Temperature-dependent developmental plasticity of Drosophila neurons: cell-autonomous roles of membrane excitability, Ca2+ influx, and cAMP signaling.
Environmental temperature is an important factor exerting pervasive influence on neuronal morphology and synaptic physiology. In the Drosophila brain, axonal arborization of mushroom body Kenyon cells was enhanced when flies were raised at high temperature (30 degrees C rather than 22 degrees C) for several days. Isolated embryonic neurons in culture that lacked cell-cell contacts also displayed a robust temperature-induced neurite outgrowth. This cell-autonomous effect was reflected by significantly increased high-order branching and enlarged growth cones. The temperature-induced morphological alterations were blocked by the Na+ channel blocker tetrodotoxin and a Ca2+ channel mutation but could be mimicked by raising cultures at room temperature with suppressed K+ channel activity. Physiological analyses revealed increased inward Ca2+ currents and decreased outward K+ currents, in conjunction with a distal shift in the site of action potential initiation and increased prevalence of TTX-sensitive spontaneous Ca2+ transients. Importantly, the overgrowth caused by both temperature and hyperexcitability K+ channel mutations were sensitive to genetic perturbations of cAMP metabolism. Thus, temperature acts in a cell-autonomous manner to regulate neuronal excitability and spontaneous activity. Presumably, activity-dependent Ca2+ accumulation triggers the cAMP cascade to confer the activity-dependent plasticity of neuronal excitability and growth.
Peng
I-Feng
IF
Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242, USA.
Berke
Brett A
BA
Zhu
Yue
Y
Lee
Wei-Hua
WH
Chen
Wenjia
W
Wu
Chun-Fang
CF
D000200:Action Potentials / Q000187:drug effects / Q000235:genetics; D000818:Animals; D001921:Brain / Q000166:cytology / Q000196:embryology / Q000254:growth & development*; D015220:Calcium Channels / Q000187:drug effects / Q000235:genetics / Q000378:metabolism; D020013:Calcium Signaling / Q000187:drug effects / Q000502:physiology*; D002454:Cell Differentiation / Q000502:physiology; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism; D002478:Cells, Cultured; D000242:Cyclic AMP / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000166:cytology / Q000196:embryology / Q000254:growth & development*; D020439:Growth Cones / Q000378:metabolism / Q000648:ultrastructure; D008564:Membrane Potentials / Q000187:drug effects / Q000235:genetics; D024521:Mushroom Bodies / Q000166:cytology / Q000196:embryology / Q000254:growth & development; D009154:Mutation / Q000235:genetics; D016501:Neurites / Q000378:metabolism / Q000648:ultrastructure; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000166:cytology / Q000378:metabolism*; D015221:Potassium Channels / Q000187:drug effects / Q000235:genetics / Q000378:metabolism; D009435:Synaptic Transmission / Q000187:drug effects / Q000235:genetics; D013696:Temperature
D015220:Calcium Channels; D015221:Potassium Channels; D000242:Cyclic AMP