Exploring Alzheimer's disease in zebrafish

Journal of Alzheimer's Disease

Volumn 20, Issue 4, 2010, Pages 981-990

  Xia, Weiming ^a  

^a HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

Alzheimer; amyloid; secretase; tau; transgenic; zebrafish

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; ANTISENSE OLIGODEOXYNUCLEOTIDE; APOLIPOPROTEIN E4; EPITOPE; GAMMA SECRETASE; GAMMA SECRETASE INHIBITOR; MESSENGER RNA; MONOPHENOL MONOOXYGENASE; NEUROGENIN 1; NOTCH RECEPTOR; PRESENILIN 1; PRESENILIN 2; TAU PROTEIN; UVOMORULIN; APOLIPOPROTEIN E; PRESENILIN 1 PROTEIN, ZEBRAFISH; PRESENILIN 2 PROTEIN, ZEBRAFISH; SECRETASE; ZEBRAFISH PROTEIN;

ALLELE; ALZHEIMER DISEASE; ANIMAL MODEL; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME DEFICIENCY; GENE EXPRESSION SYSTEM; GENE MUTATION; GENE TARGETING; IN VIVO STUDY; MOLECULAR MODEL; NERVE CELL; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; RISK FACTOR; TISSUE DISTRIBUTION; ZEBRA FISH; ANIMAL; ANTAGONISTS AND INHIBITORS; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOLIPOPROTEINS E; HUMANS; PRESENILIN-1; PRESENILIN-2; RECEPTORS, NOTCH; TAU PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77954548661     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-1412     Document Type: Review

References (83)

1. Selkoe DJ (2004) Alzheimer disease: mechanistic understanding predicts novel therapies. Ann Intern Med 140, 627-638.
2. Beis D, Stainier DY (2006) In vivo cell biology: following the zebrafish trend. Trends Cell Biol 16, 105-112.
3. Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8, 353-367.
4. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203, 253-310.
5. Peterson RT, Shaw SY, Peterson TA, Milan DJ, Zhong TP, Schreiber SL, MacRae CA, Fishman MC (2004) Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat Biotechnol 22, 595-599.
6. Jeong JY, Kwon HB, Ahn JC, Kang D, Kwon SH, Park JA, KimKW(2008) Functional and developmental analysis of the blood-brain barrier in zebrafish. Brain Res Bull 75, 619-628.
7. Esch FS, Keim PS, Beattie EC, Blacher RW, Culwell AR, Oltersdorf T, McClure D, Ward PJ (1990) Cleavage of amyloid β-peptide during constitutive processing of its precursor. Science 248, 1122-1124.
8. Sisodia SS, Koo EH, Beyreuther K, Unterbeck A, Price DL (1990) Evidence that b-amyloid protein in Alzheimer's disease is not derived by normal processing. Science 248, 492-495.
9. Haass C, Schlossmacher M, Hung AY, Vigo-Pelfrey C, Mellon A, Ostaszewski B, Lieberburg I,Koo EH, Schenk D,TeplowD, Selkoe D (1992) Amyloid β-peptide is produced by cultured cells during normal metabolism. Nature 359, 322-325.
10. Shoji M, Golde TE, Ghiso J, Cheung TT, Estus S, Shaffer LM, Cai X, McKay DM, Tintner R, Frangione B, Younkin SG (1992) Production of the Alzheimer amyloid β-protein by normal proteolytic processing. Science 258, 126-129.
11. Musa A, Lehrach H, Russo VA (2001) Distinct expression patterns of two zebrafish homologues of the human APP gene during embryonic development. Dev Genes Evol 211, 563-567.
12. Joshi P, Liang JO, Dimonte K, Sullivan J, Pimplikar SW (2009) Amyloid precursor protein is required for convergentextension movements during Zebrafish development. Dev Biol 335, 1-11.
13. Leimer U, Lun K, Romig H, Walter J, Grunberg J, Brand M, Haass C (1999) Zebrafish (Danio rerio) presenilin promotes aberrant amyloid β-peptide production and requires a critical aspartate residue for its function in amyloidogenesis. Biochem 38, 13602-13609.
14. Citron M, Westaway D, Xia W, Carlson G, Diehl T, Levesque G, Johnson-Wood K, Lee M, Seubert P, Davis A, Kholodenka D, Motter R, Sherrington R, Perry B,Yao H, Strome R, Lieberburg I, Rommens J, Kim S, Schenk D, Fraser P, St George- Hyslop P, Selkoe DJ (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid β-protein in both transfected cells and transgenic mice. Nat Med 3, 67-72.
15. Xia W, Zhang J, Kholodenko D, Citron M, Podlisny MB, Teplow DB, Haass C, Seubert P, Koo EH, Selkoe DJ (1997) Enhanced production and oligomerization of the 42-residue amyloid beta-protein by Chinese hamster ovary cells stably expressing mutant presenilins. J Biol Chem 272, 7977-7982.
16. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS, Kimberly WT, Selkoe DJ (1999) Two transmembrane aspartates in presenilin- 1 required for presenilin endoproteolysis and γ-secretase activity. Nature 398, 513-517.
17. Groth C, Nornes S, McCarty R, Tamme R, Lardelli M (2002) Identification of a second presenilin gene in zebrafish with similarity to the human Alzheimer's disease gene presenilin2. Dev Genes Evol 212, 486-490.
18. Roses AD (2006) On the discovery of the genetic association of Apolipoprotein E genotypes and common late-onset Alzheimer disease. J Alzheimers Dis 9, 361-366.
19. Babin PJ, Thisse C, Durliat M, Andre M, Akimenko MA, Thisse B (1997) Both apolipoprotein E and A-I genes are present in a nonmammalian vertebrate and are highly ex pressed during embryonic development. Proc Natl Acad Sci U S A 94, 8622-8627.
20. Yu G, Nishimura M, Arawaka S, Levitan D, Zhang L, Tandon A, Song YQ, Rogaeva E, Chen F, Kawarai T, Supala A, Levesque L, Yu H, Yang DS, Holmes E, Milman P, Liang Y, Zhang DM, Xu DH, Sato C, Rogaev E, Smith M, Janus C, Zhang Y, Aebersold R, Farrer LS, Sorbi S, Bruni A, Fraser P, St George-Hyslop P (2000) Nicastrin modulates presenilinmediated notch/glp-1 signal transduction and betaAPP processing. Nature 407, 48-54.
21. Chen F, Yu G, Arawaka S, Nishimura M, Kawarai T, Yu H, Tandon A, Supala A, Song Y, Rogaeva E, Milman P, Sato C, Yu C, Janus C, Lee J, Song L, Zhang L, Fraser P, St George- Hyslop P (2001) Nicastrin binds to membrane-tethered Notch. Nat Cell Biol 3, 751-754.
22. Francis R, McGrath G, Zhang J, Ruddy D, Sym M, Apfeld J, Nicoll M, Maxwell M, Hai B, Ellis MC, Parks AL, Xu W, Li J, Gurney M, Myers RL, Himes CS, Hiebsch R, Ruble C, Nye JS, Curtis D (2002) aph-1 and pen-2 are required for Notch pathway signaling, γ-secretase cleavage of βAPP and presenilin protein accumulation. Dev Cell 3, 85-97.
23. Lee S, Shah S, Li H, Yu C, Han W, Yu G (2002) Mammalian APH-1 interacts with presenilin and nicastrin, and is required for intramembrane proteolysis of APP and Notch. J Biol Chem 277, 45013-45019.
24. Siman R, Velji J (2003) Localization of presenilin-nicastrin complexes and gamma-secretase activity to the trans-Golgi network. J Neurochem 84, 1143-1153.
25. Shirotani K, Edbauer D, Capell A SJ, Steiner H, Haass C (2003) gamma -Secretase Activity Is Associated with a Conformational Change of Nicastrin. J Biol Chem 278, 16474-16477.
26. Costa CA, Mattson MP, Ancolio K, Checler F (2003) The C-terminal fragment of presenilin 2 triggers p53-mediated staurosporine-induced apoptosis, a function independent of the presenilinase-derived N-terminal counterpart. J Biol Chem 278, 12064-12069.
27. Li T, Ma G, Cai H, Price DL,Wong PC (2003) Nicastrin is required for assembly of presenilin/gamma-secretase complexes to mediate notch signaling and for processing and trafficking of beta-amyloid precursor protein in mammals. J Neurosci 23, 3272-3277.
28. Crystal AS, Morais VA, Pierson TC, Pijak DS, Carlin D, Lee VM, Doms RW (2003) Membrane topology of gammasecretase component PEN-2. J Biol Chem 278, 20117-20123.
29. Goutte C, Tsunozaki M, Hale VA, Priess JR (2002) APH-1 is a multipass membrane protein essential for the Notch signaling pathway in Caenorhabditis elegans embryos. Proc Natl Acad Sci U S A 99, 775-779.
30. Edbauer D,Winkler E, Regula JT, Pesold B, Steiner H, Haass C (2003) Reconstitution of gamma-secretase activity. Nat Cell Biol 5, 486-488.
31. Baulac S, LaVoie MJ, Kimberly WT, Strahle J, Wolfe MS, Selkoe DJ, Xia W (2003) Functional gamma-secretase complex assembly in Golgi/trans-Golgi network: interactions among presenilin, nicastrin, Aph1, Pen-2, and gammasecretase substrates. Neurobiol Dis 14, 194-204.
32. De Strooper B (2003) Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 38, 9-12.
33. Hu Y, FortiniM(2003) Different cofactor activities in gammasecretase assembly: evidence for a nicastrin-Aph-1 subcomplex. J Cell Biol 161, 685-690.
34. Kimberly W, LaVoie M, Ostaszewski BL YW, Wolfe MS, Selkoe DJ. (2003) Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc Natl Acad Sci U S A 100, 6382-6387.
35. Luo WJ,Wang H, Li H, Kim BS, Shah S, Lee HJ, Thinakaran G, Kim TW, Yu G, Xu H (2003) PEN-2 and APH-1 coordinately regulate proteolytic processing of presenilin 1. J Biol Chem 278, 7850-7854.
36. Takasugi N, Tomita T, Hayashi I, Tsuruoka M, Niimura M, Takahashi Y, Thinakaran G, Iwatsubo T (2003) The role of presenilin cofactors in the gamma-secretase complex. Nature 422, 438-441.
37. Strausberg RL, Feingold EA, Grouse LH, Derge JG, Klausner RD, Collins FS, Wagner L, Shenmen CM, Schuler GD, Altschul SF, Zeeberg B, Buetow KH, Schaefer CF, Bhat NK, Hopkins RF, Jordan H, Moore T, Max SI,Wang J, Hsieh F, Diatchenko L, Marusina K, Farmer AA, Rubin GM, Hong L, Stapleton M, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Brownstein MJ, Usdin TB, Toshiyuki S, Carninci P, Prange C, Raha SS, Loquellano NA, Peters GJ, Abramson RD, Mullahy SJ, Bosak SA, McEwan PJ, McKernan KJ, Malek JA, Gunaratne PH, Richards S, Worley KC, Hale S, Garcia AM, Gay LJ, Hulyk SW, Villalon DK, Muzny DM, Sodergren EJ, Lu X, Gibbs RA, Fahey J, Helton E, Ketteman M, Madan A, Rodrigues S, Sanchez A, Whiting M, Young AC, Shevchenko Y, Bouffard GG, Blakesley RW, hman JW, Green ED, Dickson MC, Rodriguez AC, Grimwood J, Schmutz J, Myers RM, Butterfield YS, Krzywinski MI, Skalska U, Smailus DE, Schnerch A, Schein JE, Jones SJ, Marra MA (2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci U S A 99, 16899-16903.
38. Haffner C, Frauli M, Topp S, Irmler M, Hofmann K, Regula JT, Bally-Cuif L, Haass C (2004) Nicalin and its binding partner Nomo are novel Nodal signaling antagonists. EMBO J 23, 3041-3050.
39. Serneels L, Van Biervliet J, Craessaerts K, Dejaegere T, Horre K, Van Houtvin T, Esselmann H, Paul S, Schafer MK, Berezovska O, Hyman BT, Sprangers B, Sciot R, Moons L, Jucker M, Yang Z, May PC, Karran E, Wiltfang J, D'Hooge R, De Strooper B (2009) gamma-Secretase heterogeneity in the Aph1 subunit: relevance for Alzheimer's disease. Science 324, 639-642.
40. De Strooper B, Annaert W, Cupers P, Saftig P, Craessaerts K, Mumm JS, Schroeter EH, Schrijvers V, Wolfe MS, Ray WJ, Goate A, Kopan R (1999) A presenilin-1-dependent gammasecretase- like protease mediates release of Notch intracellular domain. Nature 398, 518-522.
41. Okochi M, Steiner H, Fukumori A, Tanii H, Tomita T, Tanaka T, Iwatsubo T, Kudo T, Takeda M, Haass C (2002) Presenilins mediate a dual intramembranous gamma-secretase cleavage of Notch-1. EMBO J 21, 5408-5416.
42. Fortini ME (2002) Gamma-secretase-mediated proteolysis in cell-surface-receptor signalling. Nat Rev Mol Cell Biol 3, 673-684.
43. Kopan R, Goate A (2002) Aph-2/Nicastrin: an essential component of gamma-secretase and regulator of Notch signaling and Presenilin localization. Neuron 33, 321-324.
44. Taniguchi Y, Kim SH, Sisodia SS (2003) Presenilin-dependent gamma-secretase processing of deleted in colorectal cancer (DCC). J Biol Chem 278, 30425-30428.
45. Marambaud P, Shioi J, Serban G, Georgakopoulos A, Sarner S, Nagy V, Baki L,Wen P, Efthimiopoulos S, Shao Z,Wisniewski T, Robakis NK (2002) A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J 21, 1948-1956.
46. Marambaud P,Wen PH, Dutt A, Shioi J, Takashima A, Siman R, Robakis NK (2003) A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114, 635-645.
47. Ikeuchi T, Sisodia S (2003) The Notch ligands, Delta1 and Jagged2, are substrates for presenilin-dependent gammasecretase cleavage. J Biol Chem 278, 7751-7754.
48. Lele Z, Folchert A, Concha M, Rauch GJ, Geisler R, Rosa F, Wilson SW, Hammerschmidt M, Bally-Cuif L (2002) parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129, 3281-3294.
49. Lorent K, Yeo SY, Oda T, Chandrasekharappa S, Chitnis A, Matthews RP, Pack M (2004) Inhibition of Jagged-mediated Notch signaling disrupts zebrafish biliary development and generates multi-organ defects compatible with an Alagille syndrome phenocopy. Development 131, 5753-5766.
50. Malicki J, Jo H, Pujic Z (2003) Zebrafish N-cadherin, encoded by the glass onion locus, plays an essential role in retinal patterning. Dev Biol 259, 95-108.
51. Shimizu T,Yabe T, Muraoka O,Yonemura S, Aramaki S, Hatta K, Bae YK, Nojima H, Hibi M (2005) E-cadherin is required for gastrulation cell movements in zebrafish. Mech Dev 122, 747-763.
52. Suli A, Mortimer N, Shepherd I, Chien CB (2006) Netrin/DCC signaling controls contralateral dendrites of octavolateralis efferent neurons. J Neurosci 26, 13328-13337.
53. Campbell WA, Yang HW, Zetterberg H, Baulac S, Sears JA, Liu T,Wong STC, Zhong TP, XiaW(2006) Zebrafish lacking Alzheimer presenilin enhancer 2 (Pen-2) demonstrate excessive p53 dependent apoptosis and neuronal loss. J Neurochem 96, 1423-1440.
54. Geling A, Steiner H,Willem M, Bally-Cuif L, Haass C (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 3, 688-694.
55. Nornes S, NewmanM,Wells S,Verdile G, Martins RN, Lardelli M (2009) Independent and cooperative action of Psen2 with Psen1 in zebrafish embryos. Exp Cell Res 315(16), 2791-2801.
56. Camp E, Lardelli M (2001) Tyrosinase gene expression in zebrafish embryos. Dev Genes Evol 211, 150-153.
57. Thinakaran G, Borchelt DR, Lee MK, Slunt HH, Spitzer L, Kim G, Ratovitsky T, Davenport F, Nordstedt C, Seeger M, Hardy J, Levey AI, Gandy SE, Jenkins NA, Copeland NG, Price DL, Sisodia SS (1996) Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17, 181-190.
58. Nornes S, Newman M, Verdile G, Wells S, Stoick-Cooper CL, Tucker B, Frederich-Sleptsova I, Martins R, Lardelli M (2008) Interference with splicing of Presenilin transcripts has potent dominant negative effects on Presenilin activity. Hum Mol Genet 17, 402-412.
59. Sato N, Sakuma C, Kato H, Milligan CE, Oppenheim RW, Yaginuma H (2002) Bcl-2 rescues motoneurons from early cell death in the cervical spinal cord of the chicken embryo. J Neurobiol 53, 381-390.
60. Muller M, v Weizsacker E, Campos-Ortega JA (1996) Expression domains of a zebrafish homologue of the Drosophila pair-rule gene hairy correspond to primordia of alternating somites. Development 122, 2071-2078.
61. Holley SA, Julich D, Rauch GJ, Geisler R, Nusslein-Volhard C (2002) her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development 129, 1175-1183.
62. Yang T, Arslanova D, Gu Y, Augelli-Szafran C, Xia W(2008) Quantification of gamma-secretase modulation differentiates inhibitor compound selectivity between two substrates Notch and amyloid precursor protein. Mol Brain 1, 15.
63. Bernardos RL, Lentz SI, Wolfe MS, Raymond PA (2005) Notch-Delta signaling is required for spatial patterning and Muller glia differentiation in the zebrafish retina. Dev Biol 278, 381-395.
64. van Eeden FJ, Granato M, Schach U, Brand M, Furutani- Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Warga RM, Allende ML, Weinberg ES, Nusslein-Volhard C (1996) Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123, 153-164. (Pubitemid 27056744)
65. Petit A, Pasini A, Alves Da Costa C, Ayral E, Hernandez JF, Dumanchin-Njock C, Phiel CJ, Marambaud P,Wilk S, Farzan M, Fulcrand P, Martinez J, Andrau D, Checler F (2003) JLK isocoumarin inhibitors: selective gamma-secretase inhibitors that do not interfere with notch pathway in vitro or in vivo. J Neurosci Res 74, 370-377.
66. Jiang YJ, Brand M, Heisenberg CP, Beuchle D, Furutani-Seiki M, Kelsh RN, Warga RM, Granato M, Haffter P, Hammerschmidt M, Kane DA, Mullins MC, Odenthal J, van Eeden FJ, Nusslein-Volhard C (1996) Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123, 205-216. (Pubitemid 27056748)
67. Kawakami Y, Raya A, Raya RM, Rodriguez-Esteban C, Belmonte JC (2005) Retinoic acid signalling links left-right asymmetric patterning and bilaterally symmetric somitogenesis in the zebrafish embryo. Nature 435, 165-171.
68. Bulic B, Pickhardt M, Schmidt B, Mandelkow EM,Waldmann H, Mandelkow E (2009) Development of tau aggregation inhibitors for Alzheimer's disease. Angew Chem Int Ed Engl 48, 1740-1752.
69. Goedert M, Crowther RA, Spillantini MG (1998) Tau mutations cause frontotemporal dementias. Neuron 21, 955-958.
70. Tomasiewicz HG, Flaherty DB, Soria JP, Wood JG (2002) Transgenic zebrafish model of neurodegeneration. J Neuro Res 70, 734-745.
71. Bai Q, Garver JA, Hukriede NA, Burton EA (2007) Generation of a transgenic zebrafish model of Tauopathy using a novel promoter element derived from the zebrafish eno2 gene. Nucleic Acids Res 35, 6501-6516.
72. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA (1989) Multiple isoforms of human microtubuleassociated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519-526.
73. Paquet D, Bhat R, SydowA, MandelkowEM, Berg S, Hellberg S, Falting J, Distel M, Koster RW, Schmid B, Haass C (2009) A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J Clin Invest 119, 1382-1395.
74. Flaherty DB, Soria JP, Tomasiewicz HG, Wood JG (2000) Phosphorylation of human tau protein by microtubuleassociated kinases: GSK3beta and cdk5 are key participants. J Neurosci Res 62, 463-472.
75. Colbert T, Till BJ, Tompa R, Reynolds S, Steine MN, Yeung AT, McCallum CM, Comai L, Henikoff S (2001) Highthroughput screening for induced point mutations. Plant Physiol 126, 480-484.
76. Till BJ, Colbert T, Tompa R, Enns LC, Codomo CA, Johnson JE, Reynolds SH, Henikoff JG, Greene EA, Steine MN, Comai L, Henikoff S (2003) High-Throughput TILLING for Functional Genomics. Methods Mol Biol 236, 205-220.
77. Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA (2008) Targeted gene inactivation in zebrafish using engineered zincfinger nucleases. Nat Biotechnol 26, 695-701.
78. Doyon Y, McCammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, Amora R, Hocking TD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Amacher SL (2008) Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 26, 702-708. (Pubitemid 351809597)
79. Malicki J (2000) Genetic analysis of eye development in zebrafish. Results Probl Cell Differ 31, 257-282.
80. Malicki JJ, Pujic Z, Thisse C, Thisse B, Wei X (2002) Forward and reverse genetic approaches to the analysis of eye development in zebrafish. Vision Res 42, 527-533.
81. Bang PI, Yelick PC, Malicki JJ, Sewell WF (2002) Highthroughput behavioral screening method for detecting auditory response defects in zebrafish. J Neurosci Methods 118, 177-187.
82. Shin JT, Fishman MC (2002) From Zebrafish to human: modular medical models. Annu Rev Genomics Hum Genet 3, 311-340.
83. Chung WG, Sen A, Wang-Buhler JL, Yang YH, Lopez N, Merrill GF, Miranda CL, Hu CH, Buhler DR (2004) cDNAdirected expression of a functional zebrafish CYP1A in yeast. Aquatic Toxicol 70, 111-121.