Reelin glycoprotein: structure, biology and roles in health and disease (original) (raw)
DeSilva U, D'Arcangelo G, Braden VY, Chen J, Miso GG, Curran T et al. The human reelin gene: isolation, sequencing, and mapping on chromosome 7. Genome Res 1997; 7: 157–164. ArticleCASPubMed Google Scholar
Ogawa M, Miyata T, Nakajima K, Yoguy K, Seiko M, Ikenaka K et al. The reeler gene-associated antigen on Cajal–Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 1995; 14: 890–912. Article Google Scholar
D'Arcangelo G, Miao GG, Chon S-C, Soares HD, Morgan JI, Curran T . A protein related to extracellular matrix proteins detected in the mouse mutant reeler. Nature 1995; 374: 719–723. ArticleCASPubMed Google Scholar
Smallheiser NR, Costa E, Guidotti A, Impagnatiello F, Auta J, Lacor P et al. Expression of reelin in adult mammalian blood, liver, pituitary pars intermedia, and adrenal chromaffin cells. Proc Natl Acad Sci USA 2000; 97: 1281–1286. Article Google Scholar
Fatemi SH, Stary JM, Egan EA . Reduced blood levels of reelin as a vulnerability factor in pathophysiology of autistic disorder. Cell Mol Neurobiol 2002; 22: 139–152. ArticleCASPubMed Google Scholar
Lugli G, Krueger JM, Davis JM, Perico AM, Keller F, Smalheiser NR . Methodological factors influencing measurement and processing of plasma reelin in humans. BMC Biochem 2003; 4: 9. ArticlePubMedPubMed Central Google Scholar
Ignatova N, Sindic CJM, Goffinet AM . Characterization of the various farms of the Reelin protein in the cerebrospinal fluid of normal subjects and in neurological diseases. Neurobiol Dis 2004; 15: 326–330. ArticleCASPubMed Google Scholar
Quattrocchi CC, Wannenes F, Persico AM, Ciafre SA, D'Arcangelo G, Farace MG et al. Reelin is a serine protease of the extracellular matrix. J Biol Chem 2002; 277: 303–309. ArticleCASPubMed Google Scholar
DeBergeyck V, Naerhuyzen B, Goffinet AM, deRouvroit C . A panel of monoclonal antibodies against Reelin, the extracellular matrix protein defective in reeler mutant mice. J Neurosci Meth 1998; 82: 17–24. ArticleCAS Google Scholar
D'Arcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T . Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J Neurosci 1997; 17: 23–31. ArticleCASPubMedPubMed Central Google Scholar
Utsunomiya-Tate N, Kubo KI, Tate S-C, Kainosho M, Katayama E, Nakajima K et al. Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody. Proc Natl Acad Sci USA 2000; 97: 9729–9734. ArticleCASPubMedPubMed Central Google Scholar
D'Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T . Reelin is a ligand for lipoprotein receptors. Neuron 1999; 24: 471–479. ArticleCASPubMed Google Scholar
Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA et al. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 1999; 24: 481–489. ArticleCASPubMed Google Scholar
Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA et al. Reelin binds alpha 3 beta 1 integrin and inhibits neuronal migration. Neuron 2000; 27: 33–44. ArticleCASPubMed Google Scholar
Strasser V, Fasching D, Hauser C, Mayer H, Bock HH, Hiesberger T et al. Receptor clustering is involved in reelin signaling. Mol Cell Biol 2004; 24: 1378–1386. ArticleCASPubMedPubMed Central Google Scholar
Cooper J, Howell BW . Lipoprotein receptors: signaling function in the brain? Cell 1999; 97: 671–674. ArticleCASPubMed Google Scholar
Pesold C, Impagnatiello F, Pisu MG, Uzunov DP, Costa E, Guidotti A et al. Reelin is preferentially expressed in neurons synthesizing gamma-ambiobutyric acid in cortex and hippocampus of adult rats. Proc Natl Acad Sci USA 1990; 95: 3221–3226. Article Google Scholar
Fatemi SH, Emamian ES, Kist D, Sidwell RW, Nakajima K, Akhter P et al. Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol Psychiatry 1999; 4: 145–154. ArticleCASPubMed Google Scholar
Rodriguez MA, Pesold C, Liu WS, Kribo V, Guidotti A, Pappas GD et al. Colocalization of integrin receptors and reelin in dendritic spine post-synaptic densities of adult non-human primate cortex. Proc Natl Acad Sci USA 2000; 97: 3550–3555. ArticleCASPubMedPubMed Central Google Scholar
de Rouvroit CL, deBergeyck V, Cortvrindt C, Bar I, Eeckhout Y, Goffinet AM . Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Exp Neurol 1999; 156: 214–217. Article Google Scholar
Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert de Rouvroit C, Goffinet AM . The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 2004; 24: 514–521. ArticleCASPubMedPubMed Central Google Scholar
Keshvara L, Benhayon D, Magdaleno S, Curran T . Identification of Reelin-induced sites of tyrosyl phosphorylation on disabled-1. J Biol Chem 2001; 276: 16008–16014. ArticleCASPubMed Google Scholar
Beffert U, Morfini G, Bock HH, Reyna H, Brady ST, Herz J . Reelin-mediated signalling locally regulates protein kinase B/Akt and glycogen synthase kinase 3_β_. J Biol Chem 2002; 51: 49958–49964. Article Google Scholar
Arnaud L, Ballif BA, Forster E, Cooper JA . Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr Biol 2003; 13: 9–17. ArticleCASPubMed Google Scholar
Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME . Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995; 270: 1326–1331. ArticleCASPubMed Google Scholar
Kuan CY, Yang DO, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA . The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 1999; 22: 667–676. ArticleCASPubMed Google Scholar
Arnaud L, Ballif BA, Cooper JA . Regulation of protein tyrosine kinase signalling by substrate degradation during brain development. Mol Cell Biol 2003; 23: 9293–9302. ArticleCASPubMedPubMed Central Google Scholar
Suetsugu S, Tezuka T, Morimura T, Hattori M, Mikoshiba K, Yamamoto T et al. Regulation of actin cytoskeleton by mDab1 through N-WASP and ubiquitination of mDab1. Biochem J 2004 in press.
Miki H, Sasaki T, Takai Y, Takenawa T . Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 1998; 391: 93–96. ArticleCASPubMed Google Scholar
Welch MD, Iwamatsu A, Mitchison TJ . Actin polymerization is induced by Arp 2/3 protein complex at the surface of Listeria monocytogenes. Nature 1997; 385: 265–269. ArticleCASPubMed Google Scholar
Duan L, Reddi AL, Ghosh A, Dimri M, Band H . The Cbl family and other ubiquitin ligases: destructive forces in control of antigen receptor signalling. Immunity 2004; 21: 7–17. ArticleCASPubMed Google Scholar
Goffinet AM . An early developmental defect in the cerebral cortex of the Reeler mouse. Anat Embryol 1979; 157: 205–218. ArticleCAS Google Scholar
Goffinet AM . Events governing organization of postmigratory neurons: studies on brain development in normal and reeler mice. Brain Res 1984; 319: 261–296. ArticleCASPubMed Google Scholar
Falconer DS . Two new mutants, Trembler and ‘Reeler’, with neurological actions in the house mouse. J Genet 1951; 50: 182–201. Google Scholar
Goffinet AM . The reeler gene: a clue to brain development and evolution. Int J Dev Biol 1992; 36: 101–107. CASPubMed Google Scholar
Magdaleno S, Keshvara L, Curran T . Rescue of ataxia and prepalte splitting by ectopic expression of Reelin in reeler mice. Neuron 2002; 33: 573–586. ArticleCASPubMed Google Scholar
Hadj-Sahraoui N, Frederic F, Delhaye-Bouchaud N, Mariani J . Gender effect on purkinje cell loss in the cerebellum of the heterozygous reeler mouse. J Neurogenet 1996; 11: 45–58. ArticleCASPubMed Google Scholar
Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J et al. Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 1999; 97: 689–701. ArticleCASPubMed Google Scholar
Fatemi SH . Reelin mutations in mouse and man: from reeler mouse to schizophrenia, mood disorders, autism and lissencephaly. Mol Psychiatry 2001; 6: 129–133. ArticleCASPubMed Google Scholar
Tueting P, Costa E, Dwivedi Y, Guidotti A, Impagnatiello F, Manev R et al. The phenotypic characteristics of heterozygous reeler mouse. NeuroReport 1999; 10: 1327–1334. Article Google Scholar
Janusonis S, Gluncic V, Rakic P . Early serotonergic projections to Cajal-Retzius cells: Relevance for cortical development. J Neurosci 2004; 24: 1652–1659. ArticleCASPubMedPubMed Central Google Scholar
Carboni G, Tueting P, Tremolizzo L, Sugaya I, Davis J, Costa E et al. Enhanced dizocilpine efficacy in heterozygous reeler mice relates to GABA turnover downregulation. Neuropharmacology 2004; 46: 1070–1081. ArticleCASPubMed Google Scholar
Meincke U, Light GA, Geyer MA, Braff DL, Gouzoulis-Mayfrank E . Sensitization and habituation of the acoustic startle reflex in patients with schizophrenia. Psychiatry Res 2004; 126: 51–61. ArticlePubMed Google Scholar
McAlonan GM, Daly E, Kumari V, Critchley HD, van Amelsvoort T, Suckling J et al. Brain anatomy and sensorimotor gating in Asperger's syndrome. Brain 2002; 125: 1594–1606. ArticlePubMed Google Scholar
Shi L, Fatemi SH, Sidewell RW, Patterson PH . Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 2003; 23: 297–302. ArticlePubMedPubMed Central Google Scholar
Perez-Costas E, Melendez-Ferro M, Perez-Garcia CG, Caruncho HJ, Rodicio MC . Reelin immunoreactivity in the larval sea lamprey brain. J Chem Neuroanat 2004; 23: 211–221. Article Google Scholar
Absil P, Pinxten R, Balthazart J, Eens M . Effects of testosterone on Reelin expression in the brain of male European starlings. Cell Tissue Res 2003; 312: 81–98. CASPubMed Google Scholar
Ikeda Y, Terashima T . Expression of Reelin, the gene responsible for the reeler mutation, in embryonic development and adulthood in the mouse. Dev Dyn 1997; 210: 157–172. ArticleCASPubMed Google Scholar
Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG et al. A decrease of Reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci USA 1998; 95: 15718–15723. ArticleCASPubMedPubMed Central Google Scholar
Lacor P, Grayson DR, Auto J, Sugaya I, Costa E, Guidotti A . Reelin secretion from glutamatergic neurons in culture is independent from neurotransmitter regulation. Proc Natl Acad Sci USA 2000; 97: 3556–3561. ArticleCASPubMedPubMed Central Google Scholar
Fatemi SH, Earle JA, McMenomy T . Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiatry 2000; 5: 654–663. ArticleCASPubMed Google Scholar
Abraham H, Meyer G . Reelin-expressing neurons in the postnatal and adult human hippocampal formation. Hippocampus 2003; 13: 715–727. ArticleCASPubMed Google Scholar
Deguchi K, Inoue K, Avila WE, Lopez-Terrada D, Antalffy BA, Quattrocchi CC et al. Reelin and disabled-1 expression in developing and mature human cortical neurons. J Neuropathol Exp Neurol 2003; 62: 676–684. ArticleCASPubMed Google Scholar
Forster E, Tielsch A, Saum B, Weiss KH, Johanssen C, Graus-Porta D et al. Reelin, disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci USA 2002; 99: 13178–13183. ArticleCASPubMedPubMed Central Google Scholar
Luque JM, Morante-Oria J, Fairen A . Localization of ApoER2, VLDLR and Dab-1 in radial glia: groundwork for a new model of Reelin action during cortical development. Dev Brain Res 2003; 140: 195–203. ArticleCAS Google Scholar
Weeber EJ, Beffert U, Jones C, Christian JM, Forster E, Sweatt JD et al. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 2002; 277: 39944–39952. ArticleCASPubMed Google Scholar
Curristin SM, Cao A, Stewart WB, Zhang H, Madri JA, Morrow JS et al. Disrupted synaptic development in the hypoxic newborn brain. Proc Natl Acad Sci USA 2002; 99: 16729–16734. ArticleCAS Google Scholar
Guidotti AR, Auta J, Davis J, Dwivedi Y, Grayson D, Impagnatiello F et al. Decrease in Reelin and glutamic acid decarboxylase 67 (GAD 67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 2000; 57: 1061–1069. ArticleCASPubMed Google Scholar
Fatemi SH, Stary JM, Araghi-Niknam M, Egan E . Gabaergicd dysfunction in schizophrenia and mood disorders as reflected by decreased levels of Reelin and GAD 65 & 67 kDa proteins in cerebellum. Schizophr Res 2004 in press.
Eastwood SL, Law AJ, Everall IP, Harrison PJ . The axonal chemorepellant semaphorin 3A is increased in the cerebellum in schizophrenia and may contribute to its synaptic pathology. Mol Psychiatry 2003; 8: 148–155. ArticleCASPubMed Google Scholar
Eastwood SL, Harrison PJ . Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis. Mol Psychiatry 2003; 8: 821–831. ArticleCAS Google Scholar
Knable MB, Barci BM, Webster MJ, Meador-Woodruff J, Torrey EF . Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol Psychiatry 2004; 9: 609–620, 544. ArticleCASPubMed Google Scholar
Costa E, Grayson DR, Guidotti A . Epigenetic downregulation of GABAergic function in schizophrenia; potential for pharmacological intervention? Mol Intervent 2003; 3: 220–229. ArticleCAS Google Scholar
Abdolmaleky HM, Smith CL, Farone SV, Shafa R, Stone W, Glatt SJ et al. Methylomics in psychiatry: modulation of gene–environment interactions may be through DNA methylation. Am J Med Genet 2004; 127B: 51–59. ArticlePubMed Google Scholar
Costa E, Grayson DR, Mitchell CP, Tremolizzo L, Veldic M, Guidotti A . GABAertic cortical neuron chromatin as a putative target to treat schizophrenia vulnerability. Crit Rev Neurobiol 2003; 15: 121–142. ArticleCASPubMed Google Scholar
Veldic M, Caruncho HJ, Liu WS, Davis J, Satta R, Grayson DR et al. DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proc Natl Acad Sci USA 2004; 101: 348–353. ArticleCASPubMed Google Scholar
Akahane A, Kunugi H, Tanaka H, Nanko S . Association analysis of polymorphic CGG repeat in 5′ UTR of the reelin and VLDLR genes with schizophrenia. Schizophr Res 2002; 58: 37–41. ArticlePubMed Google Scholar
Chen M-I, Chen S-Y, Huang C-H, Chen C-H . Identification of a single nucleotide polymorphism at the 5′ promoter region of human reelin gene and association study with schizophrenia. Mol Psychiatry 2002; 7: 447–448. ArticleCASPubMed Google Scholar
Fatemi SH, Snow AV, Stary JM . Reelin glycoprotein is reduced in cerebellum and areas 9 & 40 of autistic brains. Biol Psychiatry 2004; 55: 806. Google Scholar
Persico AM, D'Agruma L, Maiorano N, Totaro A, Militerni R, Bravaccio C et al. Collaborative Linkage Study of Autism (2001): reelin gene alleles and haplotypes as a factor predisposing to autistic disorder. Mol Psychiatry 2001; 6: 150–159. ArticleCASPubMed Google Scholar
Zhang H, Liu X, Zhang C, Mundo E, Macciardi F, Grayson DR et al. Reelin gene alleles and susceptibility for autism spectrum disorders. Mol Psychiatry 2002; 7: 1012–1017. ArticleCASPubMed Google Scholar
Krebs MO, Betancur C, Leroy S, Bourdel MC, Gillberg C, Leboyer M . Paris Autism Research International Sibpair (PARIS) study et al. Absence of association between a polymorphic GGC repeat in the 5′ untranslated region of the reelin gene and autism. Mol Psychiatry 2002; 7: 801–804. ArticleCASPubMedPubMed Central Google Scholar
Bonora E, Beyer KS, Lamb JA, Parr JR, Klauck SM, International Molecular Genetic Study of Autism (IMGSAC) et al. Analysis of reelin as a candidate gene for autism. Mol Psychiatry 2003; 10: 885–892. ArticleCAS Google Scholar
Devlin B, Bennett P, Dawson G, Figlewicz DA, Grigorenko EL, CPEA Genetics Network et al. Alleles of a reelin CGG repeat do not convey liability to autism in a sample from the CPEA network. Am J Med Genet 2004; 126B: 46–50. ArticlePubMed Google Scholar
Li J, Nguyen L, Gleason C, Lotspeich L, Spiker D, Risch N et al. Lack of evidence for an association between WNT2 and RELN polymorphisms and autism. Am J Med Genet 2004; 126B: 51–57. ArticlePubMed Google Scholar
Hong SE, Shugart YY, Huang DT, Shahwan SA, Grant PE, Hourihane JOB et al. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 2000; 26: 93–96. ArticleCASPubMed Google Scholar
Assadi AH, Zhang G, Beffert U, McNeil RS, Renfro AL, Niu S et al. Interaction of reelin signaling and Lis1 in brain development. Nat Genet 2003; 35: 270–276. ArticleCASPubMed Google Scholar
Saez-Valero J, Costell M, Sjogren M, Andreasen N, Blennow K, Luque JM . Altered levels of cerebrospinal fluid reelin in frontotemporal dementia and Alzheimer's disease. J Neurosci Res 2003; 72: 132–136. ArticleCASPubMed Google Scholar
Bothwell M, Giniger E . Alzheimer's disease: neurodevelopment converges with neurodegeneration. Cell 2000; 102: 271–273. ArticleCASPubMed Google Scholar
Helbecque N, Amouyel P . Very low density lipoprotein in Alzheimer diseases. Mic Res Tech 2000; 50: 273–277. ArticleCAS Google Scholar
Carrol P, Gayet O, Feuillet C, Kallenbach S, de Bovis B, Dudley K et al. Juxtaposition of CNR protocadherins and reelin expression in the developing spinal cord. Mol Cell Neurosci 2001; 4: 611–623. ArticleCAS Google Scholar
Yip YP, Capriotti C, Magdaleno S, Benhayon D, Curran T, Nakajima K et al. Components of the reelin signaling pathway are expressed in the spinal cord. J Comp Neurol 2004; 470: 210–219. ArticleCASPubMed Google Scholar
Yip YP, Zhou G, Capriotti C, Yip JW . Location of preganglionic neurons is independent of birthdate but is correlated to reelin-producing cells in the spinal cord. J Comp Neurol 2004; 475: 564–574. ArticlePubMed Google Scholar
Myer G, Wahle P . The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the foetal human neocortex. Eur J Neurosci 1999; 11: 3937–3944. Article Google Scholar
Phelps PE, Rich R, Dupuy-Davies S, Rios Y, Wong T . Evidence for a cell-specific action of Reelin in the spinal cord. Dev Biol 2002; 244: 180–198. ArticleCASPubMed Google Scholar
Nishikawa S, Goto S, Hamasaki T, Ogawa M, Ushio Y . Transient and compartmental expression of the reeler gene product reelin in the developing rat striatum. Brain Res 199; 850: 244–248. Article Google Scholar
Kobold D, Grundmann A, Piscaglia F, Eisenbach C, Neubauer K, Steffgen J et al. Expression of reelin in hepatic stellate cells and during hepatic tissue repair; a novel marker for the differentiation of HSC from other liver myofibroblasts. J Hepatol 2002; 36: 607–613. ArticleCASPubMed Google Scholar
Wang Q, Lu J, Yang C, Wang X, Cheeng L, Hu G et al. CASK and its target gene Reelin were co-upregulated in human esophageal carcinoma. Cancer Lett 2002; 179: 71–77. ArticleCASPubMed Google Scholar
Buchaille R, Couble ML, Magloire H, Bleicher F . A substractive PCR-based cDNA library from human odontoblast cells: identification of novel genes expressed in tooth forming cells. Matrix Biol 2000; 19: 421–430. ArticleCASPubMed Google Scholar
Heymann R, Kallenbach S, Alonso S, Carroll P, Mitsiadis TA . Dynamic expression patterns of the new protocadherin families CNRs and Podh-gamma during mouse odontogenesis: comparison with reelin expression. Mech Dev 2001; 106: 181–184. ArticleCASPubMed Google Scholar
Underhill GH, George D, Bremer EG, Kansas GS . Gene expression profiling reveals a highly specialized genetic program of plasma cells. Blood 2003; 101: 4013–4021. ArticleCASPubMed Google Scholar