Anaplastic Lymphoma Kinase Acts in the Drosophila Mushroom Body to Negatively Regulate Sleep

PLoS Genetics

Volumn 11, Issue 11, 2015, Pages

  Bai, Lei ^a   Sehgal, Amita ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; NEUROFIBROMIN; PROTEIN TYROSINE KINASE;

ADULT; ALK GENE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE MUTATION; GENE REPRESSION; LEARNING; MALE; MEMORY; MUSHROOM BODY; MUTATIONAL ANALYSIS; NF1 GENE; NONHUMAN; PHENOTYPE; SEX DIFFERENCE; SLEEP; ANIMAL; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; DROSOPHILA; MUSHROOM BODIES; RECEPTOR PROTEIN-TYROSINE KINASES; SLEEP;

EID: 84949256758     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005611     Document Type: Article

References (66)

1. Hartse KM, (2011) The phylogeny of sleep. Handb Clin Neurol 98: 97–109. doi: 10.1016/B978-0-444-52006-7.00007-1 21056182
2. Wang G, Grone B, Colas D, Appelbaum L, Mourrain P, (2011) Synaptic plasticity in sleep: learning, homeostasis and disease. Trends Neurosci 34: 452–463. doi: 10.1016/j.tins.2011.07.005 21840068
3. Tononi G, Cirelli C, (2014) Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81: 12–34. doi: 10.1016/j.neuron.2013.12.025 24411729
4. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G, (2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci 11: 200–208. doi: 10.1038/nn2035 18204445
5. Gilestro GF, Tononi G, Cirelli C, (2009) Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324: 109–112. doi: 10.1126/science.1166673 19342593
6. Stickgold R, Hobson JA, Fosse R, Fosse M, (2001) Sleep, learning, and dreams: off-line memory reprocessing. Science 294: 1052–1057. 11691983
7. Florian C, Vecsey CG, Halassa MM, Haydon PG, Abel T, (2011) Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice. J Neurosci 31: 6956–6962. doi: 10.1523/JNEUROSCI.5761-10.2011 21562257
8. Seugnet L, Suzuki Y, Vine L, Gottschalk L, Shaw PJ, (2008) D1 receptor activation in the mushroom bodies rescues sleep-loss-induced learning impairments in Drosophila. Curr Biol 18: 1110–1117. doi: 10.1016/j.cub.2008.07.028 18674913
9. Li X, Yu F, Guo A, (2009) Sleep deprivation specifically impairs short-term olfactory memory in Drosophila. Sleep 32: 1417–1424. 19928381
10. Bushey D, Cirelli C, (2011) From genetics to structure to function: exploring sleep in Drosophila. Int Rev Neurobiol 99: 213–244. doi: 10.1016/B978-0-12-387003-2.00009-4 21906542
11. Palmer RH, Vernersson E, Grabbe C, Hallberg B, (2009) Anaplastic lymphoma kinase: signalling in development and disease. Biochem J 420: 345–361. doi: 10.1042/BJ20090387 19459784
12. Iwahara T, Fujimoto J, Wen D, Cupples R, Bucay N, et al. (1997) Molecular characterization of ALK, a receptor tyrosine kinase expressed specifically in the nervous system. Oncogene 14: 439–449. 9053841
13. Loren CE, Scully A, Grabbe C, Edeen PT, Thomas J, et al. (2001) Identification and characterization of DAlk: a novel Drosophila melanogaster RTK which drives ERK activation in vivo. Genes Cells 6: 531–544. 11442633
14. Gouzi JY, Moressis A, Walker JA, Apostolopoulou AA, Palmer RH, et al. (2011) The receptor tyrosine kinase Alk controls neurofibromin functions in Drosophila growth and learning. PLoS Genet 7: e1002281. doi: 10.1371/journal.pgen.1002281 21949657
15. Lee HH, Norris A, Weiss JB, Frasch M, (2003) Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers. Nature 425: 507–512. 14523446
16. Englund C, Loren CE, Grabbe C, Varshney GK, Deleuil F, et al. (2003) Jeb signals through the Alk receptor tyrosine kinase to drive visceral muscle fusion. Nature 425: 512–516. 14523447
17. Bazigou E, Apitz H, Johansson J, Loren CE, Hirst EM, et al. (2007) Anterograde Jelly belly and Alk receptor tyrosine kinase signaling mediates retinal axon targeting in Drosophila. Cell 128: 961–975. 17350579
18. Cheng LY, Bailey AP, Leevers SJ, Ragan TJ, Driscoll PC, et al. (2011) Anaplastic lymphoma kinase spares organ growth during nutrient restriction in Drosophila. Cell 146: 435–447. doi: 10.1016/j.cell.2011.06.040 21816278
19. Rohrbough J, Kent KS, Broadie K, Weiss JB, (2013) Jelly Belly trans-synaptic signaling to anaplastic lymphoma kinase regulates neurotransmission strength and synapse architecture. Dev Neurobiol 73: 189–208. doi: 10.1002/dneu.22056 22949158
20. Bilsland JG, Wheeldon A, Mead A, Znamenskiy P, Almond S, et al. (2008) Behavioral and neurochemical alterations in mice deficient in anaplastic lymphoma kinase suggest therapeutic potential for psychiatric indications. Neuropsychopharmacology 33: 685–700. 17487225
21. Weiss JB, Xue C, Benice T, Xue L, Morris SW, et al. (2012) Anaplastic lymphoma kinase and leukocyte tyrosine kinase: functions and genetic interactions in learning, memory and adult neurogenesis. Pharmacol Biochem Behav 100: 566–574. doi: 10.1016/j.pbb.2011.10.024 22079349
22. Williams JA, Su HS, Bernards A, Field J, Sehgal A, (2001) A circadian output in Drosophila mediated by neurofibromatosis-1 and Ras/MAPK. Science 293: 2251–2256. 11567138
23. Loren CE, Englund C, Grabbe C, Hallberg B, Hunter T, et al. (2003) A crucial role for the Anaplastic lymphoma kinase receptor tyrosine kinase in gut development in Drosophila melanogaster. EMBO Rep 4: 781–786. 12855999
24. Zimmerman JE, Chan MT, Jackson N, Maislin G, Pack AI, . (2012) Genetic background has a major impact on differences in sleep resulting from environmental influences in Drosophila. Sleep 35:545–57. doi: 10.5665/sleep.1744 22467993
25. Ryder E, Blows F, Ashburner M, Bautista-Llacer R, Coulson D, et al. (2004) The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167:797–813. 15238529
26. Low KH, Lim C, Ko HW, Edery I, (2008) Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron 60: 1054–1067. doi: 10.1016/j.neuron.2008.10.048 19109911
27. Zimmerman JE, Raizen DM, Maycock MH, Maislin G, Pack AI, (2008) A video method to study Drosophila sleep. Sleep 31: 1587–1598. 19014079
28. Faville R, Kottler B, Goodhill GJ, Shaw PJ, van Swinderen B, (2015) How deeply does your mutant sleep? Probing arousal to better understand sleep defects in Drosophila. Sci Rep 5: 8454. doi: 10.1038/srep08454 25677943
29. Barone MC, Bohmann D, (2013) Assessing neurodegenerative phenotypes in Drosophila dopaminergic neurons by climbing assays and whole brain immunostaining. J Vis Exp: e50339. doi: 10.3791/50339 23644755
30. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, et al. (2000) Rest in Drosophila is a sleep-like state. Neuron 25: 129–138. 10707978
31. Andretic R, van Swinderen B, Greenspan RJ, (2005) Dopaminergic modulation of arousal in Drosophila. Curr Biol 15: 1165–1175. 16005288
32. Kume K, Kume S, Park SK, Hirsh J, Jackson FR, (2005) Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25: 7377–7384. 16093388
33. Joiner WJ, Crocker A, White BH, Sehgal A, (2006) Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441: 757–760. 16760980
34. Pitman JL, McGill JJ, Keegan KP, Allada R, (2006) A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441: 753–756. 16760979
35. Donlea JM, Thimgan MS, Suzuki Y, Gottschalk L, Shaw PJ, (2011) Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 332: 1571–1576. doi: 10.1126/science.1202249 21700877
36. Foltenyi K, Greenspan RJ, Newport JW, (2007) Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat Neurosci 10: 1160–1167. 17694052
37. Crocker A, Shahidullah M, Levitan IB, Sehgal A, (2010) Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65: 670–681. doi: 10.1016/j.neuron.2010.01.032 20223202
38. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E, et al. (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60: 672–682. doi: 10.1016/j.neuron.2008.10.042 19038223
39. Sheeba V, Fogle KJ, Kaneko M, Rashid S, Chou YT, et al. (2008) Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18: 1537–1545. doi: 10.1016/j.cub.2008.08.033 18771923
40. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL, (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765–1768. 14657498
41. Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S, (2007) Sequential use of mushroom body neuron subsets during drosophila odor memory processing. Neuron 53: 103–115. 17196534
42. 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. doi: 10.1080/01677060802471718 19140035
43. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, et al. (2012) A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2: 991–1001. doi: 10.1016/j.celrep.2012.09.011 23063364
44. Licis AK, Vallorani A, Gao F, Chen C, Lenox J, et al. (2013) Prevalence of Sleep Disturbances in Children With Neurofibromatosis Type 1. J Child Neurol 28: 1400–1405. 24065580
45. Leschziner GD, Golding JF, Ferner RE, (2013) Sleep disturbance as part of the neurofibromatosis type 1 phenotype in adults. Am J Med Genet A 161A: 1319–1322. doi: 10.1002/ajmg.a.35915 23636844
46. The I, Hannigan GE, Cowley GS, Reginald S, Zhong Y, et al. (1997) Rescue of a Drosophila NF1 mutant phenotype by protein kinase A. Science 276: 791–794. 9115203
47. Guo HF, Tong J, Hannan F, Luo L, Zhong Y, (2000) A neurofibromatosis-1-regulated pathway is required for learning in Drosophila. Nature 403: 895–898. 10706287
48. Shinkai Y, Yamamoto Y, Fujiwara M, Tabata T, Murayama T, et al. (2011) Behavioral choice between conflicting alternatives is regulated by a receptor guanylyl cyclase, GCY-28, and a receptor tyrosine kinase, SCD-2, in AIA interneurons of Caenorhabditis elegans. J Neurosci 31: 3007–3015. doi: 10.1523/JNEUROSCI.4691-10.2011 21414922
49. Lasek AW, Gesch J, Giorgetti F, Kharazia V, Heberlein U, (2011) Alk is a transcriptional target of LMO4 and ERalpha that promotes cocaine sensitization and reward. J Neurosci 31: 14134–14141. doi: 10.1523/JNEUROSCI.3415-11.2011 21976498
50. Lasek AW, Lim J, Kliethermes CL, Berger KH, Joslyn G, et al. (2011) An evolutionary conserved role for anaplastic lymphoma kinase in behavioral responses to ethanol. PLoS One 6: e22636. doi: 10.1371/journal.pone.0022636 21799923
51. Vanderheyden WM, Gerstner JR, Tanenhaus A, Yin JC, Shaw PJ, (2013) ERK phosphorylation regulates sleep and plasticity in Drosophila. PLoS One 8: e81554. doi: 10.1371/journal.pone.0081554 24244744
52. Buchanan ME, Davis RL, (2010) A distinct set of Drosophila brain neurons required for neurofibromatosis type 1-dependent learning and memory. J Neurosci 30: 10135–10143. doi: 10.1523/JNEUROSCI.0283-10.2010 20668197
53. Harbison ST, McCoy LJ, Mackay TF, (2013) Genome-wide association study of sleep in Drosophila melanogaster. BMC Genomics 14: 281. doi: 10.1186/1471-2164-14-281 23617951
54. Diggs-Andrews KA, Brown JA, Gianino SM, Rubin JB, Wozniak DF, et al. (2014) Sex Is a major determinant of neuronal dysfunction in neurofibromatosis type 1. Ann Neurol 75: 309–316. doi: 10.1002/ana.24093 24375753
55. Bushey D, Tononi G, Cirelli C, (2011) Sleep and synaptic homeostasis: structural evidence in Drosophila. Science 332: 1576–1581. doi: 10.1126/science.1202839 21700878
56. Bushey D, Tononi G, Cirelli C, (2009) The Drosophila fragile X mental retardation gene regulates sleep need. J Neurosci 29: 1948–1961. doi: 10.1523/JNEUROSCI.4830-08.2009 19228950
57. Rohrbough J, Broadie K, (2010) Anterograde Jelly belly ligand to Alk receptor signaling at developing synapses is regulated by Mind the gap. Development 137: 3523–3533. doi: 10.1242/dev.047878 20876658
58. Tsai PI, Wang M, Kao HH, Cheng YJ, Walker JA, et al. (2012) Neurofibromin mediates FAK signaling in confining synapse growth at Drosophila neuromuscular junctions. J Neurosci 32: 16971–16981. doi: 10.1523/JNEUROSCI.1756-12.2012 23175848
59. Walker JA, Gouzi JY, Long JB, Huang S, Maher RC, et al. (2013) Genetic and functional studies implicate synaptic overgrowth and ring gland cAMP/PKA signaling defects in the Drosophila melanogaster neurofibromatosis-1 growth deficiency. PLoS Genet 9: e1003958. doi: 10.1371/journal.pgen.1003958 24278035
60. Cavanaugh DJ, Geratowski JD, Wooltorton JR, Spaethling JM, Hector CE, et al. (2014) Identification of a circadian output circuit for rest:activity rhythms in Drosophila. Cell 157: 689–701. doi: 10.1016/j.cell.2014.02.024 24766812
61. Donlea JM, Ramanan N, Shaw PJ, (2009) Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324: 105–108. doi: 10.1126/science.1166657 19342592
62. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415. 8223268
63. Gohl DM, Silies MA, Gao XJ, Bhalerao S, Luongo FJ, et al. (2011) A versatile in vivo system for directed dissection of gene expression patterns. Nat Methods 8: 231–237. 21473015
64. Salvaterra P.M., Kitamoto T., (2001). Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. Brain Res. Gene Expr. Patterns 1: 73–82.
65. Siegmund T, Korge G, (2001) Innervation of the ring gland of Drosophila melanogaster. J Comp Neurol 431: 481–491. 11223816
66. Kayser MS, Yue Z, Sehgal A, (2014). A critical period of sleep for development of courtship circuitry and behavior in Drosophila. Science 344:269–74. doi: 10.1126/science.1250553 24744368