RNA profiling of FAC-sorted neurons from the developing zebrafish spinal cord

Developmental Dynamics

Volumn 238, Issue 1, 2009, Pages 150-161

  Cerda, Gustavo A ^a   Hargrave, Murray ^a   Lewis, Katharine E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Affymetrix; CiA; Elav13; Eng1b; FACS; GFP; HuC; Interneuron; Lhx1; Lhx5; Pax2; RNA profile; Tg(elavl3:EGFP); Tg(pax2a:GFP); V1; Zebrafish

Indexed keywords

GREEN FLUORESCENT PROTEIN; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LHX1; TRANSCRIPTION FACTOR LHX5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SELECTION; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; FLUORESCENCE ACTIVATED CELL SORTING; INTERNEURON; MICROARRAY ANALYSIS; NERVE CELL; NONHUMAN; ORGAN; ORGANOGENESIS; PRIORITY JOURNAL; RNA FINGERPRINTING; SPINAL CORD; SPINAL CORD NERVE CELL; TISSUE; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL SEPARATION; GENE EXPRESSION PROFILING; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; NEURONS; RECOMBINANT FUSION PROTEINS; RNA; SPINAL CORD; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; MAMMALIA;

EID: 58149279450     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21818     Document Type: Article

References (68)

1. Abramoff MD, Magelhaes PJ, Ran SJ. 2004. Image processing with ImageJ. Biophotonics Intl 11:36.42.
2. Ahmed H, Du SJ, O'Leary N, Vasta GR. 2004. Biochemical and molecular characterization of galectins from zebrafish (Danio rerio): notochord-specific expression of a prototype galectin during early embryogenesis. Glycobiology 14:219-232.
3. Alvarez FJ, Jonas PC, Sapir T, Hartley R, Berrocal MC, Geiman EJ, Todd AJ, Goulding M. 2005. Postnatal phenotype and localization of spinal cord V1 derived interneurons. J Comp Neurol 493:177-192.
4. Batista M, Lewis KE. 2008. Pax2/8 act redundantly to specify inhibitory fates of multiple spinal interneurons. Dev Biol 323:88-97.
5. Batista M, Jacobstein J, Lewis KE. 2008. Zebrafish V2 cells develop into excitatory CiD and Delta/Notch dependent inhibitory VeLD interneurons. Dev Biol 322:263-275.
6. Bolanos-Jimenez F, Bordais A, Behra M, Strahle U, Sahel J, Rendon A. 2001. Dystrophin and Dp71, two products of the DMD gene, show a different pattern of expression during embryonic development in zebrafish. Mech Dev 102:239-241.
7. Brownlie A, Hersey C, Oates AC, Paw BH, Falick AM, Witkowska HE, Flint J, Higgs D, Jessen J, Bahary N, Zhu H, Lin S, Zon L. 2003. Characterization of embryonic globin genes of the zebrafish. Dev Biol 255:48-61.
8. Burrill JD, Moran L, Goulding MD, Saueressig H. 1997. PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1+ interneurons that require PAX6 for their development. Development 124:4493-4503.
9. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G, Robertson AJ, Perkins AC, Bruce SJ, Lee CC, Ranade SS, Peckham HE, Manning JM, McKernan KJ, Grimmond SM. 2008. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 5:613-619.
10. Coutelle O, Blagden CS, Hampson R, Halai C, Rigby PW, Hughes SM. 2001. Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis. Dev Biol 236:136-150.
11. Covassin L, Amigo JD, Suzuki K, Teplyuk V, Straubhaar J, Lawson ND. 2006. Global analysis of hematopoietic and vascular endothelial gene expression by tissue specific microarray profiling in zebrafish. Dev Biol 299:551-562.
12. Detrich HW, 3rd. 2008. Fluorescent proteins in zebrafish cell and developmental biology. Methods Cell Biol 85:219-241.
13. Devos N, Deflorian G, Biemar F, Bortolussi M, Martial JA, Peers B, Argenton F. 2002. Differential expression of two somatostatin genes during zebrafish embryonic development. Mech Dev 115:133-137.
14. Fan L, Moon J, Wong TT, Crodian J, Collodi P. 2008. Zebrafish primordial germ cell cultures derived from vasa::RFP transgenic embryos. Stem Cells Dev 17:585-597.
15. Finley KR, Davidson AE, Ekker SC. 2001. Three-color imaging using fluorescent proteins in living zebrafish embryos. Biotechniques 31:66-70, 72.
16. Gautier L, Cope L, Bolstad BM, Irizarry RA. 2004. affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307-315.
17. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80.
18. Goulding M, Pfaff SL. 2005. Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr Opin Neurobiol 15:14-20.
19. Grabher C, Joly JS, Wittbrodt J. 2004. Highly efficient zebrafish transgenesis mediated by the meganuclease I-SceI. Methods Cell Biol 77:381-401.
20. Gribble SL, Nikolaus OB, Dorsky RI. 2007. Regulation and function of Dbx genes in the zebrafish spinal cord. Dev Dyn 236:3472-3483.
21. Gross MK, Dottori M, Goulding M. 2002. Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34:535-549.
22. Hatta K, Bremiller R, Westerfield M, Kimmel CB. 1991. Diversity of expression of engrailed-like antigens in zebrafish. Development 112:821-832.
23. Higashijima S. 2008. Transgenic zebrafish expressing fluorescent proteins in central nervous system neurons. Dev Growth Differ 50:407-413.
24. Higashijima S, Okamoto H, Ueno N, Hotta Y, Eguchi G. 1997. High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev Biol 192:289-299.
25. Higashijima S, Masino M, Mandel G, Fetcho JR. 2004. Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J Neurosci 24:5827-5839.
26. Huettner JE, Baughman RW. 1986. Primary culture of identified neurons from the visual cortex of postnatal rats. J Neurosci 6:3044-3060.
27. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
28. Jones LJ, Yue ST, Cheung CY, Singer VL. 1998. RNA quantitation by fluorescence-based solution assay: RiboGreen reagent characterization. Anal Biochem 265:368-374.
29. Kawakami K. 2005. Transposon tools and methods in zebrafish. Dev Dyn 234:244-254.
30. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:253-310.
31. Kimura Y, Okamura Y, Higashijima S. 2006. alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J Neurosci 26:5684-5697.
32. Kimura Y, Satou C, Higashijima S. 2008. V2a and V2b neurons are generated by the final divisions of pair-producing progenitors in the zebrafish spinal cord. Development 135:3001-3005.
33. Koster RW, Fraser SE. 2001. Tracing transgene expression in living zebrafish embryos. Dev Biol 233:329-346.
34. Krauss S, Johansen T, Korzh V, Fjose A. 1991. Expression of the zebrafish paired box gene pax [zf-b] during early neurogenesis. Development 113:1193-1206.
35. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB. 2007. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088-3099.
36. Lewis KE. 2006. How do genes regulate simple behaviours? Understanding how different neurons in the vertebrate spinal cord are genetically specified. Phil Trans R Soc Lond B Biol Sci 361:45-66.
37. Lönnstedt I, Speed T. 2002. Replicated microarray data. Statistica Sinica 12:31-46.
38. Majumdar A, Lun K, Brand M, Drummond IA. 2000. Zebrafish no isthmus reveals a role for pax2.1 in tubule differentiation and patterning events in the pronephric primordia. Development 127:2089-2098.
39. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. 1997. Identification and characterization of the vesicular GABA transporter. Nature 389:870-876.
40. Montaner D, Tarraga J, Huerta-Cepas J, Burguet J, Vaquerizas JM, Conde L, Minguez P, Vera J, Mukherjee S, Valls J, Pujana MA, Alloza E, Herrero J, Al-Shahrour F, Dopazo J. 2006. Next station in microarray data analysis: GEPAS. Nucleic Acids Res 34:W486-491.
41. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621-628.
42. Oishi I, Kawakami Y, Raya A, Callol-Massot C, Izpisua Belmonte JC. 2006. Regulation of primary cilia formation and leftright patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nat Genet 38:1316-1322.
43. Park HC, Kim CH, Bae YK, Yeo SY, Kim SH, Hong SK, Shin J, Yoo KW, Hibi M, Hirano T, Miki N, Chitnis AB, Huh TL. 2000. Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev Biol 227:279-293.
44. Paw BH, Davidson AJ, Zhou Y, Li R, Pratt SJ, Lee C, Trede NS, Brownlie A, Donovan A, Liao EC, Ziai JM, Drejer AH, Guo W, Kim CH, Gwynn B, Peters LL, Chernova MN, Alper SL, Zapata A, Wickramasinghe SN, Lee MJ, Lux SE, Fritz A, Postlethwait JH, Zon LI. 2003. Cell-specific mitotic defect and dyserythropoiesis associated with erythroid band 3 deficiency. Nat Genet 34:59-64.
45. Picker A, Scholpp S, Bohli H, Takeda H, Brand M. 2002. A novel positive transcriptional feedback loop in midbrain-hindbrain boundary development is revealed through analysis of the zebrafish pax2.1 promoter in transgenic lines. Development 129:3227-3239.
46. Pillai A, Mansouri A, Behringer R, Westphal H, Goulding M. 2007. Lhx1 and Lhx5 maintain the inhibitory-neurotransmitter status of interneurons in the dorsal spinal cord. Development 134:357-366.
47. Pyati UJ, Cooper MS, Davidson AJ, Nechiporuk A, Kimelman D. 2006. Sustained Bmp signaling is essential for cloaca development in zebrafish. Development 133:2275-2284.
48. Qu X, Jia H, Garrity DM, Tompkins K, Batts L, Appel B, Zhong TP, Baldwin HS. 2008. Ndrg4 is required for normal myocyte proliferation during early cardiac development in zebrafish. Dev Biol 317:486-496.
49. R_Development_Core_Team. 2005. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
50. Sagne C, El Mestikawy S, Isambert MF, Hamon M, Henry JP, Giros B, Gasnier B. 1997. Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett 417:177-183.
51. Sapir T, Geiman EJ, Wang Z, Velasquez T, Mitsui S, Yoshihara Y, Frank E, Alvarez FJ, Goulding M. 2004. Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development. J Neurosci 24:1255-1264.
52. Saueressig H, Burrill J, Goulding M. 1999. Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126:4201-4212.
53. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T. 2006. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7:3.
54. Shendure J. 2008. The beginning of the end for microarrays? Nat Methods 5:585-587.
55. Sheng HZ, Bertuzzi S, Chiang C, Shawlot W, Taira M, Dawid I, Westphal H. 1997. Expression of murine Lhx5 suggests a role in specifying the forebrain. Dev Dyn 208:266-277.
56. Shihabuddin LS. 2008. Adult rodent spinal cord-derived neural stem cells: isolation and characterization. Methods Mol Biol 438:55-66.
57. 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.
58. Shu X, Huang J, Dong Y, Choi J, Langenbacher A, Chen JN. 2007. Na,K-ATPase alpha2 and Ncx4a regulate zebrafish left-right patterning. Development 134:1921-1930.
59. Smyth GK. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3.
60. Takizawa F, Araki K, Ito K, Moritomo T, Nakanishi T. 2007. Expression analysis of two Eomesodermin homologues in zebrafish lymphoid tissues and cells. Mol Immunol 44:2324-2331.
61. Tamme R, Wells S, Conran JG, Lardelli M. 2002. The identity and distribution of neural cells expressing the mesodermal determinant spadetail. BMC Dev Biol 2:9.
62. Thisse B, Heyer V, Lux A, Alunni V, Degrave A, Seiliez I, Kirchner J, Parkhill JP, Thisse C. 2004. Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol 77:505-519.
63. Toyama R, Curtiss PE, Otani H, Kimura M, Dawid IB, Taira M. 1995. The LIM class homeobox gene lim5: Implied role in CNS patterning in Xenopus and Zebrafish. Dev. Biol. 170:583-593.
64. Toyama R, Dawid I. 1997. lim6, a novel LIM homeobox gene in the zebrafish: comparison of its expression pattern with lim1. Dev Dyn 209:406-417.
65. Villefranc JA, Amigo J, Lawson ND. 2007. Gateway compatible vectors for analysis of gene function in the zebrafish. Dev Dyn 236:3077-3087.
66. Wingert RA, Selleck R, Yu J, Song HD, Chen Z, Song A, Zhou Y, Thisse B, Thisse C, McMahon AP, Davidson AJ. 2007. The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet 3:1922-1938.
67. Zhang XY, Rodaway AR. 2007. SCL-GFP transgenic zebrafish: in vivo imaging of blood and endothelial development and identification of the initial site of definitive hematopoiesis. Dev Biol 307:179-194.
68. Zou J, Beermann F, Wang J, Kawakami K, Wei X. 2006. The Fugu tyrp1 promoter directs specific GFP expression in zebrafish: tools to study the RPE and the neural crest-derived melanophores. Pigment Cell Res 19:615-627.