Protein tyrosine phosphatase receptor type O (Ptpro) regulates cerebellar formation during zebrafish development through modulating Fgf signaling

Cellular and Molecular Life Sciences

Volumn 70, Issue 13, 2013, Pages 2367-2381

  Liao, Wei Hao ^a,b   Cheng, Chia Hsiung ^b   Hung, Kuo Sheng ^c   Chiu, Wen Ta ^c   Chen, Gen Der ^b   Hwang, Pung Pung ^d   Hwang, Sheng Ping L ^d   Kuan, Yung Shu ^b,e,f   Huang, Chang Jen ^a,b,e  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f ACADEMIA SINICA   (Taiwan)

Author keywords

Cerebellum; fgf; fgfr; ptpro; Zebrafish

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DUAL SPECIFICITY PHOSPHATASE 6; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 1A; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN DEVELOPMENT; CELL FATE; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; DEVELOPMENTAL GENE; DUSP6 GENE; EMBRYO; EPHRIN A5B GENE; FOREBRAIN; GENE; GENE EXPRESSION; GENE FUNCTION; GENE ISOLATION; GENE LOCATION; GENETIC TRANSCRIPTION; LARVA; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TYROSINE PHOSPHATASE RECEPTOR TYPE O GENE; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FIBROBLAST GROWTH FACTORS; GENE KNOCKDOWN TECHNIQUES; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 3; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; VERTEBRATA;

EID: 84879083610     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1259-7     Document Type: Article

References (67)

1. Tonks NK (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7:833-846
2. Johnson KG, Van Vactor D (2003) Receptor protein tyrosine phosphatases in nervous system development. Physiol Rev 83:1-24
3. Matozaki T, Murata Y, Mori M, Kotani T, Okazawa H, Ohnishi H (2010) Expression, localization, and biological function of the R3 subtype of receptor-type protein tyrosine phosphatases in mammals. Cell Signal 22:1811-1817
4. Murata Y, Mori M, Kotani T, Supriatna Y, Okazawa H, Kusakari S, Saito Y, Ohnishi H, Matozaki T (2010) Tyrosine phosphorylation of R3 subtype receptor-type protein tyrosine phosphatases and their complex formations with Grb2 or Fyn. Genes cells: Devoted Mol Cell Mech 15:513-524
5. Mori M, Murata Y, Kotani T, Kusakari S, Ohnishi H, Saito Y, Okazawa H, Ishizuka T, Matozaki T (2010) Promotion of cell spreading and migration by vascular endothelial-protein tyrosine phosphatase (VE-PTP) in cooperation with integrins. J Cell Physiol 224:195-204
6. Shintani T, Ihara M, Sakuta H, Takahashi H, Watakabe I, Noda M (2006) Eph receptors are negatively controlled by protein tyrosine phosphatase receptor type O. Nat Neurosci 9:761-769
7. Chen B, Bixby JL (2005) Neuronal pentraxin with chromo domain (NPCD) is a novel class of protein expressed in multiple neuronal domains. J Comp Neurol 481:391-402
8. Kim M, Kim H, Jho EH (2010) Identification of ptpro as a novel target gene of Wnt signaling and its potential role as a receptor for Wnt. FEBS Lett 584:3923-3928
9. Thomas PE, Wharram BL, Goyal M, Wiggins JE, Holzman LB, Wiggins RC (1994) GLEPP1, a renal glomerular epithelial cell (podocyte) membrane protein-tyrosine phosphatase. Identification, molecular cloning, and characterization in rabbit. J Biol Chem 269:19953-19962
10. Wharram BL, Goyal M, Gillespie PJ, Wiggins JE, Kershaw DB, Holzman LB, Dysko RC, Saunders TL, Samuelson LC, Wiggins RC (2000) Altered podocyte structure in GLEPP1 (Ptpro)-deficient mice associated with hypertension and low glomerular filtration rate. J Clin Invest 106(10):1281-1290
11. Jeon M, Nguyen H, Bahri S, Zinn K (2008) Redundancy and compensation in axon guidance: genetic analysis of the Drosophila Ptp10D/Ptp4E receptor tyrosine phosphatase subfamily. Neural Dev 3:3
12. Kurusu M, Zinn K (2008) Receptor tyrosine phosphatases regulate birth order-dependent axonal fasciculation and midline repulsion during development of the Drosophila mushroom body. Mol Cell Neurosci 38:53-65
13. Sun Q, Schindelholz B, Knirr M, Schmid A, Zinn K (2001) Complex genetic interactions among four receptor tyrosine phosphatases regulate axon guidance in Drosophila. Mol Cell Neurosci 17:274-291
14. Chen B, Bixby JL (2005) A novel substrate of receptor tyrosine phosphatase PTPRO is required for nerve growth factor-induced process outgrowth. J Neurosci 25:880-888
15. Gonzalez-Brito MR, Bixby JL (2009) Protein tyrosine phosphatase receptor type O regulates development and function of the sensory nervous system. Mol Cell Neurosci 42:458-465
16. Stepanek L, Stoker AW, Stoeckli E, Bixby JL (2005) Receptor tyrosine phosphatases guide vertebrate motor axons during development. J Neurosci 25:3813-3823
17. van Eekelen M, Overvoorde J, van Rooijen C, den Hertog J (2010) Identification and expression of the family of classical protein-tyrosine phosphatases in zebrafish. PLoS ONE 5:e12573
18. Reifers F, Bohli H, Walsh EC, Crossley PH, Stainier DY, Brand M (1998) Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125:2381-2395
19. Meyers EN, Lewandoski M, Martin GR (1998) An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18:136-141
20. Picker A, Brennan C, Reifers F, Clarke JD, Holder N, Brand M (1999) Requirement for the zebrafish mid-hindbrain boundary in midbrain polarisation, mapping and confinement of the retinotectal projection. Development 126:2967-2978
21. Jaszai J, Reifers F, Picker A, Langenberg T, Brand M (2003) Isthmus-to-midbrain transformation in the absence of midbrain-hindbrain organizer activity. Development 130:6611-6623
22. Basson MA, Echevarria D, Ahn CP, Sudarov A, Joyner AL, Mason IJ, Martinez S, Martin GR (2008) Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development 135:889-898
23. Bottcher RT, Niehrs C (2005) Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26:63-77
24. Thisse B, Thisse C (2005) Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 287:390-402
25. Beltran PJ, Bixby JL, Masters BA (2003) Expression of PTPRO during mouse development suggests involvement in axonogenesis and differentiation of NT-3 and NGF-dependent neurons. J Comp Neurol 456:384-395
26. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA, Ekker SC (2007) p53 activation by knockdown technologies. PLoS Genet 3:e78
27. Wilson SW, Houart C (2004) Early steps in the development of the forebrain. Dev Cell 6:167-181
28. Scholpp S, Wolf O, Brand M, Lumsden A (2006) Hedgehog signalling from the zona limitans intrathalamica orchestrates patterning of the zebrafish diencephalon. Development 133:855-864
29. Inoue A, Takahashi M, Hatta K, Hotta Y, Okamoto H (1994) Developmental regulation of islet-1 mRNA expression during neuronal differentiation in embryonic zebrafish. Dev Dyn 199:1-11
30. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM (1996) Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84:309-320
31. Martin SC, Heinrich G, Sandell JH (1998) Sequence and expression of glutamic acid decarboxylase isoforms in the developing zebrafish. J Comp Neurol 396:253-266
32. Park HC, Mehta A, Richardson JS, Appel B (2002) olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev Biol 248:356-368
33. Borodovsky N, Ponomaryov T, Frenkel S, Levkowitz G (2009) Neural protein Olig2 acts upstream of the transcriptional regulator Sim1 to specify diencephalic dopaminergic neurons. Dev Dyn 238:826-834
34. Marin O, Rubenstein JL (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790
35. Kani S, Bae YK, Shimizu T, Tanabe K, Satou C, Parsons MJ, Scott E, Higashijima S, Hibi M (2010) Proneural gene-linked neurogenesis in zebrafish cerebellum. Dev Biol 343:1-17
36. Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31-43
37. Bae YK, Kani S, Shimizu T, Tanabe K, Nojima H, Kimura Y, Higashijima S, Hibi M (2009) Anatomy of zebrafish cerebellum and screen for mutations affecting its development. Dev Biol 330:406-426
38. Shin J, Park HC, Topczewska JM, Mawdsley DJ, Appel B (2003) Neural cell fate analysis in zebrafish using olig2 BAC transgenics. Methods Cell Sci 25:7-14
39. + neurons in the zebrafish cerebellum. Dev Biol 318:162-171
40. Thisse B, Pflumio S, Fürthauer M, Loppin B, Heyer V, Degrave A, Woehl R, Lux A, Steffan T, Charbonnier XQ, Thisse C (2001) Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission (http://zfin.org)
41. Lun K, Brand M (1998) A series of no isthmus (noi) alleles of the zebrafish pax2.1 gene reveals multiple signaling events in development of the midbrain-hindbrain boundary. Development 125:3049-3062
42. Miyata T, Maeda T, Lee JE (1999) NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev 13:1647-1652
43. Volkmann K, Rieger S, Babaryka A, Koster RW (2008) The zebrafish cerebellar rhombic lip is spatially patterned in producing granule cell populations of different functional compartments. Dev Biol 313:167-180
44. Mason I (2007) Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat Rev Neurosci 8:583-596
45. Shanmugalingam S, Houart C, Picker A, Reifers F, Macdonald R, Barth A, Griffin K, Brand M, Wilson SW (2000) Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development 127:2549-2561
46. Walshe J, Mason I (2003) Unique and combinatorial functions of Fgf3 and Fgf8 during zebrafish forebrain development. Development 130:4337-4349
47. Miyake A, Nakayama Y, Konishi M, Itoh N (2005) Fgf19 regulated by Hh signaling is required for zebrafish forebrain development. Dev Biol 288:259-275
48. Suzuki-Hirano A, Shimogori T (2009) The role of Fgf8 in telencephalic and diencephalic patterning. Semin Cell Dev Biol 20:719-725
49. Sato T, Joyner AL, Nakamura H (2004) How does Fgf signaling from the isthmic organizer induce midbrain and cerebellum development? Dev Growth Differ 46:487-494
50. Chi CL, Martinez S, Wurst W, Martin GR (2003) The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130:2633-2644
51. Furthauer M, Reifers F, Brand M, Thisse B, Thisse C (2001) sprouty4 acts in vivo as a feedback-induced antagonist of FGF signaling in zebrafish. Development 128:2175-2186
52. Roehl H, Nusslein-Volhard C (2001) Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr Biol 11:503-507
53. Molina GA, Watkins SC, Tsang M (2007) Generation of FGF reporter transgenic zebrafish and their utility in chemical screens. BMC Dev Biol 7:62
54. Tsang M, Maegawa S, Kiang A, Habas R, Weinberg E, Dawid IB (2004) A role for MKP3 in axial patterning of the zebrafish embryo. Development 131:2769-2779
55. Furthauer M, Lin W, Ang SL, Thisse B, Thisse C (2002) Sef is a feedback-induced antagonist of Ras/MAPK-mediated FGF signalling. Nat Cell Biol 4:170-174
56. Li C, Scott DA, Hatch E, Tian X, Mansour SL (2007) Dusp6 (Mkp3) is a negative feedback regulator of FGF-stimulated ERK signaling during mouse development. Development 134:167-176
57. Shinya M, Koshida S, Sawada A, Kuroiwa A, Takeda H (2001) Fgf signalling through MAPK cascade is required for development of the subpallial telencephalon in zebrafish embryos. Development 128:4153-4164
58. Trokovic R, Jukkola T, Saarimaki J, Peltopuro P, Naserke T, Weisenhorn DM, Trokovic N, Wurst W, Partanen J (2005) Fgfr1-dependent boundary cells between developing mid- and hindbrain. Dev Biol 278:428-439
59. Trokovic R, Trokovic N, Hernesniemi S, Pirvola U, Vogt Weisenhorn DM, Rossant J, McMahon AP, Wurst W, Partanen J (2003) FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J 22:1811-1823
60. Scholpp S, Groth C, Lohs C, Lardelli M, Brand M (2004) Zebrafish fgfr1 is a member of the fgf8 synexpression group and is required for fgf8 signalling at the midbrain-hindbrain boundary. Dev Genes Evol 214:285-295
61. Kotani T, Murata Y, Ohnishi H, Mori M, Kusakari S, Saito Y, Okazawa H, Bixby JL, Matozaki T (2010) Expression of PTPRO in the interneurons of adult mouse olfactory bulb. J Comp Neurol 518:119-136
62. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, Sommer L, Boussadia O, Kemler R (2001) Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128:1253-1264
63. Westerfield M (2007) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). 5th edn. University of Oregon Press, Eugene
64. Esain V, Postlethwait JH, Charnay P, Ghislain J (2010) FGF-receptor signalling controls neural cell diversity in the zebrafish hindbrain by regulating olig2 and sox9. Development 137:33-42
65. Chou CM, Chen YC, Lee MT, Chen GD, Lu IC, Chen ST, Huang CJ (2006) Expression and characterization of a brain-specific protein kinase BSK146 from zebrafish. Biochem Biophys Res Commun 340:767-775
66. Yang CH, Cheng CH, Chen GD, Liao WH, Chen YC, Huang KY, Hwang PP, Hwang SP, Huang CJ (2011) Zona pellucida domain-containing protein beta-tectorin is crucial for zebrafish proper inner ear development. PLoS ONE 6:e23078
67. Huang KY, Chen GD, Cheng CH, Liao KY, Hung CC, Chang GD, Hwang PP, Lin SY, Tsai MC, Khoo KH, Lee MT, Huang CJ (2011) Phosphorylation of the zebrafish M6Ab at serine 263 contributes to filopodium formation in PC12 cells and neurite outgrowth in zebrafish embryos. PLoS ONE 6:e26461