The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity

Stephanie S. Pavlovich, Sean P. Lovett, Galina Koroleva, Jonathan C. Guito, Catherine E. Arnold, Elyse R. Nagle, Kirsten Kulcsar, Albert Lee, Françoise Thibaud-Nissen, Adam J. Hume, Elke Mühlberger, Luke S. Uebelhoer, Jonathan S. Towner, Raul Rabadan, Mariano Sanchez-Lockhart, Thomas B. Kepler, Gustavo Palacios

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Bats harbor many viruses asymptomatically, including several notorious for causing extreme virulence in humans. To identify differences between antiviral mechanisms in humans and bats, we sequenced, assembled, and analyzed the genome of Rousettus aegyptiacus, a natural reservoir of Marburg virus and the only known reservoir for any filovirus. We found an expanded and diversified KLRC/KLRD family of natural killer cell receptors, MHC class I genes, and type I interferons, which dramatically differ from their functional counterparts in other mammals. Such concerted evolution of key components of bat immunity is strongly suggestive of novel modes of antiviral defense. An evaluation of the theoretical function of these genes suggests that an inhibitory immune state may exist in bats. Based on our findings, we hypothesize that tolerance of viral infection, rather than enhanced potency of antiviral defenses, may be a key mechanism by which bats asymptomatically host viruses that are pathogenic in humans. The genome of the Egyptian fruit bat reveals how its immune defenses allow tolerance of pathogenic viruses.

Original languageEnglish (US)
Pages (from-to)1098-1110.e18
JournalCell
Volume173
Issue number5
DOIs
StatePublished - May 17 2018

Fingerprint

Viruses
Antiviral Agents
Immunity
Genes
Genome
Natural Killer Cell Receptors
Interferon Type I
Mammals
Ports and harbors
Fruits
Marburgvirus
MHC Class I Genes
Virus Diseases
Virulence
Fruit

Keywords

  • Chiroptera
  • antiviral immunity
  • filovirus
  • genome
  • innate immunity
  • natural killer cell receptors
  • type I interferon

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Pavlovich, S. S., Lovett, S. P., Koroleva, G., Guito, J. C., Arnold, C. E., Nagle, E. R., ... Palacios, G. (2018). The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity. Cell, 173(5), 1098-1110.e18. https://doi.org/10.1016/j.cell.2018.03.070

The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity. / Pavlovich, Stephanie S.; Lovett, Sean P.; Koroleva, Galina; Guito, Jonathan C.; Arnold, Catherine E.; Nagle, Elyse R.; Kulcsar, Kirsten; Lee, Albert; Thibaud-Nissen, Françoise; Hume, Adam J.; Mühlberger, Elke; Uebelhoer, Luke S.; Towner, Jonathan S.; Rabadan, Raul; Sanchez-Lockhart, Mariano; Kepler, Thomas B.; Palacios, Gustavo.

In: Cell, Vol. 173, No. 5, 17.05.2018, p. 1098-1110.e18.

Research output: Contribution to journalArticle

Pavlovich, SS, Lovett, SP, Koroleva, G, Guito, JC, Arnold, CE, Nagle, ER, Kulcsar, K, Lee, A, Thibaud-Nissen, F, Hume, AJ, Mühlberger, E, Uebelhoer, LS, Towner, JS, Rabadan, R, Sanchez-Lockhart, M, Kepler, TB & Palacios, G 2018, 'The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity', Cell, vol. 173, no. 5, pp. 1098-1110.e18. https://doi.org/10.1016/j.cell.2018.03.070
Pavlovich SS, Lovett SP, Koroleva G, Guito JC, Arnold CE, Nagle ER et al. The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity. Cell. 2018 May 17;173(5):1098-1110.e18. https://doi.org/10.1016/j.cell.2018.03.070
Pavlovich, Stephanie S. ; Lovett, Sean P. ; Koroleva, Galina ; Guito, Jonathan C. ; Arnold, Catherine E. ; Nagle, Elyse R. ; Kulcsar, Kirsten ; Lee, Albert ; Thibaud-Nissen, Françoise ; Hume, Adam J. ; Mühlberger, Elke ; Uebelhoer, Luke S. ; Towner, Jonathan S. ; Rabadan, Raul ; Sanchez-Lockhart, Mariano ; Kepler, Thomas B. ; Palacios, Gustavo. / The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity. In: Cell. 2018 ; Vol. 173, No. 5. pp. 1098-1110.e18.
@article{b9a5146514914aaea144a5063babf9d1,
title = "The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity",
abstract = "Bats harbor many viruses asymptomatically, including several notorious for causing extreme virulence in humans. To identify differences between antiviral mechanisms in humans and bats, we sequenced, assembled, and analyzed the genome of Rousettus aegyptiacus, a natural reservoir of Marburg virus and the only known reservoir for any filovirus. We found an expanded and diversified KLRC/KLRD family of natural killer cell receptors, MHC class I genes, and type I interferons, which dramatically differ from their functional counterparts in other mammals. Such concerted evolution of key components of bat immunity is strongly suggestive of novel modes of antiviral defense. An evaluation of the theoretical function of these genes suggests that an inhibitory immune state may exist in bats. Based on our findings, we hypothesize that tolerance of viral infection, rather than enhanced potency of antiviral defenses, may be a key mechanism by which bats asymptomatically host viruses that are pathogenic in humans. The genome of the Egyptian fruit bat reveals how its immune defenses allow tolerance of pathogenic viruses.",
keywords = "Chiroptera, antiviral immunity, filovirus, genome, innate immunity, natural killer cell receptors, type I interferon",
author = "Pavlovich, {Stephanie S.} and Lovett, {Sean P.} and Galina Koroleva and Guito, {Jonathan C.} and Arnold, {Catherine E.} and Nagle, {Elyse R.} and Kirsten Kulcsar and Albert Lee and Fran{\cc}oise Thibaud-Nissen and Hume, {Adam J.} and Elke M{\"u}hlberger and Uebelhoer, {Luke S.} and Towner, {Jonathan S.} and Raul Rabadan and Mariano Sanchez-Lockhart and Kepler, {Thomas B.} and Gustavo Palacios",
year = "2018",
month = "5",
day = "17",
doi = "10.1016/j.cell.2018.03.070",
language = "English (US)",
volume = "173",
pages = "1098--1110.e18",
journal = "Cell",
issn = "0092-8674",
publisher = "Cell Press",
number = "5",

}

TY - JOUR

T1 - The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity

AU - Pavlovich, Stephanie S.

AU - Lovett, Sean P.

AU - Koroleva, Galina

AU - Guito, Jonathan C.

AU - Arnold, Catherine E.

AU - Nagle, Elyse R.

AU - Kulcsar, Kirsten

AU - Lee, Albert

AU - Thibaud-Nissen, Françoise

AU - Hume, Adam J.

AU - Mühlberger, Elke

AU - Uebelhoer, Luke S.

AU - Towner, Jonathan S.

AU - Rabadan, Raul

AU - Sanchez-Lockhart, Mariano

AU - Kepler, Thomas B.

AU - Palacios, Gustavo

PY - 2018/5/17

Y1 - 2018/5/17

N2 - Bats harbor many viruses asymptomatically, including several notorious for causing extreme virulence in humans. To identify differences between antiviral mechanisms in humans and bats, we sequenced, assembled, and analyzed the genome of Rousettus aegyptiacus, a natural reservoir of Marburg virus and the only known reservoir for any filovirus. We found an expanded and diversified KLRC/KLRD family of natural killer cell receptors, MHC class I genes, and type I interferons, which dramatically differ from their functional counterparts in other mammals. Such concerted evolution of key components of bat immunity is strongly suggestive of novel modes of antiviral defense. An evaluation of the theoretical function of these genes suggests that an inhibitory immune state may exist in bats. Based on our findings, we hypothesize that tolerance of viral infection, rather than enhanced potency of antiviral defenses, may be a key mechanism by which bats asymptomatically host viruses that are pathogenic in humans. The genome of the Egyptian fruit bat reveals how its immune defenses allow tolerance of pathogenic viruses.

AB - Bats harbor many viruses asymptomatically, including several notorious for causing extreme virulence in humans. To identify differences between antiviral mechanisms in humans and bats, we sequenced, assembled, and analyzed the genome of Rousettus aegyptiacus, a natural reservoir of Marburg virus and the only known reservoir for any filovirus. We found an expanded and diversified KLRC/KLRD family of natural killer cell receptors, MHC class I genes, and type I interferons, which dramatically differ from their functional counterparts in other mammals. Such concerted evolution of key components of bat immunity is strongly suggestive of novel modes of antiviral defense. An evaluation of the theoretical function of these genes suggests that an inhibitory immune state may exist in bats. Based on our findings, we hypothesize that tolerance of viral infection, rather than enhanced potency of antiviral defenses, may be a key mechanism by which bats asymptomatically host viruses that are pathogenic in humans. The genome of the Egyptian fruit bat reveals how its immune defenses allow tolerance of pathogenic viruses.

KW - Chiroptera

KW - antiviral immunity

KW - filovirus

KW - genome

KW - innate immunity

KW - natural killer cell receptors

KW - type I interferon

UR - http://www.scopus.com/inward/record.url?scp=85045581421&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85045581421&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2018.03.070

DO - 10.1016/j.cell.2018.03.070

M3 - Article

C2 - 29706541

AN - SCOPUS:85045581421

VL - 173

SP - 1098-1110.e18

JO - Cell

JF - Cell

SN - 0092-8674

IS - 5

ER -