Differential expression of LIM-homeodomain factors in cajal-retzius cells of primates, rodents, and birds

Cerebral Cortex

Volumn 20, Issue 8, 2010, Pages 1788-1798

  Abellan, Antonio ^a   Menuet, Arnaud ^b   Dehay, Colette ^c   Medina, Loreta ^a   Rétaux, Sylvie ^b  

^a UNIVERSITY OF LLEIDA   (Spain)

^b CNRS   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

cortex; evolution; LIM code; pallium; reelin

Indexed keywords

MESSENGER RNA; REELIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LHX1; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR LHX5; TRANSCRIPTION FACTOR LHX6; TRANSCRIPTION FACTOR LHX9; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CHICK; COILED BODY; EMBRYO; EMBRYO DEVELOPMENT; EVOLUTION; GENE EXPRESSION; GLOBUS PALLIDUS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RHESUS MONKEY;

EID: 77955398043     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp242     Document Type: Article

References (74)

1. Abellan A, Medina L. 2008. Expression of cLhx6 and cLhx7/8 suggests a pallido-pedunculo-preoptic origin for the lateral and medial parts of the avian bed nucleus of the stria terminalis. Brain Res Bull. 75:299-304.
2. Abellan A, Medina L. 2009. Subdivisions and derivatives of the chicken subpallium based on expression of LIM and other regulatory genes and markers of neuron subpopulations during development. J Comp Neurol. 515:465-501.
3. 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.
4. Alifragis P, Liapi A, Parnavelas JG. 2004. Lhx6 regulates the migration of cortical interneurons from the ventral telencephalon but does not specify their GABA phenotype. J Neurosci. 24:5643-5648.
5. Bach I, Carriere C, Ostendorff HP, Andersen B, Rosenfeld MG. 1997. A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev. 11:1370-1380.
6. Bachy I, Failli V, Retaux S. 2002. A LIM-homeodomain code for development and evolution of forebrain connectivity. Neuroreport. 13:A23-A27.
7. Bachy I, Vernier P, Retaux S. 2001. The LIM-homeodomain gene family in the developing Xenopus brain: conservation and divergences with the mouse related to the evolution of the forebrain. J Neurosci. 21:7620-7629.
8. Bar I, Goffinet AM. 2000. Evolution of cortical lamination: the reelin/Dab1 pathway. Novartis Found Symp. 228:114-125; discussion: 125-128.
9. Bar I, Lambert de Rouvroit C, Goffinet AM. 2000. The evolution of cortical development. An hypothesis based on the role of the Reelin signaling pathway. Trends Neurosci. 23:633-638.
10. Bernier B, Bar I, D'Arcangelo G, Curran T, Goffinet AM. 2000. Reelin mRNA expression during embryonic brain development in the chick. J Comp Neurol. 422:448-463.
11. Bernier B, Bar I, Pieau C, Lambert De Rouvroit C, Goffinet AM. 1999. Reelin mRNA expression during embryonic brain development in the turtle Emys orbicularis. J Comp Neurol. 413:463-479.
12. Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A. 2005. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci. 8:1002-1012.
13. Boardman PE, Sanz-Ezquerro J, Overton IM, Burt DW, Bosch E, Fong WT, Tickle C, Brown WR, Wilson SA, Hubbard SJ. 2002. A comprehensive collection of chicken cDNAs. Curr Biol. 12:1965-1969.
14. Bulchand S, Grove EA, Porter FD, Tole S. 2001. LIM-homeodomain gene Lhx2 regulates the formation of the cortical hem. Mech Dev. 100:165-175.
15. Bulchand S, Subramanian L, Tole S. 2003. Dynamic spatiotemporal expression of LIM genes and cofactors in the embryonic and postnatal cerebral cortex. Dev Dyn. 226:460-469.
16. Cabrera-Socorro A, Hernandez-Acosta NC, Gonzalez-Gomez M, Meyer G. 2007. Comparative aspects of p73 and Reelin expression in Cajal-Retzius cells and the cortical hem in lizard, mouse and human. Brain Res. 1132:59-70.
17. Costagli A, Kapsimali M, Wilson SW, Mione M. 2002. Conserved and divergent patterns of Reelin expression in the zebrafish central nervous system. J Comp Neurol. 450:73-93.
18. D'Arcangelo 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.
19. D'Arcangelo G, Miao GG, Curran T. 1996. Detection of the reelin breakpoint in reeler mice. Brain Res Mol Brain Res. 39:234-236.
20. D'Arcangelo 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.
21. Failli V, Bachy I, Retaux S. 2002. Expression of the LIM-homeodomain gene Lmx1a (dreher) during development of the mouse nervous system. Mech Dev. 118:225-228.
22. Falconer DS. 1951. Two new mutants, Trembler and Reeler, with neurological actions in the house mouse. J Genet. 50:192-201.
23. Fatemi SH, Snow AV, Stary JM, Araghi-Niknam M, Reutiman TJ, Lee S, Brooks AI, Pearce DA. 2005. Reelin signaling is impaired in autism. Biol Psychiatry. 57:777-787.
24. Garcia-Moreno F, Lopez-Mascaraque L, De Carlos JA. 2007. Origins and migratory routes of murine Cajal-Retzius cells. J Comp Neurol. 500:419-432.
25. Garda AL, Puelles L, Rubenstein JL, Medina L. 2002. Expression patterns of Wnt8b and Wnt7b in the chicken embryonic brain suggest a correlation with forebrain patterning centers and morphogenesis. Neuroscience. 113:689-698.
26. Grayson DR, Jia X, Chen Y, Sharma RP, Mitchell CP, Guidotti A, Costa E. 2005. Reelin promoter hypermethylation in schizophrenia. Proc Natl Acad Sci USA. 102:9341-9346.
27. Grigoriou M, Tucker AS, Sharpe PT, Pachnis V. 1998. Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeo-domain encoding genes, suggests a role in mammalian head development. Development. 125:2063-2074.
28. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW. 1998. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development. 125:2315-2325.
29. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol. 88:49-92.
30. Hevner RF, Neogi T, Englund C, Daza RA, Fink A. 2003. Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Brain Res Dev Brain Res. 141:39-53.
31. Hong SE, Shugart YY, Huang DT, Shahwan SA, Grant PE, Hourihane JO, Martin ND, Walsh CA. 2000. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet. 26:93-96.
32. Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert de Rouvroit C, Goffinet AM. 2004. The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci. 24:514-521.
33. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG. 1999. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci. 19:7881-7888.
34. 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.
35. Mangale VS, Hirokawa KE, Satyaki PR, Gokulchandran N, Chikbire S, Subramanian L, Shetty AS, Martynoga B, Paul J, Mai MV, et al. 2008. Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science. 319:304-309.
36. Marin O, Rubenstein JL. 2001. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci. 2:780-790.
37. Marin-Padilla M. 1998. Cajal-Retzius cells and the development of the neocortex. Trends Neurosci. 21:64-71.
38. Medina L, Abellan A. 2009. Development and evolution of the pallium. Semin Cell Dev Biol. 20:698-711.
39. Medina L, Legaz I, Gonzalez G, De Castro F, Rubenstein JL, Puelles L. 2004. Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8, and Emx1 distinguish ventral and lateral pallial histogenetic divisions in the developing mouse claustroamygdaloid complex. J Comp Neurol. 474:504-523.
40. Merot Y, Retaux S, Heng JI. 2009. Molecular mechanisms of projection neuron production and maturation in the developing cerebral cortex. Semin Cell Dev Biol. 20(6):726-734.
41. Meyer G, Goffinet AM. 1998. Prenatal development of reelin-immuno- reactive neurons in the human neocortex. J Comp Neurol. 397(1):29-40.
42. Meyer G, Goffinet AM, Fairen A. 1999. What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cereb Cortex. 9:765-775.
43. Meyer G, Gonzalez-Hernandez T. 1993. Developmental changes in layer I of the human neocortex during prenatal life: a Dil-tracing and AChE and NADPH-d histochemistry study. J Comp Neurol. 338:317-336.
44. Meyer G, Perez-Garcia CG, Abraham H, Caput D. 2002. Expression of p73 and Reelin in the developing human cortex. J Neurosci. 22:4973-4986.
45. Meyer G, Soria JM, Martinez-Galan JR, Martin-Clemente B, Fairen A. 1998. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol. 397:493-518.
46. Meyer G, Wahle P. 1999. The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the foetal human neocortex. Eur J Neurosci. 11:3937-3944.
47. Molnar Z, Metin C, Stoykova A, Tarabykin V, Price DJ, Francis F, Meyer G, Dehay C, Kennedy H. 2006. Comparative aspects of cerebral cortical development. Eur J Neurosci. 23:921-934.
48. Moreno N, Bachy I, Retaux S, Gonzalez A. 2004. LIM-homeodomain genes as developmental and adult genetic markers of Xenopus forebrain functional subdivisions. J Comp Neurol. 472:52-72.
49. Nguyen V, Joly J, Bourrat F. 2001. An in situ screen for genes controlling cell proliferation in the optic tectum of the medaka (Oryzias latipes). Mech Dev. 107:55-67.
50. 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.
51. Osorio J, Mazan S, Retaux S. 2005. Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: insights from LIM-homeo-domain, Pax and hedgehog genes. Dev Biol. 288:100-112.
52. Osorio J, Megias M, Pombal MA, Retaux S. 2006. Dynamic expression of the LIM-homeodomain gene Lhx15 through larval brain development of the sea lamprey (Petromyzon marinus). Gene Expr Patterns. 6:873-878.
53. Perez-Costas E, Melendez-Ferro M, Perez-Garcia CG, Caruncho HJ, Rodicio MC. 2004. Reelin immunoreactivity in the adult sea lamprey brain. J Chem Neuroanat. 27:7-21.
54. Perez-Costas E, Melendez-Ferro M, Santos Y, Anadon R, Rodicio MC, Caruncho HJ. 2002. Reelin immunoreactivity in the larval sea lamprey brain. J Chem Neuroanat. 23:211-221.
55. Pollard KS, Salama SR, Lambert N, Lambot MA, Coppens S, Pedersen JS, Katzman S, King B, Onodera C, Siepel A, et al. 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature. 443:167-172.
56. Pombal MA, Puelles L. 1999. Prosomeric map of the lamprey forebrain based on calretinin immunocytochemistry, Nissl stain, and ancillary markers. J Comp Neurol. 414:391-422.
57. Retaux S, Bachy I. 2002. A short history of LIM domains (1993-2002): from protein interaction to degradation. Mol Neurobiol. 26:269-281.
58. Retaux S, Rogard M, Bach I, Failli V, Besson MJ. 1999. Lhx9: a novel LIM-homeodomain gene expressed in the developing forebrain. J Neurosci. 19:783-793.
59. Rodriguez MA, Caruncho HJ, Costa E, Pesold C, Liu WS, Guidotti A. 2002. In Patas monkey, glutamic acid decarboxylase-67 and reelin mRNA coexpression varies in a manner dependent on layers and cortical areas. J Comp Neurol. 451:279-288.
60. Serajee FJ, Zhong H, Mahbubul Huq AH. 2006. Association of Reelin gene polymorphisms with autism. Genomics. 87:75-83.
61. Shimogori T, Banuchi V, Ng HY, Strauss JB, Grove EA. 2004. Embryonic signaling centers expressing BMP, WNT and FGF proteins interact to pattern the cerebral cortex. Development. 131:5639-5647.
62. Shirasaki R, Pfaff SL. 2002. Transcriptional codes and the control of neuronal identity. Annu Rev Neurosci. 25:251-281.
63. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H. 2002. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex. 12:37-53.
64. Soriano E, Del Rio JA. 2005. The cells of cajal-retzius: still a mystery one century after. Neuron. 46:389-394.
65. Takiguchi-Hayashi K, Sekiguchi M, Ashigaki S, Takamatsu M, Hasegawa H, Suzuki-Migishima R, Yokoyama M, Nakanishi S, Tanabe Y. 2004. Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J Neurosci. 24:2286-2295.
66. Tissir F, Goffinet AM. 2003. Reelin and brain development. Nat Rev Neurosci. 4:496-505.
67. 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.
68. Tissir F, Lambert De Rouvroit C, Sire JY, Meyer G, Goffinet AM. 2003. Reelin expression during embryonic brain development in Croc-odylus niloticus. J Comp Neurol. 457:250-262.
69. Torrey EF, Barci BM, Webster MJ, Bartko JJ, Meador-Woodruff JH, Knable MB. 2005. Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains. Biol Psychiatry. 57:252-260.
70. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell. 79:957-970.
71. Yamazaki H, Sekiguchi M, Takamatsu M, Tanabe Y, Nakanishi S. 2004. Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis. Proc Natl Acad Sci USA. 101:14509-14514.
72. 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.
73. Zecevic N, Rakic P. 2001. Development of layer I neurons in the primate cerebral cortex. J Neurosci. 21:5607-5619.
74. Zhao Y, Sheng HZ, Amini R, Grinberg A, Lee E, Huang S, Taira M, Westphal H. 1999. Control of hippocampal morphogenesis and neuronal differentiation by the LIM homeobox gene Lhx5. Science. 284:1155-1158