Regulation of Intracellular Copper by Induction of Endogenous Metallothioneins Improves the Disease Course in a Mouse Model of Amyotrophic Lateral Sclerosis

Neurotherapeutics

Volumn 12, Issue 2, 2015, Pages 461-476

  Tokuda, Eiichi ^a,b   Watanabe, Shunsuke ^a   Okawa, Eriko ^a   Ono, Shin ichi ^a,c  

^a NIHON UNIVERSITY   (Japan)

^b UMEÅ UNIVERSITY   (Sweden)

^c Akiru Municipal Medical Center   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Copper dyshomeostasis; Dexamethasone; Metallothioneins; Superoxide dismutase 1

Indexed keywords

ANTIINFLAMMATORY AGENT; CD11B ANTIGEN; COPPER; DEXAMETHASONE; ENOLASE; GLIAL FIBRILLARY ACIDIC PROTEIN; ISOPROTEIN; LIPID PEROXIDE; METALLOTHIONEIN; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE;

AGE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MOUSE; PATHOLOGY; SPINAL CORD; TIME FACTOR; TRANSGENIC MOUSE; UPREGULATION;

AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD11B; COPPER; DEXAMETHASONE; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; LIPID PEROXIDES; METALLOTHIONEIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHOPYRUVATE HYDRATASE; PROTEIN ISOFORMS; SPINAL CORD; SUPEROXIDE DISMUTASE; TIME FACTORS; UP-REGULATION;

EID: 84939943500     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-015-0346-x     Document Type: Article

References (44)

1. Miller RG, Mitchell JD, Moore DH. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst Rev 2012;3:Cd001447.
2. Poppe L, Rue L, Robberecht W, Van Den Bosch L. Translating biological findings into new treatment strategies for amyotrophic lateral sclerosis (ALS). Exp Neurol 2014;262:138-151.
3. Rosen DR, Siddique T, Patterson D, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993;362:59-62.
4. Gurney ME, Pu H, Chiu AY, et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994;264:1772-1775.
5. Robberecht W, Philips T. The changing scene of amyotrophic lateral sclerosis. Nat Rev Neurosci 2013;14:248-264.
6. Tokuda E, Okawa E, Watanabe S, Ono S, Marklund SL. Dysregulation of intracellular copper homeostasis is common to transgenic mice expressing human mutant superoxide dismutase-1s regardless of their copper-binding abilities. Neurobiol Dis 2013;54:308-319.
7. Li QX, Mok SS, Laughton KM, et al. Overexpression of Abeta is associated with acceleration of onset of motor impairment and superoxide dismutase 1 aggregation in an amyotrophic lateral sclerosis mouse model. Aging Cell 2006;5:153-165.
8. Tokuda E, Ono S, Ishige K, Naganuma A, Ito Y, Suzuki T. Metallothionein proteins expression, copper and zinc concentrations, and lipid peroxidation level in a rodent model for amyotrophic lateral sclerosis. Toxicology 2007;229:33-41.
9. Tokuda E, Okawa E, Ono S. Dysregulation of intracellular copper trafficking pathway in a mouse model of mutant copper/zinc superoxide dismutase-linked familial amyotrophic lateral sclerosis. J Neurochem 2009;111:181-191.
10. Lelie HL, Liba A, Bourassa MW, 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.
11. Tokuda E, Ono S, Ishige K, et al. Ammonium tetrathiomolybdate delays onset, prolongs survival, and slows progression of disease in a mouse model for amyotrophic lateral sclerosis. Exp Neurol 2008;213:122-128.
12. Kiaei M, Bush AI, Morrison BM, et al. Genetically decreased spinal cord copper concentration prolongs life in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurosci 2004;24:7945-7950.
13. West AK, Hidalgo J, Eddins D, Levin ED, Aschner M. Metallothionein in the central nervous system: Roles in protection, regeneration and cognition. Neurotoxicology 2008;29:489-503.
14. Scheiber IF, Dringen R. Astrocyte functions in the copper homeostasis of the brain. Neurochem Int 2013;62:556-565.
15. Tokuda E, Okawa E, Watanabe S, Ono S. Overexpression of metallothionein-I, a copper-regulating protein, attenuates intracellular copper dyshomeostasis and extends lifespan in a mouse model of amyotrophic lateral sclerosis caused by mutant superoxide dismutase-1. Hum Mol Genet 2014;23:1271-1285.
16. Nagano S, Satoh M, Sumi H, et al. Reduction of metallothioneins promotes the disease expression of familial amyotrophic lateral sclerosis mice in a dose-dependent manner. Eur J Neurosci 2001;13:1363-1370.
17. Puttaparthi K, Gitomer WL, Krishnan U, Son M, Rajendran B, Elliott JL. Disease progression in a transgenic model of familial amyotrophic lateral sclerosis is dependent on both neuronal and non-neuronal zinc binding proteins. J Neurosci 2002;22:8790-8796.
18. Masters BA, Kelly EJ, Quaife CJ, Brinster RL, Palmiter RD. Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc Natl Acad Sci U S A 1994;91:584-588.
19. Ludolph AC, Bendotti C, Blaugrund E, et al. Guidelines for the preclinical in vivo evaluation of pharmacological active drugs for ALS/MND: report on the 142nd ENMC international workshop. Amyotroph Lateral Scler 2007;8:217-223.
20. Scott S, Kranz JE, Cole J, et al. Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph Lateral Scler 2008;9:4-15.
21. Alexander GM, Erwin KL, Byers N, et al. Effect of transgene copy number on survival in the G93A SOD1 transgenic mouse model of ALS. Brain Res Mol Brain Res 2004;130:7-15.
22. Heiman-Patterson TD, Sher RB, Blankenhorn EA, et al. Effect of genetic background on phenotype variability in transgenic mouse models of amyotrophic lateral sclerosis: a window of opportunity in the search for genetic modifiers. Amyotroph Lateral Scler 2011;12:79-86.
23. Boillee S, Yamanaka K, Lobsiger CS, et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006;312:1389-1392.
24. Meloni G, Knipp M, Vasak M. Detection of neuronal growth inhibitory factor (metallothionein-3) in polyacrylamide gels and by Western blot analysis. J Biochem Biophys Methods 2005;64:76-81.
25. Friese A, Kaltschmidt JA, Ladle DR, Sigrist M, Jessell TM, Arber S. Gamma and alpha motor neurons distinguished by expression of transcription factor Err3. Proc Natl Acad Sci U S A 2009;106:13588-13593.
26. Mendez-Armenta M, Villeda-Hernandez J, Barroso-Moguel R, Nava-Ruiz C, Jimenez-Capdeville ME, Rios C. Brain regional lipid peroxidation and metallothionein levels of developing rats exposed to cadmium and dexamethasone. Toxicol Lett 2003;144:151-157.
27. Kelly EJ, Sandgren EP, Brinster RL, Palmiter RD. A pair of adjacent glucocorticoid response elements regulate expression of two mouse metallothionein genes. Proc Natl Acad Sci U S A 1997;94:10045-10050.
28. Gong YH, Elliott JL. Metallothionein expression is altered in a transgenic murine model of familial amyotrophic lateral sclerosis. Exp Neurol 2000;162:27-36.
29. Czock D, Keller F, Rasche FM, Haussler U. Pharmacokinetics and pharmacodynamics of systemically administered glucocorticoids. Clin Pharmacokinet 2005;44:61-98.
30. Goto JJ, Zhu H, Sanchez RJ, et al. Loss of in vitro metal ion binding specificity in mutant copper-zinc superoxide dismutases associated with familial amyotrophic lateral sclerosis. J Biol Chem 2000;275:1007-1014.
31. Rotunno MS, Bosco DA. An emerging role for misfolded wild-type SOD1 in sporadic ALS pathogenesis. Front Cell Neurosci 2013;7:253.
32. Bendotti C, Marino M, Cheroni C, et al. Dysfunction of constitutive and inducible ubiquitin-proteasome system in amyotrophic lateral sclerosis: implication for protein aggregation and immune response. Prog Neurobiol 2012;97:101-126.
33. Sillevis Smitt PA, Blaauwgeers HG, Troost D, de Jong JM. Metallothionein immunoreactivity is increased in the spinal cord of patients with amyotrophic lateral sclerosis. Neurosci Lett 1992;144:107-110.
34. Yamanaka K, Chun SJ, Boillee S, et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 2008;11:251-253.
35. Wang L, Gutmann DH, Roos RP. Astrocyte loss of mutant SOD1 delays ALS disease onset and progression in G85R transgenic mice. Hum Mol Genet 2011;20:286-293.
36. Wang L, Sharma K, Grisotti G, Roos RP. The effect of mutant SOD1 dismutase activity on non-cell autonomous degeneration in familial amyotrophic lateral sclerosis. Neurobiol Dis 2009;35:234-240.
37. Amici M, Forti K, Nobili C, et al. Effect of neurotoxic metal ions on the proteolytic activities of the 20S proteasome from bovine brain. J Biol Inorg Chem 2002;7:750-756.
38. Arnesano F, Scintilla S, Calò V, et al. Copper-triggered aggregation of ubiquitin. PLoS One 2009;4:e7052.
39. Ahtoniemi T, Goldsteins G, Keksa-Goldsteine V, et al. Pyrrolidine dithiocarbamate inhibits induction of immunoproteasome and decreases survival in a rat model of amyotrophic lateral sclerosis. Mol Pharmacol 2007;71:30-37.
40. Ferraiuolo L, Kirby J, Grierson AJ, Sendtner M, Shaw PJ. Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat Rev Neurol 2011;7:616-630.
41. Patacchioli FR, Monnazzi P, Scontrini A, et al. Adrenal dysregulation in amyotrophic lateral sclerosis. J Endocrinol Invest 2003;26:Rc23-5.
42. Fidler JA, Treleaven CM, Frakes A, et al. Disease progression in a mouse model of amyotrophic lateral sclerosis: the influence of chronic stress and corticosterone. FASEB J 2011;25:4369-4377.
43. Moser JM, Bigini P, Schmitt-John T. The wobbler mouse, an ALS animal model. Mol Genet Genomics 2013;288:207-229.
44. Gonzalez Deniselle MC, Gonzalez SL, Piroli GG, Lima AE, De Nicola AF. The 21-aminosteroid U-74389F increases the number of glial fibrillary acidic protein-expressing astrocytes in the spinal cord of control and Wobbler mice. Cell Mol Neurobiol 1996;16:61-72.