ZnII(atsm) is protective in amyotrophic lateral sclerosis model mice via a copper delivery mechanism

Neurobiology of Disease

Volumn 81, Issue , 2015, Pages 20-24

  McAllum, Erin J ^a   Roberts, Blaine R ^a   Hickey, James L ^b   Dang, Theresa N ^a   Grubman, Alexandra ^a   Donnelly, Paul S ^b   Liddell, Jeffrey R ^a   White, Anthony R ^a   Crouch, Peter J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Amyotrophic lateral sclerosis (ALS); Bisthiosemicarbazone (btsc); Copper; Copper zinc superoxide dismutase (SOD1); Inductively coupled plasma mass spectrometry (ICP MS); Metal; Mouse model; Therapeutic; Transmetallation; Zinc

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; DIACETYL BIS(4 METHYLTHIOSEMICARBAZONATO)ZINC; METAL COMPLEX; UNCLASSIFIED DRUG; (2,3-BUTANEDIONE BIS(N(4)-DIMETHYLTHIOSEMICARBAZONE))ZINC(II); COORDINATION COMPOUND; COPPER; CUPRIC CHLORIDE; ORGANOMETALLIC COMPOUND; SOD1 G37R PROTEIN, MOUSE; SUPEROXIDE DISMUTASE; THIOSEMICARBAZONE DERIVATIVE; ZINC;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LOCOMOTION; MALE; MASS SPECTROMETRY; METALLATION; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SURVIVAL RATE; SURVIVAL TIME; AGE; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; TRANSGENIC MOUSE;

AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANALYSIS OF VARIANCE; ANIMALS; COORDINATION COMPLEXES; COPPER; DISEASE MODELS, ANIMAL; LOCOMOTION; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGANOMETALLIC COMPOUNDS; SUPEROXIDE DISMUTASE; THIOSEMICARBAZONES; ZINC;

EID: 84950317645     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.02.023     Document Type: Article

References (30)

1. Andersen P.M., et al. Sixteen novel mutations in the Cu/Zn superoxide dismutase gene in amyotrophic lateral sclerosis: a decade of discoveries, defects and disputes. ALS and Other Motor Neuron Disorders 2003, 4:62-73. 10.1080/14660820310011700.
2. Barnard P., et al. Towards new copper based radiopharmaceuticals. Q. J. Nucl. Med. Mol. Imaging 2008, 52:174-184.
3. Bensimon G., Lacomblez L., Meininger V., Group A.R.S. A controlled trial of riluzole in amyotrophic lateral sclerosis. N. Engl. J. Med. 1994, 330:585-591. 10.1056/NEJM199403033300901.
4. Bourassa M.W., Brown H.H., Borchelt D.R., Vogt S., Miller L.M. Metal-deficient aggregates and diminished copper found in cells expressing SOD1 mutations that cause ALS. Front. Aging Neurosci. 2014, 6:1-6. 10.3389/fnagi.2014.00110.
5. Cowley A.R., Dilworth J.R., Donnelly P.S., Labisbal E., Sousa A. An unusual dimeric structure of a Cu(I) Bis(thiosemicarbazone) complex: implications for the mechanism of hypoxic selectivity of the Cu(II) derivatives. J. Am. Chem. Soc. 2002, 124:5270-5271. 10.1021/ja012668z.
6. Cowley A.R., et al. Fluorescence studies of the intra-cellular distribution of zinc bis(thiosemicarbazone) complexes in human cancer cells. Chem. Commun. 2005, 845-847. 10.1039/b417206j.
7. Crow J.P., Sampson J.B., Zhuang Y., Thompson J.A., Beckman J.S. Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J. Neurochem. 1997, 69:1936-1944. 10.1046/j.1471-4159.1997.69051936.x.
8. Ding F., Dokholyan N.V. Dynamical roles of metal ions and the disulfide bond in Cu, Zn superoxide dismutase folding and aggregation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19696-19701. 10.1073/pnas.0803266105.
9. Donnelly P.S., et al. Selective intracellular release of copper and zinc ions from bis(thiosemicarbazonato) complexes reduces levels of Alzheimer disease amyloid-B peptide. J. Biol. Chem. 2008, 283:4568-4577. 10.1074/jbc.M705957200.
10. Elliott J.L. Zinc and copper in the pathogenesis of amyotrophic lateral sclerosis. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2001, 25:1169-1185.
11. Estevez A.G. Induction of nitric oxide - dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 1999, 286:2498-2500. 10.1126/science.286.5449.2498.
12. Gurney M.E., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775. 10.1126/science.8209258.
13. Hayward L.J., et al. Decreased metallation and activity in subsets of mutant superoxide dismutases associated with familial amyotrophic lateral sclerosis. J. Biol. Chem. 2002, 277:15923-15931. 10.1074/jbc.M112087200.
14. Holland J., et al. Functionalized Bis(thiosemicarbazonato) complexes of zinc and copper: synthetic platforms toward site-specific radiopharmaceuticals. Inorg. Chem. 2007, 46:465-485.
15. Lelie H.L., et al. Copper and zinc metallation status of copper-zinc superoxide dismutase from amyotrophic lateral sclerosis transgenic mice. J. Biol. Chem. 2011, 286:2795-2806. 10.1074/jbc.M110.186999.
16. 62Cu-labeled bifunctional radiopharmaceuticals with metabolizable ester groups. Nucl. Med. Biol. 1992, 19:33-38.
17. Maynard C.J., et al. Gender and genetic background effects on brain metal levels in APP transgenic and normal mice: implications for Alzheimer beta-amyloid pathology. J. Inorg. Biochem. 2006, 100:952-962. 10.1016/j.jinorgbio.2006.02.010.
18. II(atsm) in the SOD1-G37R mouse model of amyotrophic lateral sclerosis. Amyotroph. Lateral. Scler. Frontotemporal Degener. 2013, 14:586-590. 10.3109/21678421.2013.824000.
19. Miller R., et al. Clinical trials of riluzole in patients with ALS. Neurology 1996, 47:86S-92S. 10.1212/WNL.47.4_Suppl_2.86S.
20. Perry J.J., Shin D.S., Getzoff E.D., Tainer J.A. The structural biochemistry of the superoxide dismutases. Biochim. Biophys. Acta 2010, 1804:245-262. 10.1016/j.bbapap.2009.11.004.
21. Petering D.H. Concerning the role of zinc in the antitumor activity of 3-ethoxy-2-oxobutyraldehyde bis(thiosemicarbazonato) zinc(II) and related chelates. Biochem. Pharmacol. 1974, 23:567-576. 10.1016/0006-2952(74)90621-2.
22. Pratt A.J., Getzoff E.D., Perry J.J. Amyotrophic lateral sclerosis: update and new developments. Degenerative Neurological and Neuromuscular Disease 2012, 1-14. 10.2147/DNND.S19803 (2012).
23. Rhoads T.W., et al. Measuring copper and zinc superoxide dismutase from spinal cord tissue using electrospray mass spectrometry. Anal. Biochem. 2011, 415:52-58. 10.1016/j.ab.2011.03.029.
24. Roberts B.R., et al. Structural characterization of zinc-deficient human superoxide dismutase and implications for ALS. J. Mol. Biol. 2007, 373:877-890. 10.1016/j.jmb.2007.07.043.
25. II(atsm) increases mutant SOD1 in vivo but protects motor neurons and improves the phenotype of a transgenic mouse model of amyotrophic lateral sclerosis. J. Neurosci. 2014, 34:8021-8031. 10.1523/jneurosci.4196-13.2014.
26. Rodriguez J.A., et al. Familial amyotrophic lateral sclerosis-associated mutations decrease the thermal stability of distinctly metallated species of human copper/zinc superoxide dismutase. J. Biol. Chem. 2002, 277:15932-15937. 10.1074/jbc.M112088200.
27. Sahawneh M.A., et al. Cu, Zn-superoxide dismutase increases toxicity of mutant and zinc-deficient superoxide dismutase by enhancing protein stability. J. Biol. Chem. 2010, 285:33885-33897. 10.1074/jbc.M110.118901.
28. Saji H., Saiga A., Iida Y., Magata Y., Yokoyama A. Synthesis and in vivo behavior of a copper-64-labeled dithiosemicarbazone derivative coupled to a dihydropyridine carrier. J. Label. Compd. Radiopharm. 1992, 33:127-135.
29. II(atsm)) protects against peroxynitrite-induced nitrosative damage and prolongs survival in amyotrophic lateral sclerosis mouse model. J. Biol. Chem. 2011, 286:44035-44044. 10.1074/jbc.M111.274407.
30. Wong P.C., et al. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 1995, 14:1105-1116. 10.1016/0896-6273(95)90259-7.