Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates

Toshiyuki Hayakawa, Zahra Khedri, Flavio Schwarz, Corinna Landig, Suh Yuen Liang, Hai Yu, Xi Chen, Naoko T. Fujito, Yoko Satta, Ajit Varki, Takashi Angata

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Background: Siglecs-11 and -16 are members of the sialic acid recognizing Ig-like lectin family, and expressed in same cells. Siglec-11 functions as an inhibitory receptor, whereas Siglec-16 exhibits activating properties. In humans, SIGLEC11 and SIGLEC16 gene sequences are extremely similar in the region encoding the extracellular domain due to gene conversions. Human SIGLEC11 was converted by the nonfunctional SIGLEC16P allele, and the converted SIGLEC11 allele became fixed in humans, possibly because it provides novel neuroprotective functions in brain microglia. However, the detailed evolutionary history of SIGLEC11 and SIGLEC16 in other primates remains unclear. Results: We analyzed SIGLEC11 and SIGLEC16 gene sequences of multiple primate species, and examined glycan binding profiles of these Siglecs. The phylogenetic tree demonstrated that gene conversions between SIGLEC11 and SIGLEC16 occurred in the region including the exon encoding the sialic acid binding domain in every primate examined. Functional assays showed that glycan binding preference is similar between Siglec-11 and Siglec-16 in all analyzed hominid species. Taken together with the fact that Siglec-11 and Siglec-16 are expressed in the same cells, Siglec-11 and Siglec-16 are regarded as paired receptors that have maintained similar ligand binding preferences via gene conversions. Relaxed functional constraints were detected on the SIGLEC11 and SIGLEC16 exons that underwent gene conversions, possibly contributing to the evolutionary acceptance of repeated gene conversions. The frequency of nonfunctional SIGLEC16P alleles is much higher than that of SIGLEC16 alleles in every human population. Conclusions: Our findings indicate that Siglec-11 and Siglec-16 have been maintained as paired receptors by repeated gene conversions under relaxed functional constraints in the primate lineage. The high prevalence of the nonfunctional SIGLEC16P allele and the fixation of the converted SIGLEC11 imply that the loss of Siglec-16 and the gain of Siglec-11 in microglia might have been favored during the evolution of human lineage.

Original languageEnglish (US)
Article number228
JournalBMC Evolutionary Biology
Volume17
Issue number1
DOIs
StatePublished - Nov 23 2017

Fingerprint

gene conversion
coevolution
primate
Primates
gene
alleles
allele
sialic acids
neuroglia
receptors
exons
polysaccharides
nucleotide sequences
Hominidae
human population
lectins
hominid
acid
cells
ligand

Keywords

  • Coevolution
  • Gene conversion
  • Paired receptors
  • Primates
  • Sialic acid

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

Cite this

Hayakawa, T., Khedri, Z., Schwarz, F., Landig, C., Liang, S. Y., Yu, H., ... Angata, T. (2017). Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates. BMC Evolutionary Biology, 17(1), [228]. https://doi.org/10.1186/s12862-017-1075-z

Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates. / Hayakawa, Toshiyuki; Khedri, Zahra; Schwarz, Flavio; Landig, Corinna; Liang, Suh Yuen; Yu, Hai; Chen, Xi; Fujito, Naoko T.; Satta, Yoko; Varki, Ajit; Angata, Takashi.

In: BMC Evolutionary Biology, Vol. 17, No. 1, 228, 23.11.2017.

Research output: Contribution to journalArticle

Hayakawa, T, Khedri, Z, Schwarz, F, Landig, C, Liang, SY, Yu, H, Chen, X, Fujito, NT, Satta, Y, Varki, A & Angata, T 2017, 'Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates', BMC Evolutionary Biology, vol. 17, no. 1, 228. https://doi.org/10.1186/s12862-017-1075-z
Hayakawa T, Khedri Z, Schwarz F, Landig C, Liang SY, Yu H et al. Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates. BMC Evolutionary Biology. 2017 Nov 23;17(1). 228. https://doi.org/10.1186/s12862-017-1075-z
Hayakawa, Toshiyuki ; Khedri, Zahra ; Schwarz, Flavio ; Landig, Corinna ; Liang, Suh Yuen ; Yu, Hai ; Chen, Xi ; Fujito, Naoko T. ; Satta, Yoko ; Varki, Ajit ; Angata, Takashi. / Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates. In: BMC Evolutionary Biology. 2017 ; Vol. 17, No. 1.
@article{c064dc631d6246188aa7eaf10a294a46,
title = "Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates",
abstract = "Background: Siglecs-11 and -16 are members of the sialic acid recognizing Ig-like lectin family, and expressed in same cells. Siglec-11 functions as an inhibitory receptor, whereas Siglec-16 exhibits activating properties. In humans, SIGLEC11 and SIGLEC16 gene sequences are extremely similar in the region encoding the extracellular domain due to gene conversions. Human SIGLEC11 was converted by the nonfunctional SIGLEC16P allele, and the converted SIGLEC11 allele became fixed in humans, possibly because it provides novel neuroprotective functions in brain microglia. However, the detailed evolutionary history of SIGLEC11 and SIGLEC16 in other primates remains unclear. Results: We analyzed SIGLEC11 and SIGLEC16 gene sequences of multiple primate species, and examined glycan binding profiles of these Siglecs. The phylogenetic tree demonstrated that gene conversions between SIGLEC11 and SIGLEC16 occurred in the region including the exon encoding the sialic acid binding domain in every primate examined. Functional assays showed that glycan binding preference is similar between Siglec-11 and Siglec-16 in all analyzed hominid species. Taken together with the fact that Siglec-11 and Siglec-16 are expressed in the same cells, Siglec-11 and Siglec-16 are regarded as paired receptors that have maintained similar ligand binding preferences via gene conversions. Relaxed functional constraints were detected on the SIGLEC11 and SIGLEC16 exons that underwent gene conversions, possibly contributing to the evolutionary acceptance of repeated gene conversions. The frequency of nonfunctional SIGLEC16P alleles is much higher than that of SIGLEC16 alleles in every human population. Conclusions: Our findings indicate that Siglec-11 and Siglec-16 have been maintained as paired receptors by repeated gene conversions under relaxed functional constraints in the primate lineage. The high prevalence of the nonfunctional SIGLEC16P allele and the fixation of the converted SIGLEC11 imply that the loss of Siglec-16 and the gain of Siglec-11 in microglia might have been favored during the evolution of human lineage.",
keywords = "Coevolution, Gene conversion, Paired receptors, Primates, Sialic acid",
author = "Toshiyuki Hayakawa and Zahra Khedri and Flavio Schwarz and Corinna Landig and Liang, {Suh Yuen} and Hai Yu and Xi Chen and Fujito, {Naoko T.} and Yoko Satta and Ajit Varki and Takashi Angata",
year = "2017",
month = "11",
day = "23",
doi = "10.1186/s12862-017-1075-z",
language = "English (US)",
volume = "17",
journal = "BMC Evolutionary Biology",
issn = "1471-2148",
publisher = "BioMed Central",
number = "1",

}

TY - JOUR

T1 - Coevolution of Siglec-11 and Siglec-16 via gene conversion in primates

AU - Hayakawa, Toshiyuki

AU - Khedri, Zahra

AU - Schwarz, Flavio

AU - Landig, Corinna

AU - Liang, Suh Yuen

AU - Yu, Hai

AU - Chen, Xi

AU - Fujito, Naoko T.

AU - Satta, Yoko

AU - Varki, Ajit

AU - Angata, Takashi

PY - 2017/11/23

Y1 - 2017/11/23

N2 - Background: Siglecs-11 and -16 are members of the sialic acid recognizing Ig-like lectin family, and expressed in same cells. Siglec-11 functions as an inhibitory receptor, whereas Siglec-16 exhibits activating properties. In humans, SIGLEC11 and SIGLEC16 gene sequences are extremely similar in the region encoding the extracellular domain due to gene conversions. Human SIGLEC11 was converted by the nonfunctional SIGLEC16P allele, and the converted SIGLEC11 allele became fixed in humans, possibly because it provides novel neuroprotective functions in brain microglia. However, the detailed evolutionary history of SIGLEC11 and SIGLEC16 in other primates remains unclear. Results: We analyzed SIGLEC11 and SIGLEC16 gene sequences of multiple primate species, and examined glycan binding profiles of these Siglecs. The phylogenetic tree demonstrated that gene conversions between SIGLEC11 and SIGLEC16 occurred in the region including the exon encoding the sialic acid binding domain in every primate examined. Functional assays showed that glycan binding preference is similar between Siglec-11 and Siglec-16 in all analyzed hominid species. Taken together with the fact that Siglec-11 and Siglec-16 are expressed in the same cells, Siglec-11 and Siglec-16 are regarded as paired receptors that have maintained similar ligand binding preferences via gene conversions. Relaxed functional constraints were detected on the SIGLEC11 and SIGLEC16 exons that underwent gene conversions, possibly contributing to the evolutionary acceptance of repeated gene conversions. The frequency of nonfunctional SIGLEC16P alleles is much higher than that of SIGLEC16 alleles in every human population. Conclusions: Our findings indicate that Siglec-11 and Siglec-16 have been maintained as paired receptors by repeated gene conversions under relaxed functional constraints in the primate lineage. The high prevalence of the nonfunctional SIGLEC16P allele and the fixation of the converted SIGLEC11 imply that the loss of Siglec-16 and the gain of Siglec-11 in microglia might have been favored during the evolution of human lineage.

AB - Background: Siglecs-11 and -16 are members of the sialic acid recognizing Ig-like lectin family, and expressed in same cells. Siglec-11 functions as an inhibitory receptor, whereas Siglec-16 exhibits activating properties. In humans, SIGLEC11 and SIGLEC16 gene sequences are extremely similar in the region encoding the extracellular domain due to gene conversions. Human SIGLEC11 was converted by the nonfunctional SIGLEC16P allele, and the converted SIGLEC11 allele became fixed in humans, possibly because it provides novel neuroprotective functions in brain microglia. However, the detailed evolutionary history of SIGLEC11 and SIGLEC16 in other primates remains unclear. Results: We analyzed SIGLEC11 and SIGLEC16 gene sequences of multiple primate species, and examined glycan binding profiles of these Siglecs. The phylogenetic tree demonstrated that gene conversions between SIGLEC11 and SIGLEC16 occurred in the region including the exon encoding the sialic acid binding domain in every primate examined. Functional assays showed that glycan binding preference is similar between Siglec-11 and Siglec-16 in all analyzed hominid species. Taken together with the fact that Siglec-11 and Siglec-16 are expressed in the same cells, Siglec-11 and Siglec-16 are regarded as paired receptors that have maintained similar ligand binding preferences via gene conversions. Relaxed functional constraints were detected on the SIGLEC11 and SIGLEC16 exons that underwent gene conversions, possibly contributing to the evolutionary acceptance of repeated gene conversions. The frequency of nonfunctional SIGLEC16P alleles is much higher than that of SIGLEC16 alleles in every human population. Conclusions: Our findings indicate that Siglec-11 and Siglec-16 have been maintained as paired receptors by repeated gene conversions under relaxed functional constraints in the primate lineage. The high prevalence of the nonfunctional SIGLEC16P allele and the fixation of the converted SIGLEC11 imply that the loss of Siglec-16 and the gain of Siglec-11 in microglia might have been favored during the evolution of human lineage.

KW - Coevolution

KW - Gene conversion

KW - Paired receptors

KW - Primates

KW - Sialic acid

UR - http://www.scopus.com/inward/record.url?scp=85035815942&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85035815942&partnerID=8YFLogxK

U2 - 10.1186/s12862-017-1075-z

DO - 10.1186/s12862-017-1075-z

M3 - Article

C2 - 29169316

AN - SCOPUS:85035815942

VL - 17

JO - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

SN - 1471-2148

IS - 1

M1 - 228

ER -