Folate salvage in plants: Pterin aldehyde reduction is mediated by multiple non-specific aldehyde reductases

Plant Journal

Volumn 51, Issue 3, 2007, Pages 378-389

  Noiriel, Alexandre ^a   Naponelli, Valeria ^b   Bozzo, Gale G ^a   Gregory III, Jesse F ^b   Hanson, Andrew D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Aldehyde reductase; Arabidopsis; Folate salvage; Pea; Pterin aldehydes

Indexed keywords

ALDEHYDE REDUCTASES; ARABIDOPSIS; PTERIN-6-ALDEHYDE; SUBCELLULAR FRACTIONATION;

ALDEHYDES; ENZYME ACTIVITY; OXIDATIVE STRESS; PROTEINS; SEED;

PLANTS (BOTANY);

ALDEHYDE DEHYDROGENASE; ALDEHYDE REDUCTASE; ARABIDOPSIS PROTEIN; AT1G10310 PROTEIN, ARABIDOPSIS; FOLIC ACID; ISOENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ANGIOSPERM; ARABIDOPSIS; ARTICLE; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION; GENE SILENCING; GENETICS; METABOLISM;

ALDEHYDE OXIDOREDUCTASES; ALDEHYDE REDUCTASE; ANGIOSPERMS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FOLIC ACID; GENE EXPRESSION; GENE SILENCING; ISOENZYMES; NADP; SUBSTRATE SPECIFICITY;

ALDEHYDE GROUPS; PLANTS; PROTEINS; SEEDS;

ARABIDOPSIS; PISUM SATIVUM;

EID: 34547124814     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03143.x     Document Type: Article

References (61)

1. Auerbach, G., Herrmann, A., Gutlich, M., Fischer, M., Jacob, U., Bacher, A. Huber, R. (1997) The 1.25 Å crystal structure of sepiapterin reductase reveals its binding mode to pterins and brain neurotransmitters. EMBO J. 16, 7219 7230.
2. Bailly, C. (2004) Active oxygen species and antioxidants in seed biology. Seed Sci. Res. 14, 93 107.
3. Baldet, P., Alban, C., Axiotis, S. Douce, R. (1993) Localization of free and bound biotin in cells from green pea leaves. Arch. Biochem. Biophys. 303, 67 73.
4. Bewley, J.D. (1997) Seed germination and dormancy. Plant Cell, 9, 1055 1066.
5. Blakley, R.L. (1969) Chemical and physical properties of pterins and folate derivatives. In The Biochemistry of Folic Acid and Related Pteridines (Blakley, R.L., ed). New York : Wiley, pp. 58 105.
6. Bouvier-Nave, P. Benveniste, P. (1995) Sterol acyl transferase and steryl ester hydrolase activities in a tobacco mutant which overproduces sterols. Plant Sci. 110, 11 19.
7. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 7, 248 254.
8. Brown, G.M., Weisman, R.A. Molnar, D.A. (1961) The biosynthesis of folic acid. I. Substrate and cofactor requirements for enzymatic synthesis by cell-free extracts of Escherichia coli. J. Biol. Chem. 236, 2534 2543.
9. Cho, S.H., Na, J.U., Youn, H., Hwang, C.S., Lee, C.H. Kang, S.O. (1999) Sepiapterin reductase producing l-threo-dihydrobiopterin from Chlorobium tepidum. Biochem. J. 340, 497 503.
10. Choi, Y.K., Jun, S.R., Cha, E.Y., Park, J.S. Park, Y.S. (2005) Sepiapterin reductases from Chlorobium tepidum and Chlorobium limicola catalyze the synthesis of l-threo-tetrahydrobiopterin from 6-pyruvoyltetrahydropterin. FEMS Microbiol. Lett. 242, 95 99.
11. Cleland, W.W. (1970) Steady state kinetics. In The Enzymes, Vol. II (Boyer, P.D., ed). New York : Academic Press, pp. 40 42.
12. Cline, K. (1986) Import of proteins into chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J. Biol. Chem. 261, 14804 14810.
13. Cossins, E.A. (2000) The fascinating world of folate and one-carbon metabolism. Can. J. Bot. 78, 691 708.
14. Díaz de la Garza, R., Quinlivan, E.P., Klaus, S.M., Basset, G.J., Gregory, J.F. 3rd. Hanson, A.D. (2004) Folate biofortification in tomatoes by engineering the pteridine branch of folate synthesis. Proc. Natl Acad. Sci. USA, 101, 13720 13725.
15. Douce, R., Bourguignon, J., Brouquisse, R. Neuburger, M. (1987) Isolation of plant mitochondria - general principles and criteria of integrity. Methods Enzymol. 148, 403 415.
16. Duax, W.L., Pletnev, V., Addlagatta, A., Bruenn, J. Weeks, C.M. (2003) Rational proteomics I. Fingerprint identification and cofactor specificity in the short-chain oxidoreductase (SCOR) enzyme family. Proteins, 53, 931 943.
17. Foyer, C.H. Noctor, G. (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28, 1056 1071.
18. Garratt, L.C., Ortori, C.A., Tucker, G.A., Sablitzky, F., Bennett, M.J. Barrett, D.A. (2005) Comprehensive metabolic profiling of mono- and polyglutamated folates and their precursors in plant and animal tissue using liquid chromatography/negative ion electrospray ionisation tandem mass spectrometry. Rapid Commun. Mass Spectrom. 19, 2390 2398.
19. Green, J.C., Nichols, B.P. Matthews, R.G. (1996) Folate biosynthesis, reduction, and polyglutamylation. In Escherichia coli and Salmonella - Cellular and Molecular Biology, Vol. 1, 2nd edn (Neidhardt, F.C. ed Washington, DC : ASM Press, pp. 665 673.
20. Gregory, J.F. 3rd. (1989) Chemical and nutritional aspects of folate research: nutritional procedures, methods of folate synthesis, stability, and bioavailability of dietary folates. Adv. Food Nutr. Res. 33, 1 101.
21. Hanson, A.D. Gregory, J.F. 3rd. (2002) Synthesis and turnover of folates in plants. Curr. Opin. Plant Biol. 5, 244 249.
22. Hillcoat, B.L., Nixon, P.F. Blakley, R.L. (1967) Effect of substrate decomposition on the spectrophotometric assay of dihydrofolate reductase. Anal. Biochem. 21, 178 189.
23. Hyde, J.E. (2005) Exploring the folate pathway in Plasmodium falciparum. Acta Trop. 94, 191 206.
24. Iino, T., Tabata, M., Takikawa, S., Sawada, H., Shintaku, H., Ishikura, S. Hara, A. (2003) Tetrahydrobiopterin is synthesized from 6-pyruvoyl- tetrahydropterin by the human aldo-keto reductase AKR1 family members. Arch. Biochem. Biophys. 416, 180 187.
25. Ito, T., Motohashi, R., Kuromori, T., Mizukado, S., Sakurai, T., Kanahara, H., Seki, M. Shinozaki, K. (2002) A new resource of locally transposed Dissociation elements for screening gene-knockout lines in silico on the Arabidopsis genome. Plant Physiol. 129, 1695 1699.
26. Jabrin, S., Ravanel, S., Gambonnet, B., Douce, R. Rébeillé, F. (2003) One-carbon metabolism in plants. Regulation of tetrahydrofolate synthesis during germination and seedling development. Plant Physiol. 131, 1431 1439.
27. Jez, J.M. Penning, T.M. (2001) The aldo-keto reductase (AKR) superfamily: an update. Chem. Biol. Interact. 130 132 499 525.
28. Jörnvall, H., Persson, B., Krook, M., Atrian, S., Gonzalez-Duarte, R., Jeffery, J. Ghosh, D. (1995) Short-chain dehydrogenases/reductases (SDR). Biochemistry, 34, 6003 6013.
29. Jörnvall, H., Hoog, J.O. Persson, B. (1999) SDR and MDR: completed genome sequences show these protein families to be large, of old origin, and of complex nature. FEBS Lett. 445, 261 264.
30. Kobayashi, K. (1982) Aldehyde reductase from Crithidia fasciculata: purification and characterization. J. Biochem. (Tokyo) 91, 783 792.
31. Kuromori, T., Hirayama, T., Kiyosue, Y., Takabe, H., Mizukado, S., Sakurai, T., Akiyama, K., Kamiya, A., Ito, T. Shinozaki, K. (2004) A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J. 37, 897 905.
32. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402 408.
33. Luba, J., Nare, B., Liang, P.H., Anderson, K.S., Beverley, S.M. Hardy, L.W. (1998) Leishmania major pteridine reductase 1 belongs to the short chain dehydrogenase family: stereochemical and kinetic evidence. Biochemistry, 37, 4093 4104.
34. Maruyama, R., Nishizawa, M., Itoi, Y., Ito, S. Inoue, M. (2002) The enzymes with benzil reductase activity conserved from bacteria to mammals. J. Biotechnol. 94, 157 169.
35. Milstien, S. Kaufman, S. (1989) The biosynthesis of tetrahydrobiopterin in rat brain. Purification and characterization of 6-pyruvoyl tetrahydropterin (2′-oxo) reductase. J. Biol. Chem. 264, 8066 8073.
36. Mitsuda, H. Suzuki, Y. (1971) Enzymatic conversion of 2-amino-4-hydroxy-6-formyl-7,8-dihydropteridine to 2-amino-4-hydroxy-6- hydroxymethyl-7,8-dihydropteridine by cell-free extracts of Escherichia coli B. J. Vitaminol. (Kyoto) 17, 5 9.
37. Nare, B., Hardy, L.W. Beverley, S.M. (1997) The roles of pteridine reductase 1 and dihydrofolate reductase-thymidylate synthase in pteridine metabolism in the protozoan parasite Leishmania major. J. Biol. Chem. 272, 13883 13891.
38. Neuburger, M., Rébeillé, F., Jourdain, A., Nakamura, S. Douce, R. (1996) Mitochondria are a major site for folate and thymidylate synthesis in plants. J. Biol. Chem. 271, 9466 9472.
39. Noiriel, A., Naponelli, V., Gregory, J.F. 3rd. Hanson, A.D. (2007) Pterin and folate salvage: plants and Escherichia coli lack capacity to reduce oxidized pterins. Plant Physiol. 143, 1101 1109.
40. Off, M.K., Steindal, A.E., Porojnicu, A.C., Juzeniene, A., Vorobey, A., Johnsson, A. Moan, J. (2005) Ultraviolet photodegradation of folic acid. J. Photochem. Photobiol. B. 80, 47 55.
41. Orsomando, G., Díaz de la Garza, R., Green, B.J., Peng, M., Rea, P.A., Ryan, T.J., Gregory, J.F. 3rd. Hanson, A.D. (2005) Plant gamma-glutamyl hydrolases and folate polyglutamates: characterization, compartmentation, and co-occurrence in vacuoles. J. Biol. Chem. 280, 28877 28884.
42. Orsomando, G., Bozzo, G.G., Basset, G.J., Quinlivan, E.P., Naponelli, V., Rébeillé, F., Ravanel, S., Gregory, J.F. 3rd. Hanson, A.D. (2006) Evidence for folate-salvage reactions in plants. Plant J. 46, 426 435.
43. Osmundsen, H. (1975) A computer programme for the determination of the kinetic constants of two enzymes acting simultaneously on the same substrate. Biochem. Biophys. Res. Commun. 67, 324 340.
44. Park, Y.S., Heizmann, C.W., Wermuth, B., Levine, R.A., Steinerstauch, P., Guzman, J. Blau, N. (1991) Human carbonyl and aldose reductases: new catalytic functions in tetrahydrobiopterin biosynthesis. Biochem. Biophys. Res. Commun. 175, 738 744.
45. Passoneau, J.V. Lowry, O.H. (1993) Enzymatic Analysis. Totowa, NJ : Humana Press.
46. Pfleiderer, W 1985) Chemistry of naturally occurring pteridines. In Folates and Pterins, Vol. 2 (Blakley, R.L. Benkovic, S.J., eds). New York : Wiley, pp. 43 114.
47. Reed, L.S. Archer, M.C. (1980) Oxidation of tetrahydrofolic acid by air. J. Agric. Food Chem. 28, 801 805.
48. Scott, J.M 1984) Catabolism of folates. In Folates and Pterins, Vol. 2 (Blakley, R.L. Benkovic, S.J., eds). New York : Wiley, pp. 307 327.
49. Scott, J.M. (1999) Folate and vitamin B12. Proc. Nutr. Soc. 58, 441 448.
50. Scott, J., Rébeillé, F. Fletcher, J. (2000) Folic acid and folates: the feasibility of nutritional enhancement in plant foods. J. Sci. Food Agric. 80, 795 824.
51. Shiota, T. (1959) Enzymic synthesis of folic acid-like compounds by cell-free extracts of Lactobacillus arabinosus. Arch. Biochem. Biophys. 80, 155 161.
52. Siddiqui, K.S. Cavicchioli, R. (2006) Cold-adapted enzymes. Annu. Rev. Biochem. 75, 403 433.
53. Strålsjö, L.M., Witthöft, C.M., Sjöholm, I.M. Jägerstad, M.I. (2003) Folate content in strawberries (Fragaria × ananassa): effects of cultivar, ripeness, year of harvest, storage, and commercial processing. J. Agric. Food Chem. 51, 128 133.
54. Sueoka, T. Katoh, S. (1985) Carbonyl reductase activity of sepiapterin reductase from rat erythrocytes. Biochim. Biophys. Acta, 843, 193 198.
55. Suh, J.R., Herbig, A.K. Stover, P.J. (2001) New perspectives on folate catabolism. Annu. Rev. Nutr. 21, 255 282.
56. Supangat, S., Seo, K.H., Choi, Y.K., Park, Y.S., Son, D., Han, C.D. Lee, K.H. (2005) Structure of Chlorobium tepidum sepiapterin reductase complex reveals the novel substrate binding mode for stereospecific production of l-threo-tetrahydrobiopterin. J. Biol. Chem. 281, 2249 2256.
57. Suzuki, Y. Mitsuda, H. (1971) NAD+-dependent formation of 2-amino-4-hydroxy-6-carboxypteridine from 2-amino-4-hydroxy-6-formylpteridine by cell-free extracts of Escherichia coli. Biochim. Biophys. Acta, 242, 504 506.
58. Vicient, C.M. Delseny, M. (1999) Isolation of total RNA from Arabidopsis thaliana seeds. Anal. Biochem. 268, 412 413.
59. Whiteley, J.M., Drais, J., Kirchner, J. Huennekens, F.M. (1968) Synthesis of 2-amino-4-hydroxy-6-formyl-7,8-dihydropteridine and its identification as a degradation product of dihydrofolate. Arch. Biochem. Biophys. 126, 955 957.
60. Yang, S., Lee, Y.J., Kim, J.M., Park, S., Peris, J., Laipis, P., Park, Y.S., Chung, J.H. Oh, S.P. (2006) A murine model for human sepiapterin-reductase deficiency. Am. J. Hum. Genet. 78, 575 587.
61. Yoon, K.H., Cha, K.W., Park, S.I. Yim, J.J. (1993) Isolation and characterization of sepiapterin reductase from Drosophila melanogaster. Pteridines 4, 43 50.