Skip to main content
SpringerLink
Log in

The Golgi Apparatus in Polarized Neuroepithelial Stem Cells and Their Progeny: Canonical and Noncanonical Features

  • Chapter
  • First Online:
Book cover The Golgi Apparatus and Centriole

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 67))

Abstract

Neurons forming the central nervous system are generated by neural stem and progenitor cells, via a process called neurogenesis (Götz and Huttner, Nat Rev Mol Cell Biol, 6:777–788, 2005). In this book chapter, we focus on neurogenesis in the dorsolateral telencephalon, the rostral-most region of the neural tube, which contains the part of the central nervous system that is most expanded in mammals (Borrell and Reillo, Dev Neurobiol, 72:955–971, 2012; Wilsch-Bräuninger et al., Curr Opin Neurobiol 39:122–132, 2016). We will discuss recent advances in the dissection of the cell biological mechanisms of neurogenesis, with particular attention to the organization and function of the Golgi apparatus and its relationship to the centrosome.

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

Access this chapter

Log in via an institution
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

  • Axelsson MA, Warren G (2004) Rapid, endoplasmic reticulum-independent diffusion of the mitotic Golgi haze. Mol Biol Cell 15:1843–1852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayala I, Colanzi A (2017) Mitotic inheritance of the Golgi complex and its role in cell division. Biol Cell 109:364–374

    Article  PubMed  Google Scholar 

  • Ayala R, Shu T, Tsai LH (2007) Trekking across the brain: the journey of neuronal migration. Cell 128:29–43

    Article  CAS  PubMed  Google Scholar 

  • Bacallao R, Antony C, Dotti C, Karsenti E, Stelzer EHK, Simons K (1989) The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J Cell Biol 109:2817–2832

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bond J, Woods CG (2005) Cytoskeletal genes regulating brain size. Curr Opin Cell Biol 18:95–101

    Article  PubMed  Google Scholar 

  • Bond J, Roberts E, Mochida GH, Hampshire DJ, Scott S et al (2002) ASPM is a major determinant of cerebral cortical size. Nat Genet 32:316–320

    Article  CAS  PubMed  Google Scholar 

  • Bond J, Roberts E, Springell K, Lizarraga S, Scott S et al (2005) A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37:353–355

    Article  CAS  PubMed  Google Scholar 

  • Borrell V, Reillo I (2012) Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev Neurobiol 72:955–971

    Article  PubMed  Google Scholar 

  • Bradke F, Dotti CG (1998) Membrane traffic in polarized neurons. Biochim Biophys Acta 1404:245–258

    Article  CAS  PubMed  Google Scholar 

  • Bradke F, Dotti CG (2000) Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr Opin Neurobiol 10:574–581

    Article  CAS  PubMed  Google Scholar 

  • Cooper JA (2014) Molecules and mechanisms that regulate multipolar migration in the intermediate zone. Front Cell Neurosci 8:386

    PubMed  PubMed Central  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  Google Scholar 

  • Di Cunto F, Calautti E, Hsiao J, Ong L, Topley G et al (1998) Citron rho-interacting kinase, a novel tissue-specific ser/thr kinase encompassing the Rho-Rac-binding protein Citron. J Biol Chem 273:29706–29711

    Article  PubMed  Google Scholar 

  • Di Cunto F, Imarisio S, Hirsch E, Broccoli V, Bulfone A et al (2000) Defective neurogenesis in citron kinase knockout mice by altered cytokinesis and massive apoptosis. Neuron 28:115–127

    Article  PubMed  Google Scholar 

  • Evans AJ, Gurung S, Wilkinson KA, Stephens DJ, Henley JM (2017) Assembly, secretory pathway trafficking, and surface delivery of kainate receptors is regulated by neuronal activity. Cell Rep 19:2613–2626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farkas LM, Haffner C, Giger T, Khaitovich P, Nowick K et al (2008) Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex. Neuron 60:40–55

    Article  CAS  PubMed  Google Scholar 

  • Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D et al (2010) OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 13:690–699

    Article  CAS  PubMed  Google Scholar 

  • Freeze HH, Eklund EA, Ng BG, Patterson MC (2015) Neurological aspects of human glycosylation disorders. Annu Rev Neurosci 38:105–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gai M, Di Cunto F (2017) Citron kinase in spindle orientation and primary microcephaly. Cell Cycle 16:245–246

    Article  CAS  PubMed  Google Scholar 

  • Gai M, Camera P, Dema A, Bianchi F, Berto G et al (2011) Citron kinase controls abscission through RhoA and anillin. Mol Biol Cell 22:3768–3778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gärtner A, Fornasiero EF, Munck S, Vennekens K, Seuntjens E et al (2012) N-cadherin specifies first asymmetry in developing neurons. EMBO J 31:1893–1903

    Article  PubMed  PubMed Central  Google Scholar 

  • Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777–788

    Article  PubMed  Google Scholar 

  • Grieve AG, Rabouille C (2011) Golgi bypass: skirting around the heart of classical secretion. Cold Spring Harb Perspect Biol 3:a005298

    Article  PubMed  PubMed Central  Google Scholar 

  • Guet D et al (2014) Mechanical role of actin dynamics in the rheology of the Golgi complex and in Golgi-associated trafficking events. Curr Biol 24(15):P1700–P1711. https://doi.org/10.1016/j.cub.2014.06.048

    Article  CAS  PubMed  Google Scholar 

  • Hansen DV, Lui JH, Parker PR, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–561

    Article  CAS  PubMed  Google Scholar 

  • Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511–539

    Article  CAS  PubMed  Google Scholar 

  • Horton AC, Ehlers MD (2003) Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci 23:6188–6199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48:757–771

    Article  CAS  PubMed  Google Scholar 

  • Huang W, She L, Chang XY, Yang RR, Wang L et al (2014) Protein kinase LKB1 regulates polarized dendrite formation of adult hippocampal newborn neurons. Proc Natl Acad Sci USA 111:469–474

    Article  CAS  PubMed  Google Scholar 

  • Hurtado L, Caballero C, Gavilan MP, Cardenas J, Bornens M, Rios RM (2011) Disconnecting the Golgi ribbon from the centrosome prevents directional cell migration and ciliogenesis. J Cell Biol 193:917–933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huttner WB, Dotti CG (1991) Exocytotic and endocytotic membrane traffic in neurons. Curr Opin Neurobiol 1:388–392

    Article  CAS  PubMed  Google Scholar 

  • Kosodo Y, Röper K, Haubensak W, Marzesco A-M, Corbeil D, Huttner WB (2004) Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J 23:2314–2324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levine TP, Misteli T, Rabouille C, Warren G (1995) Mitotic disassembly and reassembly of the Golgi apparatus. Cold Spring Harb Symp Quant Biol 60:549–557

    Article  CAS  PubMed  Google Scholar 

  • Li H, Saucedo-Cuevas L, Regla-Nava JA, Chai G, Sheets N et al (2016a) Zika virus infects neural progenitors in the adult mouse brain and alters proliferation. Cell Stem Cell 19:593–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Saucedo-Cuevas L, Shresta S, Gleeson JG (2016b) The neurobiology of Zika virus. Neuron 92:949–958

    Article  CAS  PubMed  Google Scholar 

  • Li H, Saucedo-Cuevas L, Yuan L, Ross D, Johansen A et al (2019) Zika virus protease cleavage of host protein septin-2 mediates mitotic defects in neural progenitors. Neuron 101(6):1089–1098.e4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marin O, Valiente M, Ge X, Tsai LH (2010) Guiding neuronal cell migrations. Cold Spring Harb Perspect Biol 2:a001834

    Article  PubMed  PubMed Central  Google Scholar 

  • Marthiens V, Rujano MA, Pennetier C, Tessier S, Paul-Gilloteaux P, Basto R (2013) Centrosome amplification causes microcephaly. Nat Cell Biol 15:731–40

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Cerdeno V, Noctor SC, Kriegstein AR (2006) The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex 16(Suppl 1):i152–i161

    Article  PubMed  Google Scholar 

  • Martinez-Martinez MA, Ciceri G, Espinos A, Fernandez V, Marin O, Borrell V (2018) Extensive branching of radially-migrating neurons in the mammalian cerebral cortex. J Comp Neurol 527(10):1558–1576

    Article  Google Scholar 

  • Matsuki T, Matthews RT, Cooper JA, van der Brug MP, Cookson MR et al (2010) Reelin and stk25 have opposing roles in neuronal polarization and dendritic Golgi deployment. Cell 143:826–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao S, Chen R, Ye J, Tan GH, Li S et al (2013) The Angelman syndrome protein Ube3a is required for polarized dendrite morphogenesis in pyramidal neurons. J Neurosci 33:327–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naim V, Imarisio S, Di Cunto F, Gatti M, Bonaccorsi S (2004) Drosophila citron kinase is required for the final steps of cytokinesis. Mol Biol Cell 15:5053–5063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136–144

    Article  CAS  PubMed  Google Scholar 

  • Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2007a) Contribution of intermediate progenitor cells to cortical histogenesis. Arch Neurol 64:639–642

    Article  PubMed  Google Scholar 

  • Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2007b) Neural stem and progenitor cells in cortical development. Novartis Found Symp 288: 59–73; discussion 73–78, 96–98

    Google Scholar 

  • Norden C, Young S, Link BA, Harris WA (2009) Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138:1195–1208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Dell RS, Ustine CJ, Cameron DA, Lawless SM, Williams RM et al (2012) Layer 6 cortical neurons require Reelin-Dab1 signaling for cellular orientation, Golgi deployment, and directed neurite growth into the marginal zone. Neural Dev 7:25

    Article  PubMed  PubMed Central  Google Scholar 

  • Ori-McKenney KM, Jan LY, Jan YN (2012) Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76:921–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paridaen JT, Huttner WB (2014) Neurogenesis during development of the vertebrate central nervous system. EMBO Rep 15:351–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paridaen JT, Wilsch-Brauninger M, Huttner WB (2013) Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155:333–344

    Article  CAS  PubMed  Google Scholar 

  • Persico A, Cervigni RI, Barretta ML, Colanzi A (2009) Mitotic inheritance of the Golgi complex. FEBS Lett 583:3857–3862

    Article  CAS  PubMed  Google Scholar 

  • Persico A, Cervigni RI, Barretta ML, Corda D, Colanzi A (2010) Golgi partitioning controls mitotic entry through Aurora-A kinase. Mol Biol Cell 21:3708–3721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quassollo G, Wojnacki J, Salas DA, Gastaldi L, Marzolo MP et al (2015) A RhoA signaling pathway regulates dendritic golgi outpost formation. Curr Biol 25:971–982

    Article  CAS  PubMed  Google Scholar 

  • Reillo I, Borrell V (2012) Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors. Cereb Cortex 22:2039–2054

    Article  PubMed  Google Scholar 

  • Reillo I, de Juan Romero C, Garcia-Cabezas MA, Borrell V (2011) A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 21:1674–1694

    Article  PubMed  Google Scholar 

  • Sarkisian MR, Li W, Di Cunto F, D’Mello SR, LoTurco JJ (2002) Citron-kinase, a protein essential to cytokinesis in neuronal progenitors, is deleted in the flathead mutant rat. J Neurosci 22:RC217

    Article  PubMed  PubMed Central  Google Scholar 

  • Schotman H, Karhinen L, Rabouille C (2008) dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev Cell 14:171–182

    Article  CAS  PubMed  Google Scholar 

  • Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12:37–53

    Article  PubMed  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 

  • Stenzel D, Wilsch-Bräuninger M, Wong FK, Heuer H, Huttner WB (2014) Integrin alphavbeta3 and thyroid hormones promote expansion of progenitors in embryonic neocortex. Development 141:795–806

    Article  CAS  PubMed  Google Scholar 

  • Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M et al (2010) Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704–707

    Article  CAS  PubMed  Google Scholar 

  • Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165:709–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tavano S, Taverna E, Kalebic N, Haffner C, Namba T et al (2018) Insm1 induces neural progenitor delamination in developing neocortex via downregulation of the adherens junction belt-specific protein Plekha7. Neuron 97:1299–1314 e8

    Article  CAS  PubMed  Google Scholar 

  • Taverna E, Huttner WB (2010) Neural progenitor nuclei IN motion. Neuron 67:906–914

    Article  CAS  PubMed  Google Scholar 

  • Taverna E, Haffner C, Pepperkok R, Huttner WB (2012) A new approach to manipulate the fate of single neural stem cells in tissue. Nat Neurosci 15:329–337

    Article  CAS  Google Scholar 

  • Taverna E, Götz M, Huttner WB (2014) The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu Rev Cell Dev Biol 30:465–502

    Article  CAS  PubMed  Google Scholar 

  • Taverna E, Mora-Bermudez F, Strzyz PJ, Florio M, Icha J et al (2016) Non-canonical features of the Golgi apparatus in bipolar epithelial neural stem cells. Sci Rep 6:21206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai LH, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46:383–388

    Article  CAS  PubMed  Google Scholar 

  • Valenzuela JI, Perez F (2015) Diversifying the secretory routes in neurons. Front Neurosci 9:358

    Article  PubMed  PubMed Central  Google Scholar 

  • Valiente M, Marin O (2010) Neuronal migration mechanisms in development and disease. Curr Opin Neurobiol 20:68–78

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461:947–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Tsai JW, Lamonica B, Kriegstein AR (2011) A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 14:555–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilsch-Bräuninger M, Peters J, Paridaen JTML, Huttner WB (2012) Basolateral rather than apical primary cilia on neuroepithelial cells committed to delamination. Development 139:95–105

    Article  PubMed  Google Scholar 

  • Wilsch-Bräuninger M, Florio M, Huttner WB (2016) Neocortex expansion in development and evolution – from cell biology to single genes. Curr Opin Neurobiol 39:122–132

    Article  PubMed  Google Scholar 

  • Xie Z, Hur SK, Zhao L, Abrams CS, Bankaitis VA (2018) A Golgi lipid signaling pathway controls apical Golgi distribution and cell polarity during neurogenesis. Dev Cell 44:725–740 e4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    Elena Taverna

  2. Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany

    Wieland B. Huttner

Authors
  1. Elena Taverna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wieland B. Huttner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Elena Taverna or Wieland B. Huttner .

Editor information

Editors and Affiliations

  1. Department of Surgery, Houston Methodist Hospital, Houston, TX, USA

    Malgorzata Kloc

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

Taverna, E., Huttner, W.B. (2019). The Golgi Apparatus in Polarized Neuroepithelial Stem Cells and Their Progeny: Canonical and Noncanonical Features. 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_15

Download citation

Publish with us

Policies and ethics

Search

Navigation