Inactivation of cytochrome c oxidase by mutant SOD1s in mouse motoneuronal NSC-34 cells is independent from copper availability but is because of nitric oxide

Journal of Neurochemistry

Volumn 112, Issue 1, 2010, Pages 183-192

  Arciello, Mario ^a   Capo, Concetta Rosa ^a   Cozzolino, Mauro ^b   Ferri, Alberto ^b,c   Nencini, Monica ^b   Carrì, Maria Teresa ^a,b   Rossi, Luisa ^a,d  

^a UNIVERSITY OF ROME   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c CNR   (Italy)

^d NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

Copper; Copper, zinc superoxide dismutase; Cytochrome c oxidase; Familial amyotrophic lateral sclerosis; Mitochondria; Nitric oxide

Indexed keywords

COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C OXIDASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MANGANESE SUPEROXIDE DISMUTASE; MUTANT PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PORIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME INACTIVATION; MITOCHONDRIAL TOXICITY; MOTONEURON; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SPINAL CORD; WILD TYPE;

ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; COPPER; ELECTRON TRANSPORT COMPLEX IV; ENZYME ACTIVATION; HUMANS; MICE; MOTOR NEURONS; MUTATION; NITRIC OXIDE; SUPEROXIDE DISMUTASE;

EID: 71649098280     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06441.x     Document Type: Article

References (46)

1. Almer G., Vukosavic S., Romero N. Przedborski S. (1999) Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 72, 2415 2425.
2. Beal M. F., Ferrante R. J., Browne S. E., Matthews R. T., Kowall N. W. Brown R. H. Jr. (1997) Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann. Neurol. 42, 644 654.
3. Beckman J. S., Carson M., Smith C. D. Koppenol W. H. (1993) ALS, SOD and peroxynitrite. Nature 364, 548.
4. Beckman J. S., Estevez A. G., Crow J. P. Barbeito L. (2001) Superoxide dismutase and the death of motoneurons in ALS. Trends Neurosci. 24, S15 S20.
5. Bendotti C. Carri M. T. (2004) Lessons from models of SOD1-linked familial ALS. Trends Mol. Med. 10, 393 400.
6. Bergemalm D., Jonsson P. A., Graffmo K. S., Andersen P. M., Bränström T., Rehnmark A. Marklund S. L. (2006) Overloading of stable and exclusion of unstable human superoxide dismutase-1 variants in mitochondria of murine amyotrophic lateral sclerosis models. J. Neurosci. 26, 4147 4154.
7. Borthwick G. M., Johnson M. A., Ince P. G., Shaw P. J. Turnbull D. M. (1999) Mitochondrial enzyme activity in amyotrophic lateral sclerosis: implications for the role of mitochondria in neuronal cell death. Ann. Neurol. 46, 787 790.
8. Brown R. H. Robberecht W. (2001) Amyotrophic lateral sclerosis: pathogenesis. Semin. Neurol. 21, 131 139.
9. Bruijn L. I., Miller T. M. Cleveland D. W. (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723 749.
10. Brunori M., Forte E., Arese M., Mastronicola D., Giuffrè A. Sarti P. (2006) Nitric oxide and the respiratory enzyme. Biochim. Biophys. Acta 1757, 1144 1154.
11. Carr H. H. Winge D. R. (2003) Assembly of cytochrome c oxidase within the mitochondrion. Acc. Chem. Res. 36, 309 316.
12. Cashman N. R., Durham H. D., Blusztajn J. K., Oda K., Tabira T., Shaw I. T., Dahrouge S. Antel J. P. (1992) Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dyn. 194, 209 221.
13. Casoni F., Basso M., Massignan T., Gianazza E., Cheroni C., Salmona M., Bendotti C. Bonetto V. (2005) Protein nitration in a mouse model of familial amyotrophic lateral sclerosis: possible multifunctional role in the pathogenesis. J. Biol. Chem. 280, 16295 16304.
14. Chattopadhyay M. Valentine J. S. 2009) Aggregation of copper-zinc superoxide dismutase in familial and sporadic ALS. Antioxid. Redox Signal. 11, 1603 1614.
15. Ciriolo M. R., De Martino A., Lafavia E., Rossi L., Carrì M. T. Rotilio G. (2000) Cu,Zn superoxide dismutase-dependent apoptosis induced by nitric oxide in neuronal cells. J. Biol. Chem. 275, 5065 5072.
16. Cobine P. A., Pierrel F., Bestwick M. L. Winge D. R. (2006) Mitochondrial matrix copper complex used in metallation of cytochrome oxidase and superoxide dismutase. J. Biol. Chem. 281, 36552 36559.
17. Cooper C. E., Davies N. A., Psychoulis M., Canevari L., Bates T. E., Dobbie M. S., Casley C. S. Sharpe M. A. (2003) Nitric oxide and peroxynitrite cause irreversible increases in the K(m) for oxygen of mitochondrial cytochrome oxidase: in vitro and in vivo studies. Biochim. Biophys. Acta 1607, 27 34.
18. Cozzolino M., Ferri A. Carrì M. T. (2008) Amyotrophic lateral sclerosis: from current developments in the laboratory to clinical implications. Antioxid. Redox Signal. 10, 405 443.
19. Crow J. P., Sampson J. B., Zhuang Y., Thompson J. A. Beckman J. S. (1997) Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J. Neurochem. 69, 1936 1944.
20. Ferri A., Cozzolino M., Crosio C., Nencini M., Casciati A., Gralla E. B., Rotilio G., Valentine J. S. Carrì M. T. (2006) Familial ALS-superoxide dismutases associate wit mitochondria and shift their redox potentials. Proc. Natl Acad. Sci. USA 37, 13860 13865.
21. Field L. S., Furukawa Y., O'Halloran T. V. Culotta V. C. (2003) Factors controlling the uptake of yeast copper/zinc superoxide dismutase into mitochondria. J. Biol. Chem. 278, 28052 28059.
22. Fujita K., Yamauchi M., Shibayama K., Ando M., Honda M. Nagata Y. (1996) Decreased cytochrome c oxidase activity but unchanged superoxide dismutase and glutathione peroxidase activities in the spinal cords of patients with amyotrophic lateral sclerosis. J. Neurosci. Res. 45, 276 281.
23. Higgins C. M., Jung C., Ding H. Xu Z. (2002) Mutant Cu, Zn superoxide dismutase that causes motoneuron degeneration is present in mitochondria in the CNS. J. Neurosci. 22, 1 6.
24. Julien J.-P. (2001) Amyotrophic lateral sclerosis: unfolding the toxicity of the misfolded. Cell 104, 581 591.
25. Kirkinezos I. G., Bacman S. R., Hernandez D., Oca-Cossio J., Arias L. J., Perez-Pinzon M. A., Bradley W. G. Moraes C. T. (2005) Cytochrome c association with the inner mitochondrial membrane is impaired in the CNS of G93A-SOD1 mice. J. Neurosci. 25, 164 172.
26. Kong J. Xu Z. (1998) Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J. Neurosci. 18, 3241 3250.
27. Liu J., Lillo C., Jonsson A. et al. (2004) Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43, 5 17.
28. Lombardo M. F., Ciriolo M. R., Rotilio G. Rossi L. (2003) Prolonged copper depletion induces expression of antioxidants and triggers apoptosis in SH-SY5Y neuroblastoma cells. Cell. Mol. Life Sci. 60, 1733 1743.
29. Lowry O. H., Rosebrough N. J., Farr A. L. Randall R. J. (1951) Protein measurement with the Folin-phenol reagent. J. Biol. Chem. 193, 265 275.
30. Martin L. J., Liu Z., Chen K., Price A. C., Pan Y., Swaby J. A. Golden W. C. (2007) Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: mechanisms of mitochondriopathy and cell death. J. Comp. Neurol. 500, 20 46.
31. Mattiazzi M., D'Aurelio M., Gajewski C. D., Martushova K., Kiaci M., Beal M. F. Manfredi G. (2002) Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J. Biol. Chem. 277, 29626 29633.
32. Okado-Matsumoto A. Fridovich I. (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver. J.Biol.Chem. 276, 38388 38393.
33. Raoul C., Estèvez A. G., Nishimune H., Cleveland D. W., deLapeyrière O., Henderson C. E., Haase G. Pettmann B. (2002) Motoneuron death triggered by a specific pathway downstream of Fas potentiation by ALS-linked SOD1 mutations. Neuron 35, 1067 1083.
34. Rossi L., Lippe G., Marchese E., De Martino A., Mavelli I., Rotilio G. Ciriolo M. R. (1998) Decrease of cytochrome c oxidase protein in heart mitochondria of copper deficient rats. Biometals 11, 207 212.
35. Rossi L., Marchese E., Lombardo M. F., Rotilio G. Ciriolo M. R. (2001) Increased susceptibility of copper-deficient neuroblastoma cells to oxidative stress-mediated apoptosis. Free Radic. Biol. Med. 30, 1177 1187.
36. Roy A., Jana A., Yatish K., Freidt M. B., Fung Y. K., Martinson J. A. Pahan K. (2008) Reactive oxygen species up-regulate CD11b in microglia via nitric oxide: implications for neurodegenerative diseases. Free Radic. Biol. Med. 45, 686 699.
37. Sasaki S., Warita H., Abe K. Iwata M. (2001) Inducible nitric oxide synthase (iNOS) and nitrotyrosine immunoreactivity in the spinal cords of transgenic mice with a G93A mutant SOD1 gene. J. Neuropathol. Exp. Neurol. 60, 839 846.
38. Son M., Puttaparthi K., Kawamata H., Rajendran B., Boyer P. J., Manfredi G. Elliot J. L. (2007) Overexpression of CCS in G93A-SOD1 mice leads to accelerated neurological deficits with severe mitochondrial pathology. Proc. Natl Acad. Sci. USA 14, 6072 6077.
39. Son M., Leary S. C., Romain N., Pierrel F., Winge D. R., Haller R. G. Elliott J. L. (2008) Isolated cytochrome c oxidase deficiency in G93A SOD1 mice overexpressing CCS protein. J. Biol. Chem. 283, 12267 12275.
40. Sturtz L. A., Dickert K., Jensen L. T., Lill R. Culotta V. C. (2001) A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 276, 38084 38089.
41. Trumbull K. A. Beckman J. S. 2009) A role for copper in the toxicity of zinc-deficient superoxide dismutase to motor neurons in amyotrophic lateral sclerosis. Antioxid. Redox Signal. 11, 1627 1639.
42. Vande Velde C., Miller T. M., Cashman N. R. Cleveland D. W. (2008) Selective association of misfolded ALS-linked mutant SOD1 with the cytoplasmic face of mitochondria. Proc. Natl Acad. Sci. USA 105, 4022 4027.
43. Valentine J. S., Doucette P. A. Potter S. Z. (2005) Copper-zinc superoxide dismutase and Amyotrophic lateral sclerosis. Annu. Rev. Biochem. 74, 563 593.
44. Vicente S., Pérez-Rodríguez R., Oliván A. M., Martínez Palacián A., González M. P. Oset-Gasque M. J. (2006) Nitric oxide and peroxynitrite induce cellular death in bovine chromaffin cells: evidence for a mixed necrotic and apoptotic mechanism with caspases activation. J. Neurosci. Res. 84, 78 96.
45. Wong P. C., Pardo C. A., Borchelt D. R., Lee M. K., Copeland N. G., Jenkins N. A., Sisodia S. S., Cleveland D. W. Price D. L. (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14, 1105 1116.
46. Zhang J., Bilian J., Liuzhe Li., Block E. R. Patel J. M. (2005) Nitric oxide-induced persistent inhibition and nitrosylation of active site cysteine residues of mitochondrial cytochrome c oxidase in lung endothelial cells. Am. J. Physiol. Cell Physiol. 288, C840 C849.