Genome-wide association study identifies human genetic variants associated with fatal outcome from Lassa fever

Dylan Kotliar^#^{1

2

3}, Siddharth Raju^#^{4

5}, Shervin Tabrizi^#^{4

6

7}, Ikponmwosa Odia^#⁸, Augustine Goba⁹, Mambu Momoh^{9

10}, John Demby Sandi⁹, Parvathy Nair¹¹, Eric Phelan¹², Ridhi Tariyal¹³, Philomena E Eromon^{8

14}, Samar Mehta¹⁵, Refugio Robles-Sikisaka¹⁶, Katherine J Siddle⁴, Matt Stremlau¹⁷, Simbirie Jalloh⁹, Stephen K Gire¹³, Sarah Winnicki⁴, Bridget Chak¹⁸, Stephen F Schaffner^{4

19

20}, Matthias Pauthner²¹, Elinor K Karlsson^{4

22

23}, Sarah R Chapin⁴, Sharon G Kennedy^{4

24}, Luis M Branco²⁵, Lansana Kanneh²⁶, Joseph J Vitti⁴, Nisha Broodie²⁷, Adrianne Gladden-Young²⁸, Omowunmi Omoniwa²⁹, Pan-Pan Jiang³⁰, Nathan Yozwiak³¹, Shannon Heuklom³², Lina M Moses³³, George O Akpede^{8

34}, Danny A Asogun³⁵, Kathleen Rubins³⁶, Susan Kales³⁷, Anise N Happi¹⁴, Christopher O Iruolagbe³⁸, Mercy Dic-Ijiewere³⁸, Kelly Iraoyah³⁸, Omoregie O Osazuwa³⁸, Alexander K Okonkwo³⁸, Stefan Kunz³⁹, Joseph B McCormick⁴⁰, S Humarr Khan⁹, Anna N Honko⁴¹, Eric S Lander^{4

5

42}, Michael B A Oldstone¹⁶, Lisa Hensley⁴³, Onikepe A Folarin^{14

44}, Sylvanus A Okogbenin⁸, Stephan Günther⁴⁵, Hanna M Ollila^{4

46

47

48}, Ryan Tewhey³⁷, Peter O Okokhere^{8

34

38}, John S Schieffelin⁴⁹, Kristian G Andersen¹⁶, Steven K Reilly⁵⁰, Donald S Grant^{9

26}, Robert F Garry⁵¹, Kayla G Barnes^{4

20

52

53}, Christian T Happi^{54

55

56}, Pardis C Sabeti^{57

58

59

60

61

62}

Affiliations

¹ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA, USA. dkotliar@mgb.org.
² Department of Systems Biology, Harvard Medical School, Boston, MA, USA. dkotliar@mgb.org.
³ Department of Internal Medicine, Brigham and Women's Hospital, Boston, MA, USA. dkotliar@mgb.org.
⁴ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA, USA.
⁵ Department of Systems Biology, Harvard Medical School, Boston, MA, USA.
⁶ Department of Radiation Oncology, Massachusetts General Hospital, Boston, MA, USA.
⁷ Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁸ Institute of Lassa Fever, Research and Control, Irrua Specialist Teaching Hospital, Irrua, Nigeria.
⁹ College of Medicine and Allied Health Sciences, University of Sierra Leone, Freetown, Sierra Leone.
¹⁰ Eastern Polytechnic College, Kenema, Sierra Leone.
¹¹ Howard Hughes Medical Institute, Chevy Chase, MD, USA.
¹² Prospr at Work Inc., Berlin, Germany.
¹³ NextGen Jane, Inc., Oakland, CA, USA.
¹⁴ African Centre of Excellence for Genomics of Infectious Diseases (ACEGID), Redeemer's University, Ede, Nigeria.
¹⁵ Department of Critical Care Medicine, University of Maryland Medical Center, Baltimore, MA, USA.
¹⁶ Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.
¹⁷ Equator Labs Incorporated, Washington, DC, USA.
¹⁸ Biological Sciences Division, University of Chicago, Chicago, IL, USA.
¹⁹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.
²⁰ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
²¹ Vir Biotechnology, San Francisco, CA, USA.
²² Genomics and Computational Biology, UMass Chan Medical School, Worcester, MA, USA.
²³ Program in Molecular Medicine, UMass Chan Medical School, Worcester, MA, USA.
²⁴ Department of Medicine, Massachusetts General Hospital, Boston, MA, USA.
²⁵ Zalgen Labs, Frederick, MD, USA.
²⁶ Viral Hemorrhagic Fever Program, Kenema Government Hospital, Ministry of Health and Sanitation, Kenema, Sierra Leone.
²⁷ New York-Presbyterian Hospital-Columbia and Cornell, New York, NY, USA.
²⁸ Molecular Microbiology, Graduate School of Biomedical Sciences, Tufts University, Boston, MA, USA.
²⁹ Malaria Consortium, Abuja, Nigeria.
³⁰ Google Medical Brain, Mountain View, CA, USA.
³¹ Gene and Cell Therapy Institute, Mass General Brigham, Cambridge, MA, USA.
³² San Francisco Community Health Center, San Francisco, CA, USA.
³³ Tulane University School of Public Health and Tropical Medicine, New Orleans, LA, USA.
³⁴ Department of Medicine, Ambrose Alli University, Ekpoma, Nigeria.
³⁵ Department of Community Medicine, Ambrose Alli University, Ekpoma, Nigeria.
³⁶ National Aeronautics and Space Administration, Houston, TX, USA.
³⁷ The Jackson Laboratory, Bar Harbor, ME, USA.
³⁸ Department of Medicine, Irrua Specialist Teaching Hospital, Irrua, Nigeria.
³⁹ Institute of Microbiology, University Hospital Center and University of Lausanne, Lausanne, Switzerland.
⁴⁰ UTHealth Houston School of Public Health, Brownsville Campus, Brownsville, TX, USA.
⁴¹ Boston University School of Medicine, Boston, MA, USA.
⁴² Department of Biology, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA.
⁴³ National Institutes of Health Integrated Research Facility, Frederick, MA, USA.
⁴⁴ Department of Biological Sciences, Redeemer's University, Ede, Nigeria.
⁴⁵ Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany.
⁴⁶ Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Helsinki, Finland.
⁴⁷ Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
⁴⁸ Anesthesia, Critical Care, and Pain Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁴⁹ Section of Infectious Disease, Department of Pediatrics, Tulane University School of Medicine, New Orleans, LA, USA.
⁵⁰ Department of Genetics, Yale School of Medicine, New Haven, CT, USA.
⁵¹ Tulane University School of Medicine, New Orleans, LA, USA.
⁵² Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Kamuzu University of Health Sciences, Blantyre, Malawi.
⁵³ Department of Vector Biology and Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, UK.
⁵⁴ African Centre of Excellence for Genomics of Infectious Diseases (ACEGID), Redeemer's University, Ede, Nigeria. happic@run.edu.ng.
⁵⁵ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA. happic@run.edu.ng.
⁵⁶ Department of Biological Sciences, Redeemer's University, Ede, Nigeria. happic@run.edu.ng.
⁵⁷ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA, USA. pardis@broadinstitute.org.
⁵⁸ Howard Hughes Medical Institute, Chevy Chase, MD, USA. pardis@broadinstitute.org.
⁵⁹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA. pardis@broadinstitute.org.
⁶⁰ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA. pardis@broadinstitute.org.
⁶¹ Department of Medicine, Massachusetts General Hospital, Boston, MA, USA. pardis@broadinstitute.org.
⁶² Massachusetts Consortium on Pathogen Readiness, Boston, MA, USA. pardis@broadinstitute.org.

^# Contributed equally.

PMID: 38326571
PMCID: PMC10914620
DOI: 10.1038/s41564-023-01589-3

Genome-wide association study identifies human genetic variants associated with fatal outcome from Lassa fever

Dylan Kotliar et al. Nat Microbiol. 2024 Mar.

. 2024 Mar;9(3):751-762.

doi: 10.1038/s41564-023-01589-3. Epub 2024 Feb 7.

Authors

Affiliations

¹ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA, USA. dkotliar@mgb.org.
² Department of Systems Biology, Harvard Medical School, Boston, MA, USA. dkotliar@mgb.org.
³ Department of Internal Medicine, Brigham and Women's Hospital, Boston, MA, USA. dkotliar@mgb.org.
⁴ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA, USA.
⁵ Department of Systems Biology, Harvard Medical School, Boston, MA, USA.
⁶ Department of Radiation Oncology, Massachusetts General Hospital, Boston, MA, USA.
⁷ Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁸ Institute of Lassa Fever, Research and Control, Irrua Specialist Teaching Hospital, Irrua, Nigeria.
⁹ College of Medicine and Allied Health Sciences, University of Sierra Leone, Freetown, Sierra Leone.
¹⁰ Eastern Polytechnic College, Kenema, Sierra Leone.
¹¹ Howard Hughes Medical Institute, Chevy Chase, MD, USA.
¹² Prospr at Work Inc., Berlin, Germany.
¹³ NextGen Jane, Inc., Oakland, CA, USA.
¹⁴ African Centre of Excellence for Genomics of Infectious Diseases (ACEGID), Redeemer's University, Ede, Nigeria.
¹⁵ Department of Critical Care Medicine, University of Maryland Medical Center, Baltimore, MA, USA.
¹⁶ Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, USA.
¹⁷ Equator Labs Incorporated, Washington, DC, USA.
¹⁸ Biological Sciences Division, University of Chicago, Chicago, IL, USA.
¹⁹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.
²⁰ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
²¹ Vir Biotechnology, San Francisco, CA, USA.
²² Genomics and Computational Biology, UMass Chan Medical School, Worcester, MA, USA.
²³ Program in Molecular Medicine, UMass Chan Medical School, Worcester, MA, USA.
²⁴ Department of Medicine, Massachusetts General Hospital, Boston, MA, USA.
²⁵ Zalgen Labs, Frederick, MD, USA.
²⁶ Viral Hemorrhagic Fever Program, Kenema Government Hospital, Ministry of Health and Sanitation, Kenema, Sierra Leone.
²⁷ New York-Presbyterian Hospital-Columbia and Cornell, New York, NY, USA.
²⁸ Molecular Microbiology, Graduate School of Biomedical Sciences, Tufts University, Boston, MA, USA.
²⁹ Malaria Consortium, Abuja, Nigeria.
³⁰ Google Medical Brain, Mountain View, CA, USA.
³¹ Gene and Cell Therapy Institute, Mass General Brigham, Cambridge, MA, USA.
³² San Francisco Community Health Center, San Francisco, CA, USA.
³³ Tulane University School of Public Health and Tropical Medicine, New Orleans, LA, USA.
³⁴ Department of Medicine, Ambrose Alli University, Ekpoma, Nigeria.
³⁵ Department of Community Medicine, Ambrose Alli University, Ekpoma, Nigeria.
³⁶ National Aeronautics and Space Administration, Houston, TX, USA.
³⁷ The Jackson Laboratory, Bar Harbor, ME, USA.
³⁸ Department of Medicine, Irrua Specialist Teaching Hospital, Irrua, Nigeria.
³⁹ Institute of Microbiology, University Hospital Center and University of Lausanne, Lausanne, Switzerland.
⁴⁰ UTHealth Houston School of Public Health, Brownsville Campus, Brownsville, TX, USA.
⁴¹ Boston University School of Medicine, Boston, MA, USA.
⁴² Department of Biology, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA.
⁴³ National Institutes of Health Integrated Research Facility, Frederick, MA, USA.
⁴⁴ Department of Biological Sciences, Redeemer's University, Ede, Nigeria.
⁴⁵ Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany.
⁴⁶ Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Helsinki, Finland.
⁴⁷ Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
⁴⁸ Anesthesia, Critical Care, and Pain Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁴⁹ Section of Infectious Disease, Department of Pediatrics, Tulane University School of Medicine, New Orleans, LA, USA.
⁵⁰ Department of Genetics, Yale School of Medicine, New Haven, CT, USA.
⁵¹ Tulane University School of Medicine, New Orleans, LA, USA.
⁵² Malawi-Liverpool-Wellcome Trust Clinical Research Programme, Kamuzu University of Health Sciences, Blantyre, Malawi.
⁵³ Department of Vector Biology and Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, UK.
⁵⁴ African Centre of Excellence for Genomics of Infectious Diseases (ACEGID), Redeemer's University, Ede, Nigeria. happic@run.edu.ng.
⁵⁵ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA. happic@run.edu.ng.
⁵⁶ Department of Biological Sciences, Redeemer's University, Ede, Nigeria. happic@run.edu.ng.
⁵⁷ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA, USA. pardis@broadinstitute.org.
⁵⁸ Howard Hughes Medical Institute, Chevy Chase, MD, USA. pardis@broadinstitute.org.
⁵⁹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA. pardis@broadinstitute.org.
⁶⁰ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA. pardis@broadinstitute.org.
⁶¹ Department of Medicine, Massachusetts General Hospital, Boston, MA, USA. pardis@broadinstitute.org.
⁶² Massachusetts Consortium on Pathogen Readiness, Boston, MA, USA. pardis@broadinstitute.org.

^# Contributed equally.

PMID: 38326571
PMCID: PMC10914620
DOI: 10.1038/s41564-023-01589-3

Abstract

Infection with Lassa virus (LASV) can cause Lassa fever, a haemorrhagic illness with an estimated fatality rate of 29.7%, but causes no or mild symptoms in many individuals. Here, to investigate whether human genetic variation underlies the heterogeneity of LASV infection, we carried out genome-wide association studies (GWAS) as well as seroprevalence surveys, human leukocyte antigen typing and high-throughput variant functional characterization assays. We analysed Lassa fever susceptibility and fatal outcomes in 533 cases of Lassa fever and 1,986 population controls recruited over a 7 year period in Nigeria and Sierra Leone. We detected genome-wide significant variant associations with Lassa fever fatal outcomes near GRM7 and LIF in the Nigerian cohort. We also show that a haplotype bearing signatures of positive selection and overlapping LARGE1, a required LASV entry factor, is associated with decreased risk of Lassa fever in the Nigerian cohort but not in the Sierra Leone cohort. Overall, we identified variants and genes that may impact the risk of severe Lassa fever, demonstrating how GWAS can provide insight into viral pathogenesis.

PubMed Disclaimer

Conflict of interest statement

P.C.S., R. Tewhey and S.K.R. are inventors on patents related to massively parallel reporter assays. P.C.S. is a co-founder of, shareholder in and consultant to Sherlock Biosciences, Inc. and Delve Bio, as well as a Board member of and shareholder in Danaher Corporation. The other authors declare no competing interests.

Figures

**Fig. 1. Overview of hypothesized mechanism of positive selection for resistance to Lassa fever mediated by *LARGE1*.**
a, Statistical evidence for positive selection at the *LARGE1* locus, adapted from Andersen et al.. The y axis shows the composite likelihood score which integrates evidence of positive selection based on population differentiation (fixation index), long haplotype (integrated haplotype score, delta integrated haplotype score, cross-population extended haplotype homozygosity) and derived allele frequency. On the figure, p refers to the short arm of the chromosome, while q refers to the long arm. See Andersen et al. for details. b, Hypothesized mechanism by which decreased activity of *LARGE1* increases resistance to LASV infection and Lassa fever.

**Fig. 2. GWAS of Lassa fever clinical outcome.**
a, Immunoglobulin G seropositivity rate in Nigerian (NG) and Sierra Leonean (SL) controls stratified by age. Error bars represent 95% bootstrap confidence intervals. NG: N of 24 in 0–19 years, 424 in 20–39 years, 269 in 40–59 years and 34 in 60+ years. SL: N of 33 in 0–19 years, 282 in 20–39 years, 191 in 40–59 years and 83 in 60+ years. b–d, Manhattan plots showing the −log P value for each genomic variant for the Lassa fever outcome association for Nigeria (b), Sierra Leone (c) and meta-analysis (d). P values for b and c are based on SAIGE, while P values for d are derived from meta-analysis (METAL) of P values shown in b and c.

**Fig. 3. Association of the LARGE-LRH haplotype with susceptibility to Lassa fever.**
a, K-means clustering of haplotypes in the *LARGE1* region. Rows are phased haplotypes; columns are individual variants with reference alleles shown in purple, alternate alleles shown in yellow and K-means clusters separated. b, Scatter plot of q values for allelic skew in the MPRA, coloured by the absolute value of the Pearson correlation with the haplotype. c,d, Scatter plot of GWAS association P values over the *LARGE1* region for Nigeria (c) and Sierra Leone (d) coloured by Pearson correlation of the protective allele in the GWAS with the LARGE-LRH. P values in c and d are based on SAIGE. e, Contingency table of LARGE-LRH genotype counts in cases and controls for Nigeria (NG, top) and Sierra Leone (SL, bottom). f, Ecologically estimated Lassa fever prevalence from Fichet-Calvet et al. with pie charts indicating the frequency of the *LARGE1* haplotype in 1000 Genomes populations (YRI, Yoruba; ESN, Esan; MSL, Mende; LWK, Luhya; GWD, Gambian Mandinka) or our GWAS cohorts (NG, SL). Stars indicate towns, villages or hospitals that encountered outbreaks as detailed in Fichet-Calvet et al..

**Fig. 4. Association of HLA variation with Lassa fever susceptibility.**
a, Imputation accuracy of four-digit HLA calls compared to sequencing-based ground truth sets from our Sierra Leone cohort, as well as Esan and Mende individuals from 1000 Genomes. b, Table of HLA alleles with the strongest association with Lassa fever susceptibility, ordered by meta-analysis of the NG and SL cohorts. P values are based on SAIGE, while meta-analysis P values are derived from meta-analysis (METAL) of P values generated from each cohort. ORs are computed from Firth logistic regression.

**Extended Data Fig. 1. Timeline of cohort recruitment in each country.**
Breakdown of enrolled patients by country, cohort, and disease status.

**Extended Data Fig. 2. Quality control analyses for the susceptibility GWAS.**
(A) Histogram of ages in the Nigeria and Sierra Leone cohorts, separated by case/control status. (B) Histogram of the maximum relatedness coefficient between each individual and all other individuals in the Nigerian (NG) and Sierra Leonean (SL) cohorts. (C) Principal component analysis (PCA) of the NG and SL cohorts, colored by case-control status. PCs were computed on unrelated individuals and then all individuals were projected onto those components (Methods). (D) Quantile-quantile plots of -log10 P-values from the susceptibility GWAS against expected quantiles. (E) Manhattan plots showing the -log10 P-value for each genomic variant for the LF susceptibility associations. P-values in D and E are based on saddlepoint-approximated score tests (SAIGE), while meta-analysis P-values are derived from meta-analysis (METAL) of P-values generated from each cohort.

**Extended Data Fig. 3. Quality control analyses for the GWAS of LF clinical outcome.**
(A) Principal component analysis (PCA) of the NG and SL cohorts, colored by clinical outcome. PCs were computed on unrelated individuals, and then all individuals were projected onto those components. (B) Quantile-quantile plots of -log10 P-values from the outcome GWAS against expected quantiles. (C) Comparison of the outcome GWAS lead variants with and without inclusion of age as a covariate. P-values in B and C are based on saddlepoint-approximated score tests (SAIGE), while meta-analysis P-values are derived from meta-analysis (METAL) of P-values generated from each cohort. Odds ratios are computed from Firth logistic regression.

**Extended Data Fig. 4. MPRA analyses of the susceptibility and outcome GWAS peaks.**
(A) Scatter plot of lead susceptibility GWAS loci described in the main text showing chromosomal position against -log10 association P-value. Variants are colored by the linkage disequilibrium (LD) coefficient of determination R² between each variant and the most significant ‘lead’ variant in the locus. (B) Same as A but for the lead variants in the fatal outcome GWAS. (C–F) Same as A and B but colored by whether the variant showed statistically significant skew (q-value < 0.05) in the massively parallel reporter assay in the K562 cell line (C and E) or HepG2 cell line (D and F). P-values are based on saddlepoint-approximated score tests (SAIGE), while meta-analysis P-values are derived from meta-analysis (METAL) of P-values generated from each cohort.

**Extended Data Fig. 5. LARGE1 haplotype association by recruitment period.**
(A, B) Frequencies of the long-range LARGE1 haplotype by the period of recruitment as well as by case-control status for Nigeria (A) and Sierra Leone (B). P-values are from mixed logistic models association testing within the indicated recruitment period. Error bars represent 95% bootstrap confidence intervals for allele frequency. N for each cohort within each country is defined in Table S2.

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Genome-wide association study identifies human genetic variants associated with fatal outcome from Lassa fever

Affiliations

Genome-wide association study identifies human genetic variants associated with fatal outcome from Lassa fever

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources