Multiple neuropeptides in the drosophila antennal lobe suggest complex modulatory circuits

Journal of Comparative Neurology

Volumn 518, Issue 16, 2010, Pages 3359-3380

  Carlsson, Mikael A ^a   Diesner, Max ^b   Schachtner, Joachim ^b   Nässel, Dick R ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

immunocytochemistry; insect brain; mass spectrometry; neuromodulation; olfaction

Indexed keywords

ALLATOSTATIN; ALLATOSTATIN A; IPNAMIDE; MYOINHIBITORY PEPTIDE; MYOSUPPRESSIN; NEUROPEPTIDE; NEUROPEPTIDE F; NEUROTRANSMITTER; SIFAMIDE; TACHYKININ; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HORMONE ANTAGONIST;

ANTENNA; ARTICLE; CONTROLLED STUDY; DROSOPHILA; IMMUNOHISTOCHEMISTRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NEUROTRANSMISSION; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENSORY NERVE CELL; AMINO ACID SEQUENCE; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN; CHEMISTRY; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; INTERNEURON; MALE; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; ODOR; OLFACTORY RECEPTOR; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; HORMONE ANTAGONISTS; INTERNEURONS; MALE; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SIGNAL TRANSDUCTION; SMELL; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 77954593419     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22405     Document Type: Article

References (88)

1. Anton S, Homberg U. 1999. Antennal lobe structure. In: Hans-son BS, editor. Insect olfaction. Berlin: Springer. p 97-124.
2. Baggerman G, Cerstiaens A, De Loof A, Schoofs L. 2002. Pep-tidomics of the larval Drosophila melanogaster central nervous system. J Biol Chem 277:40368-40374.
3. Baggerman G, Boonen K, Verleyen P, De Loof A, Schoofs L. 2005. Peptidomic analysis of the larval Drosophila mela-nogaster central nervous system by two-dimensional capillary liquid chromatography quadrupole time-of-flight mass spectrometry. J Mass Spectrom 40:250-260.
4. Benton R. 2008. Chemical sensing in Drosophila. Curr Opin Neurobiol 18:357-363.
5. Berg BG, Schachtner J, Utz S, Homberg U. 2007. Distribution of neuropeptides in the primary olfactory center of the heliothine moth Heliothis virescens. Cell Tissue Res 327: 385-398.
6. Berg BG, Schachtner J, Homberg U. 2009. Gamma-aminobuty-ric acid immunostaining in the antennal lobe of the moth Heliothis virescens and its colocalization with neuropepti-des. Cell Tissue Res 335:593-605.
7. Blackburn MB, Wagner RM, Kochansky JP, Harrison DJ, Thomas-Laemont P, Raina AK. 1995. The identification of two myoinhibitory peptides, with sequence similarities to the galanins, isolated from the ventral nerve cord of Man-duca sexta. Regul Pept 57:213-219.
8. Blackburn MB, Jaffe H, Kochansky J, Raina AK. 2001. Identification of four additional myoinhibitory peptides (MIPs) from the ventral nerve cord of Manduca sexta. Arch Insect Biochem Physiol 48:121-128.
9. Brockmann A, Annangudi SP, Richmond TA, Ament SA, Xie F, Southey BR, Rodriguez-Zas SR, Robinson GE, Sweedler JV. 2009. Quantitative peptidomics reveal brain peptide signatures of behavior. Proc Natl Acad Sci USA 106: 2383-2388.
10. Brown MR, Klowden MJ, Crim JW, Young L, Shrouder LA, Lea AO. 1994. Endogenous regulation of mosquito host-seeking behavior by a neuropeptide. J Insect Physiol 40:399-406.
11. Buchner E, Buchner S, Crawford G, Mason WT, Salvaterra PM, Satelle DB. 1986. Cholineacetyltransferase-like immunore-activity in the brain of Drosophila melanogaster. Cell Tissue Res 246:57-62.
12. Busch S, Selcho M, Ito K, Tanimoto H. 2009. A map of octo-paminergic neurons in the Drosophila brain. J Comp Neurol 513:643-667.
13. Couto A, Alenius M, Dickson BJ. 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535-1547.
14. Dacks AM, Christensen TA, Hildebrand JG. 2006. Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498:727-746.
15. Dacks AM, Christensen TA, Hildebrand JG. 2008. Modulation of olfactory information processing in the antennal lobe of Manduca sexta by serotonin. J Neurophysiol 99:2077-2085.
16. Dacks AM, Green DS, Root CM, Nighorn AJ, Wang JW. 2009. Serotonin modulates olfactory processing in the antennal lobe of Drosophila. J Neurogenet 23:1-13.
17. Daniels RW, Gelfand MV, Collins CA, DiAntonio A. 2008. Visualizing glutamatergic cell bodies and synapses in Drosoph-ila larval and adult CNS. J Comp Neurol 508:131-152.
18. Das A, Sen S, Lichtneckert R, Okada R, Ito K, Rodrigues V, Reichert H. 2008. Drosophila olfactory local interneurons and projection neurons derive from a common neuroblast lineage specified by the empty spiracles gene. Neural Dev 3:33.
19. De Loof A, Baggerman G, Breuer M, Claeys I, Cerstiaens A, Clynen E, Janssen T, Schoofs L, Vanden Broeck J. 2001. Gonadotropins in insects: an overview. Arch Insect Bio-chem Physiol 47:129-138.
20. Fishilevich E, Vosshall LB. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15: 1548-1553.
21. Hallem EA, Carlson JR. 2006. Coding of odors by a receptor repertoire. Cell 125:143-160.
22. Hartlieb E, Anderson P. 1999. Olfactory-released behaviours. In: Hanson BS, editor. Insect olfaction. Berlin: Springer. p 315-349.
23. Hill ES, Okada K, Kanzaki R. 2003. Visualization of modulatory effects of serotonin in the silkmoth antennal lobe. J Exp Biol 206(Pt 2):345-352.
24. Ignell R, Root CM, Birse RT, Wang JW, Nässel DR, Winther AM. 2009. Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci USA 106:13070-13075.
25. Iwano M, Kanzaki R. 2005. Immunocytochemical identification of neuroactive substances in the antennal lobe of the male silkworm moth Bombyx mori. Zool Sci 22:199-211.
26. Johard HA, Enell LE, Gustafsson E, Trifilieff P, Veenstra JA, Nässel DR. 2008. Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. J Comp Neurol 507:1479-1496.
27. Kim YJ, Zitnan D, Galizia CG, Cho KH, Adams ME. 2006. A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr Biol 16:1395-1407.
28. 2\+ channel clustering, and vesicle release. Science 312:1051-1054.
29. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buch-ner S, Buchner E. 1996. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
30. Kloppenburg P, Ferns D, Mercer AR. 1999. Serotonin enhances central olfactory neuron responses to female sex pher-omone in the male sphinx moth Manduca sexta. J Neurosci 19:8172-8181.
31. Krishnan B, Dryer SE, Hardin PE. 1999. Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400:375-378.
32. Krishnan P, Chatterjee A, Tanoue S, Hardin PE. 2008. Spike amplitude of single-unit responses in antennal sensillae is controlled by the Drosophila circadian clock. Curr Biol 18: 803-807.
33. Kurtovic A, Widmer A, Dickson BJ. 2007. A single class of olfactory neurons mediates behavioural responses to a Dro-sophila sex pheromone. Nature 446:542-546.
34. Laissue PP, Vosshall LB. 2008. The olfactory sensory map in Drosophila. Adv Exp Med Biol 628:102-114.
35. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543-552.
36. Lee KS, You KH, Choo JK, Han YM, Yu K. 2004. Drosophila short neuropeptide F regulates food intake and body size. J Biol Chem 279:50781-50789.
37. Lee KS, Kwon OY, Lee JH, Kwon K, Min KJ, Jung SA, Kim AK, You KH, Tatar M, Yu K. 2008. Drosophila short neuropep-tide F signalling regulates growth by ERK-mediated insulin signalling. Nat Cell Biol 10:468-475.
38. Lorenz MW, Kellner R, Hoffmann KH. 1995. A family of neuro-peptides that inhibit juvenile hormone biosynthesis in the cricket, Gryllus bimaculatus. J Biol Chem 270:21103-21108.
39. Masse NY, Turner GC, Jefferis GS. 2009. Olfactory information processing in Drosophila. Curr Biol 19:R700-713.
40. Matsumoto S, Brown MR, Crim JW, Vigna SR, Lea AO. 1989. Isolation and primary structure of neuropeptides from the mosquito, Aedes aegypti, immunoreactive to FMRFamide antiserum. Insect Biochem 19:277-283.
41. Meng X, Wahlström G, Immonen T, Kolmer M, Tirronen M, Pre-del R, Kalkkinen N, Heino TI, Sariola H, Roos C. 2002. The Drosophila hugin gene codes for myostimulatory and ecdy-sis-modifying neuropeptides. Mech Dev 117:5-13.
42. N̈assel DR. 2002. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodu-lators and neurohormones. Prog Neurobiol 68:1-84.
43. N̈assel DR, Homberg U. 2006. Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1-24.
44. N̈assel DR, Enell LE, Santos JG, Wegener C, Johard HA. 2008. 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.
45. Nichols R. 2003. Signaling pathways and physiological functions of Drosophila melanogaster FMRFamide-related pep-tides. Annu Rev Entomol 48:485-503.
46. Nichols R. 2006. FMRFamide-related peptides and serotonin regulate Drosophila melanogaster heart rate: mechanisms and structure requirements. Peptides 27:1130-1137.
47. Nichols R, McCormick J, Lim I. 1997a. Dromyosuppressin and drosulfakinin, two structurally related Drosophila neuropep-tides, are uniquely expressed in the adult central nervous system. Ann N Y Acad Sci 814:315-318.
48. Nichols R, McCormick J, Lim I. 1997b. Multiple antigenic pep-tides designed to structurally related Drosophila peptides. Peptides 18:41-45.
49. Okada R, Awasaki T, Ito K. 2009. Gamma-aminobutyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe. J Comp Neurol 514:74-91.
50. Olsen SR, Bhandawat V, Wilson RI. 2007. Excitatory interactions between olfactory processing channels in the Dro-sophila antennal lobe. Neuron 54:89-103.
51. Orchard I, Lange AB, Bendena WG, 2001. FMRFamide-related peptides: a multifunctional family of structurally related neuropeptides in insects, Adv Insect Physiol 28:268-329.
52. Predel R, Rapus J, Eckert M. 2001. Myoinhibitory neuropep-tides in the American cockroach. Peptides 22:199-208.
53. Predel R, Wegener C, Russell WK, Tichy SE, Russell DH, Nach-man RJ. 2004. Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: a mass spectro-metric survey of peptides from individual flies. J Comp Neurol 474:379-392.
54. Roller L, Yamanaka N, Watanabe K, Daubnerova I, Zitnan D, Kataoka H, Tanaka Y. 2008. The unique evolution of neuro-peptide genes in the silkworm Bombyx mori. Insect Bio-chem Mol Biol 38:1147-1157.
55. Root CM, Masuyama K, Green DS, Enell LE, Nässel DR, Lee CH, Wang JW. 2008. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311-321.
56. Roy B, Singh AP, Shetty C, Chaudhary V, North A, Landgraf M, Vijayraghavan K, Rodrigues V. 2007. Metamorphosis of an identified serotonergic neuron in the Drosophila olfactory system. Neural Dev 2:20.
57. Salvaterra PM, Kitamoto T. 2001. Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. Brain Res Gene Expr Patterns 1:73-82.
58. Santos JG, Vömel M, Struck R, Homberg U, N̈assel DR, Wege-ner C. 2007. Neuroarchitecture of peptidergic systems in the larval ventral ganglion of Drosophila melanogaster. PLoS ONE 2:e695.
59. Schachtner J, Schmidt M, Homberg U. 2005. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea\+ Hexapoda). Arthropod Struct Dev 34:257-299.
60. Schachtner J, Wegener C, Neupert S, Predel R. 2010. Direct peptide profiling of brain tissue by MALDI-TOF mass spec-trometry. Methods Mol Biol 615:129-135.
61. Schneider LE, Sun ET, Garland DJ, Taghert PH. 1993. An immunocytochemical study of the FMRFamide neuropep-tide gene products in Drosophila. J Comp Neurol 337: 446-460.
62. Schoofs L, Clynen E, Cerstiaens A, Baggerman G, Wei Z, Ver-cammen T, Nachman R, De Loof A, Tanaka S. 2001. Newly discovered functions for some myotropic neuropeptides in locusts. Peptides 22:219-227.
63. Shafer OT, Helfrich-Forster C, Renn SC, Taghert PH. 2006. Reevaluation of Drosophila melanogaster's neuronal circa-dian pacemakers reveals new neuronal classes. J Comp Neurol 498:180-193.
64. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenbock G. 2007. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128: 601-612.
65. Stocker RF. 1994. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3-26.
66. Stocker RF, Heimbeck G, Gendre N, de Belle JS. 1997. Neuro-blast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32:443-456.
67. Su CY, Menuz K, Carlson JR. 2009. Olfactory perception: receptors, cells, and circuits. Cell 139:45-59.
68. Taghert PH, Veenstra JA. 2003. Drosophila neuropeptide signaling. Adv Genet 49:1-65.
69. Terhzaz S, Rosay P, Goodwin SF, Veenstra JA. 2007. The neu-ropeptide SIFamide modulates sexual behavior in Drosoph-ila. Biochem Biophys Res Commun 352:305-310.
70. Utz S, Huetteroth W, Wegener C, Kahnt J, Predel R, Schacht-ner J. 2007. Direct peptide profiling of lateral cell groups of the antennal lobes of Manduca sexta reveals specific composition and changes in neuropeptide expression during development. Dev Neurobiol 67:764-777.
71. Vanden Broeck J. 2001. Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster. Peptides 22: 241-254.
72. Verleyen P, Baggerman G, Wiehart U, Schoeters E, Van Lom-mel A, De Loof A, Schoofs L. 2004a. Expression of a novel neuropeptide, NVGTLARDFQLPIPNamide, in the larval and adult brain of Drosophila melanogaster. J Neurochem 88: 311-319.
73. Verleyen P, Huybrechts J, Baggerman G, Van Lommel A, De Loof A, Schoofs L. 2004b. SIFamide is a highly conserved neuropeptide: a comparative study in different insect species. Biochem Biophys Res Commun 320:334-341.
74. Vitzthum H, Homberg U, Agricola H. 1996. Distribution of Dip-allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immu-nostaining in the central complex. J Comp Neurol 369: 419-437.
75. Vosshall LB. 2008. Scent of a fly. Neuron 59:685-689.
76. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
77. Vullings HG, Ten Voorde SE, Passier PC, Diederen JH, Van Der Horst DJ, Nässel DR. 1998. A possible role of SchistoFLR-Famide in inhibition of adipokinetic hormone release from locust corpora cardiaca. J Neurocytol 27:901-913.
78. Williamson M, Lenz C, Winther AM, Nässel DR, Grimmelikhuij-zen CJ. 2001. Molecular cloning, genomic organization, and expression of a B-type (cricket-type) allatostatin pre-prohormone from Drosophila melanogaster. Biochem Bio-phys Res Commun 281:544-550. (Pubitemid 32936603)
79. Wilson RI, Laurent G. 2005. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Dro-sophila antennal lobe. J Neurosci 25:9069-9079.
80. Winther AME, Nässel DR. 2001. Intestinal peptides as circulating hormones: release of tachykinin-relate d peptide from the locust and cockroach midgut. J Exp Biol 204: 1269-1280.
81. Winther AM, Siviter RJ, Isaac RE, Predel R, N̈assel DR. 2003. Neuronal expression of tachykinin-related peptides and gene transcript during postembryonic development of Drosophila. J Comp Neurol 464:180-196.
82. Winther AM, Acebes A, Ferrus A. 2006. Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31:399-406.
83. Woodhead AP, Stay B, Seidel SL, Khan MA, Tobe SS. 1989. Primary structure of four allatostatins: neuropeptide inhibitors of juvenile hormone synthesis. Proc Natl Acad Sci USA 86:5997-6001.
84. Yamanaka N, Hua YJ, Mizoguchi A, Watanabe K, Niwa R, Tanaka Y, Kataoka H. 2005. Identification of a novel pro-thoracicostatic hormone and its receptor in the silkworm Bombyx mori. J Biol Chem 280:14684-14690.
85. Yamanaka N, Zitnan D, Kim YJ, Adams ME, Hua YJ, Suzuki Y, Suzuki A, Satake H, Mizoguchi A, Asaoka K, Tanaka Y, Kataoka H. 2006. Regulation of insect steroid hormone biosynthesis by innervating peptidergic neurons. Proc Natl Acad Sci USA 103:8622-8627.
86. Yasuyama K, Salvaterra PM. 1999. Localization of choline ace-tyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Tech 45:65-79.
87. Yew JY, Wang Y, Barteneva N, Dikler S, Kutz-Naber KK, Li L, Kravitz EA. 2009. Analysis of neuropeptide expression and localization in adult Drosophila melanogaster central nervous system by affinity cell-capture mass spectrometry. J Proteome Res 8:1271-1284.
88. Yoon JG, Stay B. 1995. Immunocytochemical localization of Diploptera punctata allatostatin-like peptide in Drosophila melanogaster. J Comp Neurol 363:475-488.