Modeling Neurodegeneration in Zebrafish

•• Eisen JS, Smith JC. Controlling morpholino experiments: don’t stop making antisense. Development. 2008;135:1735–43. This article comprehensively described how to properly design and interpret MO experiments in zebrafish.

Thermes V, Grabher C, Ristoratore F, et al. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev. 2002;118:91–8.

Kawakami K, Shima A, Kawakami N. Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc Natl Acad Sci USA. 2000;97:11403–8.

Driever W, Solnica-Krezel L, Schier AF, et al. A genetic screen for mutations affecting embryogenesis in zebrafish. Development. 1996;123:37–46.

Rink E, Wullimann MF. Connections of the ventral telencephalon and tyrosine hydroxylase distribution in the zebrafish brain (Danio rerio) lead to identification of an ascending dopaminergic system in a teleost. Brain Res Bull. 2002;57:385–7.

Greene JC, Whitworth AJ, Kuo I, et al. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci USA. 2003;100:4078–83.

Whitworth AJ, Theodore DA, Greene JC, et al. Increased glutathione S-transferase activity rescues dopaminergic neuron loss in a Drosophila model of Parkinson’s disease. Proc Natl Acad Sci USA. 2005;102:8024–9.

Dawson TM, Ko HS, Dawson VL. Genetic animal models of Parkinson’s disease. Neuron. 2010;66:646–61.

Flinn L, Mortiboys H, Volkmann K, et al. Complex I deficiency and dopaminergic neuronal cell loss in parkin-deficient zebrafish (Danio rerio). Brain. 2009;132(Pt 6):1613–23.

Fett ME, Pilsl A, Paquet D, et al. Parkin is protective against proteotoxic stress in a transgenic zebrafish model. PLoS One. 2010; 5:doi: 10.1371/journal.pone.0011783 .

Clark IE, Dodson MW, Jiang C, et al. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature. 2006;441:1162–6.

Park J, Lee SB, Lee S, et al. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature. 2006;441:1157–61.

Kitada T, Pisani A, Porter DR, et al. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci USA. 2007;104:11441–6.

Gautier CA, Kitada T, Shen J. Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci USA. 2008;105:11364–9.

Anichtchik O, Diekmann H, Fleming A, et al. Loss of PINK1 function affects development and results in neurodegeneration in zebrafish. J Neurosci. 2008;28:8199–207.

Xi Y, Ryan J, Noble S, et al. Impaired dopaminergic neuron development and locomotor function in zebrafish with loss of pink1 function. Eur J Neurosci. 2010;31:623–33.

Sallinen V, Kolehmainen J, Priyadarshini M, et al. Dopaminergic cell damage and vulnerability to MPTP in Pink1 knockdown zebrafish. Neurobiol Dis. 2010;40:93–101.

Bandmann O, Flinn L, Mortiboys H. POMD08 Zebrafish models for early onset Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2010;81: doi: 10.1136/jnnp.2010.226340.168 .

Bai Q, Mullett SJ, Garver JA, et al. Zebrafish DJ-1 is evolutionarily conserved and expressed in dopaminergic neurons. Brain Res. 2006;1113:33–44.

Bretaud S, Allen C, Ingham PW, et al. p53-dependent neuronal cell death in a DJ-1-deficient zebrafish model of Parkinson’s disease. J Neurochem. 2007;100:1626–35.

Baulac S, Lu H, Strahle J, et al. Increased DJ-1 expression under oxidative stress and in Alzheimer’s disease brains. Mol Neurodegener. 2009;4:12.

Liu Z, Wang X, Yu Y, et al. A Drosophila model for LRRK2-linked parkinsonism. Proc Natl Acad Sci USA. 2008;105:2693–8.

Ng CH, Mok SZ, Koh C, et al. Parkin protects against LRRK2 G2019S mutant-induced dopaminergic neurodegeneration in Drosophila. J Neurosci. 2009;29:11257–62.

Li Y, Liu W, Oo TF, et al. Mutant LRRK2(R1441G) BAC transgenic mice recapitulate cardinal features of Parkinson’s disease. Nat Neurosci. 2009;12:826–8.

Li X, Patel JC, Wang J, et al. Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson’s disease mutation G2019S. J Neurosci. 2010;30:1788–97.

Sheng D, Qu D, Kwok KH, et al. Deletion of the WD40 domain of LRRK2 in Zebrafish causes Parkinsonism-like loss of neurons and locomotive defect. PLoS Genet. 2010;6:doi: 10.1371/journal.pgen.1000914 .

Son OL, Kim HT, Ji MH, et al. Cloning and expression analysis of a Parkinson’s disease gene, uch-L1, and its promoter in zebrafish. Biochem Biophys Res Commun. 2003;312:601–7.

Guella I, Pistocchi A, Asselta R, et al. Mutational screening and zebrafish functional analysis of GIGYF2 as a Parkinson-disease gene. Neurobiol Aging. 2010;doi: 10.1016/j.neurobiolaging.2009.12.016 .

Anichtchik OV, Kaslin J, Peitsaro N, et al. Neurochemical and behavioural changes in zebrafish Danio rerio after systemic administration of 6-hydroxydopamine and 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. J Neurochem. 2004;88:443–53.

Lam CS, Korzh V, Strahle U. Zebrafish embryos are susceptible to the dopaminergic neurotoxin MPTP. Eur J Neurosci. 2005;21:1758–62.

Bretaud S, Lee S, Guo S. Sensitivity of zebrafish to environmental toxins implicated in Parkinson’s disease. Neurotoxicol Teratol. 2004;26:857–64.

McKinley ET, Baranowski TC, Blavo DO, et al. Neuroprotection of MPTP-induced toxicity in zebrafish dopaminergic neurons. Brain Res Mol Brain Res. 2005;141:128–37.

Wen L, Wei W, Gu W, et al. Visualization of monoaminergic neurons and neurotoxicity of MPTP in live transgenic zebrafish. Dev Biol. 2008;314:84–92.

Sallinen V, Torkko V, Sundvik M, et al. MPTP and MPP+ target specific aminergic cell populations in larval zebrafish. J Neurochem. 2009;108:719–31.

Graveland GA, Williams RS, DiFiglia M. Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington’s disease. Science. 1985;227:770–3.

Karlovich CA, John RM, Ramirez L, et al. Characterization of the Huntington’s disease (HD) gene homologue in the zebrafish Danio rerio. Gene. 1998;217:117–25.

Zeitlin S, Liu JP, Chapman DL, et al. Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington’s disease gene homologue. Nat Genet. 1995;11:155–63.

Lumsden AL, Henshall TL, Dayan S, et al. Huntingtin-deficient zebrafish exhibit defects in iron utilization and development. Hum Mol Genet. 2007;16:1905–20.

Morrison PJ, Nevin NC. Serum iron, total iron binding capacity and ferritin in early Huntington disease patients. Ir J Med Sci. 1994;163:236–7.

Henshall TL, Tucker B, Lumsden AL, et al. Selective neuronal requirement for huntingtin in the developing zebrafish. Hum Mol Genet. 2009;18:4830–42.

Pirogovsky E, Gilbert PE, Jacobson M, et al. Impairments in source memory for olfactory and visual stimuli in preclinical and clinical stages of Huntington’s disease. J Clin Exp Neuropsychol. 2007;29:395–404.

Diekmann H, Anichtchik O, Fleming A, et al. Decreased BDNF levels are a major contributor to the embryonic phenotype of huntingtin knockdown zebrafish. J Neurosci. 2009;29:1343–9.

Schiffer NW, Broadley SA, Hirschberger T, et al. Identification of anti-prion compounds as efficient inhibitors of polyglutamine protein aggregation in a zebrafish model. J Biol Chem. 2007;282:9195–203.

Williams A, Sarkar S, Cuddon P, et al. Novel targets for Huntington’s disease in an mTOR-independent autophagy pathway. Nat Chem Biol. 2008;4:295–305.

• Subramaniam S, Sixt KM, Barrow R, et al. Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity. Science. 2009;324:1327–30. The Rhes protein found specifically in the mammalian striatum may explain the specific death of medium spiny neurons in HD.

Schilling G, Becher MW, Sharp AH, et al. Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Hum Mol Genet. 1999;8:397–407.

Musa A, Lehrach H, Russo VA. Distinct expression patterns of two zebrafish homologues of the human APP gene during embryonic development. Dev Genes Evol. 2001;211:563–7.

Leimer U, Lun K, Romig H, et al. Zebrafish (Danio rerio) presenilin promotes aberrant amyloid beta-peptide production and requires a critical aspartate residue for its function in amyloidogenesis. Biochemistry. 1999;38:13602–9.

Groth C, Nornes S, McCarty R, et al. Identification of a second presenilin gene in zebrafish with similarity to the human Alzheimer’s disease gene presenilin2. Dev Genes Evol. 2002;212:486–90.

Joshi P, Liang JO, DiMonte K, et al. Amyloid precursor protein is required for convergent-extension movements during Zebrafish development. Dev Biol. 2009;335:1–11.

Babin PJ, Thisse C, Durliat M, et al. Both apolipoprotein E and A-I genes are present in a nonmammalian vertebrate and are highly expressed during embryonic development. Proc Natl Acad Sci USA. 1997;94:8622–7.

Tomasiewicz HG, Flaherty DB, Soria JP, et al. Transgenic zebrafish model of neurodegeneration. J Neurosci Res. 2002;70:734–45.

Bai Q, Garver JA, Hukriede NA, et al. Generation of a transgenic zebrafish model of Tauopathy using a novel promoter element derived from the zebrafish eno2 gene. Nucleic Acids Res. 2007;35:6501–16.

•• Paquet D, Bhat R, Sydow A, et al. A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J Clin Invest. 2009;119:1382–95. Generation of a stable transgenic Gal4-UAS–based zebrafish model expressing human tau with a mutation found in frontotemporal dementia AD patients shows pathologic features of tauopathies.

• Rogaeva E, Meng Y, Lee JH, et al. The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat Genet. 2007;39:168–77. AD-associated SNPs are found in the SORL1 protein, which normally helps sequester APP from cleavage enzymes that generate cytotoxic Aβ.

Andersen OM, Reiche J, Schmidt V, et al. Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc Natl Acad Sci USA. 2005;102:13461–6.