δ9-Tetrahydrocannabinolic acid synthase production in Pichia pastoris enables chemical synthesis of cannabinoids

Journal of Biotechnology

Volumn 211, Issue , 2015, Pages 68-76

  Lange, Kerstin ^a,b   Schmid, Andreas ^b   Julsing, Mattijs K ^a  

^a TU DORTMUND UNIVERSITY   (Germany)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

Biocatalysis; Cannabinoids; Oxidase; Oxidative C C bond formation; Two liquid phase setup

Indexed keywords

CATALYSIS; CHEMICAL BONDS; ENZYMES; LIQUIDS; SYNTHESIS (CHEMICAL); YEAST;

BIOCATALYSIS; C-C BOND FORMATION; CANNABINOIDS; OXIDASE; TWO-LIQUID-PHASE;

CHROMATOGRAPHY;

CANNABINOID; DELTA9 TETRAHYDROCANNABINOLIC ACID SYNTHASE; DRONABINOL; HEXANE; SYNTHETASE; TETRAHYDROCANNABINOLIC ACID; UNCLASSIFIED DRUG; BENZOIC ACID DERIVATIVE; CANNABIGEROLIC ACID; DELTA(9)-TETRAHYDROCANNABINOLIC ACID; ISOMERASE;

AQUEOUS SOLUTION; ARTICLE; BIOCATALYSIS; BIOTECHNOLOGICAL PRODUCTION; CHROMATOGRAPHY; DEGLYCOSYLATION; ENZYME ACTIVITY; ENZYME ISOLATION; ENZYME PURIFICATION; ENZYME SYNTHESIS; FED BATCH FERMENTATION; FED BATCH REACTOR; FUNGAL BIOMASS; FUNGAL STRAIN; FUNGUS CULTURE; KOMAGATAELLA PASTORIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PRODUCTIVITY; STIRRED REACTOR; SUPERNATANT; SYNTHESIS; ANALOGS AND DERIVATIVES; BATCH CELL CULTURE; BIOMASS; BIOREACTOR; ENZYME SPECIFICITY; FERMENTATION; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PICHIA;

PICHIA PASTORIS;

BATCH CELL CULTURE TECHNIQUES; BENZOATES; BIOCATALYSIS; BIOMASS; BIOREACTORS; CANNABINOIDS; DRONABINOL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FERMENTATION; INTRAMOLECULAR OXIDOREDUCTASES; PICHIA; SUBSTRATE SPECIFICITY;

EID: 84938062746     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2015.06.425     Document Type: Article

References (45)

1. Baldascini H., Janssen D.B. Interfacial inactivation of epoxide hydrolase in a two-liquid-phase system. Enzyme Microb. Technol. 2005, 36:285-293.
2. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
3. Burton S.G., Cowan D.A., Woodley J.M. The search for the ideal biocatalyst. Nat. Biotechnol. 2002, 20:37-45.
4. Daly R., Hearn M.T. Expression of heterologous proteins in Pichia pastoris: a useful experimental tool in protein engineering and production. J. Mol. Recognit. 2005, 18:119-138.
5. Fellermeier M., Eisenreich W., Bacher A., Zenk M.H. Biosynthesis of cannabinoids. Incorporation experiments with (13)C-labeled glucoses. Eur. J. Biochem. 2001, 268:1596-1604.
6. Gagne S.J., Stout J.M., Liu E., Boubakir Z., Clark S.M., Page J.E. Identification of olivetolic acid cyclase from Cannabis sativa reveals a unique catalytic route to plant polyketides. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:12811-12816.
7. Goodin D. Marijuana and multiple sclerosis. Lancet. Neurol. 2004, 3:79-80.
8. Gröger H., Asano Y. Potential of enzymes in organic synthesis: enzyme reactions overview. Enzyme Catalysis in Organic Synthesis 2011, Wiley-VCH, Weinheim, Germany. 2nd ed. K. Drauz, H. Gröger, O. May (Eds.).
9. Hagel J.M., Beaudoin G.A., Fossati E., Ekins A., Martin V.J., Facchini P.J. Characterization of a flavoprotein oxidase from opium poppy catalyzing the final steps in sanguinarine and papaverine biosynthesis. J. Biol. Chem. 2012, 287:42972-42983.
10. Hannig G., Makrides S.C. Strategies for optimizing heterologous protein expression in E. coli. Trends Biotechnol. 1998, 16:54-60.
11. Hofstetter K., Lutz J., Lang I., Witholt B., Schmid A. Coupling of biocatalytic asymmetric epoxidation with NADH regeneration in organic-aqueous emulsions. Angew Chem. Int. Engl. 2004, 43:2163-2166.
12. Huang C.H., Winkler A., Chen C.L., Lai W.L., Tsai Y.C., Macheroux P., Liaw S.H. Functional roles of the 6-S-cysteinyl, 8alpha-N1-histidyl FAD in glucooligosaccharide oxidase from Acremonium strictum. J. Biol. Chem. 2008, 283:30990-30996.
13. Julsing M.K., Koulman A., Woerdenbag H.J., Quax W.J., Kayser O. Combinatorial biosynthesis of medicinal plant secondary metabolites. Biomol. Eng. 2006, 23:265-279.
14. Jungbauer A., Kaar W. Current status of technical protein refolding. J. Biotechnol. 2007, 128:587-596.
15. Jurgen B., Breitenstein A., Urlacher V., Buttner K., Lin H., Hecker M., Schweder T., Neubauer P. Quality control of inclusion bodies in E. coli. Microb. Cell Fact. 2010, 9:41.
16. Kara S., Long W.S., Berheide M., Peper S., Niemeyer B., Liese A. Influence of reaction conditions on the enantioselectivity of biocatalyzed CC bond formations under high pressure conditions. J. Biotechnol. 2011, 152:87-92.
17. Karande R., Schmid A., Buehler K. Enzyme catalysis in an aqueous/organic segment flow microreactor: ways to stabilize enzyme activity. Langmuir 2010, 26:9152-9159.
18. Kozak M. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol. Rev. 1983, 47:1-45.
19. Krainer F.W., Dietzsch C., Hajek T., Herwig C., Spadiut O., Glieder A. Recombinant protein expression in Pichia pastoris strains with an engineered methanol utilization pathway. Microb. Cell Fact. 2012, 11:22.
20. Krainer F.W., Gmeiner C., Neutsch L., Windwarder M., Pletzenauer R., Herwig C., Altmann F., Glieder A., Spadiut O. Knockout of an endogenous mannosyltransferase increases the homogeneity of glycoproteins produced in Pichia pastoris. Sci. Rep. 2013, 3:3279.
21. Laane C., Boeren S., Vos K., Veeger C. Rules for optimization of biocatalysis in organic solvents. Biotechnol. Bioeng. 1987, 30:81-87.
22. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
23. Lange, K., Poetsch, A., Schmid, A., Julsing, M.K., (2015) Enrichment and identification of δ9-Tetrahydrocannabinolic acid synthase from Pichia pastoris culture supernatants. Data in Brief. (in press).
24. Lin-Cereghino J., Wong W.W., Xiong S., Giang W., Luong L.T., Vu J., Johnson S.D., Lin-Cereghino G.P. Condensed protocol for competent cell preparation and transformation of the methylotrophic yeast Pichia pastoris. Biotechniques 2005, 38:44-48.
25. Luetz S., Giver L., Lalonde J. Engineered enzymes for chemical production. Biotechnol. Bioeng. 2008, 101:647-653.
26. Marx H., Mattanovich D., Sauer M. Overexpression of the riboflavin biosynthetic pathway in Pichia pastoris. Microb. Cell Fact. 2008, 7:23.
27. Mechoulam R. Marihuana chemistry. Science 1970, 168:1159-1166.
28. Mechoulam R., Gaoni Y. A total synthesis of Δ1-tetrahydrocannabinol, the active constituent of hashish. J. Am. Chem. Soc. 1965, 87:3273-3275.
29. Resch V., Schrittwieser J.H., Wallner S., Macheroux P., Kroutil W. Biocatalytic oxidative CC bond formation catalysed by the berberine bridge enzyme: optimal reaction conditions. Adv. Synth. Catal. 2011, 353:2377-2383.
30. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, New York. 2001.
31. Schmid A., Dordick J.S., Hauer B., Kiener A., Wubbolts M., Witholt B. Industrial biocatalysis today and tomorrow. Nature 2001, 409:258-268.
32. Serdakowski A.L., Dordick J.S. Enzyme activation for organic solvents made easy. Trends Biotechnol. 2008, 26:48-54.
33. Shoyama Y., Tamada T., Kurihara K., Takeuchi A., Taura F., Arai S., Blaber M., Morimoto S., Kuroki R. Structure and function of Δ1-tetrahydrocannabinolic acid (THCA) synthase, the enzyme controlling the psychoactivity of Cannabis sativa. J. Mol. Biol. 2012, 423:96-105.
34. Sirikantaramas S., Morimoto S., Shoyama Y., Ishikawa Y., Wada Y., Taura F. The gene controlling marijuana psychoactivity: molecular cloning and heterologous expression of Δ1-tetrahydrocannabinolic acid synthase from Cannabis sativa L. J. Biol. Chem. 2004, 279:39767-39774.
35. Sirikantaramas S., Taura F., Tanaka Y., Ishikawa Y., Morimoto S., Shoyama Y. Tetrahydrocannabinolic acid synthase, the enzyme controlling marijuana psychoactivity, is secreted into the storage cavity of the glandular trichomes. Plant Cell Physiol. 2005, 46:1578-1582.
36. Sorensen H.P., Mortensen K.K. Advanced genetic strategies for recombinant protein expression in E. coli. J. Biotechnol. 2005, 115:113-128.
37. Studier F.W., Moffatt B.A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 1986, 189:113-130.
38. Taura F., Dono E., Sirikantaramas S., Yoshimura K., Shoyama Y., Morimoto S. Production of Δ1-tetrahydrocannabinolic acid by the biosynthetic enzyme secreted from transgenic Pichia pastoris. Biochem. Biophys. Res. Commun. 2007, 361:675-680.
39. Tomaszewski B., Schmid A., Buehler K. Biocatalytic production of catechols using a high pressure tube-in-tube segmented flow microreactor. Org. Process Res. Dev. 2014, 18:1516-1526.
40. United Nations Office on Drugs and Crime (UNODC), Recommended methods forthe identification and analysis of Cannabis and Cannabis products. 2009, NewYork.
41. Wallace S., Schultz E.E., Balskus E.P. Using non-enzymatic chemistry to influence microbial metabolism. Curr. Opin. Chem. Biol. 2015, 25C:71-79.
42. Willrodt C., Karande R., Schmid A., Julsing M.K. Guiding efficient microbial synthesis of non-natural chemicals by physicochemical properties of reactants. Curr. Opin. Biotechnol. 2015, 35:52-62.
43. Winkler A., Hartner F., Kutchan T.M., Glieder A., Macheroux P. Biochemical evidence that berberine bridge enzyme belongs to a novel family of flavoproteins containing a bi-covalently attached FAD cofactor. J. Biol. Chem. 2006, 281:21276-21285.
44. Winter R.T., Fraaije M.W. Applications of flavoprotein oxidases in organic synthesis: novel reactivities that go beyond amine and alcohol oxidations. Curr. Org. Chem. 2012, 16:2542-2550.
45. Zhou J., Du, Chen G., J Novel fermentation processes for manufacturing plant natural products. Curr. Opin. Biotechnol. 2014, 25:17-23.