LRP-1 polymorphism is associated with global and regional amyloid load in Alzheimer's disease in humans in-vivo

NeuroImage: Clinical

Volumn 4, Issue , 2014, Pages 411-416

  Grimmer, Timo ^a   Goldhardt, Oliver ^a   Guo, Liang Hao ^a   Yousefi, Behrooz H ^b   Förster, Stefan ^b   Drzezga, Alexander ^c   Sorg, Christian ^a   Alexopoulos, Panagiotis ^a   Förstl, Hans ^a   Kurz, Alexander ^a   Perneczky, Robert ^a,d  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Alzheimer's disease (AD); Apolipoprotein E (ApoE); C667T polymorphism; Low density lipoprotein receptor related protein 1 (LRP 1); Pittsburgh compound B ( 11C PiB); Positron emission tomography (PET)

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; FLUORODEOXYGLUCOSE F 18; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; AMYLOID PROTEIN; BENZOTHIAZOLE DERIVATIVE; LRP1 PROTEIN, HUMAN; N-METHYL-2-(4'-METHYLAMINOPHENYL)-6-HYDROXYBENZOTHIAZOLE; RADIOPHARMACEUTICAL AGENT;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BLOOD; BRAIN; CLINICAL DEMENTIA RATING; CONTROLLED STUDY; DEMENTIA; FEMALE; FUNCTIONAL NEUROIMAGING; GENDER; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC LOAD; GENETIC VARIABILITY; GENOTYPE; HUMAN; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL CORTEX; POLYMERASE CHAIN REACTION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN TRANSPORT; REGRESSION ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; VERY ELDERLY; VOXEL BASED MORPHOMETRY; GENETIC PREDISPOSITION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; SCINTISCANNING; SENSITIVITY AND SPECIFICITY; TISSUE DISTRIBUTION;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOIDOGENIC PROTEINS; BENZOTHIAZOLES; BRAIN; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TISSUE DISTRIBUTION;

EID: 84896870717     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2014.01.016     Document Type: Article

References (57)

1. V.S. Bahia, F. Kok, S.N. Marie, S.O. Shinjo, P. Caramelli, and R. Nitrini Polymorphisms of APOE and LRP genes in Brazilian individuals with Alzheimer disease Alzheimer Dis. Assoc. Disord. 22 2008 61 65 10.1097/WAD.0b013e31815a9da7 (Pubitemid 351651399)
2. U. Beffert, C. Arguin, and J. Poirier The polymorphism in exon 3 of the low density lipoprotein receptor-related protein gene is weakly associated with Alzheimer's disease Neurosci. Lett. 259 1999 29 32 (S0304-3940(98)00888-X [pii]) (Pubitemid 29051534)
3. H. Braak, and E. Braak Neuropathological stageing of Alzheimer-related changes Acta Neuropathol. 82 1991 239 259
4. R.O. Carare, M. Bernardes-Silva, T.A. Newman, A.M. Page, J.A. Nicoll, V.H. Perry, and R.O. Weller Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology Neuropathol. Appl. Neurobiol. 34 2008 131 144 10.1111/j.1365-2990.2007.00926.x (NAN926 [pii]) (Pubitemid 351327967)
5. J.M. Castellano, J. Kim, F.R. Stewart, H. Jiang, R.B. DeMattos, B.W. Patterson, A.M. Fagan, J.C. Morris, K.G. Mawuenyega, C. Cruchaga, A.M. Goate, K.R. Bales, S.M. Paul, R.J. Bateman, and D.M. Holtzman Human apoE isoforms differentially regulate brain amyloid-beta peptide clearance Sci. Transl. Med. 3 2011 89ra57 10.1126/scitranslmed.3002156 (3/89/89ra57 [pii])
6. R. Deane, and B.V. Zlokovic Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease Curr. Alzheimer Res. 4 2007 191 197 (Pubitemid 46562394)
7. R. Deane, A. Sagare, K. Hamm, M. Parisi, S. Lane, M.B. Finn, D.M. Holtzman, and B.V. Zlokovic apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain J. Clin. Invest. 118 2008 4002 4013 10.1172/JCI36663 36663
8. R. Deane, R.D. Bell, A. Sagare, and B.V. Zlokovic Clearance of amyloid-beta peptide across the blood-brain barrier: implication for therapies in Alzheimer's disease CNS Neurol. Disord. Drug Targets 8 2009 16 30
9. Y. Deng, Y. Sun, J.J. Shi, and S.Z. Zhang Meta-analysis of the association of the LRP C766T polymorphism with the risk of Alzheimer's disease Yi Chuan 28 2006 393 398 (0253-9772(2006) 04-0393-06 [pii])
10. A. Drzezga, T. Grimmer, G. Henriksen, M. Muhlau, R. Perneczky, I. Miederer, C. Praus, C. Sorg, A. Wohlschlager, M. Riemenschneider, H.J. Wester, H. Foerstl, M. Schwaiger, and A. Kurz Effect of APOE genotype on amyloid plaque load and gray matter volume in Alzheimer disease Neurology 72 2009 1487 1494 10.1212/WNL.0b013e3181a2e8d0 (WNL.0b013e3181a2e8d0 [pii])
11. C. Duyckaerts, B. Delatour, and M.C. Potier Classification and basic pathology of Alzheimer disease Acta Neuropathol. 118 2009 5 36 10.1007/s00401-009-0532-1
12. M.F. Folstein, S.E. Folstein, and P.R. McHugh Mini-mental state. A practical method for grading the cognitive state of patients for the clinician J. Psychiatr. Res. 12 1975 189 198 (0022-3956(75)90026-6 [pii])
13. D.A. Forero, G. Arboleda, J.J. Yunis, R. Pardo, and H. Arboleda Association study of polymorphisms in LRP1, tau and 5-HTT genes and Alzheimer's disease in a sample of Colombian patients J. Neural Transm. 113 2006 1253 1262 10.1007/s00702-005-0388-z (Pubitemid 44291019)
14. K.J. Friston, G. Tononi, G.N. Reeke Jr., O. Sporns, and G.M. Edelman Value-dependent selection in the brain: simulation in a synthetic neural model Neuroscience 59 1994 229 243 (0306-4522(94)90592-4 [pii]) (Pubitemid 24098785)
15. R.A. Fuentealba, Q. Liu, J. Zhang, T. Kanekiyo, X. Hu, J.M. Lee, M.J. LaDu, and G. Bu Low-density lipoprotein receptor-related protein 1 (LRP1) mediates neuronal Abeta42 uptake and lysosomal trafficking PLoS One 5 2010 e11884 10.1371/journal.pone.0011884
16. C. Glaser, S. Schulz, K. Handschug, K. Huse, and G. Birkenmeier Genetic and functional characteristics of the human in vivo LRP1/A2MR receptor suggested as a risk marker for Alzheimer's disease and other complex (degenerative) diseases Neurosci. Res. 50 2004 85 101 10.1016/j.neures.2004.06.001 (S016801020400118X [pii]) (Pubitemid 39024305)
17. J.D. Goos, W.J. Henneman, J.D. Sluimer, H. Vrenken, I.C. Sluimer, F. Barkhof, M.A. Blankenstein, P.H. Scheltens, and W.M. van der Flier Incidence of cerebral microbleeds: a longitudinal study in a memory clinic population Neurology 74 2010 1954 1960 10.1212/WNL.0b013e3181e396ea (74/24/1954 [pii])
18. T. Grimmer, G. Henriksen, H.J. Wester, H. Forstl, W.E. Klunk, C.A. Mathis, A. Kurz, and A. Drzezga Clinical severity of Alzheimer's disease is associated with PIB uptake in PET Neurobiol. Aging 30 2009 1902 1909 10.1016/j.neurobiolaging.2008.01.016 (S0197-4580(08)00035-3 [pii])
19. T. Grimmer, M. Riemenschneider, H. Forstl, G. Henriksen, W.E. Klunk, C.A. Mathis, T. Shiga, H.J. Wester, A. Kurz, and A. Drzezga Beta amyloid in Alzheimer's disease: increased deposition in brain is reflected in reduced concentration in cerebrospinal fluid Biol. Psychiatry 65 2009 927 934 10.1016/j.biopsych.2009.01.027 (S0006-3223(09)00110-3 [pii])
20. T. Grimmer, S. Tholen, B.H. Yousefi, P. Alexopoulos, A. Forschler, H. Forstl, G. Henriksen, W.E. Klunk, C.A. Mathis, R. Perneczky, C. Sorg, A. Kurz, and A. Drzezga Progression of cerebral amyloid load is associated with the apolipoprotein E epsilon4 genotype in Alzheimer's disease Biol. Psychiatry 68 2010 879 884 10.1016/j.biopsych.2010.05.013 (S0006-3223(10)00473-7 [pii])
21. T. Grimmer, M. Faust, F. Auer, P. Alexopoulos, H. Forstl, G. Henriksen, R. Perneczky, C. Sorg, B.H. Yousefi, A. Drzezga, and A. Kurz White matter hyperintensities predict amyloid increase in Alzheimer's disease Neurobiol. Aging 2012 10.1016/j.neurobiolaging.2012.01.016 (S0197-4580(12)00037-1 [pii])
22. L.H. Guo, C. Westerteicher, X.H. Wang, M. Kratzer, A. Tsolakidou, M. Jiang, T. Grimmer, S.M. Laws, P. Alexopoulos, H. Bujo, A. Kurz, and R. Perneczky SORL1 genetic variants and cerebrospinal fluid biomarkers of Alzheimer's disease Eur. Arch. Psychiatry Clin. Neurosci 2012 10.1007/s00406-012-0295-x
23. K.H. Gylys, J.A. Fein, A.M. Tan, and G.M. Cole Apolipoprotein E enhances uptake of soluble but not aggregated amyloid-beta protein into synaptic terminals J. Neurochem. 84 2003 1442 1451 (1643 [pii]) (Pubitemid 36343610)
24. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356 10.1126/science.1072994 (297/5580/353 [pii]) (Pubitemid 34790756)
25. Y. Hatanaka, K. Kamino, K. Fukuo, N. Mitsuda, Y. Nishiwaki-Ueda, N. Sato, T. Satoh, H. Yamamoto, H. Yoneda, M. Imagawa, T. Miki, S. Ohta, and T. Ogihara Low density lipoprotein receptor-related protein gene polymorphisms and risk for late-onset Alzheimer's disease in a Japanese population Clin. Genet. 58 2000 319 323
26. J. Herz, and D.K. Strickland LRP: a multifunctional scavenger and signaling receptor J. Clin. Invest. 108 2001 779 784 10.1172/JCI13992 (Pubitemid 32880284)
27. J.M. Hoffman, K.A. Welsh-Bohmer, M. Hanson, B. Crain, C. Hulette, N. Earl, and R.E. Coleman FDG PET imaging in patients with pathologically verified dementia J. Nucl. Med. 41 2000 1920 1928
28. N. Iwata, S. Tsubuki, Y. Takaki, K. Watanabe, M. Sekiguchi, E. Hosoki, M. Kawashima-Morishima, H.J. Lee, E. Hama, Y. Sekine-Aizawa, and T.C. Saido Identification of the major Abeta1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition Nat. Med. 6 2000 143 150 10.1038/72237 (Pubitemid 30082357)
29. S. Jaeger, and C.U. Pietrzik Functional role of lipoprotein receptors in Alzheimer's disease Curr. Alzheimer Res. 5 2008 15 25 (Pubitemid 351536350)
30. W. Jagust, B. Reed, D. Mungas, W. Ellis, and C. Decarli What does fluorodeoxyglucose PET imaging add to a clinical diagnosis of dementia? Neurology 69 2007 871 877 10.1212/01.wnl.0000269790.05105.16 (69/9/871 [pii]) (Pubitemid 47329586)
31. M.I. Kamboh, R.E. Ferrell, and S.T. DeKosky Genetic association studies between Alzheimer's disease and two polymorphisms in the low density lipoprotein receptor-related protein gene Neurosci. Lett. 244 1998 65 68 (S0304-3940(98)00141-4 [pii]) (Pubitemid 28157392)
32. K.K. Kandimalla, O.G. Scott, S. Fulzele, M.W. Davidson, and J.F. Poduslo Mechanism of neuronal versus endothelial cell uptake of Alzheimer's disease amyloid beta protein PLoS One 4 2009 e4627 10.1371/journal.pone.0004627
33. D.E. Kang, T. Saitoh, X. Chen, Y. Xia, E. Masliah, L.A. Hansen, R.G. Thomas, L.J. Thal, and R. Katzman Genetic association of the low-density lipoprotein receptor-related protein gene (LRP), an apolipoprotein E receptor, with late-onset Alzheimer's disease Neurology 49 1997 56 61 (Pubitemid 27328682)
34. D.E. Kang, C.U. Pietrzik, L. Baum, N. Chevallier, D.E. Merriam, M.Z. Kounnas, S.L. Wagner, J.C. Troncoso, C.H. Kawas, R. Katzman, and E.H. Koo Modulation of amyloid beta-protein clearance and Alzheimer's disease susceptibility by the LDL receptor-related protein pathway J. Clin. Invest. 106 2000 1159 1166 10.1172/JCI11013
35. H. Kolsch, U. Ptok, I. Mohamed, S. Schmitz, M.L. Rao, W. Maier, and R. Heun Association of the C766T polymorphism of the low-density lipoprotein receptor-related protein gene with Alzheimer's disease Am. J. Med. Genet. B Neuropsychiatr. Genet. 121B 2003 128 130 10.1002/ajmg.b.20043 (Pubitemid 37064042)
36. K.G. Mawuenyega, W. Sigurdson, V. Ovod, L. Munsell, T. Kasten, J.C. Morris, K.E. Yarasheski, and R.J. Bateman Decreased clearance of CNS beta-amyloid in Alzheimer's disease Science 330 2010 1774 10.1126/science. 1197623 (science.1197623 [pii])
37. G. McKhann, D. Drachman, M. Folstein, R. Katzman, D. Price, and E.M. Stadlan 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 1984 939 944 (Pubitemid 14076461)
38. G.M. McKhann, D.S. Knopman, H. Chertkow, B.T. Hyman, C.R. Jack Jr., C.H. Kawas, W.E. Klunk, W.J. Koroshetz, J.J. Manly, R. Mayeux, R.C. Mohs, J.C. Morris, M.N. Rossor, P. Scheltens, M.C. Carrillo, B. Thies, S. Weintraub, and C.H. Phelps 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 2011 263 269 10.1016/j.jalz.2011.03.005 (S1552-5260(11)00101-4 [pii])
39. J.S. Miners, S. Baig, J. Palmer, L.E. Palmer, P.G. Kehoe, and S. Love Abeta-degrading enzymes in Alzheimer's disease Brain Pathol. 18 2008 240 252 10.1111/j.1750-3639.2008.00132.x (BPA132 [pii]) (Pubitemid 351436347)
40. S. Minoshima, K.A. Frey, R.A. Koeppe, N.L. Foster, and D.E. Kuhl A diagnostic approach in Alzheimer's disease using three-dimensional stereotactic surface projections of fluorine-18-FDG PET J. Nucl. Med. 36 1995 1238 1248
41. J.C. Morris, A. Heyman, R.C. Mohs, J.P. Hughes, G. van Belle, G. Fillenbaum, E.D. Mellits, and C. Clark The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease Neurology 39 1989 1159 1165 (Pubitemid 19239715)
42. T. Pflanzner, M.C. Janko, B. Andre-Dohmen, S. Reuss, S. Weggen, A.J. Roebroek, C.R. Kuhlmann, and C.U. Pietrzik LRP1 mediates bidirectional transcytosis of amyloid-beta across the blood-brain barrier Neurobiol. Aging 32 2323 2011 e2321 e 10.1016/j.neurobiolaging.2010.05.025 (S0197-4580(10)00239-3 [pii])
43. A. Pritchard, J. Harris, C.W. Pritchard, D. St Clair, H. Lemmon, J.C. Lambert, M.C. Chartier-Harlin, A. Hayes, U. Thaker, T. Iwatsubo, D.M. Mann, and C. Lendon Association study and meta-analysis of low-density lipoprotein receptor related protein in Alzheimer's disease Neurosci. Lett. 382 2005 221 226 10.1016/j.neulet.2005.03.016 (S0304-3940(05)00308-3 [pii]) (Pubitemid 40733626)
44. H. Qosa, A.H. Abuznait, R.A. Hill, and A. Kaddoumi Enhanced brain amyloid-beta clearance by Rifampicin and caffeine as a possible protective mechanism against Alzheimer's disease J. Alzheimer's Dis 2012 10.3233/JAD-2012-120319 (Y25020027301T215 [pii])
45. M. Shibata, S. Yamada, S.R. Kumar, M. Calero, J. Bading, B. Frangione, D.M. Holtzman, C.A. Miller, D.K. Strickland, J. Ghiso, and B.V. Zlokovic Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier J. Clin. Invest. 106 2000 1489 1499 10.1172/JCI10498 (Pubitemid 32038587)
46. I. Szentistvanyi, C.S. Patlak, R.A. Ellis, and H.F. Cserr Drainage of interstitial fluid from different regions of rat brain Am. J. Physiol. 246 1984 F835 F844
47. D.R. Thal The pre-capillary segment of the blood-brain barrier and its relation to perivascular drainage in Alzheimer's disease and small vessel disease Scientific World Journal 9 2009 557 563 10.1100/tsw.2009.72
48. D.R. Thal, U. Rub, M. Orantes, and H. Braak Phases of A beta-deposition in the human brain and its relevance for the development of AD Neurology 58 2002 1791 1800 (Pubitemid 34663580)
49. F. Van Leuven, L. Stas, C. Hilliker, K. Lorent, L. Umans, L. Serneels, L. Overbergh, S. Torrekens, D. Moechars, and B. De Strooper et al. Structure of the gene (LRP1) coding for the human alpha 2-macroglobulin receptor lipoprotein receptor-related protein Genomics 24 1994 78 89 (S0888754384715849 [pii]) (Pubitemid 24368750)
50. V.L. Villemagne, K.E. Pike, G. Chetelat, K.A. Ellis, R.S. Mulligan, P. Bourgeat, U. Ackermann, G. Jones, C. Szoeke, O. Salvado, R. Martins, G. O'Keefe, C.A. Mathis, W.E. Klunk, D. Ames, C.L. Masters, and C.C. Rowe Longitudinal assessment of Abeta and cognition in aging and Alzheimer disease Ann. Neurol. 69 2011 181 192 10.1002/ana.22248
51. R.O. Weller, A. Massey, T.A. Newman, M. Hutchings, Y.M. Kuo, and A.E. Roher Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer's disease Am. J. Pathol. 153 1998 725 733 (S0002-9440(10)65616-7 [pii]) (Pubitemid 28419027)
52. S.E. Williams, J.D. Ashcom, W.S. Argraves, and D.K. Strickland A novel mechanism for controlling the activity of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein J. Biol. Chem. 267 1992 9035 9040
53. K. Yamada, T. Hashimoto, C. Yabuki, Y. Nagae, M. Tachikawa, D.K. Strickland, Q. Liu, G. Bu, J.M. Basak, D.M. Holtzman, S. Ohtsuki, T. Terasaki, and T. Iwatsubo The low density lipoprotein receptor-related protein 1 mediates uptake of amyloid beta peptides in an in vitro model of the blood-brain barrier cells J. Biol. Chem. 283 2008 34554 34562 10.1074/jbc.M801487200 (M801487200 [pii])
54. E.T. Zhang, H.K. Richards, S. Kida, and R.O. Weller Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain Acta Neuropathol. 83 1992 233 239
55. S.K. Ziolko, L.A. Weissfeld, W.E. Klunk, C.A. Mathis, J.A. Hoge, B.J. Lopresti, S.T. DeKosky, and J.C. Price Evaluation of voxel-based methods for the statistical analysis of PIB PET amyloid imaging studies in Alzheimer's disease Neuroimage 33 2006 94 102 10.1016/j.neuroimage.2006.05.063 (S1053-8119(06)00652- 5 [pii]) (Pubitemid 44397577)
56. A. Zivelin, N. Rosenberg, H. Peretz, Y. Amit, N. Kornbrot, and U. Seligsohn Improved method for genotyping apolipoprotein E polymorphisms by a PCR-based assay simultaneously utilizing two distinct restriction enzymes Clin. Chem. 43 1997 1657 1659
57. B.V. Zlokovic, R. Deane, A.P. Sagare, R.D. Bell, and E.A. Winkler Low-density lipoprotein receptor-related protein-1: a serial clearance homeostatic mechanism controlling Alzheimer's amyloid beta-peptide elimination from the brain J. Neurochem. 115 2010 1077 1089 10.1111/j.1471-4159.2010.07002.x