Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals

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

Volumn 111, Issue 9, 2014, Pages 3597-3601

  Bulgari, Dinara ^a   Zhou, Chaoming ^a   Hewes, Randall S ^b   Deitcher, David L ^c   Levitan, Edwin S ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c Cornell University ^*  (United States)

Author keywords

LDCV; Nerve terminal; Neurotransmission; Secretory granule

Indexed keywords

NEUROPEPTIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DIMMED; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; HALF LIFE TIME; NERVE ENDING; NERVE FIBER TRANSPORT; NEUROENDOCRINE SYSTEM; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN SECRETION; SYNAPSE VESICLE; TIME LAPSE IMAGING;

LDCV; NERVE TERMINAL; NEUROTRANSMISSION; SECRETORY GRANULE;

ANIMALS; DROSOPHILA; MICROSCOPY, CONFOCAL; NEUROPEPTIDES; NEUROSECRETORY SYSTEMS; PRESYNAPTIC TERMINALS; SYNAPTIC TRANSMISSION; TRANSPORT VESICLES;

EID: 84895787326     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1322170111     Document Type: Article

References (29)

1. Taghert PH, Nitabach MN (2012) Peptide neuromodulation in invertebrate model systems. Neuron 76(1):82-97.
2. Montminy MR, Bilezikjian LM (1987) Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature 328(6126):175-178.
3. Benveniste RJ, Thor S, Thomas JB, Taghert PH (1998) Cell type-specific regulation of the Drosophila FMRF-NH2 neuropeptide gene by Apterous, a LIM homeodomain transcription factor. Development 125(23):4757-4765.
4. Allan DW, Park D, St Pierre SE, Taghert PH, Thor S (2005) Regulators acting in combinatorial codes also act independently in single differentiating neurons. Neuron 45(5):689-700.
5. Allan DW, St Pierre SE, Miguel-Aliaga I, Thor S (2003) Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell 113(1):73-86.
6. Miguel-Aliaga I, Thor S, Gould AP (2008) Postmitotic specification of Drosophila insulinergic neurons from pioneer neurons. PLoS Biol 6(3):e58.
7. Huang M, et al. (2008) Ptf1a, Lbx1 and Pax2 coordinate glycinergic and peptidergic transmitter phenotypes in dorsal spinal inhibitory neurons. Dev Biol 322(2):394-405.
8. Xu Y, et al. (2008) Tlx1 and Tlx3 coordinate specification of dorsal horn pain-modulatory peptidergic neurons. J Neurosci 28(15):4037-4046.
9. Eade KT, Fancher HA, Ridyard MS, Allan DW (2012) Developmental transcriptional networks are required to maintain neuronal subtype identity in the mature nervous system. PLoS Genet 8(2):e1002501.
10. Hewes RS, Park D, Gauthier SA, Schaefer AM, Taghert PH (2003) The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130(9):1771-1781.
11. Park D, et al. (2008) The Drosophila basic helix-loop-helix protein DIMMED directly activates PHM, a gene encoding a neuropeptide-amidating enzyme. Mol Cell Biol 28(1):410-421.
12. Park D, Veenstra JA, Park JH, Taghert PH (2008b) Mapping peptidergic cells in Drosophila: where DIMM fits in. PLoS ONE 3(3):e1896.
13. Hamanaka Y, et al. (2010) Transcriptional orchestration of the regulated secretory pathway in neurons by the bHLH protein DIMM. Curr Biol 20(1):9-18.
14. Atwood HL, Govind CK, Wu CF (1993) Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 24(8): 1008-1024.
15. Jia XX, Gorczyca M, Budnik V (1993) Ultrastructure of neuromuscular junctions in Drosophila: comparison of wild type and mutants with increased excitability. J Neurobiol 24(8):1025-1044.
16. Loveall BJ, Deitcher DL (2010) The essential role of bursicon during Drosophila development. BMC Dev Biol 10:92.
17. Shakiryanova D, Tully A, Levitan ES (2006) Activity-dependent synaptic capture of transiting peptidergic vesicles. Nat Neurosci 9(7):896-900.
18. Wong MY, et al. (2012) Neuropeptide delivery to synapses by long-range vesicle circulation and sporadic capture. Cell 148(5):1029-1038.
19. Rao S, Lang C, Levitan ES, Deitcher DL (2001) Visualization of neuropeptide expression, transport, and exocytosis in Drosophila melanogaster. J Neurobiol 49(3):159-172.
20. Hodge JJ, Choi JC, O'Kane CJ, Griffith LC (2005) Shaw potassium channel genes in Drosophila. J Neurobiol 63(3):235-254.
21. Tsuboi T, Kitaguchi T, Karasawa S, Fukuda M, Miyawaki A (2010) Age-dependent preferential dense-core vesicle exocytosis in neuroendocrine cells revealed by newly developed monomeric fluorescent timer protein. Mol Biol Cell 21(1):87-94.
22. Park D, et al. (2011) Molecular organization of Drosophila neuroendocrine cells by Dimmed. Curr Biol 21(18):1515-1524.
23. Fujioka M, et al. (2003) Even-skipped, acting as a repressor, regulates axonal projections in Drosophila. Development 130(22):5385-5400.
24. Duncan RR, et al. (2003) Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422(6928):176-180.
25. Wong MY, Shakiryanova D, Levitan ES (2009) Presynaptic ryanodine receptor-CamKII signaling is required for activity-dependent capture of transiting vesicles. J Mol Neurosci 37(2):146-150.
26. Wu YE, Huo L, Maeder CI, Feng W, Shen K (2013) The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses. Neuron 78(6):994-1011.
27. Ghannad-Rezaie M, Wang X, Mishra B, Collins C, Chronis N (2012) Microfluidic chips for in vivo imaging of cellular responses to neural injury in Drosophila larvae. PLoS ONE 7(1):e29869.
28. Burke NV, et al. (1997) Neuronal peptide release is limited by secretory granule mobility. Neuron 19(5):1095-1102.
29. Levitan ES, Lanni F, Shakiryanova D (2007) In vivo imaging of vesicle motion and release at the Drosophila neuromuscular junction. Nat Protoc 2(5):1117-1125.