Glial Hsp70 protects K + homeostasis in the Drosophila brain during repetitive anoxic depolarization

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Armstrong, Gary A B ^a   Xiao, Chengfeng ^a   Krill, Jennifer L ^b   Seroude, Laurent ^a   Dawson Scully, Ken ^b   Robertson, R Meldrum ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); HEAT SHOCK PROTEIN 70; OUABAIN; POTASSIUM ION; NITROGEN; POTASSIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOXIA; ARTICLE; BRAIN; COMA; CONTROLLED STUDY; DEATH; DEPOLARIZATION; DROSOPHILA; GLIA CELL; MALE; NEUROPROTECTION; NONHUMAN; POTASSIUM BALANCE; PROTEIN EXPRESSION; ANAEROBIC GROWTH; ANIMAL; ANTIBODY SPECIFICITY; CELL MEMBRANE POTENTIAL; DROSOPHILA MELANOGASTER; DRUG EFFECT; GLIA; HEAT SHOCK RESPONSE; HOMEOSTASIS; METABOLISM; NERVE CELL; PATHOLOGY;

ANAEROBIOSIS; ANIMALS; BRAIN; COMA; DROSOPHILA MELANOGASTER; HEAT-SHOCK RESPONSE; HOMEOSTASIS; HSP70 HEAT-SHOCK PROTEINS; MALE; MEMBRANE POTENTIALS; NEUROGLIA; NEURONS; NITROGEN; ORGAN SPECIFICITY; OUABAIN; POTASSIUM;

EID: 83155183325     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028994     Document Type: Article

References (50)

1. Haddad GG, Sun Y-a, Wyman RJ, Xu T, (1997) Genetic basis of tolerance to O2 deprivation in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 94: 10809-10812.
2. Krishnan SN, Sun Y-A, Mohsenin A, Wyman RJ, Haddad GG, (1997) Behavioral and Electrophysiologic Responses of Drosophila melanogaster to Prolonged Periods of Anoxia. Journal of Insect Physiology 43: 203-210.
3. Lighton JRB, Schilman PE, (2007) Oxygen Reperfusion Damage in an Insect. Plos One 2: e1267.
4. Schilman PE, Waters JS, Harrison JF, Lighton JRB, (2011) Effects of temperature on responses to anoxia and oxygen reperfusion in Drosophila melanogaster. Journal of Experimental Biology 214: 1271-1275.
5. Somjen GG, (2001) Mechanisms of Spreading Depression and Hypoxic Spreading Depression-Like Depolarization. Physiol Rev 81: 1065-1096.
6. Sanchez-del-Rio M, Reuter U, Moskowitz MA, (2006) New insights into migraine pathophysiology. Current Opinion in Neurology 19: 294-298 210.1097/1001.wco.0000227041.0000223694.0000227045c.
7. Fabricius M, Fuhr S, Bhatia R, Boutelle M, Hashemi P, et al. (2006) Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 129: 778-790.
8. Strong A, Dardis R, (2005) Depolarisation Phenomena in Traumatic and Ischaemic Brain Injury. In: Pickard J, Akalan N, Rocco C, Dolenc VV, Fahlbusch R, editors. Advances and Technical Standards in Neurosurgery: Springer Vienna In: Pickard J, Akalan N, Rocco C, Dolenc VV, Fahlbusch R, editors. pp. 3-49.
9. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, et al. (2011) Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 31: 17-35.
10. Takano T, Tian G-F, Peng W, Lou N, Lovatt D, et al. (2007) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10: 754-762.
11. Andrew RD, Macvicar BA, (1994) Imaging cell volume changes and neuronal excitation in the hippocampal slice. Neuroscience 62: 371-383.
12. Obeidat AS, Jarvis CR, Andrew RD, (2000) Glutamate Does Not Mediate Acute Neuronal Damage After Spreading Depression Induced By O2/Glucose Deprivation in the Hippocampal Slice. J Cereb Blood Flow Metab 20: 412-422.
13. Brown CE, Wong C, Murphy TH, (2008) Rapid Morphologic Plasticity of Peri-Infarct Dendritic Spines After Focal Ischemic Stroke. Stroke 39: 1286-1291.
14. Branston NM, Strong AJ, Symon L, (1977) Extracellular potassium activity, evoked potential and tissue blood flow: Relationships during progressive ischaemia in baboon cerebral cortex. Journal of the Neurological Sciences 32: 305-321.
15. Back T, Ginsberg MD, Dietrich WD, Watson BD, (1996) Induction of Spreading Depression in the Ischemic Hemisphere Following Experimental Middle Cerebral Artery Occlusion: Effect on Infarct Morphology. J Cereb Blood Flow Metab 16: 202-213.
16. Risher WC, Ard D, Yuan J, Kirov SA, (2010) Recurrent Spontaneous Spreading Depolarizations Facilitate Acute Dendritic Injury in the Ischemic Penumbra. The Journal of Neuroscience 30: 9859-9868.
17. Church AJ, Andrew RD, (2005) Spreading Depression Expands Traumatic Injury in Neocortical Brain Slices. Journal of Neurotrauma 22: 277-290.
18. Shinohara M, Dollinger B, Brown G, Rapoport S, Sokoloff L, (1979) Cerebral glucose utilization: local changes during and after recovery from spreading cortical depression. Science 203: 188-190.
19. Busch E, Gyngell ML, Eis M, Hoehn-Berlage M, Hossmann K-A, (1996) Potassium-Induced Cortical Spreading Depressions During Focal Cerebral Ischemia in Rats: Contribution to Lesion Growth Assessed by Diffusion-Weighted NMR and Biochemical Imaging. J Cereb Blood Flow Metab 16: 1090-1099.
20. Robertson RM, (2004) Thermal stress and neural function: adaptive mechanisms in insect model systems. Journal of Thermal Biology 29: 351-358.
21. Rodgers CI, Armstrong GAB, Shoemaker KL, LaBrie JD, Moyes CD, et al. (2007) Stress Preconditioning of Spreading Depression in the Locust CNS. Plos One 2.
22. Armstrong GAB, Rodgers CI, Money TGA, Robertson RM, (2009) Suppression of Spreading Depression-Like Events in Locusts by Inhibition of the NO/cGMP/PKG Pathway. Journal of Neuroscience 29: 8225-8235.
23. Rodgers CI, Armstrong GAB, Robertson RM, (2010) Coma in response to environmental stress in the locust: A model for cortical spreading depression. Journal of Insect Physiology 56: 980-990.
24. Van Voorhies WA, (2009) Metabolic function in Drosophila melanogaster in response to hypoxia and pure oxygen. Journal of Experimental Biology 212: 3132-3141.
25. Balestrino M, Young J, Aitken P, (1999) Block of (Na+,K+)ATPase with ouabain induces spreading depression-like depolarization in hippocampal slices. Brain Research 838: 37-44.
26. Rodgers-Garlick CI, Armstrong GAB, Robertson RM, (2011) Metabolic Stress Modulates Motor Patterning via AMP-Activated Protein Kinase. The Journal of Neuroscience 31: 3207-3216.
27. Armstrong GAB, Lopez-Guerrero JJ, Dawson-Scully K, Pena F, Robertson RM, (2010) Inhibition of protein kinase G activity protects neonatal mouse respiratory network from hyperthermic and hypoxic stress. Brain Research 1311: 64-72.
28. Dawson-Scully K, Bukvic D, Chakaborty-Chatterjee M, Ferreira R, Milton SL, et al. (2010) Controlling anoxic tolerance in adult Drosophila via the cGMP-PKG pathway. J Exp Biol 213: 2410-2416.
29. Hansen AJ, (1985) Effect of anoxia on ion distribution in the brain. Physiol Rev 65: 101-148.
30. Peters O, Back T, Lindauer U, Busch C, Megow D, et al. (1998) Increased Formation of Reactive Oxygen Species After Permanent and Reversible Middle Cerebral Artery Occlusion in the Rat. J Cereb Blood Flow Metab 18: 196-205.
31. Ransom CB, Ransom BR, Sontheimer H, (2000) Activity-dependent extracellular K+ accumulation in rat optic nerve: the role of glial and axonal Na+ pumps. The Journal of Physiology 522: 427-442.
32. Gong WJ, Golic KG, (2004) Genomic Deletions of the Drosophila melanogaster Hsp70 Genes. Genetics 168: 1467-1476.
33. Neal SJ, Karunanithi S, Best A, So AK-C, Tanguay RM, et al. (2006) Thermoprotection of synaptic transmission in a Drosophila heat shock factor mutant is accompanied by increased expression of Hsp83 and DnaJ-1. Physiol Genomics 25: 493-501.
34. Xiao C, Mileva-Seitz V, Seroude L, Robertson RM, (2007) Targeting HSP70 to motoneurons protects locomotor activity from hyperthermia in Drosophila. Developmental Neurobiology 67: 438-455.
35. Bellen HJ, Tong C, Tsuda H, (2010) 100 years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future. Nat Rev Neurosci 11: 514-522.
36. Zhou D, Visk DW, Haddad GG, (2009) Drosophila, a Golden Bug, for the Dissection of the Genetic Basis of Tolerance and Susceptibility to Hypoxia. Pediatric Research 66: 239-247.
37. Mies G, lijima T, Hossmann K-A, (1993) Correlation between periinfarct DC shifts and ischaemic neuronal damage in rat. NeuroReport 4: 709-711.
38. Azad P, Zhou D, Russo E, Haddad GG, (2009) Distinct Mechanisms Underlying Tolerance to Intermittent and Constant Hypoxia in Drosophila melanogaster. Plos One 4: e5371.
39. Rodgers CI, LaBrie JD, Robertson RM, (2009) K+ homeostasis and central pattern generation in the metathoracic ganglion of the locust. Journal of Insect Physiology 55: 599-607.
40. Hartings JA, Rolli ML, Lu X-CM, Tortella FC, (2003) Delayed Secondary Phase of Peri-Infarct Depolarizations after Focal Cerebral Ischemia: Relation to Infarct Growth and Neuroprotection. The Journal of Neuroscience 23: 11602-11610.
41. Eikermann-Haerter K, Yuzawa I, Qin T, Wang Y, Baek K, et al. (2011) Enhanced Subcortical Spreading Depression in Familial Hemiplegic Migraine Type 1 Mutant Mice. The Journal of Neuroscience 31: 5755-5763.
42. Plumier J-C, Krueger AM, Currie RW, Kontoyiannis D, Kollias G, et al. (1997) Transgenic mice expressing the human inducible Hsp70 have hippocampal neurons resistant to ischemic injury. Cell Stress Chaperones 2: 162-167.
43. Rajdev S, Hara K, Kokubo Y, Mestril R, Dillmann W, et al. (2000) Mice overexpressing rat heat shock protein 70 are protected against cerebral infarction. Annals of Neurology 47: 782-791.
44. Yenari MA, Fink SL, Sun GH, Chang LK, Patel MK, et al. (1998) Gene therapy with HSP72 is neuroprotective in rat models of stroke and epilepsy. Annals of Neurology 44: 584-591.
45. Giffard RG, Xu L, Zhao H, Carrico W, Ouyang Y, et al. (2004) Chaperones, protein aggregation, and brain protection from hypoxic/ischemic injury. J Exp Biol 207: 3213-3220.
46. Evans CG, Chang L, Gestwicki JE, (2010) Heat Shock Protein 70 (Hsp70) as an Emerging Drug Target. Journal of Medicinal Chemistry 53: 4585-4602.
47. Ekimova IV, Nitsinskaya LE, Romanova IV, Pastukhov YF, Margulis BA, et al. (2010) Exogenous protein Hsp70/Hsc70 can penetrate into brain structures and attenuate the severity of chemically-induced seizures. Journal of Neurochemistry 115: 1035-1044.
48. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF, (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions.Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 175: 179-191.
49. Dawson-Scully K, Armstrong GAB, Kent C, Robertson RM, Sokolowski MB, (2007) Natural Variation in the Thermotolerance of Neural Function and Behavior due to a cGMP-Dependent Protein Kinase. Plos One 2.
50. Wu JS, Luo L, (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat Protocols 1: 2110-2115.