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PMID: 18786414 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain.

Cell stem cell ·Vol. 3 ·No. 3 ·2008-09-11 ·Pages 265-78

Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A

Abstract

Neural stem cells (NSCs, B1 cells) are retained in the walls of the adult lateral ventricles but, unlike embryonic NSCs, are displaced from the ventricular zone (VZ) into the subventricular zone (SVZ) by ependymal cells. Apical and basal compartments, which in embryonic NSCs play essential roles in self-renewal and differentiation, are not evident in adult NSCs. Here we show that SVZ B1 cells in adult mice extend a minute apical ending to directly contact the ventricle and a long basal process ending on blood vessels. A closer look at the ventricular surface reveals a striking pinwheel organization specific to regions of adult neurogenesis. The pinwheel's core contains the apical endings of B1 cells and in its periphery two types of ependymal cells: multiciliated (E1) and a type (E2) characterized by only two cilia and extraordinarily complex basal bodies. These results reveal that adult NSCs retain fundamental epithelial properties, including apical and basal compartmentalization, significantly reshaping our understanding of this adult neurogenic niche.

MeSH Terms
Adult Stem Cells/cytology,physiology Animals Brain/blood supply,cytology,physiology Embryonic Stem Cells/cytology Humans Lateral Ventricles/cytology,physiology Mice Mice, Inbred Strains Mitosis Neuroglia/cytology
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mirzadeh Zaman
Department of Neurosurgery, University of California, San Francisco, San Francisco, CA 94143, USA.
Merkle Florian T
Soriano-Navarro Mario
Garcia-Verdugo Jose Manuel
Alvarez-Buylla Arturo
References (70)
70 references, click to expand
  1. Reconstructions of centriole formation and ciliogenesis in mammalian lungs.
    J Cell Sci. 1968 Jun;3(2):207-30 PMID: 5661997
  2. New neurons follow the flow of cerebrospinal fluid in the adult brain.
    Science. 2006 Feb 3;311(5761):629-32 PMID: 16410488
  3. Neuroblast proliferation on the surface of the adult rat striatal wall after focal ependymal loss by intracerebroventricular injection of neuraminidase.
    J Comp Neurol. 2008 Apr 1;507(4):1571-87 PMID: 18236450
  4. The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals.
    Brain Res Bull. 2002 Apr;57(6):765-75 PMID: 12031273
  5. Radial glia give rise to adult neural stem cells in the subventricular zone.
    Proc Natl Acad Sci U S A. 2004 Dec 14;101(50):17528-32 PMID: 15574494
  6. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu.
    Stem Cells. 2007 Sep;25(9):2146-57 PMID: 17569787
  7. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors.
    Science. 2002 Jul 19;297(5580):365-9 PMID: 12130776
  8. Neurons derived from radial glial cells establish radial units in neocortex.
    Nature. 2001 Feb 8;409(6821):714-20 PMID: 11217860
  9. Notch regulates cell fate and dendrite morphology of newborn neurons in the postnatal dentate gyrus.
    Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20558-63 PMID: 18077357
  10. Direct isolation of human central nervous system stem cells.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14720-5 PMID: 11121071
  11. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12425-30 PMID: 9356465
  12. Insulin-like growth factor-1 is a radial cell-associated neurotrophin that promotes neuronal recruitment from the adult songbird edpendyma/subependyma.
    J Neurobiol. 1998 Jul;36(1):1-15 PMID: 9658334
  13. A critical function of the pial basement membrane in cortical histogenesis.
    J Neurosci. 2002 Jul 15;22(14):6029-40 PMID: 12122064
  14. The centrosome: The centriole-PCM coalition.
    Cell Motil Cytoskeleton. 2004 Jan;57(1):1-7 PMID: 14648552
  15. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors.
    Nat Neurosci. 2007 Jul;10(7):819-27 PMID: 17589506
  16. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis.
    J Neurosci. 2005 Jan 5;25(1):10-8 PMID: 15634762
  17. Cell coupling and uncoupling in the ventricular zone of developing neocortex.
    J Neurosci. 1997 Sep 15;17(18):7037-44 PMID: 9278539
  18. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma.
    Mol Cell Neurosci. 1999 Jun;13(6):450-64 PMID: 10383830
  19. Ependymal/subependymal zone cells of postnatal and adult songbird brain generate both neurons and nonneuronal siblings in vitro and in vivo.
    J Neurobiol. 1996 Aug;30(4):505-20 PMID: 8844514
  20. Vascular niche for adult hippocampal neurogenesis.
    J Comp Neurol. 2000 Oct 2;425(4):479-94 PMID: 10975875
  21. Association of ASIP/mPAR-3 with adherens junctions of mouse neuroepithelial cells.
    Dev Dyn. 2002 Sep;225(1):61-9 PMID: 12203721
  22. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex.
    Neuron. 2004 Sep 2;43(5):647-61 PMID: 15339647
  23. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response.
    Nat Genet. 2007 Nov;39(11):1350-60 PMID: 17906624
  24. Ependyma: normal and pathological. A review of the literature.
    Brain Res. 1985 Apr;356(1):1-19 PMID: 3888350
  25. Phenotypic and functional characterization of adult brain neuropoiesis.
    Proc Natl Acad Sci U S A. 2005 Jun 28;102(26):9353-8 PMID: 15961540
  26. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain.
    J Neurosci. 1997 Jul 1;17(13):5046-61 PMID: 9185542
  27. Network of tangential pathways for neuronal migration in adult mammalian brain.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14895-900 PMID: 8962152
  28. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network.
    J Comp Neurol. 2002 Sep 16;451(2):170-88 PMID: 12209835
  29. Cell types of the third ventricle wall of the rabbit (Oryctolagus cuniculus).
    J Submicrosc Cytol Pathol. 1991 Jan;23(1):147-57 PMID: 2036624
  30. Tanycytes: morphology and functions: a review.
    Int Rev Cytol. 1985;96:121-55 PMID: 2416706
  31. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin.
    Science. 2003 Jan 3;299(5603):117-20 PMID: 12511652
  32. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells.
    EMBO J. 2004 Jun 2;23(11):2314-24 PMID: 15141162
  33. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function.
    J Neurosci. 2008 Jan 2;28(1):264-78 PMID: 18171944
  34. Proliferation "hot spots" in adult avian ventricular zone reveal radial cell division.
    Neuron. 1990 Jul;5(1):101-9 PMID: 2369518
  35. Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche.
    Cell. 2006 Dec 15;127(6):1253-64 PMID: 17174898
  36. Mode of cell migration to the superficial layers of fetal monkey neocortex.
    J Comp Neurol. 1972 May;145(1):61-83 PMID: 4624784
  37. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling.
    Neuron. 2006 Jul 20;51(2):187-99 PMID: 16846854
  38. Differential expression of connexins during neocortical development and neuronal circuit formation.
    J Neurosci. 1997 May 1;17(9):3096-111 PMID: 9096144
  39. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis.
    Neuron. 2000 Dec;28(3):713-26 PMID: 11163261
  40. Expression of the secreted factors noggin and bone morphogenetic proteins in the subependymal layer and olfactory bulb of the adult mouse brain.
    Neuroscience. 2004;128(4):685-96 PMID: 15464277
  41. Embryonic vertebrate central nervous system: revised terminology. The Boulder Committee.
    Anat Rec. 1970 Feb;166(2):257-61 PMID: 5414696
  42. Regeneration of a germinal layer in the adult mammalian brain.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11619-24 PMID: 10500226
  43. mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult.
    Neuroscience. 1996 Jul;73(2):581-94 PMID: 8783272
  44. Chain migration of neuronal precursors.
    Science. 1996 Feb 16;271(5251):978-81 PMID: 8584933
  45. Neural stem and progenitor cells in cortical development.
    Novartis Found Symp. 2007;288:59-73; discussion 73-8, 96-8 PMID: 18494252
  46. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain.
    Nat Neurosci. 2004 Nov;7(11):1233-41 PMID: 15494728
  47. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision.
    Genesis. 2000 Nov-Dec;28(3-4):147-55 PMID: 11105057
  48. Contribution of intermediate progenitor cells to cortical histogenesis.
    Arch Neurol. 2007 May;64(5):639-42 PMID: 17502462
  49. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells.
    Science. 2004 May 28;304(5675):1338-40 PMID: 15060285
  50. Patched1 regulates hedgehog signaling at the primary cilium.
    Science. 2007 Jul 20;317(5836):372-6 PMID: 17641202
  51. Vertebrate Smoothened functions at the primary cilium.
    Nature. 2005 Oct 13;437(7061):1018-21 PMID: 16136078
  52. Mitotic cycling of radial glial cells of the fetal murine cerebral wall: a combined autoradiographic and immunohistochemical study.
    Brain Res. 1988 Feb 1;466(2):183-90 PMID: 3359310
  53. Induction of neostriatal neurogenesis slows disease progression in a transgenic murine model of Huntington disease.
    J Clin Invest. 2007 Oct;117(10):2889-902 PMID: 17885687
  54. Glial tubes in the rostral migratory stream of the adult rat.
    Brain Res Bull. 1997;42(1):9-21 PMID: 8978930
  55. Migration of young neurons in adult avian brain.
    Nature. 1988 Sep 22;335(6188):353-4 PMID: 3419503
  56. Hedgehog signalling in the mouse requires intraflagellar transport proteins.
    Nature. 2003 Nov 6;426(6962):83-7 PMID: 14603322
  57. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1.
    J Cell Biol. 2007 Feb 12;176(4):483-95 PMID: 17283184
  58. Mechanisms and functional implications of adult neurogenesis.
    Cell. 2008 Feb 22;132(4):645-60 PMID: 18295581
  59. Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells.
    Ann Neurol. 1998 May;43(5):576-85 PMID: 9585351
  60. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain.
    Cell. 1999 Jun 11;97(6):703-16 PMID: 10380923
  61. The Ki-67 protein: from the known and the unknown.
    J Cell Physiol. 2000 Mar;182(3):311-22 PMID: 10653597
  62. Mosaic organization of neural stem cells in the adult brain.
    Science. 2007 Jul 20;317(5836):381-4 PMID: 17615304
  63. For the long run: maintaining germinal niches in the adult brain.
    Neuron. 2004 Mar 4;41(5):683-6 PMID: 15003168
  64. Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes.
    J Comp Neurol. 1989 Nov 1;289(1):74-88 PMID: 2808761
  65. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain.
    Proc Natl Acad Sci U S A. 2008 Jan 22;105(3):1026-31 PMID: 18195354
  66. Ciliogenesis and centriole formation in the mouse embryonic nervous system. An ultrastructural analysis.
    Biol Cell. 1988;62(2):165-9 PMID: 3390625
  67. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration.
    Nature. 2004 Feb 19;427(6976):740-4 PMID: 14973487
  68. Subventricular zone-mediated ependyma repair in the adult mammalian brain.
    J Neurosci. 2008 Apr 2;28(14):3804-13 PMID: 18385338
  69. Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes.
    Development. 2006 Aug;133(16):3245-54 PMID: 16873583
  70. Characterization of adult neural stem cells and their relation to brain tumors.
    Cells Tissues Organs. 2008;188(1-2):212-24 PMID: 18223308
Article Info
Journal
Cell stem cell
Abbr.
Cell Stem Cell
ISSN
1875-9777
DOI
10.1016/j.stem.2008.07.004
Published
2008-09-11
Pages
265-78
Language
English
Region
United States
NLM ID
101311472
PMCID
PMC2613692
Subset
IM
Grants
NICHD NIH HHS · R01 HD032116 · United States
NICHD NIH HHS · R01 HD032116-08 · United States
NICHD NIH HHS · R37 HD032116 · United States
NICHD NIH HHS · HD-32116 · United States
Corrections
CommentIn
PMID: 18786409
External Links
PubMed source DOI: 10.1016/j.stem.2008.07.004 PMC Full Text View journal details
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