Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme a reductase

Plant Physiology

Volumn 130, Issue 1, 2002, Pages 334-346

  Wentzinger, Laurent F ^a   Bach, Thomas J ^a   Hartmann, Marie Andrée ^a  

^a INST DE BIOL MOLEC DES PLANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; COENZYMES; ENZYME INHIBITION; FEEDBACK; LIPIDS; RNA; SUBSTRATES; TOBACCO;

REGULATORY MECHANISMS;

PLANTS (BOTANY);

MAMMALIA; NICOTIANA; NICOTIANA TABACUM;

EID: 0036740929     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.004655     Document Type: Article

References (55)

1. Attucci S, Aitken SM, Gulick PJ, Ibrahim RK (1995) Farnesyl pyrophosphate synthase from white lupin: molecular cloning, expression, and purification of the expressed protein. Arch Biochem Biophys 321: 493-500
2. Bach TJ, Benveniste P (1997) Cloning of cDNAs or genes encoding enzymes of sterol biosynthesis from plants and other eukaryotes: heterologous expression and complementation analysis of mutations for functional characterization. Prog Lipid Res 36: 197-226
3. Bach TJ, Boronat A, Caelles C, Ferrer A, Weber T, Wettstein A (1991) Aspects related to mevalonate biosynthesis in plants. Lipids 26: 637-648
4. Bach TJ, Rogers DH, Rudney H (1986) Detergent-solubilization, purification, and characterization of membrane-bound 3-hydroxy-3-methylglutaryl coenzyme A reductase from radish seedlings. Eur J Biochem 154: 103-111
5. Baxter A, Fitzgerald BJ, Hutson JL, McCarty AD, Motteram JM, Ross BC, Sapra M, Snowden MA, Watson NS, Williams RJ et al. (1992) Squalestatin 1, a potent inhibitor of squalene synthase, which lowers serum cholesterol in vivo. J Biol Chem 267: 11705-11708
6. Benveniste P (1986) Sterol biosynthesis. Annu Rev Plant Physiol 37: 275-307
7. Bergstrom JD, Kurtz MM, Rew DJ, Amend AM, Karkas JD, Bostedor RG, Bansal VS, Dufresne C, Van Middlesworth FL, Hensens OD et al. (1993) Zaragozic acids: a family of fungal metabolites that are picomolar competitive inhibitors of squalene synthase. Proc Natl Acad Sci USA 90: 80-84
8. 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: 248-254
9. Brown MS, Goldstein JL (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340
10. Chappell J (1995) Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Annu Rev Plant Physiol Plant Mol Biol 46: 521-547
11. Chappell J, Wolf F, Proulx J, Cuellar RE, Saunders C (1995) Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase a rate-limiting step for isoprenoid biosynthesis in plants? Plant Physiol 109: 1337-1343
12. Chomczynski P, Sacchi N (1987) Single step method of RNA isolation by acid guanidium thiocyanate-phenol-chlorophorm extraction. Anal Biol 162: 156-159
13. Clouse SD (2000) Plant development: a role for sterols in embryogenesis. Curr Biol 10: R601-R604
14. Crick DC, Suders J, Kluthe CM, Andres DA, Waechter CJ (1995) Selective inhibition of cholesterol biosynthesis in brain cells by squalestatin 1. J Neurochem 65: 1365-1373
15. Devarenne TP, Shin DH, Back K, Yin S, Chappell J (1998) Molecular characterization of tobacco squalene synthase and regulation in response to fungal elicitor. Arch Biochem Biophys 349: 205-215
16. Enjuto M, Lumbreras V, Matin C, Boronat A (1995) Expression of the Arabidopsis HMG2 gene, encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase, is restricted to meristematic and floral tissues. Plant Cell 7: 517-527
17. Genschik P, Criqui MC, Parmentier Y, Marbach J, Durr A, Fleck J, Jamet E (1992) Isolation and characterization of a cDNA encoding a 3-hydroxy-3-methylglutaryl coenzyme A reductase from Nicotiana sylvestris. Plant Mol Biol 20: 337-341
18. Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343: 425-430
19. Gondet L, Bronner R, Benveniste P (1994) Regulation of sterol content in membranes by subcellular compartmentation of steryl esters accumulating in a sterol-overproducing tobacco mutant. Plant Physiol 105: 509-518
20. Hanley KM, Nicolas O, Donaldson TB, Smith-Monroy C, Robinson GW, Hellmann GM (1996) Molecular cloning, in vitro expression and characterization of a plant squalene synthetase cDNA. Plant Mol Biol 30: 1139-1151
21. Hartmann M-A (1998) Plant sterols and the membrane environment. Trends Plant Sci 3: 170-175
22. Hartmann M-A, Bach TJ (2001) Incorporation of all-trans-farnesol into sterols and ubiquinone in Nicotiana tabacum L. cv Bright Yellow-2 cell cultures. Tetrahedron Lett 42: 655-657
23. Hartmann M-A, Benveniste P (1987) Plant membrane sterols: isolation, identification, and biosynthesis. Methods Enzymol 148: 632-650
24. Haudenschild C, Hartmann M-A (1995) Inhibition of sterol biosynthesis during elicitor-induced accumulation of furanocoumarins in parsley cell suspension cultures. Phytochemistry 40: 1117-1124
25. Hemmerlin A, Bach TJ (2000) Farnesol-induced cell death and stimulation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase activity in tobacco cv Bright Yellow-2 cells. Plant Physiol 123: 1257-1268
26. Hemmerlin A, Fischt I, Bach TJ (2000) Differential interaction of branch-specific inhibitors of isoprenoid biosynthesis with cell cycle progression in tobacco BY-2 cells. Physiol Plant 110: 342-349
27. Jiang G, McKenzie TL, Conrad DG, Shechter I (1993) Transcriptional regulation by lovastatin and 25-hydroxycholesterol in HepG2 cells and molecular cloning and expression of the cDNA for the human hepatic squalene synthase. J Biol Chem 268: 12818-12824
28. Keller RK, Cannons A, Vilsaint F, Zhao Z, Ness GC (1993) Identification and regulation of rat squalene synthetase mRNA. Arch Biochem Biophys 302: 304-306
29. Kribii R, Arro M, Del Arco A, Gonzalez V, Balcells L, Delourme D, Ferrer A, Karst F, Boronat A (1997) Cloning and characterization of the Arabidopsis thaliana SQS1 gene encoding squalene synthase: involvement of the C-terminal region of the enzyme in the channeling of squalene through the sterol pathway. Eur J Biochem 249: 61-69
30. Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50: 47-65
31. Lindsey S, Harwood HJ (1995) Inhibition of mammalian squalene synthetase activity by zaragozic acid A is a result of competitive inhibition followed by mechanism-based irreversible inactivation. J Biol Chem 270: 9083-9096
32. Lopez D, Chambers CM, Keller RK, Ness GC (1998) Compensatory responses to inhibition of hepatic squalene synthase. Arch Biochem Biophys 351: 159-166
33. Milla P, Athenstaedt K, Viola F, Oliaro-Bosso S, Kohlwein SD, Daum G, Balliano G (2002) Yeast oxidosqualene cyclase (Erg7p) is a major component of lipid particles. J Biol Chem 277: 2406-2412
34. Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the "Hela" cell in the cell biology of higher plants. Int Rev Cytol 132: 1-30
35. Nab J, Song SJ, Back K (2001) Partial characterization of farnesyl and geranylgeranyl diphosphatases induced in rice seedlings by UV-C irradiation. Plant Cell Physiol 42: 864-867
36. Ness GC, Eales S, Lopez D, Zhao Z (1994) Regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene expression by sterols and nonsterols in rat liver. Arch Biochem Biophys 308: 420-425
37. Poulter CD (1990) Biosynthesis of nonhead-to-tail terpenes: formation of 1′-1 and 1′-3 linkages. Acc Chem Res 23: 70-77
38. Rahier A, Benveniste P (1989) Mass spectral identification of phytosterols. In WD Nes, E Parish, eds, Analysis of Sterols and Other Significant Steroids. Academic Press, New York, pp 223-250
39. Rohmer M (1999) The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat Prod Rep 16: 565-574
40. Ryder NS (1991) Squalene epoxidase as a target for the allylamines. Biochem Soc Trans 19: 774-777
41. Sakakura Y, Shimano H, Sone H, Takahashi A, Inoue K, Toyoshima H, Suzuki S, Yamada N (2001) Sterol regulatory element-binding proteins induce an entire pathway of cholesterol synthesis. Biochem Biophys Res Comm 286: 176-183
42. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, Ed 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
43. Schäfer UA, Reed DW, Hunter DG, Yao K, Weninger AM, Tsang EWT, Reaney MJT, McKenzie SL, Covello PS (1999) An example of intron junctional sliding in the gene families encoding squalene monooxygenase homologues in Arabidopsis thaliana and Brassica napus. Plant Mol Biol 39: 721-728
44. Schaller H, Grausem B, Benveniste P, Chye ML, Tan CT, Song YH, Chua NH (1995) Expression of the Hevea brasiliensis 3-hydroxy-3-methylglutaryl coenzyme. A reductase in tobacco results in sterol overproduction. Plant Physiol 109: 761-770
45. Schulte AE, van der Heijden R, Verpoorte R (2000) Purification and characterization of mevalonate kinase from suspension-cultured cells of Catharanthus roseus (L.) G. Don. Arch Biochem Biophys 378: 287-298
46. Simmen U, Gisi U (1995) Effects of seed treatment with SAN 789F, a homopropargylamine fungicide, on germination and contents of squalene and sterols of wheat seedlings. Pestic Biochem Physiol 52: 25-32
47. Stermer BA, Bianchini GM, Korth KL (1994) Regulation of HMG-CoA reductase activity in plants. J Lipid Res 35: 1133-1140
48. Tansey TR, Shechter I (2000) Structure and regulation of mammalian squalene synthase. Biochim Biophys Acta 1529: 49-62
49. Taton M, Ullmann P, Benveniste P, Rahier A (1988) Interaction of triazole fungicides and plant growth regulators with microsomal cytochrome P-450-dependent obtusifoliol 14α-methyl demethylase. Pestic Biochem Physiol 30: 178-189
50. Threlfall DR, Whitehead IM (1988) Coordinated inhibition of squalene synthetase and induction of enzymes of sesquiterpenoids phytoalexin biosynthesis in cultures of Nicotiana tabacum. Phytochemistry 27: 2567-2580
51. Vögeli U, Chappell J (1988) Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol 88: 1291-1296
52. Weissenborn DL, Denbow CJ, Laine M, Lång SS, Yang Z, Yu X, Cramer CL (1995) HMG-CoA reductase and terpenoid phytoalexins: molecular specialization within a complex pathway. Physiol Plant 93: 393-400
53. Yates PJ, Haughan PA, Lenton JR, Goad LJ (1991) Effects of terbinafine on growth, squalene, and steryl ester content of a celery cell suspension culture. Pestic Biochem Physiol 40: 221-226
54. 5,7-sterols from terbinafine treated celery cell suspension cultures. Phytochemistry 31: 3051-3058
55. Zook MN, Kuć JA (1991) Induction of sesquiterpene cyclase and suppression of squalene synthase activity in elicitor-treated or fungal-infected potato tuber tissue. Physiol Mol Plant Pathol 39: 377-390