Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus

被引：672

作者：

Bentham, James ^{[1
]}

Morris, David L. ^{[1
]}

Graham, Deborah S. Cunninghame ^{[1
]}

Pinder, Christopher L. ^{[1
]}

Tombleson, Philip ^{[1
]}

Behrens, Timothy W. ^{[2
]}

Martin, Javier ^{[3
]}

Fairfax, Benjamin P. ^{[4
]}

Knight, Julian C. ^{[4
]}

Chen, Lingyan ^{[1
]}

Replogle, Joseph ^{[5
]}

Syvanen, Ann-Christine ^{[6
]}

Ronnblom, Lars ^{[6
]}

Graham, Robert R. ^{[2
]}

Wither, Joan E. ^{[7
]}

Rioux, John D. ^{[8
,9
]}

Alarcon-Riquelme, Marta E. ^{[10
]}

Vyse, Timothy J. ^{[1
,11
]}

机构：

[1] Kings Coll London, Div Genet & Mol Med, London WC2R 2LS, England

[2] Genentech Inc, San Francisco, CA 94080 USA

[3] CSIC, Inst Parasitol & Biomed Lopez Neyra, Granada, Spain

[4] Univ Oxford, Wellcome Trust Ctr Human Genet, Oxford, England

[5] Harvard Univ, Sch Med, Boston, MA USA

[6] Uppsala Univ, Dept Med Sci, Sci Life Lab, Uppsala, Sweden

[7] Univ Hlth Network, TWRI, Toronto, ON, Canada

[8] Univ Montreal, Genet & Genom Med Inflammat, Montreal, PQ, Canada

[9] Montreal Heart Inst, Montreal, PQ H1T 1C8, Canada

[10] Pfizer Univ Granada Junta Andalucia, Ctr Genom & Invest Oncol GENYO, Granada, Spain

[11] Kings Coll London, Div Immunol Infect & Inflammatory Dis, London WC2R 2LS, England

来源：

NATURE GENETICS | 2015年 / 47卷 / 12期

基金：

瑞典研究理事会; 加拿大健康研究院; 英国惠康基金; 美国国家卫生研究院;

关键词：

GENOME-WIDE ASSOCIATION; POPULATION STRATIFICATION; SUSCEPTIBILITY VARIANTS; HLA ALLELES; T-CELLS; POLYMORPHISM; AUTOIMMUNE; EXPRESSION; RISK; IMPUTATION;

D O I：

10.1038/ng.3434

中图分类号：

Q3 [遗传学];

学科分类号：

071007 ; 090102 ;

摘要：

Systemic lupus erythematosus (SLE) is a genetically complex autoimmune disease characterized by loss of immune tolerance to nuclear and cell surface antigens. Previous genome-wide association studies (GWAS) had modest sample sizes, reducing their scope and reliability. Our study comprised 7,219 cases and 15,991 controls of European ancestry, constituting a new GWAS, a meta-analysis with a published GWAS and a replication study. We have mapped 43 susceptibility loci, including ten new associations. Assisted by dense genome coverage, imputation provided evidence for missense variants underpinning associations in eight genes. Other likely causal genes were established by examining associated alleles for cis-acting eQTL effects in a range of ex vivo immune cells. We found an over-representation (n = 16) of transcription factors among SLE susceptibility genes. This finding supports the view that aberrantly regulated gene expression networks in multiple cell types in both the innate and adaptive immune response contribute to the risk of developing SLE.

引用

页码：1457 / +

页数：11

共 80 条

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Adrianto, Indra ;

Wen, Feng ;

Templeton, Amanda ;

Wiley, Graham ;

King, Jarrod B. ;

Lessard, Christopher J. ;

Bates, Jared S. ;

Hu, Yanqing ;

Kelly, Jennifer A. ;

Kaufman, Kenneth M. ;

Guthridge, Joel M. ;

Alarcon-Riquelme, Marta E. ;

Anaya, Juan-Manuel ;

Bae, Sang-Cheol ;

Bang, So-Young ;

Boackle, Susan A. ;

Brown, Elizabeth E. ;

Petri, Michelle A. ;

Gallant, Caroline ;

Ramsey-Goldman, Rosalind ;

Reveille, John D. ;

Vila, Luis M. ;

Criswell, Lindsey A. ;

Edberg, Jeffrey C. ;

Freedman, Barry I. ;

Gregersen, Peter K. ;

Gilkeson, Gary S. ;

Jacob, Chaim O. ;

James, Judith A. ;

Kamen, Diane L. ;

Kimberly, Robert P. ;

Martin, Javier ;

Merrill, Joan T. ;

Niewold, Timothy B. ;

Park, So-Yeon ;

Pons-Estel, Bernardo A. ;

Scofield, R. Hal ;

Stevens, Anne M. ;

Tsao, Betty P. ;

Vyse, Timothy J. ;

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Alarcón-Riquelme, ME ;

Cardiel, MH ;

Caeiro, F ;

Massardo, L ;

Villa, AR ;

Pons-Estel, BA .

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Sattler, Arne ;

Templin, Lars ;

Kohler, Siegfried ;

Gross, Christian ;

Meisel, Andreas ;

Sawitzki, Birgit ;

Burmester, Gerd-Ruediger ;

Arnold, Renate ;

Radbruch, Andreas ;

Thiel, Andreas ;

Hiepe, Falk .

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Durbin, Richard M. ;

Abecasis, Goncalo R. ;

Bentley, David R. ;

Chakravarti, Aravinda ;

Clark, Andrew G. ;

Donnelly, Peter ;

Eichler, Evan E. ;

Flicek, Paul ;

Gabriel, Stacey B. ;

Gibbs, Richard A. ;

Green, Eric D. ;

Hurles, Matthew E. ;

Knoppers, Bartha M. ;

Korbel, Jan O. ;

Lander, Eric S. ;

Lee, Charles ;

Lehrach, Hans ;

Mardis, Elaine R. ;

Marth, Gabor T. ;

McVean, Gil A. ;

Nickerson, Deborah A. ;

Schmidt, Jeanette P. ;

Sherry, Stephen T. ;

Wang, Jun ;

Wilson, Richard K. ;

Gibbs, Richard A. ;

Dinh, Huyen ;

Kovar, Christie ;

Lee, Sandra ;

Lewis, Lora ;

Muzny, Donna ;

Reid, Jeff ;

Wang, Min ;

Wang, Jun ;

Fang, Xiaodong ;

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Jiang, Hui ;

Jin, Xin ;

Li, Guoqing ;

Li, Jingxiang ;

Li, Yingrui ;

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Su, Zhe ;

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[5] The expanding genetic overlap between multiple sclerosis and type I diabetes [J].

Booth, David R. ;

Heard, Robert N. ;

Stewart, Graeme J. ;

Goris, An ;

Dobosi, Rita ;

Dubois, Benedicte ;

Lorentzen, Aslaug R. ;

Celius, Elisabeth G. ;

Harbo, Hanne F. ;

Spurkland, Anne ;

Olsson, Tomas ;

Kockum, Ingrid ;

Link, Jenny ;

Hillert, Jan ;

Ban, Maria ;

Baker, Amie ;

Sawcer, Stephen ;

Compston, Alastair ;

Mihalova, Tania ;

Strange, Richard ;

Hawkins, Clive ;

Ingram, Gillian ;

Robertson, Neil P. ;

De Jager, Philip L. ;

Hafler, David A. ;

Barcellos, Lisa F. ;

Ivinson, Adrian J. ;

Pericak-Vance, Margaret ;

Oksenberg, Jorge R. ;

Hauser, Stephen L. ;

McCauley, Jacob L. ;

Sexton, David ;

Haines, Jonathan .

GENES AND IMMUNITY, 2009, 10 (01) :11-14

[6] The rs4774 CIITA missense variant is associated with risk of systemic lupus erythematosus [J].

Bronson, P. G. ;

Goldstein, B. A. ;

Ramsay, P. P. ;

Beckman, K. B. ;

Noble, J. A. ;

Lane, J. A. ;

Seldin, M. F. ;

Kelly, J. A. ;

Harley, J. B. ;

Moser, K. L. ;

Gaffney, P. M. ;

Behrens, T. W. ;

Criswell, L. A. ;

Barcellos, L. F. .

GENES AND IMMUNITY, 2011, 12 (08) :667-671

[7] Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls [J].

Burton, Paul R. ;

Clayton, David G. ;

Cardon, Lon R. ;

Craddock, Nick ;

Deloukas, Panos ;

Duncanson, Audrey ;

Kwiatkowski, Dominic P. ;

McCarthy, Mark I. ;

Ouwehand, Willem H. ;

Samani, Nilesh J. ;

Todd, John A. ;

Donnelly, Peter ;

Barrett, Jeffrey C. ;

Davison, Dan ;

Easton, Doug ;

Evans, David ;

Leung, Hin-Tak ;

Marchini, Jonathan L. ;

Morris, Andrew P. ;

Spencer, Chris C. A. ;

Tobin, Martin D. ;

Attwood, Antony P. ;

Boorman, James P. ;

Cant, Barbara ;

Everson, Ursula ;

Hussey, Judith M. ;

Jolley, Jennifer D. ;

Knight, Alexandra S. ;

Koch, Kerstin ;

Meech, Elizabeth ;

Nutland, Sarah ;

Prowse, Christopher V. ;

Stevens, Helen E. ;

Taylor, Niall C. ;

Walters, Graham R. ;

Walker, Neil M. ;

Watkins, Nicholas A. ;

Winzer, Thilo ;

Jones, Richard W. ;

McArdle, Wendy L. ;

Ring, Susan M. ;

Strachan, David P. ;

Pembrey, Marcus ;

Breen, Gerome ;

St Clair, David ;

Caesar, Sian ;

Gordon-Smith, Katherine ;

Jones, Lisa ;

Fraser, Christine ;

Green, Elain K. .

NATURE, 2007, 447 (7145) :661-678

[8] ABIN1 Dysfunction as a Genetic Basis for Lupus Nephritis [J].

Caster, Dawn J. ;

Korte, Erik A. ;

Nanda, Sambit K. ;

McLeish, Kenneth R. ;

Oliver, Rebecca K. ;

G'Sell, Rachel T. ;

Sheehan, Ryan M. ;

Freeman, Darrell W. ;

Coventry, Susan C. ;

Kelly, Jennifer A. ;

Guthridge, Joel M. ;

James, Judith A. ;

Sivils, Kathy L. ;

Alarcon-Riquelme, Marta E. ;

Scofield, R. Hal ;

Adrianto, Indra ;

Gaffney, Patrick M. ;

Stevens, Anne M. ;

Freedman, Barry I. ;

Langefeld, Carl D. ;

Tsao, Betty P. ;

Pons-Estel, Bernardo A. ;

Jacob, Chaim O. ;

Kamen, Diane L. ;

Gilkeson, Gary S. ;

Brown, Elizabeth E. ;

Alarcon, Graciela S. ;

Edberg, Jeffrey C. ;

Kimberly, Robert P. ;

Martin, Javier ;

Merrill, Joan T. ;

Harley, John B. ;

Kaufman, Kenneth M. ;

Reveille, John D. ;

Anaya, Juan-Manuel ;

Criswell, Lindsey A. ;

Vila, Luis M. ;

Petri, Michelle ;

Ramsey-Goldman, Rosalind ;

Bae, Sang-Cheol ;

Boackle, Susan A. ;

Vyse, Timothy J. ;

Niewold, Timothy B. ;

Cohen, Philip ;

Powell, David W. .

JOURNAL OF THE AMERICAN SOCIETY OF NEPHROLOGY, 2013, 24 (11) :1743-1754

[9] Genetic and physical interaction of the B-cell systemic lupus erythematosus-associated genes BANK1 and BLK [J].

Castillejo-Lopez, Casimiro ;

Delgado-Vega, Angelica M. ;

Wojcik, Jerome ;

Kozyrev, Sergey V. ;

Thavathiru, Elangovan ;

Wu, Ying-Yu ;

Sanchez, Elena ;

Pollmann, David ;

Lopez-Egido, Juan R. ;

Fineschi, Serena ;

Dominguez, Nicolas ;

Lu, Rufei ;

James, Judith A. ;

Merrill, Joan T. ;

Kelly, Jennifer A. ;

Kaufman, Kenneth M. ;

Moser, Kathy L. ;

Gilkeson, Gary ;

Frostegard, Johan ;

Pons-Estel, Bernardo A. ;

D'Alfonso, Sandra ;

Witte, Torsten ;

Luis Callejas, Jose ;

Harley, John B. ;

Gaffney, Patrick M. ;

Martin, Javier ;

Guthridge, Joel M. ;

Alarcon-Riquelme, Marta E. .

ANNALS OF THE RHEUMATIC DISEASES, 2012, 71 (01) :136-142

[10] Genetic variation near IRF8 is associated with serologic and cytokine profiles in systemic lupus erythematosus and multiple sclerosis [J].

Chrabot, B. S. ;

Kariuki, S. N. ;

Zervou, M. I. ;

Feng, X. ;

Arrington, J. ;

Jolly, M. ;

Boumpass, D. T. ;

Reder, A. T. ;

Goulielmos, G. N. ;

Niewold, T. B. .

GENES AND IMMUNITY, 2013, 14 (08) :471-478

← 1 2 3 4 5 6 7 8 →

共 80 条

[1] Association of a functional variant downstream of TNFAIP3 with systemic lupus erythematosus [J].

Adrianto, Indra ;

Wen, Feng ;

Templeton, Amanda ;

Wiley, Graham ;

King, Jarrod B. ;

Lessard, Christopher J. ;

Bates, Jared S. ;

Hu, Yanqing ;

Kelly, Jennifer A. ;

Kaufman, Kenneth M. ;

Guthridge, Joel M. ;

Alarcon-Riquelme, Marta E. ;

Anaya, Juan-Manuel ;

Bae, Sang-Cheol ;

Bang, So-Young ;

Boackle, Susan A. ;

Brown, Elizabeth E. ;

Petri, Michelle A. ;

Gallant, Caroline ;

Ramsey-Goldman, Rosalind ;

Reveille, John D. ;

Vila, Luis M. ;

Criswell, Lindsey A. ;

Edberg, Jeffrey C. ;

Freedman, Barry I. ;

Gregersen, Peter K. ;

Gilkeson, Gary S. ;

Jacob, Chaim O. ;

James, Judith A. ;

Kamen, Diane L. ;

Kimberly, Robert P. ;

Martin, Javier ;

Merrill, Joan T. ;

Niewold, Timothy B. ;

Park, So-Yeon ;

Pons-Estel, Bernardo A. ;

Scofield, R. Hal ;

Stevens, Anne M. ;

Tsao, Betty P. ;

Vyse, Timothy J. ;

Langefeld, Carl D. ;

Harley, John B. ;

Moser, Kathy L. ;

Webb, Carol F. ;

Humphrey, Mary Beth ;

Montgomery, Courtney Gray ;

Gaffney, Patrick M. .

NATURE GENETICS, 2011, 43 (03) :253-U102

[2] Familial aggregation of systemic lupus erythematosus, rheumatoid arthritis, and other autoimmune diseases in 1,177 lupus patients from the GLADEL cohort [J].

Alarcon-Segovia, D ;

Alarcón-Riquelme, ME ;

Cardiel, MH ;

Caeiro, F ;

Massardo, L ;

Villa, AR ;

Pons-Estel, BA .

ARTHRITIS AND RHEUMATISM, 2005, 52 (04) :1138-1147

[3] Foxp3+ Helios+ regulatory T cells are expanded in active systemic lupus erythematosus [J].

Alexander, Tobias ;

Sattler, Arne ;

Templin, Lars ;

Kohler, Siegfried ;

Gross, Christian ;

Meisel, Andreas ;

Sawitzki, Birgit ;

Burmester, Gerd-Ruediger ;

Arnold, Renate ;

Radbruch, Andreas ;

Thiel, Andreas ;

Hiepe, Falk .

ANNALS OF THE RHEUMATIC DISEASES, 2013, 72 (09) :1549-1558

[4] An integrated map of genetic variation from 1,092 human genomes [J].

Altshuler, David M. ;

Durbin, Richard M. ;

Abecasis, Goncalo R. ;

Bentley, David R. ;

Chakravarti, Aravinda ;

Clark, Andrew G. ;

Donnelly, Peter ;

Eichler, Evan E. ;

Flicek, Paul ;

Gabriel, Stacey B. ;

Gibbs, Richard A. ;

Green, Eric D. ;

Hurles, Matthew E. ;

Knoppers, Bartha M. ;

Korbel, Jan O. ;

Lander, Eric S. ;

Lee, Charles ;

Lehrach, Hans ;

Mardis, Elaine R. ;

Marth, Gabor T. ;

McVean, Gil A. ;

Nickerson, Deborah A. ;

Schmidt, Jeanette P. ;

Sherry, Stephen T. ;

Wang, Jun ;

Wilson, Richard K. ;

Gibbs, Richard A. ;

Dinh, Huyen ;

Kovar, Christie ;

Lee, Sandra ;

Lewis, Lora ;

Muzny, Donna ;

Reid, Jeff ;

Wang, Min ;

Wang, Jun ;

Fang, Xiaodong ;

Guo, Xiaosen ;

Jian, Min ;

Jiang, Hui ;

Jin, Xin ;

Li, Guoqing ;

Li, Jingxiang ;

Li, Yingrui ;

Li, Zhuo ;

Liu, Xiao ;

Lu, Yao ;

Ma, Xuedi ;

Su, Zhe ;

Tai, Shuaishuai ;

Tang, Meifang .

NATURE, 2012, 491 (7422) :56-65

[5] The expanding genetic overlap between multiple sclerosis and type I diabetes [J].

Booth, David R. ;

Heard, Robert N. ;

Stewart, Graeme J. ;

Goris, An ;

Dobosi, Rita ;

Dubois, Benedicte ;

Lorentzen, Aslaug R. ;

Celius, Elisabeth G. ;

Harbo, Hanne F. ;

Spurkland, Anne ;

Olsson, Tomas ;

Kockum, Ingrid ;

Link, Jenny ;

Hillert, Jan ;

Ban, Maria ;

Baker, Amie ;

Sawcer, Stephen ;

Compston, Alastair ;

Mihalova, Tania ;

Strange, Richard ;

Hawkins, Clive ;

Ingram, Gillian ;

Robertson, Neil P. ;

De Jager, Philip L. ;

Hafler, David A. ;

Barcellos, Lisa F. ;

Ivinson, Adrian J. ;

Pericak-Vance, Margaret ;

Oksenberg, Jorge R. ;

Hauser, Stephen L. ;

McCauley, Jacob L. ;

Sexton, David ;

Haines, Jonathan .

GENES AND IMMUNITY, 2009, 10 (01) :11-14

[6] The rs4774 CIITA missense variant is associated with risk of systemic lupus erythematosus [J].

Bronson, P. G. ;

Goldstein, B. A. ;

Ramsay, P. P. ;

Beckman, K. B. ;

Noble, J. A. ;

Lane, J. A. ;

Seldin, M. F. ;

Kelly, J. A. ;

Harley, J. B. ;

Moser, K. L. ;

Gaffney, P. M. ;

Behrens, T. W. ;

Criswell, L. A. ;

Barcellos, L. F. .

GENES AND IMMUNITY, 2011, 12 (08) :667-671

[7] Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls [J].

Burton, Paul R. ;

Clayton, David G. ;

Cardon, Lon R. ;

Craddock, Nick ;

Deloukas, Panos ;

Duncanson, Audrey ;

Kwiatkowski, Dominic P. ;

McCarthy, Mark I. ;

Ouwehand, Willem H. ;

Samani, Nilesh J. ;

Todd, John A. ;

Donnelly, Peter ;

Barrett, Jeffrey C. ;

Davison, Dan ;

Easton, Doug ;

Evans, David ;

Leung, Hin-Tak ;

Marchini, Jonathan L. ;

Morris, Andrew P. ;

Spencer, Chris C. A. ;

Tobin, Martin D. ;

Attwood, Antony P. ;

Boorman, James P. ;

Cant, Barbara ;

Everson, Ursula ;

Hussey, Judith M. ;

Jolley, Jennifer D. ;

Knight, Alexandra S. ;

Koch, Kerstin ;

Meech, Elizabeth ;

Nutland, Sarah ;

Prowse, Christopher V. ;

Stevens, Helen E. ;

Taylor, Niall C. ;

Walters, Graham R. ;

Walker, Neil M. ;

Watkins, Nicholas A. ;

Winzer, Thilo ;

Jones, Richard W. ;

McArdle, Wendy L. ;

Ring, Susan M. ;

Strachan, David P. ;

Pembrey, Marcus ;

Breen, Gerome ;

St Clair, David ;

Caesar, Sian ;

Gordon-Smith, Katherine ;

Jones, Lisa ;

Fraser, Christine ;

Green, Elain K. .

NATURE, 2007, 447 (7145) :661-678

[8] ABIN1 Dysfunction as a Genetic Basis for Lupus Nephritis [J].

Caster, Dawn J. ;

Korte, Erik A. ;

Nanda, Sambit K. ;

McLeish, Kenneth R. ;

Oliver, Rebecca K. ;

G'Sell, Rachel T. ;

Sheehan, Ryan M. ;

Freeman, Darrell W. ;

Coventry, Susan C. ;

Kelly, Jennifer A. ;

Guthridge, Joel M. ;

James, Judith A. ;

Sivils, Kathy L. ;

Alarcon-Riquelme, Marta E. ;

Scofield, R. Hal ;

Adrianto, Indra ;

Gaffney, Patrick M. ;

Stevens, Anne M. ;

Freedman, Barry I. ;

Langefeld, Carl D. ;

Tsao, Betty P. ;

Pons-Estel, Bernardo A. ;

Jacob, Chaim O. ;

Kamen, Diane L. ;

Gilkeson, Gary S. ;

Brown, Elizabeth E. ;

Alarcon, Graciela S. ;

Edberg, Jeffrey C. ;

Kimberly, Robert P. ;

Martin, Javier ;

Merrill, Joan T. ;

Harley, John B. ;

Kaufman, Kenneth M. ;

Reveille, John D. ;

Anaya, Juan-Manuel ;

Criswell, Lindsey A. ;

Vila, Luis M. ;

Petri, Michelle ;

Ramsey-Goldman, Rosalind ;

Bae, Sang-Cheol ;

Boackle, Susan A. ;

Vyse, Timothy J. ;

Niewold, Timothy B. ;

Cohen, Philip ;

Powell, David W. .

JOURNAL OF THE AMERICAN SOCIETY OF NEPHROLOGY, 2013, 24 (11) :1743-1754

[9] Genetic and physical interaction of the B-cell systemic lupus erythematosus-associated genes BANK1 and BLK [J].

Castillejo-Lopez, Casimiro ;

Delgado-Vega, Angelica M. ;

Wojcik, Jerome ;

Kozyrev, Sergey V. ;

Thavathiru, Elangovan ;

Wu, Ying-Yu ;

Sanchez, Elena ;

Pollmann, David ;

Lopez-Egido, Juan R. ;

Fineschi, Serena ;

Dominguez, Nicolas ;

Lu, Rufei ;

James, Judith A. ;

Merrill, Joan T. ;

Kelly, Jennifer A. ;

Kaufman, Kenneth M. ;

Moser, Kathy L. ;

Gilkeson, Gary ;

Frostegard, Johan ;

Pons-Estel, Bernardo A. ;

D'Alfonso, Sandra ;

Witte, Torsten ;

Luis Callejas, Jose ;

Harley, John B. ;

Gaffney, Patrick M. ;

Martin, Javier ;

Guthridge, Joel M. ;

Alarcon-Riquelme, Marta E. .

ANNALS OF THE RHEUMATIC DISEASES, 2012, 71 (01) :136-142

[10] Genetic variation near IRF8 is associated with serologic and cytokine profiles in systemic lupus erythematosus and multiple sclerosis [J].

Chrabot, B. S. ;

Kariuki, S. N. ;

Zervou, M. I. ;

Feng, X. ;

Arrington, J. ;

Jolly, M. ;

Boumpass, D. T. ;

Reder, A. T. ;

Goulielmos, G. N. ;

Niewold, T. B. .

GENES AND IMMUNITY, 2013, 14 (08) :471-478

← 1 2 3 4 5 6 7 8 →