Acetylcholine elongates neuronal growth cone filopodia via activation of nicotinic acetylcholine receptors

Developmental Neurobiology

Volumn 73, Issue 7, 2013, Pages 487-501

  Zhong, Lei Ray ^a   Estes, Stephen ^a   Artinian, Liana ^a   Rehder, Vincent ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Filopodia; Growth cone; Helisoma trivolvis; Intracellular Ca; Neuronal excitability

Indexed keywords

1,1 DIMETHYL 4 PHENYLPIPERAZINIUM; ACETYLCHOLINE; CALCIUM; NICOTINIC RECEPTOR;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL CULTURE; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC ACTIVITY; FILOPODIUM; GANGLION; GROWTH CONE; HELISOMA TRIVOLVIS; MEMBRANE POTENTIAL; NERVE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; SNAIL;

EID: 84879031916     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22071     Document Type: Article

References (48)

1. Allen TG, Brown DA. 1996. Detection and modulation of acetylcholine release from neurites of rat basal forebrain cells in culture. J Physiol 492 (Part 2):453-466.
2. Artinian L, Tornieri K, Zhong L, Baro D, Rehder V. 2010. Nitric oxide acts as a volume transmitter to modulate electrical properties of spontaneously firing neurons via apamin-sensitive potassium channels. J Neurosci 30: 1699-1711.
3. Bahls F. 1987. Acetylcholine-induced responses in the salivary gland cells of Helisoma trivolvis. Cell Mol Neurobiol 7:35-47.
4. Cheng S, Geddis MS, Rehder V. 2002. Local calcium changes regulate the length of growth cone filopodia. J Neurobiol 50:263-275.
5. Clementi F, Fornasari D, Gotti C. 2000. Neuronal nicotinic receptors, important new players in brain function. Eur J Pharmacol 393:3-10.
6. Cobb SR, Davies CH. 2005. Cholinergic modulation of hippocampal cells and circuits. J Physiol 562:81-88.
7. Cohan CS. 1992. Depolarization-induced changes in neurite elongation and intracellular Ca2+ in isolated Helisoma neurons. J Neurobiol 23:983-996.
8. Cohan CS, Kater SB. 1986. Suppression of neurite elongation and growth cone motility by electrical activity. Science 232:1638-1640.
9. Elliott CJ, Vehovszky A. 2000. Comparative pharmacology of feeding in molluscs. Acta Biol Hung 51:153-163.
10. Farrar NR, Spencer GE. 2008. Pursuing a "turning point" in growth cone research. Dev Biol 318:102-111.
11. Fields RD, Neale EA, Nelson PG. 1990. Effects of patterned electrical activity on neurite outgrowth from mouse sensory neurons. J Neurosci 10:2950-2964.
12. Fu WM, Liou HC, Chen YH. 1998. Nerve terminal currents induced by autoreception of acetylcholine release. J Neurosci 18:9954-9961.
13. Gomez TM, Zheng JQ. 2006. The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7:115-125.
14. Haydon PG. 1988. The formation of chemical synapses between cell-cultured neuronal somata. J Neurosci 8:1032-1038.
15. Haydon PG, Zoran MJ. 1989. Formation and modulation of chemical connections: Evoked acetylcholine release from growth cones and neurites of specific identified neurons. Neuron 2:1483-1490.
16. Henley J, Poo MM. 2004. Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol 14:320-330.
17. Hume RI, Role LW, Fischbach GD. 1983. Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rich membranes. Nature 305:632-634.
18. Kater SB, Davenport RW, Guthrie PB. 1994. Filopodia as detectors of environmental cues: Signal integration through changes in growth cone calcium levels. Prog Brain Res 102:49-60.
19. Kater SB, Rehder V. 1995. The sensory-motor role of growth cone filopodia. Curr Opin Neurobiol 5:68-74.
20. Lauder JM, Schambra UB. 1999. Morphogenetic roles of acetylcholine. Environ Health Perspect 107 (Suppl 1):65-69.
21. Le Novere N, Changeux JP. 1995. Molecular evolution of the nicotinic acetylcholine receptor: An example of multigene family in excitable cells. J Mol Evol 40:155-172.
22. McCobb DP, Cohan CS, Connor JA, Kater SB. 1988. Interactive effects of serotonin and acetylcholine on neurite elongation. Neuron 1:377-385.
23. Ming G, Henley J, Tessier-Lavigne M, Song H, Poo M. 2001. Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29:441-452.
24. Neely MD, Nicholls JG. 1995. Electrical activity, growth cone motility and the cytoskeleton. J Exp Biol 198:1433-1446.
25. Owen A, Bird M. 1995. Acetylcholine as a regulator of neurite outgrowth and motility in cultured embryonic mouse spinal cord. Neuroreport 6:2269-2272.
26. Perry SJ, Straub VA, Kemenes G, Santama N, Worster BM, Burke JF, Benjamin PR. 1998. Neural modulation of gut motility by myomodulin peptides and acetylcholine in the snail Lymnaea. J Neurophysiol 79:2460-2474.
27. Phillis JW. 2005. Acetylcholine release from the central nervous system: a 50-year retrospective. Crit Rev Neurobiol 17:161-217.
28. Rehder V, Jensen JR, Dou P, Kater SB. 1991. A comparison of calcium homeostasis in isolated and attached growth cones of the snail Helisoma. J Neurobiol 22:499-511.
29. Rehder V, Kater SB. 1992. Regulation of neuronal growth cone filopodia by intracellular calcium. J Neurosci 12:3175-3186.
30. Rehder V, Williams CV, Kater SB. 1996. Functional compartmentalization of the neuronal growth cone: determining calcium's place in signaling cascades. Perspect Dev Neurobiol 4:215-226.
31. Rudiger T, Bolz J. 2008. Acetylcholine influences growth cone motility and morphology of developing thalamic axons. Cell Adh Migr 2:30-37.
32. Small DH, Reed G, Whitefield B, Nurcombe V. 1995. Cholinergic regulation of neurite outgrowth from isolated chick sympathetic neurons in culture. J Neurosci 15:144-151.
33. Spitzer NC. 2006. Electrical activity in early neuronal development. Nature 444:707-712.
34. Tornieri K, Rehder V. 2007. Nitric oxide release from a single cell affects filopodial motility on growth cones of neighboring neurons. Dev Neurobiol 67: 1932-1943.
35. Trimm KR, Rehder V. 2004. Nitric oxide acts as a slow-down and search signal in developing neurites. Eur J Neurosci 19:809-818.
36. van Nierop P, Bertrand S, Munno DW, Gouwenberg Y, van Minnen J, Spafford JD, Syed NI, et al. 2006. Identification and functional expression of a family of nicotinic acetylcholine receptor subunits in the central nervous system of the mollusc Lymnaea stagnalis. J Biol Chem 281:1680-1691.
37. van Nierop P, Keramidas A, Bertrand S, van Minnen J, Gouwenberg Y, Bertrand D, Smit AB. 2005. Identification of molluscan nicotinic acetylcholine receptor (nAChR) subunits involved in formation of cation- and anion-selective nAChRs. J Neurosci 25:10617-10626.
38. Van Wagenen S, Rehder V. 1999. Regulation of neuronal growth cone filopodia by nitric oxide. J Neurobiol 39:168-185.
39. Van Wagenen S, Rehder V. 2001. Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J Neurobiol 46:206-219.
40. Welshhans K, Rehder V. 2005. Local activation of the nitric oxide/cyclic guanosine monophosphate pathway in growth cones regulates filopodial length via protein kinase G, cyclic ADP ribose and intracellular Ca2+ release. Eur J Neurosci 22:3006-3016.
41. Welshhans K, Rehder V. 2007. Nitric oxide regulates growth cone filopodial dynamics via ryanodine receptor-mediated calcium release. Eur J Neurosci 26:1537-1547.
42. White SH, Magoski NS. 2012. Acetylcholine-evoked afterdischarge in Aplysia bag cell neurons. J Neurophysiol 107:2672-2685.
43. Woodin MA, Munno DW, Syed NI. 2002. Trophic factor-induced excitatory synaptogenesis involves postsynaptic modulation of nicotinic acetylcholine receptors. J Neurosci 22:505-514.
44. Yao WD, Rusch J, Poo M, Wu CF. 2000. Spontaneous acetylcholine secretion from developing growth cones of Drosophila central neurons in culture: Effects of cAMP-pathway mutations. J Neurosci 20:2626-2637.
45. Zakharenko S, Chang S, O'Donoghue M, Popov SV. 1999. Neurotransmitter secretion along growing nerve processes: Comparison with synaptic vesicle exocytosis. J Cell Biol 144:507-518.
46. Zheng JQ, Felder M, Connor JA, Poo MM. 1994. Turning of nerve growth cones induced by neurotransmitters. Nature 368:140-144.
47. Zheng JQ, Wan JJ, Poo MM. 1996. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16:1140-1149.
48. Zhong LR, Artinian L, Rehder V. 2012. Dopamine suppresses neuronal activity of Helisoma B5 neurons via a D2-like receptor, activating PLC and K channels. Neuroscience 228C:109-119.