Skip to main content

Granule Cell Migration and Differentiation

  • Living reference work entry
  • First Online:
Handbook of the Cerebellum and Cerebellar Disorders

Abstract

The developing cerebellum granule cells migrate from their birthplace to their final destination. The active translocation of granule cells is essential for the formation of a well-organized cerebellar cortex. In this chapter, we will review (1) how granule cells migrate from their origin to their resident destination in the developing cerebellum, (2) the cellular and molecular mechanisms underlying granule cell migration, (3) how exposure to toxic chemicals and natural environmental factors affects the migration of granule cells, and (4) the cellular and molecular mechanisms underlying the differentiation of postmigratory granule cells.

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

Access this chapter

Institutional subscriptions

References

  • Bakkum BW, Benevento LA, Cohen RS (1991) Effects of light/dark- and dark-rearing on synaptic morphology in the superior colliculus and visual cortex of the postnatal and adult rat. J Neurosci Res 28:65–80

    Article  CAS  PubMed  Google Scholar 

  • Bartlett WP, Li X-S, Williams M, Benkovic S (1991) Localization of insulin-like growth factor-1 mRNA in murine central nervous system during postnatal development. Dev Biol 147:239–250

    Article  CAS  PubMed  Google Scholar 

  • Basille M, Gonzalez BJ, Leroux P, Jeandel L, Fournier A, Vaudry H (1993) Localization and characterization of PACAP receptors in the rat cerebellum during development: evidence for a stimulatory effect of PACAP on immature cerebellar granule cells. Neuroscience 57:329–338

    Article  CAS  PubMed  Google Scholar 

  • Basille M, Vaudry D, Coulouarn Y, Jegou S, Lihrmann I, Fournier A, Vaudry H, Gonzalez BJ (2000) Comparative distribution of pituitary adenylate cyclase-activating polypeptide (PACAP) binding sites and PACAP receptor mRNAs in the rat brain during development. J Comp Neurol 425:495–509

    Article  CAS  PubMed  Google Scholar 

  • Basille M, Cartier D, Vaudry D, Lihrmann I, Fournier A, Freger P, Gallo-Payet N, Vaudry H, Gonzalez BJ (2006) Localization and characterization of pituitary adenylate cyclase-activating polypeptide receptors in the human cerebellum during development. J Comp Neurol 496: 468–478

    Article  CAS  PubMed  Google Scholar 

  • Bénard M, Lebon A, Komuro H, Vaudry D, Galas G (2015) Ex vivo imaging of postnatal cerebellar granule cell migration using confocal macroscopy. J Vis Exp 99:e52810

    Google Scholar 

  • Benon AL, Ya C, Martin L, Watrin C, Chounlamountri C et al (2017) The Syk kinases orchestrate cerebellar granule cell tangential migration. Neuroscience 360:230–239

    Article  CAS  PubMed  Google Scholar 

  • Bertani S, Carboni L, Criado A, Michielin F, Mangiarini L et al (2010) Circadian profile of peripheral hormone levels in Sprague-Dawley rats and in common marmosets (Callithrix jacchus). In Vivo 24:827–836

    CAS  PubMed  Google Scholar 

  • Bondy CA, Lee WH (1993) Patterns of insulin-like growth factor and IGF receptor gene expression in the brain. Functional implications. Ann N Y Acad Sci 692:33–43

    Article  CAS  PubMed  Google Scholar 

  • Botia B, Basille M, Allais A, Raoult E, Falluel-Morel A, Galas L, Jolivel V, Wurtz O, Komuro H, Fournier A, Vaudry H, Burel D, Gonzalez B, Vaudry D (2007) Neurotrophic effects of PACAP in the cerebellar cortex. Peptides 28:1746–1752

    Article  CAS  PubMed  Google Scholar 

  • Bradford AB, Mancini JD, Atchison WD (2016) Methylmercury-dependent increases in Fluo4 fluorescence in neonatal rat cerebellar slices depend on granule cell migrational stage and GABAA receptor modulation. J Pharmacol Exp Ther 356:2–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandon DH, Holditch-Davis D, Belyea M (2002) Preterm infants born at less than 31 weeks’ gestation have improved growth in cycled light compared with continuous near darkness. J Pediatr 140:192–199

    Article  PubMed  Google Scholar 

  • Brooks E, Waters E, Farrington L, Canal MM (2011) Differential hypothalamic tyrosine hydroxylase distribution and activation by light in adult mice reared under different light conditions during the suckling period. Brain Struct Funct 216:357–370

    Article  CAS  PubMed  Google Scholar 

  • Buchsbaum IY, Cappello S (2019) Neuronal migration in the CNS during development and disease: insights from in vivo and in vitro models. Development 146:dev163766

    Article  PubMed  CAS  Google Scholar 

  • Cace IB, Milardovic A, Prp I, Krajina R, Petrovic O, Vukelic P et al (2011) Relationship between the prenatal exposure to low-level of mercury and the size of a newborn’s cerebellum. Med Hypotheses 76:514–516

    Article  CAS  PubMed  Google Scholar 

  • Cameron DB, Galas L, Jiang Y, Raoult E, Vaudry D, Komuro H (2007) Cerebellar cortical-layer-specific control of neuronal migration by pituitary adenylate cyclase-activating polypeptide. Neuroscience 146:697–712

    Article  CAS  PubMed  Google Scholar 

  • Cameron DB, Raoult E, Galas L, Jiang Y, Lee K, Hu T, Vaudry D, Komuro H (2009) Role of PACAP in controlling granule cell migration. Cerebellum 8:433–440

    Article  CAS  PubMed  Google Scholar 

  • Chang LW, Wade PR, Pounds JG, Reuhl KR (1980) Prenatal and neonatal toxicology and pathology of heavy metals. Adv Pharmacol Chemother 17:195–231

    Article  CAS  PubMed  Google Scholar 

  • Chuong C-M (1990) Differential roles of multiple adhesion molecules in cell migration: granule cell migration in cerebellum. Experientia 46:892–899

    Article  CAS  PubMed  Google Scholar 

  • Chuong C-M, Crossin KL, Edelman GM (1987) Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers. J Cell Biol 104:331–342

    Article  CAS  PubMed  Google Scholar 

  • Clarkson TW (1997) The toxicology of mercury. Crit Rev Clin Lab Sci 34:369–403

    Article  CAS  PubMed  Google Scholar 

  • Clarren SK, Smith DW (1978) The fetal alcohol syndrome. N Engl J Med 298:1063–1067

    Article  CAS  PubMed  Google Scholar 

  • Clarren SK, Alvord EC, Sumi SM (1978) Brain malformations related to prenatal exposure to ethanol. J Pediatr 92:64–67

    Article  CAS  PubMed  Google Scholar 

  • Crinnion WJ (2000) Environmental medicine, part three: long-term effects of chronic low-dose mercury exposure. Altern Med Rev 5:209–223

    CAS  PubMed  Google Scholar 

  • Dulcis D, Spitzer NC (2008) Illumination controls differentiation of dopamine neurons regulating behavior. Nature 456:195–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ekino S, Susa M, Ninomiya T, Imamura K, Kitamura T (2007) Minamata disease revisited: an update on the acute and chronic manifestations of methyl mercury poisoning. J Neurol Sci 262:131–144

    Article  CAS  PubMed  Google Scholar 

  • Estep JA, Wong W, Wong YE, Loui BM, Riccomagno MM (2018) The RacGAP β-chimaerin is essential for cerebellar granule cell migration. Sci Rep 8:680

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eto K (1997) Pathology of Minamata disease. Toxicol Pathol 25:614–623

    Article  CAS  PubMed  Google Scholar 

  • Eto K, Oyanagi S, Itai Y, Tokunaga H, Takizawa Y, Suda I (1992) A fetal type of Minamata disease. An autopsy case report with special reference to the nervous system. Mol Chem Neuropathol 16:171–186

    Article  CAS  PubMed  Google Scholar 

  • Fahrion JK, Komuro Y, Li Y, Ohno N, Littner Y, Raoult E, Galas L, Vaudry D, Komuro H (2012) Rescue of neuronal migration deficits in a mouse model of fetal Minamata disease by increasing neuronal Ca2+ spike frequency. Proc Natl Acad Sci USA 109:5057–5062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farrant M, Feldmeyer D, Takahashi T, Cull-Candy SG (1994) NMDA-receptor channel diversity in the developing cerebellum. Nature 368:335–339

    Article  CAS  PubMed  Google Scholar 

  • Fernandez C, Tatard VM, Bertrand N, Dahmane N (2010) Differential modulation of sonic-hedgehog-induced cerebellar granule cell precursor proliferation by the IGF signaling network. Dev Neurosci 32:59–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fonken LK, Workman JL, Walton JC, Weil ZM, Morris JS, Haim A, Nelson RJ (2010) Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci USA 107:18664–18669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galas L, Bénard M, Lebon A, Komuro Y, Schapman D, Vaudry H, Vaudry D, Komuro H (2017) Postnatal migration of cerebellar interneurons. Brain Sci 7:62

    Article  PubMed Central  CAS  Google Scholar 

  • Gonzalez R, Leroux P, Lamacz M, Bodenant C, Balazs R, Vaudry H (1990) Pharmacological characterization of somatostatin receptors in the rat cerebellum during development. J Neurochem 55:729–737

    Article  CAS  PubMed  Google Scholar 

  • Gore AC (2008) Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front Neuroendocrinol 29:358–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gradin HH, Larsson N, Marklund U, Gullberg M (1998) Regulation of microtubule dynamics by extracellular signals: cAMP-dependent protein kinase switches off the activity of oncoprotein 18 in intact cells. J Cell Biol 140:131–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grandjean P, Jorgensen PJ, Weihe P (1994) Methylmercury from mother’s milk: accumulation in infants. Environ Health Perspect 102:74–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gressens P (2000) Mechanisms and disturbances of neuronal migration. Pediatr Res 48:725–730

    Article  CAS  PubMed  Google Scholar 

  • Guerrini R, Parrini E (2010) Neuronal migration disorders. Neurobiol Dis 38:154–166

    Article  CAS  PubMed  Google Scholar 

  • Haase A, Bicker G (2003) Nitric oxide and cyclic nucleotides are regulators of neuronal migration in an insect embryo. Development 130:3977–3987

    Article  CAS  PubMed  Google Scholar 

  • Harada M (1964) Neuropsychiatric disturbances due to organic mercury poisoning during the prenatal period. Psychiatr Neurol Jpn 66:426–468

    Google Scholar 

  • Haraguchi S, Kamata M, Tokita T, Tashiro K, Sato M et al (2019) Light-at-night exposure affects brain development through pineal allopregnanolone-dependent mechanisms. Elife 8:e45306

    Article  PubMed  PubMed Central  Google Scholar 

  • Heng JIT, Moonen G, Nguyen L (2007) Neurotransmitters regulate cell migration in the telencephalon. Eur J Neurosci 26:537–546

    Article  PubMed  Google Scholar 

  • Hsueh Y, Lee C, Chien S, Chen W, Shiue H et al (2017) Association of blood heavy metals with developmental delays and health status in children. Sci Rep 7:43608

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu G, Jin M, Lin X, Guo C, Zhang L, Sun Z (2010) Mercury distribution in neonatal rat brain after intrauterine methylmercury exposure. Environ Toxicol Pharmacol 29:7–11

    Article  CAS  PubMed  Google Scholar 

  • Huang G-J, Edwards A, Tsai C-Y, Lee Y-S, Peng L et al (2014) Ectopic cerebellar cell migration causes maldevelopment of Purkinje cells and abnormal motor behaviour in Cxcr4 null mice. PLoS One 9(2):e86471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jakovcevski I, Siering J, Hargus G, Karl N, Hoelters L et al (2009) Close homologue of adhesion molecule L1 promotes survival of Purkinje and granule cells and granule cell migration during murine cerebellar development. J Comp Neurol 513:496–510

    Article  PubMed  Google Scholar 

  • Jiang Y, Kumada T, Cameron DB, Komuro H (2008) Cerebellar granule cell migration and the effects of alcohol. Dev Neurosci 30:7–23

    Article  PubMed  CAS  Google Scholar 

  • Johnson J, Wu V, Donovan M, Majumdar S, Rentería RC et al (2010) Melanopsin-dependent light avoidance in neonatal mice. Proc Natl Acad Sci USA 107:17374–17378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komuro H, Kumada T (2005) Ca2+ transients control CNS neuronal migration. Cell Calcium 37:387–393

    Article  CAS  PubMed  Google Scholar 

  • Komuro H, Rakic P (1992) Selective role of N-type calcium channels in neuronal migration. Science 257:806–809

    Article  CAS  PubMed  Google Scholar 

  • Komuro H, Rakic P (1993) Modulation of neuronal migration by NMDA receptors. Science 260:95–97

    Article  CAS  PubMed  Google Scholar 

  • Komuro H, Rakic P (1995) Dynamics of granule cell migration: a confocal microscopic study in acute cerebellar slice preparations. J Neurosci 15:1110–1120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komuro H, Rakic P (1996) Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 17:275–285

    Article  CAS  PubMed  Google Scholar 

  • Komuro H, Rakic P (1998a) Distinct modes of neuronal migration in different domains of developing cerebellar cortex. J Neurosci 18:1478–1490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komuro H, Rakic P (1998b) Orchestration of neuronal migration by activity of ion channels, neurotransmitter receptors, and intracellular Ca2+ fluctuations. J Neurobiol 37:110–130

    Article  CAS  PubMed  Google Scholar 

  • Komuro H, Yacubova E (2003) Recent advances in cerebellar granule cell migration. Cell Mol Life Sci 60:1084–1098

    Article  CAS  PubMed  Google Scholar 

  • Komuro H, Yacubova E, Yacubova E, Rakic P (2001) Mode and tempo of tangential cell migration in the cerebellar external granular layer. J Neurosci 21:527–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komuro Y, Galas L, Lebon A, Raoult E, Fahrion JK, Tilot A, Kumada T, Ohno N, Vaudry D, Komuro H (2015) Roles of calcium and cyclic nucleotide signaling in cerebellar granule cell migration. Dev Neurobiol 75:369–387

    Article  CAS  PubMed  Google Scholar 

  • Kullmann JA, Wickertsheim I, Minnerup L, Costell M, Friauf E, Rust MB (2015) Profilin1 activity in cerebellar granule neurons is required for radial migration in vivo. Cell Adh Migr 9:247–253

    Article  CAS  PubMed  Google Scholar 

  • Kumada T, Komuro H (2004) Completion of neuronal migration regulated by loss of Ca2+ transients. Proc Natl Acad Sci USA 101:8479–8484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumada T, Lakshmana MK, Komuro H (2006) Reversal of neuronal migration in a mouse model of fetal alcohol syndrome by controlling second-messenger signalings. J Neurosci 26:742–756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumada T, Jiang Y, Cameron DB, Komuro H (2007) How does alcohol impair neuronal migration? J Neurosci Res 85:465–470

    Article  CAS  PubMed  Google Scholar 

  • Kumada T, Komuro Y, Li Y, Wang Z, Littner Y, Komuro H (2010) Inhibition of cerebellar granule cell turning by alcohol. Neuroscience 170:1328–1344

    Article  CAS  PubMed  Google Scholar 

  • Lapham LW, Cernichiari E, Cox C, Myers GJ, Baggs RB et al (1995) An analysis of autopsy brain tissue from infants prenatally exposed to methylmercury. Neurotoxicology 16:689–704

    CAS  PubMed  Google Scholar 

  • Lee WH, Javedan S, Bondy CA (1992) Coordinate expression of insulin-like growth factor system components by neurons and neuroglia during retinal and cerebellar development. J Neurosci 12:4737–4744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legué E, Riedel E, Joyner AL (2015) Clonal analysis reveals granule cell behaviors and compartmentalization that determine the folded morphology of the cerebellum. Development 142:1661–1671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • León-Olea M, Martyniuk CJ, Orlando EF, Ottinger MA, Rosenfeld C, Wolstenholme J, Trudeau VL (2014) Current concepts in neuroendocrine disruption. Gen Comp Endocrinol 203:158173

    Article  CAS  Google Scholar 

  • Levi G, Patrizio M, Gallo V (1991) Release of endogenous and newly synthesized glutamate and of other amino acids induced by non-N-methyl-d-aspartate receptor activation in cerebellar granule cell cultures. J Neurochem 56:199–206

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Komuro Y, Fahrion JK, Hu T, Ohno N, Fenner KB, Wooton J, Raoult E, Galas L, Vaudry D, Komuro H (2012) Light stimuli control neuronal migration by altering of insulin-like growth factor 1 (IGF-1) signaling. Proc Natl Acad Sci USA 109:2630–2635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luhmann HJ, Fukuda A, Kilb W (2015) Control of cortical neuronal migration by glutamate and GABA. Front Cell Neurosci 9:4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mangaru Z, Salem E, Sherman M, Van Dine SE, Bhambri A et al (2013) Neuronal migration defect of the developing cerebellar vermis in substrains of C57BL/6 mice: cytoarchitecture and prevalence of molecular layer heterotopia. Dev Neurosci 35:28–39

    Article  CAS  PubMed  Google Scholar 

  • Mann NP, Haddow R, Stokes L, Goodley S, Rutter N (1986) Effect of night and day on preterm infants in a newborn nursery: randomised trial. Br Med J 293:1265–1267

    Article  CAS  Google Scholar 

  • Marcus JC (1987) Neurological findings in the fetal alcohol syndrome. Neuropediatrics 18:158–160

    Article  CAS  PubMed  Google Scholar 

  • Marret S, Gressens P, Evrard P (1996) Arrest of neuronal migration by excitatory amino acid in hamster developing brain. Proc Natl Acad Sci USA 93:15463–15468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto H, Koya G, Takeuchi T (1965) Fetal Minamata disease. A neuropathological study of two cases of intrauterine intoxication by a methyl mercury compound. J Neuropathol Exp Neurol 24:563–574

    Article  CAS  PubMed  Google Scholar 

  • Maubert E, Slama A, Ciofi P, Viollet C, Tramu G, Dupouy JP, Epelbaum J (1994) Developmental patterns of somatostatin-receptors and somatostatin-immunoreactivity during early neurogenesis in the rat. Neuroscience 62:317–325

    Article  CAS  PubMed  Google Scholar 

  • Mellor JR, Merio D, Jones A, Wisden W, Randall AD (1998) Mouse cerebellar granule cell differentiation: electrical activity regulate the GABAA receptor α6 subunit gene. J Neurosci 18:2822–2833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Men Y, Zhang A, Li H, Jin Y, Sun X et al (2015) LKB1 regulates cerebellar development by controlling sonic hedgehog-mediated granule cell precursor proliferation and granule cell migration. Sci Rep 5:16232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miale IL, Sidman RL (1961) An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 4:277–296

    Article  CAS  PubMed  Google Scholar 

  • Miller MW (1986) Effects of alcohol on the generation and migration of cerebral cortical neurons. Science 233:1308–1311

    Article  CAS  PubMed  Google Scholar 

  • Miller MW (1993) Migration of cortical neurons is altered by gestational exposure to ethanol. Alcohol Clin Exp Res 17:304–314

    Article  CAS  PubMed  Google Scholar 

  • Milner R, Campbell IL (2002) The integrin family of cell adhesion molecules has multiple functions within the CNS. J Neurosci Res 69:286–291

    Article  CAS  PubMed  Google Scholar 

  • Monyer H, Burnashev N, Lauria DJ, Sakman B, Seeburg PH (1994) Development of regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529–540

    Article  CAS  PubMed  Google Scholar 

  • Mulherkar S, Uddin MD, Couvillon AD, Sillitoe RV, Tolias KF (2014) The small GTPases RhoA and Rac1 regulate cerebellar development by controlling cell morphogenesis, migration and foliation. Dev Biol 394:39–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munck S, Bedner P, Bottaro T, Harz H (2004) Spatiotemporal properties of cytoplasmic cyclic AMP gradients can alter the turning behavior of neuronal growth cones. Eur J Neurosci 19:791–797

    Article  PubMed  Google Scholar 

  • Nadarajah B, Parnavelas JG (2002) Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423–432

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi S, Okazawa M (2006) Membrane potential-regulated Ca2+ signaling in development and maturation of mammalian cerebellar granule cells. J Physiol 575:389–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navara KJ, Nelson RJ (2007) The dark side of light at night: physiological, epidemiological, and ecological consequences. J Pineal Res 43:215–224

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama M, Hoshino A, Tsai L, Henley JR, Goshima Y, Tessier-Lavigne M, Poo MM, Hong K (2003) Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 423:990–995

    Article  CAS  PubMed  Google Scholar 

  • Ohta H, Mitchell AC, McMahon DG (2006) Constant light disrupts the developing mouse biological clock. Pediatr Res 60:304–308

    Article  PubMed  Google Scholar 

  • Pan Y-H, Wu N, Yuan X-B (2019) Toward a better understanding of neuronal migration deficits in autism spectrum disorders. Front Cell Dev Biol 7:205

    Article  PubMed  PubMed Central  Google Scholar 

  • Parpura V, Basarski TA, Lin F, Jeftinia K, Jeftinia S et al (1994) Glutamate mediated astrocyte-neuron signaling. Nature 369:744–747

    Article  CAS  PubMed  Google Scholar 

  • Patel YC (1997) Molecular pharmacology of somatostatin receptor subtypes. J Endocrinol Invest 20:348–367

    Article  CAS  PubMed  Google Scholar 

  • Pirrone N (2001) Mercury research in Europe: towards the preparation of the EU air quality directive. Atmos Environ 35:2979–2986

    Article  CAS  Google Scholar 

  • Pon DV, Robinson SR (1994) Glutamate in some retinal neurons is derived solely from glia. Neuroscience 60:355–366

    Article  Google Scholar 

  • Rakic P (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A golgi and electron microscopic study in Macacus rhesus. J Comp Neurol 141:283–312

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–83

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (1990) Principles of neuronal cell migration. Experientia 46:882–891

    Article  CAS  PubMed  Google Scholar 

  • Rakic P, Komuro H (1995) The role of receptor/channel activity in neuronal cell migration. J Neurobiol 26:299–315

    Article  CAS  PubMed  Google Scholar 

  • Rakic P, Cameron SR, Komuro H (1994) Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr Opin Neurobiol 4:63–69

    Article  CAS  PubMed  Google Scholar 

  • Raoult E, Roussel B, Bénard M, Lefebvre T, Ravni A, Ali C, Vivien D, Komuro H, Fournier A, Vaudry H, Vaudry D, Galas L (2011) PACAP stimulates the expression and the release of tPA in neuronal cells. Involvement of tPA in neuroprotective effect of PACAP. J Neurochem 119:920–931

    Article  CAS  PubMed  Google Scholar 

  • Raoult E, Benard M, Komuro H, Lebon A, Fournier A, Vaudry H, Vaudry D, Galas L (2014) Cortical-layer-specific effects of PACAP and tPA on interneuron migration during post-natal development of the cerebellum. J Neurochem 130:241–254

    Article  CAS  PubMed  Google Scholar 

  • Reinhardt RR, Bondy CA (1994) Insulin-like growth factors cross the blood-brain barrier. Endocrinology 135:1753–1761

    Article  CAS  PubMed  Google Scholar 

  • Renaud J, Chédotal A (2014) Time-lapse analysis of tangential migration in Sema6A and PlexinA2 knockouts. Mol Cell Neurosci 63:49–59

    Article  CAS  PubMed  Google Scholar 

  • Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935–941

    Article  CAS  PubMed  Google Scholar 

  • Riley EP, McGee CL (2005) Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp Biol Med 230:357–365

    Article  CAS  Google Scholar 

  • Roman O, Seres J, Herichova I, Zeman M, Jurcovicova J (2003) Daily profiles of plasma prolactin (PRL), growth hormone (GH), insulin-like growth factor-1 (IGF-1), luteinizing hormone (LH), testosterone, and melatonin, and of pituitary PRL mRNA and GH mRNA in male Long Evans rats in acute phase of adjuvant arthritis. Chronobiol Int 20:823–836

    Article  CAS  PubMed  Google Scholar 

  • Rossi D, Slater TN (1993) The developmental onset of NMDA receptor channel activity during neuronal migration. Neuropharmacology 32:1239–1248

    Article  CAS  PubMed  Google Scholar 

  • Rossi P, Filippi GD, Armano S, Taglietti V, D’Angelo E (1998) The weaver mutation causes a loss of inward rectifier current regulation in premigratory granule cells of the mouse cerebellum. J Neurosci 18:3537–3547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rozenboim I, El Halawani ME, Kashash Y, Piestun Y, Halevy O (2013) The effect of monochromatic photostimulation on growth and development of broiler birds. Gen Comp Endocrinol 190:214–219

    Article  CAS  PubMed  Google Scholar 

  • Ryan KE, Kim PS, Fleming JT, Brignola E, Cheng FY et al (2017) Lkb1 regulates granule cell migration and cortical folding of the cerebellar cortex. Dev Biol 432:165–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Ortiz E, Cho W, Nazarenko I, Mo W, Chen J et al (2014) NF1 regulation of RAS/ERK signaling is required for appropriate granule neuron progenitor expansion and migration in cerebellar development. Genes Dev 28:2407–2420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sato M, Suzuki K, Yamazaki H, Nakanishi S (2005) A pivotal role of calcineurin signaling in development and maturation of postnatal cerebellar granule cells. Proc Natl Acad Sci USA 102:5874–5879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato M, Suzuki K, Nakanishi S (2006) Expression profile of BDNF-responsive genes during cerebellar granule cell development. Biochem Biophys Res Commun 341:304–309

    Article  CAS  PubMed  Google Scholar 

  • Schiller S, Rosewich H, Grünewald S, Gärtner J (2019) Inborn errors of metabolism leading to neuronal migration defects. J Inherit Metab Dis 2019:1–11

    Google Scholar 

  • Schindler M, Humphrey PPA, Emson PC (1996) Somatostatin receptors in the central nervous system. Prog Neurobiol 50:9–47

    Article  CAS  PubMed  Google Scholar 

  • Schmid RS, Maness PF (2008) L1 and NCAM adhesion molecules as signaling coreceptors in neuronal migration and process outgrowth. Curr Opin Neurobiol 18:245–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sidman RL, Rakic P (1973) Neuronal migration with special reference to developing human brain: a review. Brain Res 62:1–35

    Article  CAS  PubMed  Google Scholar 

  • Sirois JE, Atchison WD (2000) Methylmercury affects multiple subtypes of calcium channels in rat cerebellar granule cells. Toxicol Appl Pharmacol 167:1–11

    Article  CAS  PubMed  Google Scholar 

  • Snyder RD (1971) Congenital mercury poisoning. N Engl J Med 284:1014–1016

    Article  CAS  PubMed  Google Scholar 

  • Sokol RJ, Delaney-Black V, Nordstrom B (2003) Fetal alcohol spectrum disorder. JAMA 290:2996–2999

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Kasagi S, Murakami N, Furufuji S, Kikuchi S, Mizusawa K, Andoh T (2016) Chronic effects of light irradiated from LED on the growth performance and endocrine properties of barfin flounder Verasper moseri. Gen Comp Endocrinol 232:101–108

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi T, Morikawa N, Matsumoto H, Shiraishi Y (1962) A pathological study of Minamata disease in Japan. Acta Neuropathol 2:40–57

    Article  Google Scholar 

  • Thoss VS, Duc D, Hoyer D (1996) Somatostatin receptors in the developing rat brain. Eur J Pharmacol 297:145–155

    Article  CAS  PubMed  Google Scholar 

  • Torres-Aleman I (2010) Toward a comprehensive neurobiology of IGF-I. Dev Neurobiol 70:384–396

    CAS  PubMed  Google Scholar 

  • Trivedi N, Ramahi JS, Karakaya M, Howell D, Kerekes RA, Solecki DJ (2014) Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons. Neural Dev 9:26

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Trivedi N, Stabley DR, Cain B, Howell D, Laumonnerie C et al (2017) Drebrin-mediated microtubule–actomyosin coupling steers cerebellar granule neuron nucleokinesis and migration pathway selection. Nat Commun 8:14484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umeshima H, Kengaku M (2013) Differential roles of cyclin-dependent kinase 5 in tangential and radial migration of cerebellar granule cells. Mol Cell Neurosci 52:62–72

    Article  CAS  PubMed  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 

  • Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Foumier A, Chow BK, Hashimoto H, Galas L, Vaudry H (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61:283–357

    Article  CAS  PubMed  Google Scholar 

  • Viollet C, Bodenant C, Prunotto C, Roosterman D, Schaefer J, Meyerhof W, Epelbaum J, Vaudry H, Leroux P (1997) Differential expression of multiple somatostatin receptors in the rat cerebellum during development. J Neurochem 68:2263–2272

    Article  CAS  PubMed  Google Scholar 

  • Walker DM, Gore AC (2017) Epigenetic impacts of endocrine disruptors in the brain. Front Neuroendocrinol 44:1–26

    Article  CAS  PubMed  Google Scholar 

  • Welch-Carre E (2005) The neurodevelopmental consequences of prenatal alcohol exposure. Adv Neonatal Care 5:217–229

    Article  PubMed  Google Scholar 

  • Yacubova E, Komuro H (2002a) Intrinsic program for migration of cerebellar granule cells in vitro. J Neurosci 22:5966–5981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yacubova E, Komuro H (2002b) Stage-specific control of neuronal migration by somatostatin. Nature 415:77–81

    Article  CAS  PubMed  Google Scholar 

  • Yacubova E, Komuro H (2003) Cellular and molecular mechanisms of cerebellar granule cell migration. Cell Biochem Biophys 37:213–234

    Article  PubMed  Google Scholar 

  • Yang YF, Jin SF, Zhong ZT, Yu YH, Yang B, Yuan HB, Pan JM (2015) Growth responses of broiler chickens to different periods of artificial light. J Anim Sci 93:767–775

    Article  CAS  PubMed  Google Scholar 

  • Yong Y, Meng Y, Ding H, Fan Z, Tang Yet al. (2015) PACT/RAX regulates the migration of cerebellar granule neurons in the developing cerebellum. Sci Rep 5:7961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Atchison WD (2005) Methylmercury induces a spontaneous, transient slow inward chloride current in Purkinje cells of rat cerebellar slices. J Pharmacol Exp Ther 313:751–764

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Song L, Chang Y, Wu M, Kuang X et al (2017) Potential deficit from decreased cerebellar granule cell migration in serine racemase-deficient mice is reversed by increased expression of GluN2B and elevated levels of NMDAR agonists. Mol Cell Neurosci 85:119–126

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yutaro Komuro .

Editor information

Editors and Affiliations

Section Editor information

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Komuro, Y. et al. (2020). Granule Cell Migration and Differentiation. In: Manto, M., Gruol, D., Schmahmann, J., Koibuchi, N., Sillitoe, R. (eds) Handbook of the Cerebellum and Cerebellar Disorders. Springer, Cham. https://doi.org/10.1007/978-3-319-97911-3_7-2

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-97911-3_7-2

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-97911-3

  • Online ISBN: 978-3-319-97911-3

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics