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GWAS Study

Rare coding variants in PLCG2, ABI3, and TREM2 implicate microglial-mediated innate immunity in Alzheimer's disease.

Sims R, van der Lee SJ, Naj AC et al.

28714976 PubMed ID
GWAS Study Type
85133 Participants
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Chapter I

Publication Details

Comprehensive information about this research publication

Authors

SR
Sims R
VD
van der Lee SJ
NA
Naj AC
BC
Bellenguez C
BN
Badarinarayan N
JJ
Jakobsdottir J
KB
Kunkle BW
BA
Boland A
RR
Raybould R
BJ
Bis JC
ME
Martin ER
GB
Grenier-Boley B
HS
Heilmann-Heimbach S
CV
Chouraki V
KA
Kuzma AB
SK
Sleegers K
VM
Vronskaya M
RA
Ruiz A
GR
Graham RR
OR
Olaso R
HP
Hoffmann P
GM
Grove ML
VB
Vardarajan BN
HM
Hiltunen M
NM
Nöthen MM
WC
White CC
HK
Hamilton-Nelson KL
EJ
Epelbaum J
MW
Maier W
CS
Choi SH
BG
Beecham GW
DC
Dulary C
HS
Herms S
SA
Smith AV
FC
Funk CC
DC
Derbois C
FA
Forstner AJ
AS
Ahmad S
LH
Li H
BD
Bacq D
HD
Harold D
SC
Satizabal CL
VO
Valladares O
SA
Squassina A
TR
Thomas R
BJ
Brody JA
QL
Qu L
SP
Sánchez-Juan P
MT
Morgan T
WF
Wolters FJ
ZY
Zhao Y
GF
Garcia FS
DN
Denning N
FM
Fornage M
MJ
Malamon J
NM
Naranjo MCD
ME
Majounie E
MT
Mosley TH
DB
Dombroski B
WD
Wallon D
LM
Lupton MK
DJ
Dupuis J
WP
Whitehead P
FL
Fratiglioni L
MC
Medway C
JX
Jian X
MS
Mukherjee S
KL
Keller L
BK
Brown K
LH
Lin H
CL
Cantwell LB
PF
Panza F
MB
McGuinness B
MS
Moreno-Grau S
BJ
Burgess JD
SV
Solfrizzi V
PP
Proitsi P
AH
Adams HH
AM
Allen M
SD
Seripa D
PP
Pastor P
CL
Cupples LA
PN
Price ND
HD
Hannequin D
FA
Frank-García A
LD
Levy D
CP
Chakrabarty P
CP
Caffarra P
GI
Giegling I
BA
Beiser AS
GV
Giedraitis V
HH
Hampel H
GM
Garcia ME
WX
Wang X
LL
Lannfelt L
MP
Mecocci P
EG
Eiriksdottir G
CP
Crane PK
PF
Pasquier F
BV
Boccardi V
HI
Henández I
BR
Barber RC
SM
Scherer M
TL
Tarraga L
AP
Adams PM
LM
Leber M
CY
Chen Y
AM
Albert MS
RS
Riedel-Heller S
EV
Emilsson V
BD
Beekly D
BA
Braae A
SR
Schmidt R
BD
Blacker D
MC
Masullo C
SH
Schmidt H
DR
Doody RS
SG
Spalletta G
LW
Longstreth WT
FT
Fairchild TJ
BP
Bossù P
LO
Lopez OL
FM
Frosch MP
SE
Sacchinelli E
GB
Ghetti B
YQ
Yang Q
HR
Huebinger RM
JF
Jessen F
LS
Li S
KM
Kamboh MI
MJ
Morris J
SO
Sotolongo-Grau O
KM
Katz MJ
CC
Corcoran C
DM
Dunstan M
BA
Braddel A
TC
Thomas C
MA
Meggy A
MR
Marshall R
GA
Gerrish A
CJ
Chapman J
AM
Aguilar M
TS
Taylor S
HM
Hill M
FM
Fairén MD
HA
Hodges A
VB
Vellas B
SH
Soininen H
KI
Kloszewska I
DM
Daniilidou M
UJ
Uphill J
PY
Patel Y
HJ
Hughes JT
LJ
Lord J
TJ
Turton J
HA
Hartmann AM
CR
Cecchetti R
FC
Fenoglio C
SM
Serpente M
AM
Arcaro M
CC
Caltagirone C
OM
Orfei MD
CA
Ciaramella A
PS
Pichler S
MM
Mayhaus M
GW
Gu W
LA
Lleó A
FJ
Fortea J
BR
Blesa R
BI
Barber IS
BK
Brookes K
CC
Cupidi C
MR
Maletta RG
CD
Carrell D
SS
Sorbi S
MS
Moebus S
UM
Urbano M
PA
Pilotto A
KJ
Kornhuber J
BP
Bosco P
TS
Todd S
CD
Craig D
JJ
Johnston J
GM
Gill M
LB
Lawlor B
LA
Lynch A
FN
Fox NC
HJ
Hardy J
AR
Albin RL
AL
Apostolova LG
AS
Arnold SE
AS
Asthana S
AC
Atwood CS
BC
Baldwin CT
BL
Barnes LL
BS
Barral S
BT
Beach TG
BJ
Becker JT
BE
Bigio EH
BT
Bird TD
BB
Boeve BF
BJ
Bowen JD
BA
Boxer A
BJ
Burke JR
BJ
Burns JM
BJ
Buxbaum JD
CN
Cairns NJ
CC
Cao C
CC
Carlson CS
CC
Carlsson CM
CR
Carney RM
CM
Carrasquillo MM
CS
Carroll SL
DC
Diaz CC
CH
Chui HC
CD
Clark DG
CD
Cribbs DH
CE
Crocco EA
DC
DeCarli C
DM
Dick M
DR
Duara R
ED
Evans DA
FK
Faber KM
FK
Fallon KB
FD
Fardo DW
FM
Farlow MR
FS
Ferris S
FT
Foroud TM
GD
Galasko DR
GM
Gearing M
GD
Geschwind DH
GJ
Gilbert JR
GN
Graff-Radford NR
GR
Green RC
GJ
Growdon JH
HR
Hamilton RL
HL
Harrell LE
HL
Honig LS
HM
Huentelman MJ
HC
Hulette CM
HB
Hyman BT
JG
Jarvik GP
AE
Abner E
JL
Jin LW
JG
Jun G
KA
Karydas A
KJ
Kaye JA
KR
Kim R
KN
Kowall NW
KJ
Kramer JH
LF
LaFerla FM
LJ
Lah JJ
LJ
Leverenz JB
LA
Levey AI
LG
Li G
LA
Lieberman AP
LK
Lunetta KL
LC
Lyketsos CG
MD
Marson DC
MF
Martiniuk F
MD
Mash DC
ME
Masliah E
MW
McCormick WC
MS
McCurry SM
MA
McDavid AN
MA
McKee AC
MM
Mesulam M
MB
Miller BL
MC
Miller CA
MJ
Miller JW
MJ
Morris JC
MJ
Murrell JR
MA
Myers AJ
OS
O'Bryant S
OJ
Olichney JM
PV
Pankratz VS
PJ
Parisi JE
PH
Paulson HL
PW
Perry W
PE
Peskind E
PA
Pierce A
PW
Poon WW
PH
Potter H
QJ
Quinn JF
RA
Raj A
RM
Raskind M
RB
Reisberg B
RC
Reitz C
RJ
Ringman JM
RE
Roberson ED
RE
Rogaeva E
RH
Rosen HJ
RR
Rosenberg RN
SM
Sager MA
SA
Saykin AJ
SJ
Schneider JA
SL
Schneider LS
SW
Seeley WW
SA
Smith AG
SJ
Sonnen JA
SS
Spina S
SR
Stern RA
SR
Swerdlow RH
TR
Tanzi RE
TT
Thornton-Wells TA
TJ
Trojanowski JQ
TJ
Troncoso JC
VD
Van Deerlin VM
VE
Van Eldik LJ
VH
Vinters HV
VJ
Vonsattel JP
WS
Weintraub S
WK
Welsh-Bohmer KA
WK
Wilhelmsen KC
WJ
Williamson J
WT
Wingo TS
WR
Woltjer RL
WC
Wright CB
YC
Yu CE
YL
Yu L
GF
Garzia F
GF
Golamaully F
SG
Septier G
ES
Engelborghs S
VR
Vandenberghe R
DD
De Deyn PP
FC
Fernadez CM
BY
Benito YA
TH
Thonberg H
FC
Forsell C
LL
Lilius L
KA
Kinhult-Stählbom A
KL
Kilander L
BR
Brundin R
CL
Concari L
HS
Helisalmi S
KA
Koivisto AM
HA
Haapasalo A
DV
Dermecourt V
FN
Fievet N
HO
Hanon O
DC
Dufouil C
BA
Brice A
RK
Ritchie K
DB
Dubois B
HJ
Himali JJ
KC
Keene CD
TJ
Tschanz J
FA
Fitzpatrick AL
KW
Kukull WA
NM
Norton M
AT
Aspelund T
LE
Larson EB
MR
Munger R
RJ
Rotter JI
LR
Lipton RB
BM
Bullido MJ
HA
Hofman A
MT
Montine TJ
CE
Coto E
BE
Boerwinkle E
PR
Petersen RC
AV
Alvarez V
RF
Rivadeneira F
RE
Reiman EM
GM
Gallo M
OC
O'Donnell CJ
RJ
Reisch JS
BA
Bruni AC
RD
Royall DR
DM
Dichgans M
SM
Sano M
GD
Galimberti D
SG
St George-Hyslop P
SE
Scarpini E
TD
Tsuang DW
MM
Mancuso M
BU
Bonuccelli U
WA
Winslow AR
DA
Daniele A
WC
Wu CK
PO
Peters O
NB
Nacmias B
RM
Riemenschneider M
HR
Heun R
BC
Brayne C
RD
Rubinsztein DC
BJ
Bras J
GR
Guerreiro R
AA
Al-Chalabi A
SC
Shaw CE
CJ
Collinge J
MD
Mann D
TM
Tsolaki M
CJ
Clarimón J
SR
Sussams R
LS
Lovestone S
OM
O'Donovan MC
OM
Owen MJ
BT
Behrens TW
MS
Mead S
GA
Goate AM
UA
Uitterlinden AG
HC
Holmes C
CC
Cruchaga C
IM
Ingelsson M
BD
Bennett DA
PJ
Powell J
GT
Golde TE
GC
Graff C
DJ
De Jager PL
MK
Morgan K
EN
Ertekin-Taner N
CO
Combarros O
PB
Psaty BM
PP
Passmore P
YS
Younkin SG
BC
Berr C
GV
Gudnason V
RD
Rujescu D
DD
Dickson DW
DJ
Dartigues JF
DA
DeStefano AL
OS
Ortega-Cubero S
HH
Hakonarson H
CD
Campion D
BM
Boada M
KJ
Kauwe JK
FL
Farrer LA
VB
Van Broeckhoven C
IM
Ikram MA
JL
Jones L
HJ
Haines JL
TC
Tzourio C
LL
Launer LJ
EV
Escott-Price V
MR
Mayeux R
DJ
Deleuze JF
AN
Amin N
HP
Holmans PA
PM
Pericak-Vance MA
AP
Amouyel P
VD
van Duijn CM
RA
Ramirez A
WL
Wang LS
LJ
Lambert JC
SS
Seshadri S
WJ
Williams J
SG
Schellenberg GD
Chapter II

Abstract

Summary of the research findings

We identified rare coding variants associated with Alzheimer's disease in a three-stage case-control study of 85,133 subjects. In stage 1, we genotyped 34,174 samples using a whole-exome microarray. In stage 2, we tested associated variants (P < 1 × 10-4) in 35,962 independent samples using de novo genotyping and imputed genotypes. In stage 3, we used an additional 14,997 samples to test the most significant stage 2 associations (P < 5 × 10-8) using imputed genotypes. We observed three new genome-wide significant nonsynonymous variants associated with Alzheimer's disease: a protective variant in PLCG2 (rs72824905: p.Pro522Arg, P = 5.38 × 10-10, odds ratio (OR) = 0.68, minor allele frequency (MAF)cases = 0.0059, MAFcontrols = 0.0093), a risk variant in ABI3 (rs616338: p.Ser209Phe, P = 4.56 × 10-10, OR = 1.43, MAFcases = 0.011, MAFcontrols = 0.008), and a new genome-wide significant variant in TREM2 (rs143332484: p.Arg62His, P = 1.55 × 10-14, OR = 1.67, MAFcases = 0.0143, MAFcontrols = 0.0089), a known susceptibility gene for Alzheimer's disease. These protein-altering changes are in genes highly expressed in microglia and highlight an immune-related protein-protein interaction network enriched for previously identified risk genes in Alzheimer's disease. These genetic findings provide additional evidence that the microglia-mediated innate immune response contributes directly to the development of Alzheimer's disease.

up to 16,097 European ancestry cases, up to 18,077 European ancestry controls

Chapter III

Study Statistics

Key metrics and study information

85133
Total Participants
GWAS
Study Type
Yes
Replicated
up to 20,693 European ancestry cases, up to 30,266 European ancestry controls
Replication Participants
European
Ancestry
Canada, U.S., Austria, Belgium, France, Germany, Netherlands, Finland, Sweden, U.K., Greece, Italy, Spain, Iceland
Recruitment Country
Chapter IV

Analysis

Comprehensive review of health and genetic findings

Important Disclaimer: This review has been performed semi-automatically and is provided for informational purposes only. While we strive for accuracy, this analysis may contain errors, omissions, or misinterpretations of the original research. DNA Genics disclaims all liability for any inaccuracies, errors, or consequences arising from the use of this information. Users should independently verify all information and consult original research publications before making any decisions based on this content. This analysis is not intended as a substitute for professional scientific review or medical advice.

Analysis In Progress

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