Biphasic changes in the levels of poly(ADP-ribose) polymerase-1 and caspase 3 in the immature brain following hypoxia-ischemia

International Journal of Developmental Neuroscience

Volumn 23, Issue 8, 2005, Pages 673-686

  Martin, Shannon S ^a   Perez Polo, J Regino ^a   Noppens, Kristin M ^b   Grafe, Marjorie R ^a,b,c  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Brain; Cell death; Hypoxia; Ischemia; Neonatal; PARP 1; Rat

Indexed keywords

CASPASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BRAIN CORTEX; BRAIN INJURY; BRAIN ISCHEMIA; CAROTID ARTERY LIGATION; CELL DEATH; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; HIPPOCAMPUS; HISTOLOGY; HYPOXIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MORPHOLOGY; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; STAINING; SURVIVAL TIME; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CASPASE 3; CASPASES; CEREBRAL CORTEX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPOXIA-ISCHEMIA, BRAIN; IMMUNOHISTOCHEMISTRY; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; RATS; TIME FACTORS;

ANIMALIA;

EID: 27944496069     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2005.08.002     Document Type: Article

References (89)

1. B.C. Albensi, M.P. Schweizer, T.M. Rarick, and F. Filloux Unilateral hypoxic-ischemic injury in the neonatal rat brain evaluated by in vivo MRI: correlation with histopathology and neuroprotection by MK-801 Invest. Radiol. 34 1999 249 261
2. S. Ashwal, P.S. Dale, and L.D. Longo Regional cerebral blood flow: studies in the fetal lamb during hypoxia, hypercapnia, acidosis, and hypotension Pediatric Res. 18 1984 1309 1316
3. P. Baldi Bioinformatics 2 ed. 2001 The MIT Press Cambridge
4. E.J. Beilharz, C.E. Williams, M. Dragunow, E.S. Sirimanne, and P.D. Gluckman Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss Brain Res. Mol. Brain Res. 29 1995 1 14
5. N.A. Berger Poly(ADP-ribose) in the cellular response to DNA damage Radiat. Res. 101 1985 4 15
6. K. Blomgren, C. Zhu, X. Wang, J.O. Karlsson, A.L. Leverin, B.A. Bahr, C. Mallard, and H. Hagberg Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"? J. Biol. Chem. 276 2001 10191 10198
7. R.M. Blumberg, E.B. Cady, J.S. Wigglesworth, J.E. McKenzie, and A.D. Edwards Relation between delayed impairment of cerebral energy metabolism and infarction following transient focal hypoxia-ischaemia in the developing brain Exp. Brain Res. 113 1997 130 137
8. C. Bossenmeyer-Pourie, V. Koziel, and J.L. Daval CPP32/caspase-3-like proteases in hypoxia-induced apoptosis in developing brain neurons Brain Res. Mol. Brain Res. 71 1999 225 237
9. S. Bursztajn, J.J. Feng, S.A. Berman, and A. Nanda Poly(ADP-ribose) polymerase induction is an early signal of apoptosis in human neuroblastoma Mol. Brain Res. 76 2000 363 376
10. C. Cande, F. Cecconi, P. Dessen, and G. Kroemer Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J. Cell Sci. 115 2004 4727 4734
11. M. Cavazzuti, and T.E. Duffy Regulation of local cerebral blood flow in normal and hypoxic newborn dogs Ann. Neurol. 11 1982 247 257
12. R.S.B. Clark, M. Chen, P.M. Kochanek, S.C. Watkins, K.L. Jin, R. Draviam, P.D. Nathaniel, R. Pinto, D.W. Marion, and S.H. Graham Detection of single- and double-strand DNA breaks after traumatic brain injury in rats: comparison of in situ labeling techniques using DNA polymerase I, the Klenow fragment of DNA polymerase I, and terminal deoxynucleotidyl transferase J. Neurotrauma 18 2001 675 689
13. C. Cosi, and M. Marien Implication of poly(ADP-ribose) polymerase (PARP) in neurodegeneration and brain energy metabolism. Decreases in mouse brain NAD+ and ATP caused by MPTP are prevented by the PARP inhibitor benzamide Ann. N.Y. Acad. Sci. 890 1999 227 239
14. C. de Torres, F. Munell, I. Ferrer, J. Reventos, and A. Macaya Identification of necrotic cell death by the TUNEL assay in the hypoxic-ischemic neonatal rat brain Neurosci. Lett. 230 1997 1 4
15. J. Dobbing, and J. Sands Comparative aspects of the brain growth spurt Early Hum. Dev. 3 1979 79 83
16. S. Ducrocq, N. Benjelloun, M. Plotkine, Y. Ben Ari, and C. Charriaut-Marlangue Poly(ADP-ribose) synthase inhibition reduces ischemic injury and inflammation in neonatal rat brain J. Neurochem. 74 2000 2504 2511
17. B.E. Dwyer, R.N. Nishimura, and D.G. Fujikawa Cerebral hypoxia-ischemia in immature rats: methodological considerations Exp. Neurol. 99 1988 772 777
18. S.E. Dyson, and D.G. Jones Some effects of undernutrition on synaptic development-a quantitative ultrastructural study Brain Res. 114 1976 365 378
19. M. Endres, Z.Q. Wang, S. Namura, C. Waeber, and M.A. Moskowitz Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase J. Cereb. Blood Flow Metab. 17 1997 1143 1151
20. I. Ferrer, A. Tortosa, A. Macaya, A. Sierra, D. Moreno, F. Munell, R. Blanco, and W. Squier Evidence of nuclear DNA fragmentation following hypoxia-ischemia in the infant rat brain, and transient forebrain ischemia in the adult gerbil Brain Pathol. 4 1994 115 122
21. R.M. Gardiner Cerebral blood flow and oxidative metabolism during hypoxia and asphyxia in the new-born calf and lamb J. Physiol. 305 1980 357 376
22. R. Gill, M. Soriano, K. Blomgren, H. Hagberg, R. Wybrecht, M.T. Miss, S. Hoefer, G. Adam, O. Niederhauser, J.A. Kemp, and H. Loetscher Role of caspase-3 activation in cerebral ischemia-induced neurodegeneration in adult and neonatal brain J. Cereb. Blood Flow Metab. 22 2002 420 430
23. E. Gilland, E. Bona, and H. Hagberg Temporal changes of regional glucose use, blood flow, and microtubule-associated protein 2 immunostaining after hypoxia-ischemia in the immature rat brain J. Cereb. Blood Flow Metab. 18 1998 222 228
24. E. Gilland, M. Puka-Sundvall, L. Hillered, and H. Hagberg Mitochondrial function and energy metabolism after hypoxia-ischemia in the immature rat brain: involvement of NMDA-receptors J. Cereb. Blood Flow Metab. 18 1998 297 304
25. M.R. Grafe Developmental changes in the sensitivity of the neonatal rat brain to hypoxic/ischemic injury Brain Res. 653 1994 161 166
26. H.C. Ha, and S.H. Snyder Poly(ADP-ribose) polymerase-1 in the nervous system Neurobiol. Dis. 7 2000 225 239
27. H. Hagberg, E. Gilland, E. Bona, L.A. Hanson, M. Hahin-Zoric, M. Blennow, M. Holst, A. McRae, and O. Soder Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia-ischemia in neonatal rats Pediatric Res. 40 1996 603 609
28. H. Hagberg, M.A. Wilson, H. Matsushita, C. Zhu, M. Lange, M. Gustavsson, M.F. Poitras, T.M. Dawson, V.L. Dawson, F.J. Northington, and M.V. Johnston PARP-1 gene disruption preferentially protects males from perinatal brain injury J. Neurochem. 90 2004 1068 1075
29. Z. Herceg, and Z.Q. Wang Failure of poly(ADP-ribose) polymerase cleavage by caspases leads to induction of necrosis and enhanced apoptosis Mol. Cell. Biol. 19 1999 5124 5133
30. I.E. Hill, J.P. MacManus, I. Rasquinha, and U.I. Tuor DNA fragmentation indicative of apoptosis following unilateral cerebral hypoxia-ischemia in the neonatal rat Brain Res. 676 1995 398 403
31. P.L. Hope, A.M. Costello, E.B. Cady, D.T. Delpy, P.S. Tofts, A. Chu, P.A. Hamilton, E.O. Reynolds, and D.R. Wilkie Cerebral energy metabolism studied with phosphorus NMR spectroscopy in normal and birth-asphyxiated infants Lancet 2 1984 366 370
32. J.A. Ivacko, R. Sun, and F.S. Silverstein Hypoxic-ischemic brain injury induces an acute microglial reaction in perinatal rats Pediatric Res. 39 1996 39 47
33. U.C. Joashi, K. Greenwood, D.L. Taylor, M. Kozma, N.D. Mazarakis, A.D. Edwards, and H. Mehmet Poly(ADP ribose) polymerase cleavage precedes neuronal death in the hippocampus and cerebellum following injury to the developing rat forebrain Eur. J. Neurosci. 11 1999 91 100
34. L.-M. Joly, N. Benjelloun, M. Plotkine, and C. Charriaut-Marlangue Distribution of poly(ADP-ribosyl)ation and cell death after cerebral ischemia in the neonatal rat Pediatric Res. 53 2003 776 782
35. S.H. Kaufmann, S. Desnoyers, Y. Ottaviano, N.E. Davidson, and G.G. Poirier Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis Cancer Res. 53 1993 3976 3985
36. M.C. LaPlaca, J. Zhang, R. Raghupathi, J.H. Li, F. Smith, F.M. Bareyre, S.H. Snyder, D.I. Graham, and T.K. McIntosh Pharmacologic inhibition of poly(ADP-ribose) polymerase is neuroprotective following traumatic brain injury in rats J. Neurotrauma 18 2001 369 376
37. Y.A. Lazebnik, S.H. Kaufmann, S. Desnoyers, G.G. Poirier, and W.C. Earnshaw Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE Nature 371 1994 346 347
38. Y. Le Rhun, J.B. Kirkland, and G.M. Shah Cellular responses to DNA damage in the absence of poly(ADP-ribose) polymerase Biochem. Biophys. Res. Commun. 245 1998 1 10
39. P. Lipton Ischemic cell death in brain neurons Physiol. Rev. 79 1999 1431 1568
40. E.H. Lo, P. Bosque-Hamilton, and W. Meng Inhibition of poly(ADP-ribose) polymerase: reduction of ischemic injury and attenuation of N-methyl-d- aspartate-induced neurotransmitter dysregulation Stroke 29 1998 830 836
41. B. Lubec, A.V. Kozlov, K. Krapfenbauer, A. Berger, H. Hoeger, M. Herrera-Marschitz, H. Nohl, T. Koeck, and G. Lubec Nitric oxide and nitric oxide synthase in the early phase of perinatal asphyxia of the rat Neuroscience 93 1999 1017 1023
42. L.J. Martin, A.M. Brambrink, A.C. Price, A. Kaiser, D.M. Agnew, R.N. Ichord, and R.J. Traystman Neuronal death in newborn striatum after hypoxia-ischemia is necrosis and evolves with oxidative stress Neurobiol. Dis. 7 2000 169 191
43. A. Martin-Ancel, A. Garcia-Alix, D. Pascual-Salcedo, F. Cabanas, M. Valcarce, and J. Quero Interleukin-6 in the cerebrospinal fluid after perinatal asphyxia is related to early and late neurological manifestations Pediatrics 100 1997 789 794
44. L.D. McCullough, Z. Zeng, K.K. Blizzard, I. Debchoudhury, and P.D. Hurn Ischemic nitric oxide and poly(ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection J. Cereb. Blood Flow Metab. 25 2005 502 515
45. S.Z. Meng, M. Itoh, T. Obonai, and S. Takashima Roles of glutamate transporter and receptors, poly(ADP-ribose) polymerase, and transforming growth factor-beta 1 in pontosubicular neuron necrosis J. Child Neurol. 15 2000 362 369
46. K. Muramatsu, R.A. Sheldon, S.M. Black, M. Tauber, and D.M. Ferriero Nitric oxide synthase activity and inhibition after neonatal hypoxia ischemia in the mouse brain Brain Res. Dev. Brain Res. 123 2000 119 127
47. W. Nakajima, A. Ishida, M.S. Lange, K.L. Gabrielson, M.A. Wilson, L.J. Martin, M.E. Blue, and M.V. Johnston Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat J. Neurosci. 20 2000 7994 8004
48. J. Nedelcu, M.A. Klein, A. Aguzzi, P. Boesiger, and E. Martin Biphasic edema after hypoxic-ischemic brain injury in neonatal rats reflects early neuronal and late glial damage Pediatric Res. 46 1999 297 304
49. C. Nelson, and F.S. Silverstein Acute disruption of cytochrome oxidase activity in brain in a perinatal rat stroke model Pediatric Res. 36 1994 12 19
50. K.B. Nelson, J.M. Dambrosia, J.K. Grether, and T.M. Phillips Neonatal cytokines and coagulation factors in children with cerebral palsy Ann. Neurol. 44 1998 665 675
51. D.W. Nicholson, A. Ali, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labelle, and Y.A. Lazebnik Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis Nature 376 1995 37 43
52. F.J. Northington, D.M. Ferriero, E.M. Graham, R.J. Traystman, and L.J. Martin Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis Neurobiol. Dis. 8 2001 207 219
53. E. Oakden, M. Chiswick, N. Rothwell, and S. Loddick The influence of litter size on brain damage caused by hypoxic-ischemic injury in the neonatal rat Pediatric Res. 52 2002 692 696
54. F.J. Oliver, G. de la Rubia, V. Rolli, M.C. Ruiz-Ruiz, G. de Murcia, and J.M. Murcia Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant J. Biol. Chem. 273 1998 33533 33539
55. C. Palmer, R.M. Brucklacher, M.A. Christensen, and R.C. Vannucci Carbohydrate and energy metabolism during the evolution of hypoxic-ischemic brain damage in the immature rat J. Cereb. Blood Flow Metab. 10 1990 227 235
56. C. Portera-Cailliau, D.L. Price, and L.J. Martin Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum J. Comp. Neurol. 378 1997 70 87
57. M. Puka-Sundvall, B. Gajkowska, M. Cholewinski, K. Blomgren, J.W. Lazarewicz, and H. Hagberg Subcellular distribution of calcium and ultrastructural changes after cerebral hypoxia-ischemia in immature rats Brain Res. Dev. Brain Res. 125 2000 31 41
58. M. Puka-Sundvall, C. Wallin, E. Gilland, U. Hallin, X. Wang, M. Sandberg, J. Karlsson, K. Blomgren, and H. Hagberg Impairment of mitochondrial respiration after cerebral hypoxia-ischemia in immature rats: relationship to activation of caspase-3 and neuronal injury Brain Res. Dev. Brain Res. 125 2000 43 50
59. M. Puka-Sundvall, E. Gilland, and H. Hagberg Cerebral hypoxia-ischemia in immature rats: involvement of mitochondrial permeability transition? Dev. Neurosci. 23 2001 192 197
60. M.R. Pulera, L.M. Adams, H. Liu, D.G. Santos, R.N. Nishimura, F. Yang, G.M. Cole, and C.G. Wasterlain Apoptosis in a neonatal rat model of cerebral hypoxia-ischemia Stroke 29 1998 2622 2630
61. J.E. Rice III, R.C. Vannucci, and J.B. Brierley The influence of immaturity on hypoxic-ischemic brain damage in the rat Ann. Neurol. 9 1981 131 141
62. M. Ringel, R.M. Bryan, and R.C. Vannucci Regional cerebral blood flow during hypoxia-ischemia in the immature rat: comparison of iodoantipyrine and iodoamphetamine as radioactive tracers Brain Res. Dev. Brain Res. 59 1991 231 235
63. T. Roohey, T.N.K. Raju, and A.N. Moustogiannis Animal models for the study of perinatal hypoxic-ischemic encephalopathy: a critical analysis Early Hum. Dev. 47 1997 115 146
64. F.R. Sallmann, M.D. Vodenicharov, Z.Q. Wang, and G.G. Poirier Characterization of sPARP-1. An alternative product of PARP-1 gene with poly(ADP-ribose) polymerase activity independent of DNA strand breaks J. Biol. Chem. 275 2000 15504 15511
65. R.S. Sidhu, U.I. Tuor, and M.R. Del Bigio Nuclear condensation and fragmentation following cerebral hypoxia-ischemia occurs more frequently in immature than older rats Neurosci. Lett. 223 1997 129 132
66. F. Silverstein, K. Buchanan, and M.V. Johnston Pathogenesis of hypoxic-ischemic brain injury in a perinatal rodent model Neurosci. Lett. 49 1984 271 277
67. F. Silverstein, B. Naik, and J. Simpson Hypoxia-ischemia stimulates hippocampal glutamate efflux in perinatal rat brain: an in vivo microdialysis study Pediatric Res. 30 1991 587 590
68. S. Smith, I. Giriat, A. Schmitt, and T. de Lange Tankyrase, a poly(ADP-ribose) polymerase at human telomeres Science 282 1998 1484 1487
69. S. Susin, H. Lorenzo, N. Zamzami, I. Marzo, B. Snow, G. Brothers, J. Mangion, E. Jacotot, P. Costantini, M. Loeffler, N. Larochette, D. Goodlett, R. Aebersold, D. Siderovski, J. Penninger, and G. Kroemer Molecular characterization of mitochondrial apoptosis-inducing factor Nature 397 1999 441 446
70. J. Szaflarski, D. Burtrum, and F.S. Silverstein Cerebral hypoxia-ischemia stimulates cytokine gene expression in perinatal rats Stroke 26 1995 1093 1100
71. K. Takahashi, A.A. Pieper, S.E. Croul, J. Zhang, S.H. Snyder, and J.H. Greenberg Post-treatment with an inhibitor of poly(ADP-ribose) polymerase attenuates cerebral damage in focal ischemia Brain Res. 829 1999 46 54
72. A. Tateishi, J. Fleischer, J. Drummond, M. Scheller, M. Zornow, M. Grafe, and H. Shapiro Nimodipine does not improve neurologic outcome after 14 min of cardiac arrest in cats Stroke 20 1989 1044 1050
73. M. Tewari, L.T. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D.R. Beidler, G.G. Poirier, G.S. Salvesen, and V.M. Dixit Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase Cell 81 1995 801 809
74. T. Tokime, K. Nozaki, T. Sugino, H. Kikuchi, N. Hashimoto, and K. Ueda Enhanced poly(ADP-ribosyl)ation after focal ischemia in rat brain J. Cereb. Blood Flow Metab. 18 1998 991 997
75. T. Toliver-Kinsky, J. Papaconstantinou, and J.R. Perez-Polo Age-associated alterations in hippocampal and basal forebrain nuclear factor kappa B activity J. Neurosci. Res. 48 1997 580 587
76. J. Towfighi, N. Zec, J. Yager, C. Housman, and R.C. Vannucci Temporal evolution of neuropathologic changes in an immature rat model of cerebral hypoxia: a light microscopic study Acta Neuropathol. 90 1995 375 386
77. J. Towfighi, D. Mauger, R.C. Vannucci, and S. Vannucci Influence of age on the cerebral lesions in an immature rat model of cerebral hypoxia-ischemia: a light microscopic study Dev. Brain Res. 100 1997 149 160
78. U.I. Tuor, K.L. Malisza, and P. Kozlowski Prevention of both T2 and diffusion-weighted increases in image intensity during cerebral hypoxia-ischemia in infant rats pretreated with dexamethasone Exp. Brain Res. 125 1999 217 220
79. R.C. Vannucci, R.M. Brucklacher, and S.J. Vannucci CSF glutamate during hypoxia-ischemia in the immature rat Brain Res. Dev. Brain Res. 118 1999 147 151
80. R.C. Vannucci, D.T. Lyons, and F. Vasta Regional cerebral blood flow during hypoxia-ischemia in immature rats Stroke 19 1988 245 250
81. R.C. Vannucci, and D.J. Mujsce Effect of glucose on perinatal hypoxic-ischemic brain damage Biol. Neonate 62 1992 215 224
82. R.C. Vannucci, and J.Y. Yager Glucose, lactic acid, and perinatal hypoxic-ischemic brain damage Pediatric Neurol. 8 1992 3 12
83. B.P. Wagner, J. Nedelcu, and E. Martin Delayed postischemic hypothermia improves long-term behavioral outcome after cerebral hypoxia-ischemia in neonatal rats Pediatric Res. 51 2002 354 360
84. X. Wang, J.O. Karlsson, C. Zhu, B.A. Bahr, H. Hagberg, and K. Blomgren Caspase-3 activation after neonatal rat cerebral hypoxia-ischemia Biol. Neonate 79 2001 172 179
85. F.A. Welsh, R.C. Vannucci, and J.B. Brierley Columnar alterations of NADH fluorescence during hypoxia-ischemia in immature rat brain J. Cereb. Blood Flow Metab. 2 1982 221 228
86. J.Y. Yager, R.M. Brucklacher, and R.C. Vannucci Cerebral energy metabolism during hypoxia-ischemia and early recovery in immature rats Am. J. Physiol. 262 1992 H672 H677
87. S. Yu, H. Wang, M.F. Poitras, C. Coombs, W.J. Bowers, H.J. Federoff, G.G. Poirier, T.M. Dawson, and V.L. Dawson Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor Science 297 2002 259 263
88. J. Zhang, A. Pieper, and S.H. Snyder Poly(ADP-ribose) synthetase activation: an early indicator of neurotoxic DNA damage J. Neurochem. 65 1995 1411 1414
89. C. Zhu, X. Wang, H. Hagberg, and K. Blomgren Correlation between caspase-3 activation and three different markers of DNA damage in neonatal cerebral hypoxia-ischemia J. Neurochem. 75 2000 819 829