Metal-deficient aggregates and diminished copper found in cells expressing SOD1 mutations that cause ALS

Frontiers in Aging Neuroscience

Volumn 6, Issue JUN, 2014, Pages

  Bourassa, Megan W ^a   Brown, Hilda H ^b   Borchelt, David R ^b   Vogt, Stefan ^c   Miller, Lisa M ^a,d  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Amyotrophic lateral sclerosis; Superoxide dismutase; Synchrotron; X ray fluorescence microscopy

Indexed keywords

COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; IRON; METAL ION; YELLOW FLUORESCENT PROTEIN; ZINC;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL CULTURE; CHO CELL LINE; CYTOPLASM; IN VITRO STUDY; MICROSCOPY; MUTANT; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; X RAY FLUORESCENCE; X RAY FLUORESCENCE MICROSCOPY;

EID: 84904574268     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00110     Document Type: Article

References (42)

1. Abel, O., Shatunov, A., Jones, A. R., Andersen, P. M., Powell, J. F., and Al-Chalabi, A. (2013). Development of a smartphone app for a genetics website: the amyotrophic lateral sclerosis online genetics database (ALSoD). JMIR Mhealth Uhealth 1:e18. doi: 10.2196/mhealth.2706
2. Ayers, J., Lelie, H., Workman, A., Prudencio, M., Brown, H., Fromholt, S., et al. (2014). Distinctive features of the D101N and D101G variants of superoxide dismutase 1; two mutations that produce rapidly progressing motor neuron disease. J. Neurochem. 128, 305-314. doi: 10.1111/jnc.12451
3. Bertoncini, C. W., Jung, Y. S., Fernandez, C. O., Hoyer, W., Griesinger, C., Jovin, T. M., et al. (2005). Release of long-range tertiary interactions potentiates aggregation of natively unstructured a-synuclein. Proc. Natl. Acad. Sci. U S A 102, 1430-1435. doi: 10.1073/pnas.0407146102
4. Borchelt, D. R., Lee, M. K., Slunt, H. S., Guarnieri, M., Xu, Z. S., Wong, P. C., et al. (1994). Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc. Natl. Acad. Sci. U S A 91, 8292-8296. doi: 10.1073/pnas.91.17.8292
5. Bruijn, L., Miller, T., and Cleveland, D. (2004). Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723-749. doi: 10.1146/annurev.neuro.27.070203.144244
6. Bush, A. (2003). The metallobiology of Alzheimer's disease. Trends Neurosci. 26, 207-214. doi: 10.1016/S0166-2236(03)00067-5
7. Deng, H. X., Hentati, A., Tainer, J. A., Iqbal, Z., Cayabyab, A., Hung, W. Y., et al. (1993). Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 261, 1047-1051. doi: 10.1126/science.8351519
8. Doble, A. (1996). The pharmacology and mechanism of action of riluzole. Neurology 47(Suppl. 4), S233-S241. doi: 10.1212/wnl.47.6_suppl_4.233s
9. Ellerby, L. M., Cabelli, D. E., Graden, J. A., and Valentine, J. S. (1996). Copper-zinc superoxide dismutase: why not pH-dependent? J. Am. Chem. Soc. 118, 6556-6561. doi: 10.1021/ja953845x
10. Gaggelli, E., Kozlowski, H., Valensin, D., and Valensin, G. (2006). Copper homeostasis and neurodegenerative disorders (Alzheimer's, prion and Parkinson's diseases and amyotrophic lateral sclerosis). Chem. Rev. 106, 1995-2044. doi: 10.1021/cr040410w
11. Hayward, L., Rodriguez, J., Kim, J., Tiwari, A., Goto, J., Cabelli, D., et al. (2002). Decreased metallation and activity in subsets of mutant superoxide dismutases associated with familial amyotrophic lateral sclerosis. J. Biol. Chem. 277, 15923-15931. doi: 10.1074/jbc.m112087200
12. Huang, X., Atwood, C. S., Moir, R. D., Hartshorn, M. A., Vonsattel, J. P., Tanzi, R. E., et al. (1997). Zinc-induced Alzheimer's Aß1-40 aggregation is mediated by conformational factors. J. Biol. Chem. 272, 26464-26470. doi: 10.1074/jbc.272.42.26464
13. Karch, C., Prudencio, M., Winkler, D., Hart, P., and Borchelt, D. (2009). Role of mutant SOD1 disulfide oxidation and aggregation in the pathogenesis of familial ALS. Proc. Natl. Acad. Sci. U S A 106, 7774-7779. doi: 10.1073/pnas.0902505106
14. Lee, J. P., Gerin, C., Bindokas, V. P., Miller, R., Ghadge, G., and Roos, R. P. (2002). No correlation between aggregates of Cu/Zn superoxide dismutase and cell death in familial amyotrophic lateral sclerosis. J. Neurochem. 82, 1229-1238. doi: 10.1046/j.1471-4159.2002.01056.x
15. Lelie, H. L., Liba, A., Bourassa, M. W., Chattopadhyay, M., Chan, P. K., Gralla, E. B., et al. (2011). Copper and zinc metallation status of copper-zinc superoxide dismutase from amyotrophic lateral sclerosis transgenic mice. J. Biol. Chem. 286, 2795-2806. doi: 10.1074/jbc.m110.186999
16. Leskovjan, A. C., Lanzirotti, A., and Miller, L. M. (2009). Amyloid plaques in PSAPP mice bind less metal than plaques in human Alzheimer's disease. Neuroimage 47, 1215-1220. doi: 10.1016/j.neuroimage.2009.05.063
17. Lill, C. M., Abel, O., Bertram, L., and Al-Chalabi, A. (2011). Keeping up with genetic discoveries in amyotrophic lateral sclerosis: the ALSoD and ALSGene databases. Amyotroph. Lateral Scler. 12, 238-249. doi: 10.3109/17482968.2011.584629
18. Lotharius, J., and Brundin, P. (2002). Pathogenesis of Parkinson's disease: dopamine, vesicles and alpha-synuclein. Nat. Rev. Neurosci. 3, 932-942. doi: 10.1038/nrn983
19. Lovell, M., Robertson, J., Teesdale, W., Campbell, J., and Markesbery, W. (1998). Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci. 158, 47-52. doi: 10.1016/s0022-510x(98)00092-6
20. Lutsenko, S., Bhattacharjee, A., and Hubbard, A. L. (2010). Copper handling machinery of the brain. Metallomics 2, 596-608. doi: 10.1039/c0mt00006j
21. Maynard, C. J., Bush, A. I., Masters, C. L., Cappai, R., and Li, Q. X. (2005). Metals and amyloid in Alzheimer's disease. Int. J. Exp. Pathol. 86, 147-159. doi: 10.1111/j.0959-9673.2005.00434.x
22. Miller, R. G., Mitchell, J. D., Lyon, M., and Moore, D. H. (2007). Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst. Rev. 1:CD001447. doi: 10.1002/14651858.CD001447
23. Miller, L., Wang, Q., Telivala, T., Smith, R., Lanzirotti, A., and Miklossy, J. (2006). Synchrotron-based infrared and X-ray imaging shows focalized accumulation of Cu and Zn co-localized with ß-amyloid deposits in Alzheimer's disease. J. Struct. Biol. 155, 30-37. doi: 10.1016/j.jsb.2005.09.004
24. 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. doi: 10.1186/1750-1326-6-77
25. Prudencio, M., Hart, P. J., Borchelt, D. R., and Andersen, P. M. (2009). Variation in aggregation propensities among ALS-associated variants of SOD1: correlation to human disease. Hum. Mol. Genet. 18, 3217-3226. doi: 10.1093/hmg/ddp260
26. Prudencio, M., Lelie, H., Brown, H. H., Whitelegge, J. P., Valentine, J. S., and Borchelt, D. R. (2012). A novel variant of human superoxide dismutase 1 harboring amyotrophic lateral sclerosis-associated and experimental mutations in metal-binding residues and free cysteines lacks toxicity in vivo. J. Neurochem. 121, 475-485. doi: 10.1111/j.1471-4159.2012.07690.x
27. Qualls, D. A., Crosby, K., Brown, H., and Borchelt, D. R. (2013a). An analysis of interactions between fluorescently-tagged mutant and wild-type SOD1 in intracellular inclusions. PLoS One 8:e83981. doi: 10.1371/journal.pone.0083981
28. Qualls, D. A., Prudencio, M., Roberts, B. L., Crosby, K., Brown, H., and Borchelt, D. R. (2013b). Features of wild-type human SOD1 limit interactions with misfolded aggregates of mouse G86R Sod1. Mol. Neurodegener. 8:46. doi: 10.1186/1750-1326-8-46
29. Rodriguez, J. A., Shaw, B. F., Durazo, A., Sohn, S. H., Doucette, P. A., Nersissian, A M., et al. (2005). Destabilization of apoprotein is insufficient to explain Cu,Zn-superoxide dismutase-linked ALS pathogenesis. Proc. Natl. Acad. Sci. U S A 102, 10516-10521. doi: 10.1073/pnas.0502515102
30. Rodriguez, J. A., Valentine, J. S., Eggers, D. K., Roe, J. A., Tiwari, A., Brown, R. H., et al. (2002). Familial amyotrophic lateral sclerosis-associated mutations decrease the thermal stability of distinctly metallated species of human copper/zinc superoxide dismutase. J. Biol. Chem. 277, 15932-15937. doi: 10.1074/jbc.m112088200
31. Schmidt, P. J., Rae, T. D., Pufahl, R. A., Hamma, T., Strain, J., O'Halloran, T. V., et al. (1999). Multiple protein domains contribute to the action of the copper chaperone for superoxide dismutase. J. Biol. Chem. 274, 23719-23725. doi: 10.1074/jbc.274.34.23719
32. Seetharaman, S. V., Winkler, D. D., Taylor, A. B., Cao, X., Whitson, L. J., Doucette, P. A., et al. (2010). Disrupted zinc-binding sites in structures of pathogenic SOD1 variants D124V and H80R. Biochemistry 49, 5714-5725. doi: 10.1021/bi100314n
33. Selkoe, D. J. (2001). Alzheimer's disease: genes, proteins and therapy. Physiol. Rev. 81, 741-766.
34. Selkoe, D. J. (2003). Folding proteins in fatal ways. Nature 426, 900-904. doi: 10.1038/nature02264
35. Selkoe, D. J. (2004). Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 6, 1054-1061. doi: 10.1038/ncb1104-1054
36. Shaw, B., and Valentine, J. (2007). How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends Biochem. Sci. 32, 78-85. doi: 10.1016/j.tibs.2006.12.005
37. Shaw, B. F., Lelie, H. L., Durazo, A., Nersissian, A. M., Xu, G., Chan, P. K., et al. (2008). Detergent-insoluble aggregates associated with amyotrophic lateral sclerosis in transgenic mice contain primarily full-length, unmodified superoxide dismutase-1. J. Biol. Chem. 283, 8340-8350. doi: 10.1074/jbc.m707751200
38. Smith, A. P., and Lee, N. M. (2007). Role of zinc in ALS. Amyotroph. Lateral Scler. 8, 131-143. doi: 10.1080/17482960701249241
39. Soto, C. (2003). Unfolding the role of protein misfolding in neurodegenerative diseases. Nat. Rev. Neurosci. 4, 49-60. doi: 10.1038/nrn1007
40. Soto, C. (2013). Protein misfolding in neurodegenerative diseases: the key pending questions. J. Neurol. Transl. Neurosci. 1, 1010-1014.
41. Valentine, J., Doucette, P., and Potter, S. (2005). Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu. Rev. Biochem. 74, 563-593. doi: 10.1146/annurev.biochem.72.121801.161647
42. Vonk, W., and Klomp, L. (2008). Role of transition metals in the pathogenesis of amyotrophic lateral sclerosis. Biochem. Soc. Trans. 36(Pt. 6), 1322-1328. doi: 10.1042/bst0361322