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

Volumn 8, Issue 8, 2008, Pages 1731-1741

  Sutak, Robert ^a   Xu, Xiangcong ^a   Whitnall, Megan ^a   Kashem, Mohammed Abul ^a   Vyoral, Daniel ^b,c   Richardson, Des R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b INSTITUTE OF HEMATOLOGY AND BLOOD TRANSFUSION   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

Author keywords

2 DE; Ataxia; Biomarkers; Hypertrophic cardiomyopathy; Oxidative stress

Indexed keywords

ADENYLATE KINASE; BRANCHED CHAIN AMINO ACID; CHAPERONE; CREATINE KINASE; FRATAXIN; HEAT SHOCK PROTEIN 25; IRON; KETONE BODY; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE);

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOMYOPATHY; CATABOLISM; CELL METABOLISM; CELL MOTILITY; CELL STRESS; CELL STRUCTURE; CITRIC ACID CYCLE; CONTROLLED STUDY; DECARBOXYLATION; ENERGY METABOLISM; HOMEOSTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RESPIRATORY CHAIN; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL MOVEMENT; CELL PHYSIOLOGY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENERGY METABOLISM; FRIEDREICH ATAXIA; HEART; IRON-BINDING PROTEINS; MICE; MICE, KNOCKOUT; OXIDATIVE STRESS; PROTEINS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

MUS;

EID: 42549156654     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200701049     Document Type: Article

References (60)

1. Lodi, R., Tonon, C., Calabrese, V., Schapira, A. H., Friedreich's ataxia: From disease mechanisms to therapeutic interventions. Antioxid. Redox Signal. 2006, 8, 438-443.
2. Campuzano, V., Montermini, L., Molto, M. D., Pianese, L. et al., Friedreich's ataxia: Autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 1996, 271, 1423-1427.
3. Campuzano, V., Montermini, L., Lutz, Y., Cova, L. et al., Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet. 1997, 6, 1771-1780.
4. Koutnikova, H., Campuzano, V., Foury, F., Dolle, P. et al., Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin. Nat. Genet. 1997, 16, 345-351.
5. Pandolfo, M., Iron and Friedreich ataxia. J. Neural Transm. Suppl. 2006, 143-146.
6. Napier, I., Ponka, P., Richardson, D. R., Iron trafficking in the mitochondrion: Novel pathways revealed by disease. Blood 2005, 105, 1867-1874.
7. Wilson, R. B., Iron dysregulation in Friedreich ataxia. Semin. Pediatr. Neurol. 2006, 13, 166-175.
8. Becker, E. M., Greer, J. M., Ponka, P., Richardson, D. R., Erythroid differentiation and protoporphyrin IX down-regulate frataxin expression in Friend cells: Characterization of frataxin expression compared to molecules involved in iron metabolism and hemoglobinization. Blood 2002, 99, 3813-3822.
9. Nie, G., Chen, G., Sheftel, A. D., Pantopoulos, K., Ponka, P., In vivo tumor growth is inhibited by cytosolic iron deprivation caused by the expression of mitochondrial ferritin. Blood 2006, 108, 2428-2434.
10. Babcock, M., de Silva, D., Oaks, R., Davis-Kaplan, S. et al., Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 1997, 276, 1709-1712.
11. Foury, F., Cazzalini, O., Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett. 1997, 411, 373-377.
12. Muhlenhoff, U., Richhardt, N., Ristow, M., Kispal, G., Lill, R., The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 2002, 11, 2025-2036.
13. Shan, Y., Napoli, E., Cortopassi, G., Mitochondrial frataxin interacts with ISD11 of the NFS1/ISCU complex and multiple mitochondrial chaperones. Hum. Mol. Genet. 2007, 16, 929-941.
14. Rotig, A., de Lonlay, P., Chretien, D., Foury, F. et al., Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 1997, 17, 215-217.
15. Lesuisse, E., Santos, R., Matzanke, B. F., Knight, S. A. et al., Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum. Mol. Genet. 2003, 12, 879-889.
16. Puccio, H., Simon, D., Cossee, M., Criqui-Filipe, P. et al., Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet. 2001, 27, 181-186.
17. Cavadini, P., O'Neill, H. A., Benada, O., Isaya, G., Assembly and iron-binding properties of human frataxin, the protein deficient in Friedreich ataxia. Hum. Mol. Genet. 2002, 11, 217-227.
18. Park, S., Gakh, O., O'Neill, H. A., Mangravita, A. et al., Yeast frataxin sequentially chaperones and stores iron by coupling protein assembly with iron oxidation. J. Biol. Chem. 2003, 278, 31340-31351.
19. Calabrese, V., Lodi, R., Tonon, C., D'Agata, V. et al., Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich's ataxia. J. Neurol. Sci. 2005, 233, 145-162.
20. Gakh, O., Park, S., Liu, G., Macomber, L. et al., Mitochondrial iron detoxification is a primary function of frataxin that limits oxidative damage and preserves cell longevity. Hum. Mol. Genet. 2006, 15, 467-479.
21. Durr, A., Cossee, M., Agid, Y., Campuzano, V. et al., Clinical and genetic abnormalities in patients with Friedreich's ataxia. N. Engl. J. Med. 1996, 335, 1169-1175.
22. Kashem, M. A., James, G., Harper, C., Wilce, P., Matsumoto, I., Differential protein expression in the corpus callosum (splenium) of human alcoholics: A proteomics study. Neurochem. Int. 2007, 50, 450-459.
23. Stryer, L., Biochemistry, WH Freedman Publishers, San Francisco 1980.
24. Hunt, M. C., Alexson, S. E., The role Acyl-CoA thioesterases play in mediating intracellular lipid metabolism. Prog. Lipid Res. 2002, 41, 99-130.
25. Lodi, R., Cooper, J. M., Bradley, J. L., Manners, D. et al., Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia. Proc. Natl. Acad. Sci. USA 1999, 96, 11492-11495.
26. Doran, P., Martin, G., Dowling, P., Jockusch, H., Ohlendieck, K., Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 2006, 6, 4610-4621.
27. Wilson, R. B., Roof, D. M., Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nat. Genet. 1997, 16, 352-357.
28. Tan, G., Napoli, E., Taroni, F., Cortopassi, G., Decreased expression of genes involved in sulfur amino acid metabolism in frataxin-deficient cells. Hum. Mol. Genet. 2003, 12, 1699-1711.
29. Lodi, R., Rajagopalan, B., Blamire, A. M., Cooper, J. M. et al., Cardiac energetics are abnormal in Friedreich ataxia patients in the absence of cardiac dysfunction and hypertrophy: An in vivo 31P magnetic resonance spectroscopy study. Cardiovasc. Res. 2001, 52, 111-119.
30. Eaton, J. W., Qian, M., Molecular bases of cellular iron toxicity. Free Radic. Biol. Med. 2002, 32, 833-840.
31. Schulz, J. B., Dehmer, T., Schols, L., Mende, H. et al., Oxidative stress in patients with Friedreich ataxia. Neurology 2000, 55, 1719-1721.
32. Emond, M., Lepage, G., Vanasse, M., Pandolfo, M., Increased levels of plasma malondialdehyde in Friedreich ataxia. Neurology 2000, 55, 1752-1753.
33. Arrigo, A. P., The cellular "networking" of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis. Adv. Exp. Med. Biol. 2007, 594, 14-26.
34. Arrigo, A. P., Simon, S., Gibert, B., Kretz-Remy, C. et al., Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett 2007, 581, 3665-3674.
35. Jaattela, M., Heat shock proteins as cellular lifeguards. Ann. Med. 1999, 31, 261-271.
36. Borges, J. C., Fischer, H., Craievich, A. F., Hansen, L. D., Ramos, C. H., Free human mitochondrial GrpE is a symmetric dimer in solution. J. Biol. Chem. 2003, 278, 35337-35344.
37. Rajasekaran, N. S., Connell, P., Christians, E. S., Yan, L. J. et al., Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 2007, 130, 427-439.
38. Kolsch, H., Linnebank, M., Lutjohann, D., Jessen, F. et al., Polymorphisms in glutathione S-transferase omega-1 and AD, vascular dementia, and stroke. Neurology 2004, 63, 2255-2260.
39. Hayes, J. D., Flanagan, J. U., Jowsey, I. R., Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 2005, 45, 51-88.
40. Andres-Mateos, E., Perier, C., Zhang, L., Blanchard-Fillion, B. et al., DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl. Acad. Sci. USA 2007, 104, 14807-14812.
41. Gray, C. W., Ward, R. V., Karran, E., Turconi, S. et al., Characterization of human HtrA2, a novel serine protease involved in the mammalian cellular stress response. Eur. J. Biochem. 2000, 267, 5699-5710.
42. Di Prospero, N. A., Baker, A., Jeffries, N., Fischbeck, K. H., Neurological effects of high-dose idebenone in patients with Friedreich's ataxia: A randomised, placebo-controlled trial. Lancet Neurol. 2007, 6, 878-886.
43. Di Prospero, N. A., Sumner, C. J., Penzak, S. R., Ravina, B. et al., Safety, tolerability, and pharmacokinetics of high-dose idebenone in patients with Friedreich ataxia. Arch. Neurol. 2007, 64, 803-808.
44. Hart, P. E., Lodi, R., Rajagopalan, B., Bradley, J. L. et al., Antioxidant treatment of patients with Friedreich ataxia: Four-year follow-up. Arch. Nerol. 2005, 62, 621-626.
45. Richardson, D. R., Friedreich's ataxia: Iron chelation as a therapeutic strategy? Expert Opin. Investig. Drugs 2003, 12, 235-245.
46. Gomes, A. V., Guzman, G., Zhao, J., Potter, J. D., Cardiac troponin T isoforms affect the Ca2+ sensitivity and inhibition of force development. Insights into the role of troponin T isoforms in the heart. J. Biol. Chem. 2002, 277, 35341-35349.
47. Gomes, A. V., Potter, J. D., Szczesna-Cordary, D., The role of troponins in muscle contraction. IUBMB Life 2002, 54, 323-333.
48. Martins, E., Silva-Cardoso, J., Alves, C., Pereira, H. et al., Familial dilated cardiomyopathy with troponin T K210del mutation. Rev. Port. Cardiol. 2006, 25, 295-300.
49. Yoshida, M., Minamisawa, S., Shimura, M., Komazaki, S. et al., Impaired Ca2+ store functions in skeletal and cardiac muscle cells from sarcalumenin-deficient mice. J. Biol. Chem. 2005, 280, 3500-3506.
50. Lohan, J., Ohlendieck, K., Drastic reduction in the luminal Ca2+ -binding proteins calsequestrin and sarcalumenin in dystrophin-deficient cardiac muscle. Biochim. Biophys. Acta 2004, 1689, 252-258.
51. Tamma, G., Procino, G., Svelto, M., Valenti, G., Hypotonicity causes actin reorganization and recruitment of the actin-binding ERM protein moesin in membrane protrusions in collecting duct principal cells. Am. J. Physiol. Cell Physiol. 2007, 292, C1476-C1484.
52. Niggli, V., Rossy, J., Ezrin/radixin/moesin: Versatile controllers of signaling molecules and of the cortical cytoskeleton. Int. J. Biochem. Cell Biol. 2008, 40, 344-349.
53. Hagemann, T. L., Gaeta, S. A., Smith, M. A., Johnson, D. A. et al., Gene expression analysis in mice with elevated glial fibrillary acidic protein and Rosenthal fibers reveals a stress response followed by glial activation and neuronal dysfunction. Hum. Mol. Genet. 2005, 14, 2443-2458.
54. Lewis, G. P., Fisher, S. K., Up-regulation of glial fibrillary acidic protein in response to retinal injury: Its potential role in glial remodeling and a comparison to vimentin expression. Int. Rev. Cytol. 2003, 230, 263-290.
55. Silva, R. G., Nunes, J. E., Canduri, F., Borges, J. C. et al., Purine nucleoside phosphorylase: A potential target for the development of drugs to treat T-cell- and apicomplexan parasite-mediated diseases. Curr. Drug Targets 2007, 8, 413-422.
56. Jiao, Z., Zhang, Z. G., Hornyak, T. J., Hozeska, A. et al., Dopachrome tautomerase (Dct) regulates neural progenitor cell proliferation. Dev. Biol. 2006, 296, 396-408.
57. Lin, C. H., Chung, M. Y., Chen, W. B., Chien, C. H., Growth inhibitory effect of the human NIT2 gene and its allelic imbalance in cancers. FEBS J. 2007, 274, 2946-2956.
58. Hamilton, J. A., Benson, M. D., Transthyretin: A review from a structural perspective. Cell. Mol. Life Sci. 2001, 58, 1491-1521.
59. Hanna, J., Finley, D., A proteasome for all occasions. FEBS Lett. 2007, 581, 2854-2861.
60. Bulteau, A. L., Dancis, A., Gareil, M., Montagne, J. J. et al., Oxidative stress and protease dysfunction in the yeast model of Friedreich ataxia. Free Radic. Biol. Med. 2007, 42, 1561-1570.