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Whole Genome Sequence Analysis of the Plasma Proteome in Black Adults Provides Novel Insights Into Cardiovascular Disease

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Katz, Daniel H., Tahir, Usman A., Bick, Alexander G., Pampana, Akhil, Ngo, Debby, Benson, Mark D., Yu, Zhi, Robbins, Jeremy M. +436 more·2022·Circulation
DOI 10.1161/circulationaha.121.055117PMC PMC9158509
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Abstract

Background: Plasma proteins are critical mediators of cardiovascular processes and are the targets of many drugs. Previous efforts to characterize the genetic architecture of the plasma proteome have been limited by a focus on individuals of European descent and leveraged genotyping arrays and imputation. Here we describe whole genome sequence analysis of the plasma proteome in individuals with greater African ancestry, increasing our power to identify novel genetic determinants. Methods: Proteomic profiling of 1301 proteins was performed in 1852 Black adults from the Jackson Heart Study using aptamer-based proteomics (SomaScan). Whole genome sequencing association analysis was ascertained for all variants with minor allele count ≥5. Results were validated using an alternative, antibody-based, proteomic platform (Olink) as well as replicated in the Multi-Ethnic Study of Atherosclerosis and the HERITAGE Family Study (Health, Risk Factors, Exercise Training and Genetics). Results: We identify 569 genetic associations between 479 proteins and 438 unique genetic regions at a Bonferroni-adjusted significance level of 3.8×10 -11 . These associations include 114 novel locus-protein relationships and an additional 217 novel sentinel variant-protein relationships. Novel cardiovascular findings include new protein associations at the APOE gene locus including ZAP70 (sentinel single nucleotide polymorphism [SNP] rs7412-T, β=0.61±0.05, P =3.27×10 -30 ) and MMP-3 (β=-0.60±0.05, P =1.67×10 -32 ), as well as a completely novel pleiotropic locus at the HPX gene, associated with 9 proteins. Further, the associations suggest new mechanisms of genetically mediated cardiovascular disease linked to African ancestry; we identify a novel association between variants linked to APOL1-associated chronic kidney and heart disease and the protein CKAP2 (rs73885319-G, β=0.34±0.04, P =1.34×10 -17 ) as well as an association between ATTR amyloidosis and RBP4 levels in community-dwelling individuals without heart failure. Conclusions: Taken together, these results provide evidence for the functional importance of variants in non-European populations, and suggest new biological mechanisms for ancestry-specific determinants of lipids, coagulation, and myocardial function.

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  • The influence of rare variants on the plasma proteome is largely unknown because previous rare variant proteogenomic studies have been limited in scale.

    “However, their influence on the plasma proteome is largely unknown because previous rare variant proteogenomic studies have been limited in scale9,10.”

    From Rare variant associations with plasma protein levels in the UK Biobank (2023) · cites this paper as [10]

    The Introduction (page unavailable) says earlier proteogenomic findings came nearly entirely from European populations using genotyping arrays, and the Discussion (page unavailable) describes this study as the largest of its kind in a Black population. This supports a gap in knowledge about genetic determinants of the plasma proteome, but the paper does not say that previous rare-variant proteogenomic studies were limited in scale or identify that as the reason rare variants’ influence was largely unknown. (LLM, conf=0.77)

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Katz, D. H., Tahir, U. A., Bick, A. G., Pampana, A., Ngo, D., Benson, M. D., Yu, Z., Robbins, J. M., Chen, Z.-Z., Cruz, D. E., Deng, S., Farrell, L., Sinha, S., Schmaier, A. A., Shen, D., Gao, Y., Hall, M. E., Correa, A., Tracy, R. P., Durda, P., Taylor, K. D., Liu, Y., Johnson, W. C., Guo, X., Yao, J., Ida Chen, Y.-D., Manichaikul, A. W., Jain, D., Bouchard, C., Sarzynski, M. A., Rich, S. S., Rotter, J. I., Wang, T. J., Wilson, J. G., Natarajan, P., Gerszten, R. E., Abe, N., Abecasis, G., Aguet, F., Albert, C., Almasy, L., Alonso, A., Ament, S., Anderson, P., Anugu, P., Applebaum-Bowden, D., Ardlie, K., Arking, D., Arnett, D. K., Ashley-Koch, A., Aslibekyan, S., Assimes, T., Auer, P., Avramopoulos, D., Ayas, N., Balasubramanian, A., Barnard, J., Barnes, K., Barr, R. G., Barron-Casella, E., Barwick, L., Beaty, T., Beck, G., Becker, D., Becker, L., Beer, R., Beitelshees, A., Benjamin, E., Benos, T., Bezerra, M., Bielak, L., Bis, J., Blackwell, T., Blangero, J., Boerwinkle, E., Bowden, D. W., Bowler, R., Brody, J., Broeckel, U., Broome, J., Brown, D., Bunting, K., Burchard, E., Bustamante, C., Buth, E., Cade, B., Cardwell, J., Carey, V., Carrier, J., Carson, A., Carty, C., Casaburi, R., Casas Romero, J. P., Casella, J., Castaldi, P., Chaffin, M., Chang, C., Chang, Y.-C., Chasman, D., Chavan, S., Chen, B.-J., Chen, W.-M., Chen, Y.-D. I., Cho, M., Choi, S. H., Chuang, L.-M., Chung, M., Chung, R.-H., Clish, C., Comhair, S., Conomos, M., Cornell, E., Correa, A., Crandall, C., Crapo, J., Cupples, L. 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Affiliations
  • Beth Israel Deaconess Medical Center (US)
  • Broad Institute (US)
  • University of Mississippi Medical Center (US)
  • Department of Pathology Laboratory Medicine, Larner College of Medicine, University of Vermont, Burlington (R.P.T., P.D.).
  • University of Vermont (US)
  • University of Washington (US)
  • University of California, Los Angeles (US)
  • Institute for Translational Genomics and Population Sciences, Department of Pediatrics, Lundquist Institute for Biomedical Innovation at Harbor-University of California, Los Angeles, Medical Center, Torrance (K.D.T., X.G., J.Y., Y.-D.I.C., J.I.R.).
  • University of Virginia (US)
  • Pennington Biomedical Research Center (US)
  • University of South Carolina (US)
  • Center for Public Health Genomics (A.W.M., S.S.R.), University of Virginia, Charlottesville.
  • The University of Texas Southwestern Medical Center (US)
  • Division of Cardiovascular Medicine, Beth Israel Deaconess Medical Center, Boston, MA (D.H.K., U.A.T., D.N., M.D.B., J.M.R., Z.-Z.C., D.E.C., S.D., L.F., S.S., A.A.S., D.S., J.G.W., R.E.G.).
ORCID
Venue
Circulation
Publisher
Ovid Technologies (Wolters Kluwer Health)
Published
2022-02
Volume
145
Issue
5
Pages
357-370
ISSN
  • 0009-7322 (ISSN-L)
  • 1524-4539
DOI
10.1161/circulationaha.121.055117
PMC
PMC9158509
OpenAlex
W3216928657
Cited by
92
References
4
Citations by year
2026: 24 · 2025: 20 · 2024: 15 · 2023: 18 · 2022: 15
FWCI
6.78
Type
journal article
Language
en
Open access
Locations
  • Circulation (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • ScholarWorks @ UTRGV (The University of Texas Rio Grande Valley) (submittedVersion)
Funders
  • U.S. Department of Veterans Affairs (I01-CX001737, I01 BX005831)
  • Jackson State University (HHSN268201800015I/HHSN26800001, HHSN268201800013 I, HHSN268201800014 I)
  • Harvard Catalyst (TR002542)
  • Broad Institute (3U54HG003067‐13S1)
  • Mississippi State Department of Health (HHSN26800001, HHSN268201800015 I, HHSN268201800015I/HHSN26800001)
  • National Institutes of Health (n01hc95164-17-0-1, HHSN268201800010I, HHSN268201800011I, UL1TR001420, KL2TR002542, 1r01hl120393-01a1, HHSN268201800012I, n01hc95165-34-0-1, n01hc95161-24-0-1, n01hc095169-003, HHSN268201800014I, HHSN268201800001I, N01-HC- 95166, DP5OD029586, n01hc95166-21-0-1, N01-HC9-5168, n01hc95162-31-0-1, 5t32hl007374-41, n01hc95168-27-0-1, n01hc95160-18-0-1, HHSN268201800002I, n01hc095167-000, N01-HC- 95159, HHSN268201800013I, UL1TR001079, n01hc95163-22-0-1, HHSN268201500003I, n01hc95159-40-0-1, HHSN268201800015I, HHSN268201100037C, UL1TR000040, N01‐HC‐95161, N01- HC-95163, N01- HC-95165, N01‐HC‐95160, N01 HC95164, N01-HC-95167, N01-HC95162, N01‐HC‐95169, DK-063491, UL1TR001881)
  • National Institute on Aging (U01AG052409, K01AG059898, RF1AG063507, P30AG066546)
  • National Heart, Lung, and Blood Institute (DK-063491, 117626, R01HL047327, HHSN268201100037C, N01 HC-95159, N01-HC-95160, HHSN268201800013I, N01-HC095169, 75N92020D00001, N01 HC-95168, N01-HC-095165, HHSN26800001, 75N92020D00006, HHSN268201800002I, N01 HC95167, (N01-HC-95163, N01 HC095163, HHSN268201800012C, 3R01 HL-120393-02S1, R01-HL120393, HHSN268201800010 I, T32‐HL007374, 75N92020D00007, HHSN268201800014 I, N01 HC-95161, N01 HC95165, N01HC95164, HHSN268201800001C, HHSN268201800012 I, R01HL047317, 75N92020D00002, UL1-TR-, R01HL132320, N01-HC-095159, N01-HC, N01 HC095168, N01-HC-095162, U01HL120393, HL132320, HC-95168, N01-HC-095161, 75N92020D00005, HHSN268201800014C, 3R01HL-120393, K08HL145095, HHSN268201500003C, HHSN26820150 0003I, 75N92020D00003, N01 HC095167, HHSN268201800015I, T32HL007374-40, N01-HC-095160, R01 HL, N01 HC095166, N01 HC095164, HHSN268201800001I, N01‐HC‐95166, HHSN268201800011C, HHSN268201800011I, R01HL047323, R01HL146462, N01 HC-95162, HC95159, R01HL117626, K08HL141601, F32HL150992, R01HL045670, 75N92020D00004, R01HL142711, R01HL133870, K08HL161259, N01 HC95169)
  • National Human Genome Research Institute (U54HG003067)
  • National Cancer Institute (T32CA154274)
  • National Institute of Nursing Research (R01NR019628)
  • National Institute of General Medical Sciences (P30GM118430)
  • National Institute of Diabetes and Digestive and Kidney Diseases (K23DK127073, U01DK062413, P30DK063491, R01DK081572)
  • National Center for Advancing Translational Sciences (N01-HC-95161, 75N92020D00006, N01-HC-95168, UL1-TR, N01-HC-95162, 75N92020D00005, N01-HC-95159, DK063491, N01-HC-95160, 75N92020D00002, 75N92020D00001, HHSN268201500003I, N01-HC-95166, N01-HC-95169, N01-HC-95163, 75N92020D00007, 75N92020D00003, N01-HC-95167, N01-HC-95165, N01-HC-95164, 75N92020D00004)
  • National Institute on Minority Health and Health Disparities (HHSN268201800012I, HHSN268201800010I, U01HL-120393, N01-HC-95159, HHSN268201800014I, HHSN268201800015I, HHSN268201100037C, 75N92020D00005, HHSN268201800001I, HHSN268201800011I, HHSN268201800013I)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Physical Performance
Keywords
plasma proteome, cardiovascular disease, Black people, African ancestry, ZAP-70, MMP-3, pleiotropy, APOL1, CKAP2, transthyretin amyloidosis, retinol-binding protein 4, Jackson Heart Study
MeSH terms
Adult, Cardiovascular Diseases, Female, Humans, Male, Proteome, Black People, Genome-Wide Association Study

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