Implication of common and disease specific variants in CLU, CR1, and PICALM

Neurobiology of Aging

Volumn 33, Issue 8, 2012, Pages 1846.e7-1846.e18

  Ferrari, Raffaele ^a,b   Moreno, Jorge H ^a   Minhajuddin, Abu T ^c   O'Bryant, Sid E ^a   Reisch, Joan S ^c   Barber, Robert C ^d   Momeni, Parastoo ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Alzheimer's disease (AD); Clusterin (CLU); Complement receptor 1 (CR1); Genome wide association study (GWAS); Phosphotidylinositol binding clathrin assembly protein (PICALM)

Indexed keywords

CLUSTERIN; COMPLEMENT COMPONENT C3B RECEPTOR;

AGED; ALZHEIMER DISEASE; ARTICLE; CLUSTERIN GENE; COMPLEMENT RECEPTOR 1 GENE; COMPUTER MODEL; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; GENE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; PHOSPHATIDYLINOSITOL BINDING CLATHRIN ASSEMBLY PROTEIN GENE; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; RISK ASSESSMENT; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84861875043     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.01.110     Document Type: Article

References (46)

1. Barrett J.C., Fry B., Maller J., Daly M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21:263-265.
2. Bartl M.M., Luckenbach T., Bergner O., Ullrich O., Koch-Brandt C. Multiple receptors mediate apoJ-dependent clearance of cellular debris into nonprofessional phagocytes. Exp. Cell Res 2001, 271:130-141.
3. Belbin O., Carrasquillo M.M., Crump M., Culley O.J., Hunter T.A., Ma L., Bisceglio G., Zou F., Allen M., Dickson D.W., Graff-Radford N.R., Petersen R.C., Morgan K., Younkin S.G. Investigation of 15 of the top candidate genes for late-onset Alzheimer's disease. Hum. Genet 2011, 129:273-282.
4. Bell R.D., Sagare A.P., Friedman A.E., Bedi G.S., Holtzman D.M., Deane R., Zlokovic B.V. Transport pathways for clearance of human Alzheimer's amyloid beta-peptide and apolipoproteins E and J in the mouse central nervous system J. Cereb. Blood Flow Metab 2007, 27:909-918.
5. Benjamini Y., Hochberg Y. Controlling the false discovery rate: A new and powerful approach to multiple testing. J. R. Stat. Soc 1995, 57:1289-1300.
6. Bertram L., McQueen M.B., Mullin K., Blacker D., Tanzi R.E. Systematic meta-analyses of Alzheimer disease genetic association studies: the AlzGene database. Nat. Genet 2007, 39:17-23.
7. Brouwers N., Van Cauwenberghe C., Engelborghs S., Lambert J.C., Bettens K., Le Bastard N., Pasquier F., Montoya A.G., Peeters K., Mattheijssens M., Vandenberghe R., De Deyn P.P., Cruts M., Amouyel P., Sleegers K., Van Broeckhoven C. Alzheimer risk associated with a copy number variation in the complement receptor 1 increasing C3b/C4b binding sites. Mol. Psychiatry 2011, 17:223-233.
8. Bushlin I., Petralia R.S., Wu F., Harel A., Mughal M.R., Mattson M.P., Yao P.J. Clathrin assembly protein AP180 and CALM differentially control axogenesis and dendrite outgrowth in embryonic hippocampal neurons. Neurosci 2008, 28:10257-10271.
9. Calero M., Rostegno A., Matsubara E., Zlokovic B.V., Ghiso J. Apolipoprotein J (clusterin) and Alzheimer's disease. Micro. Res. Technol 2000, 50:305-315.
10. Campion D., Dumanchin C., Hannequin D., Dubois B., Belliard S., Puel M., Thomas-Anterion C., Michon A., Martin C., Charbonnier F., Raux G., Camuzat A., Penet C., Mesnage V., Martinez M., Clerget-Darpoux F., Brice A., Frebourg T. Early-onset autosomal dominant Alzheimer disease: prevalence, genetic heterogeneity, and mutation spectrum. Am. J. Hum. Genet 1999, 65:664-670.
11. Carrasquillo, M.M., Belbin, O., Hunter, T.A., Ma, L., Bisceglio, G.D., Zou, F., Crook, J.E., Pankratz, V.S., Dickson, D.W., Graff-Radford, N.R., Petersen, R.C., Morgan, K., Younkin, S.G. Replication of CLU, CR1, and PICALM associations with Alzheimer disease. Arch. Neurol. 67, 961-964.
12. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923.
13. Corneveaux J.J., Myers A.J., Allen A.N., Pruzin J.J., Ramirez M., Engel A., Nalls M.A., Chen K., Lee W., Chewning K., Villa S.E., Meechoovet H.B., Gerber J.D., Frost D., Benson H.L., O'Reilly S., Chibnik L.B., Shulman J.M., Singleton A.B., Craig D.W., Van Keuren-Jensen K.R., Dunckley T., Bennett D.A., De Jager P.L., Heward C., Hardy J., Reiman E.M., Huentelman M.J. Association of CR1, CLU and PICALM with Alzheimer's disease in a cohort of clinically characterized and neuropathologically verified individuals. Hum. Mol. Genet 2010, 19:3295-3301.
14. de Silva H.V., Stuart W.D., Duvic C.R., Wetterau J.R., Ray M.J., Ferguson D.G., Albers H.W., Smith W.R., Harmony J.A. A 70-kDa apolipoprotein designated ApoJ is a marker for subclasses of human plasma high density lipoproteins. J. Biol. Chem 1990, 265:13240-13247.
15. Dykman T.R., Hatch J.A., Aqua M.S., Atkinson J.P. Polymorphism of the C3b/C4b receptor (CR1): characterization of a fourth allele. J. Immunol 1985, 134:1787-1789.
16. Edeling M.A., Smith C., Owen D. Life of a clathrin coat: insights from clathrin and AP structures. Nat. Rev. Mol. Cell Biol 2006, 7:32-44.
17. Gelissen I.C., Hochgrebe T., Wilson M.R., Easterbrook-Smith S.B., Jessup W., Dean R.T., Brown A.J. Apolipoprotein J (clusterin) induces cholesterol export from macrophage-foam cells: a potential anti-atherogenic function?. Biochem. J 1998, 331:231-237.
18. Guerreiro R.J., Beck J., Gibbs J.R., Santana I., Rossor M.N., Schott J.M., Nalls M.A., Ribeiro H., Santiago B., Fox N.C., Oliveira C., Collinge J., Mead S., Singleton A., Hardy J. Genetic variability in CLU and its association with Alzheimer's disease. PLoS One 2010, 5:e9510.
19. Harold D., Abraham R., Hollingworth P., Sims R., Gerrish A., Hamshere M.L., Pahwa J.S., Moskvina V., Dowzell K., Williams A., Jones N., Thomas C., Stretton A., Morgan A.R., Lovestone S., Powell J., Proitsi P., Lupton M.K., Brayne C., Rubinsztein D.C., Gill M., Lawlor B., Lynch A., Morgan K., Brown K.S., Passmore P.A., Craig D., McGuinness B., Todd S., Holmes C., Mann D., Smith A.D., Love S., Kehoe P.G., Hardy J., Mead S., Fox N., Rossor M., Collinge J., Maier W., Jessen F., Schürmann B., van den Bussche H., Heuser I., Kornhuber J., Wiltfang J., Dichgans M., Frölich L., Hampel H., Hüll M., Rujescu D., Goate A.M., Kauwe J.S., Cruchaga C., Nowotny P., Morris J.C., Mayo K., Sleegers K., Bettens K., Engelborghs S., De Deyn P.P., Van Broeckhoven C., Livingston G., Bass N.J., Gurling H., McQuillin A., Gwilliam R., Deloukas P., Al-Chalabi A., Shaw C.E., Tsolaki M., Singleton A.B., Guerreiro R., Mühleisen T.W., Nöthen M.M., Moebus S., Jöckel K.H., Klopp N., Wichmann H.E., Carrasquillo M.M., Pankratz V.S., Younkin S.G., Holmans P.A., O'Donovan M., Owen M.J., Williams J. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet 2009, 41:1088-1093.
20. Holers V.M., Chaplin D.D., Leykam J.F., Gruner B.A., Kumar V., Atkinson J.P. Human complement C3b/C4b receptor (CR1) mRNA polymorphism that correlates with the CR1 allelic molecular weight polymorphism. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:2459-2463.
21. Jones L., Holmans P.A., Hamshere M.L., Harold D., Moskvina V., Ivanov D., Pocklington A., Abraham R., Hollingworth P., Sims R., Gerrish A., Pahwa sJ.S., Jones N., Stretton A., Morgan A.R., Lovestone S., Powell J., Proitsi P., Lupton M.K., Brayne C., Rubinsztein D.C., Gill M., Lawlor B., Lynch A., Morgan K., Brown K.S., Passmore P.A., Craig D., McGuinness B., Todd S., Holmes C., Mann D., Smith A.D., Love S., Kehoe P.G., Mead S., Fox N., Rossor M., Collinge J., Maier W., Jessen F., Schürmann B., Heun R., Kölsch H., van den Bussche H., Heuser I., Peters O., Kornhuber sJ., Wiltfang J., Dichgans M., Frölich L., Hampel H., Hüll M., Rujescu D., Goate A.M., Kauwe J.S., Cruchaga C., Nowotny P., Morris J.C., Mayo K., Livingston G., Bass N.J., Gurling H., McQuillin A., Gwilliam R., Deloukas P., Al-Chalabi A., Shaw C.E., Singleton A.B., Guerreiro R., Mühleisen T.W., Nöthen M.M., Moebus S., Jöckel K.H., Klopp N., Wichmann H.E., Rüther E., Carrasquillo M.M., Pankratz V.S., Younkin S.G., Hardy J., O'Donovan M.C., Owen M.J., Williams J. Genetic evidence implicates the immune system and cholesterol metabolism in the aetiology of Alzheimer's disease. PLoS One 2010, 5:e13950.
22. Khera R., Das N. Complement Receptor 1: disease associations and therapeutic implications. Mol. Immunol 2009, 46:761-772.
23. Lambert J.C., Heath S., Even G., Campion D., Sleegers K., Hiltunen M., Combarros O., Zelenika D., Bullido M.J., Tavernier B., Letenneur L., Bettens K., Berr C., Pasquier F., Fiévet N., Barberger-Gateau P., Engelborghs S., De Deyn P., Mateo I., Franck A., Helisalmi S., Porcellini E., Hanon O., de Pancorbo M.M., Lendon C., Dufouil C., Jaillard C., Leveillard T., Alvarez V., Bosco P., Mancuso M., Panza F., Nacmias B., Bossù P., Piccardi P., Annoni G., Seripa D., Galimberti D., Hannequin D., Licastro F., Soininen H., Ritchie K., Blanché H., Dartigues J.F., Tzourio C., Gut I., Van Broeckhoven C., Alpérovitch A., Lathrop M., Amouyel P. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat. Genet 2009, 41:1094-1099. European Alzheimer's Disease Initiative Investigators.
24. Lambert J.C., Zelenika D., Hiltunen M., Chouraki V., Combarros O., Bullido M.J., Tognoni G., Fiévet N., Boland A., Arosio B., Coto E., Del Zompo M., Mateo I., Frank-Garcia A., Helisalmi S., Porcellini E., Pilotto A., Forti P., Ferri R., Delepine M., Scarpini E., Siciliano G., Solfrizzi V., Sorbi S., Spalletta G., Ravaglia G., Valdivieso F., Alvarez V., Bosco P., Mancuso M., Panza F., Nacmias B., Bossù P., Piccardi P., Annoni G., Seripa D., Galimberti D., Licastro F., Lathrop M., Soininen H., Amouyel P. Evidence of the association of BIN1 and PICALM with the AD risk in contrasting European populations. Neurobiol. Aging 2011, 32:e11-e15.
25. Lucin K.M., Wyss-Coray T. Immune activation in brain aging and neurodegeneration: too much or too little?. Neuron 2009, 64:110-122.
26. Masliah E., Mallory M., Alford M., DeTeresa R., Hansen L.A., McKeel D.W., Morris J.C. Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 2001, 56:127-129.
27. Matsubara E., Frangione B., Ghiso J. Characterization of apolipoprotein J-Alzheimer's A beta interaction. J. Biol. Chem 1995, 270:7563-7567.
28. McGeer P.L., Kawamata T., Walker D.G. Distribution of clusterin in Alzheimer brain tissue. Brain Res 1992, 579:337-341.
29. Mengel-From J., Christensen K., McGue M., Christiansen L. Genetic variations in the CLU and PICALM genes are associated with cognitive function in the oldest old. Neurobiol. Aging 2011, 32:e7-e11.
30. Michel D., Chatelain G., North S., Brun G. Stress-induced transcription of the clusterin/apoJ gene. Biochem. J 1997, 328:45-50.
31. Naj A.C., Jun G., Beecham G.W., Wang L.S., Vardarajan B.N., Buros J., Gallins P.J., Buxbaum J.D., Jarvik G.P., Crane P.K., Larson E.B., Bird T.D., Boeve B.F., Graff-Radford N.R., De Jager P.L., Evans D., Schneider J.A., Carrasquillo M.M., Ertekin-Taner N., Younkin S.G., Cruchaga C., Kauwe J.S., Nowotny P., Kramer P., Hardy J., Huentelman M.J., Myers A.J., Barmada M.M., Demirci F.Y., Baldwin C.T., Green R.C., Rogaeva E., St George-Hyslop P., Arnold S.E., Barber R., Beach T., Bigio E.H., Bowen J.D., Boxer A., Burke J.R., Cairns N.J., Carlson C.S., Carney R.M., Carroll S.L., Chui H.C., Clark D.G., Corneveaux J., Cotman C.W., Cummings J.L., Decarli C., Dekosky S.T., Diaz-Arrastia R., Dick M., Dickson D.W., Ellis W.G., Faber K.M., Fallon K.B., Farlow M.R., Ferris S., Frosch M.P., Galasko D.R., Ganguli M., Gearing M., Geschwind D.H., Ghetti B., Gilbert J.R., Gilman S., Giordani B., Glass J.D., Growdon J.H., Hamilton R.L., Harrell L.E., Head E., Honig L.S., Hulette C.M., Hyman B.T., Jicha G.A., Jin L.W., Johnson N., Karlawish J., Karydas A., Kaye J.A., Kim R., Koo E.H., Kowall N.W., Lah J.J., Levey A.I., Lieberman A.P., Lopez O.L., Mack W.J., Marson D.C., Martiniuk F., Mash D.C., Masliah E., McCormick W.C., McCurry S.M., McDavid A.N., McKee A.C., Mesulam M., Miller B.L., Miller C.A., Miller J.W., Parisi J.E., Perl D.P., Peskind E., Petersen R.C., Poon W.W., Quinn J.F., Rajbhandary R.A., Raskind M., Reisberg B., Ringman J.M., Roberson E.D., Rosenberg R.N., Sano M., Schneider L.S., Seeley W., Shelanski M.L., Slifer M.A., Smith C.D., Sonnen J.A., Spina S., Stern R.A., Tanzi R.E., Trojanowski J.Q., Troncoso J.C., Van Deerlin V.M., Vinters H.V., Vonsattel J.P., Weintraub S., Welsh-Bohmer K.A., Williamson J., Woltjer R.L., Cantwell L.B., Dombroski B.A., Beekly D., Lunetta K.L., Martin E.R., Kamboh M.I., Saykin A.J., Reiman E.M., Bennett D.A., Morris J.C., Montine T.J., Goate A.M., Blacker D., Tsuang D.W., Hakonarson H., Kukull W.A., Foroud T.M., Haines J.L., Mayeux R., Pericak-Vance M.A., Farrer L.A., Schellenberg G.D. Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease. Nat. Genet 2011, 43:436-441.
32. Nilselid A.M., Davidsson P., Nägga K., Andreasen N., Fredman P., Blennow K. Clusterin in cerebrospinal fluid: analysis of carbohydrates and quantification of native and glycosylated forms. Neurochem. Int 2006, 48:718-728.
33. Nordstedt C., Caporaso G.L., Thyberg J., Gandy S.E., Greengard P. Identification of the Alzheimer beta/A4 amyloid precursor protein in clathrin-coated vesicles purified from PC12 cells. J. Biol. Chem 1993, 268:608-612.
34. Rogers J., Li R., Mastroeni D., Grover A., Leonard B., Ahern G., Cao P., Kolody H., Vedders L., Kolb W.P., Sabbagh M. Peripheral clearance of amyloid beta peptide by complement C3-dependent adherence to erythrocytes. Neurobiol. Aging 2006, 27:1733-1739.
35. Royle S.J., Lagnado L. Clathrin-mediated endocytosis at the synaptic terminal: bridging the gap between physiology and molecules. Traffic 2010, 11:1489-1497.
36. Seshadri S., Fitzpatrick A.L., Ikram M.A., DeStefano A.L., Gudnason V., Boada M., Bis J.C., Smith A.V., Carassquillo M.M., Lambert J.C., Harold D., Schrijvers E.M., Ramirez-Lorca R., Debette S., Longstreth W.T., Janssens A.C., Pankratz V.S., Dartigues J.F., Hollingworth P., Aspelund T., Hernandez I., Beiser A., Kuller L.H., Koudstaal P.J., Dickson D.W., Tzourio C., Abraham R., Antunez C., Du Y., Rotter J.I., Aulchenko Y.S., Harris T.B., Petersen R.C., Berr C., Owen M.J., Lopez-Arrieta J., Varadarajan B.N., Becker J.T., Rivadeneira F., Nalls M.A., Graff-Radford N.R., Campion D., Auerbach S., Rice K., Hofman A., Jonsson P.V., Schmidt H., Lathrop M., Mosley T.H., Au R., Psaty B.M., Uitterlinden A.G., Farrer L.A., Lumley T., Ruiz A., Williams J., Amouyel P., Younkin S.G., Wolf P.A., Launer L.J., Lopez O.L., van Duijn C.M., Breteler M.M. Genome-wide analysis of genetic loci associated with Alzheimer disease. JAMA 2010, 303:1832-1840. CHARGE Consortium, GERAD1 Consortium, EADI1 Consortium.
37. Simons M., Keller P., De Strooper B., Beyreuther K., Dotti C.G., Simons K. Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6460-6464.
38. Tang M.X., Maestre G., Tsai W.Y., Liu X.H., Feng L., Chung W.Y., Chun M., Schofield P., Stern Y., Tycko B., Mayeux R. Effect of age, ethnicity, and head injury on the association between APOE genotypes and Alzheimer's disease. Ann. N. Y. Acad. Sci 1996, 802:6-15.
39. Tebar F., Bohlander S.K., Sorkin A. Clathrin assembly lymphoid myeloid leukemia (CALM) protein: localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic. Mol. Biol. Cell 1999, 10:2687-2702.
40. Traub L.M. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol 2009, 10:583-596.
41. Waring S.C., O'Bryant S.E., Reisch J.S., Diaz-Arrastia R., Knebl J., Doody R. Texas Public Health Journal, Special Issue on the Texas Alzheimer's Research Consortium 2008, 60:9-13. Texas Alzheimer's Research Consortium.
42. Wong W.W., Kennedy C.A., Bonaccio E.T., Wilson J.G., Klickstein L.B., Weis J.H., Fearon D.T. Analysis of multiple restriction fragment length polymorphisms of the gene for the human complement receptor type I. Duplication of genomic sequences occurs in association with a high molecular mass receptor allotype. J. Exp. Med 1986, 164:1531-1546.
43. Wyss-Coray T., Yan F., Lin A.H., Lambris J.D., Alexander J.J., Quigg R.J., Masliah E. Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10837-10842.
44. Yerbury J.J., Poon S., Meehan S., Thompson B., Kumita J.R., Dobson C.M., Wilson M.R. The extracellular chaperone clusterin influences amyloid formation and toxicity by interacting with prefibrillar structures. FASEB J. 2007, 21:2312-2322.
45. Zanjani H., Finch C.E., Kemper C., Atkinson J., McKeel D., Morris J.C., Price J.L. Complement activation in very early Alzheimer disease Alzheimer. Dis. Assoc. Disord 2005, 19:55-66.
46. Zotova E., Nicoll J.A., Kalaria R., Holmes C., Boche D. Inflammation in Alzheimer's disease: relevance to pathogenesis and therapy. Alzheimers Res. Ther 2010, 2:1.