099-0895(199812)14:4<263::AID-DMR233>3.0.CO;2-C
4. Hu, F. B., Bronner, L., and Willett, W. C. et al. 2002, FIsh and omega-3 fatty acid intake and risk of coronary heart disease in women JAMA 287, 1815-1821 10.1001/jama.287.14.1815
5. Simopoulos, A. P. (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases Exp. Biol. Med. 233, 674-688 10.3181/0711-MR-311
6. Warburg, O. (1956) On the Origin of Cancer Cells Science 123, 309-314 10.1126/science.123.3191.309
7. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation Science 324, 1029-1033 10.1126/science.1160809
8. Pelicano, H., Martin, D. S., Xu, R. H., and Huang, P. (2006) Glycolysis inhibition for anticancer treatment Oncogene 25, 4633-4646 10.1038/sj.onc.1209597
9. Singh, S. B., Jayasuriya, H., Ondeyka, J. G., Herath, K. B., Zhang, C., Zink, D. L., Tsou, N. N., Ball, R. G., Basilio, A., Genilloud, O., Diez, M. T., Vicente, F., Pelaez, F., Young, K., and Wang, J. (2006) Isolation, Structure, and Absolute Stereochemistry of Platensimycin, A Broad Spectrum Antibiotic Discovered Using an Antisense Differential Sensitivity Strategy J. Am. Chem. Soc. 128, 11916-11920 10.1021/ja062232p
10. Campbell, J. W., John, E., and Cronan, J. (2001) Bacterial Fatty Acid Biosynthesis: Targets for Antibacterial Drug Discovery Annu. Rev. Microbiol. 55, 305-332 10.1146/annurev.micro.55.1.305
11. Liu, T., Vora, H., and Khosla, C. (2010) Quantitative analysis and engineering of fatty acid biosynthesis in E. coli Metab. Eng. 12, 378-386 10.1016/j.ymben.2010.02.003
12. Li, X., Guo, D., Cheng, Y., Zhu, F., Deng, Z., and Liu, T. (2014) Overproduction of fatty acids in engineered Saccharomyces cerevisiae Biotechnol. Bioeng. 111, 1841-1852 10.1002/bit.25239
13. Tao, H., Guo, D., Zhang, Y., Deng, Z., and Liu, T. (2015) Metabolic engineering of microbes for branched-chain biodiesel production with low-temperature property Biotechnol. Biofuels 8, 92 10.1186/s13068-015-0270-7
14. Barnett, J. A. (2003) A history of research on yeasts 5: the fermentation pathway Yeast 20, 509-543 10.1002/yea.986
15. Patel, M. S., Nemeria, N. S., Furey, W., and Jordan, F. (2014) The pyruvate dehydrogenase complexes: structure-based function and regulation J. Biol. Chem. 289, 16615-16623 10.1074/jbc.R114.563148
16. Choi-Rhee, E. and Cronan, J. E. (2003) The biotin carboxylase-biotin carboxyl carrier protein complex of Escherichia coli acetyl-CoA carboxylase J. Biol. Chem. 278, 30806-30812 10.1074/jbc.M302507200
17. Chan, D. I. and Vogel, H. J. (2010) Current understanding of fatty acid biosynthesis and the acyl carrier protein Biochem. J. 430, 1-19 10.1042/BJ20100462
18. Long, C. P., Gonzalez, J. E., Sandoval, N. R., and Antoniewicz, M. R. (2016) Characterization of physiological responses to 22 gene knockouts in Escherichia coli central carbon metabolism Metab. Eng. 37, 102-113 10.1016/j.ymben.2016.05.006
19. Hold, C. and Panke, S. (2009) Towards the engineering of in vitro systems J. R. Soc., Interface 6, S507-S521 10.1098/rsif.2009.0110.focus
20. Lowry, B., Walsh, C. T., and Khosla, C. (2015) In Vitro Reconstitution of Metabolic Pathways: Insights into Nature's Chemical Logic Synlett 26, 1008-1025 10.1055/s-0034-1380264
21. Buchner, E. and Rapp, R. (1897) Alkoholische Gährung ohne Hefezellen Ber. Dtsch. Chem. Ges. 30, 2668-2678 10.1002/cber.18970300354
22. Welch, P. and Scopes, R. K. (1985) Studies on cell-free metabolism: Ethanol production by a yeast glycolytic system reconstituted from purified enzymes J. Biotechnol. 2, 257-273 10.1016/0168-1656(85)90029-X
23. Kay, J. E. and Jewett, M. C. (2015) Lysate of engineered Escherichia coli supports high-level conversion of glucose to 2,3-butanediol Metab. Eng. 32, 133-142 10.1016/j.ymben.2015.09.015
24. Dudley, Q. M., Anderson, K. C., and Jewett, M. C. (2016) Cell-Free Mixing of Escherichia coli Crude Extracts to Prototype and Rationally Engineer High-Titer Mevalonate Synthesis ACS Synth. Biol. 5, 1578 10.1021/acssynbio.6b00154
25. Krutsakorn, B., Honda, K., Ye, X., Imagawa, T., Bei, X., Okano, K., and Ohtake, H. (2013) In vitro production of n-butanol from glucose Metab. Eng. 20, 84-91 10.1016/j.ymben.2013.09.006
26. Opgenorth, P. H., Korman, T. P., and Bowie, J. U. (2016) A synthetic biochemistry module for production of bio-based chemicals from glucose Nat. Chem. Biol. 12, 393-395 10.1038/nchembio.2062
27. Reed, L. J., Pettit, F. H., Eley, M. H., Hamilton, L., Collins, J. H., and Oliver, R. M. (1975) Reconstitution of the Escherichia coli pyruvate dehydrogenase complex Proc. Natl. Acad. Sci. U. S. A. 72, 3068-3072 10.1073/pnas.72.8.3068
28. Snoep, J. L., de Graef, M. R., Westphal, A. H., de Kok, A., de Mattos, M. J. T., and Neijssel, O. M. (1993) Differences in sensitivity to NADH of purified pyruvate dehydrogenase complexes of Enterococcus faecalis, Lactococcus lactis, Azotobacter vinelandii and Escherichia coli: implications for their activity in vivo FEMS Microbiol. Lett. 114, 279-283 10.1111/j.1574-6968.1993.tb06586.x
29. Yu, X., Liu, T., Zhu, F., and Khosla, C. (2011) In vitro reconstitution and steady-state analysis of the fatty acid synthase from Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 108, 18643-18648 10.1073/pnas.1110852108
30. Xiao, X., Yu, X., and Khosla, C. (2013) Metabolic flux between unsaturated and saturated fatty acids is controlled by the FabA:FabB ratio in the fully reconstituted fatty acid biosynthetic pathway of Escherichia coli Biochemistry 52, 8304-8312 10.1021/bi401116n
31. Bates, D. L., Danson, M. J., Hale, G., Hooper, E. A., and Perham, R. N. (1977) Self-assembly and catalytic activity of the pyruvate dehydrogenase multienzyme complex of Escherichia coli Nature 268, 313-316 10.1038/268313a0
32. Magnuson, K., Jackowski, S., Rock, C. O., and Cronan, J. E. (1993) Regulation of fatty acid biosynthesis in Escherichia coli Microbiol. Rev. 57, 522-542
33. Meyer, D., Schneider-Fresenius, C., Horlacher, R., Peist, R., and Boos, W. (1997) Molecular characterization of glucokinase from Escherichia coli K-12 J. Bacteriol. 179, 1298-1306 10.1128/jb.179.4.1298-1306.1997
34. Kotlarz, D., Garreau, H., and Buc, H. (1975) Regulation of the amount and of the activity of phosphofructokinases and pyruvate kinases in Escherichia coli Biochim. Biophys. Acta, Gen. Subj. 381, 1-5 10.1016/0304-4165(75)90232-9
35. Waygood, E. B. and Sanwal, B. (1974) The Control of Pyruvate Kinases of Escherichia coli I. Physicochemical and Regulatory Properties of the Enzyme Activated by Fructose 1,6-DiphospHATE J. Biol. Chem. 249, 265-274
36. Fraser, H. I., Kvaratskhelia, M., and White, M. F. (1999) The two analogous phosphoglycerate mutases of Escherichia coli FEBS Lett. 455, 344-348 10.1016/S0014-5793(99)00910-2
37. Garrido-Pertierra, A. and Cooper, R. A. (1983) Evidence for two dinstinct pyruvate kinase genes in Escherichia coli K-12 FEBS Lett. 162, 420-422 10.1016/0014-5793(83)80799-6
38. Ponce, E., Flores, N., Martinez, A., Valle, F., and Bolívar, F. (1995) Cloning of the two pyruvate kinase isoenzyme structural genes from Escherichia coli: the relative roles of these enzymes in pyruvate biosynthesis J. Bacteriol. 177, 5719-5722 10.1128/jb.177.19.5719-5722.1995
39. Lu, P., Vogel, C., Wang, R., Yao, X., and Marcotte, E. M. (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation Nat. Biotechnol. 25, 117-124 10.1038/nbt1270
40. Wilkinson, K. D. and Williams, C. H. (1981) NADH inhibition and NAD activation of Escherichia coli lipoamide dehydrogenase catalyzing the NADH-lipoamide reaction J. Biol. Chem. 256, 2307-2314
41. Schonauer, M. S., Kastaniotis, A. J., Kursu, V. A. S., Hiltunen, J. K., and Dieckmann, C. L. (2009) Lipoic Acid Synthesis and Attachment in Yeast Mitochondria J. Biol. Chem. 284, 23234-23242 10.1074/jbc.M109.015594
42. Kozak, B. U., van Rossum, H. M., Luttik, M. A., Akeroyd, M., Benjamin, K. R., Wu, L., de Vries, S., Daran, J.-M., Pronk, J. T., and van Maris, A. J. (2014) Engineering acetyl coenzyme A supply: functional expression of a bacterial pyruvate dehydrogenase complex in the cytosol of Saccharomyces cerevisiae mBio 5, e01696-01614 10.1128/mBio.01696-14
43. Snoep, J. L., Westphal, A. H., Benen, J. A. E., Mattos, M. J. T. D., Neijssel, O. M., and Kok, A. D. (1992) Isolation and characterisation of the pyruvate dehydrogenase complex of anaerobically grown Enterococcus faecalis NCTC 775 Eur. J. Biochem. 203, 245-250 10.1111/j.1432-1033.1992.tb19853.x
44. Zhu, F., Lu, L., Fu, S., Zhong, X., Hu, M., Deng, Z., and Liu, T. (2015) Targeted engineering and scale up of lycopene overproduction in Escherichia coli Process Biochem. 50, 341-346 10.1016/j.procbio.2014.12.008
45. Sánchez, A. M., Andrews, J., Hussein, I., Bennett, G. N., and San, K. Y. (2006) Effect of Overexpression of a Soluble Pyridine Nucleotide Transhydrogenase (UdhA) on the Production of Poly (3-hydroxybutyrate) in Escherichia coli Biotechnology progress 22, 420-425 10.1021/bp050375u
46. Bommareddy, R. R., Chen, Z., Rappert, S., and Zeng, A.-P. (2014) A de novo NADPH generation pathway for improving lysine production of Corynebacterium glutamicum by rational design of the coenzyme specificity of glyceraldehyde 3-phosphate dehydrogenase Metab. Eng. 25, 30-37 10.1016/j.ymben.2014.06.005
47. Martinez, I., Zhu, J., Lin, H., Bennett, G. N., and San, K. Y. (2008) Replacing Escherichia coli NAD-dependent glyceraldehyde 3-phosphate dehydrogenase (GAPDH) with a NADP-dependent enzyme from Clostridium acetobutylicum facilitates NADPH dependent pathways Metab. Eng. 10, 352-359 10.1016/j.ymben.2008.09.001
48. Bastian, S., Liu, X., Meyerowitz, J. T., Snow, C. D., Chen, M. M. Y., and Arnold, F. H. (2011) Engineered ketol-acid reductoisomerase and alcohol dehydrogenase enable anaerobic 2-methylpropan-1-ol production at theoretical yield in Escherichia coli Metab. Eng. 13, 345-352 10.1016/j.ymben.2011.02.004
49. Javidpour, P., Pereira, J. H., Goh, E.-B., McAndrew, R. P., Ma, S. M., Friedland, G. D., Keasling, J. D., Chhabra, S. R., Adams, P. D., and Beller, H. R. (2014) Biochemical and Structural Studies of NADH-Dependent FabG Used To Increase the Bacterial Production of Fatty Acids under Anaerobic Conditions Appl. Environ. Microbiol. 80, 497-505 10.1128/AEM.03194-13
50. Toomey, R. E. and Wakil, S. J. (1966) Studies on the mechanism of fatty acid synthesis XV. Preparation and general properties of β-ketoacyl acyl carrier protein reductase from Escherichia coli Biochim. Biophys. Acta, Lipids Lipid Metab. 116, 189-197 10.1016/0005-2760(66)90001-4
51. Bergler, H., Fuchsbichler, S., Högenauer, G., and Turnowsky, F. (1996) The Enoyl-[Acyl-Carrier-Protein] Reductase (FabI) of Escherichia coli, which Catalyzes a Key Regulatory Step in Fatty Acid Biosynthesis, Accepts NADH and NADPH as Cofactors and is Inhibited by Palmitoyl-CoA Eur. J. Biochem. 242, 689-694 10.1111/j.1432-1033.1996.0689r.x
52. Sprenger, G. A. (1995) Genetics of pentose-phosphate pathway enzymes ofEscherichia coli K-12 Arch. Microbiol. 164, 324-330 10.1007/BF02529978
53. Davis, M. S., Solbiati, J., and Cronan, J. E. (2000) Overproduction of Acetyl-CoA Carboxylase Activity Increases the Rate of Fatty Acid Biosynthesis in Escherichia coli J. Biol. Chem. 275, 28593-28598 10.1074/jbc.M004756200
54. Liu, R., Zhu, F., Lu, L., Fu, A., Lu, J., Deng, Z., and Liu, T. (2014) Metabolic engineering of fatty acyl-ACP reductase-dependent pathway to improve fatty alcohol production in Escherichia coli Metab. Eng. 22, 10-21 10.1016/j.ymben.2013.12.004
55. Zhu, F., Zhong, X., Hu, M., Lu, L., Deng, Z., and Liu, T. (2014) In vitro reconstitution of mevalonate pathway and targeted engineering of farnesene overproduction in Escherichia coli Biotechnol. Bioeng. 111, 1396-1405 10.1002/bit.25198
56. Pfeifer, B. A., Admiraal, S. J., Gramajo, H., Cane, D. E., and Khosla, C. (2001) Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli Science 291, 1790-1792 10.1126/science.1058092
57. Schwartz, E. R. and Reed, L. J. (1970) α-Keto acid dehydrogenase complexes. XIV. Regulation of the activity of the pyruvate dehydrogenase complex of Escherichia coli Biochemistry 9, 1434-1439 10.1021/bi00808a019
58. Lu, X., Vora, H., and Khosla, C. (2008) Overproduction of free fatty acids in E. coli: Implications for biodiesel production Metab. Eng. 10, 333-339 10.1016/j.ymben.2008.08.006