Pterin-Dependent Mono-oxidation for the Microbial Synthesis of a Modified Monoterpene Indole Alkaloid

ACS Synthetic Biology

Volumn 4, Issue 12, 2015, Pages 1295-1307

  Ehrenworth, A M ^a   Sarria, S ^a   Peralta Yahya, P ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b Georgia Institute of Technology   (United States)

Author keywords

alkaloids; biogenic amines; biosynthesis; tetrahydrobiopterin; yeast

Indexed keywords

10 HYDROXYSTRICTOSIDINE; 5 HYDROXYTRYPTOPHAN; ANTIMALARIAL AGENT; ANTINEOPLASTIC AGENT; INDOLE ALKALOID; LEVODOPA; MONOTERPENE INDOLE ALKALOID; PTERIN; SECOLOGANIN; SEROTONIN; STRICTOSIDINE; TERPENE; TETRAHYDROBIOPTERIN; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG; PTERIN DERIVATIVE;

ARTICLE; BIOSYNTHESIS; DECARBOXYLATION; DRUG SYNTHESIS; HYDROXYLATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; GENETICS; METABOLIC ENGINEERING; METABOLISM; OXIDATION REDUCTION REACTION; PROCEDURES;

INDOLE ALKALOIDS; METABOLIC ENGINEERING; OXIDATION-REDUCTION; PTERINS; SACCHAROMYCES CEREVISIAE;

EID: 84952837977     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.5b00025     Document Type: Article

References (78)

1. Schafer, H. and Wink, M. (2009) Medicinally important secondary metabolites in recombinant microorganisms or plants: progress in alkaloid biosynthesis Biotechnol. J. 4, 1684-1703 10.1002/biot.200900229
2. Minami, H. (2013) Fermentative Production of Plant Benzylisoquinoline Alkaloids in Microbes Biosci., Biotechnol., Biochem. 77, 1617-1622 10.1271/bbb.130106
3. Yang, L. Q. and Stockigt, J. (2010) Trends for diverse production strategies of plant medicinal alkaloids Nat. Prod. Rep. 27, 1469-1479 10.1039/c005378c
4. Hagel, J. M. and Facchini, P. J. (2013) Benzylisoquinoline Alkaloid Metabolism: A Century of Discovery and a Brave New World Plant Cell Physiol. 54, 647-672 10.1093/pcp/pct020
5. Leonard, E., Runguphan, W., Oconnor, S., and Prather, K. J. (2009) Opportunities in metabolic engineering to facilitate scalable alkaloid production Nat. Chem. Biol. 5, 292-300 10.1038/nchembio.160
6. Winter, J. M. and Tang, Y. (2012) Synthetic biological approaches to natural product biosynthesis Curr. Opin. Biotechnol. 23, 736-743 10.1016/j.copbio.2011.12.016
7. Chemler, J. A. and Koffas, M. A. (2008) Metabolic engineering for plant natural product biosynthesis in microbes Curr. Opin. Biotechnol. 19, 597-605 10.1016/j.copbio.2008.10.011
8. Kuboyama, T., Yokoshima, S., Tokuyama, H., and Fukuyama, T. (2004) Stereocontrolled total synthesis of (+)-vincristine Proc. Natl. Acad. Sci. U. S. A. 101, 11966-11970 10.1073/pnas.0401323101
9. Murata, J., Roepke, J., Gordon, H., and De Luca, V. (2008) The leaf epidermome of Catharanthus roseus reveals its biochemical specialization Plant Cell 20, 524-542 10.1105/tpc.107.056630
10. Sato, F., Hashimoto, T., Hachiya, A., Tamura, K., Choi, K. B., Morishige, T., Fujimoto, H., and Yamada, Y. (2001) Metabolic engineering of plant alkaloid biosynthesis Proc. Natl. Acad. Sci. U. S. A. 98, 367-372 10.1073/pnas.98.1.367
11. Frick, S., Kramell, R., and Kutchan, T. M. (2007) Metabolic engineering with a morphine biosynthetic P450 in opium poppy surpasses breeding Metab. Eng. 9, 169-176 10.1016/j.ymben.2006.10.004
12. Allen, R. S., Millgate, A. G., Chitty, J. A., Thisleton, J., Miller, J. A. C., Fist, A. J., Gerlach, W. L., and Larkin, P. J. (2004) RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy Nat. Biotechnol. 22, 1559-1566 10.1038/nbt1033
13. Glenn, W. S., Runguphan, W., and Oconnor, S. E. (2013) Recent progress in the metabolic engineering of alkaloids in plant systems Curr. Opin. Biotechnol. 24, 354-365 10.1016/j.copbio.2012.08.003
14. Runguphan, W. and Oconnor, S. E. (2009) Metabolic reprogramming of periwinkle plant culture Nat. Chem. Biol. 5, 151-153 10.1038/nchembio.141
15. Runguphan, W., Qu, X. D., and Oconnor, S. E. (2010) Integrating carbon-halogen bond formation into medicinal plant metabolism Nature 468, 461-464 10.1038/nature09524
16. Glenn, W. S., Nims, E., and Oconnor, S. E. (2011) Reengineering a Tryptophan Halogenase To Preferentially Chlorinate a Direct Alkaloid Precursor J. Am. Chem. Soc. 133, 19346-19349 10.1021/ja2089348
17. Harvey, A. L. (2008) Natural products in drug discovery Drug Discovery Today 13, 894-901 10.1016/j.drudis.2008.07.004
18. Dewick, P. M. Medicinal Natural Products: A Biosynthetic Approach, 2 nd ed.; John Wiley & Sons Ltd.: 2002.
19. Hawkins, K. M. and Smolke, C. D. (2008) Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae Nat. Chem. Biol. 4, 564-573 10.1038/nchembio.105
20. Minami, H., Kim, J. S., Ikezawa, N., Takemura, T., Katayama, T., Kumagai, H., and Sato, F. (2008) Microbial production of plant benzylisoquinoline alkaloids Proc. Natl. Acad. Sci. U. S. A. 105, 7393-7398 10.1073/pnas.0802981105
21. Nakagawa, A., Minami, H., Kim, J. S., Koyanagi, T., Katayama, T., Sato, F., and Kumagai, H. (2011) A bacterial platform for fermentative production of plant alkaloids Nat. Commun. 2, 326 10.1038/ncomms1327
22. Fossati, E., Ekins, A., Narcross, L., Zhu, Y., Falgueyret, J. P., Beaudoin, G. A. W., Facchini, P. J., and Martin, V. J. J. (2014) Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae Nat. Commun. 5, 3283 10.1038/ncomms4283
23. Thodey, K., Galanie, S., and Smolke, C. D. (2014) A microbial biomanufacturing platform for natural and semisynthetic opioids Nat. Chem. Biol. 10, 837-844 10.1038/nchembio.1613
24. Fossati, E., Narcross, L., Ekins, A., Falgueyret, J. P., and Martin, V. J. J. Synthesis of Morphinan Alkaloids in Saccharomyces cerevisiae. PloS One 2015, 10, DOI: 10.1371/journal.pone.0124459.
25. Nakagawa, A., Matsuzaki, C., Matsumura, E., Koyanagi, T., Katayama, T., Yamamoto, K., Sato, F., Kumagai, H., and Minami, H. (R, S)-Tetrahydropapaveroline production by stepwise fermentation using engineered Escherichia coli. Sci. Rep. 2014, 4, 6695 10.1038/srep06695.
26. Hernandez-Romero, D., Sanchez-Amat, A., and Solano, F. (2006) A tyrosinase with an abnormally high tyrosine hydroxylase/dopa oxidase ratio-Role of the seventh histidine and accessibility to the active site FEBS J. 273, 257-270 10.1111/j.1742-4658.2005.05038.x
27. Luetke-Eversloh, T., Santos, C. N. S., and Stephanopoulos, G. (2007) Perspectives of biotechnological production of L-tyrosine and its applications Appl. Microbiol. Biotechnol. 77, 751-762 10.1007/s00253-007-1243-y
28. Land, E. J., Ramsden, C. A., and Riley, P. A. (2003) Tyrosinase autoactivation and the chemistry of ortho-quinone amines Acc. Chem. Res. 36, 300-308 10.1021/ar020062p
29. DeLoache, W. C., Russ, Z. N., Narcross, L., Gonzales, A. M., Martin, V. J., and Dueber, J. E. (2015) An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose Nat. Chem. Biol. 11, 465 10.1038/nchembio.1816
30. Sun, X., Lin, Y., Yuan, Q., and Yan, Y. (2015) Precursor-Directed Biosynthesis of 5-Hydroxytryptophan Using Metabolically Engineered E. coli ACS Synth. Biol. 4, 554-558 10.1021/sb500303q
31. Lin, Y. H., Sun, X. X., Yuan, Q. P., and Yan, Y. J. (2014) Engineering Bacterial Phenylalanine 4-Hydroxylase for Microbial Synthesis of Human Neurotransmitter Precursor 5-Hydroxytryptophan ACS Synth. Biol. 3, 497-505 10.1021/sb5002505
32. Fitzpatrick, P. F. (1999) Tetrahydropterin-dependent amino acid hydroxylases Annu. Rev. Biochem. 68, 355-381 10.1146/annurev.biochem.68.1.355
33. Werner-Felmayer, G., Golderer, G., and Werner, E. R. (2002) Tetrahydrobiopterin biosynthesis, utilization and pharmacological effects Curr. Drug Metab. 3, 159-173 10.2174/1389200024605073
34. Yamamoto, K., Kataoka, E., Miyamoto, N., Furukawa, K., Ohsuye, K., and Yabuta, M. (2003) Genetic engineering of Escherichia coli for production of tetrahydrobiopterin Metab. Eng. 5, 246-254 10.1016/S1096-7176(03)00046-6
35. Satoh, Y., Tajima, K., Munekata, M., Keasling, J. D., and Lee, T. S. (2012) Engineering of L-tyrosine oxidation in Escherichia coli and microbial production of hydroxytyrosol Metab. Eng. 14, 603-610 10.1016/j.ymben.2012.08.002
36. Leiros, H. K. S., Pey, A. L., Innselset, M., Moe, E., Leiros, I., Steen, I. H., and Martinez, A. (2007) Structure of phenylalanine hydroxylase from Colwellia psychrerythraea 34H, a monomeric cold active enzyme with local flexibility around the active site and high overall stability J. Biol. Chem. 282, 21973-21986 10.1074/jbc.M610174200
37. Siddiqui, M. S., Thodey, K., Trenchard, I., and Smolke, C. D. (2012) Advancing secondary metabolite biosynthesis in yeast with synthetic biology tools FEMS Yeast Res. 12, 144-170 10.1111/j.1567-1364.2011.00774.x
38. Chang, M. C. Y., Eachus, R. A., Trieu, W., Ro, D. K., and Keasling, J. D. (2007) Engineering Escherichia coli for production of functionalized terpenoids using plant P450s Nat. Chem. Biol. 3, 274-277 10.1038/nchembio875
39. Miki, Y. and Asano, Y. (2014) Biosynthetic pathway for the cyanide-free production of phenylacetonitrile in Escherichia coli by utilizing plant cytochrome P450 79A2 and bacterial aldoxime dehydratase Appl. Environ. Microbiol. 80, 6828-6836 10.1128/AEM.01623-14
40. Barnes, H. J., Arlotto, M. P., and Waterman, M. R. (1991) Expression and Enzymatic-Activity of Recombinant Cytochrome-P450 17-Alpha-Hydroxylase in Escherichia-Coli Proc. Natl. Acad. Sci. U. S. A. 88, 5597-5601 10.1073/pnas.88.13.5597
41. Hong, K. K. and Nielsen, J. (2012) Metabolic engineering of Saccharomyces cerevisiae: a key cell factory platform for future biorefineries Cell. Mol. Life Sci. 69, 2671-2690 10.1007/s00018-012-0945-1
42. Peralta-Yahya, P. P., Zhang, F. Z., del Cardayre, S. B., and Keasling, J. D. (2012) Microbial engineering for the production of advanced biofuels Nature 488, 320-328 10.1038/nature11478
43. Da Silva, N. A. and Srikrishnan, S. (2012) Introduction and expression of genes for metabolic engineering applications in Saccharomyces cerevisiae FEMS Yeast Res. 12, 197-214 10.1111/j.1567-1364.2011.00769.x
44. Oconnor, S. E. and Maresh, J. J. (2006) Chemistry and biology of monoterpene indole alkaloid biosynthesis Nat. Prod. Rep. 23, 532-547 10.1039/b512615k
45. Silvestrini, A., Pasqua, G., Botta, B., Monacelli, B., van der Heijden, R., and Verpoorte, R. (2002) Effects of alkaloid precursor feeding on a Camptotheca acuminata cell line Plant Physiol. Biochem. 40, 749-753 10.1016/S0981-9428(02)01436-5
46. Friedrich, A., Brase, S., and Oconnor, S. E. (2009) Synthesis of 4-, 5-, 6-, and 7-azidotryptamines Tetrahedron Lett. 50, 75-76 10.1016/j.tetlet.2008.10.091
47. Davis, M. D., Kaufman, S., and Milstien, S. (1988) The auto-oxidation of tetrahydrobiopterin Eur. J. Biochem. 173, 345-351 10.1111/j.1432-1033.1988.tb14004.x
48. Thony, B., Auerbach, G., and Blau, N. (2000) Tetrahydrobiopterin biosynthesis, regeneration and functions Biochem. J. 347, 1-16 10.1042/0264-6021:3470001
49. Wang, H. C., Yang, B., Hao, G. F., Feng, Y., Chen, H. Q., Feng, L., Zhao, J. X., Zhang, H., Chen, Y. Q., Wang, L., and Chen, W. (2011) Biochemical characterization of the tetrahydrobiopterin synthesis pathway in the oleaginous fungus Mortierella alpina Microbiology 157, 3059-3070 10.1099/mic.0.051847-0
50. Yim, J. J. and Brown, G. M. (1976) Characteristics of Guanosine Triphosphate Cyclohydrolase-I Purified from Escherichia-Coli J. Biol. Chem. 251, 5087-5094
51. Schoedon, G., Redweik, U., Frank, G., Cotton, R. G. H., and Blau, N. (1992) Allosteric Characteristics of Gtp Cyclohydrolase-I from Escherichia-Coli Eur. J. Biochem. 210, 561-568 10.1111/j.1432-1033.1992.tb17455.x
52. Mancini, R., Saracino, F., Buscemi, G., Fischer, M., Schramek, N., Bracher, A., Bacher, A., Gutlich, M., and Carbone, M. L. A. (1999) Complementation of the fol2 deletion in Saccharomyces cerevisiae by human and Escherichia coli genes encoding GTP cyclohydrolase I Biochem. Biophys. Res. Commun. 255, 521-527 10.1006/bbrc.1998.9951
53. Blau, N. and Niederwieser, A. (1986) The application of 8-aminoguanosine triphosphate, a new inhibitor of GTP cyclohydrolase I, to the purification of the enzyme from human liver Biochim. Biophys. Acta, Gen. Subj. 880, 26-31 10.1016/0304-4165(86)90115-7
54. Hasler, T. and Curtius, H. C. (1989) Purification and characterization of 6-pyruvoyl tetrahydropterin synthase from salmon liver Eur. J. Biochem. 180, 205-211 10.1111/j.1432-1033.1989.tb14635.x
55. Burgisser, D. M., Thony, B., Redweik, U., Hess, D., Heizmann, C. W., Huber, R., and Nar, H. (1995) 6-Pyruvoyl Tetrahydropterin Synthase, an Enzyme with a Novel Type of Active-Site Involving Both Zinc-Binding and an Intersubunit Catalytic Triad Motif-Site-Directed Mutagenesis of the Proposed Active-Center, Characterization of the Metal-Binding Site and Modeling of Substrate-Binding J. Mol. Biol. 253, 358-369 10.1006/jmbi.1995.0558
56. Ploom, T., Thony, B., Yim, J., Lee, S., Nar, H., Leimbacher, W., Richardson, J., Huber, R., and Auerbach, G. (1999) Crystallographic and kinetic investigations on the mechanism of 6-pyruvoyl tetrahydropterin synthase J. Mol. Biol. 286, 851-860 10.1006/jmbi.1998.2511
57. Glick, B. R. (1995) Metabolic Load and Heterologous Gene-Expression Biotechnol. Adv. 13, 247-261 10.1016/0734-9750(95)00004-A
58. Jones, K. L., Kim, S. W., and Keasling, J. D. (2000) Low-Copy Plasmids can Perform as Well as or Better Than High-Copy Plasmids for Metabolic Engineering of Bacteria Metab. Eng. 2, 328-338 10.1006/mben.2000.0161
59. Carkaci-Salli, N., Flanagan, J. M., Martz, M. K., Salli, U., Walther, D. J., Bader, M., and Vrana, K. E. (2006) Functional domains of human tryptophan hydroxylase 2 (hTPH2) J. Biol. Chem. 281, 28105-28112 10.1074/jbc.M602817200
60. Brown, S., Clastre, M., Courdavault, V., and Oconnor, S. E. (2015) De novo production of the plant-derived alkaloid strictosidine in yeast Proc. Natl. Acad. Sci. U. S. A. 112, 3205-3210 10.1073/pnas.1423555112
61. Bernhardt, P., Usera, A. R., and Oconnor, S. E. (2010) Biocatalytic asymmetric formation of tetrahydro-beta-carbolines Tetrahedron Lett. 51, 4400-4402 10.1016/j.tetlet.2010.06.075
62. Geerlings, A., Redondo, F. J., Contin, A., Memelink, J., van der Heijden, R., and Verpoorte, R. (2001) Biotransformation of tryptamine and secologanin into plant terpenoid indole alkaloids by transgenic yeast Appl. Microbiol. Biotechnol. 56, 420-424 10.1007/s002530100663
63. Battersby, A. R., Burnett, A. R., and Parsons, P. G. (1969) Alkaloid Biosynthesis Part XV. Partial Synthesis and Isolation of Vincoside and Isovincoside-Biosynthesis of 3 Major Classes of Indole Alkaloids from Vincoside J. Chem. Soc. C 1193-1200 10.1039/j39690001193
64. Maresh, J. J., Giddings, L. A., Friedrich, A., Loris, E. A., Panjikar, S., Trout, B. L., Stockigt, J., Peters, B., and Oconnor, S. E. (2008) Strictosidine synthase: mechanism of a Pictet-Spengler catalyzing enzyme J. Am. Chem. Soc. 130, 710-723 10.1021/ja077190z
65. McCoy, E., Galan, M. C., and Oconnor, S. E. (2006) Substrate specificity of strictosidine synthase Bioorg. Med. Chem. Lett. 16, 2475-2478 10.1016/j.bmcl.2006.01.098
66. Miettinen, K., Dong, L. M., Navrot, N., Schneider, T., Burlat, V., Pollier, J., Woittiez, L., van der Krol, S., Lugan, R., Ilc, T., Verpoorte, R., Oksman-Caldentey, K. M., Martinoia, E., Bouwmeester, H., Goossens, A., Memelink, J., and Werck-Reichhart, D. (2014) The seco-iridoid pathway from Catharanthus roseus Nat. Commun. 5, 3606 10.1038/ncomms4606
67. Yerkes, N., Wu, J. X., McCoy, E., Galan, M. C., Chen, S., and Oconnor, S. E. (2008) Substrate specificity and diastereoselectivity of strictosidine glucosidase, a key enzyme in monoterpene indole alkaloid biosynthesis Bioorg. Med. Chem. Lett. 18, 3095-3098 10.1016/j.bmcl.2007.11.063
68. Bernhardt, P., Yerkes, N., and Oconnor, S. E. (2009) Bypassing stereoselectivity in the early steps of alkaloid biosynthesis Org. Biomol. Chem. 7, 4166-4168 10.1039/b916027m
69. Dittrich, H. and Kutchan, T. M. (1991) Molecular clonin, expression, and induction of berberine bridge enzyme, and enzyme essential to the formation of benzyophenanthridine alkaloids in the response of plants to pathogenic attack Proc. Natl. Acad. Sci. U. S. A. 88, 9969-9973 10.1073/pnas.88.22.9969
70. Luttik, M. A. H., Vuralhan, Z., Suir, E., Braus, G. H., Pronk, J. T., and Daran, J. M. (2008) Alleviation of feedback inhibition in Saccharomyces cerevisiae aromatic amino acid biosynthesis: Quantification of metabolic impact Metab. Eng. 10, 141-153 10.1016/j.ymben.2008.02.002
71. Gold, N. D., Gowen, C. M., Lussier, F. X., Cautha, S. C., Mahadevan, R., and Martin, V. J. (2015) Metabolic engineering of a tyrosine-overproducing yeast platform using targeted metabolomics Microb. Cell Fact. 14, 73 10.1186/s12934-015-0252-2
72. Sarria, S., Wong, B., Martin, H. G., Keasling, J. D., and Peralta-Yahya, P. (2014) Microbial Synthesis of Pinene ACS Synth. Biol. 3, 466-475 10.1021/sb4001382
73. Mukherjee, K., Bhattacharyya, S., and Peralta-Yahya, P. (2015) GPCR-Based Chemical Biosensors for Medium-Chain Fatty Acids ACS Synth. Biol. 150530121000007 10.1021/sb500365m
74. Belanger-Quintana, A., Burlina, A., Harding, C. O., and Muntau, A. C. (2011) Up to date knowledge on different treatment strategies for phenylketonuria Mol. Genet. Metab. 104, S19-S25 10.1016/j.ymgme.2011.08.009
75. Byerley, W. F., Judd, L. L., Reimherr, F. W., and Grosser, B. I. (1987) 5-Hydroxytryptophan-a Review of Its Antidepressant Efficacy and Adverse-Effects J. Clin. Psychopharmacol. 7, 127-137 10.1097/00004714-198706000-00002
76. Birdsall, T. C. (1998) 5-Hydroxytryptophan: A clinically-effective serotonin precursor Alt. Med. Rev. 3, 271-280
77. Bloom, F. and Kupfer, D. Psychopharmacology, the Fourth Generation of Progress; Raven Press: 1995; pp 933-944.
78. Connolly, B. S. and Lang, A. E. (2014) Pharmacological Treatment of Parkinson Disease A Review JAMA, J. Am. Med. Assoc. 311, 1670-1683 10.1001/jama.2014.3654