Skip to main content

Centriole Positioning: Not Just a Little Dot in the Cell

  • Chapter
  • First Online:
The Golgi Apparatus and Centriole

Abstract

Organelle positioning as many other morphological parameters in a cell is not random. Centriole positioning as centrosomes or ciliary basal bodies is not an exception to this rule in cell biology. Indeed, centriole positioning is a tightly regulated process that occurs during development, and it is critical for many organs to function properly, not just during development but also in the adulthood. In this book chapter, we overview our knowledge on centriole positioning in different and highly specialized animal cells like photoreceptor or ependymal cells. We will also discuss recent advances in the discovery of molecular pathways involved in this process, mostly related to the cytoskeleton and the cell polarity pathways. And finally, we present quantitative methods that have been used to assess centriole positioning in different cell types although mostly in epithelial cells.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdelhamed ZA, Natarajan S, Wheway G, Inglehearn CF, Toomes C, Johnson CA, Jagger DJ (2015) The Meckel-Gruber syndrome protein TMEM67 controls basal body positioning and epithelial branching morphogenesis in mice via the non-canonical Wnt pathway. Dis Model Mech 8:527–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adler PN (2012) The frizzled/stan pathway and planar cell polarity in the Drosophila wing. Curr Top Dev Biol 101:1–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ambuj K, Vidya R, Rao S, Rituraj P (2014) Role of centrosome in regulating immune response. Curr Drug Targets 15:558–563

    Article  CAS  Google Scholar 

  • Angus KL, Griffiths GM (2013) Cell polarisation and the immunological synapse. Curr Opin Cell Biol 25:85–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Axelrod JD (2008) Basal bodies, kinocilia and planar cell polarity. Nat Genet 40:10

    Article  CAS  PubMed  Google Scholar 

  • Baas PW, Lin S (2011) Hooks and comets: the story of microtubule polarity orientation in the neuron. Dev Neurobiol 71:403–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW (2006) Flies without centrioles. Cell 125:1375–1386

    Article  CAS  PubMed  Google Scholar 

  • Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho SA (2011) Centrosomes and cilia in human disease. Trends Genet 27:307–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boisvieux-Ulrich E, Lainé M-C, Sandoz D (1990) Cytochalasin D inhibits basal body migration and ciliary elongation in quail oviduct epithelium. Cell Tissue Res 259:443–454

    Article  CAS  PubMed  Google Scholar 

  • Bond J, Roberts E, Mochida GH, Hampshire DJ, Scott S, Askham JM, Springell K, Mahadevan M, Crow YJ, Markham AF, Walsh CA, Woods CG (2002) ASPM is a major determinant of cerebral cortical size. Nat Genet 32:316–320

    Article  CAS  PubMed  Google Scholar 

  • Bornens M (2012) The centrosome in cells and organisms. Science 335:422–426

    Article  CAS  PubMed  Google Scholar 

  • Borovina A, Superina S, Voskas D, Ciruna B (2010) Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat Cell Biol 12:407

    Article  CAS  PubMed  Google Scholar 

  • Braun DA, Hildebrandt F (2017) Ciliopathies. Cold Spring Harb Perspect Biol 9:a028191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bryant DM, Mostov KE (2008) From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9:887–901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buendia B, Bré MH, Griffiths G, Karsenti E (1990) Cytoskeletal control of centrioles movement during the establishment of polarity in Madin-Darby canine kidney cells. J Cell Biol 110:1123–1135

    Article  CAS  PubMed  Google Scholar 

  • Burute M, Prioux M, Blin G, Truchet S, Letort G, Tseng Q, Bessy T, Lowell S, Young J, Filhol O, Thery M (2017) Polarity reversal by centrosome repositioning primes cell scattering during epithelial-to-mesenchymal transition. Dev Cell 40:168–184

    Article  CAS  PubMed  Google Scholar 

  • Campanale JP, Sun TY, Montell DJ (2017) Development and dynamics of cell polarity at a glance. J Cell Sci 130:1201–1207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvajal-Gonzalez JM, Mulero-Navarro S, Mlodzik M (2016a) Centriole positioning in epithelial cells and its intimate relationship with planar cell polarity. Bioessays 38:1234–1245

    Article  PubMed  PubMed Central  Google Scholar 

  • Carvajal-Gonzalez JM, Roman A-C, Mlodzik M (2016b) Positioning of centrioles is a conserved readout of Frizzled planar cell polarity signalling. Nat Commun 7:11135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conde C, Caceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332

    Article  CAS  PubMed  Google Scholar 

  • Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, Copp AJ, Henderson DJ, Spurr N, Stanier P, Fisher EM, Nolan PM, Steel KP, Brown SDM, Gray IC, Murdoch JN (2003) Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol 13:1129–1133

    Article  CAS  PubMed  Google Scholar 

  • Damkier HH, Brown PD, Praetorius J (2013) Cerebrospinal fluid secretion by the choroid plexus. Physiol Rev 93:1847–1892

    Article  CAS  PubMed  Google Scholar 

  • Dawe HR, Farr H, Gull K (2007a) Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J Cell Sci 120:7

    Article  CAS  PubMed  Google Scholar 

  • Dawe HR, Smith UM, Cullinane AR, Gerrelli D, Cox P, Badano JL, Blair-Reid S, Sriram N, Katsanis N, Attie-Bitach T, Afford SC, Copp AJ, Kelly DA, Gull K, Johnson CA (2007b) The Meckel–Gruber Syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation. Hum Mol Genet 16:173–186

    Article  CAS  PubMed  Google Scholar 

  • de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG (2005) Centrosome localization determines neuronal polarity. Nature 436:704–708

    Article  PubMed  CAS  Google Scholar 

  • Denu RA, Zasadil LM, Kanugh C, Laffin J, Weaver BA, Burkard ME (2016) Centrosome amplification induces high grade features and is prognostic of worse outcomes in breast cancer. BMC Cancer 16:47

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Distel M, Hocking JC, Volkmann K, Koster RW (2010) The centrosome neither persistently leads migration nor determines the site of axonogenesis in migrating neurons in vivo. J Cell Biol 191:875–890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dormoy V, Tormanen K, Sütterlin C (2013) Par6γ is at the mother centriole and controls centrosomal protein composition through a Par6α-dependent pathway. J Cell Sci 126:860–870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elric J, Etienne-Manneville S (2014) Centrosome positioning in polarized cells: common themes and variations. Exp Cell Res 328:240–248

    Article  CAS  PubMed  Google Scholar 

  • Euteneuer U, Schliwa M (1985) Evidence for an involvement of actin in the positioning and motility of centrosomes. J Cell Biol 101:96–103

    Article  CAS  PubMed  Google Scholar 

  • Ezan J, Lasvaux L, Gezer A, Novakovic A, May-Simera H, Belotti E, Lhoumeau A-C, Birnbaumer L, Beer-Hammer S, Borg J-P, Le Bivic A, Nürnberg B, Sans N, Montcouquiol M (2013) Primary cilium migration depends on G-protein signalling control of subapical cytoskeleton. Nat Cell Biol 15(9):1107–1115

    Article  CAS  PubMed  Google Scholar 

  • Feldman JL, Priess JR (2012) A role for the centrosome and PAR-3 in the hand-off of MTOC function during epithelial polarization. Curr Biol 22:575–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fliegauf M, Benzing T, Omran H (2007) When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8:880–893

    Article  CAS  PubMed  Google Scholar 

  • Galli M, Muñoz J, Portegijs V, Boxem M, Grill SW, Heck AJR, van den Heuvel S (2011) aPKC phosphorylates NuMA-related LIN-5 to position the mitotic spindle during asymmetric division. Nat Cell Biol 13:1132

    Article  CAS  PubMed  Google Scholar 

  • Garrido-Jimenez S, Roman A-C, Alvarez-Barrientos A, Carvajal-Gonzalez JM (2018) Centriole planar polarity assessment in Drosophila wings. Development 145:dev169326

    Article  PubMed  CAS  Google Scholar 

  • Gegg M, Böttcher A, Burtscher I, Hasenoeder S, Van Campenhout C, Aichler M, Walch A, Grant SGN, Lickert H (2014) Flattop regulates basal body docking and positioning in mono- and multiciliated cells. eLife 3:e03842

    Article  PubMed Central  CAS  Google Scholar 

  • Glotzer M (2009) The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Biol 10:9–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein B, Macara IG (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13:609–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodman L, Zallocchi M (2017) Integrin alpha8 and Pcdh15 act as a complex to regulate cilia biogenesis in sensory cells. J Cell Sci 130:3698–3712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodrich LV, Strutt D (2011) Principles of planar polarity in animal development. Development 138:1877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML (1999) The immunological synapse: a molecular machine controlling T cell activation. Science 285:221–227

    Article  CAS  PubMed  Google Scholar 

  • Gray RS, Roszko I, Solnica-Krezel L (2011) Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev Cell 21:120–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guernsey DL, Jiang H, Hussin J, Arnold M, Bouyakdan K, Perry S, Babineau-Sturk T, Beis J, Dumas N, Evans SC, Ferguson M, Matsuoka M, Macgillivray C, Nightingale M, Patry L, Rideout AL, Thomas A, Orr A, Hoffmann I, Michaud JL, Awadalla P, Meek DC, Ludman M, Samuels ME (2010) Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4. Am J Hum Genet 87:40–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guirao B, Meunier A, Mortaud S, Aguilar A, Corsi J-M, Strehl L, Hirota Y, Desoeuvre A, Boutin C, Han Y-G, Mirzadeh Z, Cremer H, Montcouquiol M, Sawamoto K, Spassky N (2010) Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat Cell Biol 12:341

    Article  CAS  PubMed  Google Scholar 

  • Hagiwara H, Kano A, Aoki T, Ohwada N, Takata K (2000) Localization of γ–tubulin to the basal foot associated with the basal body extending a cilium. Histochem J 32:669–671

    Article  CAS  PubMed  Google Scholar 

  • Herawati E, Taniguchi D, Kanoh H, Tateishi K, Ishihara S, Tsukita S (2016) Multiciliated cell basal bodies align in stereotypical patterns coordinated by the apical cytoskeleton. J Cell Biol 214:571–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirota Y, Meunier A, Huang S, Shimozawa T, Yamada O, Kida YS, Inoue M, Ito T, Kato H, Sakaguchi M, Sunabori T, Nakaya M-A, Nonaka S, Ogura T, Higuchi H, Okano H, Spassky N, Sawamoto K (2010) Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. Development 137:3037

    Article  CAS  PubMed  Google Scholar 

  • Holland AJ, Cleveland DW (2009) Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 10:478–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iemura K, Kamemura K, Miwa M (2007) Assessment of the centrosome amplification by quantification of gamma-tubulin in Western blotting. Anal Biochem 371:256–258

    Article  CAS  PubMed  Google Scholar 

  • Jayaraman D, Kodani A, Gonzalez DM, Mancias JD, Mochida GH, Vagnoni C, Johnson J, Krogan N, Harper JW, Reiter JF, Yu TW, Bae BI, Walsh CA (2016) Microcephaly proteins Wdr62 and Aspm define a mother centriole complex regulating centriole biogenesis, apical complex, and cell fate. Neuron 92:813–828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenny A, Reynolds-Kenneally J, Das G, Burnett M, Mlodzik M (2005) Diego and Prickle regulate Frizzled planar cell polarity signalling by competing for Dishevelled binding. Nat Cell Biol 7:691

    Article  CAS  PubMed  Google Scholar 

  • Jones C, Chen P (2008) Primary cilia in planar cell polarity regulation of the inner ear. Curr Top Dev Biol 85:197–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khanna H (2015) Photoreceptor sensory cilium: traversing the ciliary gate. Cells 4:674–686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kibar Z, Vogan KJ, Groulx N, Justice MJ, Underhill DA, Gros P (2001) Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat Genet 28:251

    Article  CAS  PubMed  Google Scholar 

  • Kuijpers M, Hoogenraad CC (2011) Centrosomes, microtubules and neuronal development. Mol Cell Neurosci 48:349–358

    Article  CAS  PubMed  Google Scholar 

  • Lemullois M, Boisvieux-Ulrich E, Laine M-C, Chailley B, Sandoz D (1988) Development and functions of the cytoskeleton during ciliogenesis in metazoa. Biol Cell 63:195–208

    Article  CAS  PubMed  Google Scholar 

  • Lepelletier L, de Monvel JB, Buisson J, Desdouets C, Petit C (2013) Auditory hair cell centrioles undergo confined Brownian motion throughout the developmental migration of the kinocilium. Biophys J 105:48–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levine MS, Bakker B, Boeckx B, Moyett J, Lu J, Vitre B, Spierings DC, Lansdorp PM, Cleveland DW, Lambrechts D, Foijer F, Holland AJ (2017) Centrosome amplification is sufficient to promote spontaneous tumorigenesis in mammals. Dev Cell 40(313–322):e315

    Google Scholar 

  • Lim HH, Zhang T, Surana U (2009) Regulation of centrosome separation in yeast and vertebrates: common threads. Trends Cell Biol 19:325–333

    Article  CAS  PubMed  Google Scholar 

  • Lopes CAM, Mesquita M, Cunha AI, Cardoso J, Carapeta S, Laranjeira C, Pinto AE, Pereira-Leal JB, Dias-Pereira A, Bettencourt-Dias M, Chaves P (2018) Centrosome amplification arises before neoplasia and increases upon p53 loss in tumorigenesis. J Cell Biol 217:2353–2363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marshall WF (2001) Centrioles take center stage. Curr Biol 11:R487–R496

    Article  CAS  PubMed  Google Scholar 

  • Marteil G, Guerrero A, Vieira AF, de Almeida BP, Machado P, Mendonca S, Mesquita M, Villarreal B, Fonseca I, Francia ME, Dores K, Martins NP, Jana SC, Tranfield EM, Barbosa-Morais NL, Paredes J, Pellman D, Godinho SA, Bettencourt-Dias M (2018) Over-elongation of centrioles in cancer promotes centriole amplification and chromosome missegregation. Nat Commun 9:1258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • May-Simera HL, Gumerson JD, Gao C, Campos M, Cologna SM, Beyer T, Boldt K, Kaya KD, Patel N, Kretschmer F, Kelley MW, Petralia RS, Davey MG, Li T (2016) Loss of MACF1 abolishes ciliogenesis and disrupts apicobasal polarity establishment in the retina. Cell Rep 17:1399–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mennella V, Agard DA, Huang B, Pelletier L (2014) Amorphous no more: subdiffraction view of the pericentriolar material architecture. Trends Cell Biol 24:188–197

    Article  CAS  PubMed  Google Scholar 

  • Michel V, Goodyear RJ, Weil D, Marcotti W, Perfettini I, Wolfrum U, Kros CJ, Richardson GP, Petit C (2005) Cadherin 23 is a component of the transient lateral links in the developing hair bundles of cochlear sensory cells. Dev Biol 280:281–294

    Article  CAS  PubMed  Google Scholar 

  • Minegishi K, Hashimoto M, Ajima R, Takaoka K, Shinohara K, Ikawa Y, Nishimura H, McMahon AP, Willert K, Okada Y, Sasaki H, Shi D, Fujimori T, Ohtsuka T, Igarashi Y, Yamaguchi TP, Shimono A, Shiratori H, Hamada H (2017) A Wnt5 activity asymmetry and intercellular signaling via PCP proteins polarize node cells for left-right symmetry breaking. Dev Cell 40(439–452):e434

    Google Scholar 

  • Mirzadeh Z, Han YG, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2010) Cilia organize ependymal planar polarity. J Neurosci 30:2600–2610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell B, Jacobs R, Li J, Chien S, Kintner C (2007) A positive feedback mechanism governs the polarity and motion of motile cilia. Nature 447:97

    Article  CAS  PubMed  Google Scholar 

  • Mitchell B, Stubbs JL, Huisman F, Taborek P, Yu C, Kintner C (2009) The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr Biol 19:924–929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monks CRF, Freiberg BA, Kupfer H, Sciaky N, Kupfer A (1998) Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395:82

    Article  CAS  PubMed  Google Scholar 

  • Mostov K, Su T, ter Beest M (2003) Polarized epithelial membrane traffic: conservation and plasticity. Nat Cell Biol 5:287

    Article  CAS  PubMed  Google Scholar 

  • Narita K, Takeda S (2015) Cilia in the choroid plexus: their roles in hydrocephalus and beyond. Front Cell Neurosci 9:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Narita K, Kawate T, Kakinuma N, Takeda S (2010) Multiple primary cilia modulate the fluid transcytosis in choroid plexus epithelium. Traffic 11:287–301

    Article  CAS  PubMed  Google Scholar 

  • Narita K, Kozuka-Hata H, Nonami Y, Ao-Kondo H, Suzuki T, Nakamura H, Yamakawa K, Oyama M, Inoue T, Takeda S (2012) Proteomic analysis of multiple primary cilia reveals a novel mode of ciliary development in mammals. Biol Open 1:815–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nayak GD, Ratnayaka HS, Goodyear RJ, Richardson GP (2007) Development of the hair bundle and mechanotransduction. Int J Dev Biol 51:597–608

    Article  CAS  PubMed  Google Scholar 

  • Nguyen MM, Stone MC, Rolls MM (2011) Microtubules are organized independently of the centrosome in Drosophila neurons. Neural Dev 6:38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park TJ, Haigo SL, Wallingford JB (2006) Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat Genet 38:303

    Article  CAS  PubMed  Google Scholar 

  • Park TJ, Mitchell BJ, Abitua PB, Kintner C, Wallingford JB (2008) Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat Genet 40:871–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pazour GJ, Bloodgood RA (2008) Targeting proteins to the ciliary membrane. Curr Top Dev Biol 85:115–149

    Article  CAS  PubMed  Google Scholar 

  • Pennekamp P, Menchen T, Dworniczak B, Hamada H (2015) Situs inversus and ciliary abnormalities: 20 years later, what is the connection? Cilia 4:1–1

    Article  PubMed  PubMed Central  Google Scholar 

  • Piel M, Meyer P, Khodjakov A, Rieder CL, Bornens M (2000) The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J Cell Biol 149:317–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, Uccelli A, Lanzavecchia A, Engelhardt B, Sallusto F (2009) C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 10:514–523

    Article  CAS  PubMed  Google Scholar 

  • Redzic ZB, Preston JE, Duncan JA, Chodobski A, Szmydynger-Chodobska J (2005) The choroid plexus-cerebrospinal fluid system: from development to aging. Curr Top Dev Biol 71:1–52

    Article  CAS  PubMed  Google Scholar 

  • Reiter JF, Leroux MR (2017) Genes and molecular pathways underpinning ciliopathies. Nat Rev Mol Cell Biol 18:533–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Boulan E, Macara IG (2014) Organization and execution of the epithelial polarity programme. Nat Rev Mol Cell Biol 15:225–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roig-Martinez M, Saavedra-Lopez E, Casanova PV, Cribaro GP, Barcia C (2019) The MTOC/Golgi complex at the T cell immunological synapse. In: Kloc M (ed) The Golgi apparatus and centriole: functions, interactions and role in disease. Springer, Heidelberg

    Google Scholar 

  • Rosenbaum JL, Witman GB (2002) Intraflagellar transport. Nat Rev Mol Cell Biol 3:813–825

    Article  CAS  PubMed  Google Scholar 

  • Sakakibara A, Ando R, Sapir T, Tanaka T (2013) Microtubule dynamics in neuronal morphogenesis. Open Biol 3:130061

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanchez-Huertas C, Freixo F, Viais R, Lacasa C, Soriano E, Luders J (2016) Non-centrosomal nucleation mediated by augmin organizes microtubules in post-mitotic neurons and controls axonal microtubule polarity. Nat Commun 7:12187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satir P, Pedersen LB, Christensen ST (2010) The primary cilium at a glance. J Cell Sci 123:499–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sattler S (2017) The role of the immune system beyond the fight against infection. In: Sattler S, Kennedy-Lydon T (eds) The immunology of cardiovascular homeostasis and pathology. Springer International, Cham, pp 3–14

    Chapter  Google Scholar 

  • Sedmak T, Wolfrum U (2011) Intraflagellar transport proteins in ciliogenesis of photoreceptor cells. Biol Cell 103:449–466

    Article  CAS  PubMed  Google Scholar 

  • Sipe CW, Liu L, Lee J, Grimsley-Myers C, Lu X (2013) Lis1 mediates planar polarity of auditory hair cells through regulation of microtubule organization. Development 140:1785–1795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sir JH, Barr AR, Nicholas AK, Carvalho OP, Khurshid M, Sossick A, Reichelt S, D’Santos C, Woods CG, Gergely F (2011) A primary microcephaly protein complex forms a ring around parental centrioles. Nat Genet 43:1147–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solecki DJ, Trivedi N, Govek EE, Kerekes RA, Gleason SS, Hatten ME (2009) Myosin II motors and F-actin dynamics drive the coordinated movement of the centrosome and soma during CNS glial-guided neuronal migration. Neuron 63:63–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spassky N, Meunier A (2017) The development and functions of multiciliated epithelia. Nat Rev Mol Cell Biol 18:423

    Article  CAS  PubMed  Google Scholar 

  • St Johnston D, Sanson B (2011) Epithelial polarity and morphogenesis. Curr Opin Cell Biol 23:540–546

    Article  CAS  PubMed  Google Scholar 

  • Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M, Hoogenraad CC, Tolic-Norrelykke IM, Bradke F (2010) Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704–707

    Article  CAS  PubMed  Google Scholar 

  • Stinchcombe Jane C, Griffiths Gillian M (2014) Communication, the centrosome and the immunological synapse. Philos Trans R Soc Lond B Biol Sci 369:20130463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM (2006) Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443:462

    Article  CAS  PubMed  Google Scholar 

  • Stinchcombe JC, Salio M, Cerundolo V, Pende D, Arico M, Griffiths GM (2011) Centriole polarisation to the immunological synapse directs secretion from cytolytic cells of both the innate and adaptive immune systems. BMC Biol 9:45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanentzapf G, Tepass U (2003) Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat Cell Biol 5:46–52

    Article  CAS  PubMed  Google Scholar 

  • Tang N, Marshall WF (2012) Centrosome positioning in vertebrate development. J Cell Sci 125:4951–4961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taniguchi K, Maeda R, Ando T, Okumura T, Nakazawa N, Hatori R, Nakamura M, Hozumi S, Fujiwara H, Matsuno K (2011) Chirality in planar cell shape contributes to left-right asymmetric epithelial morphogenesis. Science 333:339–341

    Article  CAS  PubMed  Google Scholar 

  • Teixido-Travesa N, Roig J, Luders J (2012) The where, when and how of microtubule nucleation - one ring to rule them all. J Cell Sci 125:4445–4456

    Article  CAS  PubMed  Google Scholar 

  • Tissir F, Qu Y, Montcouquiol M, Zhou L, Komatsu K, Shi D, Fujimori T, Labeau J, Tyteca D, Courtoy P, Poumay Y, Uemura T, Goffinet AM (2010) Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat Neurosci 13:700–707

    Article  CAS  PubMed  Google Scholar 

  • Tsai JW, Bremner KH, Vallee RB (2007) Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 10:970–979

    Article  CAS  PubMed  Google Scholar 

  • Ueda H, Morphew MK, McIntosh JR, Davis MM (2011) CD4+ T-cell synapses involve multiple distinct stages. Proc Natl Acad Sci USA 108:17099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umeshima H, Hirano T, Kengaku M (2007) Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons. Proc Natl Acad Sci USA 104:16182–16187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaisse C, Reiter JF, Berbari NF (2017) Cilia and obesity. Cold Spring Harb Perspect Biol 9:a028217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vertii A, Doxsey S (2016) The centrosome: a phoenix organelle of the immune response. Single Cell Biol 5:1

    Article  Google Scholar 

  • Volta F, Gerdes JM (2017) The role of primary cilia in obesity and diabetes. Ann N Y Acad Sci 1391:71–84

    Article  PubMed  Google Scholar 

  • Wallingford JB (2010) Planar cell polarity signaling, cilia and polarized ciliary beating. Curr Opin Cell Biol 22:597–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallingford JB (2012) Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu Rev Cell Dev Biol 28:627–653

    Article  CAS  PubMed  Google Scholar 

  • Wallingford JB, Rowning BA, Vogeli KM, Rothbächer U, Fraser SE, Harland RM (2000) Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405:81

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Dynlacht BD (2018) The regulation of cilium assembly and disassembly in development and disease. Development 145:dev151407

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang Y, Naturale VF, Adler PN (2017) Planar cell polarity effector fritz interacts with dishevelled and has multiple functions in regulating PCP. G3 (Bethesda) 7:1323–1337

    Article  CAS  Google Scholar 

  • Webb SW, Grillet N, Andrade LR, Xiong W, Swarthout L, Della Santina CC, Kachar B, Muller U (2011) Regulation of PCDH15 function in mechanosensory hair cells by alternative splicing of the cytoplasmic domain. Development 138:1607–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei Q, Xu Q, Zhang Y, Li Y, Zhang Q, Hu Z, Harris PC, Torres VE, Ling K, Hu J (2013) Transition fibre protein FBF1 is required for the ciliary entry of assembled intraflagellar transport complexes. Nat Commun 4:2750

    Article  PubMed  CAS  Google Scholar 

  • Werner S, Pimenta-Marques A, Bettencourt-Dias M (2017) Maintaining centrosomes and cilia. J Cell Sci 130:3789–3800

    Article  CAS  PubMed  Google Scholar 

  • Yau KW, Schatzle P, Tortosa E, Pages S, Holtmaat A, Kapitein LC, Hoogenraad CC (2016) Dendrites in vitro and in vivo contain microtubules of opposite polarity and axon formation correlates with uniform plus-end-out microtubule orientation. J Neurosci 36:1071–1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ybot-Gonzalez P, Savery D, Gerrelli D, Signore M, Mitchell CE, Faux CH, Greene NDE, Copp AJ (2007) Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134:789–799

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Burakov A, Rodionov V, Mogilner A (2010) Finding the cell center by a balance of dynein and myosin pulling and microtubule pushing: a computational study. Mol Biol Cell 21:4418–4427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zmuda JF, Rivas RJ (1998) The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. Cell Motil Cytoskeleton 41:18–38

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by BFU2014-54699-P and BFU2017-85547-P grants from the Ministry of Economy to J.M. C-G. and GR15164 and GR18116 from Junta de Extremadura to F.C. Á.-C.R. S.G-J. was a recipient of a Fellowship from the Universidad de Extremadura, and S.D-Ch was a recipient of a Fellowship from Junta de Extremadura. All Spanish funding is cosponsored by the European Union FEDER program.

J.M. C-G was a recipient of an “Atraccion y Retencion de talento” contract from the GOBEX (Extremadura government) and was recipient of a Ramón y Cajal contract (RYC-2015-17867).

Competing Financial Interests

The authors declare no competing financial interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jose Maria Carvajal-Gonzalez .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Roman, AC., Garrido-Jimenez, S., Diaz-Chamorro, S., Centeno, F., Carvajal-Gonzalez, J.M. (2019). Centriole Positioning: Not Just a Little Dot in the Cell. In: Kloc, M. (eds) The Golgi Apparatus and Centriole. Results and Problems in Cell Differentiation, vol 67. Springer, Cham. https://doi.org/10.1007/978-3-030-23173-6_8

Download citation

Publish with us

Policies and ethics