Increased in vivo amyloid-b42 production, exchange, and loss in presenilin mutation carriers

Science Translational Medicine

Volumn 5, Issue 189, 2013, Pages

  Potter, Rachel ^a   Patterson, Bruce W ^a   Elbert, Donald L ^b   Ovod, Vitaliy ^a   Kasten, Tom ^a   Sigurdson, Wendy ^a   Mawuenyega, Kwasi ^a   Blazey, Tyler ^a   Goate, Alison ^a   Chott, Robert ^a   Yarasheski, Kevin E ^a   Holtzman, David M ^a   Morris, John C ^a   Benzinger, Tammie L S ^a   Bateman, Randall J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; PITTSBURGH COMPOUND B; PRESENILIN 1; PRESENILIN 2;

ADULT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLINICAL ARTICLE; CONTROLLED STUDY; DEMENTIA; FEMALE; GENE MUTATION; HETEROZYGOTE; HUMAN; KINETICS; MALE; PEDIGREE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN DEPLETION; PROTEIN METABOLISM; PROTEIN SECRETION; PSEN1 GENE; PSEN2 GENE;

ADULT; ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; FEMALE; HUMANS; MALE; MIDDLE AGED; MUTATION; POSITRON-EMISSION TOMOGRAPHY; PRESENILINS;

EID: 84880525521     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005615     Document Type: Article

References (44)

1. R. J. Bateman, P. S. Aisen, B. De Strooper, N. C. Fox, C. A. Lemere, J. M. Ringman, S. Salloway, R. A. Sperling, M. Windisch, C. Xiong, Autosomal-dominant Alzheimer's disease: A review and proposal for the prevention of Alzheimer's disease. Alzheimers Res. Ther. 3, 1 (2011).
2. R. J. Bateman, C. Xiong, T. L. S. Benzinger, A. M. Fagan, A.Goate,N. C. Fox,D. S. Marcus,N. J. Cairns, X. Xie, T. M. Blazey, D. M. Holtzman, A. Santacruz, V. Buckles, A. Oliver, K. Moulder, P. S. Aisen, B. Ghetti, W. E. Klunk, E. McDade, R. N. Martins, C. L. Masters, R. Mayeux, J. M. Ringman, M. N. Rossor, P. R. Schofield, R. A. Sperling, S. Salloway, J. C. Morris, Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N. Engl. J. Med. 367, 795-804 (2012).
3. J. Hardy, D. J. Selkoe, The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356 (2002).
4. C. Haass, B. De Strooper, The presenilins in Alzheimer's disease - Proteolysis holds the key. Science 286, 916-919 (1999).
5. R. Wang, D. Sweeney, S. E. Gandy, S. S. Sisodia, The profile of soluble amyloid b protein in cultured cell media. Detection and quantification of amyloid b protein and variants by immunoprecipitation-mass spectrometry. J. Biol. Chem. 271, 31894-31902 (1996).
6. D. L. Miller, I. A. Papayannopoulos, J. Styles, S. A. Bobin, Y. Y. Lin, K. Biemann, K. Iqbal, Peptide compositions of the cerebrovascular and senile plaque core amyloid deposits of Alzheimer's disease. Arch. Biochem. Biophys. 301, 41-52 (1993).
7. T. Jonsson, J. K. Atwal, S. Steinberg, J. Snaedal, P. V. Jonsson, S. Bjornsson, H. Stefansson, P. Sulem, D. Gudbjartsson, J. Maloney, K. Hoyte, A. Gustafson, Y. Liu, Y. Lu, T. Bhangale, R. R. Graham, J. Huttenlocher, G. Bjornsdottir, O. A. Andreassen, E. G. Jönsson, A. Palotie, T. W. Behrens, O. T. Magnusson, A. Kong, U. Thorsteinsdottir, R. J. Watts, K. Stefansson, A mutation in APP protects against Alzheimer's disease and age-related cognitive decline. Nature 488, 96-99 (2012).
8. A. Rovelet-Lecrux, D. Hannequin, G. Raux, N. L. Meur, A. Laquerrière, A. Vital, C. Dumanchin, S. Feuillette, A. Brice, M. Vercelletto, F. Dubas, T. Frebourg, D. Campion, APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat. Genet. 38, 24-26 (2006).
9. A. Goate, M.-C. Chartier-Harlin, M. Mullan, J. Brown, F. Crawford, L. Fidani, L. Giuffra, A. Haynes, N. Irving, L. James, R. Mant, P. Newton, K. Rooke, P. Roques, C. Talbot, M. Pericak-Vance, A. Roses, R. Williamson, M. Rossor, M. Owen, J. Hardy, Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349, 704-706 (1991).
10. E. Levy-Lahad, E. M. Wijsman, E. Nemens, L. Anderson, K. A. Goddard, J. L. Weber, T. D. Bird, G. D. Schellenberg, A familial Alzheimer's disease locus on chromosome 1. Science 269, 970-973 (1995).
11. D. Scheuner, C. Eckman, M. Jensen, X. Song, M. Citron, N. Suzuki, T. D. Bird, J. Hardy, M. Hutton, W. Kukull, E. Larson, E. Levy-Lahad, M. Viitanen, E. Peskind, P. Poorkaj, G. Schellenberg, R. Tanzi, W. Wasco, L. Lannfelt, D. Selkoe, S. Younkin, Secreted amyloid b-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. Nat. Med. 2, 864-870 (1996).
12. D. R. Borchelt, G. Thinakaran, C. B. Eckman, M. K. Lee, F. Davenport, T. Ratovitsky, C.-M. Prada, G. Kim, S. Seekins, D. Yager, H. H. Slunt, R.Wang,M.Seeger, A. I. Levey,S. E. Gandy,N. G. Copeland, N. A. Jenkins, D. L. Price, S. G. Younkin, S. S. Sisodia, Familial Alzheimer's disease-linked presenilin 1 variants elevate Ab1-42/1-40 ratio in vitro and in vivo. Neuron 17, 1005-1013 (1996).
13. J. M. Ringman, S. G. Younkin, D. Pratico, W. Seltzer, G. M. Cole, D. H. Geschwind, Y. Rodriguez- Agudelo, B. Schaffer, J. Fein, S. Sokolow, E. R. Rosario, K. H. Gylys, A. Varpetian, L. D. Medina, J. L. Cummings, Biochemical markers in persons with preclinical familial Alzheimer disease. Neurology 71, 85-92 (2008).
14. J. S. Kauwe, S. Jacquart, S. Chakraverty, J.Wang, K.Mayo, A. M. Fagan, D. M.Holtzman, J. C.Morris, A. M. Goate, Extreme cerebrospinal fluid amyloid b levels identify family with late-onset Alzheimer's disease presenilin 1 mutation. Ann. Neurol. 61, 446-453 (2007).
15. I. Kuperstein, K. Broersen, I. Benilova, J. Rozenski, W. Jonckheere, M.Debulpaep, A. Vandersteen, I. Segers-Nolten, K. VanDerWerf, V. Subramaniam, D. Braeken, G. Callewaert, C. Bartic, R.D'Hooge, I. C. Martins, F. Rousseau, J. Schymkowitz, B. De Strooper, Neurotoxicity of Alzheimer's diseaseAb peptides is induced by small changes in the Ab42 to Ab40 ratio. EMBO J. 29, 3408-3420 (2010).
16. J. Shioi, A. Georgakopoulos, P. Mehta, Z. Kouchi, C. M. Litterst, L. Baki, N. K. Robakis, FAD mutants unable to increase neurotoxic Ab 42 suggest thatmutation effects on neurodegeneration may be independent of effects on Ab. J. Neurochem. 101, 674-681 (2007).
17. M. Moonis, J. M. Swearer, M. P. Dayaw, P. St George-Hyslop, E. Rogaeva, T. Kawarai, D. A. Pollen, Familial Alzheimer disease: Decreases in CSF Ab42 levels precede cognitive decline. Neurology 65, 323-325 (2005).
18. K. G. Mawuenyega, W. Sigurdson, V. Ovod, L. Munsell, T. Kasten, J. C. Morris, K. E. Yarasheski, R. J. Bateman, Decreased clearance of CNS b-amyloid in Alzheimer's disease. Science 330, 1774 (2010).
19. N. Andreasen, C. Hesse, P. Davidsson, L. Minthon, A. Wallin, B. Winblad, H. Vanderstichele, E. Vanmechelen, K. Blennow, Cerebrospinal fluid b-amyloid(1-42) in Alzheimer disease: Differences between early- and late-onset Alzheimer disease and stability during the course of disease. Arch. Neurol. 56, 673-680 (1999).
20. A. M. Fagan, M. A. Mintun, R. H. Mach, S. Y. Lee, C. S. Dence, A. R. Shah, G. N. LaRossa, M. L. Spinner, W. E. Klunk, C. A. Mathis, S. T. DeKosky, J. C. Morris, D. M. Holtzman, Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Ab42 in humans. Ann. Neurol. 59, 512-519 (2006).
21. G. Nikisch, A. Hertel, B. Kiessling, T. Wagner, D. Krasz, E. Hofmann, G. Wiedemann, Threeyear follow-up of a patient with early-onset Alzheimer's disease with presenilin-2 N141I mutation - Case report and review of the literature. Eur. J. Med. Res. 13, 579-584 (2008).
22. B. De Strooper, Loss-of-function presenilin mutations in Alzheimer disease. Talking Point on the role of presenilin mutations in Alzheimer disease. EMBO Rep. 8, 141-146 (2007).
23. M. A. Mintun, G. N. Larossa, Y. I. Sheline, C. S. Dence, S. Y. Lee, R. H. Mach, W. E. Klunk, C. A. Mathis, S. T. DeKosky, J. C. Morris, [11C]PIB in a nondemented population: Potential antecedent marker of Alzheimer disease. Neurology 67, 446-452 (2006).
24. L. Chávez-Gutiérrez, L. Bammens, I. Benilova, A. Vandersteen,M. Benurwar, M. Borgers, S. Lismont, L. Zhou, S. Van Cleynenbreugel, H. Esselmann, J. Wiltfang, L. Serneels, E. Karran, H. Gijsen, J. Schymkowitz, F. Rousseau, K. Broersen, B. De Strooper, The mechanism of g-secretase dysfunction in familial Alzheimer disease. EMBO J. 31, 2261-2274 (2012).
25. S. Kumar-Singh, J. Theuns, B. Van Broeck, D. Pirici, K. Vennekens, E. Corsmit,M. Cruts, B. Dermaut, R. Wang, C. Van Broeckhoven, Mean age-of-onset of familial Alzheimer disease caused by presenilin mutations correlates with both increased Ab42 and decreased Ab40. Hum. Mutat. 27, 686-695 (2006).
26. J. J. Iliff, M. Wang, Y. Liao, B. A. Plogg, W. Peng, G. A. Gundersen, H. Benveniste, G. E. Vates, R. Deane, S. A. Goldman, E. A. Nagelhus, M. Nedergaard, A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid b. Sci. Transl. Med. 4, 147ra111 (2012).
27. J. R. Cirrito, P. C.May, M.A.O'Dell, J. W. Taylor, M. Parsadanian, J.W. Cramer, J. E. Audia, J. S.Nissen, K. R. Bales, S. M. Paul, R. B. DeMattos, D. M. Holtzman, In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-b metabolism and half-life. J. Neurosci. 23, 8844-8853 (2003).
28. S. Hong, O. Quintero-Monzon, B. L. Ostaszewski, D. R. Podlisny, W. T. Cavanaugh, T. Yang, D. M. Holtzman, J. R. Cirrito, D. J. Selkoe, Dynamic analysis of amyloid b-protein in behaving mice reveals opposing changes in ISF versus parenchymal Ab during age-related plaque formation. J. Neurosci. 31, 15861-15869 (2011).
29. T. Iwatsubo, A. Odaka, N. Suzuki, H. Mizusawa, N. Nukina, Y. Ihara, Visualization of Ab42(43) and Ab40 in senile plaques with end-specific A b monoclonals: Evidence that an initially deposited species is A b 42(43). Neuron 13, 45-53 (1994).
30. T. Grimmer, M. Riemenschneider, H. Förstl, G. Henriksen, W. E. Klunk, C. A. Mathis, T. Shiga, H. J. Wester, A. Kurz, A. Drzezga, Beta amyloid in Alzheimer's disease: Increased deposition in brain is reflected in reduced concentration in cerebrospinal fluid. Biol. Psychiatry 65, 927-934 (2009).
31. M. P. Lambert, A. K. Barlow, B. A. Chromy, C. Edwards, R. Freed, M. Liosatos, T. E. Morgan, I. Rozovsky, B. Trommer, K. L. Viola, P. Wals, C. Zhang, C. E. Finch, G. A. Krafft, W. L. Klein, Diffusible, nonfibrillar ligands derived from Ab1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453 (1998).
32. R. Kayed, E. Head, J. L. Thompson, T. M. McIntire, S. C. Milton, C. W. Cotman, C. G. Glabe, Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003).
33. W. P. Esler, E. R. Stimson, J. M. Jennings, H. V. Vinters, J. R. Ghilardi, J. P. Lee, P. W. Mantyh, J. E. Maggio, Alzheimer's disease amyloid propagation by a template-dependent dock-lock mechanism. Biochemistry 39, 6288-6295 (2000).
34. T. P. J. Knowles, C. A. Waudby, G. L. Devlin, S. I. A. Cohen, A. Aguzzi,M. Vendruscolo, E.M. Terentjev, M. E. Welland, C. M. Dobson, An analytical solution to the kinetics of breakable filament assembly. Science 326, 1533-1537 (2009).
35. D. L. Elbert, B. W. Patterson, L. Ercole, V.Ovod, T. Kasten, K. Mawuenyega, K. Yarasheski, J. C. Morris, T. Benzinger, D. M.Holtzman, R. J. Bateman, Reply to: Fractional synthesis and clearance rates for amyloid b. Nat. Med. 17, 1178-1179 (2011).
36. Y. Huang, R. Potter, W. Sigurdson, A. Santacruz, S. Shih, Y. E. Ju, T. Kasten, J. C. Morris, M. Mintun, S. Duntley, R. J. Bateman, Effects of age and amyloid deposition on Ab dynamics in the human central nervous system. Arch. Neurol. 69, 51-58 (2011).
37. J. H. Roh, Y. Huang, A. W. Bero, T. Kasten, F. R. Stewart, R. J. Bateman, D. M. Holtzman, Disruption of the sleep-wake cycle and diurnal fluctuation of b-amyloid in mice with Alzheimer's disease pathology. Sci. Transl. Med. 4, 150ra122 (2012).
38. E.M. Reiman, Y. T. Quiroz, A. S. Fleisher, K. Chen, C. Velez-Pardo,M. Jimenez-Del-Rio, A. M. Fagan, A. R. Shah, S. Alvarez, A. Arbelaez, M. Giraldo, N. Acosta-Baena, R. A. Sperling, B. Dickerson, C.E. Stern, V. Tirado, C. Munoz,R. A. Reiman, M. J. Huentelman, G.E. Alexander, J. B. S. Langbaum, K. S. Kosik, P. N. Tariot, F. Lopera, Brain imaging and fluid biomarker analysis in young adults at genetic risk for autosomal dominant Alzheimer's disease in the presenilin 1 E280A kindred: A case-control study. Lancet Neurol. 11, 1048-1056 (2012).
39. J. D. Harper, P. T. Lansbury Jr., Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu. Rev. Biochem. 66, 385-407 (1997).
40. C. Cruchaga, S. Chakraverty, K. Mayo, F. L. Vallania, R. D. Mitra, K. Faber, J. Williamson, T. Bird, R. Diaz-Arrastia, T. M. Foroud, B. F. Boeve, N. R. Graff-Radford, P. St Jean, M. Lawson, M. G. Ehm, R. Mayeux, A. M. Goate; NIA-LOAD/NCRAD Family Study Consortium, Rare variants in APP, PSEN1 and PSEN2 increase risk for AD in late-onset Alzheimer's disease families. PLoS One 7, e31039 (2012).
41. R. J. Bateman, L. Y. Munsell, J. C. Morris, R. Swarm, K. E. Yarasheski, D. M. Holtzman, Human amyloid-b synthesis and clearance rates as measured in cerebrospinal fluid in vivo. Nat. Med. 12, 856-861 (2006).
42. D. N. Reeds, W. T. Cade, B. W. Patterson, W. G. Powderly, S. Klein, K. E. Yarasheski, Whole-body proteolysis rate is elevated in HIV-associated insulin resistance. Diabetes 55, 2849-2855 (2006).
43. J. J. Cook, K. R.Wildsmith,D. B.Gilberto, M.A.Holahan,G.G. Kinney, P.D. Mathers, M. S.Michener, E. A. Price, M. S. Shearman, A. J. Simon, J. X. Wang, G. Wu, K. E. Yarasheski, R. J. Bateman, Acute g-secretase inhibition of nonhuman primate CNS shifts amyloid precursor protein (APP)metabolism from amyloid-b production to alternative APP fragments without amyloid-b rebound. J. Neurosci. 30, 6743-6750 (2010).
44. M. J. Savage, S. P. Trusko, D. S. Howland, L. R. Pinsker, S. Mistretta, A. G. Reaume, B. D. Greenberg, R. Siman, R. W. Scott, Turnover of amyloid b-protein in mouse brain and acute reduction of its level by phorbol ester. J. Neurosci. 18, 1743-1752 (1998).