Modified oxidosqualene cyclases in the formation of bioactive secondary metabolites: Biosynthesis of the antitumor clavaric acid

Fungal Genetics and Biology

Volumn 46, Issue 3, 2009, Pages 232-242

  Godio, Ramiro P ^a   Martín, Juan F ^a,b  

^a Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

^b UNIVERSITY OF LEÓN   (Spain)

Author keywords

Basidiomycete; Clavaric acid; Hypholoma; Triterpenoids

Indexed keywords

CLAVARIC ACID; FUNGAL ENZYME; LANOSTEROL SYNTHASE; TRITERPENOID; UNCLASSIFIED DRUG;

ARTICLE; BASIDIOMYCETES; BIOSYNTHESIS; BIOTRANSFORMATION; CONTROLLED STUDY; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME ANALYSIS; FUNGAL GENOME; GENE AMPLIFICATION; GENE DISRUPTION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC CODE; GENOME ANALYSIS; METABOLITE; MOLECULAR CLONING; MUTANT; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

AMINO ACID MOTIFS; BASIDIOMYCOTA; BLOTTING, NORTHERN; CATALYTIC DOMAIN; CLONING, MOLECULAR; DNA, FUNGAL; FUNGAL PROTEINS; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; INTRAMOLECULAR TRANSFERASES; LANOSTEROL; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SQUALENE;

BASIDIOMYCOTA; HYPHOLOMA; HYPHOLOMA SUBLATERITIUM;

EID: 60649112239     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2008.12.002     Document Type: Article

References (47)

1. Abe I., Bai M., Xiao X.Y., and Prestwich G.D. Affinity labeling of vertebrate oxidosqualene cyclases with a tritiated suicide substrate. Biochem. Biophys. Res. Commun. 187 (1992) 32-38
2. Abe I., Rohmer M., and Prestwich G.D. Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes. Chem. Rev. 93 (1993) 2189-2206
3. Abe I., and Prestwich G.D. Molecular cloning, characterization, and functional expression of rat oxidosqualene cyclase cDNA. Proc. Natl. Acad. Sci. USA 92 (1995) 9274-9278
4. Abe I., and Prestwich G.D. Identification of the active site of vertebrate oxidosqualene cyclase. Lipids 30 (1995) 231-234
5. Abe I., and Prestwich G.D. Squalene epoxidase and oxidosqualene: lanosterol cyclase; key enzymes in cholesterol biosynthesis. In: Barton D.H.R., and Nakanishi K. (Eds). Comprehensive Natural Products Chemistry vol. 2 (1999), Elsevier, Oxford 267-298
6. Abe I., Naito K., Takagi Y., and Noguchi H. Molecular cloning, expression, and site-directed mutations of oxidosqualene cyclase from Cephalosporium caerulens. Biochim. Biophys. Acta. 1522 (2001) 67-73
7. Abe I. Enzymatic synthesis of cyclic triterpenes. Nat. Prod. Rep. 24 (2007) 1311-1331
8. Alvarez V., Rodriguez-Saiz M., de la Fuente J.L., Gudina E.J., Godio R.P., Martin J.F., and Barredo J.L. The crtS gene of Xanthophyllomyces dendrorhous encodes a novel cytochrome-P450 hydroxylase involved in the conversion of beta-carotene into astaxanthin and other xanthophylls. Fungal Genet. Biol. 43 (2006) 261-272
9. Baker C.H., Ting A.Y., and Cheng H. Molecular cloning of a Schizosaccharomyces pombe cDNA encoding lanosterol synthase and investigation of conserved tryptophan residues. Biochem. Biophys. Res. Commun. 219 (1996) 327-331
10. Boutaud O., Dolis D., and Schuber F. Preferential cyclization of 2,3(S):22(S),23-dioxidosqualene by mammalian 2,3-oxidosqualene-lanosterol cyclase. Biochem Biophys. Res. Commun. 188 (1992) 898-904
11. Calvo A.M., Wilson R.A., Bok J.W., and Keller N.P. Relationship between secondary metabolism and fungal development. Microbiol. Mol. Biol. Rev. 66 (2002) 447-459
12. Cattel L., Cerut M., Balliano G., Viola F., Grosa G., Rocco F., and Brusa P. 2,3-Oxidosqualene cyclase: from azasqualenes to new site-directed inhibitors. Lipids 30 (1995) 235-246
13. Chen X., Stone M., Schlagnhaufer C., and Romaine C.P. A fruiting body tissue method for efficient Agrobacterium-mediated transformation of Agaricus bisporus. Appl. Environ. Microbiol. 66 (2000) 4510-4513
14. Corey E.J., Matsuda S.P., and Bartel B. Isolation of an Arabidopsis thaliana gene encoding cycloartenol synthase by functional expression in a yeast mutant lacking lanosterol synthase by the use of a chromatographic screen. Proc. Natl. Acad. Sci. USA 90 (1993) 11628-11632
15. Corey E.J., Matsuda S.P., Baker C.H., Ting A.Y., and Cheng H. Molecular cloning of a Schizosaccharomyces pombe cDNA encoding lanosterol synthase and investigation of conserved tryptophan residues. Biochem. Biophys. Res. Commun. 219 (1996) 327-331
16. Corey E.J., Cheng H., Baker C., Matsuda S.P., Li D., and Song X. Methodology for the preparation of pure recombinant S. cerevisiae lanosterol synthase using a baculovirus expression system. Evidence that oxirane cleavage and A-ring formation are concerted in the biosynthesis of lanosterol from 2,3-oxidosqualene. J. Am. Chem. Soc. 119 (1997) 1277-1288
17. Dougherty D.A. Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271 (1996) 163-168
18. Erkel G., and Anke T. Products from basidiomycetes. In: Kleinkauf H., and von Döhren H. (Eds). Biotechnology vol. 7 (1997), VCH Verlag, Weinheim 489-533
19. Fessenden R.J., and Fessenden J.S. Organic Chemistry. second ed. (1982), Willard Grant Press, Boston
20. Field B., and Osbourn A.E. Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320 (2008) 543-547
21. Godio R.P., Fouces R., Gudiña E.J., and Martín J.F. Agrobacterium tumefaciens-mediated transformation of the antitumor clavaric acid producer basidiomycete Hypholoma sublateritium. Curr. Genet. 46 (2004) 287-294
22. Godio R.P., Fouces R., and Martín J.F. A squalene epoxidase is involved in biosynthesis of both the antitumor compound clavaric acid and sterols in the basidiomycete H. sublateritium. Chem. Biol. 14 (2007) 1334-1346
23. Hayashi H., Huang P., Takada S., Obinata M., Inoue K., Shibuya M., and Ebizuka Y. Differential expression of three oxidosqualene cyclase mRNAs in Glycyrrhiza glabra. Biol. Pharm. Bull. 27 (2004) 1086-1092
24. Heintz R., Schaefer P.C., and Benveniste P. Cyclisation of squalene 2,3;22,23-diepoxide by microsomes from bramble (Rubus fruticosa) tissues grown in vitro. J. Chem. Soc. D. 15 (1970) 946-947
25. Jayasuriya H., Silverman K.C., Zink D.L., Jenkins R.G., Sánchez M., Pelaez F., Vilella D., Lingham R.B., and Singh S.B. Clavaric acid: a triterpenoid inhibitor of farnesyl-protein transferase from Clavariadelphus truncatus. J. Nat. Prod. 61 (1998) 1568-1570
26. Kawano N., Ichinose K., and Ebizuka Y. Molecular cloning and functional expression of cDNAs encoding oxidosqualene cyclases from Costus speciosus. Biol. Pharm. Bull. 25 (2002) 477-482
27. Kushiro T., Shibuya M., and Ebizuka Y. Beta-amyrin synthase-cloning of oxidosqualene cyclase that catalyzes the formation of the most popular triterpene among higher plants. Eur. J. Biochem. 256 (1998) 238-244
28. Lee S., Park S., Oh J.W., and Yang C. Natural inhibitors for protein prenyltransferase. Planta Med. 64 (1998) 303-308
29. Lingham R.B., Silverman K.C., Jayasuriya H., Kim B.M., Amo S.E., Wilson F.R., Rew D.J., Schaber M.D., Bergstrom J.D., Koblan K.S., Graham S.L., Kohl N.E., Gibbs J.B., and Singh S.B. Clavaric acid and steroidal analogues as Ras- and FPP-directed inhibitors of human farnesyl-protein transferase. J. Med. Chem. 41 (1998) 4492-4501
30. Meyer M.M., Segura M.J., Wilson W.K., and Matsuda S.P. Oxidosqualene cyclase residues that promote formation of cycloartenol, lanosterol, and parkeol. Angew. Chem. Int. Ed. Engl. 39 (2000) 4090-4092
31. Morita M., Shibuya M., Lee M.S., Sankawa U., and Ebizuka Y. Molecular cloning of pea cDNA encoding cycloartenol synthase and its functional expression in yeast. Biol. Pharm. Bull. 20 (1997) 770-775
32. Panagou E.Z., Skandamis P.N., and Nychas G.J. Use of gradient plates to study combined effects of temperature, pH, and NaCl concentration on growth of Monascus ruber van Tieghem, an Ascomycetes fungus isolated from green table olives. Appl. Environ. Microbiol. 71 (2005) 392-399
33. Poralla K. The possible role of a repetitive amino acid motif in evolution of triterpenoid cyclases. Bioorg. Medicinal. Chem. Lett. 4 (1994) 285-290
34. Poralla K., Hewelt A., Prestwich G.D., Abe I., Reipen I., and Sprenger G. A specific amino acid repeat in squalene and oxidosqualene cyclases. Trends Biochem. Sci. 19 (1994) 157-158
35. Roessner C.A., Min C., Hardin S.H., Harris-Haller L.W., Mc Collum J.C., and Scott A.I. Sequence of the Candida albicans erg7 gene. Gene 127 (1993) 149-150
36. Rowan, M.G., Dean, P.D.G., Goodwin, T.W., 1971. The enzymic conversion of squalene, 2(3),22(23)-diepoxide to a-onocerin by a cell-free extract of Ononis spinosa. 12, 229-232.
37. Sambrook J., and Russel D.W. Molecular Cloning: A Laboratory Manual (2001), Cold Spring Harbor Laboratory Press, Cold Spring Harbor
38. Schwede T., Kopp J., Guex N., and Peitsch M.C. SWISS-MODEL: an automated protein homologymodeling server. Nucleic Acids Res. 31 (2003) 3381-3385
39. Shi Z., Buntel C.J., and Griffin J.H. Isolation and characterization of the gene encoding 2,3-oxidosqualene-lanosterol cyclase from Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 91 (1994) 7370-7374
40. Sung C.K., Shibuya M., Sankawa U., and Ebizuka Y. Molecular cloning of cDNA encoding human lanosterol synthase. Biol. Pharm. Bull. 18 (1995) 1459-1461
41. Thoma R., Schulz-Gasch T., D'Arcy B., Benz J., Aebi J., Dehmlow H., Hennig M., Stihle M., and Ruf A. Insight into steroid scaffold formation from the structure of human oxidosqualene cyclase. Nature 432 (2004) 118-122
42. Van Tamelen E.E. Bioorganic characterization and mechanism of the 2,3-oxidosqualene-lanosterol conversion. J. Am. Chem. Soc. 104 (1982) 6480-6481
43. Vilella D., Sanchez M., Platas G., Salazar O., Genilloud O., Royo I., Cascales C., Martin I., Diez T., Silverman K.C., Lingham R.B., Singh S.B., Jayasuriya H., and Peláez F. Inhibitors of farnesylation of Ras from a microbial natural products screening program. J. Ind. Microbiol. Biotechnol. 25 (2000) 315-327
44. Wasser S.P. Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl. Microbiol. Biotechnol. 60 (2002) 258-274
45. Wendt K.U., Poralla K., and Schulz G.E. Structure and function of a squalene cyclase. Science 277 (1997) 1811-1815
46. Young M., Chen H., Lalioti M.D., and Antonarakis S.E. The human lanosterol synthase gene maps to chromosome 21q22.3. Hum. Genet. 97 (1996) 620-624
47. Zhang H., Shibuya M., Yokota S., and Ebizuka Y. Oxidosqualene cyclases from cell suspension cultures of Betula platyphylla var. japonica: molecular evolution of oxidosqualene cyclases in higher plants. Biol. Pharm. Bull. 26 (2003) 642-650