Switch in FGF signalling initiates glial differentiation in the Drosophila eye

被引:104
作者
Franzdottir, Sigridur Rut [1 ]
Engelen, Daniel [1 ]
Yuva-Aydemir, Yeliz [1 ]
Schmidt, Imke [1 ]
Aho, Annukka [1 ]
Klaembt, Christian [1 ]
机构
[1] Univ Munster, Inst Neurobiol, D-48149 Munster, Germany
关键词
RECEPTOR TYROSINE KINASE; CELL MIGRATION; GROWTH-FACTOR; MESSENGER-RNA; RAP1; ACTIVATION; MESODERM; EMBRYO; MORPHOGENESIS; NEUREGULIN-1;
D O I
10.1038/nature08167
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The formation of a complex nervous system requires the intricate interaction of neurons and glial cells. Glial cells generally migrate over long distances before they initiate their differentiation, which leads to wrapping and insulation of axonal processes(1,2). The molecular pathways coordinating the switch from glial migration to glial differentiation are largely unknown(3). Here we demonstrate that, within the Drosophila eye imaginal disc, fibroblast growth factor (FGF) signalling coordinates glial proliferation, migration and subsequent axonal wrapping. Glial differentiation in the Drosophila eye disc requires a succession from glia-glia interaction to glia-neuron interaction(4). The neuronal component of the fly eye develops in the peripheral nervous system within the eye-antennal imaginal disc, whereas glial cells originate from a pool of central-nervous-system-derived progenitors and migrate onto the eye imaginal disc(5-8). Initially, glial-derived Pyramus, an FGF8-like ligand, modulates glial cell number and motility. A switch to neuronally expressed Thisbe, a second FGF8-like ligand, then induces glial differentiation. This switch is accompanied by an alteration in the intracellular signalling pathway through which the FGF receptor channels information into the cell. Our findings reveal how a switch from glia-glia interactions to glia-neuron interactions can trigger formation of glial membrane around axonal trajectories. These results disclose an evolutionarily conserved control mechanism of axonal wrapping(2), indicating that Drosophila might serve as a model to understand glial disorders in humans.
引用
收藏
页码:758 / U106
页数:5
相关论文
共 32 条
[1]   The Rap1 GTPase functions as a regulator of morphogenesis in vivo [J].
Asha, H ;
de Ruiter, ND ;
Wang, MG ;
Hariharan, IK .
EMBO JOURNAL, 1999, 18 (03) :605-615
[2]   Neuregulin-1/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system [J].
Brinkmann, Bastian G. ;
Agarwal, Amit ;
Sereda, Michael W. ;
Garratt, Alistair N. ;
Mueller, Thomas ;
Wende, Hagen ;
Stassart, Ruth M. ;
Nawaz, Schanila ;
Humml, Christian ;
Velanac, Viktorija ;
Radyushkin, Konstantin ;
Goebbels, Sandra ;
Fischer, Tobias M. ;
Franklin, Robin J. ;
Lai, Cary ;
Ehrenreich, Hannelore ;
Birchmeier, Carmen ;
Schwab, Markus H. ;
Nave, Klaus Armin .
NEURON, 2008, 59 (04) :581-595
[3]   No pun intended: future directions in invertebrate glial cell migration studies [J].
Cafferty, Patrick ;
Auld, Vanessa J. .
NEURON GLIA BIOLOGY, 2007, 3 :45-54
[4]   MIGRATION OF GLIA ALONG PHOTORECEPTOR AXONS IN THE DEVELOPING DROSOPHILA EYE [J].
CHOI, KW ;
BENZER, S .
NEURON, 1994, 12 (02) :423-431
[5]   Control of the segmentation process by graded MAPK/ERK activation in the chick embryo [J].
Delfini, MC ;
Dubrulle, J ;
Malapert, P ;
Chal, J ;
Pourquié, O .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (32) :11343-11348
[6]   fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo [J].
Dubrulle, J ;
Pourquié, O .
NATURE, 2004, 427 (6973) :419-422
[7]   The splicing factor crooked neck associates with the RNA-binding protein HOW to control glial cell maturation in Drosophila [J].
Edenfeld, Gundula ;
Volohonsky, Gloria ;
Krukkert, Karin ;
Naffin, Elke ;
Lammel, Uwe ;
Grimm, Alexandra ;
Engelen, Daniel ;
Reuveny, Adriana ;
Volk, Talila ;
Klaembt, Christian .
NEURON, 2006, 52 (06) :969-980
[8]   Heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo [J].
Gisselbrecht, S ;
Skeath, JB ;
Doe, CQ ;
Michelson, AM .
GENES & DEVELOPMENT, 1996, 10 (23) :3003-3017
[9]   FGF8-like1 and FGF8-like2 encode putative ligands of the FGF receptor Htl for mesoderm migration and are required in the Drosophila gastrula [J].
Gryzik, T ;
Müller, HAJ .
CURRENT BIOLOGY, 2004, 14 (08) :659-667
[10]   Temporal control of glial cell migration in the Drosophila eye requires gilgamesh, hedgehog, and eye specification genes [J].
Hummel, T ;
Attix, S ;
Gunning, D ;
Zipursky, SL .
NEURON, 2002, 33 (02) :193-203