Apoptosis and necrosis in the newborn piglet brain following transient cerebral hypoxia-ischaemia

Neuropathology and Applied Neurobiology

Volumn 23, Issue 1, 1997, Pages 16-25

  Yue, X ^a   Mehmet, H ^a,e   Penrice, J ^b   Cooper, C ^b   Cady, E ^c   Wyatt, J S ^b   Reynolds, E O R ^b   Edwards, A D ^a   Squier, M V ^d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^d RADCLIFFE INFIRMARY   (United Kingdom)

^e HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Apoptosis; Cell death; Developing brain; Hypoxia ischaemia; Necrosis; Neonate

Indexed keywords

EOSIN; HEMATOXYLIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN NECROSIS; CELL TYPE; CEREBELLUM; CEREBELLUM CORTEX; CINGULATE GYRUS; CONTROLLED STUDY; DENTATE GYRUS; DISEASE SEVERITY; GLIA CELL; HIPPOCAMPUS; NERVE CELL; NERVE CELL DIFFERENTIATION; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SWINE; WHITE MATTER;

EID: 0031044097     PISSN: 03051846     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2990.1997.tb01181.x     Document Type: Article

References (46)

1. Abrams JM, White K, Fessler LI, Steller H. Programmed cell death during Drosophila embryogenesis. Development 1993; 117: 29-43
2. Altman J, Bayer SA. Prenatal development of the cerebellar system in the rat. 1. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. J Comp Neurol 1978; 179: 23-48
3. Ansari B, Coates PJ, Greenstein BD, Hall PA. In situ end-labelling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol 1993; 170: 1-8
4. Arends MJ, Morris RG, Wyllie AH. Apoptosis. The role of the endonuclease. Am J Pathol 1990; 136: 593-608
5. Azzopardi D, Wyatt JS, Cady EB et al. Prognosis of newborn infants with hypoxic-ischemic brain injury assessed by phosphorus magnetic resonance spectroscopy. Pediatr Res 1989; 25: 445-51
6. Bonfoco E, Kraine D, Ankarcrona M, Nicotera P, Lipton SA. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 1995; 92: 7162-6
7. Charriaut-Marlangue C, Margaill I, Represa A et al. Apoptosis and necrosis alter reversible focal ischemia: an in situ DNA fragmentation analysis. J Cereb Blood Flow Metab 1996; 16: 186-94
8. Clarke PG. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol Berl 1990; 181: 195-213
9. Collins RJ, Harmon BV, Gobe GC, Kerr JF. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int J Radiat Biol 1992; 61: 451-3
10. Crain BJ, Westerkam WD, Harrison AH, Nadler JV. Selective neuronal death after transient global brain ischaemia in the Mongolian gerbil: a silver impregnation study. Neuroscience 1988; 27: 387-402
11. Del-Bigio MR, Becker LE. Microglial aggregation in the dentate gyrus: a marker of mild hypoxic-ischaemic brain insult in human infants. Neuropathol Appl Neurobiol 1994; 20: 144-51
12. Duchen LW. General pathology of neurons and neuroglia. In: Greenfield's Neuropathology. part II. Eds JH Adams, LW Duchen. London: Edward Arnold, 1992
13. Farber JL. Biology of disease: membrane injury and calcium homeostasis in the pathogenesis of coagulative necrosis. Lab Invest 1982; 47: 114-23
14. Ferrer I, Tortosa A, Macaya A et al. Evidence of nuclear DNA fragmentation following hypoxia-ischemia in the infant rat brain, and transient forebrain ischemia in the adult gerbil. Brain Pathol 1994; 4: 115-22
15. Friede RL. Topographic Brain Chemistry. New York: Academic Press, 1966
16. Fukada K, Kojiro M, Chiu J-F. Demonstration of extensive chromatin cleavage in transplanted Morris hepatoma 7777 tissue: apoptosis or necrosis? Am J Pathol 1993; 142: 935-46
17. Garcia JH, Liu KF, Ho KL. Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke 1995; 26: 636-42
18. Garcia JH, Lossinsky AS, Kauffman FC, Conger KA. Neuronal ischemic injury: light microscopy, ultrastructure and biochemistry. Acta Neuropathol Berl 1978; 43: 85-95
19. Gavrieli Y, Sherman Y, Ben-Sasson A. Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J Cell Biol 1992; 119: 493-501
20. Gold R, Schmied M, Rothe G et al. Detection of DNA fragmentation in apoptosis: application of in situ nick translation to cell culture systems and tissue sections. J Histochem Cytochem 1993; 41: 1023-40
21. Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 1995; 21: 1465-8
22. Hill A. Current concepts of hypoxic-ischemic cerebral injury on the term newborn. Pediatr Neurol 1991; 7: 317-25
23. Hockenbery D. Defining apoptosis. Am J Pathol 1995; 146: 16-9
24. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-57
25. Kirino T, Sano K. Selective vulnerability in the gerbil hippocampus following transient ischaemia. Acta Neuropathol Berl 1984; 62: 201-8
26. Larroche JC. Massive cerebral necrosis in newborn infants. Us relation to maturation, its clinical and bioelectric symptoms. Biol Neonat 1968; 13: 340-60
27. Li Y, Chopp M, Jiang N, Zhang ZG, Zaloga C. Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am J Pathol 1995; 146: 1045-51
28. Liu HM, Chen HH. c-Fos protein expression and ischemic changes in neurons vulnerable to ischaemia/hypoxia. correlated with basic fibroblast growth factor immunoreactivity. J Neuropathol Exp Neurol 1994; 53: 598-605
29. Lorek A, Takei Y, Cady EB et al. Delayed ('secondary') cerebral energy failure after acute hypoxia-ischaemia in the newborn piglet: continuous 48-hours studies by phosphorus magnetic resonance spectroscopy. Pediatr Res 1994; 36: 699-706
30. MacLean PP. Comments on the selective vulnerability of the hippocampus. In: Selective Vulnerability of the Brain in Hypoxemia. Eds JP Schade, WH MeMenemey. Philadelphia: FA Davis, 1963: 177-256
31. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995; 146: 3-15
32. Mehmet H, Yue X, Squier MV et al. Increased apoptosis in the cingulate sulcus of newborn piglets following transient hypoxia-ischaemia is related to the degree of high energy phosphate depletion during the insult. Neurosci Lett 1994; 181: 121-5
33. Ment LR, Duncan CC, Ehrenkranz RA. Perinatal cerebral infarction. Semin Perinatal 1987; 11: 142-54
34. Oppenheim RW. Cell death during development of the nervous system. Annu Rev Neurosci 1991; 14: 453-501
35. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. Programmed cell death and the control of cell survival: lessons from the nervous system. Science 1993; 262: 695-700
36. Rakic P, Sidman RL. Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans. J Comp Neurol 1970; 139: 473-500
37. Ross ME. Cell division and the nervous system: regulating the cell cycle from neural differentiation to death. Trends Neurol Sci 1996; 19: 62-8
38. Roth SC, Edwards AD, Cady EB et al. Relation between cerebral oxidative metabolism following birth asphyxia and neurodevelopmental outcome and brain growth at one year. Dev Med Child Neurol 1992; 34: 285-95
39. Sarnat HB. Topics in Neonatal Neurology. New York: Grune and Stratton, 1984
40. Schwartz PH, Massarweh WF, Vinters HV, Wasterlain CG. A rat model of severe neonatal hypoxic-ischemic brain injury. Stroke 1992; 23: 539-46
41. Volpe JJ. Neurology oj the Newborn. 3rd edn. Philadelphia: WB Saunders Company, 1995
42. Wasterlain CG, Hattori H, Yang C et al. Selective vulnerability of neuronal subpopulations during ontogeny reflects discrete molecular events associated with normal brain development. In: Neonatal Seizures. Eds CG Wasterlain, P Vert. New York: Raven Press. 1990: 69-81
43. Wijsman JH, Jonker RR, Keijzer CJ, van de Velde CJ, Cornelisse CJ, van Dierendock JH. A new method to detect apoptosis in paraffin sections: in situ end-labelling of fragmented DNA. J Histochem Cytochem 1993; 41: 7-12
44. Wyatt JS, Edwards AD, Azzopardi D, Reynolds EOR. Magnetic resonance and near infrared spectroscopy for investigation of perinatal hypoxic-ischaemic brain injury. Arch Dis Child 1989; 64: 953-63
45. Wyllie AH, Duvall E. Cell injury and death. In: Oxford Textbook of Pathology. Eds JO'D Mcgee, PG Isaacson, NA Wright. Oxford: Oxford University Press, 1992: 141-93
46. Zakeri ZF, Quaglino D, Latham T, Lockshin A. Delayed internucleosomal DNA fragmentation in programmed cell death. FASEB J 1993; 7: 470-8