The first step in the biosynthesis of cocaine in Erythroxylum coca: The characterization of arginine and ornithine decarboxylases

Plant Molecular Biology

Volumn 78, Issue 6, 2012, Pages 599-615

  Docimo, Teresa ^a   Reichelt, Michael ^a   Schneider, Bernd ^a   Kai, Marco ^a   Kunert, Grit ^a   Gershenzon, Jonathan ^a   D'Auria, John C ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Cocaine; Erythroxylum coca; Ornithine and arginine decarboxylases; Tropane alkaloids

Indexed keywords

ARGININE DECARBOXYLASE; CARBOXYLYASE; COCAINE; ORNITHINE DECARBOXYLASE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOLOGICAL MODEL; BIOSYNTHESIS; CHEMISTRY; COCA; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT GENE; PLANT LEAF; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CARBOXY-LYASES; COCA; COCAINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC COMPLEMENTATION TEST; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; ORNITHINE DECARBOXYLASE; PHYLOGENY; PLANT LEAVES; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

ERYTHROXYLUM COCA; ESCHERICHIA COLI; SOLANACEAE;

EID: 84858860604     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-012-9886-1     Document Type: Article

References (78)

1. Ahmad A, Leete E (1970) Biosynthesis of tropine moiety of hyoscyamine from delta-N-methylornithine. Phytochemistry 9(11): 2345-2347.
2. Akiyama T, Jin S (2007) Molecular cloning and characterization of an arginine decarboxylase gene up-regulated by chilling stress in rice seedlings. J Plant Physiol 164(5): 645-654. doi: 10. 1016/j. jplph. 2006. 04. 006.
3. Altschul SF, Lipman DJ (1990) Protein database searches for multiple alignments. Proc Natl Acad Sci USA 87(14): 5509-5513.
4. Alyahya AI, Evans WC, Grout RJ (1979) Alkaloids of the genus Erythroxylum. 2. Erythroxylum-Dekindtii (Engl) oe-Schultz. J Chem Soc Perkin Trans 1(9): 2130-2132.
5. Asano N (2003) Glycosidase inhibitors: update and perspectives on practical use. Glycobiol 13(10): 93R-104R. doi: 10. 1093/glycob/cwg090.
6. Balasundaram D, Dinman JD, Tabor CW, Tabor H (1994) SPE1 and SPE2-2 essential genes in the biosynthesis of polyamines that modulates +1-ribosomial frameshifting in Saccharomyces-cerevisiae. J Bacteriol 176(22): 7126-7128.
7. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18(2): 298-305.
8. Biastoff S, Brandt W, Drager B (2009) Putrescine N-methyltransferase-the start for alkaloids. Phytochemistry 70(15-16): 1708-1718. doi: 10. 1016/j. phytochem. 2009. 06. 012.
9. Bieri S, Brachet A, Veuthey JL, Christen P (2006) Cocaine distribution in wild Erythroxylum species. J Ethnopharm 103(3): 439-447. doi: 10. 1016/j. jcp. 2005. 08. 021.
10. Birecka H, Birecki M, Frohlich MW (1987) Evidence for arginine as the endogenous precursor of necines in Heliotropium. Plant Physiol 84(1): 42-46.
11. Bjorklund JA, Leete E (1992) Biosynthesis of the tropane alkaloids and related-compounds. 49. Biosynthesis of the benzoyl moiety of cocaine from cinnamic acid via (R)-(+)-3-hydroxy-3-phenylpropanoic acid. Phytochemistry 31 (11): 3883-3887.
12. Borrell A, Culianezmacia FA, Altabella T, Besford RT, Flores D, Tiburcio AF (1995) Arginine decarboxylase is localized in chloroplasts. Plant Physiol 109(3): 771-776.
13. Bortolotti C, Cordeiro A, Alcazar R, Borrell A, Culianez-Macia FA, Tiburcio AF, Altabella T (2004) Localization of arginine decarboxylase in tobacco plants. Physiol Plant 120(1): 84-92.
14. Brachet A, Munoz O, Gupta M, Veuthey JL, Christen P (1997) Alkaloids of erythroxylum lucidum stem-bark. Phytochemistry 46(8): 1439-1442.
15. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1-2): 7.
16. Bruce NC (2008) Alkaloids. In: Biotechnol, pp 326-361, Wiley-VCH Verlag GmbH. doi: 10. 1002/9783527620906. ch7.
17. Campos Neves MT, Campos Neves A (1967) Some determinations on the leaves of Erythroxylon-Dekindtii-D from Angola Boletim da Escola de Farmacia Universidade de Coimbra Edicao Cientifica 27: 67-73.
18. Carruthers LM, Marton LJ, Peterson CL (2007) Polyamine analogues: potent inducers of nucleosomal array oligomerization and inhibitors of yeast cell growth. Biochem J 405: 541-545. doi: 10. 1042/bj20061347.
19. Chintapakorn Y, Hamill JD (2007) Antisense-mediated reduction in ADC activity causes minor alterations in the alkaloid profile of cultured hairy roots and regenerated transgenic plants of Nicotiana tabacum. Phytochemistry 68(19): 2465-2479. doi: 10. 1016/j. phytochem. 2007. 05. 025.
20. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139(1): 5-17.
21. D'Auria JC, Chen F, Pichersky E (2002) Characterization of an acyltransferase capable of synthesizing benzylbenzoate and other volatile esters in flowers and damaged leaves of Clarkia breweri. Plant Physiol 130(1): 466-476. doi: 10. 1104/pp. 006460.
22. Descenzo RA, Minocha SC (1993) Modulation of the cellular polyamines in Tobacco by transfer and expression of mouse ornithine decarboxylase cDNA. Plant Mol Biol 22(1): 113-127.
23. Dewick P (2002) Medicinal natural products: a biosynthetic approach, 2nd edn. Wiley, England.
24. Dräger B (2004) Chemistry and biology of calystegines. Nat Prod Rep 21(2): 211-223. doi: 10. 1039/b300289f.
25. Evans PT, Malmberg RL (1989) Do polyamines have roles in plant development. Annu Rev Plant Physiol Plant Mol Biol 40: 235-269.
26. Flores HE, Martin-Tanguy J (1991) Polyamines and plant secondary metabolites. In: Slocum R, Flores H (eds) Biochemistry and physiology of polyamines in plant. CRC Press, Boca Raton, pp 57-96.
27. Galston AW (1983) Polyamines as modulators of plant development. Bioscience 33(6): 382-388.
28. Griffin WJ, Lin GD (2000) Chemotaxonomy and geographical distribution of tropane alkaloids. Phytochemistry 53(6): 623-637.
29. Hanczko R, Koros A, Toth F, Molnar-Perl I (2005) Erratum to "Behavior and characteristics of biogenic amines, ornithine and lysine derivatized with the o-phthalaldehyde-ethanethiol-fluorenylmethyl chloroformate reagent. [J Chromatogr A 1087: 210-222] J Chromatogr A 1094 (1-2): 201 doi: 10. 1016/j. chroma. 2005. 08. 077.
30. Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J 27(6): 551-560.
31. Hao YJ, Kitashiba H, Honda C, Nada K, Moriguchi T (2005) Expression of arginine decarboxylase and ornithine decarboxylase genes in apple cells and stressed shoots. J Exp Bot 56(414): 1105-1115. doi: 10. 1093/jxb/eri102.
32. Hartmann T, Sander H, Adolph R, Toppel G (1988) Metabolic links between the biosynthesis of pyrrolizidine alkaloids and polyamines in root cultures of Senecio-vulgaris. Planta 175(1): 82-90.
33. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8(2): R19. doi: 10. 1186/gb-2007-8-2-r19.
34. Hoye TR, Bjorklund JA, Koltun DO, Renner MK (2000) N-methylputrescine oxidation during cocaine biosynthesis: Study of prochiral methylene hydrogen discrimination using the remote isotope method. Organic Lett 2(1): 3-5.
35. Hu ZB, Du M (2006) Hairy root and its application in plant genetic engineering. J Integr Plant Biol 48(2): 121-127.
36. Hummel I, Bourdais G, Gouesbet G, Couee I, Malmberg RL, El Amrani A (2004a) Differential gene expression of arginine decarboxylase ADC1 and ADC2 in Arabidopsis thaliana: characterization of transcriptional regulation during seed germination and seedling development. New Phytol 163(3): 519-531. doi: 10. 1111/j. 1469-8137. 2004. 01128. x.
37. Hummel I, Gouesbet G, El Amrani A, Aïnouche A, Couée I (2004b) Characterization of the two arginine decarboxylase (polyamine biosynthesis) paralogues of the endemic subantarctic cruciferous species Pringlea antiscorbutica and analysis of their differential expression during development and response to environmental stress. Gene 342(2): 199-209.
38. Jander G, Norris SR, Joshi V, Fraga M, Rugg A, Yu SX, Li LL, Last RL (2004) Application of a high-throughput HPLC-MS/MS assay to Arabidopsis mutant screening; evidence that threonine aldolase plays a role in seed nutritional quality. Plant J 39(3): 465-475. doi: 10. 1111/j. 1365-313X. 2004. 02140. x.
39. Johnson EL (1993) Diurnal fluctuations of cocaine and potential precursors in leaves of Erythroxylum-coca. Zeitschrift Fur Naturforschung C-a J Biosci 48(11-12): 863-866.
40. Johnson EL, Elsohly MA (1991) Content and denovo synthesis of cocaine in embryos and endosperms from fruit of Erythroxylum-coca Lam. Ann Bot 68(5): 451-453.
41. Johnson EL, Emche SD (1994) Variation of alkaloid content in Erythroxylum-coca leaves from leaf bud to leaf drop. Ann Bot 73(6): 645-650.
42. Kakkar RK, Sawhney VK (2002) Polyamine research in plants-a changing perspective. Physiol Plant 116(3): 281-292.
43. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228(3): 367-381. doi: 10. 1007/s00425-008-0772-7.
44. Kwak SH, Lee SH (2001) The regulation of ornithine decarboxylase gene expression by sucrose and small upstream open reading frame in tomato (Lycopersicon esculentum Mill). Plant Cell Physiol 42(3): 314-323.
45. Lee YS, Cho YD (2001a) Comparison of biochemical and immunological properties between rat and Nicotiana glutinosa ornithine decarboxylase. J Biochem Mol Biol 34(5): 408-414.
46. Lee YS, Cho YD (2001b) Identification of essential active-site residues in ornithine decarboxylase of Nicotiana glutinosa decarboxylating both l-ornithine and l-lysine. Biochem J 360: 657-665.
47. Leete E (1980) Biosynthesis of cocaine and cuscohygrine in Erythroxylon-Coca. J Chem Soc Chem Commun (23): 1170-1171.
48. Leete E (1982) Biosynthesis of the pyrrolidine rings of cocaine and cuscohygrine from [5-C-14]-labeled ornithine via a symmetrical intermidiate. J Am Chem Soc 104(5): 1403-1408.
49. Leete E (1985) Spermidine: an indirect precursor of the pyrrolidine rings of nicotine and nornicotine in Nicotiana glutinosa. Phytochemistry 24(5): 957-960. doi: 10. 1016/s0031-9422(00)83161-1.
50. Leete E, Marion L, Spenser ID (1954) The biogenesis of alkaloids. 12. The mode of formation of tropine base of Hyoscyamine. Can J Chem Rev Canadienne De Chimie 32 (12): 1116-1123.
51. Leete E, Bjorklund JA, Couladis MM, Kim SH (1991) Late intermediates in the biosynthesis of cocaine: 4-(1-methyl-2-pyrrolidinyl)-3-oxobutanoate and methyl ecgonine. J Am Chem Soc 113(24): 9286-9292.
52. Malmberg RL, Watson MB, Galloway GL, Yu W (1998) Molecular genetic analyses of plant polyamines. Crit Rev Plant Sci 17(2): 199-224.
53. Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul 34(1): 135-148.
54. McNemar MD, Gorman JA, Buckley HR (1997) Isolation and sequence of the gene encoding ornithine decarboxylase, SPE1, from Candida albicans by complementation of a spe1 Delta strain of Saccharomyces cerevisiae. Yeast 13(14): 1383-1389.
55. Michael AJ, Furze JM, Rhodes MJC, Burtin D (1996) Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA. Biochem J 314: 241-248.
56. Mizusaki S, Kisaki T, Tamaki E (1968) Phytochemical studies on tobacco alkaloids. 12. Identification of Gamma-Methylaminobutyraldehyde and its precursor role in nicotine biosynthesis. Plant Physiol 43 (1): 93-98.
57. Moore RC, Boyle SM (1990) Nucleotide-sequence and analysis of the SpeA gene encoding biosynthetic arginine decarboxylase in Escherichia-coli. J Bacteriol 172(8): 4631-4640.
58. Palazon J, Navarro-Ocana A, Hernandez-Vazquez L, Mirjalili MH (2008) Application of metabolic engineering to the production of scopolamine. Molecules 13(8): 1722-1742. doi: 10. 3390/molecules13081722.
59. Plowman T (1982) The identification of Coca (Erythroxylum species): 1860-1910 Bot J Linn Soc 84 (4): 329-353.
60. Plowman T, Rivier L (1983) Cocaine and Cinnamoylcocaine content of Erythroxylum species. Ann Bot 51(5): 641-659.
61. Poulin R, Lu L, Ackermann B, Bey P, Pegg AE (1992) Mechanism of the irreversible inactivation of the mause ornithine decarboxylase by alpha-difluoromethylornithine- characterization of sequences at the inhibitor and coenzyme binding-sites. J Biol Chem 267(1): 150-158.
62. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
63. Rivier L (1981) Analysis of alkaloids in leaves of cultivated Erythroxylum and characterization of alkaline substances used during coca chewing. J Ethnopharmacol 3(2-3): 313-335.
64. Robins RJ, Parr AJ, Payne J, Walton NJ, Rhodes MJC (1990) Factors regulating tropane-alkaloid production in a transformed root culture of a Datura-candida × D-aurea hybrid. Planta 181(3): 414-422.
65. Robins RJ, Parr AJ, Walton NJ (1991) Studies on the biosynthesis of tropane alkaloids in Datura-stramonium L Transformed root cultures. 2. On the relative contributions of l-arginine and l-ornithine to the formation of the ropane ring. Planta 183 (2): 196-201.
66. Ruetsch YA, Boni T, Borgeat A (2001) From cocaine to ropivacaine: the history of local anesthetic drugs. Curr Topics Med Chem 1(3): 175-182.
67. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
68. Sato F, Inai K, Hashimoto T (2007) Metabolic engineering in alkaloid biosynthesis: case studies in tyrosine-and putrescine-derived alkaloids. Appl Plant Metabol Eng, Springer.
69. Schipper RG, Cuijpers V, de Groot L, Thio M, Verhofstad AAJ (2004) Intracellular localization of ornithine decarboxylase and its regulatory protein, antizyme-1. J Histochem Cytochem 52 (10): 1259-1266. doi: 10. 1369/jhc. 4C6389. 2004.
70. Schwartz M, Altman A, Cohen Y, Arzee T (1986) Localization of ornithine decarboxylase and changes in polyamine content in root meristems of Zea mays. Physiol Plant 67(3): 485-492. doi: 10. 1111/j. 1399-3054. 1986. tb05767. x.
71. Soltis DE, Bell C D, Kim S, Soltis PS (2008) Origin and early evolution of angiosperms. Ann NY Acad Sci 1133: 3-25. doi: 10. 1196/annals. 1438. 005.
72. Tiburcio AF, Galston AW (1986) Arginine decarboxylase as the source of putrescine for tobacco alkaloids. Phytochemistry 25(1): 107-110.
73. Tiburcio AF, Figueras X, Claparols I, Santos M, Torne JM (1991) Improved plant-regeneration in maize callus-cultures after pretreatment with DL-alpha-difluoromethylarginine. Plant Cell Tissue Organ Cult 27(1): 27-32.
74. Tiburcio AF, Altabella T, Borrell A, Masgrau C (1997) Polyamine metabolism and its regulation. Physiol Plant 100(3): 664-674.
75. Vandesompele J, De Preter K, Pattyn F, Poppe B, van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Gen Biol 3 (7). doi: 0034. 110. 1186/gb-2002-3-7-research0034.
76. Wang HC, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106(10): 3853-3858. doi: 10. 1073/pnas. 0813376106.
77. Ziegler J, Facchini PJ (2008) Alkaloid biosynthesis: metabolism and trafficking. Ann Rev Plant Biol 59: 735-769. doi: 10. 1146/annurev. arplant. 59. 032607. 092730.
78. Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40(1): 22-34. doi: 10. 1111/j. 1365-313X. 2004. 02183. x.