Purinergic receptor stimulation reduces cytotoxic edema and brain infarcts in mouse induced by photothrombosis by energizing glial mitochondria

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Zheng, Wei ^a   Watts, Lora Talley ^a   Holstein, Deborah M ^a   Prajapati, Suresh I ^b   Keller, Charles ^a,b   Grass, Eileen H ^a   Walter, Christi A ^a   Lechleiter, James D ^a  

^a University of Texas Health Science Center   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYLTHIOLADENOSINE 5' DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; GREEN FLUORESCENT PROTEIN; INOSITOL TRISPHOSPHATE; PURINERGIC P2Y1 RECEPTOR; PURINERGIC RECEPTOR STIMULATING AGENT; UNCLASSIFIED DRUG; 2 METHYLTHIOADENOSINE DIPHOSPHATE; 2-METHYLTHIO-ADP; ADENOSINE DIPHOSPHATE; DRUG DERIVATIVE; INOSITOL 1,4,5 TRISPHOSPHATE; NUCLEOTIDE; PURINERGIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN EDEMA; BRAIN INFARCTION; BRAIN MITOCHONDRION; BRAIN PROTECTION; CALCIUM TRANSPORT; CELL FUNCTION; CELL SWELLING; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DRUG MECHANISM; ENERGY METABOLISM; IMAGE ANALYSIS; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; THERAPY DELAY; THROMBOSIS; ANIMAL; CYTOLOGY; EDEMA; GLIA; LIGHT; METABOLISM; MITOCHONDRION; PATHOLOGY;

ADENOSINE DIPHOSPHATE; ANIMALS; ASTROCYTES; BRAIN INFARCTION; CEREBRAL INFARCTION; EDEMA; INOSITOL 1,4,5-TRISPHOSPHATE; LIGHT; MALE; MICE; MITOCHONDRIA; NEUROGLIA; RECEPTORS, PURINERGIC; RECEPTORS, PURINERGIC P2Y1; THIONUCLEOTIDES; THROMBOSIS;

EID: 78650981570     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014401     Document Type: Article

References (52)

1. Rosenblum WI (2007) Cytotoxic edema: monitoring its magnitude and contribution to brain swelling. J Neuropathol Exp Neurol 66: 771-778.
2. Liang D, Bhatta S, Gerzanich V, Simard JM (2007) Cytotoxic edema: mechanisms of pathological cell swelling. Neurosurg Focus 22: E2.
3. Unterberg AW, Stover J, Kress B, Kiening KL (2004) Edema and brain trauma. Neuroscience 129: 1021-1029.
4. Heo JH, Han SW, Lee SK (2005) Free radicals as triggers of brain edema formation after stroke. Free Radic Biol Med 39: 51-70.
5. Woitzik J, Back T, Thome C (2008) Flow-dependent versus spreading-like impairment of brain tissue integrity during focal cerebral ischemia and its consequences for neuroprotective strategies. Front Biosci 13: 1500-1506.
6. Nedergaard M, Dirnagl U (2005) Role of glial cells in cerebral ischemia. Glia 50: 281-286.
7. Fisher M, Davalos A (2004) Emerging therapies for cerebrovascular disorders. Stroke 35: 367-369.
8. Hertz L, Peng L, Dienel GA (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27: 219-249.
9. Brown AM, Ransom BR (2007) Astrocyte glycogen and brain energy metabolism. Glia 55: 1263-1271.
10. Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26: 523-530.
11. Cherniak C (1990) The bounded brain: toward quantitative neuroanatomy. J Cogn Neurosci 2: 58-68.
12. Watts LT, Lechleiter JD (2008) The impact of astrocyte mitochondrial metabolism on neuroprotection during aging. In: Parpura V, Haydon PG, eds. Astrocytes in (patho) physiology of the nervous system. BostonMA: Springer. pp 569-590.
13. Meairs S, Wahlgren N, Dirnagl U, Lindvall O, Rothwell P, et al. (2006) Stroke research priorities for the next decade-A representative view of the European scientific community. Cerebrovasc Dis 22: 75-82.
14. Haberg A, Qu H, Sonnewald U (2006) Glutamate and GABA metabolism in transient and permanent middle cerebral artery occlusion in rat: importance of astrocytes for neuronal survival. Neurochem Int 48: 531-540.
15. Kimelberg HK (2005) Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia 50: 389-397.
16. Chu X, Fu X, Zou L, Qi C, Li Z, et al. (2007) Oncosis, the possible cell death pathway in astrocytes after focal cerebral ischemia. Brain Res 1149: 157-164.
17. Hajnoczky G, Csordas G, Krishnamurthy R, Szalai G (2000) Mitochondrial calcium signaling driven by the IP3 receptor. J Bioenerg Biomembr 32: 15-25.
18. McCormack JG, Halestrap AP, Denton PM (1990) Role of calcium ions regulation of mammalian intramitochondrial metabolism. Physiol Rev 70: 391-425.
19. Territo PR, Mootha VK, French SA, Balaban RS (2000) Ca(2+) activation of heart mitochondrial oxidative phosphorylation: role of the F(0)/F(1)-ATPase. Am J Physiol Cell Physiol 278: C423-C435.
20. James G, Butt AM (2002) P2Y and P2X purinoceptor mediated Ca2+ signalling in glial cell pathology in the central nervous system. Eur J Pharmacol 447: 247-260.
21. Verkhratsky A, Kettenmann H (1996) Calcium signalling in glial cells. Trends Neurosci 19: 346-352.
22. Wu J, Holstein JD, Upadhyay G, Lin DT, Conway S, et al. (2007) Purinergic receptor-stimulated IP3-mediated Ca2+ release enhances neuroprotection by increasing astrocyte mitochondrial metabolism during aging. J Neurosci 27: 6510-6520.
23. Watson BD, Dietrich WD, Busto R, Wachtel MS, Ginsberg MD (1985) Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 17: 497-504.
24. Ishikawa M, Vowinkel T, Stokes KY, Arumugam TV, Yilmaz G, et al. (2005) CD40/CD40 ligand signaling in mouse cerebral microvasculature after focal ischemia/reperfusion. Circulation 111: 1690-1696.
25. Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, et al. (1986) Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17: 1304-1308.
26. Fonnum F, Johnsen A, Hassel B (1997) Use of fluorocitrate and fluoroacetate in the study of brain metabolism. Glia 21: 106-113.
27. Grass E, Bai Y, Houten BV, Santos J, Hunter S, et al. (2009) EcoRI targeted to Mitochondria Results in Mitochondrial DNA Depletion, Dysfunction, and Myopathy. in preparation.
28. Chen Y, Swanson RA (2003) Astrocytes and brain injury. J Cereb Blood Flow Metab 23: 137-149.
29. Dienel GA, Hertz L (2005) Astrocytic contributions to bioenergetics of cerebral ischemia. Glia 50: 362-388.
30. Ballabh P, Braun A, Nedergaard M (2004) The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 16: 1-13.
31. Pangrsic T, Potokar M, Haydon PG, Zorec R, Kreft M (2006) Astrocyte swelling leads to membrane unfolding, not membrane insertion. J Neurochem 99: 514-523.
32. Chvatal A, Anderova M, Kirchhoff F (2007) Three-dimensional confocal morphometry - a new approach for studying dynamic changes in cell morphology in brain slices. J Anat 210: 671-683.
33. Risher WC, Andrew RD, Kirov SA (2009) Real-time passive volume responses of astrocytes to acute osmotic and ischemic stress in cortical slices and in vivo revealed by two-photon microscopy. Glia 57: 207-221.
34. Pauser S, Zschunke A, Khuen A, Keller K (1995) Estimation of water content and water mobility in the nucleus and cytoplasm of Xenopus laevis oocytes by NMR microscopy. Magn Reson Imaging 13: 269-276.
35. Pasantes-Morales H, Murray RA, Lilja L, Moran J (1994) Regulatory volume decrease in cultured astrocytes. I. Potassium- and chloride-activated permeability. Am J Physiol 266: C165-C171.
36. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, et al. (1998) Functional significance of cell volume regulatory mechanisms. Physiol Rev 78: 247-306.
37. Uckermann O, Wolf A, Kutzera F, Kalisch F, Beck-Sickinger AG, et al. (2006) Glutamate release by neurons evokes a purinergic inhibitory mechanism of osmotic glial cell swelling in the rat retina: activation by neuropeptide Y. J Neurosci Res 83: 538-550.
38. Mongin AA, Kimelberg HK (2002) ATP potently modulates anion channelmediated excitatory amino acid release from cultured astrocytes. Am J Physiol Cell Physiol 283: C569-C578.
39. Fujita T, Tozaki-Saitoh H, Inoue K (2009) P2Y1 receptor signaling enhances neuroprotection by astrocytes against oxidative stress via IL-6 release in hippocampal cultures. Glia 57: 244-257.
40. Darby M, Kuzmiski JB, Panenka W, Feighan D, MacVicar BA (2003) ATP released from astrocytes during swelling activates chloride channels. J Neurophysiol 89: 1870-1877.
41. Dietrich HH, Horiuchi T, Xiang C, Hongo K, Falck JR, et al. (2009) Mechanism of ATP-induced local and conducted vasomotor responses in isolated rat cerebral penetrating arterioles. J Vasc Res 46: 253-264.
42. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456: 745-749.
43. LeMaistre JL, Anderson CM (2009) Custom astrocyte-mediated vasomotor responses to neuronal energy demand. Genome Biol 10: 209.
44. Leis JA, Bekar LK, Walz W (2005) Potassium homeostasis in the ischemic brain. Glia 50: 407-416.
45. Siushansian R, Bechberger JF, Cechetto DF, Hachinski VC, Naus CC (2001) Connexin43 null mutation increases infarct size after stroke. J Comp Neurol 440: 387-394.
46. Nakase T, Fushiki S, Sohl G, Theis M, Willecke K, et al. (2003) Neuroprotective role of astrocytic gap junctions in ischemic stroke. Cell Commun Adhes 10: 413-417.
47. Ying WL, Emerson J, Clarke MJ, Sanadi DR (1991) Inhibition of mitochondrial calcium ion transport by an oxo-bridged dinuclear ruthenium ammine complex. Biochemistry 30: 4949-4952.
48. Gachet C, Cattaneo M, Ohlmann P, Hechler B, Lecchi A, et al. (1995) Purinoceptors on blood platelets: further pharmacological and clinical evidence to suggest the presence of two ADP receptors. Br J Haematol 91: 434-444.
49. Leary MC, Saver JL (2003) Annual incidence of first silent stroke in the United States: a preliminary estimate. Cerebrovasc Dis 16: 280-285.
50. Howard G, Safford MM, Meschia JF, Moy CS, Howard VJ, et al. (2007) Stroke symptoms in individuals reporting no prior stroke or transient ischemic attack are associated with a decrease in indices of mental and physical functioning. Stroke 38: 2446-2452.
51. Klohs J, Grafe M, Graf K, Steinbrink J, Dietrich T, et al. (2008) In vivo imaging of the inflammatory receptor CD40 after cerebral ischemia using a fluorescent antibody. Stroke 39: 2845-2852.
52. Wunder A, Klohs J, Dirnagl U (2009) Non-invasive visualization of CNS inflammation with nuclear and optical imaging. Neuroscience 158: 1161-1173.