Searching for artemisinin production improvement in plants and Microorganisms

Current Pharmaceutical Biotechnology

Volumn 12, Issue 11, 2011, Pages 1743-1751

  Barbacka, Katarzyna ^a   Baer Dubowska, Wanda ^a  

^a POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

ACTs; Artemisinin; Biosynthesis; Metabolic engineering

Indexed keywords

1 DEOXY DEXTRO XYLULOSE 5 PHOSPHATE REDUCTOISOMERASE; 1 DEOXY DEXTRO XYLULOSE 5 PHOSPHATE SYNTHASE; AMORPHA 4,11 DIENE HYDROXYLASE; AMORPHADIENE OXIDASE; ARTEMISINIC ALDEHYDE DELTA11(13) REDUCTASE; ARTEMISININ; ARTEMISININ DERIVATIVE; CYTOCHROME P450; GIBBERELLIC ACID; HYDROXYL 2 METHYL 2 BUTENYL 4-PHOSPHATE SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; ISOPENTENYL DIPHOSPHATE DELTA ISOMERASE; ISOPENTENYL DIPHOSPHATE: DIMETHYLALLYL DIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ANTIMALARIAL ACTIVITY; ARTEMISIA ANNUA; BIOREACTOR; BIOSYNTHESIS; CELL SUSPENSION; CHEMICAL STRUCTURE; COMMERCIAL PHENOMENA; DRUG EFFICACY; DRUG MANUFACTURE; DRUG SAFETY; DRUG SYNTHESIS; FERMENTATION TECHNIQUE; GENETIC ENGINEERING; IN VITRO PROPAGATION; MALARIA; MALARIA CONTROL; MICROORGANISM; NONHUMAN; PLANT BIOTECHNOLOGY; PLANT GENETICS; PLANT ROOT; PLANT TISSUE CULTURE; REVIEW; SHOOT GROWTH; TRANSGENIC ORGANISM;

EID: 83455235245     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920111798376923     Document Type: Review

References (87)

1. Greenwood, B.M.; Bojang, K.; Whitty, C.J.; Targett, G.A. Malaria. Lancet, 2005, 365, 1487-1498.
2. Winter, R.W.; Kelly, J.X.; Smilkstein, M.J.; Dodean, R.; Bagby, G.C.; Rathbun R.K.; Levin, J.I.; Hinrichs, D.; Riscoe, M.K. Evaluation and lead optimalization of anti-malarial acridones. Exp. Parasitol. 2006, 114, 47-56.
3. Korenromp, E.M.J.; Nahlen B.; Wardlaw T.; Young M. World Malaria Report 2005. Geneva: Roll Back Malaria; World Health Organization; UNICEF, 2005.
4. Bloland, P. Drug Resistance in Malaria. A Background Document for the WHO Global Strategy for Containment of Antimicrobial Resistance. Geneva: World Health Organization, 2001.
5. Olumese, P. Guidelines for the treatment of malaria. Geneva: World Health Organization, 2006.
6. Sutherland, C.J.; Ord, R.; Dunyo, S.; Jawara, M.; Drakeley, C.J.; Alexander, N.; Coleman, R.; Pinder, M.; Walraven, G.; Targett, G.A. Reduction of malaria transmission to Anopheles mosquitoes with six -dose regimen of co-artemether. PLoS Med., 2005, 2, e92
7. White, N. J. Quinghaosu (artemisinin): the price of success. Science, 2008, 320, 330-334.
8. Utzinger, J.; N'Goran, E.K.; N'Dri, A.; Lengeler, C.; Xiao, S.; Tanner, M. Oral artemether for prevention of Schistoma mansoni infection: ranadomised controlled trial. Lancet, 2000, 355,1320-1325.
9. Keiser, J.; Shu-Hua, X.; Chollet, J.; Tanner, M.; Utzinger, J. Evaluation of the in vivo activity of tribendimidine against Schistosoma mansoni, Fasciola hepatica, Clonorchis sinensis, and Opisthorchis viverrini. Antimicrob. Agents Chemother., 2007, 51, 1096-1098.
10. Xu, H.; He, Y.; Yang, X.; Liang, L.; Zhan, Z.; Ye, Y.; Yang, X.; Lian, F.; Sun, L. Anti-malarial agent artesunate inhibits TNF-alphainduced production of proinflammatory cytokines via inhibition of NF-kappaB and PI3 kinase/Akt signal pathway in human rheumatoid arthritis fibroblast-like synoviocytes. Rheumatology (Oxford), 2007, 46, 920-926.
11. Nakase, I.; Lai, H.;Singh, N.P.; Sasaki, T. Anticancer properties of artemisinin derivatives and their targeted delivery by transferrin conjugation. Int. J. Pharm., 2008, 354, 28-33.
12. Woodrow, C.J.; Haynes, R.; Krishna, S. Artemisinins. Postgrad Med. J., 2005, 81, 71-78.
13. Uhlemann, A.C.; Cameron, A. A single amino acid residue can determine the sensitivity of SERCAs to artemisinins. Nat. Struct. Mol. Biol., 2005, 12, 628-629.
14. Covello, P. S. Making artemisinin. Phytochemistry, 2008, 69, 2881-2885.
15. Grupper, M. Meeting on the Production of Artemisinin and ACTs. Arusha, Tanzania: DFID Health Resource Centre, Roll Back Malaria, World Health Organization, 2005.
16. Wallaart, T.E.; Pras, N.; Beekman, A.C.; Quax, W.J. Seasonal variation of artemisinin and its biosynthetic precursors in plants of Artemisia annua of different geographical origin: proof for the existence of chemotypes. Planta Med., 2000, 66, 57-62.
17. Hale, V.; Keasling, J.D.; Renninger, N.; Diagana T.T. Microbially derived artemisinin: a biotechnology solution to the global problem of access to affordable antimalarial drugs. Am. J. Trop. Med. Hyg., 2007, 77, 198-202.
18. Croteau, R.; Kutchan, T.M.; Lewis, N.G. Natural products (secondary metabolites). In: Buchanan B, Gruissem W, Jones R Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville MD, 2000, pp 1250-1318.
19. Roberts, S.C. Production and engineering of terpenoids in plant cell culture. Nat. Chem. Biol., 2007, 3, 387-395.
20. Liu, Y.; Wang, H.; Ye, H.C. and Li, G.F. J. Advances in the plant isoprenoid biosynthesis pathway and its metabolic engineering. Integr. Plant. Biol., 2005, 47, 769-782.
21. Dewick, P.M. The biosynthesis of C5-C25 terpenoid compounds. Nat. Prod. Rep., 2002, 19, 181-222.
22. Bick, J.A. and Lange, B.M. Metabolic cross talk between cytosolic and plastidal pathway of isoprenoid biosynthesis:unidirectional transport of intermediates across the chloroplast envelope membrane. Arch. Biochem. Biophys., 2003, 415, 146-154.
23. Hemmerlin, A.; Hoeffler, J.F.; Meyer, O.; Tritsch, D.; Kagan, I.A.; Grosdemange-Billiard, C.; Rohmer, M.; Bach, T.J. Crosstalk between cytosolic mevalonate and the plastidal methylerythritol phosphate pathways in Tobacco Bright Yellow-2 cells. J. Biol. Chem., 2003, 278, 26666-26676.
24. Laule, O.; Furholz, A.; Chang, H.S.; Zhu, T.; Wang, X.; Heifetz, P.B.; Gruissem, W.; Lange, M. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 2003, 100, 6866-6871.
25. Chappell, J.; Wolf, F.; Proulx, J.; Cuellar, R.; Saunders C. Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme a reductase a rate-limiting step for isoprenoid biosynthesis in plants? Plant Physiol., 1995, 109, 1337-1343.
26. Esteves, J.M.; Cantero, A.; Reindl, A.; Reichler, S.; Leon, P. 1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem., 2001, 276, 22901-22909.
27. Ajikumar, P.K.; Tyo, K.; Carlsen, S.; Mucha, O.; Phon, T.H.; Stephanopoulos, G. Terpenoids: opportunities for biosynthesis of natural product drugs using engineered microorganisms. Mol. Pharm., 2008, 5, 167-190.
28. Ogura, K.; Koyama, T. Enzymatic aspects of isoprenoid chain elongation. Chem. Rev., 1998, 98, 1263-1276.
29. Wallaart, T.E.; Bouwmeester, H.J.; Hille, J.; Poppinga, L.; Maijers, N.C. Amorpha-4,11-diene synthase:cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin Planta, 2001, 212, 460-465.
30. Kim, S.; Heo, K.; Chang, Y.J.; Park, S.H.; Rhee, S.K.; Kim, S.U. Cyclization mechanism of amorpha-4,11-diene synthase, a key enzyme in artemisinin biosynthesis. J. Nat. Prod., 2006, 69, 758-762.
31. Picaud, S.; Olofsson, L.; Brodelius, M. and Brodelius, P.E. Expression, purification, and characterization of recombinant amorpha-4,11-diene synthase from Artemisia annua L. Arch. Biochem. Biophys., 2005, 436, 215-226.
32. Mercke, P.; Bengtsson, M.; Bouwmeester, H. J.; Posthumus, M. A.; Brodelius, P.E. Molecular Cloning, Expression, and Characterization of Amorpha-4,11-diene Synthase, a Key Enzyme of Artemisinin Biosynthesis in Artemisia annua L. Arch. Biochem. Biophys., 2000, 381, 173-180.
33. Bertea, C.M.; Freije, J.R.; van der Woude, H.; Verstappen, F.W.; Perk, L.; Marquez, V.; De Kraker, J.W.; Posthumus, M.A.; Jansen, B.M.J.; de Groot, A.; Franssen, M.C.R.; Bouwmeester, H.J. Identification of intermediates and enzymes involved in the early steps of artemisinin biosynthesis in Artemisia annua. Planta Med., 2005, 71, 40-47.
34. Teoh, K.H.; Polichuk, D.R.; Reed, D.W.; Nowak, G.; Covello, P.S. Artemisia annua L. (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett., 2006, 580, 1411-1416.
35. Rydén, A.M., Ruyter-Spira, M., Quax, W., Osada H., Muranka, T.; Kayser, O.; Bouwmeester, H. The molecular cloning of dihydroartemisinic aldehyde reductase and its implication in artemisinin biosynthesis in Artemisia annua. Planta Med., 2010, 76, 1778-1783.
36. Covello, P.S.; Teoh, K.H.; Polichuk, D.R.; Reed, D.W.; Nowak, G. Functional genomics and the biosynthesis of artemisinin. Phytochemistry, 2007, 68, 1864-1871.
37. Muntendam, R.; Melillo, E.; Ryden, A.; Kayser, O. Perspectives and limits of engineering the isoprenoid metabolism in heterologous hosts. Appl. Microbiol. Biotechnol., 2009, 84,1003-1019.
38. Delabays, N.; Simonnet, X.; Gaudin, M. The genetics of artemisinin content in Artemisia annua L. and the breeding of high yielding cultivars. Curr. Med. Chem., 2001, 8, 1795-1801.
39. Nair, M. S. R.; Acton, N.; Klayman, D. L.; Kendrick, K.; Basile, D. V.; Mante, S. Production of artemisinin in tissue cultures of Artemisia annua. J. Nat. Prod., 1986, 49, 504-507.
40. Liu, C.Z.; Wang, Y.C.; Ouyang, F.; Ye, H.C.; Li, G.F. Production of artemisinin by hairy root cultures of Artemisia annua L. Biotechnol. Lett., 1997, 19, 927-930.
41. Paniego, N.B.; Giulietti, A.M. Artemisinin production by Artemisia annua L-transformed organ cultures. Enzyme Microb. Technol., 1996, 18, 526-530.
42. Liu, C.; Zhao, Y.; Wang, Y. Artemisinin: current state and perspectives for biotechnological production of an antimalarial drug. Appl. Microbiol. Biotechnol., 2006, 72, 11-20.
43. Baldi, A.; Dixit, V.K. Yield enhancement strategies for artemisinin production by suspension cultures of Artemisia annua. Bioresour Technol., 2008, 99, 4609-4614.
44. Woerdenbag, H. J.; Luers, J.F.J.; Uden, W. Van; Pras, N.; Malingre, T.H.; Alfermann, A.W. Production of the new antimalarial drug artemisinin in shoot cultures of Artemissia annua L. Plant Cell Tiss. Org. Cult., 1993, 32, 247-257.
45. Weathers, P.J.; DeJesus-Gonzalez, L.; Kim, Y.J. Alteration of biomass and artemisinin production in Artemisia annua hairy roots by media sterilization method and sugars. Plant Cell Rep., 2004, 23, 414-418
46. Vergauwe, A.; Van, G.E.; Inze, D.; Van D.E.E. Factor influencing Agrobacterium tumefaciens-mediated transformation of Artemisia annua L. Plant Cell Rep., 1998, 18,105-110.
47. Wang, J. W.; Tan, R. X. Artemisinin production in Artemisia annua hairy root cultures with improved growth by altering the nitrogen source in the medium. Biotechnol. Lett., 2002, 24, 1153-1156.
48. Weathers, P.J.; Bunk, G.; McCoy, M.C. The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cell. Dev. Bio-Plant., 2005, 41, 47-53.
49. Smith, T.C.; Weathers, P.J.; Cheetham, R.C. Effect of gibberellic acid on hair root cultures of Artemisia annua growth and artemisinin production. In vitro Cell Dev. Biol. Plant, 1997, 33, 75-79.
50. Liu, C.; Guo, C.; Wang, Y.; Ouyang, F. Effect of light irradiation on hairy root growth and artemisinin biosynthesis of Artemisia annua L. Proc. Biochem., 2002, 38, 581-585.
51. Guo, C.; Liu, C.Z.; Ye, H.C.; Li, G.F. Effect of temperature on growth and artemisinin biosynthesis in hairy root cultures of Artemisia annua. Acta Bot Boreal-Occident Sin., 2004, 24, 1828-1831.
52. Weathers, P.J.; Cheetham, R.D.; Follansbee, E.; Teohet, K. Artemisinin production by transformed roots of Artemisia annua L. Biotechnol. Lett., 1994, 16, 1281-1286.
53. Towler, M. J.; Wyslouzil, B. E.; Weathers, P.J. Using an aerosol deposition model to increase hairy root growth in a mist reactor. Biotechnol. Bioeng., 2007, 96, 881-91.
54. Chen, D.H.; Ye, H.C.; Li, G.F. Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant. Sci., 2000, 155, 179-185.
55. Aquil, S.; Husaini, A.M.; Abdin, M.Z.; Rather, G.M. Overexpression of the HMG-CoA reductase gene leads to enhanced artemisinin biosynthesis in transgenic Artemisia annua plants. Planta Med., 2009, 75, 1453-1458.
56. Zhang, L.; Jing, F.; Li, F.; Li, M.; Wang, Y.; Wang, G.; Sun, X.; Tang, K. Development of transgenic Artemisia annua (Chinese wormwood) plants with an enhanced content of artemisinin, an effective anti-malarial drug, by hairpin-RNA-mediated gene silencing. Biotechnol. Appl. Biochem., 2009, 52, 199-207.
57. Yang, R.Y.; Feng, L.L.; Yang, X.Q.; Yin, L.L.; Xu, X.L.; Zeng, Q.P. Quantitative transcript profiling reveals down-regulation of A sterol pathway relevant gene and overexpression of artemisinin biogenetic genes in transgenic Artemisia annua plants. Planta Med., 2008, 74, 1510-1516.
58. Geng, S.; Ma, M.; Ye, H.C.; Liu, B.Y.; Li, G.F.; Kang, C. Effect of ipt gene expression on the physiological and chemical characteristics of Artemisia annua L. Plant Sci., 2001, 160, 691-698.
59. Kraker, J.W.D.; Scurink, M.; Franssen, M.C.R.; König, W.A.; de Groot, A.; Bouwmeester, H.J. Hydroxylation of sesquiterpenes by enzymes from chicory (Cichorium intybus L.) roots. Tetrahedron., 2003, 59,409-418.
60. Wu, S.; Schalk, M.; Clark, A.; Miles, R.B.; Coates, R.; Chappell, J. Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat. Biotechnol., 2006, 24, 1441-1447.
61. Keasling, J.D. Synthetic biology for synthetic chemistry. ACS Chem. Biol., 2008, 3, 64-76.
62. Martin, V.J.J.; Pitera, D.J.; Withers, S.T.; Newman, J.D.; Keasling, J.D. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol., 2003, 21, 796-802.
63. Pitera, D.J.; Paddon, C.; Newman, J.D.; Keasling, J.D. Rebuilding a balanced heterologous mevalonate pathway for isoprenoid production in Escherichia coli. Metab. Eng., 2007, 9, 193-207.
64. Anthony, J.R.; Anthony, L.C.; Nowroozi, F.; Kwon, G.; Newman, J.D.; Keasling J.D. Optimization of the mevalonate-based isoprenoid biosynthetic pathway in Escherichia coli for production of the anti-malarial drug precursor amorpha-4,11-diene. Metab. Eng., 2009, 11, 13-19.
65. Chang, M.C.Y.; Eachus, R.A.; Trieu, W.; Ro, D.K.; Keasling J.D. Engineering Escherichia coli for production of functionalized terpenoids using plant P450s. Nat. Chem. Biol., 2007, 3, 274-277.
66. Dietrich, J.A.; Yoshikuni, Y.; Fisher, K.J.; Woolard, F.X.; Ockey, D.; McPhee, D.J.; Renninger, N.S.; Chang, M.C.; Baker, D. and Keasling, J.D. A novel semi-biosynthetic route for artemisinin production using engineered substrate-promiscuous P450(BM3). ACS Chem. Biol., 2009, 4, 261-267.
67. Carter, O.A.; Peters, R.J.; Croteau, R. Monoterpen biosynthesis pathway construction in Escherichia coli. Phytochemistry, 2003, 64, 425-433.
68. Lindahl, A.L.; Olsson, M.E.; Mercke, P.; Tollbom, O.; Schelin, J.; Brodelius, M.; Brodelius, P.E. Production of the artemisinin precursor amorpha-4,11-diene by engineered Saccharomyces cerevisiae. Biotechnol. Lett., 2006, 28, 571-580.
69. Ro, D.K.; Paradise, E.M.; Ouellet, M.; Fisher, K.J.; Newman, K.L.; Ndungu, J.M.; Ho, K.A.; Eachus, R.A.; Ham, T.S.; Kirby, J.; Chang, M.C.; Withers, S.T.; Shiba, Y.; Sarpong, R.; Keasling, J.D. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature, 2006, 440, 940-943.
70. Jackson, B. E.; Hart-Wells, E. A.; Matsuda, S. P. T. Metabolic engineering to produce sesquiterpenes in yeast. Org. Lett., 2003, 5, 1629-1632.
71. Zhang, Y.; Teoh, K.H.; Reed, D.W.; Maes, L.; Goossens, A.; Olson, D.J.; Ross, A.R.; Covello, P.S. The molecular cloning of artemisinic aldehyde Delta11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J. Biol. Chem., 2008, 283, 21501-21508.
72. Pronk, J.T.; Steensma, H.Y.; Van Dijken, J.P. Pyruvate metabolism in Saccharomyces cerevisiae. Yeast, 1996, 12, 1607-1633.
73. Shiba, Y.; Paradise, E.M.; Kirby, J.; Ro, D.K.; Keasling, J.D. Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab. Eng., 2007, 9, 160-168.
74. Humphrey, A. Shake flask to fermentor: What have we learned? Biotechnol. Prog., 1998, 14, 3-7.
75. Kim, Y.; Wyslouzil, B.; Weathers, P. Secondary metabolism of hairy root cultures in bioreactors. In Vitro Cell De. Bio. Plan., 2002, 38, 1-10.
76. Shanks, J.; Morgan, J. Plant 'hairy root' culture. Curr. Opin. Biotechnol., 1999, 10, 151-155.
77. Weathers, P.; Wyslouzil, B.; Whipple, M. Laboratory-scale studies of nutrient mist reactors for culturing hairy roots. In: Doran P, Editor. Hairy roots: Culture and applications. Amsterdam: Hardwood Academy Publishers., 1997, pp 191-200.
78. Liu, C.Z.; Wang, Y.C.; Guo, C.; Ouyang, F.; Ye, H.C.; Li, G.F. Enhanced production of artemisinin by Artemisia annua L. hairy root cultures in a modified inner-loop airlift bioreactor. Bioprocess Eng., 1998, 19, 389-392.
79. Kim, Y.; Wyslouzil, B.E.; Weathers, P.J. A comparative study of mist and bubble column reactors in the in vitro production of artemisinin. Plant Cell Rep., 2001, 20, 451-455.
80. Wyslouzil, B.E.; Waterbury, R.G.; Weathers, P.J. The growth of single roots of Artemisia annua in nutrient mist reactors. Biotechnol. Bioeng., 2000, 70, 143-150.
81. Kim, Y.J.; Weathers, P.J.; Wyslouzil, B.E. Growth of Artemisia annua hairy roots in liquid-and gas-phase reactors. Biotechnol. Bioeng., 2002, 80, 454-464.
82. Towler, M.J.; Wyslouzil, B.E.; Weathers P.J. Using an aerosol deposition model to increase hairy root growth in a mist reactor. Biotechnol. Bioeng., 2007, 96, 881-91.
83. Giri, A.; Narasu, L. Transgenic hairy roots: Recent trends and applications. Biotechnol. Adv., 2000, 18, 1-22.
84. Newman, J.D.; Marshall, J.; Chang, M.; Nowroozi, F.; Paradise, E.; Pitera, D.; Newman, K.L.; Keasling, J.D. High-level production of amorpha-4,11-diene in a two-phase partitioning bioreactor of metabolically engineered Escherichia coli. Biotechnol. Bioeng., 2006, 95, 684-691.
85. Lenihan, J.R.; Tsuruta, H.; Diola, D.; Renninger, N.S.; Regentin, R. Developing an industrial artemisinic acid fermentation process to support the cost-effective production of antimalarial artemisininbased combination therapies. Biotechnol. Prog., 2008, 24, 1026-1032.
86. Tsuruta, H.; Paddon, C.J.; Eng, D.; Lenihan, J.R.; Horning, T.; Anthony, L.C.; Regentin, R.; Keasling, J.D.; Renninger, N.S.; Newman, J.D. High-level production of amorpha-4,11-diene, a precursor of the antimalarial agent artemisinin, in Escherichia coli. PLoS One, 2009, 4, e4489.
87. Jambou, R.; Legrand, E.; Niang, M.; Khim, N.; Lim, P.; Volney, B.; Ekala, M.T.; Bouchier, C.; Esterre, P.; Fandeur, T.; Mercereau-Puijalon, O. Resistance of Plasmodium falciparum field isolates to in-vitro artemether and point mutations of the SERCA-type PfATPase6. Lancet, 2005, 366, 1960-1963.