Deep mRNA Sequencing Analysis to Capture the Transcriptome Landscape of Zebrafish Embryos and Larvae

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Yang, Hongxing ^a   Zhou, Yan ^a   Gu, Jianlei ^a   Xie, Shuying ^a   Xu, Yao ^a   Zhu, Genfeng ^a   Wang, Lei ^a   Huang, Jiyue ^a   Ma, Hong ^a,b   Yao, Jihua ^a  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; BLASTULA; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO SEGMENTATION; GASTRULA; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENOME ANALYSIS; HATCHING; LARVAL STAGE; NONHUMAN; OOCYTE CLEAVAGE; PHARYNGULA; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; ZEBRA FISH;

ANIMALS; BLASTULA; CLEAVAGE STAGE, OVUM; EMBRYONIC DEVELOPMENT; GASTRULA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LARVA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION FACTORS; TRANSCRIPTOME; WNT SIGNALING PATHWAY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84877898313     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064058     Document Type: Article

References (105)

1. Assou S, Boumela I, Haouzi D, Anahory T, Dechaud H, et al. (2011) Dynamic changes in gene expression during human early embryo development: from fundamental aspects to clinical applications. Hum Reprod Update 17: 272-290.
2. Ko MS, (2006) Expression profiling of the mouse early embryo: reflections and perspectives. Dev Dyn 235: 2437-2448.
3. Ko MS, (2001) Embryogenomics: developmental biology meets genomics. Trends Biotechnol 19: 511-518.
4. Smith L, Greenfield A, (2003) DNA microarrays and development. Hum Mol Genet 12 Spec No 1: R1-8.
5. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW, (1995) Serial analysis of gene expression. Science 270: 484-487.
6. Fang H, Yang Y, Li C, Fu S, Yang Z, et al. (2010) Transcriptome analysis of early organogenesis in human embryos. Dev Cell 19: 174-184.
7. Sharov AA, Piao Y, Matoba R, Dudekula DB, Qian Y, et al. (2003) Transcriptome analysis of mouse stem cells and early embryos. PLoS Biol 1: E74.
8. Vermilyea MD, Maneck M, Yoshida N, Blochberger I, Suzuki E, et al. (2011) Transcriptome asymmetry within mouse zygotes but not between early embryonic sister blastomeres. EMBO J 30: 1841-1851.
9. Mathavan S, Lee SG, Mak A, Miller LD, Murthy KR, et al. (2005) Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet 1: 260-276.
10. Lo J, Lee S, Xu M, Liu F, Ruan H, et al. (2003) 15000 unique zebrafish EST clusters and their future use in microarray for profiling gene expression patterns during embryogenesis. Genome Res 13: 455-466.
11. Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, et al. (2011) A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol 9: e1000582.
12. Wang Z, Gerstein M, Snyder M, (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
13. Han X, Wu X, Chung WY, Li T, Nekrutenko A, et al. (2009) Transcriptome of embryonic and neonatal mouse cortex by high-throughput RNA sequencing. Proc Natl Acad Sci U S A 106: 12741-12746.
14. Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, et al. (2009) mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 6: 377-382.
15. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y, (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509-1517.
16. Lieschke GJ, Currie PD, (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8: 353-367.
17. Veldman MB, Lin S, (2008) Zebrafish as a developmental model organism for pediatric research. Pediatr Res 64: 470-476.
18. Feitsma H, Cuppen E, (2008) Zebrafish as a cancer model. Mol Cancer Res 6: 685-694.
19. Hegedus Z, Zakrzewska A, Agoston VC, Ordas A, Racz P, et al. (2009) Deep sequencing of the zebrafish transcriptome response to mycobacterium infection. Mol Immunol 46: 2918-2930.
20. Aanes H, Winata CL, Lin CH, Chen JP, Srinivasan KG, et al. (2011) Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res 21: 1328-1338.
21. Vesterlund L, Jiao H, Unneberg P, Hovatta O, Kere J, (2011) The zebrafish transcriptome during early development. BMC Dev Biol 11: 30.
22. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, et al. (2012) Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22: 577-591.
23. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
24. Kohonen T, (1982) Self-organized formation of topologically correct feature maps. Biol Cybern 43: 59-69.
25. Xiao L, Wang K, Teng Y, Zhang J, (2003) Component plane presentation integrated self-organizing map for microarray data analysis. FEBS Lett 538: 117-124.
26. Harrison MR, Georgiou AS, Spaink HP, Cunliffe VT, (2011) The epigenetic regulator Histone Deacetylase 1 promotes transcription of a core neurogenic programme in zebrafish embryos. BMC Genomics 12: 24.
27. Wang R, Li Z, Wang Y, Gui JF, (2011) An Apo-14 promoter-driven transgenic zebrafish that marks liver organogenesis. PLoS One 6: e22555.
28. Schier AF, Talbot WS, (2005) Molecular genetics of axis formation in zebrafish. Annu Rev Genet 39: 561-613.
29. Wagner DS, Mullins MC, (2002) Modulation of BMP activity in dorsal-ventral pattern formation by the chordin and ogon antagonists. Dev Biol 245: 109-123.
30. Branam AM, Hoffman GG, Pelegri F, Greenspan DS, (2010) Zebrafish chordin-like and chordin are functionally redundant in regulating patterning of the dorsoventral axis. Dev Biol 341: 444-458.
31. Rebagliati MR, Toyama R, Fricke C, Haffter P, Dawid IB, (1998) Zebrafish nodal-related genes are implicated in axial patterning and establishing left-right asymmetry. Dev Biol 199: 261-272.
32. Itoh M, Kudoh T, Dedekian M, Kim CH, Chitnis AB, (2002) A role for iro1 and iro7 in the establishment of an anteroposterior compartment of the ectoderm adjacent to the midbrain-hindbrain boundary. Development 129: 2317-2327.
33. Cau E, Wilson SW, (2003) Ash1a and Neurogenin1 function downstream of Floating head to regulate epiphysial neurogenesis. Development 130: 2455-2466.
34. Weidinger G, Thorpe CJ, Wuennenberg-Stapleton K, Ngai J, Moon RT, (2005) The Sp1-related transcription factors sp5 and sp5-like act downstream of Wnt/beta-catenin signaling in mesoderm and neuroectoderm patterning. Curr Biol 15: 489-500.
35. Pezeron G, Anselme I, Laplante M, Ellingsen S, Becker TS, et al. (2006) Duplicate sfrp1 genes in zebrafish: sfrp1a is dynamically expressed in the developing central nervous system, gut and lateral line. Gene Expr Patterns 6: 835-842.
36. Norton WH, Mangoli M, Lele Z, Pogoda HM, Diamond B, et al. (2005) Monorail/Foxa2 regulates floorplate differentiation and specification of oligodendrocytes, serotonergic raphe neurones and cranial motoneurones. Development 132: 645-658.
37. Rinner O, Makhankov YV, Biehlmaier O, Neuhauss SC, (2005) Knockdown of cone-specific kinase GRK7 in larval zebrafish leads to impaired cone response recovery and delayed dark adaptation. Neuron 47: 231-242.
38. Renninger SL, Gesemann M, Neuhauss SC, (2011) Cone arrestin confers cone vision of high temporal resolution in zebrafish larvae. Eur J Neurosci 33: 658-667.
39. Stearns G, Evangelista M, Fadool JM, Brockerhoff SE, (2007) A mutation in the cone-specific pde6 gene causes rapid cone photoreceptor degeneration in zebrafish. J Neurosci 27: 13866-13874.
40. Weinstein JA, Jiang N, White RA, 3rd, Fisher DS, Quake SR (2009) High-throughput sequencing of the zebrafish antibody repertoire. Science 324: 807-810.
41. Pollard KM, Hultman P, Toomey CB, Cauvi DM, Kono DH, (2011) b2-microglobulin is required for the full expression of xenobiotic-induced systemic autoimmunity. J Immunotoxicol 8: 228-237.
42. Liu G, Zheng W, Chen X, (2007) Molecular cloning of proteasome activator PA28-beta subunit of large yellow croaker (Pseudosciana crocea) and its coordinated up-regulation with MHC class I alpha-chain and beta 2-microglobulin in poly I:C-treated fish. Mol Immunol 44: 1190-1197.
43. Bei JX, Suetake H, Araki K, Kikuchi K, Yoshiura Y, et al. (2006) Two interleukin (IL)-15 homologues in fish from two distinct origins. Mol Immunol 43: 860-869.
44. Becknell B, Caligiuri MA, (2005) Interleukin-2, interleukin-15, and their roles in human natural killer cells. Adv Immunol 86: 209-239.
45. Zhang HM, Chen H, Liu W, Liu H, Gong J, et al. (2012) AnimalTFDB: a comprehensive animal transcription factor database. Nucleic Acids Res 40: D144-149.
46. Bogdanovic O, Veenstra GJ, (2009) DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 118: 549-565.
47. Fournier A, Sasai N, Nakao M, Defossez PA (2011) The role of methyl-binding proteins in chromatin organization and epigenome maintenance. Brief Funct Genomics.
48. Le Guezennec X, Vermeulen M, Brinkman AB, Hoeijmakers WA, Cohen A, et al. (2006) MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol Cell Biol 26: 843-851.
49. Guy J, Cheval H, Selfridge J, Bird A, (2011) The role of MeCP2 in the brain. Annu Rev Cell Dev Biol 27: 631-652.
50. Ichimura T, Watanabe S, Sakamoto Y, Aoto T, Fujita N, et al. (2005) Transcriptional repression and heterochromatin formation by MBD1 and MCAF/AM family proteins. J Biol Chem 280: 13928-13935.
51. Ceol CJ, Houvras Y, Jane-Valbuena J, Bilodeau S, Orlando DA, et al. (2011) The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 471: 513-517.
52. Pearson JC, Lemons D, McGinnis W, (2005) Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6: 893-904.
53. Zhong YF, Holland PW, (2011) HomeoDB2: functional expansion of a comparative homeobox gene database for evolutionary developmental biology. Evol Dev 13: 567-568.
54. Kinkel MD, Eames SC, Alonzo MR, Prince VE, (2008) Cdx4 is required in the endoderm to localize the pancreas and limit beta-cell number. Development 135: 919-929.
55. Bellipanni G, Murakami T, Weinberg ES, (2010) Molecular dissection of Otx1 functional domains in the zebrafish embryo. J Cell Physiol 222: 286-293.
56. Scholpp S, Foucher I, Staudt N, Peukert D, Lumsden A, et al. (2007) Otx1l, Otx2 and Irx1b establish and position the ZLI in the diencephalon. Development 134: 3167-3176.
57. Shen YC, Raymond PA, (2004) Zebrafish cone-rod (crx) homeobox gene promotes retinogenesis. Dev Biol 269: 237-251.
58. Gamse JT, Shen YC, Thisse C, Thisse B, Raymond PA, et al. (2002) Otx5 regulates genes that show circadian expression in the zebrafish pineal complex. Nat Genet 30: 117-121.
59. Pillay LM, Forrester AM, Erickson T, Berman JN, Waskiewicz AJ, (2010) The Hox cofactors Meis1 and Pbx act upstream of gata1 to regulate primitive hematopoiesis. Dev Biol 340: 306-317.
60. Angotzi AR, Mungpakdee S, Stefansson S, Male R, Chourrout D, (2011) Involvement of Prop1 homeobox gene in the early development of fish pituitary gland. Gen Comp Endocrinol 171: 332-340.
61. Cheesman SE, Eisen JS, (2004) gsh1 demarcates hypothalamus and intermediate spinal cord in zebrafish. Gene Expr Patterns 5: 107-112.
62. Stros M, Launholt D, Grasser KD, (2007) The HMG-box: a versatile protein domain occurring in a wide variety of DNA-binding proteins. Cell Mol Life Sci 64: 2590-2606.
63. Moleri S, Cappellano G, Gaudenzi G, Cermenati S, Cotelli F, et al. (2011) The HMGB protein gene family in zebrafish: Evolution and embryonic expression patterns. Gene Expr Patterns 11: 3-11.
64. Wang H, Zhu S, Zhou R, Li W, Sama AE, (2008) Therapeutic potential of HMGB1-targeting agents in sepsis. Expert Rev Mol Med 10: e32.
65. Hock R, Furusawa T, Ueda T, Bustin M, (2007) HMG chromosomal proteins in development and disease. Trends Cell Biol 17: 72-79.
66. Bowles J, Schepers G, Koopman P, (2000) Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227: 239-255.
67. Argenton F, Giudici S, Deflorian G, Cimbro S, Cotelli F, et al. (2004) Ectopic expression and knockdown of a zebrafish sox21 reveal its role as a transcriptional repressor in early development. Mech Dev 121: 131-142.
68. Guth S, Wegner M, (2008) Having it both ways: Sox protein function between conservation and innovation. Cell Mol Life Sci 65: 3000-3018.
69. Croce JC, McClay DR, (2008) Evolution of the Wnt pathways. Methods Mol Biol 469: 3-18.
70. van Amerongen R, Nusse R, (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
71. Klaus A, Birchmeier W, (2008) Wnt signalling and its impact on development and cancer. Nat Rev Cancer 8: 387-398.
72. Maiese K, Li F, Chong ZZ, Shang YC, (2008) The Wnt signaling pathway: aging gracefully as a protectionist? Pharmacol Ther 118: 58-81.
73. Grigoryan T, Wend P, Klaus A, Birchmeier W, (2008) Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev 22: 2308-2341.
74. Jin J, Morse M, Frey C, Petko J, Levenson R, (2010) Expression of GPR177 (Wntless/Evi/Sprinter), a highly conserved Wnt-transport protein, in rat tissues, zebrafish embryos, and cultured human cells. Dev Dyn 239: 2426-2434.
75. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, et al. (2000) Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405: 76-81.
76. Pandur P, Lasche M, Eisenberg LM, Kuhl M, (2002) Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418: 636-641.
77. Marlow F, Topczewski J, Sepich D, Solnica-Krezel L, (2002) Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr Biol 12: 876-884.
78. Elizalde C, Campa VM, Caro M, Schlangen K, María Aransay A, et al. (2011) Distinct Roles for Wnt-4 and Wnt-11 During Retinoic Acid-Induced Neuronal Differentiation. Stem Cells 29: 141-153.
79. Cha SW, Tadjuidje E, Tao Q, Wylie C, Heasman J, (2008) Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. Development 135: 3719-3729.
80. Lu FI, Thisse C, Thisse B, (2011) Identification and mechanism of regulation of the zebrafish dorsal determinant. Proc Natl Acad Sci U S A 108: 15876-15880.
81. Garriock RJ, D'Agostino SL, Pilcher KC, Krieg PA, (2005) Wnt11-R, a protein closely related to mammalian Wnt11, is required for heart morphogenesis in Xenopus. Dev Biol 279: 179-192.
82. Matsui T, Raya A, Kawakami Y, Callol-Massot C, Capdevila J, et al. (2005) Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev 19: 164-175.
83. Kikuchi A, Yamamoto H, Sato A, (2009) Selective activation mechanisms of Wnt signaling pathways. Trends Cell Biol 19: 119-129.
84. Sisson BE, Topczewski J, (2009) Expression of five frizzleds during zebrafish craniofacial development. Gene Expr Patterns 9: 520-527.
85. Witzel S, Zimyanin V, Carreira-Barbosa F, Tada M, Heisenberg CP, (2006) Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane. J Cell Biol 175: 791-802.
86. Kim HS, Shin J, Kim SH, Chun HS, Kim JD, et al. (2007) Eye field requires the function of Sfrp1 as a Wnt antagonist. Neurosci Lett 414: 26-29.
87. Uysal-Onganer P, Kypta RM, (2012) Wnt11 in 2011- the regulation and function of a non-canonical Wnt. Acta Physiol (Oxf) 204: 52-64.
88. Gardiner MR, Daggett DF, Zon LI, Perkins AC, (2005) Zebrafish KLF4 is essential for anterior mesendoderm/pre-polster differentiation and hatching. Dev Dyn 234: 992-996.
89. Gardiner MR, Gongora MM, Grimmond SM, Perkins AC, (2007) A global role for zebrafish klf4 in embryonic erythropoiesis. Mech Dev 124: 762-774.
90. Moroy T, Geisen C, (2004) Cyclin E. Int J Biochem Cell Biol. 36: 1424-1439.
91. Zhang Y, Sheets MD, (2009) Analyses of zebrafish and Xenopus oocyte maturation reveal conserved and diverged features of translational regulation of maternal cyclin B1 mRNA. BMC Dev Biol 9: 7.
92. Yarden A, Geiger B, (1996) Zebrafish cyclin E regulation during early embryogenesis. Dev Dyn 206: 1-11.
93. Duffy KT, McAleer MF, Davidson WR, Kari L, Kari C, et al. (2005) Coordinate control of cell cycle regulatory genes in zebrafish development tested by cyclin D1 knockdown with morpholino phosphorodiamidates and hydroxyprolyl-phosphono peptide nucleic acids. Nucleic Acids Res 33: 4914-4921.
94. Zhao L, Samuels T, Winckler S, Korgaonkar C, Tompkins V, et al. (2003) Cyclin G1 has growth inhibitory activity linked to the ARF-Mdm2-p53 and pRb tumor suppressor pathways. Mol Cancer Res 1: 195-206.
95. Horne MC, Goolsby GL, Donaldson KL, Tran D, Neubauer M, et al. (1996) Cyclin G1 and cyclin G2 comprise a new family of cyclins with contrasting tissue-specific and cell cycle-regulated expression. J Biol Chem 271: 6050-6061.
96. Seo HR, Lee DH, Lee HJ, Baek M, Bae S, et al. (2006) Cyclin G1 overcomes radiation-induced G2 arrest and increases cell death through transcriptional activation of cyclin B1. Cell Death Differ 13: 1475-1484.
97. Prykhozhij SV, (2010) In the absence of Sonic hedgehog, p53 induces apoptosis and inhibits retinal cell proliferation, cell-cycle exit and differentiation in zebrafish. PLoS One 5: e13549.
98. Lee KC, Goh WL, Xu M, Kua N, Lunny D, et al. (2008) Detection of the p53 response in zebrafish embryos using new monoclonal antibodies. Oncogene 27: 629-640.
99. Nakamura T, Sanokawa R, Sasaki YF, Ayusawa D, Oishi M, et al. (1995) Cyclin I: a new cyclin encoded by a gene isolated from human brain. Exp Cell Res 221: 534-542.
100. Tsang WY, Wang L, Chen Z, Sanchez I, Dynlacht BD, (2007) SCAPER, a novel cyclin A-interacting protein that regulates cell cycle progression. J Cell Biol 178: 621-633.
101. Wilson JM, Bunte RM, Carty AJ, (2009) Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 48: 785-789.
102. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Series B Stat Methodol 57: 12.
103. Alexa A, Rahnenfuhrer J, Lengauer T, (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600-1607.
104. Team RDC (2008) R: A Language and Environment for Statistical Computing.
105. Gregory R. Warnes. Includes R source code and/or documentation contributed by: Ben Bolker (in alphabetical order) LB, Robert Gentleman, Wolfgang Huber Andy Liaw, Thomas Lumley, Martin Maechler, Arni Magnusson, Steffen Moeller, Marc Schwartz and Bill Venables (2011) gplots: Various R programming tools for plotting data.