Frataxin knockdown causes loss of cytoplasmic iron-sulfur cluster functions, redox alterations and induction of heme transcripts

Archives of Biochemistry and Biophysics

Volumn 457, Issue 1, 2007, Pages 111-122

  Lu, Chunye ^a   Cortopassi, Gino ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Frataxin; Heme pathway; Iron sulfur cluster; Redox alterations; RNAi; Unfolded protein response

Indexed keywords

5 AMINOLEVULINATE SYNTHASE; ACONITATE HYDRATASE; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C; CYTOPLASM PROTEIN; FRATAXIN; HEME; IRON SULFUR PROTEIN; MITOCHONDRIAL ENZYME; SMALL INTERFERING RNA;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; ENZYME ACTIVITY; ENZYME INDUCTION; FRIEDREICH ATAXIA; HEME SYNTHESIS; HUMAN; HUMAN CELL; KNOCKOUT GENE; MITOCHONDRION; NEUROLOGIC DISEASE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DEFICIENCY; PROTEIN FOLDING; PROTEIN FUNCTION; TRANSCRIPTION REGULATION;

CELL LINE; CYTOCHROMES C; CYTOPLASM; GENE EXPRESSION; HEME; HUMANS; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PROTEIN FOLDING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

ATAXIA;

EID: 33845693952     PISSN: 00039861     EISSN: 10960384     Source Type: Journal    
DOI: 10.1016/j.abb.2006.09.010     Document Type: Article

References (56)

1. Harding A.E. The Hereditary Ataxias and Related Disorders (1984), Churchill Livingstone, Edinburgh
2. Harding A.E. The inherited ataxias. Adv. Neurol. 48 (1988) 37-46
3. Johnson W.G. Friedreich ataxia. Clin. Neurosci. 3 (1995) 33-38
4. Campuzano V., Montermini L., Molto M.D., Pianese L., Cossee M., Cavalcanti F., Monros E., Rodius F., Duclos F., Monticelli A., Zara F., Canizares J., Koutnikova H., Bidichandani S.I., Gellera C., Brice A., Trouillas P., De Michele G., Filla A., De Frutos R., Palau F., Patel P.I., Di Donato S., Mandel J.L., Cocozza S., Koenig M., and Pandolfo M. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271 (1996) 1423-1427
5. Campuzano V., Montermini L., Lutz Y., Cova L., Hindelang C., Jiralerspong S., Trottier Y., Kish S.J., Faucheux B., Trouillas P., Authier F.J., Durr A., Mandel J.L., Vescovi A., Pandolfo M., and Koenig M. Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet. 6 (1997) 1771-1780
6. Pianese L., Turano M., Lo Casale M.S., De Biase I., Giacchetti M., Monticelli A., Criscuolo C., Filla A., and Cocozza S. Real time PCR quantification of frataxin mRNA in the peripheral blood leucocytes of Friedreich ataxia patients and carriers. J. Neurol. Neurosurg. Psychiatry 75 (2004) 1061-1063
7. Foury F., and Cazzalini O. Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett. 411 (1997) 373-377
8. Wilson R.B., and Roof D.M. Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nat. Genet. 16 (1997) 352-357
9. Rotig A., de Lonlay P., Chretien D., Foury F., Koenig M., Sidi D., Munnich A., and Rustin P. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 17 (1997) 215-217
10. D.S.J.B. Lamarche, M. Cote, B. Lemieux, Cardiac iron deposits in Friedreich's ataxia, in: R. Lechtenberg (Ed.), Handbook of Cerebellar Diseases, 1993, Marcel Dekker, pp. 453-458.
11. Schoenfeld R.A., Napoli E., Wong A., Zhan S., Reutenauer L., Morin D., Buckpitt A.R., Taroni F., Lonnerdal B., Ristow M., Puccio H., and Cortopassi G.A. Frataxin deficiency alters heme pathway transcripts and decreases mitochondrial heme metabolites in mammalian cells. Hum. Mol. Genet. 14 (2005) 3787-3799
12. Pianese L., Busino L., De Biase I., De Cristofaro T., Lo Casale M.S., Giuliano P., Monticelli A., Turano M., Criscuolo C., Filla A., Varrone S., and Cocozza S. Up-regulation of c-Jun N-terminal kinase pathway in Friedreich's ataxia cells. Hum. Mol. Genet. 11 (2002) 2989-2996
13. Puccio H., Simon D., Cossee M., Criqui-Filipe P., Tiziano F., Melki J., Hindelang C., Matyas R., Rustin P., and Koenig M. Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet. 27 (2001) 181-186
14. Stehling O., Elsasser H.P., Bruckel B., Muhlenhoff U., and Lill R. Iron-sulfur protein maturation in human cells: evidence for a function of frataxin. Hum. Mol. Genet. 13 (2004) 3007-3015
15. Coppola G., Choi S.H., Santos M.M., Miranda C.J., Tentler D., Wexler E.M., Pandolfo M., and Geschwind D.H. Gene expression profiling in frataxin deficient mice: microarray evidence for significant expression changes without detectable neurodegeneration. Neurobiol. Dis. 22 (2006) 302-311
16. Acquaviva F., De Biase I., Nezi L., Ruggiero G., Tatangelo F., Pisano C., Monticelli A., Garbi C., Acquaviva A.M., and Cocozza S. Extra-mitochondrial localisation of frataxin and its association with IscU1 during enterocyte-like differentiation of the human colon adenocarcinoma cell line Caco-2. J. Cell. Sci. 118 (2005) 3917-3924
17. Condo I., Ventura N., Malisan F., Tomassini B., and Testi R. A pool of extramitochondrial frataxin that promotes cell survival. J. Biol. Chem. 281 (2006) 16750-16756
18. Tan G., Napoli E., Taroni F., and Cortopassi G. Decreased expression of genes involved in sulfur amino acid metabolism in frataxin-deficient cells. Hum. Mol. Genet. 12 (2003) 1699-1711
19. Gardner P.R., and Fridovich I. Superoxide sensitivity of the Escherichia coli aconitase. J. Biol. Chem. 266 (1991) 19328-19333
20. Bulteau A.L., O'Neill H.A., Kennedy M.C., Ikeda-Saito M., Isaya G., and Szweda L.I. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 305 (2004) 242-245
21. Napoli E., Taroni F., and Cortopassi G.A. Frataxin, iron-sulfur clusters, heme, ROS, and aging. Antioxid. Redox Signal. 8 (2006) 506-516
22. Yoon T., and Cowan J.A. Iron-sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. J. Am. Chem. Soc. 125 (2003) 6078-6084
23. Hoozemans J.J., Veerhuis R., Van Haastert E.S., Rozemuller J.M., Baas F., Eikelenboom P., and Scheper W. The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol. (Berl.) 110 (2005) 165-172
24. Ryu E.J., Harding H.P., Angelastro J.M., Vitolo O.V., Ron D., and Greene L.A. Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J. Neurosci. 22 (2002) 10690-10698
25. Southwood C.M., Garbern J., Jiang W., and Gow A. The unfolded protein response modulates disease severity in Pelizaeus-Merzbacher disease. Neuron 36 (2002) 585-596
26. Kantor L., Harding H.P., Ron D., Schiffmann R., Kaneski C.R., Kimball S.R., and Elroy-Stein O. Heightened stress response in primary fibroblasts expressing mutant eIF2B genes from CACH/VWM leukodystrophy patients. Hum. Genet. 118 (2005) 99-106
27. Vlug A.S., Teuling E., Haasdijk E.D., French P., Hoogenraad C.C., and Jaarsma D. ATF3 expression precedes death of spinal motoneurons in amyotrophic lateral sclerosis-SOD1 transgenic mice and correlates with c-Jun phosphorylation, CHOP expression, somato-dendritic ubiquitination and Golgi fragmentation. Eur. J. Neurosci. 22 (2005) 1881-1894
28. Cortopassi G., Danielson S., Alemi M., Zhan S.S., Tong W., Carelli V., Martinuzzi A., Marzuki S., Majamaa K., and Wong A. Mitochondrial disease activates transcripts of the unfolded protein response and cell cycle and inhibits vesicular secretion and oligodendrocyte-specific transcripts. Mitochondrion 6 (2006) 161-175
29. Djaman O., Outten F.W., and Imlay J.A. Repair of oxidized iron-sulfur clusters in Escherichia coli. J. Biol. Chem. 279 (2004) 44590-44599
30. Gardner P.R. Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349 (2002) 9-23
31. Lesuisse E., Santos R., Matzanke B.F., Knight S.A., Camadro J.M., and Dancis A. Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum. Mol. Genet. 12 (2003) 879-889
32. Yoon T., and Cowan J.A. Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J. Biol. Chem. 279 (2004) 25943-25946
33. Urata G., and Granick S. Biosynthesis of alpha-aminoketones and the metabolism of aminoacetone. J. Biol. Chem. 238 (1963) 811-820
34. Fubara B., Eckenrode F., Tressel T., and Davis L. Purification and properties of aminoacetone synthetase from beef liver mitochondria. J. Biol. Chem. 261 (1986) 12189-12196
35. Tong H., and Davis L. 2-Amino-3-ketobutyrate-CoA ligase from beef liver mitochondria. Purification and partial sequence. J. Biol. Chem. 269 (1994) 4057-4064
36. Muhlenhoff U., Richhardt N., Ristow M., Kispal G., and Lill R. The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 11 (2002) 2025-2036
37. Cavadini P., O'Neill H.A., Benada O., and Isaya G. Assembly and iron-binding properties of human frataxin, the protein deficient in Friedreich ataxia. Hum. Mol. Genet. 11 (2002) 217-227
38. Park S., Gakh O., O'Neill H.A., Mangravita A., Nichol H., Ferreira G.C., and Isaya G. Yeast frataxin sequentially chaperones and stores iron by coupling protein assembly with iron oxidation. J. Biol. Chem. 278 (2003) 31340-31351
39. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D.F., Bell J.C., Hettmann T., Leiden J.M., and Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11 (2003) 619-633
40. Xue X., Piao J.H., Nakajima A., Sakon-Komazawa S., Kojima Y., Mori K., Yagita H., Okumura K., Harding H., and Nakano H. Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J. Biol. Chem. 280 (2005) 33917-33925
41. Hayashi T., Saito A., Okuno S., Ferrand-Drake M., Dodd R.L., and Chan P.H. Damage to the endoplasmic reticulum and activation of apoptotic machinery by oxidative stress in ischemic neurons. J. Cereb. Blood Flow Metab. 25 (2005) 41-53
42. Seznec H., Simon D., Bouton C., Reutenauer L., Hertzog A., Golik P., Procaccio V., Patel M., Drapier J.C., Koenig M., and Puccio H. Friedreich ataxia: the oxidative stress paradox. Hum. Mol. Genet. 14 (2005) 463-474
43. Hughes J.T., Brownell B., and Hewer R.L. 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 (1968) 803-818
44. 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. GAA repeat expansion mutation mouse models of Friedreich ataxia exhibit oxidative stress leading to progressive neuronal and cardiac pathology. Genomics 88 (2006) 580-590
45. Schulz J.B., Dehmer T., Schols L., Mende H., Hardt C., Vorgerd M., Burk K., Matson W., Dichgans J., Beal M.F., and Bogdanov M.B. Oxidative stress in patients with Friedreich ataxia. Neurology 55 (2000) 1719-1721
46. Emond M., Lepage G., Vanasse M., and Pandolfo M. Increased levels of plasma malondialdehyde in Friedreich ataxia. Neurology 55 (2000) 1752-1753
47. Thierbach R., Schulz T.J., Isken F., Voigt A., Mietzner B., Drewes G., von Kleist-Retzow J.C., Wiesner R.J., Magnuson M.A., Puccio H., Pfeiffer A.F., Steinberg P., and Ristow M. Targeted disruption of hepatic frataxin expression causes impaired mitochondrial function, decreased life span and tumor growth in mice. Hum. Mol. Genet. 14 (2005) 3857-3864
48. Ristow M., Mulder H., Pomplun D., Schulz T.J., Muller-Schmehl K., Krause A., Fex M., Puccio H., Muller J., Isken F., Spranger J., Muller-Wieland D., Magnuson M.A., Mohlig M., Koenig M., and Pfeiffer A.F. Frataxin deficiency in pancreatic islets causes diabetes due to loss of beta cell mass. J. Clin. Invest. 112 (2003) 527-534
49. Seznec H., Simon D., Monassier L., Criqui-Filipe P., Gansmuller A., Rustin P., Koenig M., and Puccio H. Idebenone delays the onset of cardiac functional alteration without correction of Fe-S enzymes deficit in a mouse model for Friedreich ataxia. Hum. Mol. Genet. 13 (2004) 1017-1024
50. Stadtman E.R., and Oliver C.N. Metal-catalyzed oxidation of proteins. Physiological consequences. J. Biol. Chem. 266 (1991) 2005-2008
51. Amrein R., Martin J.R., and Cameron A.M. Moclobemide in patients with dementia and depression. Adv. Neurol. 80 (1999) 509-519
52. Chan Y.C. Aripiprazole treatment for psychosis associated with Friedreich's ataxia. Gen. Hosp. Psychiatry 27 (2005) 372
53. Lishman W.A. Organic psychiatry, the psychological consequences of cerebral disorder (1998), Blackwell Scientific Publications, Oxford
54. Singh G., Binstadt B.A., Black D.F., Corr A.P., and Rummans T.A. Electroconvulsive therapy and Friedreich's ataxia. J. Ect. 17 (2001) 53-54
55. Crimlisk H.L. The little imitator-porphyria: a neuropsychiatric disorder. J Neurol Neurosurg. Psychiatry 62 (1997) 319-328
56. Massey E.W. Neuropsychiatric manifestations of porphyria. J. Clin. Psychiatry 41 (1980) 208-213