A Novel Role for Ecdysone in Drosophila Conditioned Behavior: Linking GPCR-Mediated Non-canonical Steroid Action to cAMP Signaling in the Adult Brain

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Ishimoto, Hiroshi ^a,f   Wang, Zhe ^b   Rao, Yi ^c,d   Wu, Chun Fang ^b,e   Kitamoto, Toshihiro ^a,e  

^a UNIVERSITY OF IOWA   (United States)

^b The University of Iowa   (United States)

^c NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^d PEKING UNIVERSITY   (China)

^e UNIVERSITY OF IOWA   (United States)

^f NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CYCLIC AMP; CYCLIC AMP PHOSPHODIESTERASE; DOPAMINE; ECDYSONE RECEPTOR; ECDYSTERONE; ECDYSTERONE RECEPTOR; G PROTEIN COUPLED RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CONTROL; BRAIN FUNCTION; BRAIN LEVEL; CENTRAL NERVOUS SYSTEM; CONDITIONING; CONTROLLED STUDY; COURTSHIP; DOPAMINE METABOLISM; DOPECR GENE; DROSOPHILA; ENZYME SPECIFICITY; FEEDING; FEMALE; GENE; GENE OVEREXPRESSION; HORMONE ACTION; LOSS OF FUNCTION MUTATION; MALE; MEMORY DISORDER; MUSHROOM BODY; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; RUTABAGA GENE; SIGNAL TRANSDUCTION;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CYCLIC AMP; DROSOPHILA MELANOGASTER; ECDYSONE; ECDYSTEROIDS; ECDYSTERONE; LEARNING; MEMORY; MUSHROOM BODIES; MUTATION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, STEROID; SIGNAL TRANSDUCTION;

EID: 84887290106     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003843     Document Type: Article

References (70)

1. Bolhuis JJ, Gahr M, (2006) Neural mechanisms of birdsong memory. Nat Rev Neurosci 7: 347-357.
2. Moore FL, Boyd SK, Kelley DB, (2005) Historical perspective: Hormonal regulation of behaviors in amphibians. Horm Behav 48: 373-383.
3. McEwen B, (2002) Estrogen actions throughout the brain. Recent Prog Horm Res 57: 357-384.
4. Hampson E, (1990) Estrogen-related variations in human spatial and articulatory-motor skills. Psychoneuroendocrinology 15: 97-111.
5. McEwen BS, (2005) Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54: 20-23.
6. McEwen BS, Akama KT, Spencer-Segal JL, Milner TA, Waters EM, (2012) Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms. Behav Neurosci 126: 4-16.
7. McEwen BS, Kalia M, (2010) The role of corticosteroids and stress in chronic pain conditions. Metabolism 59 Suppl 1: S9-15.
8. Beato M, (1989) Gene regulation by steroid hormones. Cell 56: 335-344.
9. Losel RM, Falkenstein E, Feuring M, Schultz A, Tillmann HC, et al. (2003) Nongenomic steroid action: controversies, questions, and answers. Physiol Rev 83: 965-1016.
10. Hosie AM, Wilkins ME, da Silva HM, Smart TG, (2006) Endogenous neurosteroids regulate GABAA receptors through two discrete transmembrane sites. Nature 444: 486-489.
11. Park-Chung M, Wu FS, Purdy RH, Malayev AA, Gibbs TT, et al. (1997) Distinct sites for inverse modulation of N-methyl-D-aspartate receptors by sulfated steroids. Mol Pharmacol 52: 1113-1123.
12. Prager EM, Brielmaier J, Bergstrom HC, McGuire J, Johnson LR, (2010) Localization of mineralocorticoid receptors at mammalian synapses. PLoS One 5: e14344.
13. Groeneweg FL, Karst H, de Kloet ER, Joels M, (2012) Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol Cell Endocrinol 350: 299-309.
14. Pi M, Parrill AL, Quarles LD, (2010) GPRC6A mediates the non-genomic effects of steroids. J Biol Chem 285: 39953-39964.
15. Prossnitz ER, Barton M, (2011) The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol 7: 715-726.
16. Qiu J, Bosch MA, Tobias SC, Krust A, Graham SM, et al. (2006) A G-protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J Neurosci 26: 5649-5655.
17. Toran-Allerand CD, Guan X, MacLusky NJ, Horvath TL, Diano S, et al. (2002) ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci 22: 8391-8401.
18. Langer G, Bader B, Meoli L, Isensee J, Delbeck M, et al. (2010) A critical review of fundamental controversies in the field of GPR30 research. Steroids 75: 603-610.
19. Losel R, Wehling M, (2003) Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 4: 46-56.
20. Riddiford LM (1993) Hormones and Drosophila Development In: Bate M, Arias A. M., editor. The Development of Drosophila melanogaster. New York: Cold Spring Harbor Laboratory Press. pp. 899-929.
21. Riddiford LM, Cherbas P, Truman JW, (2000) Ecdysone receptors and their biological actions. Vitam Horm 60: 1-73.
22. Truman JW, Riddiford LM, (2002) Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 47: 467-500.
23. Flatt T, Heyland A, Rus F, Porpiglia E, Sherlock C, et al. (2008) Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J Exp Biol 211: 2712-2724.
24. Simon AF, Shih C, Mack A, Benzer S, (2003) Steroid control of longevity in Drosophila melanogaster. Science 299: 1407-1410.
25. Ishimoto H, Sakai T, Kitamoto T, (2009) Ecdysone signaling regulates the formation of long-term courtship memory in adult Drosophila melanogaster. Proc Natl Acad Sci U S A 106: 6381-6386.
26. Ishimoto H, Kitamoto T, (2010) The steroid molting hormone Ecdysone regulates sleep in adult Drosophila melanogaster. Genetics 185: 269-281.
27. Koelle MR, Talbot WS, Segraves WA, Bender MT, Cherbas P, et al. (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67: 59-77.
28. Thummel CS, (1996) Flies on steroids-Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12: 306-310.
29. Srivastava DP, Yu EJ, Kennedy K, Chatwin H, Reale V, et al. (2005) Rapid, nongenomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor. J Neurosci 25: 6145-6155.
30. Inagaki HK, Ben-Tabou de-Leon S, Wong AM, Jagadish S, Ishimoto H, et al. (2012) Visualizing Neuromodulation In Vivo: TANGO-Mapping of Dopamine Signaling Reveals Appetite Control of Sugar Sensing. Cell 148: 583-595.
31. Wyman RJ, Thomas JB, Salkoff L, King DG (1984) The Drosopohila giant fiber system.; Eaton RC, editor. New York: Plenum.
32. Tanouye MA, Wyman RJ, (1980) Motor outputs of giant nerve fiber in Drosophila. J Neurophysiol 44: 405-421.
33. Martinez VG, Javadi CS, Ngo E, Ngo L, Lagow RD, et al. (2007) Age-related changes in climbing behavior and neural circuit physiology in Drosophila. Dev Neurobiol 67: 778-791.
34. Elkins T, Ganetzky B, (1990) Conduction in the giant nerve fiber pathway in temperature-sensitive paralytic mutants of Drosophila. J Neurogenet 6: 207-219.
35. Thompson RF, Spencer WA, (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73: 16-43.
36. Engel JE, Wu CF, (1996) Altered habituation of an identified escape circuit in Drosophila memory mutants. J Neurosci 16: 3486-3499.
37. Engel JE, Wu CF, (1998) Genetic dissection of functional contributions of specific potassium channel subunits in habituation of an escape circuit in Drosophila. J Neurosci 18: 2254-2267.
38. Engel JE, Wu CF, (2009) Neurogenetic approaches to habituation and dishabituation in Drosophila. Neurobiology of Learning and Memory 92: 166-175.
39. Engel JE, Xie XJ, Sokolowski MB, Wu CF, (2000) A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant fiber escape circuit in Drosophila. Learn Mem 7: 341-352.
40. Zhang T, Wang Z, Wang L, Luo N, Jiang L, et al. (2013) Role of the DSC1 channel in regulating neuronal excitability in Drosophila melanogaster: extending nervous system stability under stress. PLoS Genetics 9: e1003327.
41. Griffith LC, Ejima A, (2009) Courtship learning in Drosophila melanogaster: diverse plasticity of a reproductive behavior. Learn Mem 16: 743-750.
42. Siegel RW, Hall JC, (1979) Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc Natl Acad Sci U S A 76: 3430-3434.
43. Osterwalder T, Yoon KS, White BH, Keshishian H, (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci U S A 98: 12596-12601.
44. Joiner MA, Griffith LC, (1999) Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn Mem 6: 177-192.
45. Sakai T, Sato S, Ishimoto H, Kitamoto T, (2012) Significance of the centrally expressed TRP channel painless in Drosophila courtship memory. Learn Mem 20: 34-40.
46. Aso Y, Grubel K, Busch S, Friedrich AB, Siwanowicz I, et al. (2009) The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23: 156-172.
47. Neubueser D, Warren JT, Gilbert LI, Cohen SM, (2005) Molting defective is required for ecdysone biosynthesis. Dev Biol 280: 362-372.
48. Chavez VM, Marques G, Delbecque JP, Kobayashi K, Hollingsworth M, et al. (2000) The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome P450 enzyme that regulates embryonic ecdysone levels. Development 127: 4115-4126.
49. Gilbert LI, (2004) Halloween genes encode P450 enzymes that mediate steroid hormone biosynthesis in Drosophila melanogaster. Molecular and Cellular Endocrinology 215: 1-10.
50. Neckameyer WS, (1998) Dopamine and mushroom bodies in Drosophila: experience-dependent and-independent aspects of sexual behavior. Learn Mem 5: 157-165.
51. Keleman K, Vrontou E, Kruttner S, Yu JY, Kurtovic-Kozaric A, et al. (2012) Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 489: 145-149.
52. Kandel ER, (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030-1038.
53. Levin LR, Han PL, Hwang PM, Feinstein PG, Davis RL, et al. (1992) The Drosophila learning and memory gene rutabaga encodes a Ca2+/Calmodulin-responsive adenylyl cyclase. Cell 68: 479-489.
54. Livingstone MS, Sziber PP, Quinn WG, (1984) Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37: 205-215.
55. O'Dell KM, Jamieson D, Goodwin SF, Kaiser K, (1999) Abnormal courtship conditioning in males mutant for the RI regulatory subunit of Drosophila protein kinase A. J Neurogenet 13: 105-118.
56. Mao Z, Roman G, Zong L, Davis RL, (2004) Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch. Proc Natl Acad Sci U S A 101: 198-203.
57. Han PL, Levin LR, Reed RR, Davis RL, (1992) Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9: 619-627.
58. Feany MB, (1990) Rescue of the learning defect in dunce, a Drosophila learning mutant, by an allele of rutabaga, a second learning mutant. Proc Natl Acad Sci U S A 87: 2795-2799.
59. Renger JJ, Ueda A, Atwood HL, Govind CK, Wu CF, (2000) Role of cAMP cascade in synaptic stability and plasticity: ultrastructural and physiological analyses of individual synaptic boutons in Drosophila memory mutants. J Neurosci 20: 3980-3992.
60. Chen CN, Denome S, Davis RL, (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 U S A 83: 9313-9317.
61. Dudai Y, Jan YN, Byers D, Quinn WG, Benzer S, (1976) dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci U S A 73: 1684-1688.
62. Duerr JS, Quinn WG, (1982) Three Drosophila mutations that block associative learning also affect habituation and sensitization. Proc Natl Acad Sci U S A 79: 3646-3650.
63. Shafer OT, Kim DJ, Dunbar-Yaffe R, Nikolaev VO, Lohse MJ, et al. (2008) Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58: 223-237.
64. Das S, Sadanandappa MK, Dervan A, Larkin A, Lee JA, et al. (2011) Plasticity of local GABAergic interneurons drives olfactory habituation. Proc Natl Acad Sci U S A 108: E646-654.
65. Ruffner ME, Cromarty SI, Cooper RL, (1999) Depression of synaptic efficacy in high- and low-output Drosophila neuromuscular junctions by the molting hormone (20-HE). J Neurophysiol 81: 788-794.
66. Cooper RL, Ruffner ME, (1998) Depression of synaptic efficacy at intermolt in crayfish neuromuscular junctions by 20-hydroxyecdysone, a molting hormone. J Neurophysiol 79: 1931-1941.
67. Woolley CS, (2007) Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47: 657-680.
68. Foster TC, (2005) Interaction of rapid signal transduction cascades and gene expression in mediating estrogen effects on memory over the life span. Front Neuroendocrinol 26: 51-64.
69. Fernandez SM, Lewis MC, Pechenino AS, Harburger LL, Orr PT, et al. (2008) Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J Neurosci 28: 8660-8667.
70. Han C, Jan LY, Jan YN, (2011) Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc Natl Acad Sci U S A 108: 9673-9678.