Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks

Gina M. Peloso; Paul L. Auer; Joshua C. Bis; Arend Voorman; Alanna C. Morrison; Nathan O. Stitziel; Jennifer A. Brody; Sumeet A. Khetarpal; Jacy R. Crosby; Myriam Fornage; Aaron Isaacs; Johanna Jakobsdottir; Mary F. Feitosa; Gail Davies; Jennifer E. Huffman; Ani Manichaikul; Brian Davis; Kurt Lohman; Aron Y. Joon; Albert V. Smith; Megan L. Grove; Paolo Zanoni; Valeska Redon; Serkalem Demissie; Kim Lawson; Ulrike Peters; Christopher Carlson; Rebecca D. Jackson; Kelli K. Ryckman; Rachel H. MacKey; Jennifer G. Robinson; David S. Siscovick; Pamela J. Schreiner; Josyf C. Mychaleckyj; James S. Pankow; Albert Hofman; Andre G. Uitterlinden; Tamara B. Harris; Kent D. Taylor; Jeanette M. Stafford; Lindsay M. Reynolds; Riccardo E. Marioni; Abbas Dehghan; Oscar H. Franco; Aniruddh P. Patel; Yingchang Lu; George Hindy; Omri Gottesman; Erwin P. Bottinger; Olle Melander; Marju Orho-Melander; Ruth J F Loos; Stefano Duga; Piera Angelica Merlini; Martin Farrall; Anuj Goel; Rosanna Asselta; Domenico Girelli; Nicola Martinelli; Svati H. Shah; William E. Kraus; Mingyao Li; Daniel J. Rader; Muredach P. Reilly; Ruth McPherson; Hugh Watkins; Diego Ardissino; Qunyuan Zhang; Judy Wang; Michael Y. Tsai; Herman A. Taylor; Adolfo Correa; Michael E. Griswold; Leslie A. Lange; John M. Starr; Igor Rudan; Gudny Eiriksdottir; Lenore J. Launer; Jose M. Ordovas; Daniel Levy; Y. D Ida Chen; Alexander P. Reiner; Caroline Hayward; Ozren Polasek; Ian J. Deary; Ingrid B. Borecki; Yongmei Liu; Vilmundur Gudnason; James G. Wilson; Cornelia M. Van Duijn; Charles Kooperberg; Stephen S. Rich; Bruce M. Psaty; Jerome I. Rotter; Christopher J. O'Donnell; Kenneth Rice; Eric Boerwinkle; Sekar Kathiresan; L. Adrienne Cupples

doi:10.1016/j.ajhg.2014.01.009

Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks

Gina M. Peloso, Paul L. Auer, Joshua C. Bis, Arend Voorman, Alanna C. Morrison, Nathan O. Stitziel, Jennifer A. Brody, Sumeet A. Khetarpal, Jacy R. Crosby, Myriam Fornage, Aaron Isaacs, Johanna Jakobsdottir, Mary F. Feitosa, Gail Davies, Jennifer E. Huffman, Ani Manichaikul, Brian Davis, Kurt Lohman, Aron Y. Joon, Albert V. SmithMegan L. Grove, Paolo Zanoni, Valeska Redon, Serkalem Demissie, Kim Lawson, Ulrike Peters, Christopher Carlson, Rebecca D. Jackson, Kelli K. Ryckman, Rachel H. MacKey, Jennifer G. Robinson, David S. Siscovick, Pamela J. Schreiner, Josyf C. Mychaleckyj, James S. Pankow, Albert Hofman, Andre G. Uitterlinden, Tamara B. Harris, Kent D. Taylor, Jeanette M. Stafford, Lindsay M. Reynolds, Riccardo E. Marioni, Abbas Dehghan, Oscar H. Franco, Aniruddh P. Patel, Yingchang Lu, George Hindy, Omri Gottesman, Erwin P. Bottinger, Olle Melander, Marju Orho-Melander, Ruth J F Loos, Stefano Duga, Piera Angelica Merlini, Martin Farrall, Anuj Goel, Rosanna Asselta, Domenico Girelli, Nicola Martinelli, Svati H. Shah, William E. Kraus, Mingyao Li, Daniel J. Rader, Muredach P. Reilly, Ruth McPherson, Hugh Watkins, Diego Ardissino, Qunyuan Zhang, Judy Wang, Michael Y. Tsai, Herman A. Taylor, Adolfo Correa, Michael E. Griswold, Leslie A. Lange, John M. Starr, Igor Rudan, Gudny Eiriksdottir, Lenore J. Launer, Jose M. Ordovas, Daniel Levy, Y. D Ida Chen, Alexander P. Reiner, Caroline Hayward, Ozren Polasek, Ian J. Deary, Ingrid B. Borecki, Yongmei Liu, Vilmundur Gudnason, James G. Wilson, Cornelia M. Van Duijn, Charles Kooperberg, Stephen S. Rich, Bruce M. Psaty, Jerome I. Rotter, Christopher J. O'Donnell, Kenneth Rice, Eric Boerwinkle, Sekar Kathiresan, L. Adrienne Cupples

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263 Scopus citations

Abstract

Low-frequency coding DNA sequence variants in the proprotein convertase subtilisin/kexin type 9 gene (PCSK9) lower plasma low-density lipoprotein cholesterol (LDL-C), protect against risk of coronary heart disease (CHD), and have prompted the development of a new class of therapeutics. It is uncertain whether the PCSK9 example represents a paradigm or an isolated exception. We used the "Exome Array" to genotype >200,000 low-frequency and rare coding sequence variants across the genome in 56,538 individuals (42,208 European ancestry [EA] and 14,330 African ancestry [AA]) and tested these variants for association with LDL-C, high-density lipoprotein cholesterol (HDL-C), and triglycerides. Although we did not identify new genes associated with LDL-C, we did identify four low-frequency (frequencies between 0.1% and 2%) variants (ANGPTL8 rs145464906 [c.361C>T; p.Gln121^-], PAFAH1B2 rs186808413 [c.482C>T; p.Ser161Leu], COL18A1 rs114139997 [c.331G>A; p.Gly111Arg], and PCSK7 rs142953140 [c.1511G>A; p.Arg504His]) with large effects on HDL-C and/or triglycerides. None of these four variants was associated with risk for CHD, suggesting that examples of low-frequency coding variants with robust effects on both lipids and CHD will be limited.

Original language	English (US)
Pages (from-to)	223-232
Number of pages	10
Journal	American Journal of Human Genetics
Volume	94
Issue number	2
DOIs	https://doi.org/10.1016/j.ajhg.2014.01.009
State	Published - Feb 6 2014

Bibliographical note

Funding Information:
The authors wish to acknowledge the support of the National Heart, Lung, and Blood Institute (NHLBI) and the contributions of the research institutions, study investigators, field staff, and study participants in creating this resource for biomedical research. Funding for GO ESP was provided by NHLBI grants RC2 HL-103010 (HeartGO), RC2 HL-102923 (LungGO), and RC2 HL-102924 (WHISP). The exome sequencing was performed through NHLBI grants RC2 HL-102925 (BroadGO) and RC2 HL-102926 (SeattleGO). Infrastructure for the CHARGE Consortium is supported, in part, by the National Heart, Lung, and Blood Institute (grant HL105756). G.M.P. is supported by award number T32HL007208 from the NHLBI. S.K. is supported by a Research Scholar award from the Massachusetts General Hospital (MGH), the Howard Goodman Fellowship from MGH, the Donovan Family Foundation, R01HL107816, and a grant from Fondation Leducq. Exome Array genotyping in case-control studies of coronary heart disease was supported by NIH RC2 HL-102925 and an investigator-initiated research grant from Merck to S.K. N.O.S. is supported, in part, by a career development award from the NIH/NHLBI K08-HL114642. A.D. is supported by NWO grant (veni, 916.12.154) and the EUR Fellowship. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NHLBI or NIH. A full listing of acknowledgements is provided in Supplemental Data .

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10.1016/j.ajhg.2014.01.009

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Peloso, G. M., Auer, P. L., Bis, J. C., Voorman, A., Morrison, A. C., Stitziel, N. O., Brody, J. A., Khetarpal, S. A., Crosby, J. R., Fornage, M., Isaacs, A., Jakobsdottir, J., Feitosa, M. F., Davies, G., Huffman, J. E., Manichaikul, A., Davis, B., Lohman, K., Joon, A. Y., ... Cupples, L. A. (2014). Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks. American Journal of Human Genetics, 94(2), 223-232. https://doi.org/10.1016/j.ajhg.2014.01.009

Peloso, GM, Auer, PL, Bis, JC, Voorman, A, Morrison, AC, Stitziel, NO, Brody, JA, Khetarpal, SA, Crosby, JR, Fornage, M, Isaacs, A, Jakobsdottir, J, Feitosa, MF, Davies, G, Huffman, JE, Manichaikul, A, Davis, B, Lohman, K, Joon, AY, Smith, AV, Grove, ML, Zanoni, P, Redon, V, Demissie, S, Lawson, K, Peters, U, Carlson, C, Jackson, RD, Ryckman, KK, MacKey, RH, Robinson, JG, Siscovick, DS, Schreiner, PJ, Mychaleckyj, JC, Pankow, JS, Hofman, A, Uitterlinden, AG, Harris, TB, Taylor, KD, Stafford, JM, Reynolds, LM, Marioni, RE, Dehghan, A, Franco, OH, Patel, AP, Lu, Y, Hindy, G, Gottesman, O, Bottinger, EP, Melander, O, Orho-Melander, M, Loos, RJF, Duga, S, Merlini, PA, Farrall, M, Goel, A, Asselta, R, Girelli, D, Martinelli, N, Shah, SH, Kraus, WE, Li, M, Rader, DJ, Reilly, MP, McPherson, R, Watkins, H, Ardissino, D, Zhang, Q, Wang, J, Tsai, MY, Taylor, HA, Correa, A, Griswold, ME, Lange, LA, Starr, JM, Rudan, I, Eiriksdottir, G, Launer, LJ, Ordovas, JM, Levy, D, Chen, YDI, Reiner, AP, Hayward, C, Polasek, O, Deary, IJ, Borecki, IB, Liu, Y, Gudnason, V, Wilson, JG, Van Duijn, CM, Kooperberg, C, Rich, SS, Psaty, BM, Rotter, JI, O'Donnell, CJ, Rice, K, Boerwinkle, E, Kathiresan, S & Cupples, LA 2014, 'Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks', American Journal of Human Genetics, vol. 94, no. 2, pp. 223-232. https://doi.org/10.1016/j.ajhg.2014.01.009

@article{04e58cbffff24bf69e71dfb19920b53f,

title = "Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks",

abstract = "Low-frequency coding DNA sequence variants in the proprotein convertase subtilisin/kexin type 9 gene (PCSK9) lower plasma low-density lipoprotein cholesterol (LDL-C), protect against risk of coronary heart disease (CHD), and have prompted the development of a new class of therapeutics. It is uncertain whether the PCSK9 example represents a paradigm or an isolated exception. We used the {"}Exome Array{"} to genotype >200,000 low-frequency and rare coding sequence variants across the genome in 56,538 individuals (42,208 European ancestry [EA] and 14,330 African ancestry [AA]) and tested these variants for association with LDL-C, high-density lipoprotein cholesterol (HDL-C), and triglycerides. Although we did not identify new genes associated with LDL-C, we did identify four low-frequency (frequencies between 0.1% and 2%) variants (ANGPTL8 rs145464906 [c.361C>T; p.Gln121-], PAFAH1B2 rs186808413 [c.482C>T; p.Ser161Leu], COL18A1 rs114139997 [c.331G>A; p.Gly111Arg], and PCSK7 rs142953140 [c.1511G>A; p.Arg504His]) with large effects on HDL-C and/or triglycerides. None of these four variants was associated with risk for CHD, suggesting that examples of low-frequency coding variants with robust effects on both lipids and CHD will be limited.",

author = "Peloso, {Gina M.} and Auer, {Paul L.} and Bis, {Joshua C.} and Arend Voorman and Morrison, {Alanna C.} and Stitziel, {Nathan O.} and Brody, {Jennifer A.} and Khetarpal, {Sumeet A.} and Crosby, {Jacy R.} and Myriam Fornage and Aaron Isaacs and Johanna Jakobsdottir and Feitosa, {Mary F.} and Gail Davies and Huffman, {Jennifer E.} and Ani Manichaikul and Brian Davis and Kurt Lohman and Joon, {Aron Y.} and Smith, {Albert V.} and Grove, {Megan L.} and Paolo Zanoni and Valeska Redon and Serkalem Demissie and Kim Lawson and Ulrike Peters and Christopher Carlson and Jackson, {Rebecca D.} and Ryckman, {Kelli K.} and MacKey, {Rachel H.} and Robinson, {Jennifer G.} and Siscovick, {David S.} and Schreiner, {Pamela J.} and Mychaleckyj, {Josyf C.} and Pankow, {James S.} and Albert Hofman and Uitterlinden, {Andre G.} and Harris, {Tamara B.} and Taylor, {Kent D.} and Stafford, {Jeanette M.} and Reynolds, {Lindsay M.} and Marioni, {Riccardo E.} and Abbas Dehghan and Franco, {Oscar H.} and Patel, {Aniruddh P.} and Yingchang Lu and George Hindy and Omri Gottesman and Bottinger, {Erwin P.} and Olle Melander and Marju Orho-Melander and Loos, {Ruth J F} and Stefano Duga and Merlini, {Piera Angelica} and Martin Farrall and Anuj Goel and Rosanna Asselta and Domenico Girelli and Nicola Martinelli and Shah, {Svati H.} and Kraus, {William E.} and Mingyao Li and Rader, {Daniel J.} and Reilly, {Muredach P.} and Ruth McPherson and Hugh Watkins and Diego Ardissino and Qunyuan Zhang and Judy Wang and Tsai, {Michael Y.} and Taylor, {Herman A.} and Adolfo Correa and Griswold, {Michael E.} and Lange, {Leslie A.} and Starr, {John M.} and Igor Rudan and Gudny Eiriksdottir and Launer, {Lenore J.} and Ordovas, {Jose M.} and Daniel Levy and Chen, {Y. D Ida} and Reiner, {Alexander P.} and Caroline Hayward and Ozren Polasek and Deary, {Ian J.} and Borecki, {Ingrid B.} and Yongmei Liu and Vilmundur Gudnason and Wilson, {James G.} and {Van Duijn}, {Cornelia M.} and Charles Kooperberg and Rich, {Stephen S.} and Psaty, {Bruce M.} and Rotter, {Jerome I.} and O'Donnell, {Christopher J.} and Kenneth Rice and Eric Boerwinkle and Sekar Kathiresan and Cupples, {L. Adrienne}",

note = "Funding Information: The authors wish to acknowledge the support of the National Heart, Lung, and Blood Institute (NHLBI) and the contributions of the research institutions, study investigators, field staff, and study participants in creating this resource for biomedical research. Funding for GO ESP was provided by NHLBI grants RC2 HL-103010 (HeartGO), RC2 HL-102923 (LungGO), and RC2 HL-102924 (WHISP). The exome sequencing was performed through NHLBI grants RC2 HL-102925 (BroadGO) and RC2 HL-102926 (SeattleGO). Infrastructure for the CHARGE Consortium is supported, in part, by the National Heart, Lung, and Blood Institute (grant HL105756). G.M.P. is supported by award number T32HL007208 from the NHLBI. S.K. is supported by a Research Scholar award from the Massachusetts General Hospital (MGH), the Howard Goodman Fellowship from MGH, the Donovan Family Foundation, R01HL107816, and a grant from Fondation Leducq. Exome Array genotyping in case-control studies of coronary heart disease was supported by NIH RC2 HL-102925 and an investigator-initiated research grant from Merck to S.K. N.O.S. is supported, in part, by a career development award from the NIH/NHLBI K08-HL114642. A.D. is supported by NWO grant (veni, 916.12.154) and the EUR Fellowship. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NHLBI or NIH. A full listing of acknowledgements is provided in Supplemental Data . ",

year = "2014",

month = feb,

day = "6",

doi = "10.1016/j.ajhg.2014.01.009",

language = "English (US)",

volume = "94",

pages = "223--232",

journal = "American Journal of Human Genetics",

issn = "0002-9297",

publisher = "Cell Press",

number = "2",

}

TY - JOUR

T1 - Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks

AU - Peloso, Gina M.

AU - Auer, Paul L.

AU - Bis, Joshua C.

AU - Voorman, Arend

AU - Morrison, Alanna C.

AU - Stitziel, Nathan O.

AU - Brody, Jennifer A.

AU - Khetarpal, Sumeet A.

AU - Crosby, Jacy R.

AU - Fornage, Myriam

AU - Isaacs, Aaron

AU - Jakobsdottir, Johanna

AU - Feitosa, Mary F.

AU - Davies, Gail

AU - Huffman, Jennifer E.

AU - Manichaikul, Ani

AU - Davis, Brian

AU - Lohman, Kurt

AU - Joon, Aron Y.

AU - Smith, Albert V.

AU - Grove, Megan L.

AU - Zanoni, Paolo

AU - Redon, Valeska

AU - Demissie, Serkalem

AU - Lawson, Kim

AU - Peters, Ulrike

AU - Carlson, Christopher

AU - Jackson, Rebecca D.

AU - Ryckman, Kelli K.

AU - MacKey, Rachel H.

AU - Robinson, Jennifer G.

AU - Siscovick, David S.

AU - Schreiner, Pamela J.

AU - Mychaleckyj, Josyf C.

AU - Pankow, James S.

AU - Hofman, Albert

AU - Uitterlinden, Andre G.

AU - Harris, Tamara B.

AU - Taylor, Kent D.

AU - Stafford, Jeanette M.

AU - Reynolds, Lindsay M.

AU - Marioni, Riccardo E.

AU - Dehghan, Abbas

AU - Franco, Oscar H.

AU - Patel, Aniruddh P.

AU - Lu, Yingchang

AU - Hindy, George

AU - Gottesman, Omri

AU - Bottinger, Erwin P.

AU - Melander, Olle

AU - Orho-Melander, Marju

AU - Loos, Ruth J F

AU - Duga, Stefano

AU - Merlini, Piera Angelica

AU - Farrall, Martin

AU - Goel, Anuj

AU - Asselta, Rosanna

AU - Girelli, Domenico

AU - Martinelli, Nicola

AU - Shah, Svati H.

AU - Kraus, William E.

AU - Li, Mingyao

AU - Rader, Daniel J.

AU - Reilly, Muredach P.

AU - McPherson, Ruth

AU - Watkins, Hugh

AU - Ardissino, Diego

AU - Zhang, Qunyuan

AU - Wang, Judy

AU - Tsai, Michael Y.

AU - Taylor, Herman A.

AU - Correa, Adolfo

AU - Griswold, Michael E.

AU - Lange, Leslie A.

AU - Starr, John M.

AU - Rudan, Igor

AU - Eiriksdottir, Gudny

AU - Launer, Lenore J.

AU - Ordovas, Jose M.

AU - Levy, Daniel

AU - Chen, Y. D Ida

AU - Reiner, Alexander P.

AU - Hayward, Caroline

AU - Polasek, Ozren

AU - Deary, Ian J.

AU - Borecki, Ingrid B.

AU - Liu, Yongmei

AU - Gudnason, Vilmundur

AU - Wilson, James G.

AU - Van Duijn, Cornelia M.

AU - Kooperberg, Charles

AU - Rich, Stephen S.

AU - Psaty, Bruce M.

AU - Rotter, Jerome I.

AU - O'Donnell, Christopher J.

AU - Rice, Kenneth

AU - Boerwinkle, Eric

AU - Kathiresan, Sekar

AU - Cupples, L. Adrienne

N1 - Funding Information: The authors wish to acknowledge the support of the National Heart, Lung, and Blood Institute (NHLBI) and the contributions of the research institutions, study investigators, field staff, and study participants in creating this resource for biomedical research. Funding for GO ESP was provided by NHLBI grants RC2 HL-103010 (HeartGO), RC2 HL-102923 (LungGO), and RC2 HL-102924 (WHISP). The exome sequencing was performed through NHLBI grants RC2 HL-102925 (BroadGO) and RC2 HL-102926 (SeattleGO). Infrastructure for the CHARGE Consortium is supported, in part, by the National Heart, Lung, and Blood Institute (grant HL105756). G.M.P. is supported by award number T32HL007208 from the NHLBI. S.K. is supported by a Research Scholar award from the Massachusetts General Hospital (MGH), the Howard Goodman Fellowship from MGH, the Donovan Family Foundation, R01HL107816, and a grant from Fondation Leducq. Exome Array genotyping in case-control studies of coronary heart disease was supported by NIH RC2 HL-102925 and an investigator-initiated research grant from Merck to S.K. N.O.S. is supported, in part, by a career development award from the NIH/NHLBI K08-HL114642. A.D. is supported by NWO grant (veni, 916.12.154) and the EUR Fellowship. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NHLBI or NIH. A full listing of acknowledgements is provided in Supplemental Data .

PY - 2014/2/6

Y1 - 2014/2/6

N2 - Low-frequency coding DNA sequence variants in the proprotein convertase subtilisin/kexin type 9 gene (PCSK9) lower plasma low-density lipoprotein cholesterol (LDL-C), protect against risk of coronary heart disease (CHD), and have prompted the development of a new class of therapeutics. It is uncertain whether the PCSK9 example represents a paradigm or an isolated exception. We used the "Exome Array" to genotype >200,000 low-frequency and rare coding sequence variants across the genome in 56,538 individuals (42,208 European ancestry [EA] and 14,330 African ancestry [AA]) and tested these variants for association with LDL-C, high-density lipoprotein cholesterol (HDL-C), and triglycerides. Although we did not identify new genes associated with LDL-C, we did identify four low-frequency (frequencies between 0.1% and 2%) variants (ANGPTL8 rs145464906 [c.361C>T; p.Gln121-], PAFAH1B2 rs186808413 [c.482C>T; p.Ser161Leu], COL18A1 rs114139997 [c.331G>A; p.Gly111Arg], and PCSK7 rs142953140 [c.1511G>A; p.Arg504His]) with large effects on HDL-C and/or triglycerides. None of these four variants was associated with risk for CHD, suggesting that examples of low-frequency coding variants with robust effects on both lipids and CHD will be limited.

AB - Low-frequency coding DNA sequence variants in the proprotein convertase subtilisin/kexin type 9 gene (PCSK9) lower plasma low-density lipoprotein cholesterol (LDL-C), protect against risk of coronary heart disease (CHD), and have prompted the development of a new class of therapeutics. It is uncertain whether the PCSK9 example represents a paradigm or an isolated exception. We used the "Exome Array" to genotype >200,000 low-frequency and rare coding sequence variants across the genome in 56,538 individuals (42,208 European ancestry [EA] and 14,330 African ancestry [AA]) and tested these variants for association with LDL-C, high-density lipoprotein cholesterol (HDL-C), and triglycerides. Although we did not identify new genes associated with LDL-C, we did identify four low-frequency (frequencies between 0.1% and 2%) variants (ANGPTL8 rs145464906 [c.361C>T; p.Gln121-], PAFAH1B2 rs186808413 [c.482C>T; p.Ser161Leu], COL18A1 rs114139997 [c.331G>A; p.Gly111Arg], and PCSK7 rs142953140 [c.1511G>A; p.Arg504His]) with large effects on HDL-C and/or triglycerides. None of these four variants was associated with risk for CHD, suggesting that examples of low-frequency coding variants with robust effects on both lipids and CHD will be limited.

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DO - 10.1016/j.ajhg.2014.01.009

M3 - Article

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AN - SCOPUS:84893756641

SN - 0002-9297

VL - 94

SP - 223

EP - 232

JO - American Journal of Human Genetics

JF - American Journal of Human Genetics

IS - 2

ER -

Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks

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