Role of ATP-dependent calcium regulation in modulation of Drosophila synaptic thermotolerance

Journal of Neurophysiology

Volumn 102, Issue 2, 2009, Pages 901-913

  Klose, M K ^a,c,d   Boulianne, G L ^c   Robertson, R M ^b   Atwood, H L ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d 12 401 Toronto Medical Discovery Tower ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATE; CALCIUM; SODIUM CALCIUM EXCHANGE PROTEIN; THAPSIGARGIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN MITOCHONDRION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE; CONTROLLED STUDY; DROSOPHILA; ELECTROSTIMULATION; ENDOPLASMIC RETICULUM; ENERGY YIELD; EVOKED RESPONSE; EXTRACELLULAR CALCIUM; HEAT SENSITIVITY; HEAT TOLERANCE; MOTONEURON; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PH; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM; CALCIUM-TRANSPORTING ATPASES; CELL MEMBRANE; DROSOPHILA; ELECTRIC STIMULATION; ENDOPLASMIC RETICULUM; EVOKED POTENTIALS; HYDROGEN-ION CONCENTRATION; MITOCHONDRIA; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; SODIUM; SODIUM-CALCIUM EXCHANGER; SYNAPSES; SYNAPTIC TRANSMISSION; TEMPERATURE;

EID: 68149101512     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.91209.2008     Document Type: Article

References (81)

1. 2+ and protein dephosphorylation. Cell Calcium 35: 87-105, 2004.
2. Alnaes E, Rahamimoff R. On the role of mitochondria in transmitter release from motor nerve terminals. J Physiol 248: 285-306, 1975.
3. Altier C, Khosravani H, Evans RM, Hameed S, Peloquin JB, Vartian BA, Chen L, Beedle AM, Ferguson SS, Mezghrani A, Dubel SJ, Bourinet E, McRory JE, Zamponi GW. ORL1 receptor-mediated internalization of N-type calcium channels. Nat. Neurosci 9: 31-40, 2005.
4. Atwood HL, Swenarchuk LE, Gruenwald CR. Long-term synaptic facilitation during sodium accumulation in nerve terminals. Brain Res 100: 198-202, 1975.
5. +, pH and bioenergetic status in superfused RIF-1 tumor cells determined by 23Na and 31P magnetic resonance spectroscopy. Int J Hyperthermia 21: 141-158, 2005.
6. 2+-triggered exocytosis. J Neurophysiol 94: 1888-1903, 2005.
7. 2+ concentrations. J Exp Biol 201: 1141-1152, 1998.
8. Birks RI, Cohen MW. The action of sodium pump inhibitors on neuromuscular transmission. Proc R Soc Lond B Biol Sci 170: 381-399, 1968.
9. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 18: 401-415, 1993.
10. Bronk P, Nie Z, Klose MK, Dawson-Scully K, Zhang J, Robertson RM, Atwood HL, Zinsmaier KE. The multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. J Neurosci 25: 2204-2214, 2005.
11. Bronk P, Wenniger JJ, Dawson-Scully K, Guo X, Hong S, Atwood HL, Zinsmaier KE. Drosophila Hsc70-4 is critical for neurotransmitter exocytosis in vivo. Neuron 30: 475-488, 2001.
12. Buck LT, Pamenter ME. Adaptive responses of vertebrate neurons to anoxia-matching supply to demand. Respir Physiol Neurobiol 154: 226-240, 2006.
13. Budd SL. Mechanisms of neuronal damage in brain hypoxia/ischemia: focus on the role of mitochondrial calcium accumulation. Pharmacol Ther 80: 203-229, 1998.
14. Burg MB, Ferraris JD, Dmitrieva NI. Cellular response to hyperosmotic stresses. Physiol Rev 87: 1441-1474, 2007.
15. 2+-binding proteins. Biochem J 353: 1-12, 2001.
16. Chan SL, Mattson MP. Caspase and calpain substrates: roles in synaptic plasticity and cell death. J Neurosci Res 5: 167-190, 1999.
17. 2+ handling and myofilament desensitization underlie cardiomyocyte performance in normothermic and hyperthermic heat-acclimated rat hearts. J Appl Physiol 103: 266-275, 2007.
18. 2+ oscillations. Science 279: 227-230, 1998.
19. DiPolo R, Beaugé L. Sodium/calcium exchanger: influence of metabolic regulation on ion carrier interactions. Physiol Rev 86: 155-203, 2006.
20. Dong Z, Saikumar P, Weinberg JM, Venkatachalam MA. Calcium in cell injury and death. Annu Rev Pathol 1: 405-434, 2005.
21. 2+ exchange by KB-R7943: transport mode selectivity and antiarrhythmic consequences. Am J Physiol Heart Circ Physiol 281: H1334-H1345, 2001.
22. Gerner EW. Thermal dose and time-temperature factors for biological responses to heat shock. Int J Hyperthermia 3: 319-327, 1987.
23. Gong WJ, Golic KG. Loss of Hsp70 in Drosophila is pleiotropic, with effects on thermotolerance, recovery from heat shock and neurodegeneration. Genetics 172: 275-286, 2006.
24. Gonzalez-Mendez RR, Hahn GM. Effects of hyperthermia on the intracellular pH and membrane potential of Chinese hamster ovary cells. Int J Hyperthermia 5: 69-84, 1989.
25. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
26. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfield M, Marin L, Charlton MP, Atwood HL, Zinsmaier KE. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47: 379-393, 2005.
27. Hay JC, Scheller RH. SNAREs and NSF in targeted membrane fusion. Curr Opin Cell Biol 9: 505-512, 1997.
28. 2+-triggered release in synaptic terminals. Neuron 17: 501-512, 1996.
29. 2+ release by glycolysis in cat atrial myocytes. J Physiol 564: 697-714, 2005.
30. Karunanithi S, Barclay JW, Brown IR, Robertson RM, Atwood HL. Enhancement of presynaptic performance in transgenic Drosophila overexpressing heat shock protein Hsp70. Synapse 44: 8-14, 2002.
31. Karunanithi S, Barclay JW, Robertson RM, Brown IR, Atwood HL. Neuroprotection at Drosophila synapses conferred by prior heat shock. J Neurosci 19: 4360-4369, 1999.
32. Katschinski DM, Boos K, Schindler SG, Fandrey J. Pivotal role of reactive oxygen species as intracellular mediators of hyperthermia-induced apoptosis. J Biol Chem 275: 21094-21098, 2000.
33. 2+ exchange in human epidermoid A 431 cells. Am J Physiol Cell Physiol 263: C30-C38, 1992.
34. Klose MK, Armstrong G, Robertson RM. A role for the cytoskeleton in heat-shock-mediated thermoprotection of locust neuromuscular junctions. J Neurobiol 60: 453-462, 2004.
35. Klose MK, Atwood HL, Robertson RM. Hyperthermic preconditioning of presynaptic calcium regulation in Drosophila. J Neurophysiol 99: 2420-2430, 2008.
36. Klose MK, Chu D, Xiao C, Seroude L, Robertson RM. Heat shock-mediated thermoprotection of larval locomotion compromised by ubiquitous overexpression of Hsp70 in Drosophila melanogaster. J Neurophysiol 94: 3563-3572, 2005.
37. 2+ at the Drosophila synapse. Neuron 35: 333-343, 2002.
38. 2+ dynamics along identified synaptic terminals in Drosophila larvae. J Neurosci 26: 12283-12293, 2006.
39. 2+ channel family. Neuron 39: 951-960, 2003.
40. v2.1 channel inactivation. Eur J Neurosci 23: 3230-3244, 2006.
41. Macleod GT, Hegström-Wojtowicz M, Charlton MP, Atwood HL. Fast calcium signals in Drosophila motor neuron terminals. J Neurophysiol 88: 2659-2663, 2002.
42. Macleod GT, Suster ML, Charlton MP, Atwood HL. Single neuron activity in the Drosophila larval CNS detected with calcium indicators. J Neurosci Methods 127: 167-178, 2003.
43. Martin SW, Butcher AJ, Berrow NS, Richards MW, Paddon RE, Turner DJ, Dolphin AC, Sihra TS, Fitzgerald EM. Phosphorylation sites on calcium channel alpha1 and beta subunits regulate ERK-dependent modulation of neuronal N-type calcium channels. Cell Calcium 39: 275-292, 2006.
44. Millar AG, Zucker RS, Ellis-Davies GC, Charlton MP, Atwood HL. Calcium sensitivity of neurotransmitter release differs at phasic and tonic synapses. J Neurosci 25: 3113-3125, 2005.
45. Mozhayeva MG, Matos MF, Liu X, Kavalali ET. Minimum essential factors required for vesicle mobilization at hippocampal synapses. J Neurosci 24: 1680-1688, 2004.
46. Newmeyer DD, Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112: 481-490, 2003.
47. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790, 2000.
48. 2+ in toxic cell killing. Trends Pharmacol Sci 10: 281-285, 1989.
49. Pant HC, Gallant PE, Gould R, Gainer H. Distribution of calcium-activated protease activity and endogenous substrates in the squid nervous system. J Neurosci 2: 1578-1587, 1982.
50. Parkes TL, Elia AJ, Dickinson D, Hilliker AJ, Phillips JP, Boulianne GL. Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons. Nat Genet 19:171-174, 1998.
51. Parsell DA, Taulien J, Lindquist S. The role of heat-shock proteins in thermotolerance. Philos Trans R Soc Lond B Biol Sci 339: 279-285, 1993.
52. 2+ and asynchronous transmitter release from the same crayfish bouton. J Physiol 501: 251-262, 1997.
53. Rahamimoff R, Lev-Tov A, Meiri H. Primary and secondary regulation of quantal transmitter release: calcium and sodium. J Exp Biol 89: 5-18, 1980.
54. Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, Nakai J, Borst A. In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25: 4766-4778, 2005.
55. Ritossa F. A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18: 571-573, 1962.
56. Robinson PJ, Sontag JM, Liu JP, Fykse EM, Slaughter C, McMahon H, Südhof TC, Dynamin GT. Pase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365: 163-166, 1993.
57. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, Korsmeyer SJ. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67, 2002.
58. 2+ and spontaneous glutamate release. Philos Trans R Soc Lond B Biol Sci 354: 357-364, 1999.
59. 2+ exchanger isoform 3 (NCX3) but not isoform 2 (NCX2) and 1 (NCX1) singly transfected in BHK cells plays a protective role in a model of in vitro hypoxia. Ann NY Acad Sci 1099: 481-485, 2007.
60. Shakiryanova D, Klose MK, Zhou Y, Gu T, Deitcher DL, Atwood HL, Hewes RS, Levitan ES. Presynaptic ryanodine receptor-activated calmodulin kinase II increases vesicle mobility and potentiates neuropeptide release. J Neurosci 27: 7799-7806, 2007.
61. Sherman RG, Atwood HL. Synaptic facilitation: long-term neuromuscular facilitation in crustaceans. Science 171: 1248-1250, 1971.
62. Solomon JM, Rossi JM, Golic K, McGarry T, Lindquist S. Changes in hsp70 alter thermotolerance and heat-shock regulation in Drosophila. New Biol 3: 1106-1120, 1991.
63. Stefani G, Onofri F, Valtorta F, Vaccaro P, Greengard P, Benfenati F. Kinetic analysis of the phosphorylation-dependent interactions of synapsin I with rat brain synaptic vesicles. J Physiol 504: 501-515, 1997.
64. Stewart BA, Mohtashami M, Rivlin P, Deitcher DL, Trimble WS, Boulianne GL. Dominant-negative NSF2 disrupts the structure and function of Drosophila neuromuscular synapses. J Neurobiol 51: 261-271, 2002.
65. Stys PK. White matter injury mechanisms. Curr Mol Med 4: 113-130, 2004.
66. Suzuki N, Wu CF. Altered sensitivity to sodium channel-specific neurotoxins in cultured neurons from temperature-sensitive paralytic mutants of Drosophila. J Neurogenet 1: 225-238, 1984.
67. Szigeti G, Banyasz T, Magyar J, Kortvely A, Szigligeti P, Kovacs L, Jednakovits A, Nanasi P. Effects of bimoclomol, the novel heat shock protein coinducer, in dog ventricular myocardium. Life Sci 67: 73-79, 2000.
68. + overload-induced mitochondrial damage in the ischemic heart. Can J Physiol Pharmacol 82: 1033-1043, 2004.
69. Tank DW, Regehr WG, Delaney KR. A quantitative analysis of presynaptic calcium dynamics that contribute to short-term enhancement. J Neurosci 15: 7940-7952, 1995.
70. Torrie LS, Radford JC, Southall TD, Kean L, Dinsmore AJ, Davies SA, Dow JA. Resolution of the insect ouabain paradox. Proc Natl Acad Sci USA 10: 13689-13693, 2004.
71. 2+-ATPase (SERCA1a) and prevents thermal inactivation. J Biol Chem 279: 52382-52389, 2004.
72. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47: 365-378, 2005.
73. Vigh L, Literati PN, Horvath I, Torok Z, Balogh G, Glatz A, Kovacs E, Boros I, Ferdinandy P, Farkas B, Jaszlits L, Jednakovits A, Koranyi L, Maresca B. Bimoclomol: a nontoxic, hydroxylamine derivative with stress protein-inducing activity and cytoprotective effects. Nat Med 3: 1150-1154, 1997.
74. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112: 271-282, 2003.
75. Wang P, Saraswati S, Guan Z, Watkins CJ, Wurtman RJ, Littleton JT. A Drosophila temperature-sensitive seizure mutant in phosphoglycerate kinase disrupts ATP generation and alters synaptic function. J Neurosci 24: 4518-4529, 2004.
76. 2+ exchanger inhibitors. J Pharmacol Sci 102: 7-16, 2006.
77. Wong K, Karunanithi S, Atwood HL. Quantal unit populations at the Drosophila larval neuromuscular junction. J Neurophysiol 82: 1497-1511, 1999.
78. + overload is caused by oxidative stress and leads to activation of the caspase 3-dependent apoptotic machinery. FASEB J 18: 1442-1444, 2004.
79. 2+ ATPase in posttetanic potentiation at crayfish neuromuscular junctions. J Neurosci 21: 9598-607, 2001.
80. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.
81. Zuhlke RD, Pitt GS, Deisseroth K, Tsien RW, Reuter H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 399: 159-162, 1999.