Dectin-1 Activation Controls Maturation of β-1,3-Glucan-containing Phagosomes

Mansour, Michael K.; Tam, Jenny M.; Khan, Nida S.; Seward, Michael; Davids, Peter J.; Puranam, Sravanthi; Sokolovska, Anna; Sykes, David B.; Dagher, Zeina; Becker, Christine; Tanne, Antoine; Reedy, Jennifer L.; Stuart, Lynda M.; Vyas, Jatin M.

doi:10.1074/jbc.m113.473223

Cited by 85Immune Response and InflammationPhagocytosis and Immune RegulationNeutrophil, Myeloperoxidase and Oxidative Mechanisms

Dectin-1 Activation Controls Maturation of β-1,3-Glucan-containing Phagosomes

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Mansour, Michael K., Tam, Jenny M., Khan, Nida S., Seward, Michael, Davids, Peter J., Puranam, Sravanthi, Sokolovska, Anna, Sykes, David B. +6 more·2013·Journal of Biological Chemistry

DOI 10.1074/jbc.m113.473223PMC PMC3668760

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Abstract

Elimination of fungal pathogens by phagocytes requires phagosome maturation, a process that involves the recruitment and fusion of intracellular proteins. The role of Dectin-1, a β-1,3-glucan receptor, critical for fungal recognition and triggering of Th17 responses, to phagosomal maturation has not been defined. We show that GFP-Dectin-1 translocates to the fungal phagosome, but its signal decays after 2 h. Inhibition of acidification results in retention of GFP-Dectin-1 to phagosome membranes highlighting the requirement for an acidic pH. Following β-1,3-glucan recognition, GFP-Dectin-1 undergoes tyrosine phosphorylation by Src kinases with subsequent Syk activation. Our results demonstrate that Syk is activated independently of intraphagosomal pH. Inhibition of Src or Syk results in prolonged retention of GFP-Dectin-1 to the phagosome signifying a link between Syk and intraphagosomal pH. β-1,3-glucan phagosomes expressing a signaling incompetent Dectin-1 failed to mature as demonstrated by prolonged Dectin-1 retention, presence of Rab5B, failure to acquire LAMP-1 and inability to acidify. Phagosomes containing Candida albicans also require Dectin-1-dependent Syk activation for phagosomal maturation. Taken together, these results support a model where Dectin-1 not only controls internalization of β-1,3-glucan containing cargo and triggers proinflammatory cytokines, but also acts as a master regulator for subsequent phagolysosomal maturation through Syk activation. Background: Dectin-1 is able to recognize and phagocytose the fungal carbohydrate, β-1,3-glucan, but its contribution to phagosomal maturation has not been explored. Results: Dectin-1-dependent Syk activation promotes phagolysosomal fusion and acidification. Conclusion: Dectin-1-dependent Syk-activation permits egress of early phagosomes to mature phagolysosomes. Significance: The surface recognition receptor, Dectin-1 shapes anti-fungal responses by controlling fungal phagosome maturation.

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Dectin-1/Syk kinase signaling directly regulates maturation of β-glucan-containing phagosomes.
“Furthermore, Dectin-1/Syk kinase signaling directly regulates maturation of β-glucan-containing phagosomes (251).”
From Aspergillus fumigatus and Aspergillosis in 2019 (2019) · cites this paper as [251]

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Dectin-1 controls maturation of fungal phagosomes (55.1)
Mansour, M. K., Tam, J. M., Khan, N. S., Puranam, S., & Vyas, J. M. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.188.supp.55.1
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Dectin-1 Signaling Recruits Elements of the Autophagic Machinery to Candida albicans-containing Phagosomes (55.2)
Tam, J. M., Tanne, A. J., Khan, N. S., Mansour, M. K., Becker, C., Sokolovska, A., Stuart, L. M., Xavier, R. J., & Vyas, J. M. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.188.supp.55.2
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Dectin-1 Controls TLR9 Trafficking to Phagosomes Containing β-1,3 Glucan
Khan, N. S., Kasperkovitz, P. V., Timmons, A. K., Mansour, M. K., Tam, J. M., Seward, M. W., Reedy, J. L., Puranam, S., Feliu, M., & Vyas, J. M. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1401545 · Cited by 51 · see citing works
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SHORT COMMUNICATION Internalization of Dectin-1 terminates induction of inflammatory responses
Hernanz‐Falcón, P., Joffre, O. P., Williams, D. L., & Sousa, C. R. E. (2013)
Dectin-1-triggered Recruitment of Light Chain 3 Protein to Phagosomes Facilitates Major Histocompatibility Complex Class II Presentation of Fungal-derived Antigens
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Authors: Mansour, M. K., Tam, J. M., Khan, N. S., Seward, M., Davids, P. J., Puranam, S., Sokolovska, A., Sykes, D. B., Dagher, Z., Becker, C., Tanne, A., Reedy, J. L., Stuart, L. M., & Vyas, J. M.
Affiliations: Harvard University (US)
Bowdoin College (US)
Massachusetts Institute of Technology (US)
Broad Institute (US)
Corresponding author: Vyas, Jatin M.
ORCID: Mansour, Michael K.
Tam, Jenny M.
Khan, Nida S.
Seward, Michael
Sokolovska, Anna
Sykes, David B.
Dagher, Zeina
Becker, Christine
Tanne, Antoine
Reedy, Jennifer L.
Stuart, Lynda M.
Vyas, Jatin M.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2013-05
Volume: 288
Issue: 22
Pages: 16043-16054
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m113.473223
PMC: PMC3668760
OpenAlex: W2129533912
Cited by: 85
References: 46
Citations by year: 2026: 5 · 2025: 6 · 2024: 3 · 2023: 7 · 2022: 3 · 2021: 6 · 2020: 8 · 2019: 6 · 2018: 12 · 2017: 4 · 2016: 9 · 2015: 7 · 2014: 6 · 2013: 3
FWCI: 4.61
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 2686 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
Funders: Alex's Lemonade Stand Foundation for Childhood Cancer
National Institutes of Health
National Institute of Allergy and Infectious Diseases (R01AI092084, R01AI079198, T32-AI007061-35, T32AI007061)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK043351)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Keywords: Dectin-1, phagosome maturation, phagolysosomes, β-1,3-glucan, Syk activation, Src kinase, phagosome acidification, Rab5b, LAMP1, Candida albicans, fungal recognition, phagocytosis, tyrosine phosphorylation
MeSH terms: Syk Kinase, Dectin-1, Animals, Candida albicans, Cell Line, Enzyme Activation, Phagosomes, Protein-Tyrosine Kinases, Cytokines, Inflammation Mediators, rab5 GTP-Binding Proteins, Lectins, C-Type, beta-Glucans, Intracellular Signaling Peptides and Proteins, Mice

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Dectin-1 Activation Controls Maturation of β-1,3-Glucan-containing Phagosomes

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