Increased Zinc and Manganese in Parallel with Neurodegeneration, Synaptic Protein Changes and Activation of Akt/GSK3 Signaling in Ovine CLN6 Neuronal Ceroid Lipofuscinosis

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Kanninen, Katja M ^a   Grubman, Alexandra ^a   Meyerowitz, Jodi ^a   Duncan, Clare ^a   Tan, Jiang Li ^a   Parker, Sarah J ^a   Crouch, Peter J ^a   Paterson, Brett M ^b   Hickey, James L ^b   Donnelly, Paul S ^b   Volitakis, Irene ^a   Tammen, Imke ^c   Palmer, David N ^d   White, Anthony R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d LINCOLN UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

COBALT; COPPER; GLYCOGEN SYNTHASE KINASE 3; IRON; MAGNESIUM; MANGANESE; METALLOTHIONEIN I; METALLOTHIONEIN II; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POTASSIUM; PROTEIN KINASE B; SODIUM; SYNAPTOPHYSIN; SYNTAXIN; SYNTAXIN 6; UNCLASSIFIED DRUG; ZINC;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN LEVEL; BRAIN STEM; CEREBELLUM; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; FRONTAL LOBE; INTRACELLULAR SIGNALING; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEURONAL CEROID LIPOFUSCINOSIS; NEUROPATHOLOGY; NONHUMAN; OCCIPITAL LOBE; PARIETAL LOBE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SHEEP; THALAMUS;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; GLYCOGEN SYNTHASE KINASE 3; MANGANESE; MEMBRANE PROTEINS; METALLOTHIONEIN; MUTATION; NEURONAL CEROID-LIPOFUSCINOSES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SHEEP; SIGNAL TRANSDUCTION; SYNAPSES; ZINC;

EID: 84875032283     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058644     Document Type: Article

References (64)

1. Mole S, Williams R, Goebel H. (2011) The neuronal ceroid lipofuscinoses (batten disease). Second edition. Oxford University Press. 480 p.
2. Rider JA, Rider DL, (1988) Batten disease: Past, present, and future. American J Med Genet Supplement 5pp. 21-26.
3. Kousi M, Lehesjoki AE, Mole SE, (2012) Update of the mutation spectrum and clinical correlations of over 360 mutations in eight genes that underlie the neuronal ceroid lipofuscinoses. Hum Mutat 33: 42-63.
4. Noskova L, Stranecky V, Hartmannova H, Pristoupilova A, Baresova V, et al. (2011) Mutations in DNAJC5, encoding cysteine-string protein alpha, cause autosomal-dominant adult-onset neuronal ceroid lipofuscinosis. Am J Med Genet 89: 241-252.
5. Velinov M, Dolzhanskaya N, Gonzalez M, Powell E, Konidari I, et al. (2012) Mutations in the gene DNAJC5 cause autosomal dominant kufs disease in a proportion of cases: Study of the parry family and 8 other families. PloS One 7: e29729.
6. Haltia M, (2006) The neuronal ceroid-lipofuscinoses: From past to present. Biochim Biophys Acta 1762: 850-856.
7. Chen R, Fearnley IM, Palmer DN, Walker JE, (2004) Lysine 43 is trimethylated in subunit C from bovine mitochondrial ATP synthase and in storage bodies associated with batten disease. J Biol Chem 279: 21883-21887.
8. Palmer DN, Fearnley IM, Walker JE, Hall NA, Lake BD, et al. (1992) Mitochondrial ATP synthase subunit c storage in the ceroid-lipofuscinoses (batten disease). Am J Med Genet 42: 561-567.
9. Mole SE, Williams RE, Goebel HH, editors. (2011) The neuronal ceroid liopfuscinoses (batten disease). United States: Oxford University Press. 444 p.
10. Mole SE, Michaux G, Codlin S, Wheeler RB, Sharp JD, et al. (2004) CLN6, which is associated with a lysosomal storage disease, is an endoplasmic reticulum protein. Exp Cell Res 298: 399-406.
11. Heine C, Koch B, Storch S, Kohlschutter A, Palmer DN, et al. (2004) Defective endoplasmic reticulum-resident membrane protein CLN6 affects lysosomal degradation of endocytosed arylsulfatase A. J Biol Chem. 279: 22347-22352.
12. Jolly RD, Shimada A, Dopfmer I, Slack PM, Birtles MJ, et al. (1989) Ceroid-lipofuscinosis (batten's disease): Pathogenesis and sequential neuropathological changes in the ovine model. Neuropathol Appl Neurobiol 15: 371-383.
13. Tammen I, Houweling PJ, Frugier T, Mitchell NL, Kay GW, et al. (2006) A missense mutation (c.184C>T) in ovine CLN6 causes neuronal ceroid lipofuscinosis in merino sheep whereas affected south hampshire sheep have reduced levels of CLN6 mRNA. Biochim Biophys Acta 1762: 898-905.
14. Kay GW, Jay NP, Palmer DN, (2011) The specific loss of GnRH-positive neurons from the hypothalamus of sheep with CLN6 neuronal ceroid lipofuscinosis occurs without glial activation and has only minor effects on reproduction. Neurobiol Dis 41: 614-623.
15. Oswald MJ, Palmer DN, Kay GW, Shemilt SJ, Rezaie P, et al. (2005) Glial activation spreads from specific cerebral foci and precedes neurodegeneration in presymptomatic ovine neuronal ceroid lipofuscinosis (CLN6). Neurobiol Dis 20: 49-63.
16. Kay GW, Palmer DN, Rezaie P, Cooper JD, (2006) Activation of non-neuronal cells within the prenatal developing brain of sheep with neuronal ceroid lipofuscinosis. Brain Pathol (Zurich, Switzerland) 16: 110-116.
17. Oswald MJ, Palmer DN, Kay GW, Barwell KJ, Cooper JD, (2008) Location and connectivity determine GABAergic interneuron survival in the brains of south hampshire sheep with CLN6 neuronal ceroid lipofuscinosis. Neurobiol Dis 32: 50-65.
18. Kay GW, Jay NP, Palmer DN, (2011) The specific loss of GnRH-positive neurons from the hypothalamus of sheep with CLN6 neuronal ceroid lipofuscinosis occurs without glial activation and has only minor effects on reproduction. Neurobiol Dis 41: 614-623.
19. Bolognin S, Messori L, Zatta P, (2009) Metal ion physiopathology in neurodegenerative disorders. Neuromolecular Med 11: 223-238.
20. Duce JA, Bush AI, (2010) Biological metals and alzheimer's disease: Implications for therapeutics and diagnostics. Prog Neurobiol 92: 1-18.
21. Obrenovich ME, Shamberger RJ, Lonsdale D, (2011) Altered heavy metals and transketolase found in autistic spectrum disorder. Biol Trace Elem Res 2144 (1-3) (): 475-86.
22. Kurian MA, McNeill A, Lin JP, Maher ER, (2011) Childhood disorders of neurodegeneration with brain iron accumulation (NBIA). Dev Med Child Neurol 53: 394-404.
23. Sensi SL, Paoletti P, Koh JY, Aizenman E, Bush AI, et al. (2011) The neurophysiology and pathology of brain zinc. J Neurosci 31: 16076-16085.
24. Lee SJ, Koh JY, (2010) Roles of zinc and metallothionein-3 in oxidative stress-induced lysosomal dysfunction, cell death, and autophagy in neurons and astrocytes. Mol Brain 3: 30.
25. Johansson E, Lindh U, Westermarck T, Heiskala H, Santavuori P, (1990) Altered elemental profiles in neuronal ceroid lipofuscinosis. J Trace Elem Electrolytes Health Dis 4: 139-142.
26. Heiskala H, Gutteridge JM, Westermarck T, Alanen T, Santavuori P, (1988) Bleomycin-detectable iron and phenanthroline-detectable copper in the cerebrospinal fluid of patients with neuronal ceroid-lipofuscinoses. Am J Med Genet Suppl. 5pp. 193-202.
27. Palmer DN, Martinus RD, Barns G, Reeves RD, Jolly RD, (1988) Ovine ceroid-lipofuscinosis. I: Lipopigment composition is indicative of a lysosomal proteinosis. Am J Med Genet Suppl. 5pp. 141-158.
28. Samuelson DA, Armstrong D, Jolly R, (1990) X-ray microprobe analysis of the retina and RPE in sheep with ovine ceroid-lipofuscinosis. Neurobiol Aging 11: 663-667.
29. Frugier T, Mitchell NL, Tammen I, Houweling PJ, Arthur DG, et al. (2008) A new large animal model of CLN5 neuronal ceroid lipofuscinosis in borderdale sheep is caused by a nucleotide substitution at a consensus splice site (c.571+1G>A) leading to excision of exon 3. Neurobiol Dis 29: 306-315.
30. Maynard CJ, Cappai R, Volitakis I, Cherny RA, White AR, et al. (2002) Overexpression of alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J Biol Chem 277: 44670-44676.
31. Templeton DM, Cherian MG, (1984) Chemical modifications of metallothionein. preparation and characterization of polymers. Biochem J 221: 569-575.
32. Zangger K, Shen G, Oz G, Otvos JD, Armitage IM, (2001) Oxidative dimerization in metallothionein is a result of intermolecular disulphide bonds between cysteines in the alpha-domain. Biochem J 359: 353-360.
33. Oppermann B, Zhang W, Magabo K, Kantorow M, (2001) Identification and spatial analysis of metallothioneins expressed by the adult human lens. Invest Ophthalmol Vis Sci 42: 188-193.
34. Kielar C, Wishart TM, Palmer A, Dihanich S, Wong AM, et al. (2009) Molecular correlates of axonal and synaptic pathology in mouse models of batten disease. Hum Mol Genet 18: 4066-4080.
35. Nuttall JR, Oteiza PI, (2012) Zinc and the ERK kinases in the developing brain. Neurotox Res 21 (1) (): 128-41.
36. Lin CL, Tseng HC, Chen RF, Chen WP, Su MJ, et al. (2011) Intracellular zinc release-activated ERK-dependent GSK-3beta-p53 and noxa-mcl-1 signaling are both involved in cardiac ischemic-reperfusion injury. Cell Death Differ 18: 1651-1663.
37. Mayhew IG, Jolly RD, Pickett BT, Slack PM, (1985) Ceroid-lipofuscinosis (batten's disease): Pathogenesis of blindness in the ovine model. Neuropathol Appl Neurobiol 11: 273-290.
38. Hesketh S, Sassoon J, Knight R, Hopkins J, Brown DR, (2007) Elevated manganese levels in blood and central nervous system occur before onset of clinical signs in scrapie and bovine spongiform encephalopathy. J Anim Sci 85: 1596-1609.
39. Bakirdere S, Kizilkan N, Yaman M, (2011) Determination of zinc, copper, iron, and manganese in different regions of lamb brain. Biol Trace Elem Res 142: 492-499.
40. Dimri U, Sharma MC, Yamdagni A, Ranjan R, Zama MM, (2010) Psoroptic mange infestation increases oxidative stress and decreases antioxidant status in sheep. Vet Parasitol 168: 318-322.
41. Assaf SY, Chung SH, (1984) Release of endogenous Zn2+ from brain tissue during activity. Nature 308: 734-736.
42. Iguchi K, Usui S, Inoue T, Sugimura Y, Tatematsu M, et al. (2002) High-level expression of zinc transporter-2 in the rat lateral and dorsal prostate. J J Androl 23: 819-824.
43. Palmiter RD, Cole TB, Findley SD, (1996) ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration. EMBO J 15: 1784-1791.
44. Toth K, (2011) Zinc in neurotransmission. Annu Rev Nutr 31: 139-153.
45. Andreini C, Banci L, Bertini I, Rosato A, (2006) Zinc through the three domains of life. J Proteome Res 5: 3173-3178.
46. Garrick MD, Dolan KG, Horbinski C, Ghio AJ, Higgins D, et al. (2003) DMT1: A mammalian transporter for multiple metals. Biometals 16: 41-54.
47. Himeno S, Yanagiya T, Fujishiro H, (2009) The role of zinc transporters in cadmium and manganese transport in mammalian cells. Biochimie 91: 1218-1222.
48. Bowman AB, Kwakye GF, Herrero Hernandez E, Aschner M, (2011) Role of manganese in neurodegenerative diseases. J Trace Elem Med Biol 25: 191-203.
49. Farias FH, Zeng R, Johnson GS, Wininger FA, Taylor JF, et al. (2011) A truncating mutation in ATP13A2 is responsible for adult-onset neuronal ceroid lipofuscinosis in tibetan terriers. Neurobiol Dis 42: 468-474.
50. Ramonet D, Podhajska A, Stafa K, Sonnay S, Trancikova A, et al. (2012) PARK9-associated ATP13A2 localizes to intracellular acidic vesicles and regulates cation homeostasis and neuronal integrity. Hum Mol Genet 21: 1725-1743.
51. Podhajska A, Musso A, Trancikova A, Stafa K, Moser R, et al. (2012) Common pathogenic effects of missense mutations in the P-type ATPase ATP13A2 (PARK9) associated with early-onset parkinsonism. PloS One 7: e39942.
52. Ugolino J, Fang S, Kubisch C, Monteiro MJ, (2011) Mutant Atp13a2 proteins involved in parkinsonism are degraded by ER-associated degradation and sensitize cells to ER-stress induced cell death. Hum Mol Genet 20: 3565-3577.
53. Ramirez A, Heimbach A, Grundemann J, Stiller B, Hampshire D, et al. (2006) Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat Genet 38: 1184-1191.
54. Wohlke A, Philipp U, Bock P, Beineke A, Lichtner P, et al. (2011) A one base pair deletion in the canine ATP13A2 gene causes exon skipping and late-onset neuronal ceroid lipofuscinosis in the tibetan terrier. PLoS Genet 7: e1002304.
55. Bras J, Verloes A, Schneider SA, Mole SE, Guerreiro RJ, (2012) Mutation of the parkinsonism gene ATP13A2 causes neuronal ceroid-lipofuscinosis. Hum Mol Genet 21: 2646-2650.
56. Wang X, Li H, Fan Z, Liu Y, (2012) Effect of zinc supplementation on type 2 diabetes parameters and liver metallothionein expressions in wistar rats. J Physiol Biochem 68 (4) (): 563-72.
57. Santavuori P, Heiskala H, Westermarck T, Sainio K, Moren R, (1988) Experience over 17 years with antioxidant treatment in spielmeyer-sjogren disease. Am J Med Genet Suppl 5pp. 265-274.
58. Cheung EC, Slack RS, (2004) Emerging role for ERK as a key regulator of neuronal apoptosis. Science's STKE: Sci STKE 251: PE45.
59. Lei P, Ayton S, Bush AI, Adlard PA, (2011) GSK-3 in neurodegenerative diseases. Int J Alzheimers Dis 2011: 189246.
60. Olanow CW, (2004) Manganese-induced parkinsonism and parkinson's disease. Ann N Y Acad Sci 1012: 209-223.
61. Heine C, Tyynela J, Cooper JD, Palmer DN, Elleder M, et al. (2003) Enhanced expression of manganese-dependent superoxide dismutase in human and sheep CLN6 tissues. Biochem J 376: 369-376.
62. Uusi-Rauva K, Luiro K, Tanhuanpaa K, Kopra O, Martin-Vasallo P, et al. (2008) Novel interactions of CLN3 protein link batten disease to dysregulation of fodrin-na+, K+ ATPase complex. Exp Cell Res 314: 2895-2905.
63. Adlard PA, Bica L, White AR, Nurjono M, Filiz G, et al. (2011) Metal ionophore treatment restores dendritic spine density and synaptic protein levels in a mouse model of alzheimer's disease. PloS One 6: e17669.
64. Benedict JW, Getty AL, Wishart TM, Gillingwater TH, Pearce DA, (2009) Protein product of CLN6 gene responsible for variant late-onset infantile neuronal ceroid lipofuscinosis interacts with CRMP-2. J Neurosci Res 87: 2157-2166.