Novel inhibitory effect of galectin-3 on the respiratory burst induced by Staphylococcus aureus in human neutrophils
(2023) In Glycobiology 33(6). p.503-511- Abstract
Among the responders to microbial invasion, neutrophils represent the earliest and perhaps the most important immune cells that contribute to host defense with the primary role to kill invading microbes using a plethora of stored anti-microbial molecules. One such process is the production of reactive oxygen species (ROS) by the neutrophil enzyme complex NADPH-oxidase, which can be assembled and active either extracellularly or intracellularly in phagosomes (during phagocytosis) and/or granules (in absence of phagocytosis). One soluble factor modulating the interplay between immune cells and microbes is galectin-3 (gal-3), a carbohydrate-binding protein that regulates a wide variety of neutrophil functions. Gal-3 has been shown to... (More)
Among the responders to microbial invasion, neutrophils represent the earliest and perhaps the most important immune cells that contribute to host defense with the primary role to kill invading microbes using a plethora of stored anti-microbial molecules. One such process is the production of reactive oxygen species (ROS) by the neutrophil enzyme complex NADPH-oxidase, which can be assembled and active either extracellularly or intracellularly in phagosomes (during phagocytosis) and/or granules (in absence of phagocytosis). One soluble factor modulating the interplay between immune cells and microbes is galectin-3 (gal-3), a carbohydrate-binding protein that regulates a wide variety of neutrophil functions. Gal-3 has been shown to potentiate neutrophil interaction with bacteria, including Staphylococcus aureus, and is also a potent activator of the neutrophil respiratory burst, inducing large amounts of granule-localized ROS in primed cells. Herein, the role of gal-3 in regulating S. aureus phagocytosis and S. aureus-induced intracellular ROS was analyzed by imaging flow cytometry and luminol-based chemiluminescence, respectively. While gal-3 did not interfere with S. aureus phagocytosis per se, it potently inhibited phagocytosis-induced intracellular ROS production. Using the gal-3 inhibitor GB0139 (TD139) and gal-3C we found that the gal-3-induced inhibitory effect on ROS production was dependent on the carbohydrate recognition domain of the lectin. In summary, this is the first report of an inhibitory role of gal-3 in regulating phagocytosis-induced ROS production.
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- author
- Venkatakrishnan, Vignesh ; Elmwall, Jonas ; Lahiri, Trisha LU ; Sundqvist, Martina ; Bergqvist, Linda ; Leffler, Hakon LU ; Nilsson, Ulf J LU ; Welin, Amanda ; Bylund, Johan and Karlsson-Bengtsson, Anna
- organization
- publishing date
- 2023-06-21
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Staphylococcus aureus, galectin-3, neutrophils, phagocytosis, reactive oxygen species
- in
- Glycobiology
- volume
- 33
- issue
- 6
- pages
- 9 pages
- publisher
- Oxford University Press
- external identifiers
-
- pmid:37073717
- scopus:85164042203
- pmid:37073717
- ISSN
- 1460-2423
- DOI
- 10.1093/glycob/cwad032
- language
- English
- LU publication?
- yes
- id
- 72dba4b5-a56f-4124-82d1-ad0c29e54bc8
- date added to LUP
- 2023-05-01 22:23:41
- date last changed
- 2024-09-22 10:33:04
@article{72dba4b5-a56f-4124-82d1-ad0c29e54bc8,
abstract = {{<p>Among the responders to microbial invasion, neutrophils represent the earliest and perhaps the most important immune cells that contribute to host defense with the primary role to kill invading microbes using a plethora of stored anti-microbial molecules. One such process is the production of reactive oxygen species (ROS) by the neutrophil enzyme complex NADPH-oxidase, which can be assembled and active either extracellularly or intracellularly in phagosomes (during phagocytosis) and/or granules (in absence of phagocytosis). One soluble factor modulating the interplay between immune cells and microbes is galectin-3 (gal-3), a carbohydrate-binding protein that regulates a wide variety of neutrophil functions. Gal-3 has been shown to potentiate neutrophil interaction with bacteria, including <i>Staphylococcus aureus</i>, and is also a potent activator of the neutrophil respiratory burst, inducing large amounts of granule-localized ROS in primed cells. Herein, the role of gal-3 in regulating <i>S. aureus</i> phagocytosis and <i>S. aureus</i>-induced intracellular ROS was analyzed by imaging flow cytometry and luminol-based chemiluminescence, respectively. While gal-3 did not interfere with <i>S. aureus</i> phagocytosis per se, it potently inhibited phagocytosis-induced intracellular ROS production. Using the gal-3 inhibitor GB0139 (TD139) and gal-3C we found that the gal-3-induced inhibitory effect on ROS production was dependent on the carbohydrate recognition domain of the lectin. In summary, this is the first report of an inhibitory role of gal-3 in regulating phagocytosis-induced ROS production.</p>}},
author = {{Venkatakrishnan, Vignesh and Elmwall, Jonas and Lahiri, Trisha and Sundqvist, Martina and Bergqvist, Linda and Leffler, Hakon and Nilsson, Ulf J and Welin, Amanda and Bylund, Johan and Karlsson-Bengtsson, Anna}},
issn = {{1460-2423}},
keywords = {{Staphylococcus aureus; galectin-3; neutrophils; phagocytosis; reactive oxygen species}},
language = {{eng}},
month = {{06}},
number = {{6}},
pages = {{503--511}},
publisher = {{Oxford University Press}},
series = {{Glycobiology}},
title = {{Novel inhibitory effect of galectin-3 on the respiratory burst induced by <i>Staphylococcus aureus </i>in human neutrophils}},
url = {{http://dx.doi.org/10.1093/glycob/cwad032}},
doi = {{10.1093/glycob/cwad032}},
volume = {{33}},
year = {{2023}},
}