Cell-type-specific consequences of reelin deficiency in the mouse neocortex, hippocampus, and amygdala

Journal of Comparative Neurology

Volumn 519, Issue 11, 2011, Pages 2061-2089

  Boyle, Maureen P ^a   Bernard, Amy ^a   Thompson, Carol L ^a   Ng, Lydia ^a   Boe, Andrew ^a   Mortrud, Marty ^a   Hawrylycz, Michael J ^a   Jones, Allan R ^a   Hevner, Robert F ^b   Lein, Ed S ^a  

^a ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Development; Laminar; Molecular markers; Neuropathology; Reeler; Subiculum

Indexed keywords

CELL MARKER; REELIN;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL SPECIFICITY; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; GENE DISRUPTION; GENE LOCATION; HIGH THROUGHPUT SCREENING; HIPPOCAMPUS; HISTOLOGY; MOUSE; NEOCORTEX; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; REELER GENE; STRUCTURE ANALYSIS;

AMYGDALA; ANIMALS; BIOLOGICAL MARKERS; CELL ADHESION MOLECULES, NEURONAL; EXTRACELLULAR MATRIX PROTEINS; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MICE; MICE, NEUROLOGIC MUTANTS; NEOCORTEX; NERVE TISSUE PROTEINS; PHENOTYPE; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 79959466300     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22655     Document Type: Article

References (48)

1. Alcantara S, Ruiz M, D'Arcangelo G, Ezan F, de Lecea L, Curran T, Sotelo C, Soriano E. 1998. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18: 7779-7799.
2. Bayer SA, Altman J. 1991. Neocortical development New York: Raven Press.
3. Caviness VS Jr. 1976. Patterns of cell and fiber distribution in the neocortex of the reeler mutant mouse. J Comp Neurol 170: 435-447.
4. 3H]thymidine autoradiography. Brain Res 256: 293-302.
5. Caviness VS Jr, Sidman RL. 1972. Olfactory structures of the forebrain in the reeler mutant mouse. J Comp Neurol 145: 85-104.
6. Caviness VS Jr, 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.
7. Caviness VS Jr, Frost DO, Hayes NL. 1976. Barrels in somatosensory cortex of normal and reeler mutant mice. Neurosci Lett 3: 7-14.
8. Caviness VS Jr, Yorke CH Jr. 1976. Interhemispheric neocortical connections of the corpus callosum in the reeler mutant mouse: a study based on anterograde and retrograde methods. J Comp Neurol 170: 449-459.
9. Cooper JA. 2008. A mechanism for inside-out lamination in the neocortex. Trends Neurosci 31: 113-119.
10. Dong H. 2008. The Allen reference atlas: a digital color brain atlas of the C57BL/6J male mouse. Hoboken, NJ: Wiley-Blackwell. 366 p.
11. Ferland RJ, Cherry TJ, Preware PO, Morrisey EE, Walsh CA. 2003. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol 460: 266-279.
12. Frotscher M. 1997. Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res 290: 315-322.
13. Gilmore EC, Herrup K. 2000. Cortical development: receiving reelin. Curr Biol 10: R162-R166.
14. Goffinet AM. 1984. Events governing organization of postmigratory neurons: studies on brain development in normal and reeler mice. Brain Res 319: 261-296.
15. Grumet M, Hoffman S, Edelman GM. 1984. Two antigenically related neuronal cell adhesion molecules of different specificities mediate neuron-neuron and neuron-glia adhesion. Proc Natl Acad Sci U S A 81: 267-271.
16. Hevner RF, Daza RA, Englund C, Kohtz J, Fink A. 2004. Postnatal shifts of interneuron position in the neocortex of normal and reeler mice: evidence for inward radial migration. Neuroscience 124: 605-618.
17. Hevner RF, Daza RA, Rubenstein JL, Stunnenberg H, Olavarria JF, Englund C. 2003. Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 25: 139-151.
18. Jossin Y, Bar I, Ignatova N, Tissir F, De Rouvroit CL, Goffinet AM. 2003. The reelin signaling pathway: some recent developments. Cereb Cortex 13: 627-633.
19. Kubo K, Nakajima K. 2003. Cell and molecular mechanisms that control cortical layer formation in the brain. Keio J Med 52: 8-20.
20. Lau C, Ng L, Thompson C, Pathak S, Kuan L, Jones A, Hawrylycz M. 2008. Exploration and visualization of gene expression with neuroanatomy in the adult mouse brain. BMC Bioinformatics 9: 153.
21. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
22. Luque JM. 2007. Puzzling out the reeler brainteaser: does reelin signal to unique neural lineages? Brain Res 1140: 41-50.
23. Luque JM, Morante-Oria J, Fairen A. 2003. Localization of ApoER2, VLDLR and Dab1 in radial glia: groundwork for a new model of reelin action during cortical development. Brain Res Dev Brain Res 140: 195-203.
24. Magdaleno S, Keshvara L, Curran T. 2002. Rescue of ataxia and preplate splitting by ectopic expression of Reelin in reeler mice. Neuron 33: 573-586.
25. Magdaleno S, Jensen P, Brumwell CL, Seal A, Lehman K, Asbury A, Cheung T, Cornelius T, Batten DM, Eden C, Norland SM, Rice DS, Dosooye N, Shakya S, Mehta P, Curran T. 2006. BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol 4: e86.
26. McCarthy KD, Partlow LM. 1976. Preparation of pure neuronal and non-neuronal cultures from embryonic chick sympathetic ganglia: a new method based on both differential cell adhesiveness and the formation of homotypic neuronal aggregates. Brain Res 114: 391-414.
27. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD. 2007. Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8: 427-437.
28. Ng L, Pathak SD, Kuan C, Lau C, Dong H, Sodt A, Dang C, Avants B, Yushkevich P, Gee JC, Haynor D, Lein E, Jones A, Hawrylycz M. 2007. Neuroinformatics for genome-wide 3D gene expression mapping in the mouse brain. IEEE/ACM Trans Comput Biol Bioinform 4: 382-393.
29. Ng L, Bernard A, Lau C, Overly CC, Dong HW, Kuan C, Pathak S, Sunkin SM, Dang C, Bohland JW, Bokil H, Mitra PP, Puelles L, Hohmann J, Anderson DJ, Lein ES, Jones AR, Hawrylycz M. 2009. An anatomic gene expression atlas of the adult mouse brain. Nat Neurosci 12: 356-362.
30. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA. 2004. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 479: 168-180.
31. 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 of cortical neurons. Neuron 14: 899-912.
32. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
33. Pearlman AL, Sheppard AM. 1996. Extracellular matrix in early cortical development. Prog Brain Res 108: 117-134.
34. Polleux F, Dehay C, Kennedy H. 1998. Neurogenesis and commitment of corticospinal neurons in reeler. J Neurosci 18: 9910-9923.
35. Remedios R, Huilgol D, Saha B, Hari P, Bhatnagar L, Kowalczyk T, Hevner RF, Suda Y, Aizawa S, Ohshima T, Stoykova A, Tole S. 2007. A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neocortex. Nat Neurosci 10: 1141-1150.
36. Rice DS, Curran T. 2001. Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24: 1005-1039.
37. Schiffmann SN, Bernier B, Goffinet AM. 1997. Reelin mRNA expression during mouse brain development. Eur J Neurosci 9: 1055-1071.
38. Senft SL, Woolsey TA. 1991. Mouse barrel cortex viewed as Dirichlet domains. Cereb Cortex 1: 348-363.
39. Soriano E, Del Rio JA. 2005. The cells of Cajal-Retzius: still a mystery one century after. Neuron 46: 389-394.
40. Steindler DA, Colwell SA. 1976. reeler Mutant mouse: maintenance of appropriate and reciprocal connections in the cerebral cortex and thalamus. Brain Res 113: 386-393.
41. Steindler DA, Faissner A, Harrington KL. 1994. A unique mosaic in the visual cortex of the reeler mutant mouse. Cereb Cortex 4: 129-137.
42. Tarabykin V, Stoykova A, Usman N, Gruss P. 2001. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128: 1983-1993.
43. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, Puchalski RB, Gage FH, Jones AR, Bajic VB, Hawrylycz MJ, Lein ES. 2008. Genomic anatomy of the hippocampus. Neuron 60: 1010-1021.
44. Tissir F, Goffinet AM. 2003. Reelin and brain development. Nat Rev Neurosci 4: 496-505.
45. Tissir F, Lambert de Rouvroit C, Goffinet AM. 2002. The role of reelin in the development and evolution of the cerebral cortex. Braz J Med Biol Res 35: 1473-1484.
46. Visel A, Thaller C, Eichele G. 2004. GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32(Database issue): D552-D556.
47. Yamamoto T, Sakakibara S, Mikoshiba K, Terashima T. 2003. Ectopic corticospinal tract and corticothalamic tract neurons in the cerebral cortex of yotari and reeler mice. J Comp Neurol 461: 61-75.
48. Yoshida M, Assimacopoulos S, Jones KR, Grove EA. 2006. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133: 537-545.