Absence of layer-specific cadherin expression profiles in the neocortex of the reeler mutant mouse

Cerebral Cortex

Volumn 21, Issue 5, 2011, Pages 1105-1117

  Hertel, Nicole ^a   Redies, Christoph ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

adhesion molecules; corticogenesis; layer formation; neocortex; Reelin

Indexed keywords

CADHERIN; CADHERIN 4; CADHERIN 6; CADHERIN 7; CADHERIN 8; CELL SURFACE PROTEIN; MESSENGER RNA; P CADHERIN 11; P CADHERIN 17; P CADHERIN 19; P CADHERIN 8; P CADHERIN 9; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CINGULATE GYRUS; CONTROLLED STUDY; EMBRYO; GLIA CELL; MOTOR CORTEX; MOUSE; NEOCORTEX; NEUROBLAST; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; BODY PATTERNING; CADHERINS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, NEUROLOGIC MUTANTS; NEOCORTEX; NERVOUS SYSTEM MALFORMATIONS; NEUROGENESIS; NEURONS; ORGANOGENESIS;

EID: 79954622977     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq183     Document Type: Article

References (87)

1. Angevine JB, Sidman RL. 1961. Autoradiography study of cell migration during histogenesis of cerebral cortex in the mouse. Nature. 192:766-768.
2. Arber S, Ladle D, Lin J, Frank E, Jessell TM. 2000. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell. 101:485-498.
3. Bekirov IH, Needleman LA, Zhang W, Benson DL. 2002. Identification and localization of multiple classic cadherins in developing rat limbic system. Neuroscience. 115:213-227. (Pubitemid 35238054)
4. Bishop KM, Goudreau G, O'Leary DD. 2000. Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science. 288:344-349. (Pubitemid 30226197)
5. Bulfone A, Smiga SM, Shimamura K, Peterson A, Puelles L, Rubenstein JL. 1995. T-brain-1: a homolog ofBrachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron. 15:63-78.
6. Caviness VS. 1982. Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res. 256:293-302.
7. Caviness VS, Sidman RL. 1973. Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis.J Comp Neurol. 148:141-151.
8. Chung WW, Lagenaur CF, Yan YM, Lund JS. 1991. Developmental expression of neural cell adhesion molecules in the mouse neocortex and olfactory bulb. J Comp Neurol. 314:290-305.
9. DArcangelo G. 2006. Reelin mouse mutants as models of cortical development disorders. Epilepsy Behav. 8:81-90.
10. DArcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T. 1995. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature. 374:719-723.
11. DArcangelo G, Miao GG, Curran T. 1996. Detection of the reelin breakpoint in reeler mice. Brain Res Mol Brain Res. 39:234-236. (Pubitemid 26179163)
12. DArcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T. 1997. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J Neurosci. 17:23-31. (Pubitemid 27008847)
13. Dekimoto H, Terashima T, Katsuyama Y. 2010. Dispersion of the neurons expressing layer specific markers in the reeler brain. Dev Growth Differ. 52:181-193.
14. Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES. 2000. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron. 27:33-44.
15. Etzrodt J, Krishna-K, Redies C. 2009. Expression of classic cadherins and delta-protocadherins in the developing ferret retina. BMC Neurosci. 10:153.
16. Faulkner-Jones BE, Godinho LN, Tan SS. 1999. Multiple cadherin mRNA expression and developmental regulation of a novel cadherin in the developing mouse eye. Exp Neurol. 156:316-325. (Pubitemid 29205006)
17. Ferrere A, Vitalis T, Gingras H, Gaspar P, Cases O. 2006. Expression of Cux-1 and Cux-2 in the developing somatosensory cortex of normal and barrel-defective mice. Anat Rec A Discov Mol Cell Evol Biol. 288:158-165. (Pubitemid 43208626)
18. Frotscher M, Chai X, Bock HH, Haas CA, Forster E, Zhao S. 2009. Role of Reelin in the development and maintenance of cortical lamination. J Neural Transm. 116:1451-1455.
19. Gaitan Y, Bouchard M. 2006. Expression of the delta-protocadherin gene Pcdh19 in the developing mouse embryo. Gene Expr Patterns. 6:893-899 (Pubitemid 44309440)
20. Gil OD, Needleman L, Huntley GW. 2002. Developmental patterns of cadherin expression and localization in relation to compartmentalized thalamocortical terminations in rat barrel cortex. J Comp Neurol. 453:372-388. (Pubitemid 35231189)
21. Godfraind C, Schachner M, Goffinet AM. 1988. Immunohistological localization of cell adhesion molecules L1, J1, N-CAM and their common carbohydrate L2 in the embryonic cortex of normal and reeler mice. Brain Res. 470:99-111.
22. Hack I, Hellwig S, Junghans D, Brunne B, Bock HH, Zhao S, Frotscher M. 2007. Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development. 134:3883-3891. (Pubitemid 350187347)
23. Hamburgh M. 1963. Analysis of the postnatal developmental effects of reeler, a neurological mutation in mice. A study in developmental genetics. Dev Biol. 8:165-185.
24. Hartfuss E, Forster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Gotz M. 2003. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development. 130:4597-4609. (Pubitemid 37279413)
25. Hertel N, Krishna-K, Nuernberger M, Redies C. 2008. A cadherin-based code for the divisions of the mouse basal ganglia. J Comp Neurol. 508:511-528. (Pubitemid 351656382)
26. Hevner RF, Daza RAM, Rubenstein JLR, Stunnenberg H, Olavarria JF, Englund C. 2003. Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci. 25:139-151. (Pubitemid 37100209)
27. Heyers D, Kovjanic D, Redies C. 2003. Cadherin expression coincides with birth dating patterns in patchy compartments of the developing chicken telencephalon. J Comp Neurol. 460:155-166. (Pubitemid 36512927)
28. Hirano S, Suzuki ST, Redies C. 2003. The cadherin superfamily in neural development: diversity, function and interaction with other molecules. Front Biosci. 8:306-355.
29. Hirano S, Yan Q, Suzuki ST. 1999. Expression of a novel protocadherin, OL-protocadherin, in a subset of functional systems of the developing mouse brain. J Neurosci. 19:995-1005. (Pubitemid 29066162)
30. Hoerder-Suabedissen A, Wang WZ, Lee S, Davies KE, Goffinet AM, Rakic S, Parnavelas J, Reim K, Nicolic M, Paulsen O, et al. 2009. Novel markers reveal subpopulations of subplate neurons in the murine cerebral cortex. Cereb Cortex. 19:1738-1750.
31. Honjo M, Tanihara H, Suzuki S, Tanaka T, Honda Y, Takeichi M. 2000. Differential expression of cadherin adhesion receptors in neural retina of the postnatal mouse. Invest Ophthalmol Vis Sci. 41:546-551. (Pubitemid 30080460)
32. Ichinohe N, Knight A, Ogawa M, Ohshima T, Mikoshiba K, Yoshihara Y, Terashima T, Rockland KS. 2008. Unusual patchmatrix organization in the retrosplenial cortex of the reeler mouse and shaking rat Kawasaki. Cereb Cortex. 18:1125-1138.
33. Inoue T, Chisaka O, Matsunami H, Takeichi M. 1997. Cadherin-6 expression transiently delineates specific rhombomeres, other neural tube subdivisions, and neural crest subpopulations in mouse embryos. Dev Biol. 183:183-194. (Pubitemid 27148646)
34. Inoue A, Sanes JR. 1997. Lamina-specific connectivity in the brain: regulation by N-cadherin, neurotrophins, and glycoconjugates. Science. 276:1428-1431. (Pubitemid 27235414)
35. Inoue K, Terashima T, Nishikawa T, Takumi T. 2004. Fez1 is layerspecifically expressed in the adult mouse neocortex. Eur J Neurosci. 20:2909-2916. (Pubitemid 40007285)
36. Ju MJ, Aroca P, Luo J, Puelles L, Redies C. 2004. Molecular profiling indicates avian branchiomotor nuclei invade the hindbrain alar plate. Neuroscience. 128:785-796. (Pubitemid 39298431)
37. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, et al. 2005. Antisense transcription in the mammalian transcriptome. Science. 309:1564-1566.
38. Katsuyama Y, Terashima T. 2009. Developmental anatomy of reeler mutant mouse. Dev Growth Differ. 51:271-286.
39. Kim SY, Chung HS, Sun W, Kim H. 2007. Spatiotemporal expression pattern of non-clustered protocadherin family members in the developing rat brain. Neuroscience. 147:996-1021. (Pubitemid 47102539)
40. Kojima T, Nakajima K, Mikoshiba K. 2000. The disabled 1 gene is disrupted by a replacement with L1 fragment in yotari mice. Brain Res Mol Brain Res. 75:121-127. (Pubitemid 30058333)
41. Korematsu K, Redies C. 1997a. Expression of cadherin-8 mRNA in the developing mouse central nervous system. J Comp Neurol. 387:291-306. (Pubitemid 27430352)
42. Korematsu K, Redies C. 1997b. Restricted expression of cadherin-8 in segmental and functional subdivisions of the embryonic mouse brain. Dev Dyn. 208:178-189. (Pubitemid 27068873)
43. Krishna-K, Nuernberger M, Weth F, Redies C. 2009. Layer-specific expression of multiple cadherins in the developing visual cortex (V1) ofthe ferret. Cereb Cortex. 19:388-401.
44. Krushel LA, van der Kooy D. 1993. Pattern formation in the developing mammalian forebrain: selective adhesion of early but not late postmitotic cortical and striatal neurons within forebrain reaggregate cultures. Dev Biol. 158:145-162. (Pubitemid 23222721)
45. Kubo K, Nakajima K. 2003. Cell and molecular mechanisms that control cortical layer formation in the brain. Keio J Med. 52:8-20. (Pubitemid 36460530)
46. Lambert de Rouvroit C, Goffinet AM. 1998. The reeler mouse as a model ofbrain development. Adv Anat Embryol Cell Biol. 150:1-106.
47. Luo J, Treubert-Zimmermann U, Redies C. 2004. Cadherins guide migrating Purkinje cells to specific parasagittal domains during cerebellar development. Mol Cell Neurosci. 25:138-152. (Pubitemid 38220870)
48. Marin O, Rubenstein JL. 2003. Cell migration in the forebrain. Annu Rev Neurosci. 26:441-483. (Pubitemid 37064941)
49. Matsunami H, Miyatani S, Inoue T, Copeland NG, Gilbert DJ, Jenkins NA, Takeichi M. 1993. Cell binding specificity of mouse R-cadherin and chromosomal mapping of the gene. J Cell Sci. 106:401-409. (Pubitemid 23286810)
50. Miyashita-Lin EM, Hevner R, Wassarman KM, Martinez S, Rubenstein JL. 1999. Early neocortical regionalization in the absence of thalamic innervation. Science. 285:906-909 (Pubitemid 29381994)
51. Molnar Z, Adams R, Goffinet AM, Blakemore C. 1998. The role of the first postmitotic cortical cells in the development of thalamocortical innervation in the reeler mouse. J Neurosci. 18:5746-5765. (Pubitemid 28341353)
52. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL. 2001. Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci. 4:143-150. (Pubitemid 32125258)
53. Nakagawa Y, Johnson JE, O'Leary DD. 1999. Graded and areal expression patterns of regulatory genes and cadherins in embryonic neocortex independent of thalamocortical input. J Neurosci. 19:10877-10885. (Pubitemid 30235732)
54. Nern A, Zhu Y, Zipursky SL. 2008. Local N-cadherin interactions mediate distinct steps in the targeting of lamina neurons. Neuron. 58:34-41. (Pubitemid 351467037)
55. Nollet F, Kools P, van Roy F. 2000. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol. 299:551-572.
56. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K. 1995. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization ofcortical neurons. Neuron. 14:899-912.
57. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. 2nd ed. San Diego (CA): Academic Press.
58. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. 4th ed. San Diego (CA): Academic Press.
59. Pinto Lord MC, Caviness VS. 1979. Determinants of cell shape and orientation: a comparative Golgi analysis of cell-axon interrelationships in the developing neocortex of normal and reeler mice. J Comp Neurol. 187:49-69.
60. Polleux F, Dehay C, Goffinet A, Kennedy H. 2001. Pre-and post-mitotic events contribute to the progressive acquisition of area-specific connectional fate in the neocortex. Cereb Cortex. 11:1027-1039. (Pubitemid 33021233)
61. Polleux F, Dehay C, Kennedy H. 1998. Neurogenesis and commitment of corticospinal neurons in reeler. J Neurosci. 18:9910-9923. (Pubitemid 28543767)
62. Quaggin SE, Heuvel GB, Golden K, Bodmer R, Igarashi P. 1996. Primary structure, neural-specific expression, and chromosomal localization of Cux-2, a second murine homeobox gene related to Drosophila cut. J Biol Chem. 271:22624-22634. (Pubitemid 26304704)
63. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol. 145:61-84.
64. Rakic P, Caviness VS. 1995. Cortical development: view from neurological mutants two decades later. Neuron. 14:1101-1104.
65. Redies C. 2000. Cadherins in the central nervous system. Prog Neurobiol. 61:611-648. (Pubitemid 30207058)
66. Redies C, Engelhart K, Takeichi M. 1993. Differential expression of Nand R-cadherin in functional neuronal systems and other structures of the developing chicken brain. J Comp Neurol. 333:398-416. (Pubitemid 23187535)
67. Redies C, Kovjanic D, Heyers D, Medina L, Hirano S, Suzuki ST, Puelles L. 2002. Patch/matrix patterns of gray matter differentiation in the telencephalon of chicken and mouse. Brain Res Bull. 57:489-493. (Pubitemid 34234913)
68. Redies C, Takeichi M. 1993. Expression of N-cadherin mRNA during development of the mouse brain. Dev Dyn. 197:26-39. (Pubitemid 23254780)
69. Redies C, Vanhalst K, Roy F. 2005. Delta-protocadherins: unique structures and functions. Cell Mol Life Sci. 62:2840-2852.
70. Rice DS, Curran T. 2001. Role ofthe reelin signalling pathway in central nervous system development. Annu Rev Neurosci. 24:1005-1039. (Pubitemid 32695252)
71. Rubenstein JL, Anderson S, Shi L, Miyashita-Lin E, Bulfone A, Hevner R. 1999. Genetic control of cortical regionalization and connectivity. Cereb Cortex. 9:524-532. (Pubitemid 29441493)
72. Schaefer A, Poluch S, Juliano S. 2008. Reelin is essential for neuronal migration but not for radial glia elongation in neonatal ferret cortex. Dev Neurobiol. 68:590-604. (Pubitemid 351466290)
73. Sheldon M, Rice DS, DArcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T. 1997. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature. 389:730-733. (Pubitemid 27458959)
74. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M. 1997. Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci. 9:433-447. (Pubitemid 27467494)
75. Sweet HO, Bronson RT, Johnson KR, Cook SA, Davisson MT. 1996. Scrambler, a new neurological mutation of the mouse with abnormalities of neuronal migration. Mamm Genome. 7:798-802. (Pubitemid 126440452)
76. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS. 1999. Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci. 19:10357-10371. (Pubitemid 30228043)
77. Takeichi M. 2007. The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci. 8:11-20. (Pubitemid 46011995)
78. Taniguchi H, Kawauchi D, Nishida K, Murakami F. 2006. Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain. Development. 133:1923-1931. (Pubitemid 43881258)
79. Tissir F, Goffinet AM. 2003. Reelin and brain development. Nat Rev Neurosci. 4:496-505. (Pubitemid 37280170)
80. Treubert-Zimmermann U, Heyers D, Redies C. 2002. Targeting axons to specific fiber tracts in vivo by altering cadherin expression. J Neurosci. 22:7617-7626. (Pubitemid 35386362)
81. Vanhalst K, Kools P, Staes K, van Roy F, Redies C. 2005. Deltaprotocadherins: a gene family expressed differentially in the mouse brain. Cell Mol Life Sci. 62:1247-1259. (Pubitemid 40880128)
82. Visel A, Carson J, Oldekamp J, Warnecke M, Jakubcakova V, Zhou X, Shaw CA, Alvarez-Bolado G, Eichele G. 2007. Regulatory pathway analysis by high-throughput in situ hybridization. PLoS Genet. 3:1867-1883. (Pubitemid 350072053)
83. Ware ML, Fox JW, Gonzalez JL, Davis NM, Lambert de Rouvroit C, Russo CJ, Chua SC, Goffinet AM, Walsh CA. 1997. Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron. 19:239-249. (Pubitemid 27374225)
84. Wohrn JC, Nakagawa S, Ast M, Takeichi M, Redies C. 1999. Combinatorial expression of cadherins in the tectum and the sorting of neurites in the tectofugal pathways of the chicken embryo. Neuroscience. 90:985-1000. (Pubitemid 29156763)
85. Wohrn JC, Puelles L, Nakagawa S, Takeichi M, Redies C. 1998. Cadherin expression in the retina and retinofugal pathways of the chicken embryo. J Comp Neurol. 396:20-38. (Pubitemid 28242449)
86. Yoneshima H, Nagata E, Matsumoto M, Yamada M, Nakajima K, Miyata T, Ogawa M, Mikoshiba K. 1997. A novel neurological mutant mouse, yotari, which exhibits reeler-like phenotype but expresses CR-50 antigen/reelin. Neurosci Res. 29:217-223. (Pubitemid 27520821)
87. Zimmer C, Tiveron MC, Bodmer R, Cremer H. 2004. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex. 14:1408-1420. (Pubitemid 39507292)