Posttranslational nitro-glycative modifications of albumin in alzheimer's disease: Implications in cytotoxicity and amyloid-β peptide aggregation

Journal of Alzheimer's Disease

Volumn 40, Issue 3, 2014, Pages 643-657

  Ramos Fernández, Eva ^a   Tajes, Marta ^a   Palomer, Ernest ^a   Ill Raga, Gerard ^a   Bosch Morató, Mònica ^a   Guivernau, Biuse ^a   Román Dégano, Irene ^b   Eraso Pichot, Abel ^a   Alcolea, Daniel ^c   Fortea, Juan ^c   Nuñez, Laura ^d   Paez, Antonio ^d   Alameda, Francesc ^e   Fernández Busquets, Xavier ^f,g,h   Lleó, Alberto ^c   Elosúa, Roberto ^b   Boada, Mercé ^i,j   Valverde, Miguel A ^a   Muñoz, Francisco J ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b HOSPITAL DEL MAR   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^d Instituto Grifols   (Spain)

^e UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^f INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

^g CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^h UNIVERSITY OF BARCELONA   (Spain)

ⁱ Institut Catala de Neurociencies Aplicades   (Spain)

^j HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

more..

Author keywords

Albumin; Alzheimer's disease; amyloid; glycation; nitrotyrosination; oxidative stress

Indexed keywords

ALBUMIN; AMYLOID BETA PROTEIN; GLYCOSYLATED ALBUMIN; 3-NITROTYROSINE; ALBUMINOID; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA-PROTEIN (1-42); LINSIDOMINE; MOLSIDOMINE; PEPTIDE FRAGMENT; PROTEIN AGGREGATE; TAU PROTEIN; TRYPSIN; TYROSINE;

AGED; ALBUMIN BLOOD LEVEL; ALZHEIMER DISEASE; ARTICLE; BIOCHEMICAL COMPOSITION; CELL TRANSPORT; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; HEPG2 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; NEUROPATHOLOGY; OSMOLARITY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; PROTEIN NITROTYROSINATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; TURBIDIMETRY; ANALOGS AND DERIVATIVES; BLOOD; BRAIN; CELL CULTURE; CEREBROSPINAL FLUID; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; ENDOTHELIUM CELL; GLYCOSYLATION; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

AGED; ALBUMINS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; BRAIN; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; FEMALE; GLYCOSYLATION; HUMANS; MALE; MOLSIDOMINE; NEURONS; PEPTIDE FRAGMENTS; PROTEIN AGGREGATES; PROTEIN PROCESSING, POST-TRANSLATIONAL; TAU PROTEINS; TRYPSIN; TYROSINE;

EID: 84901935628     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-130914     Document Type: Article

References (58)

1. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci U S A 82, 4245-4249. (Pubitemid 15053619)
2. Coria F, Castano EM, Frangione B (1987) Brain amyloid in normal aging and cerebral amyloid angiopathy is antigenically related to Alzheimer's disease beta-protein. Am J Pathol 129, 422-428. (Pubitemid 18029984)
3. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95, 6448-6453.
4. Ill-Raga G, Ramos-Fernandez E, Guix FX, Tajes M, Bosch- Morato M, Palomer E, Godoy J, Belmar S, CerpaW, Simpkins JW, Inestrosa NC, Munoz FJ (2010) Amyloid-beta peptide fibrils induce nitro-oxidative stress in neuronal cells. J Alzheimers Dis 22, 641-652.
5. Huang X, Atwood CS, Hartshorn MA, Multhaup G, Goldstein LE, Scarpa RC, Cuajungco MP, Gray DN, Lim J, Moir RD, Tanzi RE, Bush AI (1999) The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry 38, 7609-7616. (Pubitemid 29289332)
6. Guix FX, Uribesalgo I, Coma M, Munoz FJ (2005) The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76, 126-152. (Pubitemid 41242885)
7. Boje KM, Arora PK (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res 587, 250-256.
8. Coma M, Guix FX, Uribesalgo I, Espuna G, Sole M, Andreu D, Munoz FJ (2005) Lack of oestrogen protection in amyloidmediated endothelial damage due to protein nitrotyrosination. Brain 128, 1613-1621. (Pubitemid 41373680)
9. Yuan C, Yi L, Yang Z, Deng Q, Huang Y, Li H, Gao Z (2012) Amyloid beta-heme peroxidase promoted protein nitrotyrosination: Relevance to widespread protein nitration in Alzheimer's disease. J Biol Inorg Chem 17, 197-207.
10. Crow JP, Beckman JS (1995) Reactions between nitric oxide superoxide and peroxynitrite: Footprints of peroxynitrite in vivo. Adv Pharmacol 34, 17-43.
11. Guix FX, Ill-Raga G, Bravo R, Nakaya T, de Fabritis G, Coma M, Miscione GP, Villa-Freixa J, Suzuki T, Fernandez- Busquets X, Valverde MA, De Strooper B, Munoz FJ (2009) Amyloid-dependent triosephosphate isomerase nitrotyrosination induces glycation and tau fibrillation. Brain 132, 1335-1345.
12. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G (1997) Widespread peroxynitrite-mediated damage in Alzheimer's disease. JNeurosci 17, 2653-2657. (Pubitemid 27154998)
13. Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR, Butterfield DA (2003) Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem 85, 1394-1401. (Pubitemid 36702552)
14. Reed TT, Pierce WM Jr, Turner DM, Markesbery WR, Butterfield DA (2009) Proteomic identification of nitrated brain proteins in early Alzheimer's disease inferior parietal lobule. J Cell Mol Med 13, 2019-2029.
15. Dildar K, Sinem F, Gokhan E, Orhan Y, FilizM(2010) Serum nitrosative stress levels are increased in Alzheimer disease but not in vascular dementia. Alzheimer Dis Assoc Disord 24, 194-197.
16. Vitek MP, Bhattacharya K, Glendening JM, Stopa E, Vlassara H, Bucala R, Manogue K, Cerami A (1994) Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc Natl Acad Sci U S A 91, 4766-4770. (Pubitemid 24177730)
17. Monnier VM, Cerami A (1981) Nonenzymatic browning in vivo: Possible process for aging of long-lived proteins. Science 211, 491-493. (Pubitemid 11145319)
18. Harrington CR, Colaco CA (1994) Alzheimer's disease a glycation connection. Nature 370, 247-248.
19. Srikanth V, Westcott B, Forbes J, Phan TG, Beare R, Venn A, Pearson S, Greenaway T, Parameswaran V, Munch G (2013) Methylglyoxal cognitive function and cerebral atrophy in older people. J Gerontol A Biol Sci Med Sci 68, 68-73.
20. ValenteT, Gella A, Fernandez-Busquets X, Unzeta M, Durany N (2010) Immunohistochemical analysis of human brain suggests pathological synergism of Alzheimer's disease and diabetes mellitus. Neurobiol Dis 37, 67-76.
21. Prajapati KD, Sharma SS, Roy N (2011) Current perspectives on potential role of albumin in neuroprotection. Rev Neurosci 22, 355-363.
22. Ahn SM, Byun K, Cho K, Kim JY, Yoo JS, Kim D, Paek SH, Kim SU, Simpson RJ, Lee B (2008) Human microglial cells synthesize albumin in brain. PLoS One 3, e2829.
23. Era S, Kuwata K, Imai H, Nakamura K, Hayashi T, Sogami M (1995) Age-related change in redox state of human serum albumin. Biochim Biophys Acta 1247, 12-16.
24. Biere AL, Ostaszewski B, Stimson ER, Hyman BT, Maggio JE, Selkoe DJ (1996) Amyloid beta-peptide is transported on lipoproteins and albumin in human plasma. J Biol Chem 271, 32916-32922. (Pubitemid 27008725)
25. Marini I, Moschini R, Del CA, Mura U (2005) Chaperonelike features of bovine serum albumin: A comparison with alpha-crystallin. Cell Mol Life Sci 62, 3092-3099. (Pubitemid 43004757)
26. Bohrmann B, Tjernberg L, Kuner P, Poli S, Levet-Trafit B, Naslund J, Richards G, Huber W, Dobeli H, Nordstedt C (1999) Endogenous proteins controlling amyloid beta-peptide polymerization Possible implications for beta-amyloid formation in the central nervous system and in peripheral tissues. J Biol Chem 274, 15990-15995.
27. Ghesquiere B, Goethals M, Van DJ, Staes A, Timmerman E, Vandekerckhove J, Gevaert K (2006) Improved tandem mass spectrometric characterization of 3-nitrotyrosine sites in peptides. Rapid Commun Mass Spectrom 20, 2885- 2893. (Pubitemid 44526626)
28. Ledesma-Osuna AI, Ramos-Clamont G, Vazquez-Moreno L (2008) Characterization of bovine serum albumin glycated with glucose galactose and lactose. Acta Biochim Pol 55, 491- 497.
29. Pera M, Alcolea D, S'anchez-Valle R, Guardia-Laguarta C, Colom-Cadena M, Badiola N, Su'arez-Calvet M, Llad'o A, Barrera-Ocampo AA, Sepulveda-Falla D, Blesa R, Molinuevo JL, Clarim'on J, Ferrer I, Gelpi E, Lle'o A (2013) Distinct patterns ofAPPprocessing in theCNSin autosomal-dominant and sporadic Alzheimer disease. Acta Neuropathol 125, 201- 213.
30. Grau M, Subirana I, Elosua R, Solanas P, Ramos R, Masia R, Cordon F, Sala J, Juvinya D, Cerezo C, Fito M, Vila J, Covas MI, Marrugat J (2007) Trends in cardiovascular risk factor prevalence (1995-2000-2005) in northeastern Spain. Eur J Cardiovasc Prev Rehabil 14, 653-659. (Pubitemid 47556402)
31. Ahmed N, Thornalley PJ (2002) Chromatographic assay of glycation adducts in human serum albumin glycated in vitro by derivatization with 6-aminoquinolyl-Nhydroxysuccinimidyl- carbamate and intrinsic fluorescence. Biochem J 364, 15-24. (Pubitemid 34538941)
32. Mukohda M, Okada M, Hara Y, Yamawaki H (2012) Exploring mechanisms of diabetes-related macrovascular complications: Role of methylglyoxal, a metabolite of glucose on regulation of vascular contractility. J Pharmacol Sci 118, 303-310.
33. Kouti L, Noroozian M, Akhondzadeh S, Abdollahi M, Javadi MR, Faramarzi MA, Mousavi S, Ghaeli P (2013) Nitric oxide and peroxynitrite serum levels in Parkinson's disease: Correlation of oxidative stress and the severity of the disease. Eur Rev Med Pharmacol Sci 17, 964-970.
34. Bennhold H, Kallee E (1959) Comparative studies on the half-life of I 131-labeled albumins and nonradioactive human serum albumin in a case of analbuminemia. J Clin Invest 38, 863-872.
35. Ozdemir AM, Hopfer U, Rosca MV, Fan XJ, Monnier VM, Weiss MF (2008) Effects of advanced glycation end product modification on proximal tubule epithelial cell processing of albumin. Am J Nephrol 28, 14-24. (Pubitemid 350126489)
36. Subramaniam R, Fan XJ, ScivittaroV,Yang J,HaCE, Petersen CE, Surewicz WK, Bhagavan NV, Weiss MF, Monnier VM (2002) Cellular oxidant stress and advanced glycation endproducts of albumin: Caveats of the dichlorofluorescein assay. Arch Biochem Biophys 400, 15-25. (Pubitemid 34852255)
37. Zoellner H, Siddiqui S, Kelly E, Medbury H (2009) The antiapoptotic activity of albumin for endothelium is inhibited by advanced glycation end products restricting intramolecular movement. Cell Mol Biol Lett 14, 575-586.
38. Lau S, Graham B, Cao N, Boyd BJ, Pouton CW, White PJ (2012) Enhanced extravasation stability and in vivo cardiac gene silencing via in situ siRNA-albumin conjugation. Mol Pharm 9, 71-80.
39. Karmakar N (2001) Interaction of transmural pressure and shear stress in the transport of albumin across the rabbit aortic wall. Atherosclerosis 156, 321-327. (Pubitemid 32522912)
40. Rozga M, Kloniecki M, Jablonowska A, Dadlez M, Bal W (2007) The binding constant for amyloid Abeta40 peptide interaction with human serum albumin. Biochem Biophys Res Commun 364, 714-718. (Pubitemid 350026521)
41. Smith CD, Carney JM, Starke-Reed PE, Oliver CN, Stadtman ER, Floyd RA, Markesbery WR (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc Natl Acad Sci U S A 88, 10540- 10543. (Pubitemid 21915871)
42. Thorns V, Hansen L, Masliah E (1998) nNOS expressing neurons in the entorhinal cortex and hippocampus are affected in patients with Alzheimer's disease. Exp Neurol 150, 14-20. (Pubitemid 28146418)
43. Kuhla B, Luth HJ, Haferburg D, Boeck K, Arendt T, Munch G (2005) Methylglyoxal glyoxal and their detoxification in Alzheimer's disease. Ann NY Acad Sci 1043, 211-216. (Pubitemid 41123908)
44. Byun K, Bayarsaikhan E, Kim D, Kim CY, Mook-Jung I, Paek SH, Kim SU, Yamamoto T, Won MH, Song BJ, Park YM, Lee B (2012) Induction of neuronal death by microglial AGE-albumin: Implications for Alzheimer's disease. PLoS One 7, e37917
45. Foerder CA, Shapiro BM (1977) Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. Proc Natl Acad Sci U S A 74, 4214-4218. (Pubitemid 8228384)
46. Cerami A, Vlassara H, BrownleeM(1987) Glucose and aging. Sci Am 256, 90-96.
47. Friguet B, Bulteau AL, Chondrogianni N, Conconi M, Petropoulos I (2000) Protein degradation by the proteasome and its implications in aging. Ann NY Acad Sci 908, 143-154. (Pubitemid 30462000)
48. Shringarpure R, Davies KJ (2002) Protein turnover by the proteasome in aging and disease. Free Radic Biol Med 32, 1084-1089. (Pubitemid 34603346)
49. Brownlee M, Vlassara H, Cerami A (1983) Nonenzymatic glycosylation reduces the susceptibility of fibrin to degradation by plasmin. Diabetes 32, 680-684. (Pubitemid 13062854)
50. Hipkiss AR (2010) Aging proteotoxicity mitochondria glycation NAD and carnosine: Possible inter-relationships and resolution of the oxygen paradox. Front Aging Neurosci 2, 10.
51. Bourque CW, Oliet SH (1997) Osmoreceptors in the central nervous system. Annu Rev Physiol 59, 601-619. (Pubitemid 27142457)
52. Fleck A, Raines G, Hawker F, Trotter J, Wallace PI, Ledingham IM, Calman KC (1985) Increased vascular permeability: A major cause of hypoalbuminaemia in disease and injury. Lancet 1, 781-784. (Pubitemid 15111938)
53. Kirsch R, Frith L, Black E, Hoffenberg R (1968) Regulation of albumin synthesis and catabolism by alteration of dietary protein. Nature 217, 578-579.
54. Bar-Or D, Rael LT, Lau EP, Rao NK, Thomas GW, Winkler JV,Yukl RL, Kingston RG, CurtisCG(2001) An analog of the human albumin N-terminus (Asp-Ala-His-Lys) prevents formation of copper-induced reactive oxygen species. Biochem Biophys Res Commun 284, 856-862. (Pubitemid 32926747)
55. Stanyon HF, Viles JH (2012) Human serum albumin can regulate amyloid- peptide fiber growth in the brain interstitium: Implications for Alzheimer disease. J Biol Chem 287, 28163- 28168.
56. Curry S, Mandelkow H, Brick P, Franks N (1998) Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites. Nat Struct Biol 5, 827-835. (Pubitemid 28402087)
57. Rubel AA, Ryzhova TA, Antonets KS, Chernoff YO, Galkin A (2013) Identification of PrP sequences essential for the interaction between the PrP polymers and A peptide in a yeast-based assay. Prion 7, doi: 10.4161/pri.26867
58. Younan ND, Sarell CJ, Davies P, Brown DR, Viles JH (2013) The cellular prion protein traps Alzheimer's A in an oligomeric form and disassembles amyloid fibers. FASEB J 27, 1847-1858.