Presenilin-1 adopts pathogenic conformation in normal aging and in sporadic Alzheimer's disease

Acta Neuropathologica

Volumn 125, Issue 2, 2013, Pages 187-199

  Wahlster, Lara ^a,b   Arimon, Muriel ^a   Nasser Ghodsi, Navine ^a   Post, Kathryn Leigh ^a   Serrano Pozo, Alberto ^a   Uemura, Kengo ^a   Berezovska, Oksana ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Aging; Alzheimer's disease; Amyloid beta; Oxidative stress; Presenilin 1

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; GAMMA SECRETASE; PRESENILIN 1;

AGE; AGED; AGING; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO; FAMILIAL DISEASE; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MALE; MOLECULAR PATHOLOGY; MOUSE; MUTANT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SPORADIC ALZHEIMER DISEASE; WILD TYPE;

AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELLS, CULTURED; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; NEURONS; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; PRESENILIN-1; PROTEIN CONFORMATION;

EID: 84878847155     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-012-1065-6     Document Type: Article

References (73)

1. Annaert WG, Esselens C, Baert V et al (2001) Interaction with telencephalin and the amyloid precursor protein predicts a ring structure for presenilins. Neuron 32(4):579-589
2. Arriagada PV, Marzloff K, Hyman BT (1992) Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology 42(9):1681-1688
3. Berezovska O, Frosch M, McLean P et al (1999) The Alzheimer-related gene presenilin 1 facilitates notch 1 in primary mammalian neurons. Brain Res Mol Brain Res 69(2):273-280
4. Berezovska O, Lleo A, Herl LD et al (2005) Familial Alzheimer's disease presenilin 1 mutations cause alterations in the conformation of presenilin and interactions with amyloid precursor protein. J Neurosci 25(11):3009-3017
5. Borchelt DR, Thinakaran G, Eckman CB et al (1996) Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo. Neuron 17(5):1005-1013
6. Bosco DA, Morfini G, Karabacak NM et al (2010) Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nature Neurosci 13(11):1396-1403
7. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropath 82(4):239-259
8. Brown GC, Bal-Price A (2003) Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria. Mol Neurobiol 27(3):325-355
9. Burke WJ, Roccaforte WH, Wengel SP et al (1993) L-deprenyl in the treatment of mild dementia of the Alzheimer type: results of a 15-month trial. J Am Geriatr Soc 41(11):1219-1225
10. Butterfield DA, Reed T, Sultana R (2011) Roles of 3-nitrotyrosine- and 4-hydroxynonenal-modified brain proteins in the progression and pathogenesis of Alzheimer's disease. Free Radical Res 45(1):59-72
11. Citron M, Westaway D, Xia W et al (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nature Med 3(1):67-72
12. Cutler RG, Kelly J, Storie K et al (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc Natl Acad Sci USA 101(7):2070-2075
13. De Strooper B, Saftig P, Craessaerts K et al (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391(6665):387-390
14. De Strooper B, Vassar R, Golde T (2010) The secretases: enzymes with therapeutic potential in Alzheimer disease. Nat Rev Neurol 6(2):99-107
15. DeKosky ST, Scheff SW (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 27(5):457-464
16. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408(6809):239-247
17. Galasko DR, Peskind E, Clark CM et al (2012) Antioxidants for Alzheimer disease: a randomized clinical trial with cerebrospinal fluid biomarker measures. Arch Neurol 69(7):836-841
18. Garcia-Alloza M, Dodwell SA, Meyer-Luehmann M et al (2006) Plaque-derived oxidative stress mediates distorted neurite trajectories in the Alzheimer mouse model. J Neuropathol Exp Neurol 65(11):1082-1089
19. Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, Parisi JE, Hyman BT (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. J Neuropathol Exp Neurol 65(11):1082-1089
20. Gomez-Isla T, Price JL, McKeel DW et al (1996) Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16(14):4491-4500
21. Guareschi S, Cova E, Cereda C et al (2012) An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1. Proc Natl Acad Sci USA 109(13):5074-5079
22. Guix FX, Wahle T, Vennekens K et al (2012) Modification of gamma-secretase by nitrosative stress links neuronal aging to sporadic Alzheimer's disease. EMBO Mol Med 4(7):660-673
23. Gwon AR, Park JS, Arumugam TV et al. (2012) Oxidative lipid modification of nicastrin enhances amyloidogenic gamma-secretase activity in Alzheimer's disease. Aging Cell 11(4):559-568
24. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Aging Cell 11(4):559-568
25. Hsiao K, Chapman P, Nilsen S et al (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274(5284):99-102
26. Hyman BT (2011) Amyloid-dependent and amyloid-independent stages of Alzheimer disease. Arch Neurol 68(8):1062-1064
27. Ingelsson M, Fukumoto H, Newell KL et al (2004) Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 62(6):925-931
28. Isoo N, Sato C, Miyashita H et al (2007) Abeta42 overproduction associated with structural changes in the catalytic pore of gamma-secretase: common effects of Pen-2 N-terminal elongation and fenofibrate. J Biol Chem 282(17):12388-12396
29. Jack CR Jr, Lowe VJ, Weigand SD et al (2009) Serial PIB and MRI in normal, mild cognitive impairment and Alzheimer's disease: implications for sequence of pathological events in Alzheimer's disease. Brain 132(Pt 5):1355-1365
30. Jones PB, Rozkalne A, Meyer-Luehmann M et al (2008) Two postprocessing techniques for the elimination of background autofluorescence for fluorescence lifetime imaging microscopy. J Biomed Opt 13(1):014008
31. Josephs KA (2008) Frontotemporal dementia and related disorders: deciphering the enigma. Ann Neurol 64(1):4-14
32. Kakuda N, Akazawa K, Hatsuta H et al (2012) Suspected limited efficacy of gamma-secretase modulators. Neurobiol Aging. doi: 10.1016/j.neurobiolaging. 2012.08.017
33. Kawarabayashi T, Younkin LH, Saido TC et al (2001) Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21(2):372-381
34. Kertesz A, McMonagle P, Blair M et al (2005) The evolution and pathology of frontotemporal dementia. Brain 128(Pt 9):1996-2005
35. Koffie RM, Meyer-Luehmann M, Hashimoto T et al (2009) Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci USA 106(10):4012-4017
36. Kuchibhotla KV, Goldman ST, Lattarulo CR et al (2008) Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron 59(2):214-225
37. Kuperstein I, Broersen K, Benilova I et al (2010) Neurotoxicity of Alzheimer's disease Abeta peptides is induced by small changes in the Abeta42 to Abeta40 ratio. EMBO J 29(19):3408-3420
38. Lakowicz JR (1988) Principles of frequency-domain fluorescence spectroscopy and applications to cell membranes. Sub-cellular Biochem 13:89-126
39. Lakowicz JR, Szmacinski H, Nowaczyk K et al (1992) Fluorescence lifetime imaging. Anal Biochem 202(2):316-330
40. Lesne S, Koh MT, Kotilinek L et al (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440(7082):352-357
41. Lewczuk P, Esselmann H, Otto M et al (2004) Neurochemical diagnosis of Alzheimer's dementia by CSF Abeta42, Abeta42/Abeta40 ratio and total tau. Neurobiol Aging 25(3):273-281
42. Lleo A, Berezovska O, Herl L et al (2004) Nonsteroidal anti-inflammatory drugs lower Abeta42 and change presenilin 1 conformation. Nature Med 10(10):1065-1066
43. Lovell MA, Markesbery WR (2007) Oxidative damage in mild cognitive impairment and early Alzheimer's disease. J Neurosci Res 85(14):3036-3040
44. Mackenzie IR, Neumann M, Bigio EH et al (2010) Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: an update. Acta Neuropathol 119(1):1-4
45. Masliah E, Mallory M, Hansen L et al (1993) Quantitative synaptic alterations in the human neocortex during normal aging. Neurology 43(1):192-197
46. McKhann G, Drachman D, Folstein M et al (1984) Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 34(7):939-944
47. McKhann GM, Albert MS, Grossman M et al (2001) Clinical and pathological diagnosis of frontotemporal dementia: report of the Work Group on frontotemporal dementia and Pick's disease. Archives Neurol 58(11):1803-1809
48. McKhann GM, Knopman DS, Chertkow H et al (2011) The diagnosis of dementia due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's Dement 7(3):263-269
49. McLellan ME, Kajdasz ST, Hyman BT, Bacskai BJ (2003) In vivo imaging of reactive oxygen species specifically associated with thioflavine S-positive amyloid plaques by multiphoton microscopy. J Neurosci 23(6):2212-2217
50. Morishima-Kawashima M, Ihara Y (2002) Alzheimer's disease: beta-Amyloid protein and tau. J Neurosci Res 70(3):392-401
51. NIA-RI (1997) Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Neurobiol Aging 18(4 Suppl):S1-S2
52. Placanica L, Zhu L, Li YM (2009) Gender- and age-dependent gamma-secretase activity in mouse brain and its implication in sporadic Alzheimer disease. PLoS One 4(4):e5088
53. Pratico D, Uryu K, Leight S et al (2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci 21(12):4183-4187
54. Rodrigue KM, Kennedy KM, Park DC (2009) Beta-amyloid deposition and the aging brain. Neuropsychol Rev 19(4):436-450
55. Saito T, Suemoto T, Brouwers N et al (2011) Potent amyloidogenicity and pathogenicity of Abeta43. Nat Neurosci 14(8):1023-1032
56. Sano M, Ernesto C, Thomas RG et al (1997) A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer's disease. The Alzheimer's disease Cooperative Study. NE J Med 336(17):1216-1222
57. Savonenko A, Xu GM, Melnikova T et al (2005) Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 18(3):602-617
58. Sayre LM, Zelasko DA, Harris PL et al (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J Neurochem 68(5):2092-2097
59. Scheuner D, Eckman C, Jensen M et al (1996) Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nature Med 2(8):864-870
60. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81(2):741-766
61. Serneels L, Van Biervliet J, Craessaerts K et al (2009) gamma-Secretase heterogeneity in the Aph1 subunit: relevance for Alzheimer's disease. Science 324(5927):639-642
62. Serrano-Pozo A, Mielke ML, Gomez-Isla T et al (2011) Reactive glia not only associates with plaques but also parallels tangles in Alzheimer's disease. Amer J Pathol 179(3):1373-1384
63. Sultana R, Butterfield DA (2010) Role of oxidative stress in the progression of Alzheimer's disease. J Alzheimer's Dis: JAD 19(1):341-353
64. Terry RD, Masliah E, Salmon DP et al (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30(4):572-580
65. Texido L, Martin-Satue M, Alberdi E et al (2011) Amyloid beta peptide oligomers directly activate NMDA receptors. Cell Calcium 49(3):184-190
66. Thinakaran G, Borchelt DR, Lee MK et al (1996) Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17(1):181-190
67. Uemura K, Farner KC, Nasser-Ghodsi N et al (2011) Reciprocal relationship between APP positioning relative to the membrane and PS1 conformation. Mol Neurodegener 6(1):15
68. Uemura K, Lill CM, Li X, Peters JA et al (2009) Allosteric modulation of PS1/gamma-secretase conformation correlates with amyloid beta (42/40) ratio. PLoS One 4(11):e7893
69. Williams TI, Lynn BC, Markesbery WR, Lovell MA (2006) Increased levels of 4-hydroxynonenal and acrolein, neurotoxic markers of lipid peroxidation, in the brain in Mild Cognitive Impairment and early Alzheimer's disease. Neurobiol Aging 27(8):1094-1099
70. Wiltfang J, Esselmann H, Bibl M et al (2007) Amyloid beta peptide ratio 42/40 but not A beta 42 correlates with phospho-Tau in patients with low- and high-CSF A beta 40 load. J Neurochem 101(4):1053-1059
71. Wolfe MS (2007) When loss is gain: reduced presenilin proteolytic function leads to increased Abeta42/Abeta40. Talking Point on the role of presenilin mutations in Alzheimer disease. EMBO Rep 8(2):136-140
72. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS et al (1999) Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 398(6727):513-517
73. Yanagida K, Okochi M, Tagami S et al (2009) The 28-amino acid form of an APLP1-derived Abeta-like peptide is a surrogate marker for Abeta42 production in the central nervous system. EMBO Mol Med 1(4):223-235