nalyot, a Mutation of the Drosophila Myb-Related Adf1 Transcription Factor, Disrupts Synapse Formation and Olfactory Memory

nalyot (nal) is a novel olfactory memory mutant of Drosophila, encoding Adf1, a myb-related transcription factor. Following extended training sessions, Adf1 mutants show normal early memory but defective longterm memory. Adf1 shows widespread spatiotemporal expression, yet mutant alleles reveal no discernible disruptions in gross morphology of the nervous system. Studies at the larval neuromuscular junction, however, reveal a role for Adf1 in the modulation of synaptic growth-in contrast to the role established for dCREB2 in the control of synaptic function (Davis et al., 1996). These findings suggest that Adf1 and dCREB2 regulate distinct transcriptional cascades involved in terminal stages of synapse maturation. More generally, Adf1 provides a novel link between molecular mechanisms of developmental and behavioral plasticity.

[1]  T. Préat,et al.  IDENTIFICATION OF LINOTTE, A NEW GENE AFFECTING LEARNING AND MEMORY IN DROSOPHILA MELANOGASTER , 2007, Journal of neurogenetics.

[2]  A. Brand,et al.  Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. , 1995, Development.

[3]  R. Kelly,et al.  Traffic of Dynamin within Individual DrosophilaSynaptic Boutons Relative to Compartment-Specific Markers , 1996, The Journal of Neuroscience.

[4]  M. Heisenberg,et al.  ARE THE STRUCTURAL CHANGES IN ADULT DROSOPHILA MUSHROOM BODIES MEMORY TRACES? STUDIES ON BIOCHEMICAL LEARNING MUTANTS , 2007, Journal of neurogenetics.

[5]  Tim Tully,et al.  Associative Learning Disrupted by Impaired Gs Signaling in Drosophila Mushroom Bodies , 1996, Science.

[6]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[7]  T. Tully,et al.  latheo Encodes a Subunit of the Origin Recognition Complex and Disrupts Neuronal Proliferation and Adult Olfactory Memory When Mutant , 1999, Neuron.

[8]  M Heisenberg,et al.  Vision affects mushroom bodies and central complex in Drosophila melanogaster. , 1997, Learning & memory.

[9]  Kendal Broadie,et al.  Activity-dependent development of the neuromuscular synapse during drosophila embryogenesis , 1993, Neuron.

[10]  Y. Zhong,et al.  Second messenger systems underlying plasticity at the neuromuscular junction. , 1999, International review of neurobiology.

[11]  T. Tully,et al.  CREB as a Memory Modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in drosophila , 1995, Cell.

[12]  E. Reddy,et al.  The myb gene family in cell growth, differentiation and apoptosis , 1999, Oncogene.

[13]  T. Préat,et al.  Genetic dissection of consolidated memory in Drosophila , 1994, Cell.

[14]  J. Sanes,et al.  Development of the vertebrate neuromuscular junction. , 1999, Annual review of neuroscience.

[15]  M. Ramaswami,et al.  A Product of the Drosophila stoned Locus Regulates Neurotransmitter Release , 1998, The Journal of Neuroscience.

[16]  Ronald L. Davis,et al.  Integrin-mediated short-term memory in Drosophila , 1998, Nature.

[17]  Roland Strauss,et al.  Highwire Regulates Synaptic Growth in Drosophila , 2000, Neuron.

[18]  T. Tully,et al.  Molecular cloning of linotte in Drosophila: A novel gene that functions in adults during associative learning , 1995, Neuron.

[19]  G. Davis,et al.  Drosophila Futsch Regulates Synaptic Microtubule Organization and Is Necessary for Synaptic Growth , 2000, Neuron.

[20]  T. Tully,et al.  latheo, a Drosophila Gene Involved in Learning, Regulates Functional Synaptic Plasticity , 1999, Neuron.

[21]  R. Tjian,et al.  Purified Drosophila transcription factor, Adh distal factor-1 (Adf-1), binds to sites in several Drosophila promoters and activates transcription. , 1990, The Journal of biological chemistry.

[22]  D. Mckearin,et al.  The Drosophila stonewall gene encodes a putative transcription factor essential for germ cell development. , 1996, Development.

[23]  M Heisenberg,et al.  Structural plasticity in the Drosophila brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  R. Tjian,et al.  Adf-1 Is a Nonmodular Transcription Factor That Contains a TAF-Binding Myb-Like Motif , 1998, Molecular and Cellular Biology.

[25]  Claire Russell,et al.  Dosage-Sensitive and Complementary Functions of Roundabout and Commissureless Control Axon Crossing of the CNS Midline , 1998, Neuron.

[26]  T. Tully,et al.  latheo, a new gene involved in associative learning and memory in Drosophila melanogaster, identified from P element mutagenesis. , 1992, Genetics.

[27]  G. Davis,et al.  Drosophila Futsch/22C10 Is a MAP1B-like Protein Required for Dendritic and Axonal Development , 2000, Neuron.

[28]  M. Constantine-Paton,et al.  Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. , 1990, Annual review of neuroscience.

[29]  Mary Chen,et al.  Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change , 1995, Cell.

[30]  T. Tully,et al.  Developmental Expression of an amn+ Transgene Rescues the Mutant Memory Defect of amnesiacAdults , 1999, The Journal of Neuroscience.

[31]  Tim Tully,et al.  Dissection of memory formation: from behavioral pharmacology to molecular genetics , 1995, Trends in Neurosciences.

[32]  E. Kandel,et al.  cAMP response element-binding protein is activated by Ca2+/calmodulin- as well as cAMP-dependent protein kinase. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[33]  R. Tjian,et al.  Cloning of Drosophila transcription factor Adf-1 reveals homology to Myb oncoproteins. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M Heisenberg,et al.  Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. , 1994, Science.

[35]  J. Dubnau,et al.  Gene discovery in Drosophila: new insights for learning and memory. , 1998, Annual review of neuroscience.

[36]  W. Quinn,et al.  Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila , 1994, Cell.

[37]  M Heisenberg,et al.  Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Eric R Kandel,et al.  CREB1 Encodes a Nuclear Activator, a Repressor, and a Cytoplasmic Modulator that Form a Regulatory Unit Critical for Long-Term Facilitation , 1998, Cell.

[39]  R. Tjian,et al.  Characterization of drosophila transcription factors that activate the tandem promoters of the alcohol dehydrogenase gene , 1985, Cell.

[40]  C. Goodman,et al.  Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. III. CREB Is Necessary for Presynaptic Functional Plasticity , 1996, Neuron.

[41]  T. Préat,et al.  The Drosophila putative kinase Linotte (Derailed) prevents central brain axons from converging on a newly described interhemispheric ring , 1998, Mechanisms of Development.

[42]  O. H. Lowry Academic press. , 1972, Analytical chemistry.

[43]  Anne-Marie Chang,et al.  Functional Identification of the Mouse Circadian Clock Gene by Transgenic BAC Rescue , 1997, Cell.

[44]  A. Antonini,et al.  Pioneer neurons and target selection in cerebral cortical development. , 1990, Cold Spring Harbor symposia on quantitative biology.

[45]  T. Robinson,et al.  Brain Plasticity and Behavior , 2003, Annual review of psychology.

[46]  C. Shatz,et al.  Developmental mechanisms that generate precise patterns of neuronal connectivity , 1993, Cell.

[47]  V. Budnik,et al.  Assembly and maturation of the Drosophila larval neuromuscular junction. , 1999, International review of neurobiology.

[48]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.