Denisovan, modern human and mouse TNFAIP3 alleles tune A20 phosphorylation and immunity
Open accessAbstract
Resisting and tolerating microbes are alternative strategies to survive infection, but little is known about the evolutionary mechanisms controlling this balance. Here genomic analyses of anatomically modern humans, extinct Denisovan hominins and mice revealed a TNFAIP3 allelic series with alterations in the encoded immune response inhibitor A20. Each TNFAIP3 allele encoded substitutions at non-catalytic residues of the ubiquitin protease OTU domain that diminished IκB kinase-dependent phosphorylation and activation of A20. Two TNFAIP3 alleles encoding A20 proteins with partial phosphorylation deficits seemed to be beneficial by increasing immunity without causing spontaneous inflammatory disease: A20 T108A;I207L, originating in Denisovans and introgressed in modern humans throughout Oceania, and A20 I325N, from an N-ethyl-N-nitrosourea (ENU)-mutagenized mouse strain. By contrast, a rare human TNFAIP3 allele encoding an A20 protein with 95% loss of phosphorylation, C243Y, caused spontaneous inflammatory disease in humans and mice. Analysis of the partial-phosphorylation A20 I325N allele in mice revealed diminished tolerance of bacterial lipopolysaccharide and poxvirus inoculation as tradeoffs for enhanced immunity.
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TNFAIP3, OAS2 and OAS3 have been repeatedly identified as harbouring archaic hominin contribution that impact immune responses to pathogens.
“all of which have been repeatedly identified as harbouring archaic hominin contribution that impact immune responses to pathogens [51, 52, 56].”
From Denisovan introgression has shaped the immune system of present-day Papuans (2022) · cites this paper as [51]
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“Interestingly, among the set of putative genes regulated by Denisovan TFBS-disrupting aSNPs, we noted the presence of TNFAIP3, OAS1, OAS2 and OAS3, all of which have been repeatedly identified as harbouring archaic hominin contribution that impact immune responses to pathogens [38–40].”
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- Authors
- Zammit, N. W., Siggs, O. M., Gray, P. E., Horikawa, K., Langley, D. B., Walters, S. N., Daley, S. R., Loetsch, C., Warren, J., Yap, J. Y., Cultrone, D., Russell, A., Malle, E. K., Villanueva, J. E., Cowley, M. J., Gayevskiy, V., Dinger, M. E., Brink, R., Zahra, D., Chaudhri, G., Karupiah, G., Whittle, B., Roots, C., Bertram, E., Yamada, M., Jeelall, Y., Enders, A., Clifton, B. E., Mabbitt, P. D., Jackson, C. J., Watson, S. R., Jenne, C. N., Lanier, L. L., Wiltshire, T., Spitzer, M. H., Nolan, G. P., Schmitz, F., Aderem, A., Porebski, B. T., Buckle, A. M., Abbott, D. W., Ziegler, J. B., Craig, M. E., Benitez-Aguirre, P., Teo, J., Tangye, S. G., King, C., Wong, M., Cox, M. P., Phung, W., Tang, J., Sandoval, W., Wertz, I. E., Christ, D., Goodnow, C. C., & Grey, S. T.
- Affiliations
- Garvan Institute of Medical Research (AU)
- UNSW Sydney (AU)
- Australian National University (AU)
- University of California, San Francisco (US)
- University of Calgary (CA)
- University of North Carolina at Chapel Hill (US)
- Stanford University (US)
- Center for Infectious Disease Research (US)
- Monash University (AU)
- Case Western Reserve University (US)
- Children's Hospital at Westmead (AU)
- Massey University (NZ)
- Genentech (US)
- Corresponding author
- Goodnow, Christopher C.
- Grey, Shane T.
- ORCID
- Zammit, Nathan W.
- Siggs, Owen M.
- Gray, Paul E.
- Horikawa, Keisuke
- Langley, David B.
- Walters, Stacey N.
- Daley, Stephen R.
- Warren, Joanna
- Yap, Jin Yan
- Russell, Amanda
- Villanueva, Jeanette E.
- Cowley, Mark J.
- Gayevskiy, Velimir
- Dinger, Marcel E.
- Brink, Robert
- Zahra, David
- Chaudhri, Geeta
- Karupiah, Gunasegaran
- Bertram, Edward
- Yamada, Michiko
- Jeelall, Yogesh
- Enders, Anselm
- Mabbitt, Peter D.
- Jackson, Colin J.
- Jenne, Craig N.
- Lanier, Lewis L.
- Wiltshire, Tim
- Spitzer, Matthew H.
- Nolan, Garry P.
- Schmitz, Frank
- Aderem, Alan
- Porebski, Benjamin T.
- Buckle, Ashley M.
- Abbott, Derek W.
- Ziegler, John B.
- Craig, Maria E.
- Teo, Juliana
- Tangye, Stuart G.
- Wong, Melanie
- Cox, Murray P.
- Phung, Wilson
- Tang, Jia
- Sandoval, Wendy
- Wertz, Ingrid E.
- Christ, Daniel
- Goodnow, Christopher C.
- Grey, Shane T.
- Venue
- Nature Immunology
- Published
- 2019-09-18
- Volume
- 20
- Issue
- 10
- Pages
- 1299-1310
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- OpenAlex
- W2974704311
- Cited by
- 80
- References
- 75
- Citations by year
- 2026: 12 · 2025: 6 · 2024: 8 · 2023: 9 · 2022: 17 · 2021: 10 · 2020: 14 · 2019: 4
- FWCI
- 3.55
- Type
- journal article
- Language
- en
- Open access
- green
- figshare.com
- Licence
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion)
- UTAS Research Repository (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- QUT ePrints (Queensland University of Technology) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Department of Health | National Health and Medical Research Council (1130222, 1140691, 585490)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- A20, Denisovans, human, OTU domain, NF-κB signaling, autoinflammatory disease, immune tolerance, bacterial lipopolysaccharide, poxvirus, Denisovan introgression, Oceania, Wallace's Line, N-ethyl-N-nitrosourea mutagenesis, allelic variation
- MeSH terms
- Protein Domains, Tumor Necrosis Factor alpha-Induced Protein 3, Alleles, Animals, Humans, Immunity, Inflammation, Mice, Inbred C57BL, Mice, Transgenic, Phosphorylation, Poxviridae, Poxviridae Infections, Mutation, Missense, Mice, Extinction, Biological
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