Targeting HSP70 to motoneurons protects locomotor activity from hyperthermia in Drosophila

Developmental Neurobiology

Volumn 67, Issue 4, 2007, Pages 438-455

  Xiao, Chengfeng ^a   Mileva Seitz, Viara ^a   Seroude, Laurent ^a   Robertson, R Meldrum ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

HSP70; Locomotor activity; Motoneuron; Thermoprotection

Indexed keywords

HEAT SHOCK PROTEIN 70; DROSOPHILA PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA; GENE ACTIVATION; GENETIC TRANSCRIPTION; HYPERTHERMIA; LOCOMOTION; MOTONEURON; MUSCLE CELL; NERVE CELL PLASTICITY; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NEUROPROTECTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SEROTONINERGIC NERVE CELL; ANIMAL; ANIMAL BEHAVIOR; FEVER; GENETICS; HEAT SHOCK RESPONSE; LARVA; METABOLISM; METHODOLOGY; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; FEVER; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; LARVA; MOTOR ACTIVITY; MOTOR NEURONS; MUSCLE CELLS; NEUROMUSCULAR JUNCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 34249661777     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20344     Document Type: Article

References (59)

1. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, Goodman CS. 2002. Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33:545-558.
2. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM. 2002. Chaperone suppression of α-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295:865-868.
3. Barclay JW, Atwood HL, Robertson RM. 2002. Impairment of central pattern generation in Drosophila cysteine string protein mutants. J Comp Physiol A 188:71-78.
4. Barclay JW, Robertson RM. 2000. Heat-shock-induced thermoprotection of hindleg motor control in the locust. J Exp Biol 203:941-950.
5. Bettencourt BR, Feder ME. 2002. Rapid concerted evolution via gene conversion at the Drosophila hsp70 genes. J Mol Evol 54:569-586.
6. Bonini NM. 2002. Chaperoning brain degeneration. Proc Natl Acad Sci USA 99 (Suppl 4):16407-16411.
7. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
8. Bronk P, Nie Z, Klose MK, Dawson-Scully K, Zhang J, Robertson RM, Atwood HL, et al. 2005. The multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. J Neurosci 25:2204-2214.
9. Bronk P, Wenniger JJ, Dawson-Scully K, Guo X, Hong S, Atwood HL, Zinsmaier KE. 2001. Drosophila Hsc70-4 is critical for neurotransmitter exocytosis in vivo. Neuron 30:475-488.
10. Cooper RL, Neckameyer WS. 1999. Dopaminergic modulation of motor neuron activity and neuromuscular function in Drosophila melanogaster. Comp Biochem Physiol B Biochem Mol Biol 122:199-210.
11. Feeney CJ, Karunanithi S, Pearce J, Govind CK, Atwood HL. 1998. Motor nerve terminals on abdominal muscles in larval flesh flies, Sarcophaga bullata: Comparisons with Drosophila. J Comp Neurol 402:197-209.
12. Fox LE, Soll DR, Wu CF. 2006. Coordination and modulation of locomotion pattern generators in Drosophila larvae: Effects of altered biogenic amine levels by the tyramine β-hydroxlyase mutation. J Neurosci 26:1486-1498.
13. Giffard RG, Yenari MA. 2004. Many mechanisms for hsp70 protection from cerebral ischemia. J Neurosurg Anesthesiol 16:53-61.
14. Gong WJ, Golic KG. 2004. Genomic deletions of the Drosophila melanogaster Hsp70 genes. Genetics 168:1467-1476.
15. Gong WJ, Golic KG. 2006. Loss of hsp70 in Drosophila is pleiotropic, with effects on thermotolerance, recovery from heat shock and neurodegeneration. Genetics 172:275-286.
16. Hawkins RD, Kandel ER, Bailey CH. 2006. Molecular mechanisms of memory storage in Aplysia. Biol Bull 210:174-191.
17. Hummel T, Krukkert K, Roos J, Davis G, Klambt C. 2000. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26:357-370.
18. Jin X, Xiao C, Tanguay RM, Yang L, Wang F, Chen M, Fu X, et al. 2004. Correlation of lymphocyte heat shock protein 70 levels with neurologic deficits in elderly patients with cerebral infarction. Am J Med 117:406-411.
19. Karunanithi S, Barclay JW, Brown IR, Robertson RM, Atwood HL. 2002. Enhancement of presynaptic performance in transgenic Drosophila overexpressing heat shock protein Hsp70. Synapse 44:8-14.
20. Karunanithi S, Barclay JW, Robertson RM, Brown IR, Atwood HL. 1999. Neuroprotection at Drosophila synapses conferred by prior heat shock. J Neurosci 19:4360-4369.
21. Kelly S, Yenari MA. 2002. Neuroprotection: Heat shock proteins. Curr Med Res Opin 18 (Suppl 2):s55-s60.
22. Kelty JD, Noseworthy PA, Feder ME, Robertson RM, Ramirez JM. 2002. Thermal preconditioning and heat-shock protein 72 preserve synaptic transmission during thermal stress. J Neurosci 22:RC193.
23. Klose MK, Charlton MP, Atwood HL, Robertson RM. 2004. Alterations in Presynaptic Calcium Handling During Heat Shock-Induced Thermoprotection of Synaptic Transmission. Washington, DC: Society for Neuroscience.
24. Klose MK, Chu D, Xiao C, Seroude L, Robertson RM. 2005. Heat shock-mediated thermoprotection of larval locomotion compromised by ubiquitous overexpression of Hsp70 in Drosophila melanogaster. J Neurophysiol 94:3563-3572.
25. Krebs RA, Feder ME. 1997. Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60-71.
26. Krebs RA, Feder ME. 1998. Hsp70 and larval thermotolerance in Drosophila melanogaster: How much is enough and when is more too much? J Insect Physiol 44:1091-1101.
27. Kullander K. 2005. Genetics moving to neuronal networks. Trends Neurosci 28:239-247.
28. Lang AE, Lozano AM. 1998. Parkinson's disease. First of two parts. N Engl J Med 339:1044-1053.
29. Li H, Chaney S, Roberts IJ, Forte M, Hirsh J. 2000. Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol 10:211-214.
30. Liang P, MacRae TH. 1997. Molecular chaperones and the cytoskeleton. J Cell Sci 110 (Part 13):1431-1440.
31. Lindquist S. 1992. Heat-shock proteins and stress tolerance in microorganisms. Curr Opin Genet Dev 2:748-755.
32. Lindquist S, Craig EA. 1988. The heat-shock proteins. Annu Rev Genet 22:631-677.
33. 2+ homeostasis in rat ventricular myocytes subjected to simulated ischemia. Am J Physiol Cell Physiol 290:C583-C591.
34. Liu L, Yermolaieva O, Johnson WA, Abboud FM, Welsh MJ. 2003. Identification and function of thermosensory neurons in Drosophila larvae. Nat Neurosci 6:267-273.
35. Mayer MP, Bukau B. 2005. Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci 62:670-684.
36. McGuire SE, Roman G, Davis RL. 2004. Gene expression systems in Drosophila: A synthesis of time and space. Trends Genet 20:384-391.
37. McLachlan EM, Martin AR. 1981. Non-linear summation of end-plate potentials in the frog and mouse. J Physiol 311:307-324.
38. Money TG, Anstey ML, Robertson RM. 2005. Heat stress-mediated plasticity in a locust looming-sensitive visual interneuron. J Neurophysiol 93:1908-1919.
39. Morimoto RI. 1993. Cells in stress: Transcriptional activation of heat shock genes. Science 259:1409-1410.
40. Muchowski PJ, Wacker JL. 2005. Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11-22.
41. Nollen EA, Brunsting JF, Roelofsen H, Weber LA, Kampinga HH. 1999. In vivo chaperone activity of heat shock protein 70 and thermotolerance. Mol Cell Biol 19:2069-2079.
42. Parkes TL, Elia AJ, Dickinson D, Hilliker AJ, Phillips JP, Boulianne GL. 1998. Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons. Nat Genet 19:171-174.
43. Pespeni M, Hodnett M, Pittet JF. 2005. In vivo stress preconditioning. Methods 35:158-164.
44. Robertson RM. 2004a. Thermal stress and neural function: Adaptive mechanisms in insect model systems. J Therm Biol 29:351-358.
45. Robertson RM. 2004b. Modulation of neural circuit operation by prior environmental stress. Integr Comp Biol 44:21-27.
46. Rosenzweig M, Brennan KM, Tayler TD, Phelps PO, Patapoutian A, Garrity PA. 2005. The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419-424.
47. Schedl P, Artavanis-Tsakonas S, Steward R, Gehring WJ, Mirault ME, Goldschmidt-Clermont M, Moran L, et al. 1978. Two hybrid plasmids with D. melanogaster DNA sequences complementary to mRNA coding for the major heat shock protein. Cell 14:921-929.
48. Schuster CM, Davis GW, Fetter RD, Goodman CS. 1996. Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17:655-667.
49. Sigrist SJ, Reiff DF, Thiel PR, Steinert JR, Schuster CM. 2003. Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci 23:6546-6556.
50. Sokolowski MB. 2001. Drosophila: Genetics meets behaviour. Nat Rev Genet 2:879-890.
51. Stevens CF. 1976. A comment on Martin's relation. Biophys J 16:891-895.
52. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175:179-191.
53. Suster ML, Bate M. 2002. Embryonic assembly of a central pattern generator without sensory input. Nature 416:174-178.
54. Tobaben S, Thakur P, Fernandez-Chacon R, Sudhof TC, Rettig J, Stahl B. 2001. A trimeric protein complex functions as a synaptic chaperone machine. Neuron 31:987-999.
55. 2+-ATPase (SERCA1a) and prevents thermal inactivation. J Biol Chem 279:52382-52389.
56. Weibezahn J, Tessarz P, Schlieker C, Zahn R, Maglica Z, Lee S, Zentgraf H, et al. 2004. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119:653-665.
57. Welte MA, Tetrault JM, Dellavalle RP, Lindquist SL. 1993. A new method for manipulating transgenes: Engineering heat tolerance in a complex, multicellular organism. Curr Biol 3:842-853.
58. Wu BS, Walker VK, Robertson RM. 2001. Heat shock-induced thermoprotection of action potentials in the locust flight system. J Neurobiol 49:188-199.
59. Wulff P, Wisden W. 2005. Dissecting neural circuitry by combining genetics and pharmacology. Trends Neurosci 28:44-50.