Apoptosis of retrogradely degenerating neurons occurs in association with the accumulation of perikaryal mitochondria and oxidative damage to the nucleus

American Journal of Pathology

Volumn 153, Issue 2, 1998, Pages 447-456

  Al Abdulla, Nael A ^a   Martin, Lee J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C;

APOPTOSIS; ARTICLE; BRAIN MITOCHONDRION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN CELL; MALE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NERVE FIBER TRANSPORT; NONHUMAN; OXIDATIVE STRESS; PERIKARYON; PRIORITY JOURNAL; RAT;

EID: 0031856524     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)65588-5     Document Type: Article

References (45)

1. Ratan RR, Murphy TH, Baraban JM: Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 1994, 62:376-379
2. Wood KA, Youle RJ: The role of tree radicals and p53 in neuron apoptosis in vivo. J Neurosci 1995, 15:5851-5857
3. Newmeyer DD, Farschon DM, Reed JC: Cell-free apoptosis in Xenopus egg extracts: inhibition by bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 1994, 79:353-364
4. Skulachev VP: Why are mitochondria involved in apoptosis? FEBS Lett 1996, 397:7-10
5. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G: Mitochondrial control of nuclear apoptosis. J Exp Med 1996, 183:1533-1544
6. Kroemer G, Petit P, Zamzami N, Vayssiere JL, Mignotte B: The biochemistry of programmed cell death. FASEB J 1995, 9:1277-1287
7. Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT, Thompson CB: Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 1997, 91:627-637
8. Hockenberry DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ: Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993, 75:241-251
9. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X: Prevention of apoptosis by bcl-2: release of cytochrome c from mitochondria blocked. Science 1997, 275:1129-1132
10. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD: The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997, 275:1132-1136
11. Liu X, Kim CN, Yang J, Jemmerson R, Wang X: Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome C. Cell 1996, 86:147-157
12. Al-Abdulla NA, Portera-Cailliau C, Martin LJ: Occipital cortex ablation in adult rat causes retrograde neuronal death in the lateral geniculate nucleus that resembles apoptosis. Neuroscience 1998, 86:191-209
13. Kerr JFR, Gobé GC, Winterford CM, Harmon BV: Anatomical methods in cell death. Cell Death. Edited by LM Schwartz, BA Osborne. New York, Academic Press, 1995, pp 1-27
14. Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C: Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull 1998, 46:281-309
15. 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
16. Kasai H, Nishimura S: Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res 1984, 12:2137-2145
17. Devasagayam TPA, Steenken S, Obendorf MSW, Schultz WA, Sies H: Formation of 8-hydroxy(deoxy)-guanosine and generation of strand breaks at guanine residues in DNA by singlet oxygen. Biochemistry 1991, 30:6283-6289
18. lnoue S, Kawanishi S: Oxidative DNA damage induced by simultaneous generation of nitric oxide, and superoxide. FEBS Lett 1995, 371:86-88
19. Wong-Riley MTT: Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histocnemistry. Brain Res 1979, 171:11-28
20. Martin LJ, Brambrink A, Koehler RC, Traystman RJ: Primary sensory and forebrain motor systems in the newborn brain are preferentially damaged by hypoxia-ischemia. J Comp Neurol 1997, 377:262-285
21. Lieberman AR: The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol 1971, 14:49-124
22. Lin K-T, Xue J-Y, Nomen M, Spur B, Wong PYK: Peroxynitrite-induced apoptosis in HL60 cells. J Biol Chem 1995, 270:16487-16490
23. Verhaegen S, McGowan AJ, Brophy AR, Fernandes RS, Cotter TG: Inhibition of apoptosis by antioxidants in the human HL-60 leukemia cell line. Biochem Pharmacol 1995, 50:1021-1029
24. Ratan RR, Murphy TH, Baraban JM: Macromolecular synthesis inhibitors prevent oxidative stress-induced apoptosis in embryonic cortical neurons by shunting cysteine from protein synthesis to glutathione. J Neurosci 1994, 14:4385-4392
25. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA: Apoptosis and necrosis: two distinct events induced respectively by mild and intense insults with NMDA or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 1995, 92:72162-72166
26. Mirabelli F, Salis A, Marinoni V, Finardi G, Bellomo G, Thor H, Orrenius S: Menadione-induced bleb formation in hepatocytes is associated with the oxidation of thiol groups in actin. Arch Biochem Biophys 1988, 264:261-269
27. Mirabelli F, Salis A, Perotti M, Taddei F, Bellomo G, Orrenius S: Alterations of surface morphology caused by metabolism of menadione in mammalian cells are associated with the oxidation of critical sulfhydryl groups in cytoskeletal proteins. Biochem Pharmacol 1998, 37:3423-3427
28. Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, Ohtsuka E, Nishimura S: Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 1987, 327:77-79
29. Fraga CG, Shigenaga MK, Park J-W, Degan P, Ames BN: Oxidative damage to DNA during aging: 8-hydroxy-2′-deoxyguanosine in rat organ DNA and urine. Proc Natl Acad Sci USA 1990, 87:4533-4537
30. Boveris A, Cadenas E: Cellular sources and steady-state levels of reactive oxygen species. Oxygen, Gene Expression, and Cellular Function. Edited by L Biadasz Clerch, DJ Massaro. New York, Marcel Dekker, 1997, pp 1-25
31. Hartmann JF: Electron microscopy of motor nerve cells following section of axones. Anat Rec 1954, 118:19-33
32. Weiss P, Pillai A: Convection and fate of mitochondria in nerve fibers: axonal flow as vehicle. Proc Natl Acad Sci USA 1965, 54:48-56
33. Blümcke S, Neidorf HR, Rode J: Axoplasmic alterations in the proximal and distal stumps of transsected nerves. Acta Neuropathol 1966, 7:44-61
34. Hamori J, Lakos I: Ultrastructural alterations in the initial segments and in the recurrent collateral terminals of Purkinje cells following axotomy. Cell Tissue Res 1980, 212:415-427
35. Fawcett DW: Observations on the cytology and electron microscopy of hepatic cells. J Natl Cancer Inst 1955, 15:1475-1512
36. Bandy B, Davison AJ: Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Rad Biol Med 1990, 8:523-539
37. Friede RL: Transport of oxidative enzymes in nerve fibers: a histochemical investigation of the regenerative cycle in neurons. Exp Neurol 1959, 1:441-466
38. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G: Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 1996, 184:1331-1341
39. Beal MF, Ferrante RJ, Browne SE, Matthews RT, Kowall NW, Brown RH: Increased 3-nitrotyrosine in both sporadic, and familial amyotrophic lateral sclerosis. Ann Neurol 1997, 42:646-654
40. Smith MA, Rudnicka-Nawrot M, Richey PL, Praprotnik D, Mulvihill P, Miller CA, Sayre LM, Perry G: Carbonyl-related posttranslational modification of neurofilament protein in the neurofibrillary pathology of Alzheimer's disease. J Neurochem 1995, 64:2660-2666
41. Good PF, Werner P, Hsu A, Olanow CW, Perl DP: Evidence of neuronal oxidative damage in Alzheimer's disease. Am J Pathol 1996, 149:21-28
42. Rosen DR, Siddique T, Patterson D, Figiewicz DA, Sapp P. Hentati A, Donalsson D, Goto J, O'Regan JP, Deng H-X, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston AM, Berger R, Tanzi RE, Halperin JJ, Harzfeldt B, Van den Bergh R, Hung W-Y, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vance MA, Haines J, Rouleau GA, Gusella JS, Horvitz HR, Brown RH: Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62
43. Deng H-X, Hentati A, Tainer JA, Iqbal Z, Cayabyab A, Hung W-Y, Getzoff ED, Hu P, Herzfeldt B, Roos RP, Warner C, Deng G, Soriano E, Smyth C, Parge HE, Ahmed A, Roses AD, Hallewell RA, Pericak-Vance MA, Siddique T: Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 1993, 261:1047-1051
44. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hantati A, Kwon YW, Deng H-X, Chen W, Zhai P, Sufit RL, Siddique T: Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994, 264: 1772-1775
45. Martin LJ: Neurodegeneration in amyotrophic lateral sclerosis (ALS) resembles apoptosis and may occur by a programmed cell death mechanism. Soc Neurosci Abstr 1998 (in press)