Evolution: Decoy Receptors as Unique Weapons to Fight Pathogens

Zimmermann, Wolfgang

doi:10.1016/j.cub.2018.12.006

Cited by 9 publications

(8 citation statements)

References 18 publications

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“…It has been suggested that gene conversion between CEACAM paralogs works to preserve the ability of CEACAM3 to effectively mimic bacterially antagonized CEACAMs and thereby maintain its function as a decoy receptor (Zid and Drouin, 2013;Zimmermann, 2019). Indeed, our results and those of Adrian et al (Adrian et al, 2019) support the importance of gene conversion for maintaining the similarity of CEACAM3 to other bacterial adhesin binding CEACAMs in apes and Old World monkeys.…”

Section: Discussionsupporting

confidence: 72%

“…Overall, the rapid shuffling of genetic variation among CEACAM genes that we observe could greatly augment the 1 potential for host adaptation in the face of microbial antagonism. 2It has been suggested that gene conversion between CEACAM paralogs works to preserve the ability of 3 CEACAM3 to effectively mimic bacterially antagonized CEACAMs and thereby maintain its function as a decoy receptor (Zid and Drouin, 2013;Zimmermann, 2019). Indeed, our results and those There is no evidence that New World monkeys encode a CEACAM3 homolog, yet within this group gene conversion appears to be frequent between CEACAM1, CEACAM5, and CEACAM6 (Figure 4C).…”

Section: Discussionmentioning

confidence: 56%

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Evolution of host-microbe cell adherence by receptor domain shuffling

Baker

Sayegh

Köhler

et al. 2021

Preprint

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Stable adherence to epithelial surfaces is required for colonization by diverse host-associated microbes. Successful attachment of pathogenic microbes via surface adhesin molecules is also the first step in many devastating infections. Despite the primacy of epithelial adherence in establishing host-microbe associations, the evolutionary processes that shape this crucial interface remain enigmatic. Carcinoembryonic antigen associated cell adhesion molecules (CEACAMs) encompass a multifunctional family of vertebrate cell surface proteins which are recurrent targets of bacterial surface adhesins at epithelial surfaces. Here we show that multiple members of the primate CEACAM family exhibit evidence of repeated natural selection at protein surfaces targeted by bacteria, consistent with pathogen-driven evolution. Inter-species diversity of CEACAM proteins, between even closely-related great apes, determines molecular interactions with a range of bacterial adhesins. Phylogenetic analyses reveal that repeated gene conversion of CEACAM extracellular domains during primate divergence plays a key role in limiting bacterial adhesin tropism. Moreover, we demonstrate that gene conversion has continued to shape CEACAM diversity within human populations, with abundant CEACAM1 variants mediating evasion of adhesins from Neisseria gonorrhoeae, the causative agent of gonorrhea. Together this work reveals a mechanism by which gene conversion shapes first contact between microbes and animal hosts.

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Section: Discussionsupporting

confidence: 72%

Section: Discussionmentioning

confidence: 56%

Evolution of host-microbe cell adherence by receptor domain shuffling

Baker

Sayegh

Köhler

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…It has been suggested that gene conversion between CEACAM paralogs preserves the ability of CEACAM3 to effectively mimic bacterially antagonized CEACAMs and thereby maintain its function as a decoy receptor ( Zid and Drouin, 2013 ; Zimmermann, 2019 ). Indeed, our results and those of Adrian et al, 2019 , support the importance of maintaining the similarity of CEACAM3 to other adhesin-binding CEACAMs in apes and Old World monkeys.…”

Section: Discussionmentioning

confidence: 99%

Evolution of host-microbe cell adherence by receptor domain shuffling

Baker

Sayegh

Köhler

et al. 2022

eLife

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Stable adherence to epithelial surfaces is required for colonization by diverse host-associated microbes. Successful attachment of pathogenic microbes to host cells via adhesin molecules is also the first step in many devastating infections. Despite the primacy of epithelial adherence in establishing host-microbe associations, the evolutionary processes that shape this crucial interface remain enigmatic. Carcinoembryonic antigen associated cell adhesion molecules (CEACAMs) encompass a multifunctional family of vertebrate cell surface proteins which are recurrent targets of bacterial adhesins at epithelial barriers. Here we show that multiple members of the primate CEACAM family exhibit evidence of repeated natural selection at protein surfaces targeted by bacteria, consistent with pathogen-driven evolution. Divergence of CEACAM proteins between even closely related great apes is sufficient to control molecular interactions with a range of bacterial adhesins. Phylogenetic analyses further reveal that repeated gene conversion of CEACAM extracellular domains during primate divergence plays a key role in limiting bacterial adhesin host tropism. Moreover, we demonstrate that gene conversion has continued to shape CEACAM diversity within human populations, with abundant human CEACAM1 variants mediating evasion of adhesins from pathogenic Neisseria. Together this work reveals a mechanism by which gene conversion shapes first contact between microbes and animal hosts.

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“…This is one of the many forms of "molecular deception" that may take place between parasites and hosts (Massey and Mishra 2018). A well-studied example of decoy molecules in humans is carcinoembryonic antigen-related cell adhesion 3 (CEACAM3), which mimics the cell adhesion molecule and immune inhibitory receptor CEACAM1 (Zimmermann 2019). Several bacterial and fungal pathogens bind CEACAM1 in order to attach to host cells, penetrate them, and/ or modulate innate immune responses.…”

Section: Decoy Moleculesmentioning

confidence: 99%

“…Granulocytes express CEACAM3, which has a similar structure but induces phagocytosis of the parasites that bind it. In the resulting coevolutionary race, CEACAM1 is selected to avoid binding to parasites, parasites are selected to selectively bind CEACAM1 while avoiding CEACAM3, and CEACAM3 is selected to counteract the resulting binding loss (Zimmermann 2019). Unsurprisingly, CEACAM3 is one of the fastest-evolving genes in the human genome; moreover, CEACAM3 homologues from various primate species bind preferentially to host-specific parasites (Adrian et al 2019).…”

Section: Decoy Moleculesmentioning

confidence: 99%

Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

Giudice¹

2019

The Quarterly Review of Biology

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keywords behavior, brain evolution, hormones, neurobiology, parasite-host interactions, parasite manipulation abstract The ability of parasites to manipulate host behavior to their advantage has been studied extensively, but the impact of parasite manipulation on the evolution of neural and endocrine mechanisms has remained virtually unexplored. If selection for countermeasures has shaped the evolution of nervous systems, many aspects of neural functioning are likely to remain poorly understood until parasites-the brain's invisible designers-are included in the picture. This article offers the first systematic discussion of brain evolution in light of parasite manipulation. After reviewing the strategies and mechanisms employed by parasites, the paper presents a taxonomy of host countermeasures with four main categories, namely: restrict access to the brain; increase the costs of manipulation; increase the complexity of signals; and increase robustness. For each category, possible examples of countermeasures are explored, and the likely evolutionary responses by parasites are considered. The article then discusses the metabolic, computational, and ecological constraints that limit the evolution of countermeasures. The final sections offer suggestions for future research and consider some implications for basic neuroscience and psychopharmacology. The paper aims to present a novel perspective on brain evolution, chart a provisional way forward, and stimulate research across the relevant disciplines.

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Evolution: Decoy Receptors as Unique Weapons to Fight Pathogens

Cited by 9 publications

References 18 publications

Evolution of host-microbe cell adherence by receptor domain shuffling

Evolution of host-microbe cell adherence by receptor domain shuffling

Evolution of host-microbe cell adherence by receptor domain shuffling

Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

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