Dissecting the sterol C-4 demethylation process in higher plants. from structures and genes to catalytic mechanism

Steroids

Volumn 76, Issue 4, 2011, Pages 340-352

  Rahier, Alain ^a  

^a INST DE BIOL MOLEC DES PLANTES   (France)

Author keywords

C 4 demethylation; Homology modeling; Hydroxysteroid dehydrogenase; Non heme iron oxygenase; Sterols

Indexed keywords

24 ETHYLIDENELOPHENOL; 24 METHYLENECYCLOARTANOL; 24 METHYLENELOPHENOL; 3 OXOSTEROID DERIVATIVE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; 31 NORCYCLOARTENOL; 31 NORCYCLOLAUDENONE; 3BETA HYDROXY DELTA5 STEROID DEHYDROGENASE; 4 METHYLSTEROL DERIVATIVE; 4,4 DIMETHYLSTEROL 4ALPHA METHYLOXIDASE; 4ALPHA CARBOXYSTEROL DERIVATIVE; 4ALPHA METHYLSTEROL 4ALPHA METHYLOXIDASE; ACYL COENZYME A DESATURASE; CARBOXYLIC ACID DERIVATIVE; CYCLOABYSSINONE; CYCLOARTENOL; CYCLOEUCALENOL; GALAXAUROL A; GALAXAUROL C; LANOSTEROL; METHYL GROUP; OBTUSIFOLIOL; OXIDOREDUCTASE; OXOSTEROID; OXYGENASE; PHYTOSTEROL; PORIFERASTEROL; STEROID REDUCTASE; STEROL METHYLOXIDASE; UNCLASSIFIED DRUG;

BIOSYNTHESIS; CATALYSIS; DEMETHYLATION; ENZYME SPECIFICITY; HIGHER PLANT; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; NONHUMAN; PLANT GENE; PRECURSOR; REVIEW; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STEROL DEMETHYLATION; STEROL SYNTHESIS; YEAST;

3-HYDROXYSTEROID DEHYDROGENASES; ARABIDOPSIS; CARBOXY-LYASES; CATALYTIC DOMAIN; ENZYME INHIBITORS; METHYLATION; MOLECULAR STRUCTURE; MULTIENZYME COMPLEXES; PHYTOSTEROLS; PLANTS; PROTEIN CONFORMATION; STEROID HYDROXYLASES; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY;

ANIMALIA; EMBRYOPHYTA;

EID: 79951512207     PISSN: 0039128X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.steroids.2010.11.011     Document Type: Review

References (97)

1. K.E. Bloch Sterol structure and membrane function CRC Crit Rev Biochem 14 1983 47 92
2. H. Ohvo-Rekilä, B. Ramstedt, P. Leppimäki, and J.P. Slotte Cholesterol interactions with phospholipids in membranes Prog Lipid Res 41 2002 66 97 (Pubitemid 32998278)
3. L. Miao, M. Nielsen, J. Thewalt, J.H. Ipsen, M. Bloom, and M.J. Zuckermann From lanosterol to cholesterol: structural evolution and differential effects on lipid bilayers Biophys J 82 2002 1429 1444 (Pubitemid 34204763)
4. Y. Barenholtz Cholesterol and other membrane active sterols: from membrane evolution to rafts Prog Lipid Res 41 2002 1 5
5. C.J. Fielding, and P.E. Fielding Cholesterol and caveolae: structural and functional relationships Biochim Biophys Acta 1529 2000 210 222
6. L.W. Parks, S.J. Smith, and J.H. Crowley Biochemical and physiological effects of sterol alterations in yeast a review Lipids 30 1995 227 230
7. J.R. Silvius Role of cholesterol in lipid raft formation: lessons from lipid model systems Biochem Biophys Acta 1610 2003 174 183 (Pubitemid 36324462)
8. M.A. Hartmann Plant sterols and the membrane environment Trends Plant Sci 3 1998 170 175
9. R.K. Guy Inhibition of sonic hedgehog autoprocessing in cultured mammalian cells by sterol deprivation Proc Natl Acad Sci USA 97 2000 7307 7312 (Pubitemid 30431459)
10. H.E. Karpen, J.T. Bukowski, T. Hughes, J.P. Gratton, W.C. Sessa, and M.R. Gailani The sonic hedgehog receptor patched associates with caveolin-1 in cholesterol-rich microdomains of the plasma membrane J Biol Chem 276 2001 19503 19511
11. Y. Roche, P. Gerbeau-Pissot, B. Buhot, D. Thomas, L. Bonneau, and J. Gresti Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts FASEB J 22 2008 3980 3991
12. F.F. Moebius, U. Fitzky, and H. Glossmann Genetic defects in postsqualene cholesterol biosynthesis Trends Endoc Metab 11 2000 106 114 (Pubitemid 30164203)
13. J.A. Svoboda, and G.F. Weirich Sterol metabolism in the tobacco hornworm, Manduca sexta Lipids 30 1995 263 267
14. J.H. Adler, and R.J. Grebenok Occurrence, biosynthesis, and putative role of ecdysteroids in plants Crit Rev Biochem Mol Biol 34 1999 253 264 (Pubitemid 29422821)
15. S.A. Brunt, and J.C. Silver Molecular cloning and characterization of two distinct hsp85 sequences from the steroid responsive fungus Achlya ambisexualis Curr Genet 19 1991 383 388
16. N. Mandava Plant growth-promoting brassinosteroids Annu Rev Plant Physiol Plant Mol Biol 39 1988 23 52
17. A. Sakurai Brassinosteroid biosynthesis Plant Physiol Biochem 37 1999 351 361 (Pubitemid 29324239)
18. G.J. Bishop, and T. Yokota Plants steroid hormones, brassinosteroids: current highlights of molecular aspects on their synthesis/metabolism, transport, perception and response Plant Cell Physiol 42 2001 114 120 (Pubitemid 32232396)
19. P. Benveniste Biosynthesis and accumulation of sterols Annu Rev Plant Biol 55 2004 429 457 (Pubitemid 38940939)
20. B.M. Lange, and M. Ghassemian Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism Plant Mol Biol 51 2003 925 948 (Pubitemid 36579709)
21. F. Bouvier, A. Rahier, and B. Camara Biogenesis, molecular regulation and function of plant isoprenoids Prog Lipid Res 44 2005 357 429 (Pubitemid 41608703)
22. S.D. Clouse Arabidopsis mutants reveal multiple roles for sterols in plant development Plant Cell 14 2002 1995 2000
23. K. Lindsey, M.L. Pullen, and J.F. Topping Importance of plant sterols in pattern formation and hormone signalling Trends Plant Sci 8 2003 521 525 (Pubitemid 37481529)
24. Y. Boutté, and M. Grebe Cellular processes relying on sterol function in plants Curr Opin Plant Biol 12 2009 705 713
25. A.G. Byskov, C.Y. Andersen, L. Nordholm, H. Thøgersen, G. Xia, and O. Wassmann Chemical structure of sterols that activate oocyte meiosis Nature 374 1995 559 562
26. C. Hegele-Hartung, T. Blume, M. Lessl, J.L. Ottesen, and C. Grøndahl Meioseaktivierende Sterole verbessern die Perspektive für die Eizellreifung in vitro Reproduktionmedizin 16 2000 129 139 (Pubitemid 30262577)
27. A. König, R. Happle, D. Bornholdt, H. Engel, and K.H. Grzeschik Mutations in the NSDHL gene, encoding a 3beta-hydroxysteroid dehydrogenase, cause CHILD syndrome Am J Med Genet 90 2000 339 346 (Pubitemid 30084263)
28. M. Bard, P.A. Bruner, C.A. Pierson, N.D. Lees, B. Biermann, and L. Frye Cloning and characterization of ERG25, the Saccharomyces cerevisiae gene encoding C-4 sterol methyl oxidase Proc Natl Acad Sci USA 93 1996 186 190 (Pubitemid 26038124)
29. A.L. Hughes, C.Y. Lee, C.M. Bien, and P.J. Espenshade 4-Methyl sterols regulate fission yeast SREBP-Scap under low oxygen and cell stress J Biol Chem 282 2007 24388 24396 (Pubitemid 47328027)
30. S. Choe, T. Noguchi, S. Fujioka, S. Takatsuto, C.P. Tissier, and B.D. Gregory The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis Plant Cell 11 1999 207 221
31. K. Schrick, U. Mayer, A. Horrichs, C. Kuhnt, C. Bellini, and J. Dangl FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis Genes Dev 14 2000 1471 1484 (Pubitemid 30421840)
32. L. Gondet, T. Weber, P. Maillot-Vernier, P. Benveniste, and T. Bach Regulatory role of microsomal 3-hydroxy-3-methylglutaryl-coenzyme A reductase in a tobacco mutant that overproduces sterols Biochem Biophys Res Commun 186 1992 88 893
33. P. Maillot-Vernier, L. Gondet, H. Schaller, P. Benveniste, and G. Belliard Genetic study and further biochemical characterization of a tobacco mutant that overproduces sterols Mol Gen Genet 231 1991 33 40
34. N. Homberg, M. Harker, A.D. Wallace, J.C. Clayton, C.L. Gibbard, and R. Safford Co-expression of N-terminal truncated 3-hydroxy-3-methylglutaryl CoA reductase and C24-sterol methyltransferase type 1 in transgenic tobacco enhances carbon flux towards end-product sterols Plant J 36 2003 12 20 (Pubitemid 37231653)
35. W.R. Nes, K. Krevitz, J. Joseph, W.D. Nes, B. Harris, and G.F. Gibbons The phylogenetic distribution of sterols in tracheophytes Lipids 12 1977 511 527 (Pubitemid 8131362)
36. T. Akihisa, W.C.M.C. Kokke, and T. Tamura Naturally occurring sterols and related compounds from plants G.W. Patterson, W.D. Nes, Physiology and biochemistry of sterols 1991 American Oil Chemist's Society 172 228
37. D.H.R. Barton Triterpenoids, Part III. cycloArtenone, a triterpenoid ketone J Chem Soc 1951 1951 1444 1451
38. A. Eschenmoser, L. Ruzicka, O. Jeger, and D. Arigoni A stereochemical interpretation of the isoprene rule for the triterpenes Helv Chem Acta 38 1955 1890 1904
39. T.W. Goodwin Biosynthesis of terpenoids Ann Rev Plant Physiol 30 1979 369 404
40. I. Abe, M. Rohmer, and G.D. Prestwich Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes Chem Rev 93 1993 2189 2206
41. M.D. Kolesnikova, Q. Xiong, S. Lodeiro, L. Hua, and S.P.T. Matsuda Lanosterol biosynthesis in plants Arch Biochem Biophys 447 2006 87 95
42. K. Ohyama, M. Suzuki, J. Kikuchi, K. Saito, and T. Muranaka Dual biosynthetic pathways to phytosterol via cycloartenol and lanosterol in Arabidopsis Proc Natl Acad Sci USA 106 2009 725 730
43. A. Rahier, M. Taton, and P. Benveniste Cycloeucalenol-obtusifoliol isomerase. Structural requirements for transformation or binding of substrates and inhibitors Eur J Biochem 181 1989 615 626 (Pubitemid 19146925)
44. F.F. Knapp, and H.J. Nicholas The biosynthesis of 31-norcyclolaudenone in Musa sapientum Phytochemistry 10 1971 97 102
45. T. Itoh, T. Kikuchi, T. Tamura, and T. Matsumoto Two 3-oxo steroids in Thea sinensis seeds Phytochemistry 20 1981 175 176
46. T. Akihisa, N. Shimizu, T. Tamura, and T. Matsumoto (24S)-14α,24- Dimethyl-9β19-cyclo-5α-cholest-25-en-3β-ol: a new sterol and other sterols in Musa sapientum Lipids 21 1986 494 498
47. T. Akihisa, Y. Kimura, W.C.M.C. Kokke, S. Takase, K. Yakusawa, and A. Jin-Nai 4-Epicycloeucalenone and 4-epicyclomusalenone: Two 3-oxo-28- norcycloartanes from the fruit peel of Musa sapientum L Chem Pharm Bull 45 1997 744 746 (Pubitemid 27209314)
48. A.M. Baldé, S. Apers, M. Claeys, L. Pieters, and A.J. Vlietinck Cycloabyssinone, a new cycloterpene from Harrisonia abyssinica Fitoterapia 72 2001 438 440 (Pubitemid 32515309)
49. J. Galley, and B. De Kruijff Correlation between molecular shape and hexagonal HII phase promoting ability of sterols FEBS Lett 143 1982 133 143
50. W.D. Nes, G.G. Janssen, F.G. Crumley, M. Kalinowska, and T. Akihisa The structural requirements of sterols for membrane function in Saccharomyces cerevisiae Arch Biochem Biophys 300 1993 724 733 (Pubitemid 23232934)
51. W-H. Zhang, H-M. Zhong, and C-T. Che Cycloartanes from the red alga Galaxaura sp J Asian Nat Prod Res 7 2005 59 65
52. M.T. Gutierrez-Lugo, M.P. Singh, W.M. Maiese, and B.N. Timmermann New antimicrobial cycloartane triterpenes from Acalypha communis J Nat Prod 65 2002 872 875 (Pubitemid 34733991)
53. Y-H. Choi, A.D. Kinghorn, X. Shi, H. Zhang, and B.K. Teo Abrusoside A: a new type of highly sweet triterpene glycoside J Chem Soc Chem Commun 1989 1989 887 888 (Pubitemid 19170773)
54. D. Gachotte, R. Barbuch, J. Gaylor, E. Nickel, and M. Bard Characterization of the Saccharomyces cerevisiae ERG26 gene encoding the C-3 sterol dehydrogenase (C-4 decarboxylase) involved in sterol biosynthesis Proc Natl Acad Sci USA 95 1998 13794 13799 (Pubitemid 28523052)
55. X.Y. Liu, A.W. Dangel, R.I. Kelley, W. Zhao, P. Denny, and M. Botcherby The gene mutated in bare patches and striated mice encodes a novel 3beta-hydroxysteroid dehydrogenase Nat Genet 22 1999 182 187 (Pubitemid 29264815)
56. L.J. Goad, and T.W. Goodwin The biosynthesis of sterols in higher plants Biochem J 99 1966 735 746
57. E.L. Ghisalberti, N.J. de Souza, H.H. Rees, L.J. Goad, and T.W. Goodwin Biological removal of the 4α-methyl group during the conversion of cycloartanol into 31-norcycloartanol in Polypodium vulgare Linn J Chem Soc D Chem Commun 1 1969 1403 1405
58. H.H. Rees, E.I. Mercer, and T.W. Goodwin The stereospecific biosynthesis of plant sterols and alpha- and beta-amyrin Biochem J 99 1966 726 734
59. F.F. Knapp, and H.J. Nicholas Phytosterol biosynthesis in banana peel. Initial removal of the 4α-methyl group of 24-methylenecycloartanol during its conversion into cycloeucalenol in Musa sapientum J Chem Soc D Chem Commun 1970 399 400
60. F.F. Knapp, L.J. Goad, and T.W. Goodwin Inversion of the 4β-hydrogen during the conversion of the sterol obtusifoliol into poriferasterol by Ochromonas malhamensis J Chem Soc D Chem Commun 1973 149 150
61. F.F. Knapp, L.J. Goad, and T.W. Goodwin Stereochemistry of C-4 demethylation during conversion of obtusifoliol into poriferasterol by Ochromonas malhamensis Phytochemistry 16 1977 1677 1681
62. G.W. Patterson, L.G. Doyle, L.G. Dickson, and J.T. Chan Effects of triparanol and AY-9944 upon sterol biosynthesis in Chorella Lipids 9 1974 567 574
63. N.N. Ragsdale Specific effects of triarimol on sterol biosynthesis in Ustilago maydis Biochem Biophys Acta 380 1975 80 96
64. M. Taton, P. Ullmann, P. Benveniste, and A. Rahier Interaction of triazole fungicides and plant growth regulators with microsomal cytochrome P-450-dependent obtusifoliol 14α-demethylase Pestic Biochem Physiol 30 1988 178 189
65. P. Maillot-Vernier, H. Schaller, P. Benveniste, and G. Belliard In vitro selection of calli resistant to a triazole cytochrome-p-450-obtusifoliol-14- demethylase inhibitor from protoplasts of Nicotiana tabacum L. cv Xanthi Plant Physiol 93 1990 1190 1195 (Pubitemid 120029935)
66. J.R. Faust, J.M. Trzaskos, and J.L. Gaylor Cholesterol biosynthesis P.L. Yeagle, Biology of cholesterol 1988 CRC Press Boca Raton 19 38
67. H. Fukushima, G.F. Grinstead, and J.L. Gaylor Total enzymic synthesis of cholesterol from lanosterol, Cytochrome b5-dependence of 4-methyl sterol oxidase J Biol Chem 256 1981 4822 4826
68. S. Pascal, M. Taton, and A. Rahier Plant sterol biosynthesis: identification and characterization of two distinct microsomal oxidative enzymatic systems involved in sterol C4-demethylation J Biol Chem 268 1993 11639 11654 (Pubitemid 23168112)
69. A. Rahier, M. Smith, and M. Taton The role of cytochrome b5 in 4α-methyl-oxidation and C5(6) desaturation of plant sterol precursors Biochem Biophys Res Commun 236 1997 434 437 (Pubitemid 27373315)
70. S. Darnet, and A. Rahier Enzymological properties of sterol-C4-methyl- oxidase of yeast sterol biosynthesis Biochim Biophys Acta 1633 2003 106 117 (Pubitemid 36851636)
71. J. Shanklin, and E.B. Cahoon Desaturation and relared modifications of fatty acids Annu Rev Plant Physiol Plant Mol Biol 49 1998 611 641
72. S. Rondet, M. Taton, and A. Rahier Identification, characterization and partial purification of 4α-carboxysterol-C3-dehydrogenase-C4-decarboxylase from Zea mays Arch Biochem Biophys 366 1999 249 260 (Pubitemid 29394217)
73. S. Pascal, M. Taton, and A. Rahier Plant sterol biosynthesis: identification of a NADPH dependant plant sterone reductase involved in the sterol-4-demethylation Arch Biochem Biophys 312 1994 260 271 (Pubitemid 24243827)
74. T.J. Scallen, A.K. Dhar, and E.D. Loughran Isolation and characterization of C-4 methyl intermediates in cholesterol biosynthesis after treatment of rat liver in vitro with cholestan-3β,5α,6β-triol J Biol Chem 246 1971 3168 3174
75. D.L. Bartlett, and C.H. Robinson Mechanism-based inactivation of 4-methylsterol oxidase by 4α-cyanomethyl-5α-cholestan-3β-ol J Am Chem Soc 104 1982 4729 4730
76. I.V. Ekhato, and C.H. Robinson Synthesis of novel 4-alpha.-substituted sterols J Org Chem 54 1989 1327 1331
77. T. Kuchta, K. Bartkova, and R. Kubinec Ergosterol depletion and 4-methyl sterol accumulation in the yeast Saccharomyces cerevisiae treated with an antifungal, 6-amino-2-n-pentylthio-benzothiazole Biochem Biophys Res Commun 189 1992 85 91 (Pubitemid 23030012)
78. H. Nose, H. Fushimi, A. Seki, T. Sasaki, H. Watabe, and S. Hoshiko a novel antifungal agent, inhibit ergosterol biosynthesis at C-4 sterol methyl oxidase J Antibiot (Tokyo) 55 2002 969 974 (Pubitemid 35428782)
79. H.J. Rosslenbroich, W. Brandes, B.W. Krueger, K.H. Kuck, R. Pontzen, and K. Stenzel (KBR 2738) a novel fungicide for control of Botrytis cinerea and related pathogens Proc Brighton Crop Prot Conf-Pests and Diseases, BCPC, Farnham, Surrey, UK, vol. 2 1998 327 334
80. D. Debieu, J. Bach, M. Hugon, C. Malosse, and P. Leroux The hydroxyanilide fenhexamid, a new sterol biosynthesis inhibitor fungicide efficient against the plant pathogenic fungus Botryotinia fuckeliana (Botrytis cinerea) Pest Manag Sci 57 2001 1060 1067
81. U. Oppermann, C. Filling, and H. Jörnvall Forms and functions of human SDR enzymes Chem Biol Interact 130-132 2001 699 705 (Pubitemid 32295856)
82. U. Oppermann, C. Filling, M. Hult, N. Shafqat, X. Wu, and M. Kindh Short-chain dehydrogenases/reductases (SDR): the 2002 update Chem Biol Interact 143-144 2003 247 253 (Pubitemid 36253589)
83. Y. Kallberg, U. Oppermann, H. Jörnvall, and B. Persson Short-chain dehydrogenase/reductase (SDR) relationships: a large family with eight clusters common to human, animal, and plant genomes Protein Sci 11 2002 636 641 (Pubitemid 34173025)
84. S. Darnet, M. Bard, and A. Rahier Functional identification of sterol-4α-methyl oxidase cDNAs from Arabidopsis thaliana by complementation of a yeast erg25 mutant lacking sterol-4α-methyl oxidation FEBS Lett 508 2001 39 43 (Pubitemid 33055663)
85. S. Darnet, and A. Rahier Plant sterol biosynthesis: identification of two distinct families of sterol 4α-methyl oxidases Biochem J 378 2004 889 898 (Pubitemid 38406866)
86. A. Rahier, S. Darnet, F. Bouvier, B. Camara, and M. Bard Molecular and enzymatic characterizations of novel bifunctional 3β-hydroxysteroid dehydrogenases/C4 decarboxylases from Arabidopsis thaliana J Biol Chem 281 2006 27264 27277 (Pubitemid 44403813)
87. H. Jornvall, B. Persson, M. Krook, S. Atrian, R. Gonzales-Duarte, and J. Jeffery Short-chain dehydrogenases/reductases (SDR) Biochemistry 34 1995 6003 6013
88. A.D. Rahimtula, and J.L. Gaylor Partial purification of a microsomal sterol 4-carboxylic acid decarboxylase J Biol Chem 247 1972 9 15
89. C. Mo, M. Valachovic, S.K. Randall, J.T. Nickels, and M. Bard Protein-protein interactions among C-4 demethylation enzymes involved in yeast sterol biosynthesis Proc Natl Acad Sci USA 99 2002 9739 9744 (Pubitemid 34831117)
90. S.T. Allard, W.W. Cleland, and H.M. Holden High resolution X-ray structure of dTDP-glucose 4,6-dehydratase from Streptomyces venezuelae J Biol Chem 279 2004 2211 2220 (Pubitemid 38084494)
91. A. Rahier, M. Bergdoll, G. Génot, F. Bouvier, and B. Camara Homology modeling and site-directed mutagenesis reveal catalytic key amino acids of 3β-hydroxysteroid-dehydrogenase/C4-decarboxylase from Arabidopsis Plant Physiol 149 2009 1872 1886
92. C. Mo, and M. Bard Erg28p is a key protein in the yeast sterol biosynthetic enzyme complex J Lipid Res 46 2005 1991 1998 (Pubitemid 41248496)
93. D. Gachotte, J. Eckstein, R. Barbuch, T. Hughes, C. Roberts, and M. Bard A novel gene conserved from yeast to humans is involved in sterol biosynthesis J Lipid Res 42 2001 152 154
94. V. Smith, K.N. Chou, D. Lashkari, D. Botstein, and P.O. Brown Functional analysis of the genes of yeast chromosome V by genetic footprinting Science 274 1996 2069 2074 (Pubitemid 27020699)
95. P.L. Yeagle, R.B. Martin, A.K. Lala, H.K. Lin, and K. Bloch Differential effects of cholesterol and lanosterol on artificial membranes Proc Natl Acad Sci USA 74 1977 4924 4926 (Pubitemid 8241007)
96. G. Vinci, X. Xia, and R.A. Veitia Preservation of genes involved in sterol metabolism in cholesterol auxotrophs: facts and hypotheses PLoS One 3 2008 e2883
97. DeLano WL. The PyMOL molecular graphics system. World Wide Web, http://www.pymol.org ; 2002.