Neural Development | |
Developmental time rather than local environment regulates the schedule of epithelial polarization in the zebrafish neural rod | |
Jonathan DW Clarke3  Xiaoyun Ren1  Claudio Araya4  Gemma C Girdler2  | |
[1] Invasive Pathogens Laboratory, Institute of Environmental Science and Research, 34 Kenepuru Drive, Porirua, Wellington, New Zealand;MRC-LMB, Francis Crick Avenue, Cambridge Biomedical Campus, Cambridge, CB2 0QH, UK;MRC Centre for Developmental Neurobiology, King’s College London, Guy’s Campus, London, SE1 1UL, UK;Laboratory of Developmental Biology, Institute of Marine Sciences and Limnology, Faculty of Sciences, Universidad Austral de Chile, Campus Isla Teja s/n, Valdivia, 5090000, Chile | |
关键词: Zebrafish; Neural tube; Neuroepithelial polarity; Lumen; Intrinsic program; | |
Others : 806429 DOI : 10.1186/1749-8104-8-5 |
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received in 2012-12-14, accepted in 2013-03-01, 发布年份 2013 | |
【 摘 要 】
Background
Morphogenesis requires developmental processes to occur both at the right time and in the right place. During neural tube formation in the zebrafish embryo, the generation of the apical specializations of the lumen must occur in the center of the neural rod after the neural cells have undergone convergence, invagination and interdigitation across the midline. How this coordination is achieved is uncertain. One possibility is that environmental signaling at the midline of the neural rod controls the schedule of apical polarization. Alternatively, polarization could be regulated by a timing mechanism and then independent morphogenetic processes ensure the cells are in the correct spatial location.
Results
Ectopic transplantation demonstrates the local environment of the neural midline is not required for neural cell polarization. Neural cells can self-organize into epithelial cysts in ectopic locations in the embryo and also in three-dimensional gel cultures. Heterochronic transplants demonstrate that the schedule of polarization and the specialized cell divisions characteristic of the neural rod are more strongly regulated by time than local environmental signals. The cells’ schedule for polarization is set prior to gastrulation, is stable through several rounds of cell division and appears independent of the morphogenetic movements of gastrulation and neurulation.
Conclusions
Time rather than local environment regulates the schedule of epithelial polarization in zebrafish neural rod.
【 授权许可】
2013 Girdler et al.; licensee BioMed Central Ltd.
【 预 览 】
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20140708093242269.pdf | 1632KB | download | |
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Figure 2. | 230KB | Image | download |
Figure 1. | 274KB | Image | download |
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【 参考文献 】
- [1]Pourquie O: Vertebrate segmentation: from cyclic gene networks to scoliosis. Cell 2011, 145:650-663.
- [2]Livesey FJ, Cepko CL: Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2001, 2:109-118.
- [3]Raff M: The mystery of intracellular developmental programmes and timers. Biochem Soc Trans 2006, 34:663-670.
- [4]Isshiki T, Pearson B, Holbrook S, Doe CQ: Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 2001, 106:511-521.
- [5]Howe JA, Newport JW: A developmental timer regulates degradation of cyclin E1 at the midblastula transition during Xenopus embryogenesis. Proc Natl Acad Sci USA 1996, 93:2060-2064.
- [6]Newport J, Kirschner M: A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 1982, 30:675-686.
- [7]Tadros W, Lipshitz HD: The maternal-to-zygotic transition: a play in two acts. Development 2009, 136:3033-3042.
- [8]Hensey C, Gautier J: A developmental timer that regulates apoptosis at the onset of gastrulation. Mech Dev 1997, 69:183-195.
- [9]Moss EG: Heterochronic genes and the nature of developmental time. Curr Biol 2007, 17:R425-434.
- [10]Buckley CE, Ren X, Ward LC, Girdler GC, Araya C, Green MJ, Clark BS, Link BA, Clarke JDW: Mirror-symmetric microtubule assembly and cell interactions drive lumen formation in the zebrafish neural rod. EMBO J 2013, 32:30-44.
- [11]Tawk M, Araya C, Lyons DA, Reugels AM, Girdler GC, Bayley PR, Hyde DR, Tada M, Clarke JD: A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 2007, 446:797-800.
- [12]Ciruna B, Jenny A, Lee D, Mlodzik M, Schier AF: Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 2006, 439:220-224.
- [13]Quesada-Hernandez E, Caneparo L, Schneider S, Winkler S, Liebling M, Fraser SE, Heisenberg CP: Stereotypical cell division orientation controls neural rod midline formation in zebrafish. Curr Biol 2010, 20:1966-1972.
- [14]Zigman M, Trinh le A, Fraser SE, Moens CB: Zebrafish neural tube morphogenesis requires Scribble-dependent oriented cell divisions. Curr Biol 2011, 21:79-86.
- [15]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: Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev Biol 2000, 227:279-293.
- [16]Alexandre P, Reugels AM, Barker D, Blanc E, Clarke JD: Neurons derive from the more apical daughter in asymmetric divisions in the zebrafish neural tube. Nat Neurosci 2010, 13:673-679.
- [17]Kimmel CB, Warga RM, Kane DA: Cell cycles and clonal strings during formation of the zebrafish central nervous system. Development 1994, 120:265-276.
- [18]Geldmacher-Voss B, Reugels AM, Pauls S, Campos-Ortega JA: A 90-degree rotation of the mitotic spindle changes the orientation of mitoses of zebrafish neuroepithelial cells. Development 2003, 130:3767-3780.
- [19]Harris WA, Hartenstein V: Neuronal determination without cell division in Xenopus embryos. Neuron 1991, 6:499-515.
- [20]Lowery LA, Sive H: Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 2005, 132:2057-2067.
- [21]Lyons DA, Pogoda HM, Voas MG, Woods IG, Diamond B, Nix R, Arana N, Jacobs J, Talbot WS: erbb3 and erbb2 are essential for schwann cell migration and myelination in zebrafish. Curr Biol 2005, 15:513-524.
- [22]Yang X, Zou J, Hyde DR, Davidson LA, Wei X: Stepwise maturation of apicobasal polarity of the neuroepithelium is essential for vertebrate neurulation. J Neurosci 2009, 29:11426-11440.
- [23]Lele Z, Folchert A, Concha M, Rauch GJ, Geisler R, Rosa F, Wilson SW, Hammerschmidt M, Bally-Cuif L: Parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 2002, 129:3281-3294.
- [24]O’Brien LE, Zegers MM, Mostov KE: Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol 2002, 3:531-537.
- [25]O’Brien LE, Jou TS, Pollack AL, Zhang Q, Hansen SH, Yurchenco P, Mostov KE: Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat Cell Biol 2001, 3:831-838.
- [26]Tseng Q, Duchemin-Pelletier E, Deshiere A, Balland M, Guillou H, Filhol O, Thery M: Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proc Natl Acad Sci USA 2012, 109:1506-1511.
- [27]Concha ML, Adams RJ: Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis. Development 1998, 125:983-994.
- [28]Dupin I, Camand E, Etienne-Manneville S: Classical cadherins control nucleus and centrosome position and cell polarity. J Cell Biol 2009, 185:779-786.
- [29]Small JV, Kaverina I: Microtubules meet substrate adhesions to arrange cell polarity. Curr Opin Cell Biol 2003, 15:40-47.
- [30]Jia L, Liu F, Hansen SH, Ter Beest MB, Zegers MM: Distinct roles of cadherin-6 and E-cadherin in tubulogenesis and lumen formation. Mol Biol Cell 2011, 22:2031-2041.
- [31]Tepass U, Truong K, Godt D, Ikura M, Peifer M: Cadherins in embryonic and neural morphogenesis. Nat Rev Mol Cell Biol 2000, 1:91-100.
- [32]Brody T, Odenwald WF: Regulation of temporal identities during Drosophila neuroblast lineage development. Curr Opin Cell Biol 2005, 17:672-675.
- [33]Grosskortenhaus R, Pearson BJ, Marusich A, Doe CQ: Regulation of temporal identity transitions in Drosophila neuroblasts. Dev Cell 2005, 8:193-202.
- [34]Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, Pasquinelli AE: Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 2005, 122:553-563.
- [35]Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R: Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 2006, 20:515-524.
- [36]Lee RC, Feinbaum RL, Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
- [37]Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Müller P, Spring J, Srinivasan A, Fishman M, Finnerty J, Corbo J, Levine M, Leahy P, Davidson E, Ruvkun G: Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000, 408:86-89.
- [38]Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G: The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
- [39]Decembrini S, Bressan D, Vignali R, Pitto L, Mariotti S, Rainaldi G, Wang X, Evangelista M, Barsacchi G, Cremisi F: MicroRNAs couple cell fate and developmental timing in retina. Proc Natl Acad Sci USA 2009, 106:21179-21184.
- [40]Cayouette M, Barres BA, Raff M: Importance of intrinsic mechanisms in cell fate decisions in the developing rat retina. Neuron 2003, 40:897-904.
- [41]Kay JN, Link BA, Baier H: Staggered cell-intrinsic timing of ath5 expression underlies the wave of ganglion cell neurogenesis in the zebrafish retina. Development 2005, 132:2573-2585.
- [42]Rapaport DH, Patheal SL, Harris WA: Cellular competence plays a role in photoreceptor differentiation in the developing Xenopus retina. J Neurobiol 2001, 49:129-141.
- [43]Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, Hammond SM, Bartel DP, Schier AF: MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308:833-838.
- [44]Brook FA, Shum AS, Van Straaten HW, Copp AJ: Curvature of the caudal region is responsible for failure of neural tube closure in the curly tail (ct) mouse embryo. Development 1991, 113:671-678.
- [45]Peeters MC, Hekking JW, Shiota K, Drukker J, Van Straaten HW: Differences in axial curvature correlate with species-specific rate of neural tube closure in embryos of chick, rabbit, mouse, rat and human. Anat Embryol (Berl) 1998, 198:185-194.
- [46]Peeters MC, Shum AS, Hekking JW, Copp AJ, van Straaten HW: Relationship between altered axial curvature and neural tube closure in normal and mutant (curly tail) mouse embryos. Anat Embryol (Berl) 1996, 193:123-130.
- [47]van Straaten HW, Hekking JW, Consten C, Copp AJ: Intrinsic and extrinsic factors in the mechanism of neurulation: effect of curvature of the body axis on closure of the posterior neuropore. Development 1993, 117:1163-1172.
- [48]Abdul-Aziz NM, Turmaine M, Greene ND, Copp AJ: EphrinA-EphA receptor interactions in mouse spinal neurulation: implications for neural fold fusion. Int J Dev Biol 2009, 53:559-568.
- [49]Pai YJ, Abdullah NL, Mohd-Zin SW, Mohammed RS, Rolo A, Greene ND, Abdul-Aziz NM, Copp AJ: Epithelial fusion during neural tube morphogenesis. Birth Defects Res A Clin Mol Teratol 2012, 94:817-823.
- [50]Waterman RE: Topographical changes along the neural fold associated with neurulation in the hamster and mouse. Am J Anat 1976, 146:151-171.
- [51]Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF: Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203:253-310.
- [52]Westerfield M: The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press; 2000.
- [53]Deschene ER, Barresi MJ: Tissue targeted embryonic chimeras: zebrafish gastrula cell transplantation. J Vis Exp 2009, 31:1422.
- [54]Kemp HA, Carmany-Rampey A, Moens C: Generating chimeric zebrafish embryos by transplantation. J Vis Exp 2009, 29:1394.