Differential expression and redox proteomics analyses of an Alzheimer disease transgenic mouse model: Effects of the amyloid-β peptide of amyloid precursor protein

Neuroscience

Volumn 177, Issue , 2011, Pages 207-222

  Robinson, R A S ^a,e   Lange, M B ^a   Sultana, R ^a   Galvan, V ^b,f   Fombonne, J ^b   Gorostiza, O ^b   Zhang, J ^b   Warrier, G ^a   Cai, J ^c   Pierce, W M ^c   Bredesen, D E ^b,d   Butterfield, D A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF PITTSBURGH   (United States)

^f Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Alzheimer disease; Amyloid peptide; Expression proteomics; Redox proteomics; Transgenic mouse model of Alzheimer disease

Indexed keywords

3 NITROTYROSINE; ALPHA ENOLASE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BINDING PROTEIN; CALCINEURIN; CALCINEURIN SUBUNIT B TYPE 1; CHAPERONIN CONTAINING TCP1; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1; MESSENGER RNA; PEPTIDYLPROLYL ISOMERASE PIN1; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN 1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE ALPHA; T COMPLEX PROTEIN 1 SUBUNIT ALPHA A; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN TISSUE; CONTROLLED STUDY; IMMUNOPRECIPITATION; MALE; MOUSE; NEUROPATHOLOGY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEOMICS; SIGNAL TRANSDUCTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTEOME; PROTEOMICS;

EID: 79952009348     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.01.005     Document Type: Article

References (83)

1. Abdul H.M., Sama M.A., Furman J.L., Mathis D.M., Beckett T.L., Weidner A.M., Patel E.S., Baig I., Murphy M.P., LeVine H., Kraner S.D., Norris C.M. Cognitive decline in Alzheimer's disease is associated with selective changes in calcineurin/NFAT signaling. J Neurosci 2009, 29:12957-12969.
2. Abdul H.M., Sultana R., St Clair D.K., Markesbery W.R., Butterfield D.A. Oxidative damage in brain from human mutant APP/PS-1 double knock-in mice as a function of age. Free Radic Biol Med 2008, 45:1420-1425.
3. Agostinho P., Lopes J.P., Velez Z., Oliveira C.R. Overactivation of calcineurin induced by amyloid-β and prion proteins. Neurochem Int 2008, 52:1226-1233.
4. Aitken A., Klee C.B., Cohen P. The structure of the B subunit of calcineurin. Eur J Biochem 1984, 139:663-671.
5. Ansari M.A., Joshi G., Huang Q., Opii W.O., Abdul H.M., Sultana R., Butterfield D.A. In vivo administration of D609 leads to protection of subsequently isolated gerbil brain mitochondria subjected to in vitro oxidative stress induced by amyloid β-peptide and other oxidative stressors: relevance to Alzheimer's disease and other oxidative stress-related neurodegenerative disorders. Free Radic Biol Med 2006, 41:1694-1703.
6. Blacker D., Wilcox M.A., Laird N.M., Rodes L., Horvath S.M., Go R.C., Perry R., Watson B., Bassett S.S., McInnis M.G., Albert M.S., Hyman B.T., Tanzi R.E. α2-macroglobulin is genetically associated with Alzheimer disease. Nat Genet 1998, 19:357-360.
7. Blass J.P., Gibson G.E., Hoyer S. The role of the metabolic lesion in Alzheimer's disease. J Alzheimers Dis 2002, 4:225-232.
8. Boyd-Kimball D., Castegna A., Sultana R., Poon H.F., Petroze R., Lynn B.C., Klein J.B., Butterfield D.A. Proteomic identification of proteins oxidized by Aβ(1-42) in synaptosomes: implications for Alzheimer's disease. Brain Res 2005, 1044:206-215.
9. Boyd-Kimball D., Mohmmad Abdul H., Reed T., Sultana R., Butterfield D.A. Role of phenylalanine 20 in Alzheimer's amyloid β-peptide (1-42)-induced oxidative stress and neurotoxicity. Chem Res Toxicol 2004, 17:1743-1749.
10. Boyd-Kimball D., Sultana R., Mohmmad-Abdul H., Butterfield D.A. Neurotoxicity and oxidative stress in D1M-substituted Alzheimer's Aβ(1-42): relevance to N-terminal methionine chemistry in small model peptides. Peptides 2005, 26:665-673.
11. Boyd-Kimball D., Sultana R., Poon H.F., Lynn B.C., Casamenti F., Pepeu G., Klein J.B., Butterfield D.A. Proteomic identification of proteins specifically oxidized by intracerebral injection of amyloid β-peptide (1-42) into rat brain: implications for Alzheimer's disease. Neuroscience 2005, 132:313-324.
12. Brown C.R., Doxsey S.J., Hong-Brown L.Q., Martin R.L., Welch W.J. Molecular chaperones and the centrosome. A role for TCP-1 in microtubule nucleation. J Biol Chem 1996, 271:824-832.
13. Bubber P., Haroutunian V., Fisch G., Blass J.P., Gibson G.E. Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann Neurol 2005, 57:695-703.
14. Butterfield D.A., Abdul H.M., Opii W., Newman S.F., Joshi G., Ansari M.A., Sultana R. Pin-1 in Alzheimer's disease. J Neurochem 2006, 98:1697-1706.
15. Butterfield D.A., Boyd-Kimball D. Amyloid β-peptide(1-42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain Pathol 2004, 14:426-432.
16. Butterfield D.A., Galvan V., Lange M.B., Tang H., Sowell R.A., Spilman P., Fombonne J., Gorostiza O., Zhang J., Sultana R., Bredesen D.E. In vivo oxidative stress in brain of Alzheimer disease transgenic mice: requirement for methionine 35 in amyloid β-peptide of APP. Free Radic Biol Med 2010, 48:136-144.
17. Butterfield D.A., Lange M.L. Multifunctional roles of enolase in Alzheimer's disease brain: beyond altered glucose metabolism. J Neurochem 2009, 111:915-933.
18. Butterfield D.A., Lauderback C.M. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid β-peptide-associated free radical oxidative stress. Free Radic Biol Med 2002, 32:1050-1060.
19. Butterfield D.A., Perluigi M., Sultana R. Oxidative stress in Alzheimer's disease brain: new insights from redox proteomics. Eur J Pharmacol 2006, 545:39-50.
20. Butterfield D.A., Stadtman E.R. Protein oxidation processes in aging brain. Adv Cell Aging Gerontol 1997, 2:161-191.
21. Butterfield D.A., Sultana R. Identification of 3-nitrotyrosine-modified brain proteins by redox proteomics. Methods Enzymol 2008, 440:295-308.
22. Castegna A., Aksenov M., Aksenova M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., Butterfield D.A. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 2002, 33:562-571.
23. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., Butterfield D.A. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, α-enolase, and heat shock cognate 71. J Neurochem 2002, 82:1524-1532.
24. Castegna A., Thongboonkerd V., Klein J.B., Lynn B., Markesbery W.R., Butterfield D.A. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem 2003, 85:1394-1401.
25. Celsi F., Svedberg M., Unger C., Cotman C.W., Carri M.T., Ottersen O.P., Nordberg A., Torp R. β-amyloid causes downregulation of calcineurin in neurons through induction of oxidative stress. Neurobiol Dis 2007, 26:342-352.
26. Chen Q., Wang S., Thompson S.N., Hall E.D., Guttmann R.P. Identification and characterization of PEBP as a calpain substrate. J Neurochem 2006, 99:1133-1141.
27. Chen X., Sullivan D.S., Huffaker T.C. Two yeast genes with similarity to TCP-1 are required for microtubule and actin function in vivo. Proc Natl Acad Sci U S A 1994, 91:9111-9115.
28. Cruts M., van Duijn C.M., Backhovens H., Van den Broeck M., Wehnert A., Serneels S., Sherrington R., Hutton M., Hardy J., St George-Hyslop P.H., Hofman A., Van Broeckhoven C. Estimation of the genetic contribution of presenilin-1 and -2 mutations in a population-based study of presenile Alzheimer disease. Hum Mol Genet 1998, 7:43-51.
29. Dahiyat M., Cumming A., Harrington C., Wischik C., Xuereb J., Corrigan F., Breen G., Shaw D., St Clair D. Association between Alzheimer's disease and the NOS3 gene. Ann Neurol 1999, 46:664-667.
30. Demuro A., Mina E., Kayed R., Milton S.C., Parker I., Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J Biol Chem 2005, 280:17294-17300.
31. Drake J., Link C.D., Butterfield D.A. Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid β-peptide (1-42) in a transgenic Caenorhabditis elegans model. Neurobiol Aging 2003, 24:415-420.
32. Foster T.C., Sharrow K.M., Masse J.R., Norris C.M., Kumar A. Calcineurin links Ca2+ dysregulation with brain aging. J Neurosci 2001, 21:4066-4073.
33. Galvan V., Gorostiza O.F., Banwait S., Ataie M., Logvinova A.V., Sitaraman S., Carlson E., Sagi S.A., Chevallier N., Jin K., Greenberg D.A., Bredesen D.E. Reversal of Alzheimer's-like pathology and behavior in human APP transgenic mice by mutation of Asp664. Proc Natl Acad Sci U S A 2006, 103:7130-7135.
34. Goate A., Chartier-Harlin M.C., Mullan M., Brown J., Crawford F., Fidani L., Giuffra L., Haynes A., Irving N., James L., et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 1991, 349:704-706.
35. Good P.F., Werner P., Hsu A., Olanow C.W., Perl D.P. Evidence of neuronal oxidative damage in Alzheimer's disease. Am J Pathol 1996, 149:21-28.
36. Goto S., Matsukado Y., Mihara Y., Inoue N., Miyamoto E. Calcineurin in human brain and its relation to extrapyramidal system. Immunohistochemical study on postmortem human brains. Acta Neuropathol 1986, 72:150-156.
37. Gupta R.S. Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol Microbiol 1995, 15:1-11.
38. Hata R., Masumura M., Akatsu H., Li F., Fujita H., Nagai Y., Yamamoto T., Okada H., Kosaka K., Sakanaka M., Sawada T. Up-regulation of calcineurin Aβ mRNA in the Alzheimer's disease brain: assessment by cDNA microarray. Biochem Biophys Res Commun 2001, 284:310-316.
39. Hemenway C.S., Heitman J. Calcineurin. Structure, function, and inhibition. Cell Biochem Biophys 1999, 30:115-151.
40. Hsia A.Y., Masliah E., McConlogue L., Yu G.Q., Tatsuno G., Hu K., Kholodenko D., Malenka R.C., Nicoll R.A., Mucke L. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci U S A 1999, 96:3228-3233.
41. Joerchel S., Raap M., Bigl M., Eschrich K., Schliebs R. Oligomeric β-amyloid(1-42) induces the expression of Alzheimer disease-relevant proteins in cholinergic SN56B5. G4 cells as revealed by proteomic analysis. Int J Dev Neurosci 2008, 26:301-308.
42. Klee C.B., Ren H., Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 1998, 273:13367-13370.
43. Lee M.S., Tsai L.H. Cdk5: one of the links between senile plaques and neurofibrillary tangles?. J Alzheimers Dis 2003, 5:127-137.
44. Levy-Lahad E., Lahad A., Wijsman E.M., Bird T.D., Schellenberg G.D. Apolipoprotein E genotypes and age of onset in early-onset familial Alzheimer's disease. Ann Neurol 1995, 38:678-680.
45. Lian Q., Ladner C.J., Magnuson D., Lee J.M. Selective changes of calcineurin (protein phosphatase 2B) activity in Alzheimer's disease cerebral cortex. Exp Neurol 2001, 167:158-165.
46. Lu K.P., Liou Y.C., Vincent I. Proline-directed phosphorylation and isomerization in mitotic regulation and in Alzheimer's disease. Bioessays 2003, 25:174-181.
47. Maillet M., Robert S.J., Cacquevel M., Gastineau M., Vivien D., Bertoglio J., Zugaza J.L., Fischmeister R., Lezoualc'h F. Crosstalk between Rap1 and Rac regulates secretion of sAPPα. Nat Cell Biol 2003, 5:633-639.
48. Maki M., Matsukawa N., Yuasa H., Otsuka Y., Yamamoto T., Akatsu H., Okamoto T., Ueda R., Ojika K. Decreased expression of hippocampal cholinergic neurostimulating peptide precursor protein mRNA in the hippocampus in Alzheimer disease. J Neuropathol Exp Neurol 2002, 61:176-185.
49. Markesbery W.R. Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 1997, 23:134-147.
50. Mattson M.P., Chan S.L. Dysregulation of cellular calcium homeostasis in Alzheimer's disease: bad genes and bad habits. J Mol Neurosci 2001, 17:205-224.
51. Merat D.L., Cheung W.Y. Calmodulin-dependent protein phosphatase: isolation of subunits and reconstitution to holoenzyme. Methods Enzymol 1987, 139:79-87.
52. Mohmmad Abdul H., Sultana R., Keller J.N., St Clair D.K., Markesbery W.R., Butterfield D.A. Mutations in amyloid precursor protein and presenilin-1 genes increase the basal oxidative stress in murine neuronal cells and lead to increased sensitivity to oxidative stress mediated by amyloid β-peptide (1-42), H2O2 and kainic acid: implications for Alzheimer's disease. J Neurochem 2006, 96:1322-1335.
53. Mohmmad Abdul H., Wenk G.L., Gramling M., Hauss-Wegrzyniak B., Butterfield D.A. APP and PS-1 mutations induce brain oxidative stress independent of dietary cholesterol: implications for Alzheimer's disease. Neurosci Lett 2004, 368:148-150.
54. Mucke L., Masliah E., Yu G.Q., Mallory M., Rockenstein E.M., Tatsuno G., Hu K., Kholodenko D., Johnson-Wood K., McConlogue L. High-level neuronal expression of Aβ 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 2000, 20:4050-4058.
55. Norris C.M., Kadish I., Blalock E.M., Chen K.C., Thibault V., Porter N.M., Landfield P.W., Kraner S.D. Calcineurin triggers reactive/inflammatory processes in astrocytes and is up-regulated in aging and Alzheimer's models. J Neurosci 2005, 25:4649-4658.
56. Ojika K. [Hippocampal cholinergic neurostimulating peptide]. Seikagaku 1998, 70:1175-1180.
57. Owen J.B., Di Domenico F., Sultana R., Perluigi M., Cini C., Pierce W.M., Butterfield D.A. Proteomics-determined differences in the concanavalin-A-fractionated proteome of hippocampus and inferior parietal lobule in subjects with Alzheimer's disease and mild cognitive impairment: implications for progression of AD. J Proteome Res 2009, 8:471-482.
58. Pappolla M.A., Chyan Y.J., Poeggeler B., Bozner P., Ghiso J., LeDoux S.P., Wilson G.L. Alzheimer β protein mediated oxidative damage of mitochondrial DNA: prevention by melatonin. J Pineal Res 1999, 27:226-229.
59. Pastorino L., Sun A., Lu P.J., Zhou X.Z., Balastik M., Finn G., Wulf G., Lim J., Li S.H., Li X., Xia W., Nicholson L.K., Lu K.P. The prolyl isomerase Pin-1 regulates amyloid precursor protein processing and amyloid-β production. Nature 2006, 440:528-534.
60. Price D.L., Tanzi R.E., Borchelt D.R., Sisodia S.S. Alzheimer's disease: genetic studies and transgenic models. Annu Rev Genet 1998, 32:461-493.
61. Resende R., Moreira P.I., Proenca T., Deshpande A., Busciglio J., Pereira C., Oliveira C.R. Brain oxidative stress in a triple-transgenic mouse model of Alzheimer disease. Free Radic Biol Med 2008, 44:2051-2057.
62. Schagger H., Ohm T.G. Human diseases with defects in oxidative phosphorylation. 2. F1F0 ATP-synthase defects in Alzheimer disease revealed by blue native polyacrylamide gel electrophoresis. Eur J Biochem 1995, 227:916-921.
63. Schuller E., Gulesserian T., Seidl R., Cairns N., Lube G. Brain T-complex polypeptide 1 (TCP- 1) related to its natural substrate β1 tubulin is decreased in Alzheimer's disease. Life Sci 2001, 69:263-270.
64. Selkoe D.J. Amyloid β-protein and the genetics of Alzheimer's disease. J Biol Chem 1996, 271:18295-18298.
65. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001, 81:741-766.
66. Selkoe D.J. Soluble oligomers of the amyloid β-protein impair synaptic plasticity and behavior. Behav Brain Res 2008, 192:106-113.
67. Shankar G.M., Leissring M.A., Adame A., Sun X., Spooner E., Masliah E., Selkoe D.J., Lemere C.A., Walsh D.M. Biochemical and immunohistochemical analysis of an Alzheimer's disease mouse model reveals the presence of multiple cerebral Abeta assembly forms throughout life. Neurobiol Dis 2009, 36:293-302.
68. Slooter A.J., Cruts M., Kalmijn S., Hofman A., Breteler M.M., Van Broeckhoven C., van Duijn C.M. Risk estimates of dementia by apolipoprotein E genotypes from a population-based incidence study: the Rotterdam Study. Arch Neurol 1998, 55:964-968.
69. Smith M.A., Richey Harris P.L., Sayre L.M., Beckman J.S., Perry G. Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 1997, 17:2653-2657.
70. Smith M.A., Richey P.L., Taneda S., Kutty R.K., Sayre L.M., Monnier V.M., Perry G. Advanced Maillard reaction end products, free radicals, and protein oxidation in Alzheimer's disease. Ann N Y Acad Sci 1994, 738:447-454.
71. Sultana R., Boyd-Kimball D., Cai J., Pierce W.M., Klein J.B., Merchant M., Butterfield D.A. Proteomics analysis of the Alzheimer's disease hippocampal proteome. J Alzheimers Dis 2007, 11:153-164.
72. Sultana R., Boyd-Kimball D., Poon H.F., Cai J., Pierce W.M., Klein J.B., Markesbery W.R., Zhou X.Z., Lu K.P., Butterfield D.A. Oxidative modification and down-regulation of Pin-1 in Alzheimer's disease hippocampus: a redox proteomics analysis. Neurobiol Aging 2006, 27:918-925.
73. Sultana R., Boyd-Kimball D., Poon H.F., Cai J., Pierce W.M., Klein J.B., Merchant M., Markesbery W.R., Butterfield D.A. Redox proteomics identification of oxidized proteins in Alzheimer's disease hippocampus and cerebellum: an approach to understand pathological and biochemical alterations in AD. Neurobiol Aging 2006, 27:1564-1576.
74. Sultana R., Poon H.F., Cai J., Pierce W.M., Merchant M., Klein J.B., Markesbery W.R., Butterfield D.A. Identification of nitrated proteins in Alzheimer's disease brain using a redox proteomics approach. Neurobiol Dis 2006, 22:76-87.
75. Sultana R., Ravagna A., Mohmmad-Abdul H., Calabrese V., Butterfield D.A. Ferulic acid ethyl ester protects neurons against amyloid β-peptide(1-42)-induced oxidative stress and neurotoxicity: relationship to antioxidant activity. J Neurochem 2005, 92:749-758.
76. Thongboonkerd V., Luengpailin J., Cao J., Pierce W.M., Cai J., Klein J.B., Doyle R.J. Fluoride exposure attenuates expression of Streptococcus pyogenes virulence factors. J Biol Chem 2002, 277:16599-16605.
77. Ursic D., Sedbrook J.C., Himmel K.L., Culbertson M.R. The essential yeast Tcp1 protein affects actin and microtubules. Mol Biol Cell 1994, 5:1065-1080.
78. Viola K.L., Velasco P.T., Klein W.L. Why Alzheimer's is a disease of memory: the attack on synapses by Aβ oligomers (ADDLs). J Nutr Health Aging 2008, 12:51S-57S.
79. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
80. Watson G.S., Craft S. Modulation of memory by insulin and glucose: neuropsychological observations in Alzheimer's disease. Eur J Pharmacol 2004, 490:97-113.
81. Wu S.K., Zeng K., Wilson I.A., Balch W.E. Structural insights into the function of the Rab GDI superfamily. Trends Biochem Sci 1996, 21:472-476.
82. Yoo B.C., Kim S.H., Cairns N., Fountoulakis M., Lubec G. Deranged expression of molecular chaperones in brains of patients with Alzheimer's disease. Biochem Biophys Res Commun 2001, 280:249-258.
83. Zhu M., Gu F., Shi J., Hu J., Hu Y., Zhao Z. Increased oxidative stress and astrogliosis responses in conditional double-knockout mice of Alzheimer-like presenilin-1 and presenilin-2. Free Radic Biol Med 2008, 45:1493-1499.