Optimization of yeast-based production of medicinal protoberberine alkaloids

Microbial Cell Factories

Volumn 14, Issue 1, 2015, Pages

  Galanie, Stephanie ^a   Smolke, Christina D ^b  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

Author keywords

Alkaloid; Cytochrome P450; Membrane protein; Plant natural product; Saccharomyces cerevisiae

Indexed keywords

BERBERINE; CANADINE; CYTOCHROME P450 REDUCTASE; FLAVIN DEPENDENT OXIDASE; OXIDOREDUCTASE; PROTOBERBERINE DERIVATIVE; UNCLASSIFIED DRUG; BERBERINE DERIVATIVE; CYTOCHROME P450; PROTOBERBERINE; TETRAHYDROPAPAVEROLINE;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; BATCH FERMENTATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; COPY NUMBER VARIATION; CULTURE OPTIMIZATION; ENZYME DEGRADATION; ENZYME LOCALIZATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; METABOLIC ENGINEERING; NONHUMAN; PAPAVER SOMNIFERUM; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; SYNTHETIC BIOLOGY; THALICTRUM; THALICTRUM FLAVUM; ANALOGS AND DERIVATIVES; BATCH CELL CULTURE; BIOREACTOR; BIOSYNTHESIS; CHEMISTRY; FERMENTATION; GENE DOSAGE; GENETICS; METABOLISM; PILOT STUDY; PROCEDURES;

BATCH CELL CULTURE TECHNIQUES; BERBERINE; BERBERINE ALKALOIDS; BIOREACTORS; BIOSYNTHETIC PATHWAYS; CYTOCHROME P-450 ENZYME SYSTEM; FERMENTATION; GENE DOSAGE; METABOLIC ENGINEERING; PILOT PROJECTS; SACCHAROMYCES CEREVISIAE; TETRAHYDROPAPAVEROLINE;

EID: 84941639495     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-015-0332-3     Document Type: Article

References (51)

1. Da-Cunha EV, Fechinei IM, Guedes DN, Barbosa-Filho JM, Da Silva MS. Protoberberine alkaloids. Alkaloids Chem Biol. 2005;62:1-75.
2. Qin X, Guo BT, Wan B, Fang L, Lu L, Wu L, Zang YQ, Zhang JZ. Regulation of Th1 and Th17 cell differentiation and amelioration of experimental autoimmune encephalomyelitis by natural product compound berberine. J Immunol. 2010;185:1855-63.
3. Pereira GC, Branco AF, Matos JA, Pereira SL, Parke D, Perkins EL, Serafim TL, Sardao VA, Santos MS, Moreno AJ, et al. Mitochondrially targeted effects of berberine [Natural Yellow 18, 5,6-dihydro-9,10-dimethoxybenzo(g)-1,3-benzodioxolo(5,6-a) quinolizinium] on K1735-M2 mouse melanoma cells: comparison with direct effects on isolated mitochondrial fractions. J Pharmacol Exp Ther. 2007;323:636-49.
4. Zhang Y, Li X, Zou D, Liu W, Yang J, Zhu N, Huo L, Wang M, Hong J, Wu P, et al. Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine. J Clin Endocrinol Metab. 2008;93:2559-65.
5. Paddon CJ, Keasling JD. Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development. Nat Rev Microbiol. 2014;12:355-67.
6. Leonard E, Runguphan W, O'Connor S, Prather KJ. Opportunities in metabolic engineering to facilitate scalable alkaloid production. Nat Chem Biol. 2009;5:292-300.
7. McCoy E, O'Connor SE. Natural products from plant cell cultures. Prog Drug Res. 2008;65(329):331-70.
8. Kametani T, Ihara M, Honda T. Recent chemical progress in berberine alkaloids. Heterocycles. 1976;4:483-526.
9. Schrittwieser JH, Resch V, Wallner S, Lienhart WD, Sattler JH, Resch J, Macheroux P, Kroutil W. Biocatalytic organic synthesis of optically pure (S)-scoulerine and berbine and benzylisoquinoline alkaloids. J Org Chem. 2011;76:6703-14.
10. Minami H, Kim JS, Ikezawa N, Takemura T, Katayama T, Kumagai H, Sato F. Microbial production of plant benzylisoquinoline alkaloids. Proc Natl Acad Sci USA. 2008;105:7393-8.
11. Nakagawa A, Minami H, Kim JS, Koyanagi T, Katayama T, Sato F, Kumagai H. A bacterial platform for fermentative production of plant alkaloids. Nat Commun. 2011;2:326.
12. Nakagawa A, Minami H, Kim JS, Koyanagi T, Katayama T, Sato F, Kumagai H. Bench-top fermentative production of plant benzylisoquinoline alkaloids using a bacterial platform. Bioeng Bugs. 2012;3:49-53.
13. Hawkins KM, Smolke CD. Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae. Nat Chem Biol. 2008;4:564-73.
14. Trenchard I, Smolke CD. Engineering strategies for the fermentative production of plant alkaloids in yeast. Metab Eng. 2015;30:96-104.
15. Diaz Chavez ML, Rolf M, Gesell A, Kutchan TM. Characterization of two methylenedioxy bridge-forming cytochrome P450-dependent enzymes of alkaloid formation in the Mexican prickly poppy Argemone mexicana. Arch Biochem Biophys. 2011;507:186-93.
16. Ikezawa N, Tanaka M, Nagayoshi M, Shinkyo R, Sakaki T, Inouye K, Sato F. Molecular cloning and characterization of CYP719, a methylenedioxy bridge-forming enzyme that belongs to a novel P450 family, from cultured Coptis japonica cells. J Biol Chem. 2003;278:38557-65.
17. Sandig G, Kargel E, Menzel R, Vogel F, Zimmer T, Schunck WH. Regulation of endoplasmic reticulum biogenesis in response to cytochrome P450 overproduction. Drug Metab Rev. 1999;31:393-410.
18. Thodey K, Galanie S, Smolke CD. A microbial biomanufacturing platform for natural and semisynthetic opioids. Nat Chem Biol. 2014;10:837-44.
19. Desgagne-Penix I, Khan MF, Schriemer DC, Cram D, Nowak J, Facchini PJ. Integration of deep transcriptome and proteome analyses reveals the components of alkaloid metabolism in opium poppy cell cultures. BMC Plant Biol. 2010;10:252.
20. Gesell A, Chavez ML, Kramell R, Piotrowski M, Macheroux P, Kutchan TM. Heterologous expression of two FAD-dependent oxidases with (S)-tetrahydroprotoberberine oxidase activity from Argemone mexicana and Berberis wilsoniae in insect cells. Planta. 2011;233:1185-97.
21. Fossati E, Ekins A, Narcross L, Zhu Y, Falgueyret JP, Beaudoin GA, Facchini PJ, Martin VJ. Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae. Nat Commun. 2014;5:3283.
22. Paulsen J, Yahyazadeh M, Hansel S, Kleinwachter M, Ibrom K, Selmar D. 13,14-Dihydrocoptisine-the genuine alkaloid from Chelidonium majus. Phytochemistry. 2015;111:149-53.
23. Jones EW. Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 1991;194:428-53.
24. Nevoigt E, Kohnke J, Fischer CR, Alper H, Stahl U, Stephanopoulos G. Engineering of promoter replacement cassettes for fine-tuning of gene expression in Saccharomyces cerevisiae. Appl Environ Microbiol. 2006;72:5266-73.
25. Steffens P, Nagakura N, Zenk MH. Purification and characterization of the berberine bridge enzyme from Berberis beaniana cell cultures. Phytochemistry. 1985;24:2577-83.
26. Amann M, Nagakura N, Zenk MH. Purification and properties of (S)-tetrahydroprotoberberine oxidase from suspension-cultured cells of Berberis wilsoniae. Eur J Biochem. 1988;175:17-25.
27. Sato F, Tsujita T, Katagiri Y, Yoshida S, Yamada Y. Purification and characterization of S-adenosyl-l-methionine-norcoclaurine 6-O-methyltransferase from cultured Coptis japonica cells. Eur J Biochem. 1994;225:125-31.
28. Brown S, Clastre M, Courdavault V, O'Connor SE. De novo production of the plant-derived alkaloid strictosidine in yeast. Proc Natl Acad Sci USA. 2015;112:3205-10.
29. Ideker T, Thorsson V, Ranish JA, Christmas R, Buhler J, Eng JK, Bumgarner R, Goodlett DR, Aebersold R, Hood L. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science. 2001;292:929-34.
30. Hancock RD, Galpin JR, Viola R. Biosynthesis of l-ascorbic acid (vitamin C) by Saccharomyces cerevisiae. FEMS Microbiol Lett. 2000;186:245-50.
31. Nakagawa A, Matsuzaki C, Matsumura E, Koyanagi T, Katayama T, Yamamoto K, Sato F, Kumagai H, Minami H. (R,S)-tetrahydropapaveroline production by stepwise fermentation using engineered Escherichia coli. Sci Rep. 2014;4:6695.
32. Kleman GL, Strohl WR. High cell density and high-productivity microbial fermentation. Curr Opin Biotechnol. 1992;3:93-8.
33. Goldstein WE, Ingle MB, Lasure L. Product cost analysis. In: Staba EJ, editor. Plant tissue culture as a source of biochemicals. Boca Raton, FL: CRC Press; 1980. p. 191-234.
34. Matsubara K, Kitani S, Yoshioka T, Morimoto T, Fujita Y, Yamada Y. High density culture of Coptis japonica cells increases berberine production. J Chem Technol Biotechnol. 2007;46:61-9.
35. Hatch RT, Hardy R. Microorganisms as producers of feedstock chemicals. In: Marx JL, editor. A revolution in biotechnology. Cambridge: Cambridge University Press; 1989. p. 28-41.
36. Trenchard IJ, Siddiqui MS, Thodey K, Smolke CD. De novo production of the key branch point benzylisoquinoline alkaloid reticuline in yeast. Metab Eng. 2015;31:74-83.
37. DeLoache WC, Russ ZN, Narcross L, Gonzales AM, Martin VJ, Dueber JE. An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose. Nat Chem Biol. 2015;11:465-71.
38. Tabata H. Production of paclitaxel and the related taxanes by cell suspension cultures of Taxus species. Curr Drug Targets. 2006;7:453-61.
39. Martens JH, Barg H, Warren MJ, Jahn D. Microbial production of vitamin B12. Appl Microbiol Biotechnol. 2002;58:275-85.
40. Kreis W, Reinhard E. The production of secondary metabolites by plant cells cultivated in bioreactors. Planta Med. 1989;55:409-16.
41. Mahmoudian M, Rahimi-Moghaddam P. The anti-cancer activity of noscapine: a review. Recent Pat Anticancer Drug Discov. 2009;4:92-7.
42. Alberti S, Gitler AD, Lindquist S. A suite of gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast. 2007;24:913-9.
43. Gietz RD, Schiestl RH. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007;2:31-4.
44. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6:343-5.
45. Chao G, Lau WL, Hackel BJ, Sazinsky SL, Lippow SM, Wittrup KD. Isolating and engineering human antibodies using yeast surface display. Nat Protoc. 2006;1:755-68.
46. Sadowski I, Su TC, Parent J. Disintegrator vectors for single-copy yeast chromosomal integration. Yeast. 2007;24:447-55.
47. Hegemann JH, Guldener U, Kohler GJ. Gene disruption in the budding yeast Saccharomyces cerevisiae. Methods Mol Biol. 2006;313:129-44.
48. Kwiatkowski TJ Jr, Zoghbi HY, Ledbetter SA, Ellison KA, Chinault AC. Rapid identification of yeast artificial chromosome clones by matrix pooling and crude lysate PCR. Nucleic Acids Res. 1990;18:7191-2.
49. Schmidt J, Boettcher C, Kuhnt C, Kutchan TM, Zenk MH. Poppy alkaloid profiling by electrospray tandem mass spectrometry and electrospray FT-ICR mass spectrometry after [ring-13C6]-tyramine feeding. Phytochemistry. 2007;68:189-202.
50. Sikorski RS, Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989;122:19-27.
51. Mikkelsen MD, Buron LD, Salomonsen B, Olsen CE, Hansen BG, Mortensen UH, Halkier BA. Microbial production of indolylglucosinolate through engineering of a multi-gene pathway in a versatile yeast expression platform. Metab Eng. 2012;14:104-11.