Control of early neurogenesis of the Drosophila brain by the head gap genes tll, otd, ems, and btd.

The progenitors of the Drosophila central nervous system (CNS), called neuroblasts, segregate from the neurectoderm of the early embryo in a stereotyped pattern. The neuroblasts that give rise to the brain segregate from the procephalic neurectoderm and form three neuromeres, called protocerebrum, deuterocerebrum, and tritocerebrum. The expression of the proneural genes of the achaete-scute complex (AS-C) is required for neurectodermal cells to acquire the competency to form neuroblasts. We show here that the expression of the proneural gene lethal of scute (l'sc) is required for the development of the majority of the procephalic neuroblasts. l'sc expression in the procephalic neurectoderm is controlled by the head gap genes tailless (tll), orthodenticle (otd), buttonhead (btd), and empty spiracles (ems), which are expressed in partially overlapping domains of the head neurectoderm. Loss of function of a given head gap gene results in the absence of l'sc expression in its domain, followed by the absence of neuroblasts that would normally segregate from this domain. Loss of tll function results in the absence of all protocerebral neuroblasts, otd functions in a domain that includes a large part of the protocerebrum and a smaller part of the adjacent deuterocerebrum. Both ems and btd are required in partially overlapping subsets of neuroblasts of the deuterocerebrum and tritocerebrum.

[1]  Prof. Dr. José A. Campos-Ortega,et al.  The Embryonic Development of Drosophila melanogaster , 1997, Springer Berlin Heidelberg.

[2]  V. Hartenstein,et al.  Early neurogenesis of the Drosophila brain , 1996, The Journal of comparative neurology.

[3]  Ruth Díez del Corral,et al.  araucan and caupolican, Two Members of the Novel Iroquois Complex, Encode Homeoproteins That Control Proneural and Vein-Forming Genes , 1996, Cell.

[4]  Katsuo Furukubo-Tokunaga,et al.  Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila , 1995, Neuron.

[5]  J. Posakony,et al.  Posterior stripe expression of hunchback is driven from two promoters by a common enhancer element. , 1995, Development.

[6]  L. Velasco,et al.  vnd, a gene required for early neurogenesis of Drosophila, encodes a homeodomain protein. , 1995, The EMBO journal.

[7]  J. Posakony,et al.  Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. , 1994, Genes & development.

[8]  M. Caudy,et al.  Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. , 1994, Genes & development.

[9]  H. Jäckle,et al.  Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[10]  S. Carroll,et al.  The ventral nervous system defective gene controls proneural gene expression at two distinct steps during neuroblast formation in Drosophila. , 1994, Development.

[11]  H. Jäckle,et al.  A Drosophila homologue of human Sp1 is a head-specific segmentation gene , 1993, Nature.

[12]  C. Doe,et al.  Neuroblast specification and formation regulated by wingless in the Drosophila CNS. , 1993, Science.

[13]  Y. Jan,et al.  asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. , 1993, Development.

[14]  Y. Jan,et al.  The regulation and function of the helix-loop-helix gene, asense, in Drosophila neural precursors. , 1993, Development.

[15]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[16]  C. Doe.  Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. , 1992, Development.

[17]  G. Technau,et al.  Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. , 1992, Development.

[18]  W. Gehring,et al.  Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. , 1992, The EMBO journal.

[19]  S. Carroll,et al.  Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. , 1992, Development.

[20]  D. Lindsley,et al.  The Genome of Drosophila Melanogaster , 1992 .

[21]  M Hoch,et al.  Spatial control of the gap gene knirps in the Drosophila embryo by posterior morphogen system. , 1992, Science.

[22]  C. Goodman,et al.  Genetic analysis of growth cone guidance in drosophila: Fasciclin II functions as a neuronal recognition molecule , 1991, Cell.

[23]  F. Jiménez,et al.  Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. , 1991, Development.

[24]  Norbert Perrimon,et al.  The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development , 1990, Nature.

[25]  S. Cohen,et al.  Mediation of Drosophila head development by gap-like segmentation genes , 1990, Nature.

[26]  Robert J. Diaz,et al.  The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily , 1990, Cell.

[27]  J. Campos-Ortega,et al.  Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of D. melanogaster , 1990, Neuron.

[28]  J. Posakony,et al.  extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins , 1990, Cell.

[29]  J. Modolell,et al.  The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein , 1990, Cell.

[30]  G. Rubin,et al.  The drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates , 1990, Cell.

[31]  M. Ashburner,et al.  Drosophila: A laboratory manual , 1990 .

[32]  W. McGinnis,et al.  Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. , 1989, Genes & development.

[33]  A. Ghysen,et al.  Genesis of the Drosophila peripheral nervous system. , 1989, Trends in genetics : TIG.

[34]  Y. Jan,et al.  daughterless, a Drosophila gene essential for both neurogenesis and sex determination, has sequence similarities to myc and the achaete-scute complex , 1988, Cell.

[35]  J. Lengyel,et al.  Graded requirement for the zygotic terminal gene, tailless, in the brain and tail region of the Drosophila embryo. , 1988, Development.

[36]  M. Bate,et al.  The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila , 1987, Cell.

[37]  J. Modolell,et al.  The achaete‐scute complex is expressed in neurogenic regions of Drosophila embryos , 1987, The EMBO journal.

[38]  J. Hubbard,et al.  The Peripheral Nervous System , 1974, Springer US.