Identification of AGE-modified proteins in SH-SY5Y and OLN-93 Cells

Neurotoxicity Research

Volumn 9, Issue 4, 2006, Pages 255-268

  Langer, André K ^a   Poon, H Fai ^c   Münch, Gerald ^d   Lynn, Bert C ^c   Arendt, Thomas ^b   Butterfield, D Allan ^c  

^a UNIVERSITY HOSPITAL LEIPZIG   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c UNIVERSITY OF KENTUCKY   (United States)

^d JAMES COOK UNIVERSITY   (Australia)

Author keywords

abulin; Advanced glycation end products; AGEs; Aging; Alzheimer disease; Diabetes; Eukaryotic elongation factor 1 ; Neurodecogenerative diseas; OLN 93cells; SH SY5Y cells

Indexed keywords

ADVANCED GLYCATION END PRODUCT;

ANIMAL; ARTICLE; BIOSYNTHESIS; CHEMISTRY; CHINCHILLA; COMPARATIVE STUDY; HUMAN; METABOLISM; OLIGODENDROGLIA; RABBIT; RAT; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CHINCHILLA; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; OLIGODENDROGLIA; RABBITS; RATS;

EID: 33747454975     PISSN: 10298428     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF03033316     Document Type: Article

References (87)

1. Agarwal PK, A Geist and A Gorin (2004) Protein dynamics and enzymatic catalysis: Investigating the peptidyl-prolyl cis-trans isomerization activity of cyclophilin A. Biochemistry 43, 10605-10618.
2. Ahmed N and PJ Thornalley (2002) Chromatographic assay of glycation adducts in human serum albumin glycated in vitro by derivatization with 6-aminoquinolyl-N-hydroxysuccinimidyl-carbamate and intrinsic fluorescence. Biochem. J. 364, 15-24.
3. Aksenov MY, MV Aksenova, DA Butterfield, JW Geddes and WR Markesbery (2001) Protein oxidation in the Alzheimer's disease brain: Analysis of protein carbonyls by immunocytochemistry and two-dimensional Western blotting. Neuroscience 103, 373-383.
4. Arendt T (2002) Dysregulation of neuronal differentiation and cell cycle control in Alzheimer's disease. J. Neural Transm. Suppl. 77-85.
5. Avramut M and CL Achim (2002) Immunophilins and their ligands: Insights into survival and growth of human neurons. Physiol. Behav. 77, 463-468.
6. Avramut M and CL Achim (2003) Immunophilins in nervous system degeneration and regeneration. Curr. Top. Med. Chem. 3, 1376-1382.
7. Bachmair A, D Finley and A Varshavsky (1986) In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-186.
8. Baynes JW (2002) The Maillard hypothesis on aging: Time to focus on DNA. Ann. NYAcad. Sci. 959, 360-367.
9. Berg D, C Holzmann and O Riess (2003) 14-3-3 Proteins in the nervous system. Nat. Rev. Neurosci. 40, 752-762.
10. Bevec D, H Klier, W Holter, E Tschachler, P Valent, F Lottspeich, T Baumrukerand J Hauber (1994) Induced gene expression of the hypusine-containing protein eukaryotic initiation factor 5A in activated human T lymphocytes. Proc. Natl. Acad. Sci. USA 91, 10829-10833.
11. Bommer UA and BJ Thiele (2004) The translationally controlled tumour protein (TCTP). Int. J. Biochem. Cell. Biol. 36, 379-385.
12. Bousova I, D Vukasovic, D Juretic, V Palicka and J Drsata (2005) Enzyme activity and AGE formation in a model of AST glycoxidation by D-fructose in vitro. Acta Pharm. 55, 107-114.
13. Boyd-Kimball D, A Castegna, R Sultana, HF Poon, R Petroze, BC Lynn, JB Klein and DA Butterfield (2005) Proteomic identification of proteins oxidized by Aβ(1-42) in synaptosomes: Implications for Alzheimer's disease. Brain Res. 1044, 206-215.
14. Brock JW, DJ Hinton, WE Cotham, TO Metz, SR Thorpe, JW Baynes and JM Ames (2003) Proteomic analysis of the site specificity of glycation and carboxymethylation of ribonuclease. J. Proteome Res. 2, 506-513.
15. Butterfield DA (2004) Proteomics: A new approach to investigate oxidative stress in Alzheimer's disease brain. Brain Res. 1000, 1-7.
16. Butterfield DA, D Boyd-Kimball and A Castegna (2003) Proteomics in Alzheimer's disease: Insights into mechanisms of neurodegeneration. J. Neurochem. 86, 1313-1327.
17. Cans C, BJ Passer, V Shalak, V Nancy-Portebois, V Crible, N Amzallag, D Allanic, R Tufino, M Argentini, D Moras, G Fiucci, B Goud, M Mirande, R Amson and A Telerman (2003) Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc. Natl. Acad. Sci. USA 100, 13892-13897.
18. Caraglia M, M Marra, G Giuberti, AM D'Alessandro, A Budillon, S del Prete, A Lentini, S Beninati and A Abbruzzese (2001) The role of eukaryotic initiation factor 5A in the control of cell proliferation and apoptosis. Amino Acids 20, 91-104.
19. Clarkson E, CF Costa and LM Machesky (2004) Congenital myopathies: diseases of the actin cytoskeleton. J. Pathol. 204, 407-417.
20. Clement PM, CA Henderson, ZA Jenkins, Z Smit-McBride, EC Wolff, JW Hershey, MH Park and HE Johansson (2003) Identification and characterization of eukaryotic initiation factor 5A-2. Eur. J. Biochem. 270, 4254-4263.
21. de Arriba SG, C Loske, I Meiners, G Fleischer, M Lobisch, K Wessel, H Tritschler, R Schinzel and G Munch (2003) Advanced glycation endproducts induce changes in glucose consumption, lactate production, and ATP levels in SH-SY5Y neuroblastoma cells by a redox-sensitive mechanism. J. Cereb. Blood Flow Metab. 23, 1307-1313.
22. Downing KH and E Nogales (1999) Crystallographic structure of tubulin: implications for dynamics and drug binding. Cell Struct. Funct. 24, 269-275.
23. Dukic-Stefanovic S, D Schicktanz, A Wong, D Palm, P Riederer, T Niwa, R Schinzel and G Munch (2002) Characterization of antibody affinities using an AGE-modified dipeptide spot library. J. Immunol. Methods 266, 45-52.
24. Dukic-Stefanovic S, J Gasic-Milenkovic, W Deuther-Conrad and G Munch (2003) Signal transduction pathways in mouse microglia N-11 cells activated by advanced glycation endproducts (AGEs). J. Neurochem. 87, 44-55.
25. Ejiri S (2002) Moonlighting functions of polypeptide elongation factor 1: From actin bundling to zinc finger protein R1-associated nuclear localization. Biosci. Biotechnol. Biochem. 66, 1-21.
26. Fasman GD (1989) Predictions of protein structure and the principles of protein conformation. Planum Press.
27. Gachet Y, S Tournier, M Lee, A Lazaris-Karatzas, T Poulton and UA Bommer (1999) The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J. Cell. Sci. 112 (Pt 8), 1257-1271.
28. Galbraith JA and PE Gallant (2000) Axonal transport of tubulin and actin. J. Neurocytol. 29, 889-911.
29. Ganoza MC, MC Kiel and H Aoki (2002) Evolutionary conservation of reactions in translation. Microbiol. Mol. Biol. Rev. 66, 460-85, table.
30. Gasic-Milenkovic J, S Dukic-Stefanovic, W Deuther-Conrad, U Gartner and G Munch (2003) beta-Amyloid peptide potentiates inflammatory responses induced by lipopolysaccharide, interferon-gamma and 'advanced glycation endproducts' in a murine microglia cell line. Eur. J. Neurosci. 17, 813-821.
31. Giardino I, D Edelstein and M Brownlee (1994) Nonenzymatic glycosylation in vitro and in bovine endothelial cells alters basic fibroblast growth factor activity. A model for intracellular glycosylation in diabetes. J. Clin. Invest. 94, 110-117.
32. Gorg A, C Obermaier, G Boguth, A Harder, B Scheibe, R Wildgruber and W Weiss (2000) The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21, 1037-1053.
33. Gothel SF and MA Marahiel (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 55, 423-436.
34. Gutala RV and PH Reddy (2004) The use of real-time PCR analysis in a gene expression study of Alzheimer's disease post-mortem brains. J. Neurosci. Methods 132, 101-107.
35. Hasenkopf K, B Ronner, H Hiller and M Pischetsrieder (2002) Analysis of glycated and ascorbylated proteins by gas chromatography-mass spectrometry. J. Agric. Food Chem. 50, 5697-5703.
36. Hashiguchi M, K Sobue and HK Paudel (2000) 14-3-3Zeta is an effector of tau protein phosphorylation. J. Biol. Chem. 275, 25247-25254.
37. Hershey JW (1991) Translational control in mammalian cells. Annu. Rev. Biochem. 60, 717-755.
38. Horie K, T Miyata, K Maeda, S Miyata, S Sugiyama, H Sakai, DS van Ypersole, V Monnier, JL Witztum and K Kurokawa (1997) Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy. J. Clin. Invest. 100, 2995-3004.
39. Jensen ON, M Wilm, A Shevchenko and M Mann (1999) Sample preparation methods for mass spectrometric peptide mapping directly from 2-DE gels. Methods Mol. Biol. 112, 513-530.
40. Jin ZG, MG Melaragno, DF Liao, C Yan, J Haendeler, YA Suh, JD Lambeth and BC Berk (2000) Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ. Res. 87, 789-796.
41. Johnson G, J Gotlib, V Haroutunian, L Bierer, AC Nairn, C Merril and W Wallace (1992) Increased phosphorylation of elongation factor 2 in Alzheimer's disease. Brain Res. Mol. Brain Res. 15, 319-326.
42. Kabsch W and KC Holmes (1995) The actin fold. FASEB J. 9, 167-174.
43. Kennedy L and JW Baynes (1984) Non-enzymatic glycosylation and the chronic complications of diabetes: An overview. Diabetologia 26, 93-98.
44. Kikuchi S, K Shinpo, M Takeuchi, S Yamagishi, Z Makita, N Sasaki and K Tashiro (2003) Glycation - a sweet tempter for neuronal death. Brain Res. Brain Res. Rev. 41, 306-323.
45. Kil IS, JH Lee, AH Shin and JW Park (2004) Glycation-induced inactivation of NADP(+)-dependent isocitrate dehydrogenase: Implications for diabetes and aging. Free Radic. Biol. Med. 37, 1765-1778.
46. Kozak M (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234, 187-208.
47. Lee HJ, SK Howell, RJ Sanford and PJ Beisswenger (2005) Methylglyoxal can modify GAPDH activity and structure. Ann. NY Acad. Sci. 1043, 135-145.
48. Loske C, A Neumann, AM Cunningham, K Nichol, R Schinzel, P Riederer and G Munch (1998) Cytotoxicity of advanced glycation endproducts is mediated by oxidative stress. J. Neural Transm. 105, 1005-1015.
49. Lue LF, DG Walkerand J Rogers (2001) Modeling microglial activation in Alzheimer's disease with human postmortem microglial cultures. Neurobiol. Aging 22, 945-956.
50. Medori R, H Jenich, L Autilio-Gambettiand P Gambetti (1988) Experimental diabetic neuropathy: Similar changes of slow axonal transport and axonal size in different animal models. J. Neurosci. 8, 1814-1821.
51. Miyata T, N Ishiguro, Y Yasuda, T Ito, M Nangaku, H Iwata and K Kurokawa (1998) Increased pentosidine, an advanced glycation end product, in plasma and synovial fluid from patients with rheumatoid arthritis and its relation with inflammatory markers. Biochem. Biophys. Res. Commun. 244, 45-49.
52. Monnier VM and A Cerami (1981) Nonenzymatic browning in vivo: Possible process for aging of long-lived proteins. Science 211, 491-493.
53. Munch G, R Schinzel, C Loske, A Wong, N Durany, JJ Li, H Vlassara, MA Smith, G Perry and P Riederer (1998) Alzheimer's disease-synergistic effects of glucose deficit, oxidative stress and advanced glycation endproducts. J. Neural Transm. 105, 439-461.
54. Munch G, D Schicktanz, A Behme, M Gerlach, P Riederer, D Palm and R Schinzel (1999) Amino acid specificity of glycation and protein-AGE crosslinking reactivities determined with a dipeptide SPOT library. Nat. Biotechnol. 17, 1006-1010.
55. Munch G, B Kuhla, HJ Luth, T Arendt and SR Robinson (2003) Anti-AGEing defences against Alzheimer's disease. Biochem. Soc. Trans. 31, 1397-1399.
56. Nagai R, CM Hayashi, L Xia, M Takeya and S Horiuchi (2002) Identification in human atherosclerotic lesions of GA-pyridine, a novel structure derived from glycolaldehyde-modified proteins. J. Biol. Chem. 277, 48905-48912
57. Nakamura K, Y Nakazawa and K Ienaga (1997) Acid-stable fluorescent advanced glycation end products: Vesperlysines A, B, and C are formed as crosslinked products in the Maillard reaction between lysine or proteins with glucose. Biochem. Biophys. Res. Commun. 232, 227-230.
58. Neye H (2000) [Immunophilins: Having immunosuppressive activity and physiological function]. Pharm. Unserer Zeit 29, 297-302.
59. Pamplona R, E Dalfo, V Ayala, MJ Bellmunt, J Prat, I Ferrer and M Portero-Otin (2005) Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation. Effects of Alzheimer disease and identification of lipoxidation targets. J. Biol. Chem. 280, 21522-21530.
60. Pancholi V (2001) Multifunctional alpha-enolase: Its role in diseases. Cell. Mol. Life Sci. 58, 902-920.
61. Park MH (1987) Regulation of biosynthesis of hypusine in Chinese hamster ovary cells. Evidence for eIF-4D precursor polypeptides. J. Biol. Chem. 262, 12730-12734.
62. Park MH, SI Chung, HL Cooper and JE Folk (1984) The mammalian hypusine-containing protein, eukaryotic initiation factor 4D. Structural homology of this protein from several species. J. Biol. Chem. 259, 4563-4565.
63. Pawlowski PG and R Dringen (2003) Identification of Nepsilon-(carboxymethyl)lysine-positive cells in astroglia-rich primary cultures. J. Neural Transm. 110, 1077-1090.
64. Poggioli S, H Bakala and B Friguet (2002) Age-related increase of protein glycation in peripheral blood lymphocytes is restricted to preferential target proteins. Exp. Gerontol. 37, 1207-1215.
65. Poon HF, A Castegna, SA Farr, V Thongboonkerd, BC Lynn, WA Banks, JE Morley, JB Klein and DA Butterfield (2004) Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated-prone 8 mice brain. Neuroscience 126, 915-926.
66. Reynet C and CR Kahn (2001) Unbalanced expression of the different subunits of elongation factor 1 in diabetic skeletal muscle. Proc. Natl. Acad. Sci. USA 98, 3422-3427.
67. Richter T, G Munch, HJ Luth, T Arendt, R Kientsch-Engel, P Stahl, D Fengler and B Kuhla (2005) Immunochemical crossreactivity of antibodies specific for "advanced glycation endproducts" with "advanced lipoxidation endproducts". Neurobiol. Aging 26, 465-474.
68. Sasaki N, R Fukatsu, K Tsuzuki, Y Hayashi, T Yoshida, N Fujii, T Koike, I Wakayama, R Yanagihara, R Garruto, N Amano and Z Makita (1998) Advanced glycation end products in Alzheimer's disease and other neurodegenerative diseases. Am. J. Pathol. 153, 1149-1155.
69. Selvaggini C, L De Gioia, L Cantu, E Ghibaudi, L Diomede, F Passerini, G Forloni, O Bugiani, F Tagliavini and M Salmona (1993) Molecular characteristics of a protease-resistant, amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. Biochem. Biophys. Tes. Commun. 194, 1380-1386.
70. Steinberg TH, LJ Jones, RP Haugland and VL Singer (1996) SYPRO orange and SYPRO red protein gel stains: One-step fluorescent staining of denaturing gels for detection of nanogram levels of protein. Anal. Biochem. 239, 223-237.
71. Talent JM, Y Kong and RW Gracy (1998) A double stain for total and oxidized proteins from two-dimensional fingerprints. Anal. Biochem. 263, 31-38.
72. Thiele H, M Berger, A Skalweit and BJ Thiele (2000) Expression of the gene and processed pseudogenes encoding the human and rabbit translationally controlled tumour protein (TCTP). Eur. J. Biochem. 267, 5473-5481.
73. Thongboonkerd V, J Luengpailin, J Cao, WM Pierce, J Cai, JB Klein and RJ Doyle (2002) Fluoride exposure attenuates expression of Streptococcus pyogenes virulence factors. J. Biol. Chem. 277, 16599-16605.
74. Thornalley PJ (1998) Cell activation by glycated proteins. AGE receptors, receptor recognition factors and functional classification of AGEs. Cell. Mol. Biol. (Noisy-le-grand) 44, 1013-1023.
75. Thornalley PJ, S Battah, N Ahmed, N Karachalias, S Agalou, R Babaei-Jadidi and A Dawnay (2003) Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem. J. 375, 581-592.
76. Tzivion G and J Avruch (2002) 14-3-3 Proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 277, 3061-3064.
77. Tzivion G, YH Shen and J Zhu (2001) 14-3-3 Proteins; bringing new definitions to scaffolding. Oncogene 20, 6331-6338.
78. Ueberham U, A Hessel and T Arendt (2003) Cyclin C expression is involved in the pathogenesis of Alzheimer's disease. Neurobiol. Aging 24, 427-435.
79. Verzar F (1964) Aging of the collagen fiber. Int. Rev. Connect. Tissue Res. 2, 243-300.
80. Vijayan S, E El Akkad, I Grundke-Iqbal and K Iqbal (2001) A pool of beta-tubulin is hyperphosphorylated at serine residues in Alzheimer disease brain. FEBSLett. 509, 375-381.
81. Vogelsberg-Ragaglia V, T Schuck, JQ Trojanowski and VM Lee (2001) PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus. Exp. Neurol. 168, 402-412.
82. Walsh CT, LD Zydowsky and FD McKeon (1992) Cyclosporin A, the cyclophilin class of peptidylprolyl isomerases, and blockade of T cell signal transduction. J. Biol. Chem. 267, 13115-13118.
83. Westhead EW (1966) Enolase from yeast and rabbit muscle. Methods Enzymol. 9, 670-679.
84. Williams SK, NL Howarth, JJ Devenny and MW Bitensky (1982) Structural and functional consequences of increased tubulin glycosylation in diabetes mellitus. Proc. Natl. Acad. Sci. USA 79, 6546-6550.
85. Wistow GJ, T Lietman, LA Williams, SO Stapel, WW de Jong, J Horwitz and J Piatigorsky (1988) Tau-crystallin/alpha-enolase: One gene encodes both an enzyme and a lens structural protein. J. Cell. Biol. 107, 2729-2736.
86. Yaffe MB (2002) How do 14-3-3 proteins work? - Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57.
87. Yan H and JJ Harding (2005) Carnosine protects against the inactivation of esterase induced by glycation and a steroid. Biochim. Biophys. Acta 1741, 120-126.