Identification of genes that promote or inhibit olfactory memory formation in Drosophila

Genetics

Volumn 199, Issue 4, 2015, Pages 1173-1182

  Walkinshaw, Erica ^a   Gai, Yunchao ^a   Farkas, Caitlin ^a   Richter, Daniel ^a   Nicholas, Eric ^a   Keleman, Krystyna ^b   Davis, Ronald L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Janelia Farms ^*  (United States)

Author keywords

Drosophila; Memory; Memory suppressor genes; RNAi screen

Indexed keywords

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA MELANOGASTER; FEMALE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; MALE; MUSHROOM BODY; NONHUMAN; OLFACTORY MEMORY; PRIORITY JOURNAL; RNA INTERFERENCE; ANIMAL; CYTOLOGY; GENETICS; MEMORY; METABOLISM; ODOR; OLFACTORY RECEPTOR NEURON; PHYSIOLOGY; SMELLING;

ANIMALIA; BASIDIOMYCOTA; BRASSICA NAPUS VAR. NAPOBRASSICA; DROSOPHILA MELANOGASTER;

DROSOPHILA PROTEIN; DUNCE PROTEIN, DROSOPHILA; NERVE PROTEIN; SICKIE PROTEIN, DROSOPHILA;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MEMORY; MUSHROOM BODIES; NERVE TISSUE PROTEINS; OLFACTORY PERCEPTION; OLFACTORY RECEPTOR NEURONS; SMELL;

EID: 84926443574     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.173575     Document Type: Article

References (51)

1. Abel, T., K. C. Martin, D. Bartsch, and E. R. Kandel, 1998 Memory suppressor genes: inhibitory constraints on the storage of longterm memory. Science 279: 338–341
2. Aso, Y., K. Grübel, S. Busch, A. B. Friedrich, I. Siwanowicz et al., 2009 The mushroom body of adult Drosophila characterized by GAL4 drivers. J. Neurogenet. 23: 156–172
3. Beck, C. D. O., B. Schroeder, and R. L. Davis, 2000 Gene expression systems in Drosophila: a synthesis of time and space. J. Neurosci. 20: 2944–2953
4. Bellen, H. J., R. W. Levis, Y. He, J. W. Carlson, M. Evans-Holm et al., 2011 The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188: 731–743
5. Berry, J. A., I. Cervantes-Sandoval, E. P. Nicholas, and R. L. Davis, 2012 Dopamine is required for learning and forgetting in Drosophila. Neuron 74: 530–542
6. Brand, A. H., and N. Perrimon, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415
7. Byers, D., R. L. Davis, and J. A. Kiger, Jr.., 1981 Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289: 79–81
8. Cajigas, I. J., G. Tushev, T. J. Will, S. tom Dieck, N. Fuerst et al., 2012 The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74: 453–466
9. Chen, C. N., S. Denome, and R. L. Davis, 1986 Molecular analysis of cDNA clones and the corresponding genomic coding sequences of the Drosophila dunce+ gene, the structural gene for cAMP phosphodiesterase. Proc. Natl. Acad. Sci. USA 83: 9313–9317
10. Cheng, Y., K. Endo, K. Wu, A. R. Rodan, and R. L. Davis, 2001 Drosophila fasciclinII is required for the formation of odor memories for normal sensitivity to alcohol. Cell 105: 757–768
11. Connolly, J. B., I. J. Roberts, J. D. Armstrong, K. Kaiser, M. Forte et al., 1996 Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274: 2104–2107
12. Davis, R. L., 2005 Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu. Rev. Neurosci. 28: 275–302
13. Davis, R. L., and N. Davidson, 1986 The memory gene dunce+ encodes a remarkable set of RNAs with internal heterogeneity. Mol. Cell. Biol. 6: 1464–1470
14. Dubnau, J., A. S. Chiang, L. Grady, J. Barditch, S. Gossweiler et al., 2003 The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr. Biol. 13: 286–296
15. Dubruc, E., A. Putoux, A. Labalme, C. Rougeot, D. Sanlaville et al., 2014 A new intellectual disability syndrome caused by CTNNB1 haploinsufficiency. Am. J. Med. Genet. A. 164A: 1571–1575
16. Dudai, Y., Y. N. Jan, D. Byers, W. G. Quinn, and S. Benzer, 1976 dunce, a mutant of Drosophila deficient in learning. Proc. Natl. Acad. Sci. USA 73: 1684–1688
17. Foley, E., and P. H. O’Farrell, 2004 Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol. 2(8): e203
18. Folkers, E., P. Drain, and W. G. Quinn, 1993 Radish, a Drosophila mutant deficient in consolidated memory. Proc. Natl. Acad. Sci. USA 90: 8123–8127
19. Friggi-Grelin, F., H. Coulom, M. Meller, D. Gomez, J. Hirsh et al., 2003 Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54: 618–627
20. Green, E. W., G. Fedele, F. Giorgini, and C. P. Kyriacou, 2014 A Drosophila RNAi collection is subject to dominant phenotypic effects. Nat. Methods 11: 222–223
21. Grotewiel, M. S., C. D. O. Beck, K. H. Wu, X.-R. Zhu, and R. L. Davis, 1998 Integrin-mediated short-term memory in Drosophila. Nature 391: 455–460
22. Han, P. L., V. H. Meller, and R. L. Davis, 1996 The Drosophila brain revisited by enhancer detection. J. Neurobiol. 31: 88–102
23. Ho, I. S., F. Hannan, H.-F. Guo, I. Hakker, and Y. Zhong, 2007 Distinct functional domains of neurofibromatosis type1 regulate immediate vs. long-term memory formation. J. Neurosci. 27: 6852–6857
24. Hodas, J. J. L., A. Nehring, N. Ho, N. Hoche, M. J. Sweredoski et al., 2012 Dopaminergic modulation of the hippocampal neuropil proteome identified by bioorthogonal noncanonical amino acid tagging (BONCAT). Proteomics 12: 2464–2476
25. Jensen, L. R., M. Amende, U. Gurok, B. Moser, V. Gimmel et al., 2005 Mutations in the JARID1C gene, which is involved in transcriptional regulation and chromatin remodeling, cause X-linked mental retardation. Am. J. Hum. Genet. 76: 227–236
26. Jinek, M., K. Chylinski, I. Fonfara, M. Hauer, J. A. Doudna et al., 2012 A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816–821
27. Knapek, S., B. Gerber, and H. Tanimoto, 2010 Synapsin is selectively required for anesthesia-sensitive memory. Learn. Mem. 17: 76–79
28. Lee, Y. S., 2014 Genes and signaling pathways involved in memory enhancement in mutant mice. Mol. Brain 7: 43
29. Levin, L., P. L. Han, P. M. Hwang, P. G. Feinstein, R. L. Davis et al., 1992 The Drosophila learning and memory gene rutabaga encodes a Ca2+/calmodulin-responsive adenylyl cyclase. Cell 68: 479–489
30. Livingstone, M. S., P. P. Sziber, and W. G. Quinn, 1984 Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37: 205–215
31. Madalan, A., X. Yang, J. Ferris, S. Zhang, and G. Roman, 2011 G (o)activation is required for both appetitive and aversive memory acquisition in Drosophila. Learn. Mem. 19: 26–34
32. Magini, P., T. Pippucci, I. C. Tsai, S. Coppola, E. Stellacci et al., 2014 A mutation in PAK3 with a dual molecular effect deregulates the RAS/MAPK pathway and drives an X-linked syndromic phenotype. Hum. Mol. Genet. 23: 3607–3617
33. Mao, Z., and R. L. Davis, 2009 Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits 3: 5
34. McDonald, M.-L., C. MacMullen, D. J. Liu, S. M. Leal, and R. L. Davis, 2012 Genetic association of cyclic AMP signaling genes with bipolar disorder. Transl. Psychiatr. 2: e169
35. McGuire, S. E., G. Roman, and R. L. Davis, 2004 Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet. 20: 384–391
36. Moreau-Fauvarque, C., E. Taillebourg, T. Préat, and J. M. Dura, 2002 Mutation of linotte causes behavioral defects independently of pigeon in Drosophila. Neuroreport 13: 2309–2312
37. Najmabadi, H., H. Hu, M. Garshasbi, T. Zemojtel, S. S. Abedini et al., 2011 Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature 478: 57–63
38. Nighorn, A., M. Healy, and R. L. Davis, 1991 The cAMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in mushroom body neuropil. Neuron 6: 455–467
39. Qiu, Y., C. N. Chen, T. Malone, L. Richter, S. K. Beckendorf et al., 1991 Characterization of the memory gene dunce of Drosophila melanogaster. J. Mol. Biol. 222: 553–565
40. Quinn, W. G., P. P. Sziber, and R. Booker, 1979 The Drosophila memory mutant amnesiac. Nature 277: 212–214
41. Scheunemann, L., E. Jost, A. Richlitzi, J. P. Day, S. Sebastian et al., 2012 Consolidated and labile odor memory are separately encoded within the Drosophila brain. J. Neurosci. 32: 17163–17171
42. Schizophrenia Working Group of the Psychiatric Genomics Consortium, 2014 Biological insights from 108 schizophrenia-associated genetic loci. Nature 511: 421–427
43. Shuai, Y., B. Lu, Y. Hu, L. Wang, K. Sun et al., 2010 Forgetting is regulated through Rac activity in Drosophila. Cell 140: 579–589
44. Sternberg, S. H., S. Redding, M. Jinek, E. C. Greene, and J. A. Doudna, 2014 DNA interrogation by the CRISPR RNA-guided endonuclease Cas9 Nature 507: 62–67
45. Tempel, B. L., N. Bonini, D. R. Dawson, and W. G. Quinn, 1983 Reward learning in normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 80: 1482–1486
46. Tomchik, S., and R. L. Davis, 2013 Drosophila memory research through four eras: genetic, molecular biology, neuroanatomy, and systems neuroscience, pp. 359–377 in Invertebrate Learning and Memory, edited by R. Menzel, and P. Benjamin. Elsevier, London.
47. Tucci, V., T. Kleefstra, A. Hardy, I. Heise, S. Maggi et al., 2014 Dominant beta-catenin mutations cause intellectual disability with recognizable syndromic features. J. Clin. Invest. 124: 1468–1482
48. Tully, T., and W. G. Quinn, 1985 Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 157: 263–277
49. Tully, T., T. Preat, S. C. Boynton, and M. Del Vecchio, 1994 Genetic dissection of consolidated memory in Drosophila. Cell 79: 35–47
50. Venken, K. J., J. H. Simpson, and H. J. Bellen, 2011 Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72: 202–230
51. Willemsen, M. H., W. Ba, W. M. Wissink-Lindhout, A. P. de Brouwer, S. A. Haas et al., 2014 Involvement of the kinesin family members KIF4A and KIF5C in intellectual disability and synaptic function. J. Med. Genet. 51: 487–494.