RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease

Journal of Neuroscience

Volumn 19, Issue 6, 1999, Pages 1959-1964

  Nunomura, Akihiko ^a   Perry, George ^c   Pappolla, Miguel A ^c   Wade, Ramon ^d   Hirai, Keisuke ^b   Chiba, Shigeru ^a   Smith, Mark A ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

^c UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

^d TAKEDA PHARMACEUTICAL COMPANY LIMITED   (Japan)

Author keywords

8 hydroxyguanosine; 8 hydroxydeoxyguanosine; Alzheimer's disease; DNA oxidation; Mitochondrial damage; Oxidative stress; RNA oxidation

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; GUANOSINE DERIVATIVE; MITOCHONDRIAL DNA; MITOCHONDRIAL RNA; REACTIVE OXYGEN METABOLITE; RNA;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN MITOCHONDRION; BRAIN NERVE CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE MARKER; DNA METABOLISM; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MAJOR CLINICAL STUDY; OXIDATION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; RNA METABOLISM;

EID: 0033559462     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-06-01959.1999     Document Type: Article

References (47)

1. Al-Abdulla NA, Martin LJ (1998) Apoptosis of retrogradely degenerating neurons occurs in association with the accumulation of perikaryal mitochondria and oxidative damage to the nucleus. Am J Pathol 153:447-456.
2. Bancroft JD, Stevens A (1996) Theory and practice of histological techniques. Fourth edition. New York: Churchill-Livingstone.
3. Beul MF (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 38:357-366.
4. Claycamp HG (1992) Phenol sensitization of DNA to subsequent oxidative damage in 8-hydroxyguanine assays. Carcinogenesis 13:1289-1292.
5. Collins AR, Dusinska M, Gedik CM, Stetina R (1996) Oxidative damage to DNA: do we have a reliable biomarker? Environ Health Perspect 104[Suppl 3]:465-469.
6. Colurso GJ, Kan RK, Anthony A (1995) Microdensitometric measures of cytoplasmic RNA and total protein in pyramidal neurons of the insular cortex and midfrontal gyrus in patients with Alzheimer's disease. Cell Biochem Fund 13:287-292.
7. Dani SU (1997) Molecular turnover and aging. In: Principles of neural aging (Dani SU, Hori A, Walter GF, eds), pp 83-101. Amsterdam: Elsevier.
8. Davison AN (1981) Biochemistry of the nervous system. In: The molecular basis of neuropathology (Davison AN, Thompson RHS, eds). pp 1-13, London: Arnold.
9. Fiala ES, Conaway CC, Mathis JE (1989) Oxidative DNA and RNA damage in the livers of Sprague Dawley rats treated with the hepatocarcinoijen 2-nitropropane. Cancer Res 49:5518-5522.
10. Floyd RA, West MS, Eneff KL, Schneider JE, Wong PK, Tingey DT, Hogsett WE (1990) Conditions influencing yield and analysis of 8-hydroxy-2′-deuxyguanosine in oxidatively damaged DNA. Anal Biochem 188:155-158.
11. Ginsberg SD, Crino PB, Lee VM-Y, Eberwine JH, Trojanowski JQ (1997) Sequestration of RNA in Alzheimer's disease neurofibrillary tangles and senile plaques. Ann Neurol 41:200-209.
12. Giuffrida AM (1983) Nucleic acids in developing brain. In: Handbook of neurochcrnistry. Vol 5, Metabolic turnover in the nervous system, 2nd Ed (Lajtha A, ed). pp 227-250. New York: Plenum.
13. Good PF, Werner P, Hsu A, Olanow CW, Perl DP (1996) Evidence for neuronal oxidative damage in Alzheimer's disease. Am J Pathol 149:21-28.
14. Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, Yeo HC, Ames BN (1998) DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxogaunine. Proc Natl Acad Sci USA 95:288-293.
15. Joenje H (1989) Genetic toxicology of oxygen. Mutat Res 219:193-208.
16. Khachaturian ZS (1985) Diagnosis of Alzheimer's disease. Arch Neurol 42:1097-1105.
17. Mann DMA, Neary D, Yates PO, Lincoln J, Snowden JS, Stanworth P (1981) Alterations in protein synthetic capability of nerve cells in Alzheimer's disease. J Neurol Neurosurg Psychiatry 44:97-102.
18. Markeshery WR (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23:134-147.
19. Masliah E, Terry RD, Alford M, DeTeresa R (1990) Quantitative immunohistochemislry of synaptophysin in human neocortex: an alternative method to estimate density of presynaptic terminals in paraffin sections. J Histochem Cytochem 38:837-844.
20. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, Beal MF (1993) Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol 34:609-616.
21. Mecocci P, MacGarvey U, Beal MF (1994) Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann Neurol 36:747-751.
22. Meeocci P, Beal MF, Ceechetti R, Polidori MC, Cherubini A, Chionne F, Avellini L, Romano G, Senin U (1997) Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain. Mol Chem Neuropathol 31:53-64.
23. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The consortium to establish a registry for Alzheimer's disease (CERAD). II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41:479-486.
24. Montine TJ, Amarnath V, Martin ME, Strittmatter WJ, Graham DG (1996) E-4-hydroxy-2-nonenal is cytotoxic and cross-links cytoskeletal proteins in P19 neuroglial cultures. Am J Pathol 148:89-93.
25. Pappolla MA, Omar RA, Kim KS, Robakis NK (1992) Immunohistochemical evidence of oxidative stress in Alzheimer's disease. Am J Pathol 140:621-628.
26. Park EM, Shigenaga MK, Degan P, Korn TS, Kitzler JW, Wehr CM, Kolachana P, Ames BN (1992) Assay of excised oxidativc DNA lesions: isolation of 8-oxoguanine and its nucleosidc derivatives from biological fluids with a monoclonal antibody column. Proc Natl Acad Sci USA 89:3375-3379.
27. Perry G, Kawai M, Tabaton M, Onorato M, Mulvihill P, Richey P, Morandi A, Connolly JA, Gambetti P (1991) Neuropil threads of Alzheimer's disease show a marked alteration of the normal cytoskeleton. J Neurosci 11:1748-1755.
28. Peters A, Palay SL, Webster H deF (1991) The fine structure of the nervous system, 3rd Ed. New York: Oxford UP.
29. Premkumar DRD, Smith MA, Richey PL, Petersen RB, Castellani R, Kutty RK, Wiggert B, Perry G, Kalaria RN (1995) Induction of heme oxygenase-1 mRNA and protein in neocorlex and cerebral vessels in Alzheimer's disease. J Neurochem 65:1399-1402.
30. Prohaska JR (1987) Functions of trace elements in brain metabolism. Physiol Rev 67:858-901.
31. Rhee Y, Valentine MR, Termini J (1995) Oxidative base damage in RNA detected by reverse transcriptase. Nucleic Acids Res 23:3275-3282.
32. Sayre LM, Zelasko DA, Harris PLR, Perry G, Salomon RG, Smith MA (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J Neurochem 68:2(192-2097.
33. Schubert J, Wilmer JW (1991) Does hydrogen peroxide exist "free" in biological systems? Free Radic Biol Med 11:545-555.
34. Smith MA, Perry G (1998) The role of oxidative stress in the pathological sequelae of Alzheimer disease. In: Free radicals, oxidative stress, and antioxidants: pathological and physiological significance (Özben T, ed), pp 195-204. New York: Plenum.
35. Smith MA, Taneda S, Richey PL, Miyata S, Yan S-D, Stern D, Sayre LM, Monnier VM, Perry G (1994) Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc Natl Acad Sci USA 91:5710-5714.
36. Smith MA, Sayre L, Perry G (1996a) Is Alzheimer's a disease of oxidative stress? Alzheimer Dis Rev 1:63-67.
37. Smith MA, Perry G, Richey PL, Sayre LM, Anderson VE, Beal MF, Kowall N (1996b) Oxidative damage in Alzheimer's. Nature 382:120-121.
38. Smith MA, Harris PLR, Sayre LM, Perry G (1997a) Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc Natl Acad Sci USA 94:9866-9868.
39. Smith MA, Harris PLR. Sayre LM, Beckman JS, Perry G (1997b) Widespread peroxynitrite-medialed damage in Alzheimer's disease. J Neurosci 17:2653-2657.
40. Smith MA, Sayre LM, Anderson VE, Harris PLR. Beal MF, Kowall N, Perry G (1998) Cytochemical demonstration of oxidative damage in Alzheimer disease by immunochemical enhancement of the earbonyl reaction with 2,4-dinitrophenylhydrazine. J Histochem Cytochem 46:731-735.
41. Sternberger LA (1986) Immunocytochemistry, 3rd Ed. New York: Wiley.
42. Takahashi M, Asada K (1983) Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids. Arch Biochem Biophys 226:558-566.
43. Takahashi Y (1984) Brain nuclei. In: Handbook of neurochemistry. Vol 7, Structural elements of the nervous system. 2nd Ed (Lajtha A, ed), pp 205-230. New York: Plenum.
44. Uppu RM, Cueto R, Squadrito GL, Salgo MG, Pryor WA (1996) Competitive reactions of peroxynitrite with 2′-deoxyguanosine and 7,8-dihydro-8-oxo-2′-deoxyguanosine (8-oxodG): relevance to the formation of 8-oxodG in DNA exposed to peroxynitrite. Free Radic Biol Med 21:407-411.
45. Wamer WG, Wei RR (1997) In vitro photooxidation of nucleic acids by ultraviolet A radiation. Photochem Photobiol 65:560-563.
46. Warner WG, Yin JJ, Wei RR (1997) Oxidative damage to nucleic acids photosensitized by titanium dioxide. Free Radic Biol Med 23:851-858.
47. Yin B, Whyatt RM, Perera FP, Randall MC, Cooper TB, Santella RM (1995) Determination of 8-hydroxydeoxyguanosine by an immunoaffinity chromatography-monoclonal antibody-based ELISA. Free Radic Biol Med 18:1023-1032.