Complete biosynthesis of noscapine and halogenated alkaloids in yeast

Proceedings of the National Academy of Sciences of the United States of America

Volumn 115, Issue 17, 2018, Pages E3922-E3931

  Li, Yanran ^a   Li, Sijin ^b   Thodey, Kate ^c   Trenchard, Isis ^c   Cravens, Aaron ^b   Smolke, Christina D ^b,d  

^a University of California Riverside   (United States)

^b Stanford University   (United States)

^c Antheia Inc   (United States)

^d CHAN ZUCKERBERG BIOHUB   (United States)

Author keywords

Benzylisoquinoline alkaloids; metabolic engineering; plant alkaloids; Saccharomyces cerevisiae

Indexed keywords

HALOGENATED HYDROCARBON; NOSCAPINE;

GENETICS; METABOLIC ENGINEERING; METABOLISM; SACCHAROMYCES CEREVISIAE;

HYDROCARBONS, HALOGENATED; METABOLIC ENGINEERING; NOSCAPINE; SACCHAROMYCES CEREVISIAE;

EID: 85045924977     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1721469115     Document Type: Article

References (40)

1. Ye K, et al. (1998) Opium alkaloid noscapine is an antitumor agent that arrests metaphase and induces apoptosis in dividing cells. Proc Natl Acad Sci USA 95: 1601–1606.
2. Barken I, Geller J, Rogosnitzky M (2008) Noscapine inhibits human prostate cancer progression and metastasis in a mouse model. Anticancer Res 28:3701–3704.
3. Joshi HC, Salil A, Bughani U, Naik P (2010) Noscapinoids: A new class of anticancer drugs demand biotechnological intervention. Medicinal Plant Biotechnology (Centre for Agriculture and Bioscience International South Asia Edition, Wallingford, UK), pp 303–320.
4. Mahmoudian M, Rahimi-Moghaddam P (2009) The anti-cancer activity of noscapine: A review. Recent Patents Anticancer Drug Discov 4:92–97.
5. DeBono A, Capuano B, Scammells PJ (2015) Progress toward the development of noscapine and derivatives as anticancer agents. J Med Chem 58:5699–5727.
6. Ke Y, et al. (2000) Noscapine inhibits tumor growth with little toxicity to normal tissues or inhibition of immune responses. Cancer Immunol Immunother 49:217–225.
7. Pushpangadan P, George V, Singh SP (2012) Poppy. Handbook of Herbs and Spices, ed Peter KV (Woodhead Publishing, Cambridge, England), A2, pp 437–448.
8. Bradsher K (July 20, 2014) Shake-up on opium island. New York Times. Available at https://www.nytimes.com/2014/07/20/business/international/tasmania-big-supplier-todrug-companies-faces-changes.html. Accessed on March 19, 2018.
9. Chen X, Dang TT, Facchini PJ (2015) Noscapine comes of age. Phytochemistry 111: 7–13.
10. Brown S, Clastre M, Courdavault V, O’Connor SE (2015) De novo production of the plant-derived alkaloid strictosidine in yeast. Proc Natl Acad Sci USA 112:3205–3210.
11. Galanie S, Thodey K, Trenchard IJ, Filsinger Interrante M, Smolke CD (2015) Complete biosynthesis of opioids in yeast. Science 349:1095–1100.
12. Winzer T, et al. (2012) A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336:1704–1708.
13. Dang T-TT, Chen X, Facchini PJ (2015) Acetylation serves as a protective group in noscapine biosynthesis in opium poppy. Nat Chem Biol 11:104–106.
14. Li Y, Smolke CD (2016) Engineering biosynthesis of the anticancer alkaloid noscapine in yeast. Nat Commun 7:12137.
15. Trenchard IJ, Siddiqui MS, Thodey K, Smolke CD (2015) De novo production of the key branch point benzylisoquinoline alkaloid reticuline in yeast. Metab Eng 31:74–83.
16. Galanie S, Smolke CD (2015) Optimization of yeast-based production of medicinal protoberberine alkaloids. Microb Cell Fact 14:144.
17. Urlacher VB, Girhard M (2012) Cytochrome P450 monooxygenases: An update on perspectives for synthetic application. Trends Biotechnol 30:26–36.
18. Nogae I, Johnston M (1990) Isolation and characterization of the ZWF1 gene of Saccharomyces cerevisiae, encoding glucose-6-phosphate dehydrogenase. Gene 96: 161–169.
19. Li J, Lee EJ, Chang L, Facchini PJ (2016) Genes encoding norcoclaurine synthase occur as tandem fusions in the Papaveraceae. Sci Rep 6:39256.
20. Ryan OW, Poddar S, Cate JH (2016) CRISPR-Cas9 genome engineering in Saccharomyces cerevisiae cells. Cold Spring Harb Protoc 2016:pdb.prot086827.
21. Wu Y, et al. (2015) Improvement of NADPH-dependent P450-mediated bio-transformation of 7α,15α-diOH-DHEA from DHEA by a dual cosubstrate-coupled system. Steroids 101:15–20.
22. Kayikci Ö, Nielsen J (2015) Glucose repression in Saccharomyces cerevisiae. FEMS Yeast Res 15:fov068.
23. Baneyx F, Mujacic M (2004) Recombinant protein folding and misfolding in Escherichia coli. Nat Biotechnol 22:1399–1408.
24. Marques WL, Raghavendran V, Stambuk BU, Gombert AK (2016) Sucrose and Saccharomyces cerevisiae: A relationship most sweet. FEMS Yeast Res 16:fov107.
25. Bolen DW (2001) Protein stabilization by naturally occurring osmolytes. Protein Structure, Stability, and Folding, ed Murphy KP (Humana Press, Totowa, NJ), pp 17–36.
26. Gekko K, Timasheff SN (1981) Mechanism of protein stabilization by glycerol: Preferential hydration in glycerol-water mixtures. Biochemistry 20:4667–4676.
27. Crowe JH, et al. (1988) Interactions of sugars with membranes. Biochim Biophys Acta 947:367–384.
28. Crowe LM, Mouradian R, Crowe JH, Jackson SA, Womersley C (1984) Effects of carbohydrates on membrane stability at low water activities. Biochim Biophys Acta 769: 141–150.
29. Sato S, Ward CL, Krouse ME, Wine JJ, Kopito RR (1996) Glycerol reverses the misfolding phenotype of the misfolding phenotype of the most common cystic fibrosis mutation. Mol Biol Cell 7:1534.
30. Meng F, Park Y, Zhou H (2001) Role of proline, glycerol, and heparin as protein folding aids during refolding of rabbit muscle creatine kinase. Int J Biochem Cell Biol 33:701–709.
31. Perlmutter DH (2002) Chemical chaperones: A pharmacological strategy for disorders of protein folding and trafficking. Pediatr Res 52:832–836.
32. Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591.
33. Costenoble R, Valadi H, Gustafsson L, Niklasson C, Franzén CJ (2000) Microaerobic glycerol formation in Saccharomyces cerevisiae. Yeast 16:1483–1495.
34. Carey JS, Laffan D, Thomson C, Williams MT (2006) Analysis of the reactions used for the preparation of drug candidate molecules. Org Biomol Chem 4: 2337–2347.
35. Tomar V, Kukreti S, Prakash S, Madan J, Chandra R (2017) Noscapine and its analogs as chemotherapeutic agent: Current updates. Curr Top Med Chem 17: 174–188.
36. Borodina I, Nielsen J (2014) Advances in metabolic engineering of yeast Saccharomyces cerevisiae for production of chemicals. Biotechnol J 9:609–620.
37. Alberti S, Gitler AD, Lindquist S (2007) A suite of gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24:913–919.
38. Siddiqui MS, Choksi A, Smolke CD (2014) A system for multilocus chromosomal integration and transformation-free selection marker rescue. FEMS Yeast Res 14: 1171–1185.
39. Shao Z, Zhao H, Zhao H (2009) DNA assembler, an in vivo genetic method for rapid construction of biochemical pathways. Nucleic Acids Res 37:e16.
40. Güldener U, Heck S, Fielder T, Beinhauer J, Hegemann JH (1996) A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24: 2519–2524.