Altered lipid metabolism in a Drosophila model of Friedreich's ataxia

Human Molecular Genetics

Volumn 19, Issue 14, 2010, Pages 2828-2840

  Navarro, Juan A ^a   Ohmann, Elisabeth ^a   Sanchez, Diego ^b   Botella, José A ^a   Liebisch, Gerhard ^a   Moltó, María D ^c   Ganfornina, María D ^b   Schmitz, Gerd ^a   Schneuwly, Stephan ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF VALLADOLID   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN D; FAT DROPLET; FRATAXIN; LIPID; LIPID PEROXIDE; CARRIER PROTEIN; DROSOPHILA PROTEIN; FATTY ACID; GLIAL LAZARILLO PROTEIN, DROSOPHILA; IRON BINDING PROTEIN; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE MODEL; DOWN REGULATION; DROSOPHILA; DYSLIPIDEMIA; FRIEDREICH ATAXIA; GENE EXPRESSION; GENE LOSS; GLIA CELL; LIFESPAN; LIPID PEROXIDATION; MOTOR DYSFUNCTION; NONHUMAN; ORTHOLOGY; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; RNA INTERFERENCE; ANIMAL; BLOOD; CELL SURVIVAL; COMPLICATION; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; GENETICS; GLIA; HUMAN; MALE; METABOLISM; NERVOUS SYSTEM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; FATTY ACIDS; FRIEDREICH ATAXIA; HUMANS; IRON-BINDING PROTEINS; LIPID METABOLISM DISORDERS; LIPID PEROXIDATION; MALE; MEMBRANE GLYCOPROTEINS; NERVOUS SYSTEM; NEUROGLIA; OXIDATIVE STRESS;

EID: 77954464940     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq183     Document Type: Article

References (94)

1. Harding, A.E. (1981) Friedreich's ataxia: a clinical and genetic study of 90 families with an analysis of early diagnostic criteria and intrafamilial clustering of clinical features. Brain, 104, 589-620.
2. Harding, A.E. (1993) Clinical features and classification of inherited ataxias. Adv. Neurol., 61, 1-14.
3. Pandolfo, M. (2009) Friedreich ataxia: the clinical picture. J. Neurol., 256, 3-8.
4. Koeppen, A.H. (1998) The hereditary ataxias. J. Neuropathol. Exp. Neurol., 57, 531-543.
5. Harding, A.E. and Hewer, R.L. (1983) The heart disease of Friedreich's ataxia: a clinical and electrocardiographic study of 115 patients, with an analysis of serial electrocardiographic changes in 30 cases. Q. J. Med., 52, 489-502.
6. Delatycki, M.B., Camakaris, J., Brooks, H., Evans-Whipp, T., Thorburn, D.R., Williamson, R. and Forrest, S.M. (1999) Direct evidence that mitochondrial iron accumulation occurs in Friedreich ataxia. Ann. Neurol., 45, 673-675.
7. Campuzano, V., Montermini, L., Moltó, M.D., Pianese, L., Cossée, M., Cavalcanti, F., Monros, E., Rodius, F., Duclos, F., Monticelli, A. et al. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science, 271, 1423-1427.
8. Campuzano, V., Montermini, L., Lutz, Y., Cova, L., Hindelang, C., Jiralerspong, S., Trottier, Y., Kish, S.J., Faucheux, B., Trouillas, P. et al. (1997) Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet., 6, 1771-1780.
9. Rotig, A., de Lonlay, P., Chretien, D., Foury, F., Koenig, M., Sidi, D., Munnich, A. and Rustin, P. (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet., 17, 215-217.
10. Lodi, R., Cooper, J.M., Bradley, J.L., Manners, D., Styles, P., Taylor, D.J. and Schapira, A.H. (1999) Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia. Proc. Natl Acad. Sci. USA, 96, 11492-11495.
11. Bradley, J.L., Blake, J.C., Chamberlain, S., Thomas, P.K., Cooper, J.M. and Schapira, A.H. (2000) Clinical, biochemical and molecular genetic correlations in Friedreich's ataxia. Hum. Mol. Genet., 9, 275-282.
12. Wong, A., Yang, J., Cavadini, P., Gellera, C., Lonnerdal, B., Taroni, F. and Cortopassi, G. (1999) The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis. Hum. Mol. Genet., 8, 425-430.
13. Santos, R., Buisson, N., Knight, S.A., Dancis, A., Camadro, J.M. and Lesuisse, E. (2004) Candida albicans lacking the frataxin homologue: a relevant yeast model for studying the role of frataxin. Mol. Microbiol., 54, 507-519.
14. Vázquez-Manrique, R.P., González-Cabo, P., Ros, S., Aziz, H., Baylis, H.A. and Palau, F. (2006) Reduction of Caenorhabditis elegans frataxin increases sensitivity to oxidative stress, reduces lifespan, and causes lethality in a mitochondrial complex II mutant. FASEB J., 20, 172-174.
15. Llorens, J.V., Navarro, J.A., Martínez-Sebastián, M.J., Baylies, M.K., Schneuwly, S., Botella, J.A. and Moltó, M.D. (2007) Causative role of oxidative stress in a Drosophila model of Friedreich ataxia. FASEB J., 21, 333-344.
16. Bulteau, A.L., Dancis, A., Gareil, M., Montagne, J.J., Camadro, J.M. and Lesuisse, E. (2007) Oxidative stress and protease dysfunction in the yeast model of Friedreich ataxia. Free Radic. Biol. Med., 42, 1561-1570.
17. Anderson, P.R., Kirby, K., Orr, W.C., Hilliker, A.J. and Phillips, J.P. (2008) Hydrogen peroxide scavenging rescues frataxin deficiency in a Drosophila model of Friedreich's ataxia. Proc. Natl Acad. Sci. USA, 105, 611-616.
18. Emond, M., Lepage, G., Vanasse, M. and Pandolfo, M. (2000) Increased levels of plasma malondialdehyde in Friedreich ataxia. Neurology, 55, 1752-1753.
19. Schulz, J.B., Dehmer, T., Schöls, L., Mende, H., Hardt, C., Vorgerd, M., Bürk, K., Matson, W., Dichgans, J., Beal, M.F. and Bogdanov, M.B. (2000) Oxidative stress in patients with Friedreich ataxia. Neurology, 55, 1719-1721.
20. Tozzi, G., Nuccetelli, M., Lo Bello, M., Bernardini, S., Bellincampi, L., Ballerini, S., Gaeta, L.M., Casali, C., Pastore, A., Federici, G. et al. (2002) Antioxidant enzymes in blood of patients with Friedreich's ataxia. Arch. Dis. Child., 86, 376-379.
21. Burck, U., Goebel, H.H., Kuhlendahl, H.D., Meier, C. and Goebel, K.M. (1981) Neuromyopathy and vitamin E deficiency in man. Neuropediatrics, 12, 267-278.
22. Watmough, N.J., Bindoff, L.A., Birch-Machin, M.A., Jackson, S., Bartlett, K., Ragan, C.I., Poulton, J., Gardiner, R.M., Sherratt, H.S. and Turnbull, D.M. (1990) Impaired mitochondrial beta-oxidation in a patient with an abnormality of the respiratory chain. Studies in skeletal muscle mitochondria. J. Clin. Invest., 85, 177-184.
23. Xu, Y., Condell, M., Plesken, H., Edelman-Novemsky, I., Ma, J., Ren, M. and Schlame, M. (2006) A Drosophila model of Barth syndrome. Proc. Natl Acad. Sci. USA, 103, 11584-11588.
24. Picklo, M.J. and Montine, T.J. (2007) Mitochondrial effects of lipid-derived neurotoxins. J. Alzheimers Dis., 12, 185-193.
25. Adibhatla, R.M. and Hatcher, J.F. (2008) Altered lipid metabolism in brain injury and disorders. Subcell. Biochem., 49, 241-268.
26. Adibhatla, R.M. and Hatcher, J.F. (2008) Phospoholipase A(2), reactive oxygen species and lipid peroxidation in CNS pathologies. BMB Rep., 41, 560-567.
27. Lessing, D. and Bonini, N.M. (2009) Maintaining the brain: insight into human neurodegeneration from Drosophila melanogaster mutants. Nat. Rev. Genet., 10, 359-370.
28. Feki, M., Belal, S., Feki, H., Souissi, M., Frih-Ayed, M., Kaabachi, N., Hentati, F., Ben Hamida, M. and Mebazaa, A. (2002) Serum vitamin E and lipid-adjusted vitamin E assessment in Friedreich ataxia phenotype patients and unaffected family members. Clin. Chem., 48, 577-579.
29. Iorio, L., De Michele, G., Filla, A., Di Martino, L., Postiglione, A., Patti, L. and Campanella, G. (1993) Serum lipoprotein fatty acid profile in hereditary ataxias. Can. J. Neurol. Sci., 20, 206-209.
30. Walker, J.L., Chamberlain, S. and Robinson, N. (1980) Failure to detect abnormal fatty acid profiles in serum lipoproteins in Friedreich's ataxia. Ann. Neurol., 8, 74-76.
31. Ross, B.M., Eder, K., Moszczynska, A., Mamalias, N., Lamarche, J., Ang, L., Pandolfo, M., Rouleau, G., Kirchgessner, M. and Kish, S.J. (2000) Abnormal activity of membrane phospholipid synthetic enzymes in the brain of patients with Friedreich's ataxia and spinocerebellar atrophy type-1. Mov. Disord., 15, 294-300.
32. Eder, K., Kish, S.J., Kirchgessner, M. and Ross, B.M. (1998) Brain phospholipids and fatty acids in Friedreich's ataxia and spinocerebellar atrophy type-1. Mov. Disord., 13, 813-819.
33. Puccio, H., Simon, D., Cossée, M., Criqui-Filipe, P., Tiziano, F., Melki, J., Hindelang, C., Matyas, R., Rustin, P. and Koenig, M. (2001) Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet., 27, 181-186.
34. Rassart, E., Bedirian, A., Do Carmo, S., Guinard, O., Sirois, J., Terrisse, L. and Milne, R. (2000) Apolipoprotein D. Biochim. Biophys. Acta, 1482, 185-198.
35. Ganfornina, M.D., Sanchez, D., Greene, L.H. and Flower, D.R. (2006) The lipocalin protein family: protein sequence, structure and relationships to the calycin superfamily. In Akerström, B., Borregaard, N., Flower, D.R. and Salier, J.P. (eds), Lipocalins. Landes Bioscience, Georgetown, TX, pp. 17-27.
36. Vogt, M. and Skerra, A. (2001) Bacterially produced apolipoprotein D binds progesterone and arachidonic acid, but not bilirubin or E-3M2H. J. Mol. Recognit., 14, 79-86.
37. Sánchez, D., Ganfornina, M.D., Torres-Schumann, S., Speese, S.D., Lora, J.M. and Bastiani, M.J. (2000) Characterization of two novel lipocalins expressed in the Drosophila embryonic nervous system. Int. J. Dev. Biol., 44, 349-359.
38. Navarro, A., Del Valle, E. and Tolivia, J. (2004) Differential expression of apolipoprotein D in human astroglial and oligodendroglial cells. J. Histochem. Cytochem., 52, 1031-1036.
39. Sanchez, D., López-Arias, B., Torroja, L., Canal, I., Wang, X., Bastiani, M.J. and Ganfornina, M.D. (2006) Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Curr. Biol., 16, 680-686.
40. Charron, J.B., Ouellet, F., Houde, M. and Sarhan, F. (2008) The plant apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biol., 8, 86-98.
41. Ganfornina, M.D., Do Carmo, S., Lora, J.M., Torres-Schumann, S., Vogel, M., Allhorn, M., González, C., Bastiani, M.J., Rassart, E. and Sanchez, D. (2008) Apolipoprotein D is involved in the mechanisms regulating protection from oxidative stress. Aging Cell, 7, 506-515.
42. Walker, D.W., Muffat, J., Rundel, C. and Benzer, S. (2006) Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Curr. Biol., 16, 674-679.
43. Muffat, J., Walker, D.W. and Benzer, S. (2008) Human ApoD, an apolipoprotein up-regulated in neurodegenerative diseases, extends lifespan and increases stress resistance in Drosophila. Proc. Natl Acad. Sci. USA, 105, 7088-7093.
44. Hughes, J.T., Brownell, B. and Hewer, R.L. (1968) The peripheral sensory pathway in Friedreich's ataxia. An examination by light and electron microscopy of the posterior nerve roots, posterior root ganglia, and peripheral sensory nerves in cases of Friedreich's ataxia. Brain, 91, 803-818.
45. Simon, D., Seznec, H., Gansmuller, A., Carelle, N., Weber, P., Metzger, D., Rustin, P., Koenig, M. and Puccio, H. (2004) Friedreich ataxia mouse models with progressive cerebellar and sensory ataxia reveal autophagic neurodegeneration in dorsal root ganglia. J. Neurosci., 24, 1987-1995.
46. Al-Mahdawi, S., Pinto, R.M., Varshney, D., Lawrence, L., Lowrie, M.B., Hughes, S., Webster, Z., Blake, J., Cooper, J.M., King, R. and Pook, M.A. (2006) GAA repeat expansion mutation mouse models of Friedreich ataxia exhibit oxidative stress leading to progressive neuronal and cardiac pathology. Genomics, 88, 580-590.
47. Sepp, K.J., Schulte, J. and Auld, V.J. (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev. Biol., 238, 47-63.
48. Campbell, G., Göring, H., Lin, T., Spana, E., Andersson, S., Doe, C.Q. and Tomlinson, A. (1994) RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development, 120, 2957-2966.
49. Anderson, P.R., Kirby, K., Hilliker, A.J. and Phillips, J.P. (2005) RNAi-mediated suppression of the mitochondrial iron chaperone, frataxin, in Drosophila. Hum. Mol. Genet., 14, 3397-3405.
50. Gruenewald, C., Botella, J.A., Bayersdorfer, F., Navarro, J.A. and Schneuwly, S. (2009) Hyperoxia-induced neurodegeneration as a tool to identify neuroprotective genes in Drosophila melanogaster. Free Radic. Biol. Med., 46, 1668-1676.
51. De Martino, C., Natali, P.G., Bruni, C.B. and Accinni, L. (1968) Influence of plastic embedding media on staining and morphology of lipid bodies. A light and ultrastructural study. Histochemie, 16, 350-360.
52. Marmolino, D., Acquaviva, F., Pinelli, M., Monticelli, A., Castaldo, I., Filla, A. and Cocozza, S. (2009) PPAR-gamma agonist azelaoyl PAF increases frataxin protein and mRNA expression. New implications for the Friedreich's ataxia therapy. Cerebellum, 8, 98-103.
53. Shapcott, D., Melancon, S., Butterworth, R.F., Khoury, K., Collu, R., Breton, G., Geoffroy, G., Lemieux, B. and Barbeau, A. (1976) Glucose and insulin metabolism in Friedreich's ataxia. Can. J. Neurol. Sci., 3, 361-364.
54. Petersen, K.F., Dufour, S., Befroy, D., Garcia, R. and Shulman, G.I. (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med., 350, 664-671.
55. Befroy, D.E., Petersen, K.F., Dufour, S., Mason, G.F., de Graaf, R.A., Rothman, D.L. and Shulman, G.I. (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes, 56, 1376-1381.
56. Vankoningsloo, S., Piens, M., Lecocq, C., Gilson, A., De Pauw, A., Renard, P., Demazy, C., Houbion, A., Raes, M. and Arnould, T.J. (2005) Mitochondrial dysfunction induces triglyceride accumulation in 3T3-L1 cells: role of fatty acid beta-oxidation and glucose. Lipid Res., 46, 1133-1149.
57. Zahavi, M. and Tahori, A.S. (1965) Citric acid accumulation with age in houseflies and other Diptera. J. Insect Physiol., 11, 811-816.
58. Tong, W.H. and Rouault, T.A. (2007) Metabolic regulation of citrate and iron by aconitases: role of iron-sulfur cluster biogenesis. Biometals, 20, 549-564.
59. Coppola, G., Marmolino, D., Lu, D., Wang, Q., Cnop, M., Rai, M., Acquaviva, F., Cocozza, S., Pandolfo, M. and Geschwind, D.H. (2009) Functional genomic analysis of frataxin deficiency reveals tissue-specific alterations and identifies the PPAR {gamma} pathway as a therapeutic target in Friedreich's ataxia. Hum. Mol. Genet., 18, 2452-2461.
60. Sutak, R., Xu, X., Whitnall, M., Kashem, M.A., Vyoral, D. and Richardson, D.R. (2008) Proteomic analysis of hearts from frataxin knockout mice: marked rearrangement of energy metabolism, a response to cellular stress and altered expression of proteins involved in cell structure, motility and metabolism. Proteomics, 8, 1731-1741.
61. Nicolson, G.L. (2007) Metabolic syndrome and mitochondrial function: molecular replacement and antioxidant supplements to prevent membrane peroxidation and restore mitochondrial function. J. Cell. Biochem., 100, 1352-1369.
62. Busi, M.V., Maliandi, M.V., Valdez, H., Clemente, M., Zabaleta, E.J., Araya, A. and Gomez-Casati, D.F. (2006) Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe-S proteins and induces oxidative stress. Plant J., 48, 873-882.
63. Condò, I., Ventura, N., Malisan, F., Tomassini, B. and Testi, R. (2006) A pool of extramitochondrial frataxin that promotes cell survival. J. Biol. Chem., 281, 16750-16756.
64. Napoli, E., Taroni, F. and Cortopassi, G.A. (2006) Frataxin, iron-sulfur clusters, heme, ROS, and aging. Antioxid. Redox Signal., 8, 506-516.
65. Irazusta, V., Moreno-Cermeño, A., Cabiscol, E., Ros, J. and Tamarit, J. (2008) Major targets of iron-induced protein oxidative damage in frataxin-deficient yeasts are magnesium-binding proteins. Free Radic. Biol. Med., 44, 1712-1723.
66. Rustin, P., Von Kleist-Retzow, J.C., Chantrel-Groussard, K., Sidi, D., Munnich, A. and Rötig, A. (1999) Effect of idebenone on cardiomyopathy in Friedreich's ataxia: a preliminary study. Lancet, 354, 477-479.
67. Shoichet, S.A., Bäumer, A.T., Stamenkovic, D., Sauer, H., Pfeiffer, A.F., Kahn, C.R., Müller-Wieland, D., Richter, C. and Ristow, M. (2002) Frataxin promotes antioxidant defense in a thiol-dependent manner resulting in diminished malignant transformation in vitro. Hum. Mol. Genet., 11, 815-821.
68. Runko, A.P., Griswold, A.J. and Min, K.T. (2008) Overexpression of frataxin in the mitochondria increases resistance to oxidative stress and extends lifespan in Drosophila. FEBS Lett., 582, 715-719.
69. 2+ and includes lipid peroxidation and alterations in membrane proteins. Arch. Biochem. Biophys., 308, 158-164.
70. Castilho, R.F., Meinicke, A.R., Vercesi, A.E. and Hermes-Lima, M. (1999) The role of Fe(III) in Fe(II)-citrate mediated peroxidation of mitochondrial membrane lipids. Mol. Cell. Biochem., 196, 163-168.
71. Liochev, S.I. (1999) The mechanism of 'Fenton-like' reactions and their importance for biological systems. A biologist's view. Met. Ions Biol. Syst., 36, 1-39.
72. Chen, O.S., Hemenway, S. and Kaplan, J. (2002) Genetic analysis of iron citrate toxicity in yeast: implications for mammalian iron homeostasis. Proc. Natl Acad. Sci. USA, 99, 16922-16927.
73. Babcock, M., de Silva, D., Oaks, R., Davis-Kaplan, S., Jiralerspong, S., Montermini, L., Pandolfo, M. and Kaplan, J. (1997) Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science, 276, 1709-1712.
74. Pandolfo, M. and Koenig, M. (1998) Friedreich's ataxia. In Wells, R.D. and Warren, S.T. (eds), Genetic Instabilities and Hereditary Neurological Diseases, Academic Press, Texas A&M University, Houston, USA, pp. 371-398.
75. Lu, C., Schoenfeld, R., Shan, Y., Tsai, C., Hammock, B. and Cortopassi, G. (2009) Frataxin deficiency induces Schwann cell inflammation and death. Biochim. Biophys. Acta, 1792, 1052-1061.
76. Sanchez, D., Ortega-Cubero, S., Akerström, B., Herrera, M., Bastiani, M.J. and Ganfornina, M.D. (2008) Molecular interactions of the neuronal GPI-anchored lipocalin Lazarillo. J. Mol. Recognit., 21, 313-323.
77. Do Carmo, S., Fournier, D., Mounier, C. and Rassart, E. (2009) Human apolipoprotein D overexpression in transgenic mice induces insulin resistance and alters lipid metabolism. Am. J. Physiol. Endocrinol. Metab., 296, E802-E811.
78. Hull-Thompson, J., Muffat, J., Sanchez, D., Walker, D.W., Benzer, S., Ganfornina, M.D. and Jasper, H. (2009) Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLoS Genet., 5, e1000460.
79. Thomas, E.A. and Yao, J.K. (2007) Clozapine specifically alters the arachidonic acid pathway in mice lacking apolipoprotein D. Schizophr. Res., 89, 147-153.
80. Lechner, M., Wojnar, P. and Redl, B. (2001) Human tear lipocalin acts as an oxidative-stress induced scavenger of potentially harmful lipid peroxidation products in a cell culture system. Biochem. J., 356, 129-135.
81. Kakhlon, O., Manning, H., Breuer, W., Melamed-Book, N., Lu, C., Cortopassi, G., Munnich, A. and Cabantchik, Z.I. (2008) Cell functions impaired by frataxin deficiency are restored by drug-mediated iron relocation. Blood, 112, 5219-5227.
82. Zanella, I., Derosas, M., Corrado, M., Cocco, E., Cavadini, P., Biasiotto, G., Poli, M., Verardi, R. and Arosio, P. (2008) The effects of frataxin silencing in HeLa cells are rescued by the expression of human mitochondrial ferritin. Biochim. Biophys. Acta, 1782, 90-98.
83. O'Neill, H.A., Gakh, O., Park, S., Cui, J., Mooney, S.M., Sampson, M., Ferreira, G.C. and Isaya, G. (2005) Assembly of human frataxin is a mechanism for detoxifying redox-active iron. Biochemistry, 44, 537-545.
84. Gakh, O., Park, S., Liu, G., Macomber, L., Imlay, J.A., Ferreira, G.C. and Isaya, G. (2006) Mitochondrial iron detoxification is a primary function of frataxin that limits oxidative damage and preserves cell longevity. Hum. Mol. Genet., 15, 467-479.
85. Adinolfi, S., Iannuzzi, C., Prischi, F., Pastore, C., Iametti, S., Martin, S.R., Bonomi, F. and Pastore, A. (2009) Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS. Nat. Struct. Mol. Biol., 16, 390-396.
86. Chantrel-Groussard, K., Geromel, V., Puccio, H., Koenig, M., Munnich, A., Rötig, A. and Rustin, P. (2001) Disabled early recruitment of antioxidant defenses in Friedreich's ataxia. Hum. Mol. Genet., 10, 2061-2067.
87. Jiralerspong, S., Ge, B., Hudson, T.J. and Pandolfo, M. (2001) Manganese superoxide dismutase induction by iron is impaired in Friedreich ataxia cells. FEBS Lett., 509, 101-105.
88. Paupe, V., Dassa, E.P., Goncalves, S., Auchère, F., Lönn, M., Holmgren, A. and Rustin, P. (2009) Impaired nuclear Nrf2 translocation undermines the oxidative stress response in Friedreich ataxia. PLoS ONE, 4, e4253.
89. Van Dijk, W., Do Carmo, S., Rassart, E., Dahlbäck, B. and Sodetz, J.M. (2006) The plasma lipocalins a1-acid glycoprotein, apolipoprotein D, apolipoprotein M and complement protein C8g. In Akerström, B., Borregaard, N., Flower, D.R. and Salier, J.P. (eds), Lipocalins, Landes Bioscience, Georgetown, TX, pp. 140-166.
90. Do Carmo, S., Jacomy, H., Talbot, P.J. and Rassart, E. (2008) Neuroprotective effect of apolipoprotein D against human coronavirus OC43-induced encephalitis in mice. J. Neurosci., 28, 10330-10338.
91. He, X., Jittiwat, J., Kim, J.H., Jenner, A.M., Farooqui, A.A., Patel, S.C. and Ong, W.Y. (2009) Apolipoprotein D modulates F2-isoprostane and 7-ketocholesterol formation and has a neuroprotective effect on organotypic hippocampal cultures after kainate-induced excitotoxic injury. Neurosci. Lett., 455, 183-186.
92. Perrimon, N. and Mathey-Prevot, B. (2007) Matter arising: off-targets and genome-scale RNAi screens in Drosophila. Fly (Austin), 1,1-5.
93. Botella, J.A., Ulschmid, J.K., Gruenewald, C., Moehle, C., Kretzschmar, D., Becker, K. and Schneuwly, S. (2004) The Drosophila carbonyl reductase sniffer prevents oxidative stress-induced neurodegeneration. Curr. Biol., 14, 782-786.
94. Bligh, E.G. and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 37, 911-917.