Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy

American Journal of Pathology

Volumn 169, Issue 2, 2006, Pages 566-583

  Adhami, Faisal ^a,b   Liao, Guanghong ^a   Morozov, Yury M ^c   Schloemer, Aryn ^a   Schmithorst, Vincent J ^a   Lorenz, John N ^b   Dunn, R Scott ^a   Vorhees, Charles V ^a   Wills Karp, Marsha ^a   Degen, Jay L ^a   Davis, Roger J ^d   Mizushima, Noboru ^e,f   Rakic, Pasko ^c   Dardzinski, Bernard J ^a   Holland, Scott K ^a   Sharp, Frank R ^g   Kuan, Chia Yi ^a,h  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; CYTOCHROME C; HEAT SHOCK PROTEIN 70; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN CIRCULATION; BRAIN HYPOXIA; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN PERFUSION; CAROTID ARTERY OBSTRUCTION; CELL DEATH; CELL SURVIVAL; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISSEMINATED INTRAVASCULAR CLOTTING; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 33746637534     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.051066     Document Type: Article

References (59)

1. Baron JC: Perfusion thresholds in human cerebral ischemia: historical perspective and therapeutic implications. Cerebrovasc Dis 2001, 11(Suppl 1):S2-S8
2. Sobesky J, Zaro Weber O, Lehnhardt FG, Hesselmann V, Neveling M, Jacobs A, Heiss WD: Does the mismatch match the penumbra? Magnetic resonance imaging and positron emission tomography in early ischemic stroke. Stroke 2005, 36:980-985
3. Yan SF, Mackman N, Kisiel W, Stern DM, Pinsky DJ: Hypoxia/hypoxemia- induced activation of the procoagulant pathways and the pathogenesis of ischemia-associated thrombosis. Arterioscler Thromb Vasc Biol 1999, 19:2029-2035
4. Ten VS, Pinsky DJ: Endothelial response to hypoxia: physiologic adaptation and pathologic dysfunction. Curr Opin Crit Care 2002, 8:242-250
5. Majno G, Ames AI, Chiang J, Wright R: No reflow after cerebral ischaemia. Lancet 1967, 2:569-570
6. Rezkalla SH, Kloner RA: No-reflow phenomenon. Circulation 2002, 105:656-662
7. Levine B, Klionsky DJ: Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004, 6:463-477
8. Clarke PG: Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 1990, 181:195-213
9. Yan L, Vatner DE, Kim SJ, Ge H, Masurekar M, Massover WH, Yang G, Matsui Y, Sadoshima J, Vatner SF: Autophagy in chronically ischemic myocardium. Proc Natl Acad Sci USA 2005, 102:13807-13812
10. Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, Kominami E, Uchiyama Y: Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 1995, 15:1001-1011
11. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uehiyama Y, Hagberg H, Blomgren K: The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 2005, 12:162-176
12. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J: Chemical inhibitor of non-apoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005, 1:112-119
13. Levine S: Anoxic-ischemic encephalopathy in rats. Am J Pathol 1960, 36:1-17
14. Rice III JE, Vannucci RC, Brierley JB: The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 1981, 9:131-141
15. Vannucci SJ, Willing LB, Goto S, Alkayed NJ, Brucklacher RM, Wood TL, Towfighi J, Hum PD, Simpson IA: Experimental stroke in the female diabetic, db/db, mouse. J Cereb Blood Flow Metab 2001, 21:52-60
16. Basu A, Lazovic J, Krady JK, Mauger DT, Rothstein RP, Smith MB, Levison SW: Interleukin-1 and the interleukin-1 type 1 receptor are essential for the progressive neurodegeneration that ensues subsequent to a mild hypoxic/ischemic injury. J Cereb Blood Flow Metab 2005, 25:17-29
17. Busto R, Dietrich WD, Globus MY, Valdes I, Scheinberg P, Ginsberg MD: Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury. J Cereb Blood Flow Metab 1987, 7:729-738
18. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y: In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004, 15:1101-1111
19. Suh TT, Holmback K, Jensen NJ, Daugherty CC, Small K, Simon DI, Potter S, Degen JL: Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev 1995, 9:2020-2033
20. Longa EZ, Weinstein PR, Carlson S, Cummins R: Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989, 20:84-91
21. Franklin KBJ, Paxinos G: The Mouse Brain in Stereotaxic Coordinates. San Diego, Academic Press, 1997
22. Kuan CY, Schloemer AJ, Lu A, Burns KA, Weng WL, Williams MT, Strauss KI, Vorhees CV, Flavell RA, Davis RJ, Sharp FR, Rakic P: Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci 2004, 24:10763-10772
23. Chen J, Jin K, Chen M, Pei W, Kawaguchi K, Greenberg DA, Simon RP: Early detection of DNA strand breaks in the brain after transient focal ischemia: implications for the role of DNA damage in apoptosis and neuronal cell death. J Neurochem 1997, 69:232-245
24. Ding G, Jiang Q, Zhang L, Zhang ZG, Li L, Knight RA, Ewing JR, Wang Y, Chopp M: Analysis of combined treatment of embolic stroke in rat with r-tPA and a GPIIb/IIIa inhibitor. J Cereb Blood Flow Metab 2005, 25:87-97
25. Fishman RA: Brain edema. N Engl J Med 1975, 293:706-711
26. Ginsberg MD: Adventures in the pathophysiology of brain ischemia: penumbra, gene expression, neuroprotection: the 2002 Thomas Willis Lecture. Stroke 2003, 34:214-223
27. Heistad DD, Kontos HA: Cerebral Circulation. Edited by Shepherd JT, Abboud FM, Geiger SR. Bethesda, American Physiological Society, 1983, pp 137-182
28. Williams DS, Detre JA, Leigh JS, Koretsky AP: Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci USA 1992, 89:212-216
29. Moseley ME, Cohen Y, Mintorovitch J, Chileuitt L, Shimizu H, Kucharczyk J, Wendland MF, Weinstein PR: Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med 1990, 14:330-346
30. Steiner T, Ringleb P, Hacke W: Treatment options for large hemispheric stroke. Neurology 2001, 57(Suppl 2):S61-S8
31. Wang X, Barone FC, Aiyar NV, Feuerstein GZ: Interleukin-1 receptor and receptor antagonist gene expression after focal stroke in rats. Stroke 1997, 28:152-161
32. Allan SM, Rothwell NJ: Cytokines and acute neurodegeneration. Nat Rev Neurosci 2001, 2:734-744
33. Noshita N, Lewen A, Sugawara T, Chan PH: Evidence of phosphorylation of Akt and neuronal survival after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 2001, 21:1442-1450
34. Ferrer I, Friguls B, Dalfo E, Planas AM: Early modifications in the expression of mitogen-activated protein kinase (MAPK/ERK), stress-activated kinases SAPK/JNK and p38, and their phosphorylated substrates following focal cerebral ischemia. Acta Neuropathol (Berl) 2003, 105:425-437
35. Kokubo Y, Liu J, Rajdev S, Kayama T, Sharp FR, Weinstein PR: Differential cerebral protein synthesis and heat shock protein 70 expression in the core and penumbra of rat brain after transient focal ischemia. Neurosurgery 2003, 53:186-190
36. Sharp FR, Lu A, Tang Y, Millhorn DE: Multiple molecular penumbras after focal cerebral ischemia. J Cereb Blood Flow Metab 2000, 20:1011-1032
37. Ferrer I, Planas AM: Signaling of cell death and cell survival following focal cerebral ischemia: life and death struggle in the penumbra. J Neuropathol Exp Neurol 2003, 62:329-339
38. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin TT, Yu VL, Miller DK: Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995, 376:37-43
39. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA: Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 1996, 384:368-372
40. Hillhouse EW, Kida S, Iannotti F: Middle cerebral artery occlusion in the rat causes a biphasic production of immunoreactive interleukin-1beta in the cerebral cortex. Neurosci Lett 1998, 249:177-179
41. Benchoua A, Guegan C, Couriaud C, Hosseini H, Sampaio N, Morin D, Onteniente B: Specific caspase pathways are activated in the two stages of cerebral infarction. J Neurosci 2001, 21:7127-7134
42. Xue L, Fletcher GC, Tolkovsky AM: Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol Cell Neurosci 1999, 14:180-198
43. Edinger AL, Thompson CB: Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004, 16:663-669
44. Kroemer G, Jaattela M: Lysosomes and autophagy in cell death control. Nat Rev Cancer 2005, 5:886-897
45. Tsujimoto Y, Shimizu S: Another way to die: autophagic programmed cell death. Cell Death Differ 2005, 12(Suppl 2):S1528-S1534
46. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000, 19:5720-5728
47. Mann SS, Hammarback JA: Molecular characterization of light chain 3. A microtubule binding subunit of MAP1A and MAP1B. J Biol Chem 1994, 269:11492-11497
48. Mizushima N: Methods for monitoring autophagy. Int J Biochem Cell Biol 2004, 36:2491-2502
49. del Zoppo GJ, Mabuchi T: Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab 2003, 23:879-894
50. Okada Y, Copeland BR, Mori E, Tung MM, Thomas WS, del Zoppo GJ: P-selectin and intercellular adhesion molecule-1 expression after focal brain ischemia and reperfusion. Stroke 1994, 25:202-211
51. Okada Y, Copeland BR, Fitridge R, Koziol JA, del Zoppo GJ: Fibrin contributes to microvascular obstructions and parenchymal changes during early focal cerebral ischemia and reperfusion. Stroke 1994, 25:1847-1853
52. Zhang R, Chopp M, Zhang Z, Jiang N, Powers C: The expression of P- and E-selectins in three models of middle cerebral artery occlusion. Brain Res 1998, 785:207-214
53. Ishikawa M, Cooper D, Russell J, Salter JW, Zhang JH, Nanda A, Granger DN: Molecular determinants of the prothrombogenic and inflammatory phenotype assumed by the postischemic cerebral microcirculation. Stroke 2003, 34:1777-1782
54. Fujii M, Hara H, Meng W, Vonsattel JP, Huang Z, Moskowitz MA: Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57black/6 mice. Stroke 1997, 28:1805-1811
55. Majid A, He YY, Gidday JM, Kaplan SS, Gonzales ER, Park TS, Fenstermacher JD, Wei L, Choi DW, Hsu CY: Differences in vulnerability to permanent focal cerebral ischemia among 3 common mouse strains. Stroke 2000, 31:2707-2714
56. Fischer M, Hossmann KA: No-reflow after cardiac arrest. Intensive Care Med 1995, 21:132-141
57. Colbourne F, Sutherland GR, Auer RN: Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J Neurosci 1999, 19:4200-4210
58. Northington FJ, Ferriero DM, Graham EM, Traystman RJ, Martin LJ: Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol Dis 2001, 8:207-219
59. Joly LM, Mucignat V, Mariani J, Plotkine M, Charriaut-Marlangue C: Caspase inhibition after neonatal ischemia in the rat brain. J Cereb Blood Flow Metab 2004, 24:124-131