The Correlation between Inflammatory Biomarkers and Polygenic Risk Score in Alzheimer's Disease

被引：49

作者：

Morgan, Angharad R. ^{[1
]}

Touchard, Samuel ^{[1
]}

O'Hagan, Caroline ^{[1
]}

Sims, Rebecca ^{[2
]}

Majounie, Elisa ^{[2
]}

Escott-Price, Valentina ^{[2
]}

Jones, Lesley ^{[2
]}

Williams, Julie ^{[2
]}

Morgan, B. Paul ^{[1
]}

机构：

[1] Cardiff Univ, Sch Med, Div Infect & Immun, Heath Pk, Cardiff CF14 4XN, S Glam, Wales

[2] Cardiff Univ, Sch Med, Div Psychol Med & Clin Neurosci, Cardiff CF10 3AX, S Glam, Wales

来源：

JOURNAL OF ALZHEIMERS DISEASE | 2017年 / 56卷 / 01期

基金：

英国惠康基金; 英国医学研究理事会;

关键词：

Alzheimer's disease; biomarker; complement; inflammation; polygenic risk score; PLASMA CLUSTERIN CONCENTRATION; GENOME-WIDE ASSOCIATION; IDENTIFIES VARIANTS; CLU; PROGRESSION; COMPLEMENT; PICALM; CR-1; LOCI; METAANALYSIS;

D O I：

10.3233/JAD-160889

中图分类号：

Q189 [神经科学];

学科分类号：

071006 ;

摘要：

Plasma biomarkers to aid the early diagnosis of Alzheimer's disease (AD) or to monitor disease progression have long been sought and continue to be widely studied. Biomarkers that correlate with AD polygenic risk score, a measure of the polygenic architecture of the disease and highly predictive of AD status, would be excellent candidates. Therefore, we undertook a preliminary study to assess the association of plasma inflammatory biomarkers with an overall AD polygenic risk score as well as with an inflammation-specific AD polygenic risk score in a sample set of 93 AD cases. We measured five complement biomarkers [complement receptor 1 (CR1), clusterin, complement component 9 (C9), C1 inhibitor (C1inh), terminal complement complex (TCC)] and the benchmark inflammatory marker C-reactive protein (CRP). Plasma clusterin level showed an association with overall AD polygenic risk score, while clusterin, C1inh, and CRP levels each displayed some association with the inflammatory-specific AD polygenic risk score. The results suggest that elevated plasma levels of inflammatory biomarkers, including complement proteins, associate with polygenic risk scores in AD, further strengthening the link between genetic and biomarker disease predictors and indicating a potential role for these markers in disease prediction and patient stratification in AD.

引用

页码：25 / 36

页数：12

共 39 条

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Hakobyan, Svetlana ;

Harding, Katharine ;

Aiyaz, Mohammed ;

Hye, Abdul ;

Dobson, Richard ;

Baird, Alison ;

Liu, Benjamine ;

Harris, Claire Louise ;

Lovestone, Simon ;

Morgan, Bryan Paul .

JOURNAL OF ALZHEIMERS DISEASE, 2016, 54 (02) :707-716

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Harold, Denise ;

Abraham, Richard ;

Hollingworth, Paul ;

Sims, Rebecca ;

Gerrish, Amy ;

Hamshere, Marian L. ;

Pahwa, Jaspreet Singh ;

Moskvina, Valentina ;

Dowzell, Kimberley ;

Williams, Amy ;

Jones, Nicola ;

Thomas, Charlene ;

Stretton, Alexandra ;

Morgan, Angharad R. ;

Lovestone, Simon ;

Powell, John ;

Proitsi, Petroula ;

Lupton, Michelle K. ;

Brayne, Carol ;

Rubinsztein, David C. ;

Gill, Michael ;

Lawlor, Brian ;

Lynch, Aoibhinn ;

Morgan, Kevin ;

Brown, Kristelle S. ;

Passmore, Peter A. ;

Craig, David ;

McGuinness, Bernadette ;

Todd, Stephen ;

Holmes, Clive ;

Mann, David ;

Smith, A. David ;

Love, Seth ;

Kehoe, Patrick G. ;

Hardy, John ;

Mead, Simon ;

Fox, Nick ;

Rossor, Martin ;

Collinge, John ;

Maier, Wolfgang ;

Jessen, Frank ;

Schuermann, Britta ;

van den Bussche, Hendrik ;

Heuser, Isabella ;

Kornhuber, Johannes ;

Wiltfang, Jens ;

Dichgans, Martin ;

Froelich, Lutz ;

Hampel, Harald ;

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Hooper, C. ;

Rijsdijk, F. ;

Tabrizi, S. J. ;

Banner, S. ;

Shaw, C. E. ;

Foy, C. ;

Poppe, M. ;

Archer, N. ;

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Ward, M. ;

Lovestone, S. .

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Jones, Lesley ;

Lambert, Jean-Charles ;

Wang, Li-San ;

Choi, Seung-Hoan ;

Harold, Denise ;

Vedernikov, Alexey ;

Escott-Price, Valentina ;

Stone, Timothy ;

Richards, Alexander ;

Bellenguez, Celine ;

Ibrahim-Verbaas, Carla A. ;

Naj, Adam C. ;

Sims, Rebecca ;

Gerrish, Amy ;

Jun, Gyungah ;

DeStefano, Anita L. ;

Bis, Joshua C. ;

Beecham, Gary W. ;

Grenier-Boley, Benjamin ;

Russo, Giancarlo ;

Thornton-Wells, Tricia A. ;

Jones, Nicola ;

Smith, Albert V. ;

Chouraki, Vincent ;

Thomas, Charlene ;

Ikram, M. Arfan ;

Zelenika, Diana ;

Vardarajan, Badri N. ;

Kamatani, Yoichiro ;

Lin, Chiao-Feng ;

Schmidt, Helena ;

Kunkle, Brian W. ;

Dunstan, Melanie L. ;

Ruiz, Agustin ;

Bihoreau, Marie-Therese ;

Reitz, Christiane ;

Pasquier, Florence ;

Hollingworth, Paul ;

Hanon, Olivier ;

Fitzpatrick, Annette L. ;

Buxbaum, Joseph D. ;

Campion, Dominique ;

Crane, Paul K. ;

Becker, Tim ;

Gudnason, Vilmundur ;

Cruchaga, Carlos ;

Craig, David ;

Amin, Najaf ;

Berr, Claudine ;

Lopez, Oscar L. .

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[15] Genetic Evidence Implicates the Immune System and Cholesterol Metabolism in the Aetiology of Alzheimer's Disease [J].

Jones, Lesley ;

Holmans, Peter A. ;

Hamshere, Marian L. ;

Harold, Denise ;

Moskvina, Valentina ;

Ivanov, Dobril ;

Pocklington, Andrew ;

Abraham, Richard ;

Hollingworth, Paul ;

Sims, Rebecca ;

Gerrish, Amy ;

Pahwa, Jaspreet Singh ;

Jones, Nicola ;

Stretton, Alexandra ;

Morgan, Angharad R. ;

Lovestone, Simon ;

Powell, John ;

Proitsi, Petroula ;

Lupton, Michelle K. ;

Brayne, Carol ;

Rubinsztein, David C. ;

Gill, Michael ;

Lawlor, Brian ;

Lynch, Aoibhinn ;

Morgan, Kevin ;

Brown, Kristelle S. ;

Passmore, Peter A. ;

Craig, David ;

McGuinness, Bernadette ;

Todd, Stephen ;

Holmes, Clive ;

Mann, David ;

Smith, A. David ;

Love, Seth ;

Kehoe, Patrick G. ;

Mead, Simon ;

Fox, Nick ;

Rossor, Martin ;

Collinge, John ;

Maier, Wolfgang ;

Jessen, Frank ;

Schuermann, Britta ;

van den Bussche, Hendrik ;

Heuser, Isabella ;

Peters, Oliver ;

Kornhuber, Johannes ;

Wiltfang, Jens ;

Dichgans, Martin ;

Froelich, Lutz ;

Hampel, Harald .

PLOS ONE, 2010, 5 (11)

[16] Clusterin Levels in Plasma Predict Cognitive Decline and Progression to Alzheimer's Disease [J].

Jongbloed, Wesley ;

van Dijk, Karin D. ;

Mulder, Sandra D. ;

van de Berg, Wilma D. J. ;

Blankenstein, Marinus A. ;

van der Flier, Wiesje ;

Veerhuis, Robert .

JOURNAL OF ALZHEIMERS DISEASE, 2015, 46 (04) :1103-1110

[17] Variant of TREM2 Associated with the Risk of Alzheimer's Disease [J].

Jonsson, Thorlakur ;

Stefansson, Hreinn ;

Steinberg, Stacy ;

Jonsdottir, Ingileif ;

Jonsson, Palmi V. ;

Snaedal, Jon ;

Bjornsson, Sigurbjorn ;

Huttenlocher, Johanna ;

Levey, Allan I. ;

Lah, James J. ;

Rujescu, Dan ;

Hampel, Harald ;

Giegling, Ina ;

Andreassen, Ole A. ;

Engedal, Knut ;

Ulstein, Ingun ;

Djurovic, Srdjan ;

Ibrahim-Verbaas, Carla ;

Hofman, Albert ;

Ikram, M. Arfan ;

van Duijn, Cornelia M. ;

Thorsteinsdottir, Unnur ;

Kong, Augustine ;

Stefansson, Kari .

NEW ENGLAND JOURNAL OF MEDICINE, 2013, 368 (02) :107-116

[18] Meta-analysis Confirms CR1, CLU, and PICALM as Alzheimer Disease Risk Loci and Reveals Interactions With APOE Genotypes [J].

Jun, Gyungah ;

Naj, Adam C. ;

Beecham, Gary W. ;

Wang, Li-San ;

Buros, Jacqueline ;

Gallins, Paul J. ;

Buxbaum, Joseph D. ;

Ertekin-Taner, Nilufer ;

Fallin, Daniele ;

Friedland, Robert ;

Inzelberg, Rivka ;

Kramer, Patricia ;

Rogaeva, Ekaterina ;

George-Hyslop, Peter St. ;

Cantwell, Laura B. ;

Dombroski, Beth A. ;

Saykin, Andrew J. ;

Reiman, Eric M. ;

Bennett, David A. ;

Morris, John C. ;

Lunetta, Kathryn L. ;

Martin, Eden R. ;

Montine, Thomas J. ;

Goate, Alison M. ;

Blacker, Deborah ;

Tsuang, Debby W. ;

Beekly, Duane ;

Cupples, L. Adrienne ;

Hakonarson, Hakon ;

Kukull, Walter ;

Foroud, Tatiana M. ;

Haines, Jonathan ;

Mayeux, Richard ;

Farrer, Lindsay A. ;

Pericak-Vance, Margaret A. ;

Schellenberg, Gerard D. .

ARCHIVES OF NEUROLOGY, 2010, 67 (12) :1473-1484

[19] Candidate Blood Proteome Markers of Alzheimer's Disease Onset and Progression: A Systematic Review and Replication Study [J].

Kiddle, Steven J. ;

Sattlecker, Martina ;

Proitsi, Petroula ;

Simmons, Andrew ;

Westman, Eric ;

Bazenet, Chantal ;

Nelson, Sally K. ;

Williams, Stephen ;

Hodges, Angela ;

Johnston, Caroline ;

Soininen, Hilkka ;

Kloszewska, Iwona ;

Mecocci, Patrizia ;

Tsolaki, Magda ;

Vellas, Bruno ;

Newhouse, Stephen ;

Lovestone, Simon ;

Dobson, Richard J. B. .

JOURNAL OF ALZHEIMERS DISEASE, 2014, 38 (03) :515-531

[20] Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease [J].

Lambert, Jean-Charles ;

Ibrahim-Verbaas, Carla A. ;

Harold, Denise ;

Naj, Adam C. ;

Sims, Rebecca ;

Bellenguez, Celine ;

Jun, Gyungah ;

DeStefano, Anita L. ;

Bis, Joshua C. ;

Beecham, Gary W. ;

Grenier-Boley, Benjamin ;

Russo, Giancarlo ;

Thornton-Wells, Tricia A. ;

Jones, Nicola ;

Smith, Albert V. ;

Chouraki, Vincent ;

Thomas, Charlene ;

Ikram, M. Arfan ;

Zelenika, Diana ;

Vardarajan, Badri N. ;

Kamatani, Yoichiro ;

Lin, Chiao-Feng ;

Gerrish, Amy ;

Schmidt, Helena ;

Kunkle, Brian ;

Dunstan, Melanie L. ;

Ruiz, Agustin ;

Bihoreau, Marie-Therese ;

Choi, Seung-Hoan ;

Reitz, Christiane ;

Pasquier, Florence ;

Hollingworth, Paul ;

Ramirez, Alfredo ;

Hanon, Olivier ;

Fitzpatrick, Annette L. ;

Buxbaum, Joseph D. ;

Campion, Dominique ;

Crane, Paul K. ;

Baldwin, Clinton ;

Becker, Tim ;

Gudnason, Vilmundur ;

Cruchaga, Carlos ;

Craig, David ;

Amin, Najaf ;

Berr, Claudine ;

Lopez, Oscar L. ;

De Jager, Philip L. ;

Deramecourt, Vincent ;

Johnston, Janet A. ;

Evans, Denis .

NATURE GENETICS, 2013, 45 (12) :1452-U206

← 1 2 3 4 →

共 39 条

[11] Complement Biomarkers as Predictors of Disease Progression in Alzheimer's Disease [J].

Hakobyan, Svetlana ;

Harding, Katharine ;

Aiyaz, Mohammed ;

Hye, Abdul ;

Dobson, Richard ;

Baird, Alison ;

Liu, Benjamine ;

Harris, Claire Louise ;

Lovestone, Simon ;

Morgan, Bryan Paul .

JOURNAL OF ALZHEIMERS DISEASE, 2016, 54 (02) :707-716

[12] Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease [J].

Harold, Denise ;

Abraham, Richard ;

Hollingworth, Paul ;

Sims, Rebecca ;

Gerrish, Amy ;

Hamshere, Marian L. ;

Pahwa, Jaspreet Singh ;

Moskvina, Valentina ;

Dowzell, Kimberley ;

Williams, Amy ;

Jones, Nicola ;

Thomas, Charlene ;

Stretton, Alexandra ;

Morgan, Angharad R. ;

Lovestone, Simon ;

Powell, John ;

Proitsi, Petroula ;

Lupton, Michelle K. ;

Brayne, Carol ;

Rubinsztein, David C. ;

Gill, Michael ;

Lawlor, Brian ;

Lynch, Aoibhinn ;

Morgan, Kevin ;

Brown, Kristelle S. ;

Passmore, Peter A. ;

Craig, David ;

McGuinness, Bernadette ;

Todd, Stephen ;

Holmes, Clive ;

Mann, David ;

Smith, A. David ;

Love, Seth ;

Kehoe, Patrick G. ;

Hardy, John ;

Mead, Simon ;

Fox, Nick ;

Rossor, Martin ;

Collinge, John ;

Maier, Wolfgang ;

Jessen, Frank ;

Schuermann, Britta ;

van den Bussche, Hendrik ;

Heuser, Isabella ;

Kornhuber, Johannes ;

Wiltfang, Jens ;

Dichgans, Martin ;

Froelich, Lutz ;

Hampel, Harald ;

Huell, Michael .

NATURE GENETICS, 2009, 41 (10) :1088-U61

[13] Proteome-based plasma biomarkers for Alzheimer's disease [J].

Hye, A. ;

Lynham, S. ;

Thambisetty, M. ;

Causevic, M. ;

Campbell, J. ;

Byers, H. L. ;

Hooper, C. ;

Rijsdijk, F. ;

Tabrizi, S. J. ;

Banner, S. ;

Shaw, C. E. ;

Foy, C. ;

Poppe, M. ;

Archer, N. ;

Hamilton, G. ;

Powell, J. ;

Brown, R. G. ;

Sham, P. ;

Ward, M. ;

Lovestone, S. .

BRAIN, 2006, 129 :3042-3050

[14] Convergent genetic and expression data implicate immunity in Alzheimer's disease [J].

Jones, Lesley ;

Lambert, Jean-Charles ;

Wang, Li-San ;

Choi, Seung-Hoan ;

Harold, Denise ;

Vedernikov, Alexey ;

Escott-Price, Valentina ;

Stone, Timothy ;

Richards, Alexander ;

Bellenguez, Celine ;

Ibrahim-Verbaas, Carla A. ;

Naj, Adam C. ;

Sims, Rebecca ;

Gerrish, Amy ;

Jun, Gyungah ;

DeStefano, Anita L. ;

Bis, Joshua C. ;

Beecham, Gary W. ;

Grenier-Boley, Benjamin ;

Russo, Giancarlo ;

Thornton-Wells, Tricia A. ;

Jones, Nicola ;

Smith, Albert V. ;

Chouraki, Vincent ;

Thomas, Charlene ;

Ikram, M. Arfan ;

Zelenika, Diana ;

Vardarajan, Badri N. ;

Kamatani, Yoichiro ;

Lin, Chiao-Feng ;

Schmidt, Helena ;

Kunkle, Brian W. ;

Dunstan, Melanie L. ;

Ruiz, Agustin ;

Bihoreau, Marie-Therese ;

Reitz, Christiane ;

Pasquier, Florence ;

Hollingworth, Paul ;

Hanon, Olivier ;

Fitzpatrick, Annette L. ;

Buxbaum, Joseph D. ;

Campion, Dominique ;

Crane, Paul K. ;

Becker, Tim ;

Gudnason, Vilmundur ;

Cruchaga, Carlos ;

Craig, David ;

Amin, Najaf ;

Berr, Claudine ;

Lopez, Oscar L. .

ALZHEIMERS & DEMENTIA, 2015, 11 (06) :658-671

[15] Genetic Evidence Implicates the Immune System and Cholesterol Metabolism in the Aetiology of Alzheimer's Disease [J].

Jones, Lesley ;

Holmans, Peter A. ;

Hamshere, Marian L. ;

Harold, Denise ;

Moskvina, Valentina ;

Ivanov, Dobril ;

Pocklington, Andrew ;

Abraham, Richard ;

Hollingworth, Paul ;

Sims, Rebecca ;

Gerrish, Amy ;

Pahwa, Jaspreet Singh ;

Jones, Nicola ;

Stretton, Alexandra ;

Morgan, Angharad R. ;

Lovestone, Simon ;

Powell, John ;

Proitsi, Petroula ;

Lupton, Michelle K. ;

Brayne, Carol ;

Rubinsztein, David C. ;

Gill, Michael ;

Lawlor, Brian ;

Lynch, Aoibhinn ;

Morgan, Kevin ;

Brown, Kristelle S. ;

Passmore, Peter A. ;

Craig, David ;

McGuinness, Bernadette ;

Todd, Stephen ;

Holmes, Clive ;

Mann, David ;

Smith, A. David ;

Love, Seth ;

Kehoe, Patrick G. ;

Mead, Simon ;

Fox, Nick ;

Rossor, Martin ;

Collinge, John ;

Maier, Wolfgang ;

Jessen, Frank ;

Schuermann, Britta ;

van den Bussche, Hendrik ;

Heuser, Isabella ;

Peters, Oliver ;

Kornhuber, Johannes ;

Wiltfang, Jens ;

Dichgans, Martin ;

Froelich, Lutz ;

Hampel, Harald .

PLOS ONE, 2010, 5 (11)

[16] Clusterin Levels in Plasma Predict Cognitive Decline and Progression to Alzheimer's Disease [J].

Jongbloed, Wesley ;

van Dijk, Karin D. ;

Mulder, Sandra D. ;

van de Berg, Wilma D. J. ;

Blankenstein, Marinus A. ;

van der Flier, Wiesje ;

Veerhuis, Robert .

JOURNAL OF ALZHEIMERS DISEASE, 2015, 46 (04) :1103-1110

[17] Variant of TREM2 Associated with the Risk of Alzheimer's Disease [J].

Jonsson, Thorlakur ;

Stefansson, Hreinn ;

Steinberg, Stacy ;

Jonsdottir, Ingileif ;

Jonsson, Palmi V. ;

Snaedal, Jon ;

Bjornsson, Sigurbjorn ;

Huttenlocher, Johanna ;

Levey, Allan I. ;

Lah, James J. ;

Rujescu, Dan ;

Hampel, Harald ;

Giegling, Ina ;

Andreassen, Ole A. ;

Engedal, Knut ;

Ulstein, Ingun ;

Djurovic, Srdjan ;

Ibrahim-Verbaas, Carla ;

Hofman, Albert ;

Ikram, M. Arfan ;

van Duijn, Cornelia M. ;

Thorsteinsdottir, Unnur ;

Kong, Augustine ;

Stefansson, Kari .

NEW ENGLAND JOURNAL OF MEDICINE, 2013, 368 (02) :107-116

[18] Meta-analysis Confirms CR1, CLU, and PICALM as Alzheimer Disease Risk Loci and Reveals Interactions With APOE Genotypes [J].

Jun, Gyungah ;

Naj, Adam C. ;

Beecham, Gary W. ;

Wang, Li-San ;

Buros, Jacqueline ;

Gallins, Paul J. ;

Buxbaum, Joseph D. ;

Ertekin-Taner, Nilufer ;

Fallin, Daniele ;

Friedland, Robert ;

Inzelberg, Rivka ;

Kramer, Patricia ;

Rogaeva, Ekaterina ;

George-Hyslop, Peter St. ;

Cantwell, Laura B. ;

Dombroski, Beth A. ;

Saykin, Andrew J. ;

Reiman, Eric M. ;

Bennett, David A. ;

Morris, John C. ;

Lunetta, Kathryn L. ;

Martin, Eden R. ;

Montine, Thomas J. ;

Goate, Alison M. ;

Blacker, Deborah ;

Tsuang, Debby W. ;

Beekly, Duane ;

Cupples, L. Adrienne ;

Hakonarson, Hakon ;

Kukull, Walter ;

Foroud, Tatiana M. ;

Haines, Jonathan ;

Mayeux, Richard ;

Farrer, Lindsay A. ;

Pericak-Vance, Margaret A. ;

Schellenberg, Gerard D. .

ARCHIVES OF NEUROLOGY, 2010, 67 (12) :1473-1484

[19] Candidate Blood Proteome Markers of Alzheimer's Disease Onset and Progression: A Systematic Review and Replication Study [J].

Kiddle, Steven J. ;

Sattlecker, Martina ;

Proitsi, Petroula ;

Simmons, Andrew ;

Westman, Eric ;

Bazenet, Chantal ;

Nelson, Sally K. ;

Williams, Stephen ;

Hodges, Angela ;

Johnston, Caroline ;

Soininen, Hilkka ;

Kloszewska, Iwona ;

Mecocci, Patrizia ;

Tsolaki, Magda ;

Vellas, Bruno ;

Newhouse, Stephen ;

Lovestone, Simon ;

Dobson, Richard J. B. .

JOURNAL OF ALZHEIMERS DISEASE, 2014, 38 (03) :515-531

[20] Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease [J].

Lambert, Jean-Charles ;

Ibrahim-Verbaas, Carla A. ;

Harold, Denise ;

Naj, Adam C. ;

Sims, Rebecca ;

Bellenguez, Celine ;

Jun, Gyungah ;

DeStefano, Anita L. ;

Bis, Joshua C. ;

Beecham, Gary W. ;

Grenier-Boley, Benjamin ;

Russo, Giancarlo ;

Thornton-Wells, Tricia A. ;

Jones, Nicola ;

Smith, Albert V. ;

Chouraki, Vincent ;

Thomas, Charlene ;

Ikram, M. Arfan ;

Zelenika, Diana ;

Vardarajan, Badri N. ;

Kamatani, Yoichiro ;

Lin, Chiao-Feng ;

Gerrish, Amy ;

Schmidt, Helena ;

Kunkle, Brian ;

Dunstan, Melanie L. ;

Ruiz, Agustin ;

Bihoreau, Marie-Therese ;

Choi, Seung-Hoan ;

Reitz, Christiane ;

Pasquier, Florence ;

Hollingworth, Paul ;

Ramirez, Alfredo ;

Hanon, Olivier ;

Fitzpatrick, Annette L. ;

Buxbaum, Joseph D. ;

Campion, Dominique ;

Crane, Paul K. ;

Baldwin, Clinton ;

Becker, Tim ;

Gudnason, Vilmundur ;

Cruchaga, Carlos ;

Craig, David ;

Amin, Najaf ;

Berr, Claudine ;

Lopez, Oscar L. ;

De Jager, Philip L. ;

Deramecourt, Vincent ;

Johnston, Janet A. ;

Evans, Denis .

NATURE GENETICS, 2013, 45 (12) :1452-U206

← 1 2 3 4 →