Structures of Xenopus Embryonic Epidermal Lectin Reveal a Conserved Mechanism of Microbial Glycan Recognition
Abstract
Intelectins (X-type lectins), broadly distributed throughout chordates, have been implicated in innate immunity. Xenopus laevis embryonic epidermal lectin (XEEL), an intelectin secreted into environmental water by the X. laevis embryo, is postulated to function as a defense against microbes. XEEL is homologous (64% identical) to human intelectin-1 (hIntL-1), which is also implicated in innate immune defense. We showed previously that hIntL-1 binds microbial glycans bearing exocyclic vicinal diol groups. It is unknown whether XEEL has the same ligand specificity. Also unclear is whether XEEL and hIntL-1 have similar quaternary structures, as XEEL lacks the corresponding cysteine residues in hIntL-1 that stabilize the disulfide-linked trimer. These observations prompted us to further characterize XEEL. We found that hIntL-1 and XEEL have similar structural features. Even without the corresponding intermolecular disulfide bonds present in hIntL-1, the carbohydrate recognition domain of XEEL (XEELCRD) forms a stable trimer in solution. The structure of XEELCRD in complex with d-glycerol-1-phosphate, a residue present in microbe-specific glycans, indicated that the exocyclic vicinal diol coordinates to a protein-bound calcium ion. This ligand-binding mode is conserved between XEEL and hIntL-1. The domain architecture of full-length XEEL is reminiscent of a barbell, with two sets of three glycan-binding sites oriented inmore »
- Authors:
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Inst. of Health; National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1770501
- Alternate Identifier(s):
- OSTI ID: 1254508
- Grant/Contract Number:
- AC02–06CH11357; AC02–76SF00515; AC02-06CH11357; AC02-76SF00515; R01GM55984; R01AI063596; T32 GM008505; IOS1353674; DGE-1256259; P41GM103393; BIR-9512577; S10 RR13790
- Resource Type:
- Journal Article: Published Article
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Name: Journal of Biological Chemistry Journal Volume: 291 Journal Issue: 11; Journal ID: ISSN 0021-9258
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; carbohydrate-binding protein; galactofuranose; innate immunity; lectin; protein cross-linking; X-ray crystallography; bacterial agglutination; glycerol phosphate; intelectin; omentin
Citation Formats
Wangkanont, Kittikhun, Wesener, Darryl A., Vidani, Jack A., Kiessling, Laura L., and Forest, Katrina T. Structures of Xenopus Embryonic Epidermal Lectin Reveal a Conserved Mechanism of Microbial Glycan Recognition. United States: N. p., 2016.
Web. doi:10.1074/jbc.M115.709212.
Wangkanont, Kittikhun, Wesener, Darryl A., Vidani, Jack A., Kiessling, Laura L., & Forest, Katrina T. Structures of Xenopus Embryonic Epidermal Lectin Reveal a Conserved Mechanism of Microbial Glycan Recognition. United States. https://doi.org/10.1074/jbc.M115.709212
Wangkanont, Kittikhun, Wesener, Darryl A., Vidani, Jack A., Kiessling, Laura L., and Forest, Katrina T. 2016.
"Structures of Xenopus Embryonic Epidermal Lectin Reveal a Conserved Mechanism of Microbial Glycan Recognition". United States. https://doi.org/10.1074/jbc.M115.709212.
@article{osti_1770501,
title = {Structures of Xenopus Embryonic Epidermal Lectin Reveal a Conserved Mechanism of Microbial Glycan Recognition},
author = {Wangkanont, Kittikhun and Wesener, Darryl A. and Vidani, Jack A. and Kiessling, Laura L. and Forest, Katrina T.},
abstractNote = {Intelectins (X-type lectins), broadly distributed throughout chordates, have been implicated in innate immunity. Xenopus laevis embryonic epidermal lectin (XEEL), an intelectin secreted into environmental water by the X. laevis embryo, is postulated to function as a defense against microbes. XEEL is homologous (64% identical) to human intelectin-1 (hIntL-1), which is also implicated in innate immune defense. We showed previously that hIntL-1 binds microbial glycans bearing exocyclic vicinal diol groups. It is unknown whether XEEL has the same ligand specificity. Also unclear is whether XEEL and hIntL-1 have similar quaternary structures, as XEEL lacks the corresponding cysteine residues in hIntL-1 that stabilize the disulfide-linked trimer. These observations prompted us to further characterize XEEL. We found that hIntL-1 and XEEL have similar structural features. Even without the corresponding intermolecular disulfide bonds present in hIntL-1, the carbohydrate recognition domain of XEEL (XEELCRD) forms a stable trimer in solution. The structure of XEELCRD in complex with d-glycerol-1-phosphate, a residue present in microbe-specific glycans, indicated that the exocyclic vicinal diol coordinates to a protein-bound calcium ion. This ligand-binding mode is conserved between XEEL and hIntL-1. The domain architecture of full-length XEEL is reminiscent of a barbell, with two sets of three glycan-binding sites oriented in opposite directions. This orientation is consistent with our observation that XEEL can promote the agglutination of specific serotypes of Streptococcus pneumoniae. Here, these data support a role for XEEL in innate immunity, and they highlight structural and functional conservation of X-type lectins among chordates.},
doi = {10.1074/jbc.M115.709212},
url = {https://www.osti.gov/biblio/1770501},
journal = {Journal of Biological Chemistry},
issn = {0021-9258},
number = 11,
volume = 291,
place = {United States},
year = {Tue Mar 01 00:00:00 EST 2016},
month = {Tue Mar 01 00:00:00 EST 2016}
}
Web of Science
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