An In Silico agent-based model demonstrates reelin function in directing lamination of neurons during cortical development

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Caffrey, James R ^a   Hughes, Barry D ^a   Britto, Joanne M ^a   Landman, Kerry A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

REELIN; DAB1 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL ASSAY; CELL CONVERSION; CELL MIGRATION; CELL MOTILITY; CELL VIABILITY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; ALGORITHM; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; DEFICIENCY; EMBRYO DEVELOPMENT; GENETICS; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHENOTYPE;

ALGORITHMS; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EXTRACELLULAR MATRIX PROTEINS; GREEN FLUORESCENT PROTEINS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURONS; PHENOTYPE; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84908191913     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110415     Document Type: Article

References (41)

1. Streit P (1984) Glutamate and aspartate as transmitter candidates for systems of the cerebral cortex. In Cerebral Cortex, Jones EG, Peters A, eds., pp. 119-143, Plenum, New York.
2. Schubert D, Kötter R, Staiger JF (2007) Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits. Brain Struct. Funct. 212: 107-119.
3. Rakic P (2009) Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci 10: 724-735.
4. Hong SE, Shugart YY, Huang D.T., Al Shahwan S, Grant PE, et al. (2000) Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nature Genetics, 26: 93-96.
5. Barkovich AJ, Guerrini R Kuzniecky RI, Jackson GD, Dobyns WB (2012) A developmental and genetic classification for malformations of cortical development: update Brain 135: 1348-1369.
6. Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192: 766-768.
7. Caviness VS, Jr, Sidman RL (1973) Retrohippocampal, hippocampal and related structures of the forebrain in the reeler mutant mouse. J Comp Neurol 147: 235-254.
8. Falconer DS (1951) Two new mutants, 'trembler' and 'reeler', with neurological actions in the house (Mus musculus L.). J. Genetics 50: 192-201.
9. Caviness VS (1976) Patterns of cell and fiber distribution in the neocortex of the reeler mutant. J. Comp. Neurol. 170: 435-47.
10. Sheppard AM, Pearlman AL (1997) Abnormal reorganization of preplate neurons and their associated extracellular matrix: An early manifestation of altered neocortical development in the reeler mutant mouse, J. Comp. Neurol, 378: 173-179.
11. Folsom TD, Fatemi SH (2013) The involvement of Reelin in neurodevelop-mental disorders Neuropharmacology, 68: 122-135.
12. Fatemi SH (2001) Reelin mutations in mouse and man: from reeler mouse to schizophrenia, mood disorders, autism and lissencephaly. Molec. Psychiatry 6: 129-133.
13. Sekine K, Honda T, Kawauchi T., Kubo K, Nakajima K (2011) The outermost region of the developing cortical plate is crucial for both the switch of the radial migration mode and the Dab1-dependent inside-out lamination in the neocortex. J. Neurosci. 31: 9426-9439.
14. Xuejun C, Förster E, Zhao S., Bock HH, Frotscher M (2009) Reelin acts as a stop signal for radially migrating neurons by inducing phosphorylation of n-cofilin at the leading edge. Comm. Integ. Biol. 2: 375-377.
15. Courtès S, Vernerey J, Pujadas L., Magalon K, Cremer H, et al. (2011) Reelin controls progenitor cell migration in the healthy and pathological adult brain. PLoS ONE 6: e20430.
16. Rice DS, Curran T (2001) Role of the Reelin signaling pathway in central nervous system development. Ann. Rev. Neuroscience 24: 1005-1039.
17. D'Arcangelo G., Curran T (1998) Reeler: new tales on an old mutant. BioEssays 20: 235-244.
18. Cooper JA (2008) A mechanism for inside-out lamination in the neocortex. Trends Neurosci 31: 113-119.
19. Jossin Y, Cooper JA (2011) Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat Neurosci 14: 697-703.
20. Britto JM, Tait KJ, Lee E.P., Gamble RS, Hattori M, et al. (2013) Exogenous reelin modifies the migratory behavior of neurons depending on cortical location. Cereb. Cortex Cereb. Cortex doi:10.1093/cercor/bht123.
21. Deutsch A, Dormann S (2005) Cellular automaton modeling of biological formation: characterization, applications and analysis. Birkhauser: Boston.
22. Sander LM, Deisboeck TS (2002) Growth patterns of microscopic brain tumors Phys. Rev. E 66: 051901.
23. Zhang D, Brinas IM, Binder B.J., Landman KA, Newgreen DF (2010) Neural crest regionalisation for enteric nervous system formation: Implications for Hirschsprung's disease and stem cell therapy. Dev. Biol. 339: 280-294.
24. Binder BJ, Landman KA, Newgreen D.F., Simkin JE, Takahashi Y, et al. (2012) Spatial analysis of multi-species exclusion processes: application to neural crest cell migration in the embryonic gut. Bull. Math. Biol. 74: 474-490.
25. Hammond VE, Howell B, Godinho L., Tan SS (2001) Disabled-1 functions cell autonomously during radial migration and cortical layering of pyramidal neurons. J. Neuroscience 21: 8798-8808.
26. Franco SJ, Martinez-Garay I, Gil-Sanz C, Harkins-Perry SR, Müller U (2011) Reelin regulates cadherin function via dab1/rap1 to control neuronal migration and lamination in the neocortex. Neuron 69: 482-497.
27. Britto JM, Tait KJ, Johnston L.A., Hammond VE, Kalloniatis M, et al. (2011) Altered speeds and trajectories of neurons migrating in the ventricular and subventricular zones of the reeler neocortex, Cereb. Cortex 21: 1018-1027.
28. Matsuda T, Cepko CC (2004) Electroporation and RNA interference in the rodent retina in vivo and in vitro. PNAS 101: 16-22.
29. LoTurco JJ, Bai J (2006) The multipolar stage and disruptions in neuronal migration. Trends Neurosci 29: 407-413.
30. Noctor SC, Martinez-Cerdeno V, Ivic L., Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7: 136-144.
31. Lakomá J, Garcia-Alonso L, Luque JM (2011) Reelin sets the pace of neocortical neurogenesis. Development 138: 5223-5234.
32. Schiffmann SN, Bernier B, Goffinet AM (1997) Reelin mRNA expression during mousebrain development. Eur. J. Neurosci. 9: 1055-1071.
33. Frotscher M. (1997) Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res. 290: 315-322.
34. Dulabon L, Olsen EC, Taglienti M.G., Eisenhuth S., McGrath B, et al. (2000) Reelin binds a3b1 integrin and inhibits neuronal migration. Neuron 27: 33-44.
35. Chowdhury D, Schadschneider A, Nishinari K (2005) Physics of transport and traffic phenomena in biology: from molecular motors and cells to organisms. Phys. Life Rev. 2: 318-352.
36. Olson EC, Kim S, Walsh CA (2006) Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression J Neuroscience 26: 1767-1775.
37. Simó S, Jossin Y, Cooper JA (2010) Cullin 5 regulates cortical layering by modulating the speed and duration of Dab1-dependent neuronal migration J Neuroscience, 30: 5668-5676.
38. Lizarraga SB, Margossian SP, Harris M.H., Campagna DR, Han AP, et al. (2010) Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Dev. 137: 1907-1917.
39. 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.
40. Zubler F, Hauri A, Pfister S., Bauer R, Anderson JC, et al. (2013) Simulating cortical development as a self constructing process: a novel multi-scale approach combining molecular and physical aspects. PLOS Comp. Biol. 9, e1003173.
41. Alcantara S, Ruiz M, D'Arcangelo G, Ezan F, de Lecea L, et al. (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18: 7779-7799.