Mitochondrial damage revealed by immunoselection for ALS-linked misfolded SOD1

Human Molecular Genetics

Volumn 22, Issue 19, 2013, Pages 3947-3959

  Pickles, Sarah ^a,b   Destroismaisons, Laurie ^a   Peyrard, Sarah L ^a   Cadot, Sarah ^a   Rouleau, Guy A ^a,b   Brown, Robert H ^c   Julien, Jean Pierre ^d   Arbour, Nathalie ^a,b   Velde, Christine Vande ^a,b  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; SUPEROXIDE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LYSATE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FLOW CYTOMETRY; LYMPHOBLAST; MUTATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIBODIES; CELL LINE; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GLIOSIS; HOMEOSTASIS; HUMANS; MICE; MITOCHONDRIA; NEURONS; PROTEIN FOLDING; RATS; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 84886239490     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt249     Document Type: Article

References (56)

1. Boillee, S., Vande Velde, C. and Cleveland, D.W. (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron, 52, 1-21.
2. Sasaki, S. and Iwata, M. (1996) Impairment of fast axonal transport in the proximal axons of anterior horn neurons in amyotrophic lateral sclerosis. Neurology, 47, 535-540.
3. Dal Canto, M.C. and Gurney, M.E. (1994) Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am. J. Pathol., 145, 1271-1279.
4. Higgins, C.M., Jung, C., Ding, H. and Xu, Z. (2002) Mutant Cu, Zn superoxide dismutase that causes motoneuron degeneration is present in mitochondria in the CNS. J. Neurosci., 22, RC215. Human Molecular Genetics, 2013, Vol. 22, No. 19 3957
5. Kong, J. and 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.
6. Browne, S.E., Bowling, A.C., Baik, M.J., Gurney, M., Brown, R.H. Jr and Beal, M.F. (1998) Metabolic dysfunction in familial, but not sporadic, amyotrophic lateral sclerosis. J. Neurochem., 71, 281-287.
7. Mattiazzi, M., D'Aurelio, M., Gajewski, C.D., Martushova, K., Kiaei, M., Beal, M.F. and Manfredi, G. (2002) Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J. Biol. Chem., 277, 29626-29633.
8. Tradewell, M.L., Cooper, L.A., Minotti, S. and Durham, H.D. (2011) Calcium dysregulation, mitochondrial pathology and protein aggregation in a culture model of amyotrophic lateral sclerosis: mechanistic relationship and differential sensitivity to intervention. Neurobiol. Dis., 42, 265-275.
9. Damiano, M., Starkov, A.A., Petri, S., Kipiani, K., Kiaei, M., Mattiazzi, M., Flint, B.M. and Manfredi, G. (2006) Neural mitochondrial Ca2+ capacity impairment precedes the onset of motor symptoms in G93A Cu/ Zn-superoxide dismutase mutant mice. J. Neurochem., 96, 1349-1361.
10. Li, Q., Vande Velde, C., Israelson, A., Xie, J., Bailey, A.O., Dong, M.Q., Chun, S.J., Roy, T., Winer, L., Yates, J.R. et al. (2010) ALS-linked mutant superoxide dismutase 1 (SOD1) alters mitochondrial protein composition and decreases protein import. Proc. Natl Acad. Sci. USA, 107, 21146-21151.
11. Pedrini, S., Sau, D., Guareschi, S., Bogush, M., Brown, R.H. Jr, Naniche, N., Kia, A., Trotti, D. and Pasinelli, P. (2010) ALS-linked mutant SOD1 damages mitochondria by promoting conformational changes in Bcl-2. Hum. Mol. Genet., 19, 2974-2986.
12. Israelson, A., Arbel, N., Da Cruz, S., Ilieva, H., Yamanaka, K., Shoshan-Barmatz, V. and Cleveland, D.W. (2010) Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron, 67, 575-587.
13. Liu, J., Lillo, C., Jonsson, P.A., Vande Velde, C., Ward, C.M., Miller, T.M., Subramaniam, J.R., Rothstein, J.D., Marklund, S., Andersen, P.M. et al. (2004) Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron, 43, 5-17.
14. Pasinelli, P., Belford, M.E., Lennon, N., Bacskai, B.J., Hyman, B.T., Trotti, D. and Brown, R.H. Jr. (2004) Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron, 43, 19-30.
15. Vande Velde, C., Miller, T.M., Cashman, N.R. and 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.
16. Okado-Matsumoto, A. and Fridovich, I. (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu,Zn-SOD in mitochondria. J. Biol. Chem., 276, 38388-38393.
17. Igoudjil, A., Magrane, J., Fischer, L.R., Kim, H.J., Hervias, I., Dumont, M., Cortez, C., Glass, J.D., Starkov, A.A. and Manfredi, G. (2011) In vivo pathogenic role of mutant SOD1 localized in the mitochondrial intermembrane space. J. Neurosci., 31, 15826-15837.
18. Rakhit, R., Robertson, J., Vande Velde, C., Horne, P., Ruth, D.M., Griffin, J., Cleveland, D.W., Cashman, N.R. and Chakrabartty, A. (2007) An immunological epitope selective for pathological monomer-misfolded SOD1 in ALS. Nat. Med., 13, 754-759.
19. Gros-Louis, F., Soucy, G., Lariviere, R. and Julien, J.P. (2010) Intracerebroventricular infusion of monoclonal antibody or its derived Fab fragment against misfolded forms of SOD1 mutant delays mortality in a mouse model of ALS. J. Neurochem., 113, 1188-1199.
20. Bosco, D.A., Morfini, G., Karabacak, N.M., Song, Y., Gros-Louis, F., Pasinelli, P., Goolsby, H., Fontaine, B.A., Lemay, N., McKenna-Yasek, D. et al. (2010) Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci., 13, 1396-1403.
21. Kerman, A., Liu, H.N., Croul, S., Bilbao, J., Rogaeva, E., Zinman, L., Robertson, J. and Chakrabartty, A. (2010) Amyotrophic lateral sclerosis is a non-amyloid disease in which extensive misfolding ofSOD1is unique to the familial form. Acta Neuropathol., 119, 335-344.
22. Forsberg, K., Jonsson, P.A., Andersen, P.M., Bergemalm, D., Graffmo, K.S., Hultdin, M., Jacobsson, J., Rosquist, R., Marklund, S.L. and Brannstrom, T. (2010) Novel antibodies reveal inclusions containing non-native SOD1 in sporadic ALS patients. PLoS One, 5, e11552.
23. Grad, L.I., Guest, W.C., Yanai, A., Pokrishevsky, E., O'Neill, M.A., Gibbs, E., Semenchenko, V., Yousefi, M., Wishart, D.S., Plotkin, S.S. and Cashman, N.R. (2011) Intermolecular transmission of superoxide dismutase 1 misfolding in living cells. Proc. Nat. Acad. Sci. USA, 108, 16398-16403.
24. Brotherton, T.E., Li, Y., Cooper, D., Gearing, M., Julien, J.P., Rothstein, J.D., Boylan, K. and Glass, J.D. (2012) Localization of a toxic form of superoxide dismutase 1 protein to pathologically affected tissues in familial ALS. Proc. Nat. Acad. Sci. USA, 109, 5505-5510.
25. Vande Velde, C., McDonald, K.K., Boukhedimi, Y., McAlonis-Downes, M., Lobsiger, C.S., Bel Hadj, S., Zandona, A., Julien, J.P., Shah, S.B. and Cleveland, D.W. (2011) Misfolded SOD1 associated with motor neuron mitochondria alters mitochondrial shape and distribution prior to clinical onset. PLoS One, 6, e22031.
26. Wang, J., Slunt, H., Gonzales, V., Fromholt, D., Coonfield, M., Copeland, N.G., Jenkins, N.A. and Borchelt, D.R. (2003) Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum. Mol. Genet., 12, 2753-2764.
27. Lobsiger, C.S., Boillee, S. and Cleveland, D.W. (2007) Toxicity from different SOD1 mutants dysregulates the complement system and the neuronal regenerative response in ALS motor neurons. Proc. Natl Acad. Sci. USA, 104, 7319-7326.
28. Mullaney, P.F., Van Dilla, M.A., Coulter, J.R. and Dean, P.N. (1969) Cell sizing: a light scattering photometer for rapid volume determination. Rev. Sci. Instrum., 40, 1029-1032.
29. Kowaltowski, A.J., Cosso, R.G., Campos, C.B. and Fiskum, G. (2002) Effect of Bcl-2 overexpression on mitochondrial structure and function. J. Biol. Chem., 277, 42802-42807.
30. Metivier, D., Dallaporta, B., Zamzami, N., Larochette, N., Susin, S.A., Marzo, I. and Kroemer, G. (1998) Cytofluorometric detection of mitochondrial alterations in early CD95/Fas/APO-1-triggered apoptosis of Jurkat T lymphoma cells. Comparison of seven mitochondrion-specific fluorochromes. Immunol. Lett., 61, 157-163.
31. Xu, X. and Arriaga, E.A. (2009) Qualitative determination of superoxide release at both sides of the mitochondrial inner membrane by capillary electrophoretic analysis of the oxidation products of triphenylphosphonium hydroethidine. Free Radic. Biol. Med., 46, 905-913.
32. Robinson, K.M., Janes, M.S., Pehar, M., Monette, J.S., Ross, M.F., Hagen, T.M., Murphy, M.P. andBeckman, J.S. (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl Acad. Sci. USA, 103, 15038-15043.
33. Mukhopadhyay, P., Rajesh, M., Yoshihiro, K., Hasko, G. and Pacher, P. (2007) Simple quantitative detection of mitochondrial superoxide production in live cells. Biochem. Biophys. Res. Commun., 358, 203-208.
34. Loew, L.M., Tuft, R.A., Carrington, W. and Fay, F.S. (1993) Imaging in five dimensions: time-dependent membrane potentials in individual mitochondria. Biophys. J., 65, 2396-2407.
35. Carriedo, S.G., Sensi, S.L., Yin, H.Z. and Weiss, J.H. (2000) AMPA exposures induce mitochondrial Ca(2+) overload and ROS generation in spinal motor neurons in vitro. J. Neurosci., 20, 240-250.
36. Boillee, S., Yamanaka, K., Lobsiger, C.S., Copeland, N.G., Jenkins, N.A., Kassiotis, G., Kollias, G. and Cleveland, D.W. (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science, 312, 1389-1392.
37. Sasaki, S. and Iwata, M. (2007) Mitochondrial alterations in the spinal cord of patients with sporadic amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol., 66, 10-16.
38. Higgins, C.M., Jung, C. and Xu, Z. (2003) ALS-associated mutant SOD1G93A causes mitochondrial vacuolation by expansion of the intermembrane space and by involvement of SOD1 aggregation and peroxisomes. BMC Neurosci., 4, 16.
39. Sasaki, S., Warita, H., Abe, K. and Iwata, M. (2005) Impairment of axonal transport in the axon hillock and the initial segment of anterior horn neurons in transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol. (Berl), 110, 48-56.
40. Menzies, F.M., Ince, P.G. and Shaw, P.J. (2002) Mitochondrial involvement in amyotrophic lateral sclerosis. Neurochem. Int., 40, 543-551.
41. Raimondi, A., Mangolini, A., Rizzardini, M., Tartari, S., Massari, S., Bendotti, C., Francolini, M., Borgese, N., Cantoni, L. and Pietrini, G. (2006) Cell culture models to investigate the selective vulnerability of motoneuronal mitochondria to familial ALS-linked G93ASOD1. Eur. J. Neurosci., 24, 387-399.
42. Tikunov, A., Johnson, C.B., Pediaditakis, P., Markevich, N., Macdonald, J.M., Lemasters, J.J. and Holmuhamedov, E. (2010) Closure of VDAC causes oxidative stress and accelerates the Ca(2+)-induced mitochondrial permeability transition in rat liver mitochondria. Arch. Biochem. Biophys., 495, 174-181.
43. Han, D., Antunes, F., Canali, R., Rettori, D. and Cadenas, E. (2003) Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem., 278, 5557-5563.
44. Lustgarten, M.S., Bhattacharya, A., Muller, F.L., Jang, Y.C., Shimizu, T., Shirasawa, T., Richardson, A. and Van, R.H. (2012) Complex I generated, mitochondrial matrix-directed superoxide is released from the mitochondria through voltage dependent anion channels. Biochem. Biophys. Res. Commun., 422, 515-521.
45. Zimmerman, M.C., Oberley, L.W. and Flanagan, S.W. (2007) Mutant SOD1-induced neuronal toxicity is mediated by increased mitochondrial superoxide levels. J. Neurochem., 102, 609-618.
46. Muller, F.L., Liu, Y., Jernigan, A., Borchelt, D., Richardson, A. and Van, R.H. (2008) MnSOD deficiency has a differential effect on disease progression in two different ALS mutant mouse models. Muscle Nerve, 38, 1173-1183.
47. Ferri, A., Cozzolino, M., Crosio, C., Nencini, M., Casciati, A., Gralla, E.B., Rotilio, G., Valentine, J.S. and Carri, M.T. (2006) Familial ALS-superoxide dismutases associate with mitochondria and shift their redox potentials. Proc. Natl Acad. Sci. USA, 103, 13860-13865.
48. Pesaresi, M.G., Amori, I., Giorgi, C., Ferri, A., Fiorenzo, P., Gabanella, F., Salvatore, A.M., Giorgio, M., Pelicci, P.G., Pinton, P. et al. (2011) Mitochondrial redox signalling by p66Shc mediates ALS-like disease through Rac1 inactivation. Hum. Mol. Genet., 20, 4196-4208.
49. Zimmermann, A.K., Loucks, F.A., Schroeder, E.K., Bouchard, R.J., Tyler, K.L. and Linseman, D.A. (2007) Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria. J. Biol. Chem., 282, 29296-29304.
50. Howland, D.S., Liu, J., She, Y.J., Goad, B., Maragakis, N.J., Kim, B., Erickson, J., Kulik, J., DeVito, L., Psaltis, G. et al. (2002) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl Acad. Sci. USA, 99, 1604-1609.
51. Prudencio, M. and Borchelt, D.R. (2011) Superoxide dismutase 1 encoding mutations linked to ALS adopts a spectrum of misfolded states. Mol. Neurodegener., 6, 77.
52. Fujisawa, T., Homma, K., Yamaguchi, N., Kadowaki, H., Tsuburaya, N., Naguro, I., Matsuzawa, A., Takeda, K., Takahashi, Y., Goto, J. et al. (2012) A novel monoclonal antibody reveals a conformational alteration shared by amyotrophic lateral sclerosis-linked SOD1 mutants. Ann. Neurol., 72, 739-749.
53. Guareschi, S., Cova, E., Cereda, C., Ceroni, M., Donetti, E., Bosco, D.A., Trotti, D. and Pasinelli, P. (2012) An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1. Proc. Natl Acad. Sci. USA, 109, 5074-5079.
54. Chan, P.H., Kawase, M., Murakami, K., Chen, S.F., Li, Y., Calagui, B., Reola, L., Carlson, E. and Epstein, C.J. (1998) Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J. Neurosci., 18, 8292-8299.
55. Vande Velde, C., Garcia, M.L., Yin, X., Trapp, B.D. and Cleveland, D.W. (2004) The neuroprotective factor Wlds does not attenuate mutant SOD1-mediated motor neuron disease. Neuromol. Med., 5, 193-203.
56. Pramatarova, A., Figlewicz, D.A., Krizus, A., Han, F.Y., Ceballos-Picot, I., Nicole, A., Dib, M., Meininger, V., Brown, R.H. and Rouleau, G.A. (1995) Identification of new mutations in the Cu/Zn superoxide dismutase gene of patients with familial amyotrophic lateral sclerosis. Am. J. Hum. Genet., 56, 592-596.