Differential expression of LIM-homeodomain factors in Cajal-Retzius cells of primates, rodents, and birds.

Reelin-expressing Cajal-Retzius (CR) cells are among the earliest generated cells in the mammalian cerebral cortex and are believed to be crucial for both the development and the evolution of a laminated pattern in the pallial wall of the telencephalon. LIM-homeodomain (LIM-hd) transcription factors are expressed during brain development in a highly restricted and combinatorial manner, and they specify regional and cellular identity. We have investigated the expression of the LIM-hd members Lhx1/Lhx2/Lhx5/Lhx6/Lhx9 in the reelin-expressing cells, the pallium, and the regions of origin of CR cells including the cortical hem of 3 amniote species: the mouse, the chick, and the macaque monkey. We found major differences in the combinatorial LIM-hd expression in the marginal zone as well as in the hem. 1) Lhx5 is a "preferential LIM-hd" for CR cells in mammals but not expressed by these cells in chicks. 2) Lhx2 is expressed in the hem of the chick, whereas it is excluded from this region in mouse. 3) Whereas mouse CR cells express Lhx5/Lhx1, their monkey counterparts express 4 of these factors: Lhx1/Lhx2/Lhx5/Lhx9. We discuss our findings in evolutionary terms for the specification of the midline hem and CR cell type and the emergence of the cortical lamination pattern.

[1]  Stephen W. Wilson,et al.  Conserved and divergent patterns of Reelin expression in the zebrafish central nervous system , 2002, The Journal of comparative neurology.

[2]  E. Grove,et al.  Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order , 2006, Development.

[3]  C. W. Ragsdale,et al.  The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. , 1998, Development.

[4]  S. Nakanishi,et al.  Generation of Reelin-Positive Marginal Zone Cells from the Caudomedial Wall of Telencephalic Vesicles , 2004, The Journal of Neuroscience.

[5]  A. Goffinet,et al.  Evolution of cortical lamination: the reelin/Dab1 pathway. , 2000, Novartis Foundation symposium.

[6]  S. Rétaux,et al.  A short history of LIM domains (1993–2002) , 2002, Molecular Neurobiology.

[7]  T. Curran,et al.  Detection of the reelin breakpoint in reeler mice. , 1996, Brain research. Molecular brain research.

[8]  Henry Kennedy,et al.  Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. , 2002, Cerebral cortex.

[9]  S. Rétaux,et al.  Dynamic expression of the LIM-homeodomain gene Lhx15 through larval brain development of the sea lamprey (Petromyzon marinus). , 2006, Gene expression patterns : GEP.

[10]  P. Rakić,et al.  Development of Layer I Neurons in the Primate Cerebral Cortex , 2001, The Journal of Neuroscience.

[11]  Paul E. Boardman,et al.  A Comprehensive Collection of Chicken cDNAs , 2002, Current Biology.

[12]  A. Lavdas,et al.  The Medial Ganglionic Eminence Gives Rise to a Population of Early Neurons in the Developing Cerebral Cortex , 1999, The Journal of Neuroscience.

[13]  J. Parnavelas,et al.  Lhx6 Regulates the Migration of Cortical Interneurons from the Ventral Telencephalon But Does Not Specify their GABA Phenotype , 2004, The Journal of Neuroscience.

[14]  A. Fairén,et al.  Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex , 1998, The Journal of comparative neurology.

[15]  Franck Bourrat,et al.  An in situ screen for genes controlling cell proliferation in the optic tectum of the medaka (Oryzias latipes) , 2001, Mechanisms of Development.

[16]  A. Guidotti,et al.  In Patas monkey, glutamic acid decarboxylase‐67 and reelin mRNA coexpression varies in a manner dependent on layers and cortical areas , 2002, The Journal of comparative neurology.

[17]  A. Guidotti,et al.  Reelin promoter hypermethylation in schizophrenia. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  L. Medina,et al.  Expression patterns of Wnt8b and Wnt7b in the chicken embryonic brain suggest a correlation with forebrain patterning centers and morphogenesis , 2002, Neuroscience.

[19]  Miguel Marín-Padilla,et al.  Cajal–Retzius cells and the development of the neocortex , 1998, Trends in Neurosciences.

[20]  T. Jessell,et al.  Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes , 1994, Cell.

[21]  S. Rétaux,et al.  Molecular mechanisms of projection neuron production and maturation in the developing cerebral cortex. , 2009, Seminars in cell & developmental biology.

[22]  A. Goffinet,et al.  The evolution of cortical development. An hypothesis based on the role of the Reelin signaling pathway , 2000, Trends in Neurosciences.

[23]  M. Rosenfeld,et al.  A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. , 1997, Genes & development.

[24]  G. Meyer,et al.  Expression of p73 and Reelin in the Developing Human Cortex , 2002, The Journal of Neuroscience.

[25]  K. Mikoshiba,et al.  Reelin Is a Secreted Glycoprotein Recognized by the CR-50 Monoclonal Antibody , 1997, The Journal of Neuroscience.

[26]  A. Goffinet,et al.  Reelin expression during embryonic brain development in Crocodylus niloticus , 2003, The Journal of comparative neurology.

[27]  C. Sotelo,et al.  Regional and Cellular Patterns of reelin mRNA Expression in the Forebrain of the Developing and Adult Mouse , 1998, The Journal of Neuroscience.

[28]  C. Englund,et al.  Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. , 2003, Brain research. Developmental brain research.

[29]  G. Meyer,et al.  Developmental changes in layer I of the human neocortex during prenatal life: A DiI‐tracing and AChE and NADPH‐d histochemistry study , 1993, The Journal of comparative neurology.

[30]  A. Goffinet,et al.  The role of reelin in the development and evolution of the cerebral cortex. , 2002, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[31]  M. Webster,et al.  Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains , 2005, Biological Psychiatry.

[32]  F. Serajee,et al.  Association of Reelin gene polymorphisms with autism. , 2006, Genomics.

[33]  David A. Pearce,et al.  Reelin signaling is impaired in autism , 2005, Biological Psychiatry.

[34]  L. Puelles,et al.  Prosomeric map of the lamprey forebrain based on calretinin immunocytochemistry, nissl stain, and ancillary markers , 1999, The Journal of comparative neurology.

[35]  Karla E. Hirokawa,et al.  Lhx2 Selector Activity Specifies Cortical Identity and Suppresses Hippocampal Organizer Fate , 2008, Science.

[36]  L. Medina,et al.  Subdivisions and derivatives of the chicken subpallium based on expression of LIM and other regulatory genes and markers of neuron subpopulations during development , 2009, The Journal of comparative neurology.

[37]  C. Walsh,et al.  Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations , 2000, Nature Genetics.

[38]  A. Goffinet,et al.  Reelin and brain development , 2003, Nature Reviews Neuroscience.

[39]  G. Meyer,et al.  Comparative aspects of p73 and Reelin expression in Cajal-Retzius cells and the cortical hem in lizard, mouse and human , 2007, Brain Research.

[40]  S. Rétaux,et al.  The LIM-Homeodomain Gene Family in the DevelopingXenopus Brain: Conservation and Divergences with the Mouse Related to the Evolution of the Forebrain , 2001, The Journal of Neuroscience.

[41]  S. Nakanishi,et al.  Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Seike,et al.  The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons , 1995, Neuron.

[43]  S. Pfaff,et al.  Transcriptional codes and the control of neuronal identity. , 2002, Annual review of neuroscience.

[44]  H. Westphal,et al.  Control of hippocampal morphogenesis and neuronal differentiation by the LIM homeobox gene Lhx5. , 1999, Science.

[45]  Tomomi Shimogori,et al.  Embryonic signaling centers expressing BMP, WNT and FGF proteins interact to pattern the cerebral cortex , 2004, Development.

[46]  A. Goffinet,et al.  Reelin mRNA expression during embryonic brain development in the turtle Emys orbicularis , 1999, The Journal of comparative neurology.

[47]  S. Rétaux,et al.  Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: insights from LIM-homeodomain, Pax and hedgehog genes. , 2005, Developmental biology.

[48]  P. Sharpe,et al.  Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. , 1998, Development.

[49]  E. Soriano,et al.  The Cells of Cajal-Retzius: Still a Mystery One Century After , 2005, Neuron.

[50]  A. Fairén,et al.  What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. , 1999, Cerebral cortex.

[51]  S. Rétaux,et al.  A LIM-homeodomain code for development and evolution of forebrain connectivity. , 2002, Neuroreport.

[52]  T. Curran,et al.  Rescue of Ataxia and Preplate Splitting by Ectopic Expression of Reelin in reeler Mice , 2002, Neuron.

[53]  L. Medina,et al.  Development and evolution of the pallium. , 2009, Seminars in cell & developmental biology.

[54]  D. Haussler,et al.  An RNA gene expressed during cortical development evolved rapidly in humans , 2006, Nature.

[55]  G. Meyer,et al.  Prenatal development of reelin‐immunoreactive neurons in the human neocortex , 1998, The Journal of comparative neurology.

[56]  M. Rodicio,et al.  Reelin immunoreactivity in the adult sea lamprey brain , 2004, Journal of Chemical Neuroanatomy.

[57]  T. Curran,et al.  Reelin mRNA expression during embryonic brain development in the chick , 2000, The Journal of comparative neurology.

[58]  G. Meyer,et al.  The paleocortical ventricle is the origin of reelin‐expressing neurons in the marginal zone of the foetal human neocortex , 1999, The European journal of neuroscience.

[59]  S. Rétaux,et al.  Expression of the LIM-homeodomain gene Lmx1a (dreher) during development of the mouse nervous system , 2002, Mechanisms of Development.

[60]  D. Falconer Two new mutants, ‘trembler’ and ‘reeler’, with neurological actions in the house mouse (Mus musculus L.) , 2008, Journal of Genetics.

[61]  S. Rétaux,et al.  LIM‐homeodomain genes as developmental and adult genetic markers of Xenopus forebrain functional subdivisions , 2004, The Journal of comparative neurology.

[62]  E. Grove,et al.  LIM-homeodomain gene Lhx2 regulates the formation of the cortical hem , 2001, Mechanisms of Development.

[63]  L. López-Mascaraque,et al.  Origins and migratory routes of murine Cajal‐Retzius cells , 2007, The Journal of comparative neurology.

[64]  A. Goffinet,et al.  The Central Fragment of Reelin, Generated by Proteolytic Processing In Vivo, Is Critical to Its Function during Cortical Plate Development , 2004, The Journal of Neuroscience.

[65]  H. Kennedy,et al.  Comparative aspects of cerebral cortical development , 2006, The European journal of neuroscience.

[66]  Sébastien Vigneau,et al.  Multiple origins of Cajal-Retzius cells at the borders of the developing pallium , 2005, Nature Neuroscience.

[67]  T. Curran,et al.  A protein related to extracellular matrix proteins deleted in the mouse mutant reeler , 1995, Nature.

[68]  R. Anadón,et al.  Reelin immunoreactivity in the larval sea lamprey brain , 2002, Journal of Chemical Neuroanatomy.

[69]  J. Rubenstein,et al.  Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8, and Emx1 distinguish ventral and lateral pallial histogenetic divisions in the developing mouse claustroamygdaloid complex , 2004, The Journal of comparative neurology.

[70]  L. Medina,et al.  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 , 2008, Brain Research Bulletin.

[71]  L. Subramanian,et al.  Dynamic spatiotemporal expression of LIM genes and cofactors in the embryonic and postnatal cerebral cortex , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[72]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[73]  O. Marín,et al.  A long, remarkable journey: Tangential migration in the telencephalon , 2001, Nature Reviews Neuroscience.

[74]  M. Besson,et al.  Lhx9: A Novel LIM-Homeodomain Gene Expressed in the Developing Forebrain , 1999, The Journal of Neuroscience.