Role of gap junctions in early brain injury following subarachnoid hemorrhage

Brain Research

Volumn 1315, Issue , 2010, Pages 150-158

  Ayer, Robert ^b   Chen, Wanqiu ^a   Sugawara, Takashi ^a   Suzuki, Hidenori ^a   Zhang, John H ^a,b  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOMA LINDA UNIVERSITY   (United States)

Author keywords

Carbenoxolone; Connexin 43; Early Brain Injury; Gap Junction; Octanol; Subarachnoid Hemorrhage

Indexed keywords

CARBANEXOLONE; GAP JUNCTION INHIBITOR; NEUROPROTECTIVE AGENT; OCTANAL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN VASOSPASM; CELL COMMUNICATION; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG INHIBITION; GAP JUNCTION; IN VIVO STUDY; MALE; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; SUBARACHNOID HEMORRHAGE; TREATMENT FAILURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BRAIN; BRAIN INJURIES; CARBENOXOLONE; DISEASE MODELS, ANIMAL; GAP JUNCTIONS; INJECTIONS, INTRAPERITONEAL; MALE; NEUROPROTECTIVE AGENTS; OCTANOLS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SEVERITY OF ILLNESS INDEX; SUBARACHNOID HEMORRHAGE; TIME FACTORS; TREATMENT OUTCOME;

RATTUS;

EID: 75349099752     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.12.016     Document Type: Article

References (61)

1. Asano T. Oxyhemoglobin as the principal cause of cerebral vasospasm: a holistic view of its actions. Crit Rev. Neurosurg. 9 5 (1999) 303-318
2. Ayer R.E., and Zhang J.H. The clinical significance of acute brain injury in subarachnoid hemorrhage and opportunity for intervention. Acta Neurochir. Suppl. 105 (2008) 179-184
3. Ayer R.E., Sugawara T., Chen W., Tong W., and Zhang J.H. Melatonin decreases mortality following severe subarachnoid hemorrhage. J. Pineal Res. 44 2 (2008) 197-204
4. Bederson J.B., Germano I.M., and Guarino L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 26 6 (1995) 1086-1091
5. Bennett M.V., and Goodenough D.A. Gap junctions, electrotonic coupling, and intercellular communication. Neurosci. Res. Program Bull. 16 3 (1978) 1-486
6. Broderick J.P., Brott T., Tomsick T., Huster G., and Miller R. The risk of subarachnoid and intracerebral hemorrhages in blacks as compared with whites. N. Engl. J. Med. 326 11 (1992) 733-736
7. Broderick J.P., Brott T.G., Duldner J.E., Tomsick T., and Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 25 7 (1994) 1342-1347
8. Cahill J., Calvert J.W., Solaroglu I., and Zhang J.H. Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 37 7 (2006) 1868-1874
9. Cahill J., Calvert J.W., and Zhang J.H. Mechanisms of early brain injury after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 26 11 (2006) 1341-1353
10. Cahill J., Calvert J.W., Marcantonio S., and Zhang J.H. p53 may play an orchestrating role in apoptotic cell death after experimental subarachnoid hemorrhage. Neurosurgery 60 3 (2007) 531-545
11. Claassen J., Bernardini G.L., Kreiter K., Bates J., Du Y.E., Copeland D., Connolly E.S., and Mayer S.A. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 32 9 (2001) 2012-2020
12. Colombel C., Lalonde R., and Caston J. The effects of unilateral removal of the cerebellar hemispheres on motor functions and weight gain in rats. Brain Res. 950 1-2 (2002) 231-238
13. Cusato K., Bosco A., Rozental R., Guimaraes C.A., Reese B.E., Linden R., and Spray D.C. Gap junctions mediate bystander cell death in developing retina. J. Neurosci. 23 16 (2003) 6413-6422
14. de Pina-Benabou M.H., Szostak V., Kyrozis A., Rempe D., Uziel D., Urban-Maldonado M., Benabou S., Spray D.C., Federoff H.J., Stanton P.K., and Rozental R. Blockade of gap junctions in vivo provides neuroprotection after perinatal global ischemia. Stroke 36 10 (2005) 2232-2237
15. Dermietzel R., Traub O., Hwang T.K., Beyer E., Bennett M.V., Spray D.C., and Willecke K. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc. Natl. Acad. Sci. U. S. A. 86 24 (1989) 10148-10152
16. Endo H., Nito C., Kamada H., Yu F., and Chan P.H. Reduction in oxidative stress by superoxide dismutase overexpression attenuates acute brain injury after subarachnoid hemorrhage via activation of Akt/glycogen synthase kinase-3beta survival signaling. J. Cereb. Blood Flow Metab. 27 5 (2007) 975-982
17. Fergusen S., and Macdonald R.L. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery 60 4 (2007) 658-667
18. Fisher C.M., Roberson G.H., and Ojemann R.G. Cerebral vasospasm with ruptured saccular aneurysm-the clinical manifestations. Neurosurgery 1 3 (1977) 245-248
19. Frantseva M.V., Kokarovtseva L., Naus C.G., Carlen P.L., MacFabe D., and Perez Velazquez J.L. Specific gap junctions enhance the neuronal vulnerability to brain traumatic injury. J. Neurosci. 22 3 (2002) 644-653
20. Garcia J.H., Wagner S., Liu K.F., and Hu X.J. Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Statistical validation. Stroke 26 4 (1995) 627-634
21. Goldman D.W., Breyer III R.J., Yeh D., Brockner-Ryan B.A., and Alayash A.I. Acellular hemoglobin-mediated oxidative stress toward endothelium: a role for ferryl iron. Am. J. Physiol 275 3 Pt 2 (1998) H1046-H1053
22. Haley Jr. E.C., Kassell N.F., and Torner J.C. A randomized trial of nicardipine in subarachnoid hemorrhage: angiographic and transcranial Doppler ultrasound results. A report of the Cooperative Aneurysm Study. J. Neurosurg. 78 4 (1993) 548-553
23. Hong T., Wang Y., Wang H.T., and Wang H. Inhibitory effect of gap junction blockers on cerebral vasospasm. J. Neurosurg. 108 3 (2008) 551-557
24. Hong T., Wang H., Wang Y., and Wang H. Effects of gap junctional blockers on cerebral vasospasm after subarachnoid hemorrhage in rabbits. Neurol. Res. 31 3 (2009) 238-244
25. Jellinck P.H., Monder C., McEwen B.S., and Sakai R.R. Differential inhibition of 11 beta-hydroxysteroid dehydrogenase by carbenoxolone in rat brain regions and peripheral tissues. J. Steroid Biochem. Mol. Biol. 46 2 (1993) 209-213
26. Kamiya K., Kuyama H., and Symon L. An experimental study of the acute stage of subarachnoid hemorrhage. J. Neurosurg. 59 6 (1983) 917-924
27. Kassell N.F., Sasaki T., Colohan A.R., and Nazar G. Cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Stroke 16 4 (1985) 562-572
28. Kaynar M.Y., Tanriverdi T., Kemerdere R., Atukeren P., and Gumustas K. Cerebrospinal fluid superoxide dismutase and serum malondialdehyde levels in patients with aneurysmal subarachnoid hemorrhage: preliminary results. Neurol. Res. 27 5 (2005) 562-567
29. Kubota T., Handa Y., Tsuchida A., Kaneko M., Kobayashi H., and Kubota T. The kinetics of lymphocyte subsets and macrophages in subarachnoid space after subarachnoid hemorrhage in rats. Stroke 24 12 (1993) 1993-2000
30. Lampe P.D., TenBroek E.M., Burt J.M., Kurata W.E., Johnson R.G., and Lau A.F. Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication. J. Cell Biol. 149 7 (2000) 1503-1512
31. Laszlo F.A., Varga C., and Doczi T. Cerebral oedema after subarachnoid haemorrhage. Pathogenetic significance of vasopressin. Acta Neurochir. (Wien.) 133 3-4 (1995) 122-133
32. Lin J.H., Weigel H., Cotrina M.L., Liu S., Bueno E., Hansen A.J., Hansen T.W., Goldman S., and Nedergaard M. Gap-junction-mediated propagation and amplification of cell injury. Nat. Neurosci. 1 6 (1998) 494-500
33. Macdonald R.L., Kassell N.F., Mayer S., Ruefenacht D., Schmiedek P., Weidauer S., Frey A., Roux S., and Pasqualin A. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke 39 11 (2008) 3015-3021
34. Mackay J G.A.M.S.M.K. The Atlas of Heart Disease and Stroke (2004), World Health Organization
35. Mandal M., Mandal A., Das S., Chakraborti T., and Sajal C. Clinical implications of matrix metalloproteinases. Mol. Cell. Biochem. 252 1-2 (2003) 305-329
36. Martin F.C., and Handforth A. Carbenoxolone and mefloquine suppress tremor in the harmaline mouse model of essential tremor. Mov. Disord. 21 10 (2006) 1641-1649
37. Mathiesen T., and Lefvert A.K. Cerebrospinal fluid and blood lymphocyte subpopulations following subarachnoid haemorrhage. Br. J. Neurosurg. 10 1 (1996) 89-92
38. Matz P.G., Fujimura M., and Chan P.H. Subarachnoid hemolysate produces DNA fragmentation in a pattern similar to apoptosis in mouse brain. Brain Res. 858 2 (2000) 312-319
39. McCormick W.F., and Nofzinger J.D. Saccular intracranial aneurysms: an autopsy study. J. Neurosurg. 22 (1965) 155-159
40. Nagy J.I., and Rash J.E. Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res. Brain Res. Rev. 32 1 (2000) 29-44
41. Naus C.C., and Bani-Yaghoub M. Gap junctional communication in the developing central nervous system. Cell Biol. Int. 22 11-12 (1998) 751-763
42. Nolan C.P., and Macdonald R.L. Can angiographic vasospasm be used as a surrogate marker in evaluating therapeutic interventions for cerebral vasospasm?. Neurosurg. Focus 21 3 (2006) E1
43. Ostrowski R.P., Colohan A.R., and Zhang J.H. Mechanisms of hyperbaric oxygen-induced neuroprotection in a rat model of subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 25 5 (2005) 554-571
44. Ostrowski R.P., Colohan A.R., and Zhang J.H. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol. Res. 28 4 (2006) 399-414
45. Perez Velazquez J.L., Kokarovtseva L., Sarbaziha R., Jeyapalan Z., and Leshchenko Y. Role of gap junctional coupling in astrocytic networks in the determination of global ischaemia-induced oxidative stress and hippocampal damage. Eur. J. Neurosci. 23 1 (2006) 1-10
46. Petruk K.C., West M., Mohr G., Weir B.K., Benoit B.G., Gentili F., Disney L.B., Khan M.I., Grace M., and Holness R.O. Nimodipine treatment in poor-grade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial. J. Neurosurg. 68 4 (1988) 505-517
47. Polidori M.C., Frei B., Rordorf G., Ogilvy C.S., Koroshetz W.J., and Beal M.F. Increased levels of plasma cholesteryl ester hydroperoxides in patients with subarachnoid hemorrhage. Free Radic. Biol. Med. 23 5 (1997) 762-767
48. Prunell G.F., Svendgaard N.A., Alkass K., and Mathiesen T. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J. Neurosurg. 102 6 (2005) 1046-1054
49. Rabinstein A.A., Friedman J.A., Weigand S.D., McClelland R.L., Fulgham J.R., Manno E.M., Atkinson J.L., and Wijdicks E.F. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 35 8 (2004) 1862-1866
50. Rami A., Volkmann T., and Winckler J. Effective reduction of neuronal death by inhibiting gap junctional intercellular communication in a rodent model of global transient cerebral ischemia. Exp. Neurol. 170 2 (2001) 297-304
51. Rawanduzy A., Hansen A., Hansen T.W., and Nedergaard M. Effective reduction of infarct volume by gap junction blockade in a rodent model of stroke. J. Neurosurg. 87 6 (1997) 916-920
52. Rogers M.S., Patel R.P., Reeder B.J., Sarti P., Wilson M.T., and Alayash A.I. Pro-oxidant effects of cross-linked haemoglobins explored using liposome and cytochrome c oxidase vesicle model membranes. Biochem. J. 310 Pt 3 (1995) 827-833
53. Sarti P., Hogg N., Darley-Usmar V.M., Sanna M.T., and Wilson M.T. The oxidation of cytochrome-c oxidase vesicles by hemoglobin. Biochim. Biophys. Acta 1208 1 (1994) 38-44
54. Schievink W.I., Wijdicks E.F., Parisi J.E., Piepgras D.G., and Whisnant J.P. Sudden death from aneurysmal subarachnoid hemorrhage. Neurology 45 5 (1995) 871-874
55. Shimoda M., Takeuchi M., Tominaga J., Oda S., Kumasaka A., and Tsugane R. Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarachnoid hemorrhage: serial magnetic resonance imaging. Neurosurgery 49 6 (2001) 1341-1348
56. Solan J.L., and Lampe P.D. Key connexin 43 phosphorylation events regulate the gap junction life cycle. J. Membr. Biol. 217 1-3 (2007) 35-41
57. Sugawara T., Ayer R., Jadhav V., and Zhang J.H. A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J. Neurosci. Methods 167 2 (2008) 327-334
58. Sugawara T., Jadhav V., Ayer R., Chen W., Suzuki H., and Zhang J.H. Thrombin inhibition by argatroban ameliorates early brain injury and improves neurological outcomes after experimental subarachnoid hemorrhage in rats. Stroke 40 4 (2009) 1530-1532
59. Vajkoczy P., Meyer B., Weidauer S., Raabe A., Thome C., Ringel F., Breu V., and Schmiedek P. Clazosentan (AXV-034343), a selective endothelin A receptor antagonist, in the prevention of cerebral vasospasm following severe aneurysmal subarachnoid hemorrhage: results of a randomized, double-blind, placebo-controlled, multicenter phase IIa study. J. Neurosurg. 103 1 (2005) 9-17
60. Yatsushige H., Ostrowski R.P., Tsubokawa T., Colohan A., and Zhang J.H. Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J. Neurosci. Res. 85 7 (2007) 1436-1448
61. Zhang Z.G., Zhang L., Jiang Q., Zhang R., Davies K., Powers C., Bruggen N., and Chopp M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 106 7 (2000) 829-838