neuronal migration; primary cilium; Cell Movement/physiology; Centrosome; Neurogenesis; Cilia/metabolism; Neurons/metabolism; Cell Movement; Cilia; Neurons; Biochemistry, Genetics and Molecular Biology (all); General Medicine
Abstract :
[en] The primary cilium (PC) is a microtubule-based tiny sensory organelle emanating from the centrosome and protruding from the surface of most eukaryotic cells, including neurons. The extremely severe phenotypes of ciliopathies have suggested their paramount importance for multiple developmental events, including brain formation. Neuronal migration is an essential step of neural development, with all neurons traveling from their site of birth to their site of integration. Neurons perform a unique type of cellular migration called cyclic saltatory migration, where their soma periodically jumps along with the stereotyped movement of their centrosome. We will review here how the role of the PC on cell motility was first described in non-neuronal cells as a guide pointing to the direction of migration. We will see then how these findings are extended to neuronal migration. In neurons, the PC appears to regulate the rhythm of cyclic saltatory neuronal migration in multiple systems. Finally, we will review recent findings starting to elucidate how extracellular cues sensed by the PC could be intracellularly transduced to regulate the machinery of neuronal migration. The PC of migrating neurons was unexpectedly discovered to display a rhythmic extracellular emergence during each cycle of migration, with this transient exposure to the external environment associated with periodic transduction of cyclic adenosine monophosphate (cAMP) signaling at the centrosome. The PC in migrating neurons thus uniquely appears as a beat maker, regulating the tempo of cyclic saltatory migration.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Stoufflet, Julie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Caillé, Isabelle ; Inserm U1130, Institut de Biologie Paris Seine (IBPS), Neuroscience Paris Seine (NPS), Sorbonne University, CNRS UMR8246, 75005 Paris, France ; University of Paris Cité, 75020 Paris, France
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Bibliography
Nachury M.V. Mick D.U. Establishing and Regulating the Composition of Cilia for Signal Transduction Nat. Rev. Mol. Cell Biol. 2019 20 389 405 10.1038/s41580-019-0116-4 30948801
Wei Q. Xu Q. Zhang Y. Li Y. Zhang Q. Hu Z. Harris P.C. Torres V.E. Ling K. Hu J. Transition Fibre Protein FBF1 Is Required for the Ciliary Entry of Assembled Intraflagellar Transport Complexes Nat. Commun. 2013 4 2750 10.1038/ncomms3750
Ecker A. Flimmerbewegung Im Gehörorgan von Petromyzon Marinus Arch. Anat. Physiol. Wiss. Med. 1844 520 521
Sorokin S. Centrioles and the Formation of Rudimentary Cilia by Fibroblasts and Smooth Muscle Cells J. Cell Biol. 1962 15 363 377 10.1083/jcb.15.2.363 13978319
Sorokin S.P. Reconstructions of Centrile Formation and Ciliogenesis in Mammalian Lungs J. Cell Sci. 1968 3 207 230 10.1242/jcs.3.2.207 5661997
Guemez-Gamboa A. Coufal N.G. Gleeson J.G. Primary Cilia in the Developing and Mature Brain Neuron 2014 82 511 521 10.1016/j.neuron.2014.04.024 24811376
Pazour G.J. Witman G.B. The Vertebrate Primary Cilium Is a Sensory Organelle Curr. Opin. Cell Biol. 2003 15 105 110 10.1016/S0955-0674(02)00012-1
Sattar S. Gleeson J.G. The Ciliopathies in Neuronal Development: A Clinical Approach to Investigation of Joubert Syndrome and Joubert Syndrome-Related Disorders: Review Dev. Med. Child Neurol. 2011 53 793 798 10.1111/j.1469-8749.2011.04021.x
Liu S. Trupiano M.X. Simon J. Guo J. Anton E.S. The Essential Role of Primary Cilia in Cerebral Cortical Development and Disorders Current Topics in Developmental Biology Elsevier Amsterdam, The Netherlands 2021 Volume 142 99 146 978-0-12-815281-2
Guo J. Higginbotham H. Li J. Nichols J. Hirt J. Ghukasyan V. Anton E.S. Developmental Disruptions Underlying Brain Abnormalities in Ciliopathies Nat. Commun. 2015 6 7857 10.1038/ncomms8857
Higginbotham H. Eom T.-Y. Mariani L.E. Bachleda A. Hirt J. Gukassyan V. Cusack C.L. Lai C. Caspary T. Anton E.S. Arl13b in Primary Cilia Regulates the Migration and Placement of Interneurons in the Developing Cerebral Cortex Dev. Cell 2012 23 925 938 10.1016/j.devcel.2012.09.019
Baudoin J.-P. Viou L. Launay P.-S. Luccardini C. Espeso Gil S. Kiyasova V. Irinopoulou T. Alvarez C. Rio J.-P. Boudier T. et al. Tangentially Migrating Neurons Assemble a Primary Cilium That Promotes Their Reorientation to the Cortical Plate Neuron 2012 76 1108 1122 10.1016/j.neuron.2012.10.027 23259947
Matsumoto M. Sawada M. García-González D. Herranz-Pérez V. Ogino T. Bang Nguyen H. Quynh Thai T. Narita K. Kumamoto N. Ugawa S. et al. Dynamic Changes in Ultrastructure of the Primary Cilium in Migrating Neuroblasts in the Postnatal Brain J. Neurosci. 2019 39 9967 9988 10.1523/JNEUROSCI.1503-19.2019 31685650
Stoufflet J. Chaulet M. Doulazmi M. Fouquet C. Dubacq C. Métin C. Schneider-Maunoury S. Trembleau A. Vincent P. Caille I. Primary Cilium-Dependent CAMP/PKA Signaling at the Centrosome Regulates Neuronal Migration Sci. Adv. 2020 6 eaba3992 10.1126/sciadv.aba3992 32917588
Anvarian Z. Mykytyn K. Mukhopadhyay S. Pedersen L.B. Christensen S.T. Cellular Signalling by Primary Cilia in Development, Organ Function and Disease Nat. Rev. Nephrol. 2019 15 199 219 10.1038/s41581-019-0116-9
Ferreira R. Fukui H. Chow R. Vilfan A. Vermot J. The Cilium as a Force Sensor−myth versus Reality J. Cell Sci. 2019 132 jcs213496 10.1242/jcs.213496
Wheway G. Nazlamova L. Hancock J.T. Signaling through the Primary Cilium Front. Cell Dev. Biol. 2018 6 8 10.3389/fcell.2018.00008
Mykytyn K. Askwith C. G-Protein-Coupled Receptor Signaling in Cilia Cold Spring Harb. Perspect. Biol. 2017 9 a028183 10.1101/cshperspect.a028183
Nauli S.M. Pala R. Kleene S.J. Calcium Channels in Primary Cilia Curr. Opin. Nephrol. Hypertens. 2016 25 452 458 10.1097/MNH.0000000000000251
Jiang J.Y. Falcone J.L. Curci S. Hofer A.M. Direct Visualization of CAMP Signaling in Primary Cilia Reveals Up-Regulation of Ciliary GPCR Activity Following Hedgehog Activation Proc. Natl. Acad. Sci. USA 2019 116 12066 12071 10.1073/pnas.1819730116
Sherpa R.T. Mohieldin A.M. Pala R. Wachten D. Ostrom R.S. Nauli S.M. Sensory Primary Cilium Is a Responsive CAMP Microdomain in Renal Epithelia Sci. Rep. 2019 9 6523 10.1038/s41598-019-43002-2
Moore B.S. Stepanchick A.N. Tewson P.H. Hartle C.M. Zhang J. Quinn A.M. Hughes T.E. Mirshahi T. Cilia Have High CAMP Levels That Are Inhibited by Sonic Hedgehog-Regulated Calcium Dynamics Proc. Natl. Acad. Sci. USA 2016 113 13069 13074 10.1073/pnas.1602393113 27799542
Lee K.L. Guevarra M.D. Nguyen A.M. Chua M.C. Wang Y. Jacobs C.R. The Primary Cilium Functions as a Mechanical and Calcium Signaling Nexus Cilia 2015 4 7 10.1186/s13630-015-0016-y 26029358
Albrecht-Buehler G. Phagokinetic Tracks of 3T3 Cells: Parallels between the Orientation of Track Segments and of Cellular Structures Which Contain Actin or Tubulin Cell 1977 12 333 339 10.1016/0092-8674(77)90109-X
Katsumoto T. Higaki K. Ohno K. Onodera K. The Orientation of Primary Cilia during the Wound Response in 3Y1 Cells Biol. Cell 1994 81 17 21 10.1016/0248-4900(94)90050-7
McGowan S.E. McCoy D.M. Platelet-Derived Growth Factor-A and Sonic Hedgehog Signaling Direct Lung Fibroblast Precursors during Alveolar Septal Formation Am. J. Physiol. Lung Cell. Mol. Physiol. 2013 305 L229 L239 10.1152/ajplung.00011.2013
Lu C.J. Du H. Wu J. Jansen D.A. Jordan K.L. Xu N. Sieck G.C. Qian Q. Non-Random Distribution and Sensory Functions of Primary Cilia in Vascular Smooth Muscle Cells Kidney Blood Press Res. 2008 31 171 184 10.1159/000132462
Clement D.L. Mally S. Stock C. Lethan M. Satir P. Schwab A. Pedersen S.F. Christensen S.T. PDGFRα Signaling in the Primary Cilium Regulates NHE1-Dependent Fibroblast Migration via Coordinated Differential Activity of MEK1/2-ERK1/2-P90RSK and AKT Signaling Pathways J. Cell Sci. 2012 126 953 965 10.1242/jcs.116426
Schneider L. Clement C.A. Teilmann S.C. Pazour G.J. Hoffmann E.K. Satir P. Christensen S.T. PDGFRαα Signaling Is Regulated through the Primary Cilium in Fibroblasts Curr. Biol. 2005 15 1861 1866 10.1016/j.cub.2005.09.012
Schneider L. Cammer M. Lehman J. Nielsen S. Guerra C. Veland I. Stock C. Hoffmann E. Yoder B. Schwab A. et al. Directional Cell Migration and Chemotaxis in Wound Healing Response to PDGF-AA Are Coordinated by the Primary Cilium in Fibroblasts Cell Physiol. Biochem. 2010 25 279 292 10.1159/000276562
Schneider L. Stock C.-M. Dieterich P. Jensen B.H. Pedersen L.B. Satir P. Schwab A. Christensen S.T. Pedersen S.F. The Na+/H+ Exchanger NHE1 Is Required for Directional Migration Stimulated via PDGFR-α in the Primary Cilium J. Cell Biol. 2009 185 163 176 10.1083/jcb.200806019
Jones T.J. Adapala R.K. Geldenhuys W.J. Bursley C. AbouAlaiwi W.A. Nauli S.M. Thodeti C.K. Primary Cilia Regulates the Directional Migration and Barrier Integrity of Endothelial Cells through the Modulation of Hsp27 Dependent Actin Cytoskeletal Organization J. Cell. Physiol. 2012 227 70 76 10.1002/jcp.22704 21837772
Blitzer A.L. Panagis L. Gusella G.L. Danias J. Mlodzik M. Iomini C. Primary Cilia Dynamics Instruct Tissue Patterning and Repair of Corneal Endothelium Proc. Natl. Acad. Sci. USA 2011 108 2819 2824 10.1073/pnas.1016702108 21285373
Labour M.-N. Riffault M. Christensen S.T. Hoey D.A. TGFβ1—Induced Recruitment of Human Bone Mesenchymal Stem Cells Is Mediated by the Primary Cilium in a SMAD3-Dependent Manner Sci. Rep. 2016 6 35542 10.1038/srep35542 27748449
Lee M.N. Song J.H. Oh S.-H. Tham N.T. Kim J.-W. Yang J.-W. Kim E.-S. Koh J.-T. The Primary Cilium Directs Osteopontin-Induced Migration of Mesenchymal Stem Cells by Regulating CD44 Signaling and Cdc42 Activation Stem Cell Res. 2020 45 101799 10.1016/j.scr.2020.101799 32339903
Romero D.M. Bahi-Buisson N. Francis F. Genetics and Mechanisms Leading to Human Cortical Malformations Semin. Cell Dev. Biol. 2018 76 33 75 10.1016/j.semcdb.2017.09.031 28951247
Bellion A. Baudoin J.-P. Alvarez C. Bornens M. Métin C. 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. 2005 25 5691 5699 10.1523/JNEUROSCI.1030-05.2005
Schaar B.T. McConnell S.K. Cytoskeletal Coordination during Neuronal Migration Proc. Natl. Acad. Sci. USA 2005 102 13652 13657 10.1073/pnas.0506008102
Adams M. Simms R.J. Abdelhamed Z. Dawe H.R. Szymanska K. Logan C.V. Wheway G. Pitt E. Gull K. Knowles M.A. et al. A Meckelin–Filamin A Interaction Mediates Ciliogenesis Hum. Mol. Genet. 2012 21 1272 1286 10.1093/hmg/ddr557
Juric-Sekhar G. Adkins J. Doherty D. Hevner R.F. Joubert Syndrome: Brain and Spinal Cord Malformations in Genotyped Cases and Implications for Neurodevelopmental Functions of Primary Cilia Acta Neuropathol. 2012 123 695 709 10.1007/s00401-012-0951-2
Poretti A. Huisman T.A.G.M. Scheer I. Boltshauser E. Joubert Syndrome and Related Disorders: Spectrum of Neuroimaging Findings in 75 Patients AJNR Am. J. Neuroradiol. 2011 32 1459 1463 10.3174/ajnr.A2517
Vilboux T. Malicdan M.C.V. Roney J.C. Cullinane A.R. Stephen J. Yildirimli D. Bryant J. Fischer R. Vemulapalli M. Mullikin J.C. et al. CELSR2, Encoding a Planar Cell Polarity Protein, Is a Putative Gene in Joubert Syndrome with Cortical Heterotopia, Microophthalmia, and Growth Hormone Deficiency Am. J. Med. Genet. 2017 173 661 666 10.1002/ajmg.a.38005 28052552
Rakic P. Specification of Cerebral Cortical Areas Science 1988 241 170 176 10.1126/science.3291116 3291116
Anderson S.A. Eisenstat D.D. Shi L. Rubenstein J.L.R. Interneuron Migration from Basal Forebrain to Neocortex: Dependence on Dlx Genes Science 1997 278 474 476 10.1126/science.278.5337.474 9334308
Caspary T. Larkins C.E. Anderson K.V. The Graded Response to Sonic Hedgehog Depends on Cilia Architecture Dev. Cell 2007 12 767 778 10.1016/j.devcel.2007.03.004 17488627
Altman J. Autoradiographic and Histological Studies of Postnatal Neurogenesis. III. Dating the Time of Production and Onset of Differentiation of Cerebellar Microneurons in Rats J. Comp. Neurol. 1969 136 269 293 10.1002/cne.901360303
Lois C. Alvarez-BuyIIa A. Long-Distance Neuronal Migration in the Adult Mammalian Brain Science 1994 264 5 10.1126/science.8178174
Peretto P. Giachino C. Aimar P. Fasolo A. Bonfanti L. Chain Formation and Glial Tube Assembly in the Shift from Neonatal to Adult Subventricular Zone of the Rodent Forebrain J. Comp. Neurol. 2005 487 407 427 10.1002/cne.20576
Bozoyan L. Khlghatyan J. Saghatelyan A. Astrocytes Control the Development of the Migration-Promoting Vasculature Scaffold in the Postnatal Brain via VEGF Signaling J. Neurosci. 2012 32 1687 1704 10.1523/JNEUROSCI.5531-11.2012
Wichterle H. García-Verdugo J.M. Alvarez-Buylla A. Direct Evidence for Homotypic, Glia-Independent Neuronal Migration Neuron 1997 18 779 791 10.1016/S0896-6273(00)80317-7
Arellano J.I. Guadiana S.M. Breunig J.J. Rakic P. Sarkisian M.R. Development and Distribution of Neuronal Cilia in Mouse Neocortex J. Comp. Neurol. 2012 520 848 873 10.1002/cne.22793 22020803
Higginbotham H.R. Gleeson J.G. The Centrosome in Neuronal Development Trends Neurosci. 2007 30 276 283 10.1016/j.tins.2007.04.001 17420058
Pruski M. Rajnicek A. Yang Z. Clancy H. Ding Y.-Q. McCaig C.D. Lang B. The Ciliary GTPase Arl13b Regulates Cell Migration and Cell Cycle Progression Cell Adhes. Migr. 2016 10 393 405 10.1080/19336918.2016.1159380 26963749
Park S.M. Lim J.S. Ramakrishina S. Kim S.H. Kim W.K. Lee J. Kang H.-C. Reiter J.F. Kim D.S. Kim H. et al. Brain Somatic Mutations in MTOR Disrupt Neuronal Ciliogenesis, Leading to Focal Cortical Dyslamination Neuron 2018 99 83 97.e7 10.1016/j.neuron.2018.05.039
Tobin J.L. Di Franco M. Eichers E. May-Simera H. Garcia M. Yan J. Quinlan R. Justice M.J. Hennekam R.C. Briscoe J. et al. Inhibition of Neural Crest Migration Underlies Craniofacial Dysmorphology and Hirschsprung’s Disease in Bardet-Biedl Syndrome Proc. Natl. Acad. Sci. USA 2008 105 6714 6719 10.1073/pnas.0707057105
Trivedi N. Ramahi J.S. Karakaya M. Howell D. Kerekes R.A. Solecki D.J. Leading-Process Actomyosin Coordinates Organelle Positioning and Adhesion Receptor Dynamics in Radially Migrating Cerebellar Granule Neurons Neural Dev. 2014 9 26 10.1186/1749-8104-9-26
Saade M. Gonzalez-Gobartt E. Escalona R. Usieto S. Martí E. Shh-Mediated Centrosomal Recruitment of PKA Promotes Symmetric Proliferative Neuroepithelial Cell Division Nat. Cell Biol. 2017 19 493 503 10.1038/ncb3512
Pruski M. Hu L. Yang C. Wang Y. Zhang J.-B. Zhang L. Huang Y. Rajnicek A.M. St Clair D. McCaig C.D. et al. Roles for IFT172 and Primary Cilia in Cell Migration, Cell Division, and Neocortex Development Front. Cell Dev. Biol. 2019 7 287 10.3389/fcell.2019.00287
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