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Neuropediatrics 2017; 48(05): 329-339
DOI: 10.1055/s-0037-1601322
Review Article
Georg Thieme Verlag KG Stuttgart · New York

The Cerebellum and Its Wrapping Meninge: Developmental Interplay between Two Major Structures

Martin Catala
1   Laboratoire de Biologie du Développement, CNRS and Université Pierre et Marie Curie (UPMC), Paris, France
2   Fédération de Neurologie, Groupe Hospitalier Pitié-Salpêtrière, Paris, France
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Publication History

23 December 2016

21 February 2017

Publication Date:
23 March 2017 (online)

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Abstract

Meninges have long been considered as a protective and supportive tissue for the central nervous system. Nevertheless, new developmental roles are now attributed to them. The meninges that surround the cerebellum come from the cephalic mesoderm. They are essential for the cerebellum to develop normally. They induce and maintain the basal lamina and glia limitans. In the absence of these structures, the external granular cells of the cerebellum migrate aberrantly and penetrate the subarachnoid space. The molecules involved in the recognition between the cerebellar primordium and the basal lamina belong to two groups in humans: dystroglycan and laminin on the one hand, and GPR56 and collagen III on the other. Finally, molecules secreted by the meninges and acting on the cerebellum begin to be demonstrated; such is the case of SDF1 secreted under the action of FOXC1.

Keywords

developmental biology - cell interaction - genes - cerebellar polymicrogyria
 

  • References

  • 1 Schachenmayr W, Friede RL. The origin of subdural neomembranes. I. Fine structure of the dura-arachnoid interface in man. Am J Pathol 1978; 92 (01) 53-68
    PubMedGoogle Scholar
  • 2 Nabeshima S, Reese TS, Landis DMD, Brightman MW. Junctions in the meninges and marginal glia. J Comp Neurol 1975; 164 (02) 127-169
    CrossrefPubMedGoogle Scholar
  • 3 Haines DE. On the question of a subdural space. Anat Rec 1991; 230 (01) 3-21
    CrossrefPubMedGoogle Scholar
  • 4 Alcolado R, Weller RO, Parrish EP, Garrod D. The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol 1988; 14 (01) 1-17
    CrossrefPubMedGoogle Scholar
  • 5 Klika E. L'ultrastructure des méninges en ontogenèse de l'homme. Z Mikrosk Anat Forsch 1968; 79 (02) 209-222
    PubMedGoogle Scholar
  • 6 Osaka K, Handa H, Matsumoto S, Yasuda M. Development of the cerebrospinal fluid pathway in the normal and abnormal human embryos. Childs Brain 1980; 6 (01) 26-38
    PubMedGoogle Scholar
  • 7 O'Rahilly R, Müller F. The meninges in human development. J Neuropathol Exp Neurol 1986; 45 (05) 588-608
    CrossrefPubMedGoogle Scholar
  • 8 Couly GF, Coltey PM, Le Douarin NM. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 1992; 114 (01) 1-15
    PubMedGoogle Scholar
  • 9 McBratney-Owen B, Iseki S, Bamforth SD, Olsen BR, Morriss-Kay GM. Development and tissue origins of the mammalian cranial base. Dev Biol 2008; 322 (01) 121-132
    CrossrefPubMedGoogle Scholar
  • 10 Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. Tissue origins and interactions in the mammalian skull vault. Dev Biol 2002; 241 (01) 106-116
    CrossrefPubMedGoogle Scholar
  • 11 Yoshida T, Vivatbutsiri P, Morriss-Kay G, Saga Y, Iseki S. Cell lineage in mammalian craniofacial mesenchyme. Mech Dev 2008; 125 (9-10): 797-808
    CrossrefPubMedGoogle Scholar
  • 12 Aoto K, Sandell LL, Butler Tjaden NE. , et al. Mef2c-F10N enhancer driven b-galactosidase (LacZ) and Cre recombinase mice facilitate analyses of gene function and lineage fate in neural crest cells. Dev Biol 2015; 402 (01) 3-16
    CrossrefPubMedGoogle Scholar
  • 13 Sievers J, Klemm HP, Jenner S, Baumgarten HG, Berry M. Neuronal and extraneuronal effects of intracisternally administered 6-hydroxydopamine on the developing rat brain. J Neurochem 1980; 34 (04) 765-771
    CrossrefPubMedGoogle Scholar
  • 14 Sievers J, Mangold U, Berry M, Allen C, Schlossberger HG. Experimental studies on cerebellar foliation. I. A qualitative morphological analysis of cerebellar fissuration defects after neonatal treatment with 6-OHDA in the rat. J Comp Neurol 1981; 203 (04) 751-769
    CrossrefPubMedGoogle Scholar
  • 15 Allen C, Sievers J, Berry M, Jenner S. Experimental studies on cerebellar foliation. II. A morphometric analysis of cerebellar fissuration defects and growth retardation after neonatal treatment with 6-OHDA in the rat. J Comp Neurol 1981; 203 (04) 771-783
    CrossrefPubMedGoogle Scholar
  • 16 Sievers J, Mangold U, Berry M. 6-OHDA-induced ectopia of external granule cells in the subarachnoid space covering the cerebellum. Genesis and topography. Cell Tissue Res 1983; 230 (02) 309-336
    PubMedGoogle Scholar
  • 17 Sievers H, Sievers J, Baumgarten H-G, König N, Schlossberger HG. Distribution of tritium label in the neonate rat brain following intracisternal or subcutaneous administration of [3H]6-OHDA. An autoradiographic study. Brain Res 1983; 275 (01) 23-45
    CrossrefPubMedGoogle Scholar
  • 18 Mangold U, Sievers J, Berry M. 6-Hydroxydopamine induced ectopia of external granule cells in the subarachnoid space covering the cerebellum. II. Differentiation of granule cells: a scanning and transmission electron microscopic study. J Comp Neurol 1984; 227 (02) 267-284
    CrossrefPubMedGoogle Scholar
  • 19 Sievers J, Mangold U, Berry M. 6-OHDA-induced ectopia of external granule cells in the subarachnoid space covering the cerebellum. III. Morphology and synaptic organization of ectopic cerebellar neurons: a scanning and transmission electron microscopic study. J Comp Neurol 1985; 232 (03) 319-330
    CrossrefPubMedGoogle Scholar
  • 20 von Knebel Doeberitz C, Sievers J, Sadler M, Pehlemann FW, Berry M, Halliwell P. Destruction of meningeal cells over the newborn hamster cerebellum with 6-hydroxydopamine prevents foliation and lamination in the rostral cerebellum. Neuroscience 1986; 17 (02) 409-426
    CrossrefPubMedGoogle Scholar
  • 21 Sievers J, von Knebel Doeberitz C, Pehlemann F-W, Berry M. Meningeal cells influence cerebellar development over a critical period. Anat Embryol (Berl) 1986; 175 (01) 91-100
    CrossrefPubMedGoogle Scholar
  • 22 Sievers J, Pehlemann FW, Gude S, Berry M. A time course study of the alterations in the development of the hamster cerebellar cortex after destruction of the overlying meningeal cells with 6-hydroxydopamine on the day of birth. J Neurocytol 1994; 23 (02) 117-134
    CrossrefPubMedGoogle Scholar
  • 23 Sievers J, Pehlemann FW, Gude S, Berry M. Meningeal cells organize the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane. J Neurocytol 1994; 23 (02) 135-149
    CrossrefPubMedGoogle Scholar
  • 24 Hartmann D, Ziegenhagen MW, Sievers J. Meningeal cells stimulate neuronal migration and the formation of radial glial fascicles from the cerebellar external granular layer. Neurosci Lett 1998; 244 (03) 129-132
    CrossrefPubMedGoogle Scholar
  • 25 Hartmann D, Schulze M, Sievers J. Meningeal cells stimulate and direct the migration of cerebellar external granule cells in vitro. J Neurocytol 1998; 27 (06) 395-409
    CrossrefPubMedGoogle Scholar
  • 26 Ma Q, Jones D, Borghesani PR. , et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci U S A 1998; 95 (16) 9448-9453
    CrossrefPubMedGoogle Scholar
  • 27 Zou Y-R, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998; 393 (6685): 595-599
    CrossrefPubMedGoogle Scholar
  • 28 McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol 1999; 213 (02) 442-456
    CrossrefPubMedGoogle Scholar
  • 29 Tham TN, Lazarini F, Franceschini IA, Lachapelle F, Amara A, Dubois-Dalcq M. Developmental pattern of expression of the alpha chemokine stromal cell-derived factor 1 in the rat central nervous system. Eur J Neurosci 2001; 13 (05) 845-856
    CrossrefPubMedGoogle Scholar
  • 30 Reiss K, Mentlein R, Sievers J, Hartmann D. Stromal cell-derived factor 1 is secreted by meningeal cells and acts as chemotactic factor on neuronal stem cells of the cerebellar external granular layer. Neuroscience 2002; 115 (01) 295-305
    CrossrefPubMedGoogle Scholar
  • 31 Tissir F, Wang C-E, Goffinet AM. Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res Dev Brain Res 2004; 149 (01) 63-71
    CrossrefPubMedGoogle Scholar
  • 32 Zhu Y, Yu T, Zhang X-C, Nagasawa T, Wu JY, Rao Y. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat Neurosci 2002; 5 (08) 719-720
    CrossrefPubMedGoogle Scholar
  • 33 Dambska M, Wisniewski K, Sher JH. Lissencephaly: two distinct clinico-pathological types. Brain Dev 1983; 5 (03) 302-310
    CrossrefPubMedGoogle Scholar
  • 34 Barkovich AJ, Guerrini R, Kuzniecky RI, Jackson GD, Dobyns WB. A developmental and genetic classification for malformations of cortical development: update 2012. Brain 2012; 135 (Pt 5): 1348-1369
    CrossrefPubMedGoogle Scholar
  • 35 Takada K, Nakamura H, Tanaka J. Cortical dysplasia in congenital muscular dystrophy with central nervous system involvement (Fukuyama type). J Neuropathol Exp Neurol 1984; 43 (04) 395-407
    CrossrefPubMedGoogle Scholar
  • 36 Lyon G, Raymond G, Mogami K, Gadisseux J-F, Della Giustina E. Disorder of cerebellar foliation in Walker's lissencephaly and neu-laxova syndrome. J Neuropathol Exp Neurol 1993; 52 (06) 633-639
    CrossrefPubMedGoogle Scholar
  • 37 Haltia M, Leivo I, Somer H. , et al. Muscle-eye-brain disease: a neuropathological study. Ann Neurol 1997; 41 (02) 173-180
    CrossrefPubMedGoogle Scholar
  • 38 Takada K, Nakamura H. Cerebellar micropolygyria in Fukuyama congenital muscular dystrophy: observations in fetal and pediatric cases. Brain Dev 1990; 12 (06) 774-778
    CrossrefPubMedGoogle Scholar
  • 39 Barkovich AJ. Neuroimaging manifestations and classification of congenital muscular dystrophies. AJNR Am J Neuroradiol 1998; 19 (08) 1389-1396
    PubMedGoogle Scholar
  • 40 Aida N, Yagishita A, Takada K, Katsumata Y. Cerebellar MR in Fukuyama congenital muscular dystrophy: polymicrogyria with cystic lesions. AJNR Am J Neuroradiol 1994; 15 (09) 1755-1759
    PubMedGoogle Scholar
  • 41 van der Knaap MS, Smit LM, Barth PG. , et al. Magnetic resonance imaging in classification of congenital muscular dystrophies with brain abnormalities. Ann Neurol 1997; 42 (01) 50-59
    CrossrefPubMedGoogle Scholar
  • 42 Valanne L, Pihko H, Katevuo K, Karttunen P, Somer H, Santavuori P. MRI of the brain in muscle-eye-brain (MEB) disease. Neuroradiology 1994; 36 (06) 473-476
    CrossrefPubMedGoogle Scholar
  • 43 Hewitt JE. Abnormal glycosylation of dystroglycan in human genetic disease. Biochim Biophys Acta 2009; 1792 (09) 853-861
    CrossrefPubMedGoogle Scholar
  • 44 Montanaro F, Lindenbaum M, Carbonetto S. alpha-Dystroglycan is a laminin receptor involved in extracellular matrix assembly on myotubes and muscle cell viability. J Cell Biol 1999; 145 (06) 1325-1340
    CrossrefPubMedGoogle Scholar
  • 45 Henion TR, Qu Q, Smith FI. Expression of dystroglycan, fukutin and POMGnT1 during mouse cerebellar development. Brain Res Mol Brain Res 2003; 112 (1-2): 177-181
    CrossrefPubMedGoogle Scholar
  • 46 Williamson RA, Henry MD, Daniels KJ. , et al. Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum Mol Genet 1997; 6 (06) 831-841
    CrossrefPubMedGoogle Scholar
  • 47 Geis T, Marquard K, Rödl T. , et al. Homozygous dystroglycan mutation associated with a novel muscle-eye-brain disease-like phenotype with multicystic leucodystrophy. Neurogenetics 2013; 14 (3-4): 205-213
    CrossrefPubMedGoogle Scholar
  • 48 Riemersma M, Mandel H, van Beusekom E. , et al. Absence of a- and b-dystroglycan is associated with Walker-Warburg syndrome. Neurology 2015; 84 (21) 2177-2182
    CrossrefPubMedGoogle Scholar
  • 49 Moore SA, Saito F, Chen J. , et al. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 2002; 418 (6896): 422-425
    CrossrefPubMedGoogle Scholar
  • 50 Satz JS, Barresi R, Durbeej M. , et al. Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast. J Neurosci 2008; 28 (42) 10567-10575
    CrossrefPubMedGoogle Scholar
  • 51 Satz JS, Ostendorf AP, Hou S. , et al. Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J Neurosci 2010; 30 (43) 14560-14572
    CrossrefPubMedGoogle Scholar
  • 52 Nguyen H, Ostendorf AP, Satz JS. , et al. Glial scaffold required for cerebellar granule cell migration is dependent on dystroglycan function as a receptor for basement membrane proteins. Acta Neuropathol Commun 2013; 1: 58
    CrossrefPubMedGoogle Scholar
  • 53 Willer T, Prados B, Falcón-Pérez JM. , et al. Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci U S A 2004; 101 (39) 14126-14131
    CrossrefPubMedGoogle Scholar
  • 54 Hu H, Li J, Gagen CS. , et al. Conditional knockout of protein O-mannosyltransferase 2 reveals tissue-specific roles of O-mannosyl glycosylation in brain development. J Comp Neurol 2011; 519 (07) 1320-1337
    CrossrefPubMedGoogle Scholar
  • 55 Kurahashi H, Taniguchi M, Meno C. , et al. Basement membrane fragility underlies embryonic lethality in fukutin-null mice. Neurobiol Dis 2005; 19 (1-2): 208-217
    CrossrefPubMedGoogle Scholar
  • 56 Liu J, Ball SL, Yang Y. , et al. A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev 2006; 123 (03) 228-240
    CrossrefPubMedGoogle Scholar
  • 57 Holzfeind PJ, Grewal PK, Reitsamer HA. , et al. Skeletal, cardiac and tongue muscle pathology, defective retinal transmission, and neuronal migration defects in the Large(myd) mouse defines a natural model for glycosylation-deficient muscle - eye - brain disorders. Hum Mol Genet 2002; 11 (21) 2673-2687
    CrossrefPubMedGoogle Scholar
  • 58 Michele DE, Barresi R, Kanagawa M. , et al. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 2002; 418 (6896): 417-422
    CrossrefPubMedGoogle Scholar
  • 59 Li X, Zhang P, Yang Y, Xiong Y, Qi Y, Hu H. Differentiation and developmental origin of cerebellar granule neuron ectopia in protein O-mannose UDP-N-acetylglucosaminyl transferase 1 knockout mice. Neuroscience 2008; 152 (02) 391-406
    CrossrefPubMedGoogle Scholar
  • 60 Poretti A, Häusler M, von Moers A. , et al. Ataxia, intellectual disability, and ocular apraxia with cerebellar cysts: a new disease?. Cerebellum 2014; 13 (01) 79-88
    CrossrefPubMedGoogle Scholar
  • 61 Aldinger KA, Mosca SJ, Tétreault M. , et al; University of Washington Center for Mendelian Genomics; Care4Rare Canada. Mutations in LAMA1 cause cerebellar dysplasia and cysts with and without retinal dystrophy. Am J Hum Genet 2014; 95 (02) 227-234
    CrossrefPubMedGoogle Scholar
  • 62 Micalizzi A, Poretti A, Romani M. , et al. Clinical, neuroradiological and molecular characterization of cerebellar dysplasia with cysts (Poretti-Boltshauser syndrome). Eur J Hum Genet 2016; 24 (09) 1262-1267
    CrossrefPubMedGoogle Scholar
  • 63 Vilboux T, Malicdan MCV, Chang YM. , et al; NISC Comparative Sequencing Program. Cystic cerebellar dysplasia and biallelic LAMA1 mutations: a lamininopathy associated with tics, obsessive compulsive traits and myopia due to cell adhesion and migration defects. J Med Genet 2016; 53 (05) 318-329
    CrossrefPubMedGoogle Scholar
  • 64 Miner JH, Li C, Mudd JL, Go G, Sutherland AE. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 2004; 131 (10) 2247-2256
    CrossrefPubMedGoogle Scholar
  • 65 Alpy F, Jivkov I, Sorokin L. , et al. Generation of a conditionally null allele of the laminin alpha1 gene. Genesis 2005; 43 (02) 59-70
    CrossrefPubMedGoogle Scholar
  • 66 Heng C, Lefebvre O, Klein A. , et al. Functional role of laminin a1 chain during cerebellum development. Cell Adhes Migr 2011; 5 (06) 480-489
    CrossrefPubMedGoogle Scholar
  • 67 Ichikawa-Tomikawa N, Ogawa J, Douet V. , et al. Laminin a1 is essential for mouse cerebellar development. Matrix Biol 2012; 31 (01) 17-28
    CrossrefPubMedGoogle Scholar
  • 68 Radmanesh F, Caglayan AO, Silhavy JL. , et al. Mutations in LAMB1 cause cobblestone brain malformation without muscular or ocular abnormalities. Am J Hum Genet 2013; 92 (03) 468-474
    CrossrefPubMedGoogle Scholar
  • 69 Barak T, Kwan KY, Louvi A. , et al. Recessive LAMC3 mutations cause malformations of occipital cortical development. Nat Genet 2011; 43 (06) 590-594
    CrossrefPubMedGoogle Scholar
  • 70 Harbord MG, Boyd S, Hall-Craggs MA, Kendall B, McShane MA, Baraitser M. Ataxia, developmental delay and an extensive neuronal migration abnormality in 2 siblings. Neuropediatrics 1990; 21 (04) 218-221
    Article in Thieme ConnectPubMedGoogle Scholar
  • 71 Piao X, Hill RS, Bodell A. , et al. G protein-coupled receptor-dependent development of human frontal cortex. Science 2004; 303 (5666): 2033-2036
    CrossrefPubMedGoogle Scholar
  • 72 Piao X, Chang BS, Bodell A. , et al. Genotype-phenotype analysis of human frontoparietal polymicrogyria syndromes. Ann Neurol 2005; 58 (05) 680-687
    CrossrefPubMedGoogle Scholar
  • 73 Bahi-Buisson N, Poirier K, Boddaert N. , et al. GPR56-related bilateral frontoparietal polymicrogyria: further evidence for an overlap with the cobblestone complex. Brain 2010; 133 (11) 3194-3209
    CrossrefPubMedGoogle Scholar
  • 74 Quattrocchi CC, Zanni G, Napolitano A. , et al. Conventional magnetic resonance imaging and diffusion tensor imaging studies in children with novel GPR56 mutations: further delineation of a cobblestone-like phenotype. Neurogenetics 2013; 14 (01) 77-83
    CrossrefPubMedGoogle Scholar
  • 75 Luo R, Jeong S-J, Jin Z, Strokes N, Li S, Piao X. G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc Natl Acad Sci U S A 2011; 108 (31) 12925-12930
    CrossrefPubMedGoogle Scholar
  • 76 Jeong S-J, Li S, Luo R, Strokes N, Piao X. Loss of Col3a1, the gene for Ehlers-Danlos syndrome type IV, results in neocortical dyslamination. PLoS One 2012; 7 (01) e29767 . Doi: 10.1371/journal.pone.0029767
    CrossrefPubMedGoogle Scholar
  • 77 Plancke A, Holder-Espinasse M, Rigau V, Manouvrier S, Claustres M, Khau Van Kien P. Homozygosity for a null allele of COL3A1 results in recessive Ehlers-Danlos syndrome. Eur J Hum Genet 2009; 17 (11) 1411-1416
    CrossrefPubMedGoogle Scholar
  • 78 Aldinger KA, Lehmann OJ, Hudgins L. , et al. FOXC1 is required for normal cerebellar development and is a major contributor to chromosome 6p25.3 Dandy-Walker malformation. Nat Genet 2009; 41 (09) 1037-1042
    CrossrefPubMedGoogle Scholar
  • 79 Haldipur P, Gillies GS, Janson OK. , et al. Foxc1 dependent mesenchymal signalling drives embryonic cerebellar growth. eLife 2014; 3: e03962 . Doi: 10.7554/elife.03962
    CrossrefPubMedGoogle Scholar