In-cell NMR reveals potential precursor of toxic species from SOD1 fALS mutants

Nature Communications

Volumn 5, Issue , 2014, Pages

  Luchinat, Enrico ^a,b   Barbieri, Letizia ^a   Rubino, Jeffrey T ^a   Kozyreva, Tatiana ^c   Cantini, Francesca ^a   Banci, Lucia ^a,d  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c SRL   (Italy)

^d Fondazione Farmacogenomica FIORGEN ONLUS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 13; CHAPERONE; COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; METAL ION; NITROGEN 15; OLIGOMER; THIOL; ZINC; CCS PROTEIN, HUMAN; SUPEROXIDE DISMUTASE;

COPPER; ENZYME ACTIVITY; GENE EXPRESSION; GERM CELL; MUTATION; NUCLEAR MAGNETIC RESONANCE; TOXIC ORGANISM;

ALKYLATION; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; ATOMIC EMISSION SPECTROMETRY; BINDING SITE; DISULFIDE BOND; FAMILIAL DISEASE; GEL FILTRATION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN CELL NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; WESTERN BLOTTING; GENETICS; HEK293 CELL LINE; METABOLISM; NUCLEAR MAGNETIC RESONANCE;

AMYOTROPHIC LATERAL SCLEROSIS; COPPER; HEK293 CELLS; HUMANS; MOLECULAR CHAPERONES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; SUPEROXIDE DISMUTASE; ZINC;

EID: 84923099242     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6502     Document Type: Article

References (58)

1. Selenko, P. & Wagner, G. Looking into live cells with in-cell NMR spectroscopy. J. Struct. Biol. 158, 244-253 (2007).
2. Reckel, S., Hansel, R., Lohr, F. & Dotsch, V. In-cell NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc. 51, 91-101 (2007).
3. Inomata, K. et al. High-resolution multi-dimensional NMR spectroscopy of proteins in human cells. Nature 458, 106-109 (2009).
4. Banci, L., Barbieri, L., Bertini, I., Cantini, F. & Luchinat, E. In-cell NMR in E. coli to monitor maturation steps of hSOD1. PLoS ONE 6, e23561 (2011).
5. Schlesinger, A. P., Wang, Y. Q., Tadeo, X., Millet, O. & Pielak, G. Macromolecular crowding fails to fold a globular protein in cells. J. Am. Chem. Soc. 133, 8082-8085 (2011).
6. Bertrand, K., Reverdatto, S., Burz, D. S., Zitomer, R. & Shekhtman, A. Structure of proteins in eukaryotic compartments. J. Am. Chem. Soc. 134, 12798-12806 (2012).
7. Danielsson, J. et al. Pruning the ALS-associated protein SOD1 for in-cell NMR. J. Am. Chem. Soc. 135, 10266-10269 (2013).
8. Burz, D. S., Dutta, K., Cowburn, D. & Shekhtman, A. Mapping structural interactions using in-cell NMR spectroscopy (STINT-NMR). Nat. Methods 3, 91-93 (2006).
9. Maldonado, A. Y., Burz, D. S. & Shekhtman, A. In-cell NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc. 59, 197-212 (2011).
10. Banci, L. et al. Atomic-resolution monitoring of protein maturation in live human cells by NMR. Nat. Chem. Biol. 9, 297-299 (2013).
11. Banci, L., Barbieri, L., Luchinat, E. & Secci, E. Visualization of redox-controlled protein fold in living cells. Chem. Biol. 20, 747-752 (2013).
12. Culotta, V. C. et al. The copper chaperone for superoxide dismutase. J. Biol. Chem. 272, 23469-23472 (1997).
13. Furukawa, Y., Torres, A. S. & O'Halloran, T. V. Oxygen-induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS. EMBO J. 23, 2872-2881 (2004).
14. Carroll, M. C. et al. Mechanisms for activating Cu-and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proc. Natl Acad. Sci. USA 101, 5964-5969 (2004).
15. Banci, L. et al. Human superoxide dismutase 1 (hSOD1) maturation through interaction with human copper chaperone for SOD1 (hCCS). Proc. Natl Acad. Sci. USA 109, 13555-13560 (2012).
16. Rosen, D. R. et al. Mutations in Cu/Zn superoxide-dismutase gene are associated with familial amyotrophic-lateral-sclerosis. Nature 362, 59-62 (1993).
17. Shibata, N. et al. Intense superoxide dismutase-1 immunoreactivity in intracytoplasmic hyaline inclusions of familial amyotrophic lateral sclerosis with posterior column involvement. J. Neuropathol. Exp. Neurol. 55, 481-490 (1996).
18. Watanabe, M. et al. Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol. Dis. 8, 933-941 (2001).
19. Jonsson, P. A. et al. Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain 127, 73-88 (2004).
20. Bruijn, L. I. et al. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18, 327-338 (1997).
21. Bruijn, L. I. et al. Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281, 1851-1854 (1998).
22. Johnston, J. A., Dalton, M. J., Gurney, M. E. & Kopito, R. R. Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 97, 12571-12576 (2000).
23. Wang, J., Xu, G. & Borchelt, D. R. High molecular weight complexes of mutant superoxide dismutase 1: age-dependent and tissue-specific accumulation. Neurobiol. Dis. 9, 139-148 (2002).
24. Mulligan, V. K. & Chakrabartty, A. Protein misfolding in the late-onset neurodegenerative diseases: common themes and the unique case of amyotrophic lateral sclerosis. Proteins 81, 1285-1303 (2013).
25. Ross, C. A. & Poirier, M. A. Protein aggregation and neurodegenerative disease. Nat. Med. 10, S10-S17 (2004).
26. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem 75, 333-366 (2006).
27. Bucciantini, M. et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416, 507-511 (2002).
28. Banci, L. et al. Metal-free superoxide dismutase forms soluble oligomers under physiological conditions: a possible general mechanism for familial ALS. Proc. Natl Acad. Sci. USA 104, 11263-11267 (2007).
29. Toichi, K., Yamanaka, K. & Furukawa, Y. Disulfide scrambling describes the oligomer formation of superoxide dismutase (SOD1) proteins in the familial form of amyotrophic lateral sclerosis. J. Biol. Chem. 288, 4970-4980 (2013).
30. Wang, J., Xu, G. L. & Borchelt, D. R. Mapping superoxide dismutase 1 domains of non-native interaction: roles of intra-and intermolecular disulfide bonding in aggregation. J. Neurochem. 96, 1277-1288 (2006).
31. Teilum, K. et al. Transient structural distortion of metal-free Cu/Zn superoxide dismutase triggers aberrant oligomerization. Proc. Natl Acad. Sci. USA 106, 18273-18278 (2009).
32. Kerman, A. et al. Amyotrophic lateral sclerosis is a non-amyloid disease in which extensive misfolding of SOD1 is unique to the familial form. Acta. Neuropathol. 119, 335-344 (2010).
33. Wang, J. et al. Somatodendritic accumulation of misfolded SOD1-L126Z in motor neurons mediates degeneration: alpha B-crystallin modulates aggregation. Hum. Mol. Genet. 14, 2335-2347 (2005).
34. Banci, L. et al. SOD1 and amyotrophic lateral sclerosis: mutations and oligomerization. PLoS ONE 3, e1677 (2008).
35. Wang, J. et al. Fibrillar inclusions and motor neuron degeneration in transgenic mice expressing superoxide dismutase 1 with a disrupted copper-binding site. Neurobiol. Dis. 10, 128-138 (2002).
36. Lindberg, M. J., Tibell, L. & Oliveberg, M. Common denominator of Cu/Zn superoxide dismutase mutants associated with amyotrophic lateral sclerosis: decreased stability of the apo state. Proc. Natl Acad. Sci. USA 99, 16607-16612 (2002).
37. Furukawa, Y., Kaneko, K., Yamanaka, K., O'Halloran, T. V. & Nukina, N. Complete loss of post-translational modifications triggers fibrillar aggregation of SOD1 in the familial form of amyotrophic lateral sclerosis. J. Biol. Chem. 283, 24167-24176 (2008).
38. Durer, Z. A. O. et al. Loss of metal ions, disulfide reduction and mutations related to familial ALS promote formation of amyloid-like aggregates from superoxide dismutase. PLoS ONE 4, e5004 (2009).
39. Hayward, L. J. et al. Decreased metallation and activity in subsets of mutant superoxide dismutases associated with familial amyotrophic lateral sclerosis. J. Biol. Chem. 277, 15923-15931 (2002).
40. Lelie, H. L. et al. Copper and zinc metallation status of copper-zinc superoxide dismutase from amyotrophic lateral sclerosis transgenic mice. J. Biol. Chem. 286, 2795-2806 (2011).
41. Hough, M. A. et al. Dimer destabilization in superoxide dismutase may result in disease-causing properties: structures of motor neuron disease mutants. Proc. Natl Acad. Sci. USA 101, 5976-5981 (2004).
42. Svensson, A.-K. E. et al. Metal-free ALS variants of dimeric human Cu, Zn-superoxide dismutase have enhanced populations of monomeric species. PLoS ONE 5, e10064 (2010).
43. Tiwari, A. & Hayward, L. J. Familial amyotrophic lateral sclerosis mutants of copper/zinc superoxide dismutase are susceptible to disulfide reduction. J. Biol. Chem. 278, 5984-5992 (2003).
44. Cao, X. H. et al. Structures of the G85R variant of SOD1 in familial amyotrophic lateral sclerosis. J. Biol. Chem. 283, 16169-16177 (2008).
45. Proescher, J. B., Son, M., Elliott, J. L. & Culotta, V. C. Biological effects of CCS in the absence of SOD1 enzyme activation: implications for disease in a mouse model for ALS. Hum. Mol. Genet. 17, 1728-1737 (2008).
46. Witan, H. et al. Wild-type Cu/Zn superoxide dismutase (SOD1) does not facilitate, but impedes the formation of protein aggregates of amyotrophic lateral sclerosis causing mutant SOD1. Neurobiol. Dis. 36, 331-342 (2009).
47. Lindberg, M. J., Normark, J., Holmgren, A. & Oliveberg, M. Folding of human superoxide dismutase: disulfide reduction prevents dimerization and produces marginally stable monomers. Proc. Natl Acad. Sci. USA 101, 15893-15898 (2004).
48. Rumfeldt, J. A. O., Lepock, J. R. & Meiering, E. M. Unfolding and folding kinetics of amyotrophic lateral sclerosis-associated mutant Cu, Zn superoxide dismutases. J. Mol. Biol. 385, 278-298 (2009).
49. Lindberg, M. J., Bystrom, R., Boknas, N., Andersen, P. M. & Oliveberg, M. Systematically perturbed folding patterns of amyotrophic lateral sclerosis (ALS)-associated SOD1 mutants. Proc. Natl Acad. Sci. USA 102, 9754-9759 (2005).
50. Kayatekin, C., Zitzewitz, J. A. & Matthews, C. R. Disulfide-reduced ALS variants of Cu, Zn superoxide dismutase exhibit increased populations of unfolded species. J. Mol. Biol. 398, 320-331 (2010).
51. Kayatekin, C., Zitzewitz, J. A. & Matthews, C. R. Zinc binding modulates the entire folding free energy surface of human Cu, Zn superoxide dismutase. J. Mol. Biol. 384, 540-555 (2008).
52. Zetterstrom, P., Graffmo, K. S., Andersen, P. M., Brannstrom, T. & Marklund, S. L. Composition of soluble misfolded superoxide dismutase-1 in murine models of amyotrophic lateral sclerosis. Neuromolecular Med. 15, 147-158 (2013).
53. Aricescu, A. R., Lu, W. X. & Jones, E. Y. A time-and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr. D Biol. Crystallogr. 62, 1243-1250 (2006).
54. Banci, L., Bertini, I., Cantini, F., D'Amelio, N. & Gaggelli, E. Human SOD1 before harboring the catalytic metal-solution structure of copper-depleted, disulfide-reduced form. J. Biol. Chem. 281, 2333-2337 (2006).
55. Banci, L., Bertini, I., Cramaro, F., Del Conte, R. & Viezzoli, M. S. The solution structure of reduced dimeric copper zinc superoxide dismutase-the structural effects of dimerization. Eur. J. Biochem. 269, 1905-1915 (2002).
56. Tamiola, K., Acar, B. & Mulder, F. A. A. Sequence-specific random coil chemical shifts of intrinsically disordered proteins. J. Am. Chem. Soc. 132, 18000-18003 (2010).
57. Tamiola, K. & Mulder, F. A. A. Using NMR chemical shifts to calculate the propensity for structural order and disorder in proteins. Biochem. Soc. Trans. 40, 1014-1020 (2012).
58. Banci, L. et al. Structural and dynamic aspects related to oligomerization of apo SOD1 and its mutants. Proc. Natl Acad. Sci. USA 106, 6980-6985 (2009).