The Drosophila neuropeptides PDF and sNPF have opposing electrophysiological and molecular effects on central neurons

Journal of Neurophysiology

Volumn 111, Issue 5, 2014, Pages 1033-1045

  Vecsey, Christopher G ^a   Pírez, Nicolás ^a   Griffith, Leslie C ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

cAMP; Pigment dispersing factor; Sleep; Small neuropeptide F

Indexed keywords

CYCLIC AMP; NEUROPEPTIDE; PERTUSSIS TOXIN; PIGMENT DISPERSING FACTOR; SMALL NEUROPEPTIDE F; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CALCIUM CELL LEVEL; DEPOLARIZATION; DROSOPHILA MELANOGASTER; EXCITABILITY; FEEDING; FEMALE; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYPERPOLARIZATION; MALE; MEMBRANE STEADY POTENTIAL; METABOLISM; MOTONEURON; NERVE CELL NETWORK; NONHUMAN; OOCYTE; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; RHYTHM; RNA INTERFERENCE; SLEEP; VENTRAL ROOT; XENOPUS LAEVIS;

CAMP; PIGMENT DISPERSING FACTOR; SLEEP; SMALL NEUROPEPTIDE F;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MOTOR NEURONS; NEUROPEPTIDES;

EID: 84900816670     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00712.2013     Document Type: Article

References (86)

1. Aton SJ, Colwell CS, Harmar AJ, Waschek J, Herzog ED. Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci 8: 476-483, 2005.
2. Beck B. KO's and organisation of peptidergic feeding behavior mechanisms. Neurosci Biobehav Rev 25: 143-158, 2001.
3. Betke KM, Wells CA, Hamm HE. GPCR mediated regulation of synaptic transmission. Progr Neurobiol 96: 304-321, 2012.
4. Caers J, Verlinden H, Zels S, Vandersmissen HP, Vuerinckx K, Schoofs L. More than two decades of research on insect neuropeptide GPCRs: an overview. Front Endocrinol (Lausanne) 3: 151, 2012.
5. Carlsson MA, Enell LE, Nassel DR. Distribution of short neuropeptide F and its receptor in neuronal circuits related to feeding in larval Drosophila. Cell Tissue Res 353: 511-523, 2013.
6. Cattaert D, Birman S. Blockade of the central generator of locomotor rhythm by noncompetitive NMDA receptor antagonists in Drosophila larvae. J Neurobiol 48: 58-73, 2001.
7. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, Fitch TE, Nakazato M, Hammer RE, Saper CB, Yanagisawa M. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98: 437-451, 1999.
8. Chen W, Shi W, Li L, Zheng Z, Li T, Bai W, Zhao Z. Regulation of sleep by the short neuropeptide F (sNPF) in Drosophila melanogaster. Insect Biochem Mol Biol 43: 809-819, 2013.
9. Chintapalli VR, Wang J, Dow JA. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39: 715-720, 2007.
10. Choi C, Cao G, Tanenhaus AK, McCarthy EV, Jung M, Schleyer W, Shang Y, Rosbash M, Yin JC, Nitabach MN. Autoreceptor control of peptide/neurotransmitter corelease from PDF neurons determines allocation of circadian activity in drosophila. Cell Rep 2: 332-344, 2012.
11. Choi C, Fortin JP, McCarthy E, Oksman L, Kopin AS, Nitabach MN. Cellular dissection of circadian peptide signals with genetically encoded membrane-tethered ligands. Curr Biol 19: 1167-1175, 2009.
12. Choi JC, Park D, Griffith LC. Electrophysiological and morphological characterization of identified motor neurons in the Drosophila third instar larva central nervous system. J Neurol 91: 2353-2365, 2004.
13. Chung BY, Kilman VL, Keath JR, Pitman JL, Allada R. The GABA(A) receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr Biol 19: 386-390, 2009.
14. Clynen E, Reumer A, Baggerman G, Mertens I, Schoofs L. Neuropeptide biology in Drosophila. Adv Exp Med Biol 692: 192-210, 2010.
15. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS, Frankel WN 2nd, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95: 322-327, 1998.
16. Duffy JB. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34: 1-15, 2002.
17. Duvall LB, Taghert PH. The circadian neuropeptide PDF signals preferentially through a specific adenylate cyclase isoform AC3 in M pacemakers of Drosophila. PLoS Biol 10: e1001337, 2012.
18. Duvall LB, Taghert PH. E and M circadian pacemaker neurons use different PDF receptor signalosome components in Drosophila. J Biol Rhythms 28: 239-248, 2013.
19. Dyzma M, Boudjeltia KZ, Faraut B, Kerkhofs M. Neuropeptide Y and sleep. Sleep Med Rev 14: 161-165, 2010.
20. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N. Computer control of microscopes using microManager. Curr Protoc Mol Biol 14: Unit 14.20, 2010.
21. Feng G, Reale V, Chatwin H, Kennedy K, Venard R, Ericsson C, Yu K, Evans PD, Hall LM. Functional characterization of a neuropeptide F-like receptor from Drosophila melanogaster. Eur J Neurosci 18: 227-238, 2003.
22. Ferris J, Ge H, Liu L, Roman G. G(o) signaling is required for Drosophila associative learning. Nat Neurosci 9: 1036-1040, 2006.
23. Fox LE, Soll DR, Wu CF. Coordination and modulation of locomotion pattern generators in Drosophila larvae: effects of altered biogenic amine levels by the tyramine beta hydroxlyase mutation. J Neurosci 26: 1486-1498, 2006.
24. Garczynski SF, Brown MR, Crim JW. Structural studies of Drosophila short neuropeptide F: occurrence and receptor binding activity. Peptides 27: 575-582, 2006.
25. Guo F, Yi W, Zhou M, Guo A. Go signaling in mushroom bodies regulates sleep in Drosophila. Sleep 34: 273-281, 2011.
26. Harrison NL. Mechanisms of sleep induction by GABA(A) receptor agonists. J Clin Psychiatry 68, Suppl 5: 6-12, 2007.
27. Helfrich-Forster C. The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci USA 92: 612-616, 1995.
28. Hendry SH, Schwark HD, Jones EG, Yan J. Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7: 1503-1519, 1987.
29. Hewes RS, Taghert PH. Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res 11: 1126-1142, 2001.
30. Hong SH, Lee KS, Kwak SJ, Kim AK, Bai H, Jung MS, Kwon OY, Song WJ, Tatar M, Yu K. Minibrain/Dyrk1a regulates food intake through the Sir2-FOXO-sNPF/NPY pathway in Drosophila and mammals. PLoS Genetics 8: e1002857, 2012.
31. Hyun S, Lee Y, Hong ST, Bang S, Paik D, Kang J, Shin J, Lee J, Jeon K, Hwang S, Bae E, Kim J. Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48: 267-278, 2005.
32. Im SH, Taghert PH. PDF receptor expression reveals direct interactions between circadian oscillators in Drosophila. J Comp Neurol 518: 1925-1945, 2010.
33. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotech 21: 635-637, 2003.
34. Jiang M, Bajpayee NS. Molecular mechanisms of go signaling. Neurosignals 17: 23-41, 2009.
35. Johard HA, Yoishii T, Dircksen H, Cusumano P, Rouyer F, Helfrich- Forster C, Nassel DR. Peptidergic clock neurons in Drosophila: ion transport peptide and short neuropeptide F in subsets of dorsal and ventral lateral neurons. J Comp Neurol 516: 59-73, 2009.
36. Kapan N, Lushchak OV, Luo J, Nassel DR. Identified peptidergic neurons in the Drosophila brain regulate insulin-producing cells, stress responses and metabolism by coexpressed short neuropeptide F and corazonin. Cell Mol Life Sci 2012 Jul 25 [Epub ahead of print]
37. Katanayeva N, Kopein D, Portmann R, Hess D, Katanaev VL. Competing activities of heterotrimeric G proteins in Drosophila wing maturation. PLoS One 5: e12331, 2010.
38. Larhammar D, Salaneck E. Molecular evolution of NPY receptor subtypes. Neuropeptides 38: 141-151, 2004.
39. Lawrence CB, Turnbull AV, Rothwell NJ. Hypothalamic control of feeding. Curr Opin Neurobiol 9: 778-783, 1999.
40. Lear BC, Merrill CE, Lin JM, Schroeder A, Zhang L, Allada R. A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 48: 221-227, 2005.
41. Lear BC, Zhang L, Allada R. The neuropeptide PDF acts directly on evening pacemaker neurons to regulate multiple features of circadian behavior. PLoS Biol 7: e1000154, 2009.
42. Lee KS, Hong SH, Kim AK, Ju SK, Kwon OY, Yu K. Processed short neuropeptide F peptides regulate growth through the ERK-insulin pathway in Drosophila melanogaster. FEBS Lett 583: 2573-2577, 2009.
43. Lee KS, Kwon OY, Lee JH, Kwon K, Min KJ, Jung SA, Kim AK, You KH, Tatar M, Yu K. Drosophila short neuropeptide F signalling regulates growth by ERK-mediated insulin signalling. Nat Cell Biol 10: 468-475, 2008.
44. Lee KS, You KH, Choo JK, Han YM, Yu K. Drosophila short neuropeptide F regulates food intake and body size. J Biol Chem 279: 50781-50789, 2004.
45. Lin L, Faraco J, Li R, Kadotani H, Rogers W, Lin X, Qiu X, de Jong PJ, Nishino S, Mignot E. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98: 365-376, 1999.
46. Mahr A, Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr 6: 299-309, 2006.
47. Mertens I, Meeusen T, Huybrechts R, De Loof A, Schoofs L. Characterization of the short neuropeptide F receptor from Drosophila melanogaster. Biochem Biophys Res Commun 297: 1140-1148, 2002.
48. Mertens I, Vandingenen A, Johnson EC, Shafer OT, Li W, Trigg JS, De Loof A, Schoofs L, Taghert PH. PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48: 213-219, 2005.
49. Nassel DR, Enell LE, Santos JG, Wegener C, Johard HA. A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions. BMC Neurosci 9: 90, 2008.
50. Nassel DR, Wegener C. A comparative review of short and long neuropeptide F signaling in invertebrates: Any similarities to vertebrate neuropeptide Y signaling? Peptides 32: 1335-1355, 2011.
51. Nassel DR, Winther AM. Drosophila neuropeptides in regulation of physiology and behavior. Progr Neurobiol 92: 42-104, 2010.
52. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ. Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279: 37215-37218, 2004.
53. Nikolaev VO, Lohse MJ. Monitoring of cAMP synthesis and degradation in living cells. Physiology (Bethesda, Md) 21: 86-92, 2006.
54. Pakhotin P, Harmar AJ, Verkhratsky A, Piggins H. VIP receptors control excitability of suprachiasmatic nuclei neurones. Pflügers Arch 452: 7-15, 2006.
55. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E, Hodge JJ, Kang K, Liu X, Garrity PA, Rosbash M, Griffith LC. PDF cells are a GABAresponsive wake-promoting component of the Drosophila sleep circuit. Neuron 60: 672-682, 2008.
56. Persson MG, Eklund MB, Dircksen H, Muren JE, Nassel DR. Pigmentdispersing factor in the locust abdominal ganglia may have roles as circulating neurohormone and central neuromodulator. J Neurobiol 48: 19-41, 2001.
57. Pírez N, Christmann BL, Griffith LC. Daily rhythms in locomotor circuits in Drosophila involve pigment-dispersing factor (PDF). J Neurophysiol 110: 700-708, 2013.
58. + pump current dynamics. Nat Neurosci 13: 53-59, 2010.
59. + channels by a cloned Drosophila melanogaster neuropeptide F-like receptor. Eur J Neurosci 19: 570-576, 2004.
60. Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99: 791-802, 1999.
61. Rohrbough J, Broadie K. Electrophysiological analysis of synaptic transmission in central neurons of Drosophila larvae. J Neurol 88: 847-860, 2002.
62. Root CM, Ko KI, Jafari A, Wang JW. Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145: 133-144, 2011.
63. Ryglewski S, Lance K, Levine RB, Duch C. Ca(v)2 channels mediate low and high voltage-activated calcium currents in Drosophila motoneurons. J Physiol 590: 809-825, 2012.
64. Sahara S, Yanagawa Y, O'Leary DD, Stevens CF. The fraction of cortical GABAergic neurons is constant from near the start of cortical neurogenesis to adulthood. J Neurosci 32: 4755-4761, 2012.
65. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richarson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G proteincoupled receptors that regulate feeding behavior. Cell 92: 1 page following 696, 1998.
66. Schaefer JE, Worrell JW, Levine RB. Role of intrinsic properties in Drosophila motoneuron recruitment during fictive crawling. J Neurophysiol 104: 1257-1266, 2010.
67. Seamon KB, Daly JW. Forskolin: its biological and chemical properties. Adv Cyclic Nucleotide Protein Phosphorylation Res 20: 1-150, 1986.
68. Seinen E, Burgerhof JG, Jansen RC, Sibon OC. RNAi-induced off-target effects in Drosophila melanogaster: frequencies and solutions. Brief Funct Genomics 10: 206-214, 2011.
69. Shafer OT, Kim DJ, Dunbar-Yaffe R, Nikolaev VO, Lohse MJ, Taghert PH. Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58: 223-237, 2008.
70. Shang Y, Donelson NC, Vecsey CG, Guo F, Rosbash M, Griffith LC. Short neuropeptide F is a sleep-promoting inhibitory modulator. Neuron 80: 171-183, 2013.
71. Sheeba V, Fogle KJ, Kaneko M, Rashid S, Chou YT, Sharma VK, Holmes TC. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18: 1537-1545, 2008.
72. Srinivasan S, Lance K, Levine RB. Contribution of EAG to excitability and potassium currents in Drosophila larval motoneurons. J Neurophysiol 107: 2660-2671, 2012a
73. Srinivasan S, Lance K, Levine RB. Segmental differences in firing properties and potassium currents in Drosophila larval motoneurons. J Neurophysiol 107: 1356-1365, 2012b
74. Taghert PH, Nitabach MN. Peptide neuromodulation in invertebrate model systems. Neuron 76: 82-97, 2012.
75. Talsma AD, Christov CP, Terriente-Felix A, Linneweber GA, Perea D, Wayland M, Shafer OT, Miguel-Aliaga I. Remote control of renal physiology by the intestinal neuropeptide pigment-dispersing factor in Drosophila. Proc Natl Acad Sci USA 109: 12177-12182, 2012.
76. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875-881, 2009
77. van den Pol AN. Neuropeptide transmission in brain circuits. Neuron 76: 98-115, 2012.
78. Vanden Broeck J. Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster. Peptides 22: 241-254, 2001.
79. Venken KJ, Simpson JH, Bellen HJ. Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72: 202-230, 2011.
80. Vosko AM, Schroeder A, Loh DH, Colwell CS. Vasoactive intestinal peptide and the mammalian circadian system. Gen Comp Endocrinol 152: 165-175, 2007.
81. Wagner CA, Friedrich B, Setiawan I, Lang F, Broer S. The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell Physiol Biochem 10: 1-12, 2000.
82. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112: 271-282, 2003.
83. Wegener C, Reinl T, Jansch L, Predel R. Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma-specific peptide expression and differential processing. J Neurochem 96: 1362-1374, 2006.
84. 2+ currents in identified Drosophila motoneurons in situ. J Neurophysiol 100: 868-878, 2008.
85. Wu Y, Cao G, Nitabach MN. Electrical silencing of PDF neurons advances the phase of non-PDF clock neurons in Drosophila. J Biol Rhythms 23: 117-128, 2008.
86. Yoshii T, Wulbeck C, Sehadova H, Veleri S, Bichler D, Stanewsky R, Helfrich-Forster C. The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila's clock. J Neurosci 29: 2597-2610, 2009.