Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 31, 2009, Pages 13070-13075

  Ignell, Rickard ^a   Root, Cory M ^b   Birse, Ryan T ^c,d   Wang, Jing W ^b   Nässel, Dick R ^c   Winther, Åsa M E ^c  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d BURNHAM INSTITUTE   (United States)

Author keywords

Olfactory behavior; Presynaptic inhibition; Tachykinin; Two photon imaging

Indexed keywords

TACHYKININ; TACHYKININ RECEPTOR; DROSOPHILA PROTEIN; DTK PROTEIN, DROSOPHILA; NEUROTRANSMITTER RECEPTOR; PROTEIN PRECURSOR; TAKR99D PROTEIN, DROSOPHILA;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; MICROSCOPY; NONHUMAN; ODOR; OLFACTORY RECEPTOR; PHENOTYPE; PRESYNAPTIC INHIBITION; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMELLING; ANIMAL; NERVE CELL INHIBITION; PHYSIOLOGY;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; NEURAL INHIBITION; ODORS; OLFACTORY RECEPTOR NEURONS; PROTEIN PRECURSORS; RECEPTORS, NEUROTRANSMITTER; SIGNAL TRANSDUCTION; TACHYKININS;

EID: 69149111016     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0813004106     Document Type: Article

References (51)

1. Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3:780-785.
2. Clyne PJ, et al. (1999) A novel family of divergent seven-transmembrane proteins: Candidate odorant receptors in Drosophila. Neuron 22:327-338.
3. Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147-159.
4. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725-736.
5. Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548-1553.
6. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535-1547.
7. Stocker RF, Heimbeck G, Gendre N, de Belle JS (1997) Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32:443-456.
8. Olsen SR, Wilson RI (2008) Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956-960.
9. Root CM, et al. (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311-321.
10. Murphy GJ, Darcy DP, Isaacson JS (2005) Intraglomerular inhibition: Signaling mechanisms of an olfactory microcircuit. Nat Neurosci 8:354-364.
11. McGann JP, et al. (2005) Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48:1039-1053.
12. Aroniadou-Anderjaska V, Zhou FM, Priest CA, Ennis M, Shipley MT (2000) Tonic and synaptically evoked presynaptic inhibition of sensory input to the rat olfactory bulb via GABA(B) heteroreceptors. J Neurophysiol 84:1194-1203.
13. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenböck G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601-612.
14. Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89-103.
15. Nässel DR, Homberg U (2006) Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1-24.
16. Utz S, et al. (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.
17. Ni MM, Luo Y, Liu J, Liao DQ, Tang YD (2008) FMRFamide modulates outward potassium currents in mouse olfactory sensory neurons. Clin Exp Pharmacol Physiol 35:563-567.
18. Gutierrez-Mecinas M, et al. (2005) Characterization of somatostatin- and cholecystokinin-immunoreactive periglomerular cells in the rat olfactory bulb. J Comp Neurol 489:467-479.
19. Winther ÅM, Acebes A, Ferrus A (2006) Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31:399-406.
20. Siviter RJ, et al. (2000) Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A. J Biol Chem 275:23273-23280.
21. Winther ÅM, Siviter RJ, Isaac RE, Predel R, Nässel DR (2003) Neuronal expression of tachykinin-related peptides and gene transcript during postembryonic development of Drosophila. J Comp Neurol 464:180-196.
22. Li XJ, Wolfgang W, Wu YN, North RA, Forte M (1991) Cloning, heterologous expression and developmental regulation of a Drosophila receptor for tachykinin-like peptides. EMBO J 10:3221-3229.
23. Monnier D, et al. (1992) NKD, a developmentally regulated tachykinin receptor in Drosophila. J Biol Chem 267:1298-1302.
24. Birse RT, Johnson EC, Taghert PH, Nässel DR (2006) Widely distributed Drosophila G-protein-coupled receptor (CG7887) is activated by endogenous tachykinin-related peptides. J Neurobiol 66:33-46.
25. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505-533.
26. Bhandawat V, Olsen SR, Gouwens NW, Schlief ML,Wilson RI (2007) Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat Neurosci 10:1474-1482.
27. Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966-11977.
28. Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069-9079.
29. Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW (2007) Propagation of olfactory information in Drosophila. Proc Natl Acad Sci USA 104:11826-11831.
30. Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19:137-141.
31. Wang JW,Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-282.
32. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
33. Dekker T, Ibba I, Siju KP, Stensmyr MC, Hansson BS (2006) Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling,Dsechellia. Curr Biol 16:101-109.
34. Larsson MC, et al. (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703-714.
35. Devaud JM, Keane J, Ferrus A (2003) Blocking sensory inputs to identified antennal glomeruli selectively modifies odorant perception in Drosophila. J Neurobiol 56:1-12.
36. Stensmyr MC, Giordano E, Balloi A, Angioy AM, Hansson BS (2003) Novel natural ligands for Drosophila olfactory receptor neurones. J Exp Biol 206:715-724.
37. Wang Y, et al. (2003) Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion. Curr Biol 13:1900-1904.
38. Malun D (1991) Synaptic relationships between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana: A double-labeling electron microscopic study. Histochemistry 96:197-207.
39. Distler PG, Boeckh J (1997) Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: II. Local multiglomerular interneurons. J Comp Neurol 383:529-540.
40. Wachowiak M, Cohen LB (1999) Presynaptic inhibition of primary olfactory afferents mediated by different mechanisms in lobster and turtle. J Neurosci 19:8808-8817.
41. Schindler M, Humphrey PP, Lohrke S, Friauf E (1999) Immunohistochemical localization of the somatostatin sst2 (b) receptor splice variant in the rat central nervous system. Neuroscience 90:859-874.
42. Mousley A, Polese G, Marks NJ, Eisthen HL (2006) Terminal nerve-derived neuropeptide y modulates physiological responses in the olfactory epithelium of hungry axolotls (Ambystoma mexicanum). J Neurosci 26:7707-7717.
43. Park D, Zawacki SR, Eisthen HL (2003) Olfactory signal modulation by molluscan cardioexcitatory tetrapeptide (FMRFamide) in axolotls (Ambystoma mexicanum). Chem Senses 28:339-348.
44. Semmelhack JL, Wang JW (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459:218-223.
45. Hökfelt T, et al. (2000) Neuropeptides-an overview. Neuropharmacology 39:1337-1356.
46. Burnstock G (2004) Cotransmission. Curr Opin Pharmacol 4:47-52.
47. Glantz RM, Miller CS, Nässel DR (2000) Tachykinin-related peptide and GABA-mediated presynaptic inhibition of crayfish photoreceptors. J Neurosci 20:1780-1790.
48. Giordano E, Rendina R, Peluso I, Furia M (2002) RNAi triggered by symmetrically transcribed transgenes in Drosophila melanogaster. Genetics 160:637-648.
49. Wong AM,Wang JW, Axel R (2002) Spatial representation of the glomerularmapin the Drosophila protocerebrum. Cell 109:229-241.
50. Ng M, et al. (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463-474.
51. Merrill CE, et al. (2002) Visual arrestins in olfactory pathways of Drosophila and the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci USA 99:1633-1638.