Abstract
As the primary microtubule-organizing centre of the mammalian cell, the centrosome plays many important roles during cell growth and organization. This is evident across a broad range of cell types and processes, such as the proliferation, differentiation and polarity of neural cells. Additionally, given its localization and function, there are likely to be many more processes that rely on the centrosome that have not yet been characterized. Currently, little is known about centrosomal dynamics during mammalian development. In this study, we have analyzed Nedd1 protein expression to characterize the localization of the centrosome during some aspects of mouse embryogenesis. Using a Nedd1 antibody we have demonstrated the colocalization of Nedd1 with centrosomal markers. We found strong expression of Nedd1, and therefore the centrosome, in highly proliferating cells during neural development. Additionally, Nedd1 was found to have high expression in the cytoplasm of a subset of cells in the dorsal root ganglia. We have also shown a distinct, polarized centrosomal localization of Nedd1 in the developing lens, retina and other polarized tissues. This study reveals the localization of Nedd1 and the centrosome during important processes in mouse embryogenesis and provides a basis for further study into its role in development.
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References
Aaku-Saraste E, Hellwig A, Huttner WB (1996) Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-remodeling of the neuroepithelium prior to neurogenesis. Dev Biol 180:664–679
Akitaya T, Bronner-Fraser M (1992) Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration. Dev Dyn 194:12–20
Bellion A, Baudoin JP, Alvarez C, Bornens M, Metin C (2005) Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J Neurosci 25:5691–5699
Bermingham-McDonogh O, Oesterle EC, Stone JS, Hume CR, Huynh HM, Hayashi T (2006) Expression of Prox1 during mouse cochlear development. J Comp Neurol 496:172–186
Besharse JC, Horst CJ (1990) The photoreceptor connecting cilium. A model for the transition zone. Plenum Press, New York
Bobinnec Y, Khodjakov A, Mir LM, Rieder CL, Edde B, Bornens M (1998) Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J Cell Biol 143:1575–1589
Brazel CY, Romanko MJ, Rothstein RP, Levison SW (2003) Roles of the mammalian subventricular zone in brain development. Prog Neurobiol 69:49–69
Chang B, Khanna H, Hawes N, Jimeno D, He S, Lillo C, Parapuram SK, Cheng H, Scott A, Hurd RE, others (2006) In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet 15:1847–1857
Chenn A, Zhang YA, Chang BT, McConnell SK (1998) Intrinsic polarity of mammalian neuroepithelial cells. Mol Cell Neurosci 11:183–193
Chow RL, Lang RA (2001) Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255–296
Dahm R, Procter JE, Ireland ME, Lo WK, Mogensen MM, Quinlan RA, Prescott AR (2007) Reorganization of centrosomal marker proteins coincides with epithelial cell differentiation in the vertebrate lens. Exp Eye Res 85:696–713
de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG (2005) Centrosome localization determines neuronal polarity. Nature 436:704–708
Donovan SL, Dyer MA (2005) Regulation of proliferation during central nervous system development. Semin Cell Dev Biol 16:407–421
Doxsey S, McCollum D, Theurkauf W (2005) Centrosomes in cellular regulation. Annu Rev Cell Dev Biol
Foster FS, Zhang M, Duckett AS, Cucevic V, Pavlin CJ (2003) In vivo imaging of embryonic development in the mouse eye by ultrasound biomicroscopy. Invest Ophthalmol Vis Sci 44:2361–2366
Fuller SD, Gowen BE, Reinsch S, Sawyer A, Buendia B, Wepf R, Karsenti E (1995) The core of the mammalian centriole contains gamma-tubulin. Curr Biol 5:1384–1393
Gilbert SF (2000) The central nervous system and the epidermis. In: Developmental biology, 6th edn. Sinauer Associates Inc., Sunderland, pp 379–445
Gregory WA, Edmondson JC, Hatten ME, Mason CA (1988) Cytology and neuron-glial apposition of migrating cerebellar granule cells in vitro. J Neurosci 8:1728–1738
Haren L, Remy MH, Bazin I, Callebaut I, Wright M, Merdes A (2006) NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J Cell Biol 172:505–515
Higginbotham HR, Gleeson JG (2007) The centrosome in neuronal development. Trends Neurosci 30:276–283
Kasemeier-Kulesa JC, Kulesa PM, Lefcort F (2005) Imaging neural crest cell dynamics during formation of dorsal root ganglia and sympathetic ganglia. Development 132:235–245
Kaufman M (1992) The atlas of mouse development, revised edn. Academic Press, London
Keating TJ, Peloquin JG, Rodionov VI, Momcilovic D, Borisy GG (1997) Microtubule release from the centrosome. Proc Natl Acad Sci USA 94:5078–5083
Kellogg DR, Moritz M, Alberts BM (1994) The centrosome and cellular organization. Annu Rev Biochem 63:639–674
Koblar SA, Krull CE, Pasquale EB, McLennan R, Peale FD, Cerretti DP, Bothwell M (2000) Spinal motor axons and neural crest cells use different molecular guides for segmental migration through the rostral half-somite. J Neurobiol 42:437–447
Kumar S, Tomooka Y, Noda M (1992) Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem Biophys Res Commun 185:1155–1161
Kumar S, Matsuzaki T, Yoshida Y, Noda M (1994) Molecular cloning and biological activity of a novel developmentally regulated gene encoding a protein with beta-transducin-like structure. J Biol Chem 269:11318–11326
Ligon LA, Karki S, Tokito M, Holzbaur EL (2001) Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat Cell Biol 3:913–917
Luders J, Patel UK, Stearns T (2006) GCP-WD is a gamma-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat Cell Biol 8:137–147
Malicki J, Driever W (1999) oko meduzy mutations affect neuronal patterning in the zebrafish retina and reveal cell–cell interactions of the retinal neuroepithelial sheet. Development 126:1235–1246
Manning J, Kumar S (2007) NEDD1: function in microtubule nucleation, spindle assembly and beyond. Int J Biochem Cell Biol 39:7–11
McKenzie E, Krupin A, Kelley MW (2004) Cellular growth and rearrangement during the development of the mammalian organ of Corti. Dev Dyn 229:802–812
Meads T, Schroer TA (1995) Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil Cytoskeleton 32:273–288
Muresan V, Joshi HC, Besharse JC (1993) Gamma-tubulin in differentiated cell types: localization in the vicinity of basal bodies in retinal photoreceptors and ciliated epithelia. J Cell Sci 104(Pt 4):1229–1237
Musch A (2004) Microtubule organization and function in epithelial cells. Traffic 5:1–9
Nakagawa S, Takeichi M (1998) Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125:2963–2971
Pan J, Snell W (2007) The primary cilium: keeper of the key to cell division. Cell 129:1255–1257
Paoletti A, Moudjou M, Paintrand M, Salisbury JL, Bornens M (1996) Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J Cell Sci 109(Pt 13):3089–3102
Pei YF, Rhodin JA (1970) The prenatal development of the mouse eye. Anat Rec 168:105–125
Piperno G, LeDizet M, Chang XJ (1987) Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J Cell Biol 104:289–302
Rizzolo LJ, Joshi HC (1993) Apical orientation of the microtubule organizing center and associated gamma-tubulin during the polarization of the retinal pigment epithelium in vivo. Dev Biol 157:147–156
Salas PJ, Rodriguez ML, Viciana AL, Vega-Salas DE, Hauri HP (1997) The apical submembrane cytoskeleton participates in the organization of the apical pole in epithelial cells. J Cell Biol 137:359–375
Schoenwolf GC (1984) Histological and ultrastructural studies of secondary neurulation in mouse embryos. Am J Anat 169:361–376
Sloboda RD, Rosenbaum JL (2007) Making sense of cilia and flagella. J Cell Biol 179:575–582
Sluder G (2005) Two-way traffic: centrosomes and the cell cycle. Nat Rev Mol Cell Biol 6:743–748
Srsen V, Merdes A (2006) The centrosome and cell proliferation. Cell Div 1:26
Trainor PA (2005) Specification of neural crest cell formation and migration in mouse embryos. Semin Cell Dev Biol 16:683–693
Tucker JB, Paton CC, Richardson GP, Mogensen MM, Russell IJ (1992) A cell surface-associated centrosomal layer of microtubule-organizing material in the inner pillar cell of the mouse cochlea. J Cell Sci 102(Pt 2):215–226
Yuba-Kubo A, Kubo A, Hata M, Tsukita S (2005) Gene knockout analysis of two gamma-tubulin isoforms in mice. Dev Biol 282:361–373
Zolessi FR, Poggi L, Wilkinson CJ, Chien CB, Harris WA (2006) Polarization and orientation of retinal ganglion cells in vivo. Neural Develop 1:2
Acknowledgments
This work was supported by funds from the IMVS and the Cancer Council of South Australia. JM is supported by an Australian Postgraduate Award. SK is a Senior Principal Research Fellow of the National Health and Medical Research Council. We thank Professor J. L. Salisbury for gift of the centrin antibody Dr. B. Edde for the gift of the GT335 antibody, and Dr. Natasha Harvey for technical advice and providing several of the mouse sections.
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Manning, J.A., Colussi, P.A., Koblar, S.A. et al. Nedd1 expression as a marker of dynamic centrosomal localization during mouse embryonic development. Histochem Cell Biol 129, 751–764 (2008). https://doi.org/10.1007/s00418-008-0392-0
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DOI: https://doi.org/10.1007/s00418-008-0392-0