The NADPH-cytochrome P450 reductase family in Trypanosoma cruzi is involved in the sterol biosynthesis pathway

International Journal for Parasitology

Volumn 41, Issue 1, 2011, Pages 99-108

  De Vas, Matías G ^a,b,c   Portal, Patricio ^a   Alonso, Guillermo D ^a,b   Schlesinger, Mariana ^a   Flawiá, Mirtha M ^a,b   Torres, Héctor N ^a,b   Villamil, Silvia Fernández ^a   Paveto, Cristina ^a  

^a INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Sorbonne Universités   (France)

Author keywords

NADPH dependent cytochrome P450 reductases; Sterol metabolism; Trypanosoma cruzi

Indexed keywords

GENOMIC DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE;

CYTOCHROME; ENZYME ACTIVITY; GENE EXPRESSION; METABOLISM; PARASITE; STEROL;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA CONTENT; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; GENE OVEREXPRESSION; IMMUNOFLUORESCENCE MICROSCOPY; MEMBRANE FLUIDITY; MEMBRANE PERMEABILITY; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEROL SYNTHESIS; TRANSGENE; TRYPANOSOMA CRUZI;

ANIMALS; BIOSYNTHETIC PATHWAYS; CELL MEMBRANE; GENE EXPRESSION; NADP; NADPH-FERRIHEMOPROTEIN REDUCTASE; ORGANELLES; PHAGOCYTOSIS; STEROLS; TRYPANOSOMA CRUZI;

TRYPANOSOMA CRUZI;

EID: 78650176906     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2010.07.016     Document Type: Article

References (74)

1. Albi E., Viola Magni M.P. The role of intranuclear lipids. Biol. Cell 2004, 96:657-667.
2. Aoyama Y., Yoshida Y., Sonoda Y., Sato Y. Deformylation of 32-oxo-24, 25-dihydrolanosterol by the purified cytochrome P-45014DM (lanosterol 14 alpha-demethylase) from yeast evidence confirming the intermediate step of lanosterol 14 alpha-demethylation. J. Biol. Chem. 1989, 264:18502-18505.
3. Aoyama Y., Noshiro M., Gotoh O., Imaoka S., Funae Y., Kurosawa N., et al. Sterol 14-demethylase P450 (P45014DM*) is one of the most ancient and conserved P450 species. J. Biochem. 1996, 119:926-933.
4. Arora A., Raghuraman H., Chattopadhyay A. Influence of cholesterol and ergosterol on membrane dynamics: a fluorescence approach. Biochem. Biophys. Res. Commun. 2004, 318:920-926.
5. + metabolism in health and disease. Trends Biochem. Sci. 2007, 32:12-19.
6. Berger F., Ramirez-Hernandez M.H., Ziegler M. The new life of a centenarian: signalling functions of NAD(P). Trends Biochem. Sci. 2004, 29:111-118.
7. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959, 37:911-917.
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
9. Braga M.V., Urbina J.A., de Souza W. Effects of squalene synthase inhibitors on the growth and ultrastructure of Trypanosoma cruzi. Int. J. Antimicrob. Agents 2004, 24:72-78.
10. Cannon R.D., Kerridge D. Correlation between the sterol composition of membranes and morphology in Candida albicans. J. Med. Vet. Mycol. 1988, 26:57-65.
11. Conney A.H. Pharmacological implications of microsomal enzyme induction. Pharmacol. Rev. 1967, 19:317-366.
12. Cournia Z., Ullmann G.M., Smith J.C. Differential effects of cholesterol, ergosterol and lanosterol on a dipalmitoyl phosphatidylcholine membrane: a molecular dynamics simulation study. J. Phys. Chem. B 2007, 111:1786-1801.
13. Das A., Sligar S.G. Modulation of the cytochrome P450 reductase redox potential by the phospholipid bilayer. Biochemistry 2009, 48:12104-12112.
14. de Souza W., Rodrigues J.C. Sterol biosynthesis pathway as target for anti-trypanosomatid drugs. Interdiscip Perspect Infect Dis 2009, 2009:642502.
15. Denisov I.G., Makris T.M., Sligar S.G., Schlichting I. Structure and chemistry of cytochrome P450. Chem. Rev. 2005, 105:2253-2277.
16. Dixon H., Ginger C.D., Williamson J. Trypanosome sterols and their metabolic origins. Comp Biochem Physiol B 1972, 41:1-18.
17. Esteves M.G., Gonzales-Perdomo M., Alviano C.S., Angluster J., Goldenberg S. Changes in fatty acid composition associated with differentiation of Trypanosoma cruzi. FEMS Microbiol. Lett. 1989, 50:31-34.
18. Florin-Christensen M., Florin-Christensen J., de Isola E.D., Lammel E., Meinardi E., Brenner R.R., Rasmussen L. Temperature acclimation of Trypanosoma cruzi epimastigote and metacyclic trypomastigote lipids. Mol. Biochem. Parasitol. 1997, 88:25-33.
19. Garzoni L.R., Caldera A., Meirelles Mde N., de Castro S.L., Docampo R., Meints G.A. Selective in vitro effects of the farnesyl pyrophosphate synthase inhibitor risedronate on Trypanosoma cruzi. Int. J. Antimicrob. Agents 2004, 23:273-285.
20. Gelboin H.V. Carcinogens, enzyme induction, and gene action. Adv. Cancer Res. 1967, 10:1-81.
21. Gibbs R.A., Weinstock G.M., Metzker M.L., Muzny D.M., Sodergren E.J., Scherer Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 2004, 428:493-521.
22. Gillette J.R. Biochemistry of drug oxidation and reduction by enzymes in hepatic endoplasmic reticulum. Adv. Pharmacol. 1966, 4:219-261.
23. Gillette J.R., Davis D.C., Sasame H.A. Cytochrome P-450 and its role in drug metabolism. Annu Rev Pharmacol 1972, 12:57-84.
24. Gonzalez-Kristeller D.C., Farage L., Fiorini L.C., Loomis W.F., da Silva A.M. The P450 oxidoreductase, RedA, controls development beyond the mound stage in Dictyostelium discoideum. BMC Dev. Biol 2008, 8:8.
25. Guhl F. Chagas disease in Andean countries. Mem. Inst. Oswaldo Cruz 2007, 102(Suppl. 1):29-38.
26. Hankins E.G., Gillespie J.R., Aikenhead K., Buckner F.S. Upregulation of sterol C14-demethylase expression in Trypanosoma cruzi treated with sterol biosynthesis inhibitors. Mol. Biochem. Parasitol. 2005, 144(1):68-75.
27. Hammarton T.C., Monnerat S., Mottram J.C. Cytokinesis in trypanosomatids. Curr. Opin. Microbiol. 2007, 10:520-527.
28. Hannemann F., Bichet A., Ewen K.M., Bernhardt R. Cytochrome P450 systems - biological variations of electron transport chains. Biochim. Biophys. Acta 2007, 1770:330-344.
29. Iyanagi T. Structure and function of NADPH-cytochrome P450 reductase and nitric oxide synthase reductase domain. Biochem. Biophys. Res. Commun. 2005, 338:520-528.
30. Jandrositz A., Turnowsky F., Hogenauer G. The gene encoding squalene epoxidase from Saccharomyces cerevisiae: cloning and characterization. Gene 1991, 107:155-160.
31. Kaneda Y., Nagakura K., Goutsu T. Lipid composition of three morphological stages of Trypanosoma cruzi. Comp Biochem Physiol B 1986, 83:533-536.
32. Kelly S.L., Lamb D.C., Corran A.J., Baldwin B.C., Parks L.W., Kelly D.E. Purification and reconstitution of activity of Saccharomyces cerevisiae P450 61, a sterol delta 22-desaturase. FEBS Lett. 1995, 377:217-220.
33. Koopmann E., Hahlbrock K. Differentially regulated NADPH:cytochrome P450 oxidoreductases in parsley. Proc. Natl Acad. Sci. USA 1997, 94:14954-14959.
34. Korn E.D., Von Brand T., Tobie E.J. The sterols of Trypanosoma cruzi and Crithidia fasciculata. Comp. Biochem. Physiol. 1969, 30:601-610.
35. Kuwahara T., White R.A., Agosin M. A cytosolic FAD-containing enzyme catalyzing cytochrome c reduction in Trypanosoma cruzi. I. Purification and some properties. Arch. Biochem. Biophys. 1985, 239:18-28.
36. Kwasnicka-Crawford D.A., Vincent S.R. Role of a novel dual flavin reductase (NR1) and an associated histidine triad protein (DCS-1) in menadione-induced cytotoxicity. Biochem. Biophys. Res. Commun. 2005, 336:565-571.
37. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
38. Lees N.D., Broughton M.C., Sanglard D., Bard M. Azole susceptibility and hyphal formation in a cytochrome P-450-deficient mutant of Candida albicans. Antimicrob. Agents Chemother. 1990, 34:831-836.
39. Lees N.D., Skaggs B., Kirsch D.R., Bard M. Cloning of the late genes in the ergosterol biosynthetic pathway of Saccharomyces cerevisiae - a review. Lipids 1995, 30:221-226.
40. Lees N.D., Bard M., Kirsch D.R. Biochemistry and molecular biology of sterol synthesis in Saccharomyces cerevisiae. Crit. Rev. Biochem. Mol. Biol. 1999, 34:33-47.
41. Leonardo M.R., Dailly Y., Clark D.P. Role of NAD in regulating the adhE gene of Escherichia coli. J. Bacteriol. 1996, 178:6013-6018.
42. Lepesheva, G.I., Hargrove, T.Y., Anderson S., Kleshchenko Y., Futak, V., Wawrzak, Z., Villalta, F., Waterman, M.R. (in press). Structural insights into inhibition of sterol 14α-demethylase in the human pathogen Trypanosoma cruzi. J. Biol. Chem.
43. Matsumura H., Miyachi S. Cycling assay for nicotinamide adenine dinucleotides. Methods Enzymol. 1980, 69:465-470.
44. Mercer E.I. Inhibitors of sterol biosynthesis and their applications. Prog. Lipid Res. 1993, 32:357-416.
45. Meyer H., Holz G.G. Biosynthesis of lipids by kinetoplastid flagellates. J. Biol. Chem. 1966, 241:5000-5007.
46. Mukhopadhyay K., Kohli A., Prasad R. Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrob. Agents Chemother. 2002, 46:3695-3705.
47. Murataliev M.B., Feyereisen R., Walker F.A. Electron transfer by diflavin reductases. Biochim. Biophys. Acta 2004, 1698:1-26.
48. Nicoletti I., Migliorati G., Pagliacci M.C., Grignani F., Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 1991, 139:271-279.
49. Nyholm T., Nylund M., Soderholm A., Slotte J.P. Properties of palmitoyl phosphatidylcholine, sphingomyelin, and dihydrosphingomyelin bilayer membranes as reported by different fluorescent reporter molecules. Biophys. J. 2003, 84:987-997.
50. Paine M.J., Garner A.P., Powell D., Sibbald J., Sales M., Pratt N. Cloning and characterization of a novel human dual flavin reductase. J. Biol. Chem. 2000, 275:1471-1478.
51. Parasassi T., De Stasio G., d'Ubaldo A., Gratton E. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys. J. 1990, 57:1179-1186.
52. Parks L.W., Casey W.M. Physiological implications of sterol biosynthesis in yeast. Annu. Rev. Microbiol. 1995, 49:95-116.
53. Pena-Diaz J., Montalvetti A., Flores C.L., Constan A., Hurtado-Guerrero R., De Souza W., et al. Mitochondrial localization of the mevalonate pathway enzyme 3-hydroxy-3-methyl-glutaryl-CoA reductase in the Trypanosomatidae. Mol. Biol. Cell 2004, 15:1356-1363.
54. Pereira C.A., Alonso G.D., Paveto M.C., Iribarren A., Cabanas M.L., Torres H.N., Flawia M.M. Trypanosoma cruzi arginine kinase characterization and cloning. A novel energetic pathway in protozoan parasites. J. Biol. Chem. 2000, 275:1495-1501.
55. Pollak N., Dolle C., Ziegler M. The power to reduce: pyridine nucleotides - small molecules with a multitude of functions. Biochem. J. 2007, 402:205-218.
56. Portal P., Villamil S.F., Alonso G.D., De Vas M.G., Flawia M.M., Torres H.N., Paveto C. Multiple NADPH-cytochrome P450 reductases from Trypanosoma cruzi suggested role on drug resistance. Mol. Biochem. Parasitol. 2008, 160:42-51.
57. Porter T.D., Wilson T.E., Kasper C.B. Expression of a functional 78,000 dalton mammalian flavoprotein, NADPH-cytochrome P-450 oxidoreductase, in Escherichia coli. Arch. Biochem. Biophys. 1987, 254:353-367.
58. Quinones W., Urbina J.A., Dubourdieu M., Luis Concepcion J. The glycosome membrane of Trypanosoma cruzi epimastigotes: protein and lipid composition. Exp. Parasitol. 2004, 106:135-149.
59. Roberts C.W., McLeod R., Rice D.W., Ginger M., Chance M.L., Goad L.J. Fatty acid and sterol metabolism: potential antimicrobial targets in apicomplexan and trypanosomatid parasitic protozoa. Mol. Biochem. Parasitol. 2003, 126:129-142.
60. Rodrigues C.O., Catisti R., Uyemura S.A., Vercesi A.E., Lira R., Rodriguez C., et al. The sterol composition of Trypanosoma cruzi changes after growth in different culture media and results in different sensitivity to digitonin-permeabilization. J. Eukaryot. Microbiol. 2001, 48:588-594.
61. Rohloff P., Montalvetti A., Docampo R. Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi. J. Biol. Chem. 2004, 279:52270-52281.
62. Sant'Anna C., de Souza W., Cunha E.S.N. Biogenesis of the reservosomes of Trypanosoma cruzi. Microsc. Microanal. 2004, 10:637-646.
63. Sant'Anna C., Nakayasu E.S., Pereira M.G., Lourenco D., de Souza W., Almeida I.C., Cunha E.S.N.L. Subcellular proteomics of Trypanosoma cruzi reservosomes. Proteomics 2009, 9:1782-1794.
64. Santa-Rita R.M., Lira R., Barbosa H.S., Urbina J.A., de Castro S.L. Anti-proliferative synergy of lysophospholipid analogues and ketoconazole against Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae): cellular and ultrastructural analysis. J. Antimicrob. Chemother. 2005, 55:780-784.
65. Skaggs B.A., Alexander J.F., Pierson C.A., Schweitzer K.S., Chun K.T., Koegel C., et al. Cloning and characterization of the Saccharomyces cerevisiae C-22 sterol desaturase gene, encoding a second cytochrome P-450 involved in ergosterol biosynthesis. Gene 1996, 169:105-109.
66. Urbina J.A., Vivas J., Ramos H., Larralde G., Aguilar Z., Avilan L. Alteration of lipid order profile and permeability of plasma membranes from Trypanosoma cruzi epimastigotes grown in the presence of ketoconazole. Mol. Biochem. Parasitol. 1988, 30:185-195.
67. Urbina J.A. Ergosterol biosynthesis and drug development for Chagas disease. Mem. Inst. Oswaldo Cruz 2009, 104(Suppl. 1):311-318.
68. Vanden Bossche H. Chemotherapy of Human Fungal Infections 1995, Gustav Fisher Verlag, Jena, Germany.
69. Vazquez M.P., Levin M.J. Functional analysis of the intergenic regions of TcP2beta gene loci allowed the construction of an improved Trypanosoma cruzi expression vector. Gene 1999, 239:217-225.
70. Vernis L., Facca C., Delagoutte E., Soler N., Chanet R., Guiard B., et al. A newly identified essential complex, Dre2-Tah18, controls mitochondria integrity and cell death after oxidative stress in yeast. PLoS ONE 2009, 4:e4376.
71. + and NADH in brain functions, brain diseases and brain aging. Front Biosci 2007, 12:1863-1888.
72. + and NADH in neuronal death. J Neuroimmune Pharmacol 2007, 2:270-275.
73. +/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid. Redox Signal. 2008, 10:179-206.
74. Yoshida Y. Cytochrome P450 of fungi: primary target for azole antifungal agents. Curr. Top. Med. Mycol. 1988, 2:388-418.