Reduced neuronal expression of synaptic transmission modulator HNK-1/neural cell adhesion molecule as a potential consequence of amyloid β-mediated oxidative stress: A proteomic approach

Journal of Neurochemistry

Volumn 92, Issue 4, 2005, Pages 705-717

  Thomas, Stefani N ^a   Soreghan, Brian A ^a   Nistor, Mihaela ^b   Sarsoza, Floyd ^b   Head, Elizabeth ^b   Yang, Austin J ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid ; Glucuronyltransferase; Human Natural Killer (HNK 1); Liquid chromatography tandem mass spectrometry; Oxidative stress

Indexed keywords

AMYLOID BETA PROTEIN; BIOCYTIN; GLUCURONOSYLTRANSFERASE; HYDRAZIDE; NERVE CELL ADHESION MOLECULE; STREPTAVIDIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PURIFICATION; ARTICLE; BIOINFORMATICS; BIOSYNTHESIS; BRAIN CELL; CARBONYLATION; CELL CULTURE; CELLULAR DISTRIBUTION; COGNITIVE DEFECT; CULTURE MEDIUM; ENZYME ACTIVITY; ENZYME METABOLISM; GOLGI COMPLEX; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NATURAL KILLER CELL; NERVE CELL PLASTICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SYNAPTIC TRANSMISSION; TANDEM MASS SPECTROMETRY; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN; ANIMALS; ANTIGENS, CD57; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CELLS, CULTURED; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION; GLUCURONOSYLTRANSFERASE; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NEURAL CELL ADHESION MOLECULES; NEURONS; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PREGNANCY; PROTEOMICS; SYNAPTIC TRANSMISSION;

EID: 13644259768     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02892.x     Document Type: Article

References (61)

1. Abo T. and Balch C. M. (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J. Immunol. 127, 1024-1029.
2. Aksenova M. V., Aksenov M. Y., Payne R. M., Trojanowski J. Q., Schmidt M. L., Carney J. M., Butterfield D. A. and Markesbery W. R. (1999) Oxidation of cytosolic proteins and expression of creatine kinase BB in frontal lobe in different neurodegenerative disorders. Dement. Geriatr. Cogn. Disord. 10, 158-165.
3. Aksenov M. Y., Aksenova M. V., Butterfield D. A., Geddes J. W. and Markesbery W. R. (2001) Protein oxidation in the brain in Alzheimer's disease. Neuroscience 103, 373-383.
4. Atwood C. S., Moir R. D., Huang X., Scarpa R. C., Bacarra N. M., Romano D. M., Hartshorn M. A., Tanzi R. E. and Bush A. I. (1998) Dramatic aggregation of Alzheimer Abeta by Cu(II) is induced by conditions representing physiological acidosis. J. Biol. Chem. 273, 12817-12826.
5. Berlett B. S. and Stadtman E. R. (1997) Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20 313-20 316.
6. Blackburn A. C., Doe W. F. and Buffinton G. D. (1999) Protein carbonyl formation on mucosal proteins in vitro and in dextran sulfate-induced colitis. Free Radic. Biol. Med. 27, 262-270.
7. Burdick D., Soreghan B., Kwon M., Kosmoski J., Knauer M., Henschen A., Yates J., Cotman C. and Glabe C. (1992) Assembly and aggregation properties of synthetic Alzheimer's A4/beta amyloid peptide analogs. J. Biol. Chem. 267, 546-554.
8. Butterfield D. A. (1997) Beta-amyloid-associated free radical oxidative stress and neurotoxicity: implications for Alzheimer's disease. Chem. Res. Toxicol. 10, 495-506.
9. Butterfield D. A., Hensley K., Harris M., Mattson M. and Carney J. (1994) Beta-amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer's disease. Biochem. Biophys. Res. Commun. 200, 710-715.
10. Chan C.-W., Dharmarajan A., Atwood C. S., Huang X., Tanzi R. E., Bush A. I. and Martins R. N. (1999) Anti-apoptotic action of Alzheimer Aβ. Alz. Report 2, 113-119.
11. Das K. K., Basu M., Li Z. X., Basu S. and Jungalwala F. (1990) Characterization of solubilized GlcAT-1 (UDP-GlcA: nLcOse4Cer beta 1-3 glucuronyltransferase) activity from embryonic chicken brain and its inhibition by D-erythrosphingosine. Indian J. Biochem. Biophys. 27, 396-401.
12. Das N., Levine R. L., Orr W. C. and Sohal R. S. (2001) Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochem. J. 360, 209-216.
13. Ehmann W. D., Markesbery W. R., Alauddin M., Hossain T. I. and Brubaker E. H. (1986) Brain trace elements in Alzheimer's disease. Neurotoxicology 7, 195-206.
14. Good P. F., Werner P., Hsu A., Olanow C. W. and Perl D. P. (1996) Evidence of neuronal oxidative damage in Alzheimer's disease. Am. J. Pathol. 149, 21-28.
15. Goodman Y. and Mattson M. P. (1994) Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peptide-induced oxidative injury. Exp. Neurol. 128, 1-12.
16. Hardy J. and Selkoe D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
17. Head E., McCleary R., Hahn F. F., Milgram N. W. and Cotman C. W. (2000) Region-specific age at onset of beta-amyloid in dogs. Neurobiol. Aging 21, 89-96.
18. Holcomb L., Gordon M. N., McGowan E. et al. (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med. 4, 97-100.
19. Huang X., Cuajungco M. P., Atwood C. S. et al. (1999) Cu(II) potentiation of Alzheimer Abeta neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction. J. Biol. Chem. 274, 37 111-37 116.
20. Imiya K., Ishizaki T., Seiki T., Saito F., Inazawa J., Oka S. and Kawasaki T. (2002) cDNA cloning, genomic structure and chromosomal mapping of the mouse glucuronyltransferase-S involved in the biosynthesis of the HNK-1 carbohydrate epitope. Gene 296, 29-36.
21. Jesberger J. A. and Richardson J. S. (1991) Oxygen free radicals and brain dysfunction. Int. J. Neurosci. 5, 1-17.
22. Knauer M. F., Soreghan B., Burdick D., Kosmoski J. and Glabe C. G. (1992) Intracellular accumulation and resistance to degradation of the Alzheimer amyloid A4/beta protein. Proc. Natl Acad. Sci. USA 89, 7437-7441.
23. Kontush A. (2001) Amyloid-β: an antioxidant that becomes a prooxidant and critically contributes to Alzheimer's disease. Free Radic. Biol. Med. 31, 1120-1131.
24. Kontush A., Berndt C., Weber W., Akopyan V., Arlt S., Schippling S. and Beisiegel U. (2001) Amyloid-beta is an antioxidant for lipoproteins in cerebrospinal fluid and plasma. Free Radic. Biol. Med. 30, 119-128.
25. Korolainen M. A., Goldsteins G., Alafuzoff I., Koistinaho J. and Pirttila T. (2002) Proteomic analysis of protein oxidation in Alzheimer's disease brain. Electrophoresis 23, 3428-3433.
26. Ma Y. S., Chao C. C. and Stadtman E. R. (1999) Oxidative modification of glutamine synthetase by 2,2′-azobis (2-amidinopropane) dihydrochloride. Arch. Biochem. Biophys. 363, 129-134.
27. Markesbery W. R. (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic. Biol. Med. 23, 134-147.
28. Matsuoka Y., Picciano M., La Francois J. and Duff K. (2001) Fibrillar beta-amyloid evokes oxidative damage in a transgenic mouse model of Alzheimer's disease. Neuroscience 104, 609-613.
29. Mattson M. P., Barger S. W., Begley J. G. and Mark R. J. (1995) Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol. 46, 187-216.
30. Mesulam M. M. (1999) Neuroplasticity failure in Alzheimer's disease: bridging the gap between plaques and tangles. Neuron 24, 521-529.
31. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival. J. Immunol. Methods 65, 55-63.
32. Oka S., Terayama K., Kawashima C. and Kawasaki T. (1992) A novel glucuronyltransferase in nervous system presumably associated with the biosynthesis of HNK-1 carbohydrate epitope on glycoproteins. J. Biol. Chem. 267, 22 711-22 714.
33. Ouzzine M., Gulberti S., Netter P., Magdalou J. and Fournel-Gigleux S. (2000) Structure/function of the human Galbeta1,3-glucuronosyltransferase. Dimerization and functional activity are mediated by two crucial cysteine residues. J. Biol. Chem. 275, 28 254-28 260.
34. Pappolla M. A., Omar R. A., Kim K. S. and Robakis N. K. (1992) Immunohistochemical evidence of oxidative [corrected] stress in Alzheimer's disease. Am. J. Pathol. 140, 621-628.
35. Peng J. and Gygi S. P. (2001) Proteomics: the move to mixtures. J. Mass Spectrom. 36, 1083-1091.
36. Picklo M. J., Montine T. J., Amarnath V. and Neely M. D. (2002) Carbonyl toxicology and Alzheimer's disease. Toxicol. Appl. Pharmacol. 184, 187-197.
37. Pike C. J., Walencewicz A. J., Glabe C. J. and Cotman C. W. (1991) In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res. 563, 311-314.
38. Price J. M., Chi X., Hellermann G. and Sutton E. T. (2001) Physiological levels of beta-amyloid induce cerebral vessel dysfunction and reduce endothelial nitric oxide production. Neurol. Res. 23, 506-512.
39. Prydz K. and Dalen K. T. (2000) Synthesis and sorting of proteoglycans. J. Cell Sci. 113(Part 2), 193-205.
40. Saghatelyan A. K., Gorissen S., Albert M., Hertlein B., Schachner M. and Dityatev A. (2000) The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA1 region of the hippocampus. Eur. J. Neurosci. 12, 3331-3342.
41. Sayre L. M., Zelasko D. A., Harris P. L., Perry G., Salomon R. G. and Smith M. A. (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J. Neurochem. 68, 2092-2097.
42. Schachner M. (1997) Neural recognition molecules and synaptic plasticity. Curr. Opin. Cell Biol. 9, 627-634.
43. Selkoe D. J. (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766.
44. Senn C., Kutsche M., Saghatelyan A., Bosl M. R., Lohler J., Bartsch U., Morellini F. and Schachner M. (2002) Mice deficient for the HNK-1 sulfotransferase show alterations in synaptic efficacy and spatial learning and memory. Mol. Cell. Neurosci. 20, 712-729.
45. Shacter E. (2000) Quantification and significance of protein oxidation in biological samples. Drug Metab. Rev. 32, 307-326.
46. Shearman M. S., Ragan C. I. and Iversen L. L. (1994) Inhibition of PC12 cell redox activity is a specific, early indicator of the mechanism of β-amyloid-mediated cell death. Proc. Natl Acad. Sci. USA 91, 1470-1474.
47. Shringarpure R. and Davies K. J. A. (2002) Protein turnover by the proteasome in aging and disease. Free Radic. Biol. Med. 32, 1084-1089.
48. Smith C. D., Carney J. M., Starke-Reed P. E., Oliver C. N., Stadtman E. R., Floyd R. A. and Markesbery W. R. (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc. Natl Acad. Sci. USA 88, 10 540-10 543.
49. Smith M. A., Rottkamp C. A., Nunomura A., Raina A. K. and Perry G. (2000) Oxidative stress in Alzheimer's disease. Biochim. Biophys. Acta 1502, 139-144.
50. Soreghan B., Thomas S. N. and Yang A. J. (2003a) Aberrant sphingomyelin/ceramide metabolic-induced neuronal endosomal/ lysosomal dysfunction: potential pathological consequences in age-related neurodegeneration. Adv. Drug Deliv. Rev. 55, 1515-1524.
51. Soreghan B., Yang F., Thomas S., Hsu J. and Yang A. (2003b) High-throughput proteomic-based identification of oxidatively induced protein carbonylation in mouse brain. Pharmacol. Res. 20, 1713-1720.
52. Stephan A., Laroche S. and Davis S. (2001) Generation of aggregated beta-amyloid in the rat hippocampus impairs synaptic transmission and plasticity and causes memory deficits. J. Neurosci. 21, 5703-5714.
53. Strekalova T., Wotjak C. T. and Schachner M. (2001) Intrahippocampal administration of an antibody against the HNK-1 carbohydrate impairs memory consolidation in an inhibitory learning task in mice. Mol. Cell. Neurosci. 17, 1102-1113.
54. Takahashi R. H., Milner T. A., Li F., Nam E. E., Edgar M. A., Yamaguchi H., Beal M. F., Xu H., Greengard P. and Gouras G. K. (2002) Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am. J. Pathol. 161, 1869-1879.
55. Walsh D. M., Klyubin I., Fadeeva J. V., Cullen W. K., Anwyl R., Wolfe M. S., Rowan M. J. and Selkoe D. J. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
56. Wataya T., Nunomura A., Smith M. A. et al. (2002) High molecular weight neurofilament proteins are physiological substrates of adduction by the lipid peroxidation product hydroxynonenal. J. Biol. Chem. 277, 4644-4648.
57. Wright J. W., Kramar E. A., Meighan S. E. and Harding J. W. (2002) Extracellular matrix molecules, long-term potentiation, memory consolidation and the brain angiotensin system. Peptides 23, 221-246.
58. Yamamoto S. and Oka S. (2001) Glucuronyltransferases involved in the HNK-1 carbohydrate epitope biosynthesis. Trends Glycosci. Glycotechn. 13, 193-208.
59. Yamamoto S., Oka S., Inoue M. et al. (2002) Mice deficient in nervous system-specific carbohydrate epitope HNK-1 exhibit impaired synaptic plasticity and spatial learning. J. Biol. Chem. 277, 27 227-27 231.
60. Yan S. D., Chen X., Schmidt A. M. et al. (1994) Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc. Natl Acad. Sci. USA 91, 7787-7791.
61. Yang A. J., Chandswangbhuvana D., Shu T., Henschen A. and Glabe C. G. (1999) Intracellular accumulation of insoluble, newly synthesized abetan-42 in amyloid precursor protein-transfected cells that have been treated with Abeta1-42. J. Biol. Chem. 274, 20 650-20 656.