Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its region-specific relationship to apoptotic mechanisms

American Journal of Pathology

Volumn 175, Issue 5, 2009, Pages 1962-1974

  Ginet, Vanessa ^a,b   Puyal, Julien ^b   Clarke, Peter G H ^a   Truttmann, Anita C ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; BETA N ACETYLHEXOSAMINIDASE; CASPASE 3; CATHEPSIN D; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 11; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERY LIGATION; ARTICLE; AUTOPHAGY; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN NERVE CELL; CELL DEATH; CEREBRAL BLINDNESS; COMMON CAROTID ARTERY; CONTROLLED STUDY; HIPPOCAMPUS; LYSOSOME; MALE; MICROTUBULE; NECROSIS; NEWBORN HYPOXIA; NONHUMAN; PERINATAL ASPHYXIA; PHENOTYPE; PRIORITY JOURNAL; RAT;

EID: 73849114180     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.090463     Document Type: Article

References (61)

1. Volpe JJ: Perinatal brain injury: from pathogenesis to neuroprotection. Ment Retard Dev Disabil Res Rev 2001, 7:56-64
2. Ferriero DM: Neonatal brain injury. N Engl J Med 2004, 351:1985-1995
3. Sahni R, Sanocka UM: Hypothermia for hypoxic-ischemic encephalopathy. Clin Perinatol 2008, 35:717-734
4. Portera-Cailliau C, Price DL, Martin LJ: Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 1997, 378:70-87
5. Northington FJ, Zelaya ME, O'Riordan DP, Blomgren K, Flock DL, Hagberg H, Ferriero DM, Martin LJ: Failure to complete apoptosis following neonatal hypoxia-ischemia manifests as "continuum" phenotype of cell death and occurs with multiple manifestations of mitochondrial dysfunction in rodent forebrain. Neuroscience 2007, 149:822-833
6. Clarke PGH: Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 1990, 181:195-213
7. Clarke PGH, Puyal J, Vaslin A, Ginet V, Truttmann A: Multiple types of programmed cell death and their relevance to perinatal brain damage. In perinatal brain damage: from pathogenesis to neuroprotection, chp 3. Edited by LA Ramenghi, P Evrard, and E. Mercuri. Mariani Foundation Paediatric Neurology Series 19, John Libbey Eurotext, Montrouge, France, 2008, pp. 23-35
8. Shintani T, Klionsky DJ: Autophagy in health and disease: a double-edged sword. Science 2004, 306:990-995
9. Codogno P, Meijer AJ: Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 2005, 12:1509-1518
10. Boland B, Nixon RA: Neuronal macroautophagy: from development to degeneration. Mol Aspects Med 2006, 27:503-519
11. Borsello T, Croquelois K, Hornung JP, Clarke PGH: N-Methyl-D-aspartate-triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway. Eur J Neurosci 2003, 18:473-485
12. Matyja E, Taraszewska A, Nagańska E, Rafałowska J: Autophagic degeneration of motor neurons in a model of slow glutamate excito-toxicity in vitro. Ultrastruct Pathol 2005, 29:331-339
13. Shacka JJ, Lu J, Xie ZL, Uchiyama Y, Roth KA, Zhang J: Kainic acid induces early and transient autophagic stress in mouse hippocampus. Neurosci Lett 2007, 414:57-60
14. Wang Y, Han R, Liang ZQ, Wu JC, Zhang XD, Gu ZL, Qin ZH: An autophagic mechanism is involved in apoptotic death of rat striatal neurons induced by the non-N-methyl-D-aspartate receptor agonist kainic acid. Autophagy 2008, 4:214-226
15. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y, Hagberg H, Blomgren K: The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death and Diff 2005, 12:162-176
16. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, Dunn RS, Vorhees CV, Wills-Karp M, Degen JL, Davis RJ, Mizushima N, Rakic P, Dardzinski BJ, Holland SK, Sharp FR, Kuan CY: Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 2006, 169:566-583
17. Wen YD, Sheng R, Zhang LS, Han R, Zhang X, Zhang XD, Han F, Fukunaga K, Qin ZH: Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 2008, 4:762-769
18. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, Tanaka K, Uchiyama Y: Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 2008, 172:454-469
19. Rice JE, Vannucci RC, Brierley JB: The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 1981, 9:131-141
20. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, Nixon RA: Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci 2008, 28:6926-6937
21. Levine S: Anoxic-ischemic encephalopathy in rats. Am J Pathol 1960, 36:1-17
22. Gömöri G: Distribution of acid phosphatase in tissues under normal and under pathologic conditions. Arch Path 1941, 32:189-199
23. Katayama Y, Kobatake H, Shida H: A modified technique of histochemical demonstration for N-acetyl-β-hexosaminidase. Acta Histochem Cytochem 1976, 9:111-124
24. Wang KK: Calpain and caspase: can you tell the difference? Trends Neurosci 2000, 23:20-26
25. Ginet V, Puyal J, Magnin G, Clarke PG, Truttmann AC: Limited role of the c-Jun N-terminal kinase pathway in a neonatal rat model of cerebral hypoxia-ischemia. J Neurochem 2009, 108:552-562
26. Vannucci RC, Vannucci SJ: A model of perinatal hypoxic-ischemic brain damage. Ann NY Acad Sci 1997, 835:234-249
27. Hagberg H, Ichord R, Palmer C, Yager JY, Vannucci SJ: Animal models of developmental brain injury: relevance to human disease - a summary of the panel discussion from the Third Hershey Conference on Developmental Cerebral Blood Flow and Metabolism. Dev Neurosci 2002, 24:364-366
28. Johnston MV, Trescher WH, Ishida A, Nakajima W: Neurobiology of hypoxic-ischemic injury in the developing brain. Pediatr Res 2003, 49:735-741
29. 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 autophagosomes membranes after processing EMBO J 2000, 19:5720-5728
30. Tanida I, Ueno T, Kominami E: LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 2004, 36:2503-2518
31. Nitatori T, Sato N, Kominami E, Uchiyama Y: Participation of cathepsins B, H, and L in perikaryal condensation of CA1 pyramidal neurons undergoing apoptosis after brief ischemia. Adv Exp Med Biol 1996, 389:177-185
32. Kohda Y, Yamashima T, Sakuda K, Yamashita J, Ueno T, Kominami E, Yoshioka T: Dynamic changes of cathepsins B and L expression in the monkey hippocampus after transient ischemia. Biochem Biophys Res Commun 1996, 228:616-622
33. Seyfried D, Han Y, Zheng Z, Day N, Moin K, Rempel S, Sloane B, Chopp M: Cathepsin B and middle cerebral artery occlusion in the rat. J Neurosurg 1997, 87:716-723
34. Chen JW, Murphy TL, Willingham MC, Pastan I, August JT: Identification of two lysosomal membrane glycoproteins. J Cell Biol 1985, 101:85-95
35. Yamashima T, Tonchev AB, Tsukada T, Saido TC, Imajoh-Ohmi S, Momoi T, Kominami E: Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus 2003, 13:791-800
36. Puyal J, Vaslin A, Mottier V, Clarke PGH: Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 2009, doi: 10.1002/ana.21714
37. Carloni S, Buonocore G, Balduini W: Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 2008, 32:329-339
38. Rami A, Langhagen A, Steiger S: Focal cerebral ischemia induces up-regulation of Beclin 1 and autophagy-like cell death. Neurobiol Dis 2008, 29:132-141
39. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G: Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007, 8:741-752
40. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU: Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006, 8:1124-1132
41. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B: Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939
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. Canu N, Tufi R, Serafino AL, Amadoro G, Ciotti MT, Calissano P: Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J Neurochem 2005, 92:1228-1242
44. Nakajima W, Ishida A, Lange MS, Gabrielson KL, Wilson MA, Martin LJ, Blue ME, Johnston MV: Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci 2000, 20:7994-8004
45. Sheldon RA, Hall JJ, Noble LJ, Ferriero DM: Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neurosci Lett 2001, 304:165-168
46. Blomgren K, Zhu C, Wang X, Karlsson JO, Leverin AL, Bahr BA, Mallard C, Hagberg H: Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis?" J Biol Chem 2001, 276:10191-10198
47. Vannucci RC, Towfighi J, Vannucci SJ: Secondary energy failure after cerebral hypoxia-ischemia in the immature rat. J Cereb Blood Flow Metab 2004, 24:1090-1097
48. Lorek A, Takei Y, Cady EB, Wyatt JS, Penrice J, Edwards AD, Peebles D, Wylezinska M, Owen-Reece H, Kirkbride V, Cooper CE, Aldridge RF, Roth SC, Brown G, Delpy DT, Reynolds EOR: Delayed ("secondary") cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatr Res 1994, 36:699-706
49. Tolkovsky AM, Xue L, Fletcher GC, Borutaite V: Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease? Biochimie 2002, 84:233-240
50. Kawamura M, Nakajima W, Ishida A, Ohmura A, Miura S, Takada G: Calpain inhibitor MDL 28170 protects hypoxic-ischemic brain injury in neonatal rats by inhibition of both apoptosis and necrosis. Brain Res 2005, 1037:59-69
51. Cheng Y, Deshmukh M, D'Costa A, Demaro JA, Gidday JM, Shah A, Sun Y, Jacquin MF, Johnson EM, Holtzman DM: Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury. J Clin Invest 1998, 101:1992-1999
52. Adachi M, Sohma O, Tsuneishi S, Takada S, Nakamura H: Combination effect of systemic hypothermia and caspase inhibitor administration against hypoxic-ischemic brain damage in neonatal rats. Pediatr Res 2001, 50:590-595
53. Han BH, Xu D, Choi J, Han Y, Xanthoudakis S, Roy S, Tam J, Vaillancourt J, Colucci J, Siman R, Giroux A, Robertson GS, Zamboni R, Nicholson DW, Holtzman DM: Selective, reversible caspase-3 inhibitor is neuroprotective and reveals distinct pathways of cell death after neonatal hypoxic-ischemic brain injury. J Biol Chem 2002, 277:30128-30136
54. Gozal E, Gozal D, Pierce WM, Thongboonkerd V, Scherzer JA, Sachleben LR Jr, Brittian KR, Guo SZ, Cai J, Klein JB: Proteomic analysis of CA1 and CA3 regions of rat hippocampus and differential susceptibility to intermittent hypoxia. J Neurochem 2002, 83:331-345
55. Lein ES, Zhao X, Gage FH: Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci 24:3879-3889
56. Greene JG, Borges K, Dingledine R: Quantitative transcriptional neuroanatomy of the rat hippocampus: evidence for wide-ranging, pathway-specific heterogeneity among three principal cell layers. Hippocampus 2009, 19:253-264
57. Jackson TC, Rani A, Kumar A, Foster TC: Regional hippocampal differences in AKT survival signaling across the lifespan: implications for CA1 vulnerability with aging. Cell Death Differ 2009, 16:439-448
58. Grishin AA, Gee CE, Gerber U, Benquet PJ: Differential calcium-dependent modulation of NMDA currents in CA1 and CA3 hippocampal pyramidal cells. Neurosci 2004, 24:350-355
59. Gee CE, Benquet P, Raineteau O, Rietschin L, Kirbach SW, Gerber U: NMDA receptors and the differential ischemic vulnerability of hippocampal neurons. Eur J Neurosci 2006, 23:2595-2603
60. Cronberg T, Jensen K, Rytter A, Wieloch T: Selective sparing of hippocampal CA3 cells following in vitro ischemia is due to selective inhibition by acidosis. Eur J Neurosci 2005, 22:310-316
61. Mattiasson G, Friberg H, Hansson M, Elmér E, Wieloch T: Flow cytometric analysis of mitochondria from CA1 and CA3 regions of rat hippocampus reveals differences in permeability transition pore activation. J Neurochem 2003, 87:532-544