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Dectin-1–Dependent LC3 Recruitment to Phagosomes Enhances Fungicidal Activity in Macrophages
Open accessAbstract
Autophagy has been postulated to play role in mammalian host defense against fungal pathogens, although the molecular details remain unclear. Here, we show that primary macrophages deficient in the autophagic factor LC3 demonstrate diminished fungicidal activity but increased cytokine production in response to Candida albicans stimulation. LC3 recruitment to fungal phagosomes requires activation of the fungal pattern receptor dectin-1. LC3 recruitment to the phagosome also requires Syk signaling but is independent of all activity by Toll-like receptors and does not require the presence of the adaptor protein Card9. We further demonstrate that reactive oxygen species generation by NADPH oxidase is required for LC3 recruitment to the fungal phagosome. These observations directly link LC3 to the inflammatory pathway against C. albicans in macrophages.
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“Of interest, the role of LAP in immunity against Aspergillus (200, 245) has not been shown for other fungi (255–257).”
From Aspergillus fumigatus and Aspergillosis in 2019 (2019) · cites this paper as [255]
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Aspergillus Cell Wall Melanin Blocks LC3-Associated Phagocytosis to Promote Pathogenicity
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BackgroundBetter Together: Current Insights Into Phagosome-Lysosome Fusion
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“Dectin-1 activation controls a wide range of immune responses, including regulation of leukocyte phagocytosis, recruitment of Toll-like receptor (TLR) 9 to phagolysosomes, phagolysosome maturation, activation of autophagy, production of reactive oxygen species (ROS), activation of the inflammasome, and induction of pr…”
BackgroundThe role of dectin-1 in health and disease
Kalia, N., Singh, J., & Kaur, M. (2021) · Immunobiology · doi:10.1016/j.imbio.2021.152071 · Cited by 102
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αv Integrins combine with LC3 and atg5 to regulate Toll-like receptor signalling in B cells
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“In addition to the direct effect on fungicidal functions, LAP impairment altersmacrophage antifungal cytokine response (20, 22), indicating the involvement of LAP in inflammation modulation.”
BackgroundMolecular Functions of Glycoconjugates in Autophagy
Fahie, K., & Zachara, N. E. (2016) · Journal of Molecular Biology · doi:10.1016/j.jmb.2016.06.011 · Cited by 53
“Beclin 1 and p62/sequestosome-1 were also localized at phagocytic vacuoles during Dectin 1-induced phagocytosis [95].”
BackgroundImmune cells fold and damage fungal hyphae
Bain, J. M., Alonso, M. F., Childers, D. S., Walls, C. A., Mackenzie, K. S., Pradhan, A., Lewis, L. E., Louw, J., Avelar, G. M., Larcombe, D. E., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2020484118 · Cited by 56
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LC3-associated phagocytosis in microbial pathogenesis
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Evans, R. J., Sundaramurthy, V., & Frickel, E. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00118 · Cited by 49
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“Indeed, consistent with the previous report (20), we found that C.”
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“(MHC-II) presentation of fungal-derived antigens to CD4þ T cells [217,219].”
BackgroundRoles of Autophagy and Autophagy-Related Proteins in Antifungal Immunity
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Canonical and Non-Canonical Autophagy in HIV-1 Replication Cycle
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Spleen Tyrosine Kinase Is a Critical Regulator of Neutrophil Responses to Candida Species
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“Reactive oxygen species production was measured as previously described (25).”
BackgroundSelf-citationLC3-Associated Phagocytosis in Bacterial Infection
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“ROS in macrophages drives the autophagic factor LC3 to phagosomes to enhance fungicidal activity [41].”
BackgroundSelf-citationTam, J. M., Reedy, J. L., Lukason, D. P., Kuna, S. G., Acharya, M., Khan, N. S., Negoro, P. E., Xu, S., Ward, R., Feldman, M. B., et al. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801384 · Cited by 33
“albicans phagosome, as we have shown previously (50).”
MethodSelf-citationβ-Glucan induces autophagy in dendritic cells and influences T-cell differentiation
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Host Response to Coccidioides Infection: Fungal Immunity
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“Specifically, Dectin-1 and TLR2 interactions with Coccidioides facilitates clearance by macrophages by promoting oxide species and pro-inflammatory cytokine production (Viriyakosol et al., 2005; Tam et al., 2014).”
BackgroundThe Role of Autophagy-Related Proteins in Candida albicans Infections
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“The generation of ROS in response to Candida regulates autophagy through a Dectin-1-Syk dependent mechanism [10].”
BackgroundSelf-citationAutophagy links antimicrobial activity with antigen presentation in Langerhans cells
Dang, A. T., Teles, R. M. B., Liu, P. T., Choi, A. W., Legaspi, A. J., Sarno, E. N., Ochoa, M. T., Parvatiyar, K., Cheng, G., Gilliet, M. F., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.126955 · Cited by 28
Self-citationThe C-Type Lectin Receptor Dectin-2 Is a Receptor for Aspergillus fumigatus Galactomannan
Reedy, J. L., Crossen, A. J., Negoro, P. E., Brown, H. E., Ward, R., Vargas-Blanco, D. A., Timmer, K. D., Reardon, C. M., Basham, K. J., Mansour, M. K., et al. (2023) · mBio · doi:10.1128/mbio.03184-22 · Cited by 26
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“…with the identification of NOX2 as a key regulator of LAP (Geng et al., 2022; Huang et al., 2009; Ligeon et al., 2021; Martinez et al., 2015; Tam et al., 2014), we report that LC3 recruitment to early endosomes and subsequent endolysosomal trafficking is reduced in NCF1 -deficient B cells,…”
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“53 Dectin-1, a Syk-coupled CLR expressing on myeloid cells, recognizes β-(1,3)-glucan 54 carbohydrates on various fungi (8-12).”
BackgroundAutophagy and LAP in the Fight against Fungal Infections: Regulation and Therapeutics
Oikonomou, V., Renga, G., LUCA, A. D., Borghi, M., Pariano, M., Puccetti, M., Paolicelli, G., Stincardini, C., Costantini, C., Bartoli, A., et al. (2018) · Mediators of Inflammation · doi:10.1155/2018/6195958 · Cited by 24
“LAP also occurred in response to Candida albicans depending upon the exposure of enough β-glucan on the cell surface [30].”
BackgroundInfluentialIt takes a village: Phagocytes play a central role in fungal immunity
Feldman, M. B., Vyas, J. M., & Mansour, M. K. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.04.008 · Cited by 27
Self-citationAspergillosis and stem cell transplantation: An overview of experimental pathogenesis studies
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The HIF-1α/LC3-II Axis Impacts Fungal Immunity in Human Macrophages
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“glabrata given its described contribution to phagolysosomal maturation (22) and autophagy (31).”
BackgroundMethodSelf-citationPhagocytosis of Candida albicans Inhibits Autophagic Flux in Macrophages
Duan, Z., Chen, Q., Du, L., Tong, J., Xu, S., Zeng, R., Ma, Y., Chen, X., & Li, M. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/4938649 · Cited by 16
“The finding that β-glucan can increase LC3-II level is in accordance with a previous report [12].”
ResultCrosstalk Between Autophagy and Hypoxia-Inducible Factor-1α in Antifungal Immunity
Quäschling, T., Friedrich, D., Deepe, G. S., & Rupp, J. (2020) · Cells · doi:10.3390/cells9102150 · Cited by 17
“albicans induce formation of microtubule-associated protein 1A/1B-light chain 3 (LC3) to the phagosome membrane, while there is not enough LC3 recruited to completely cover its surface [47].”
BackgroundCatalytic defense against fungal pathogens using nanozymes
Wu, Q., Zou, S., Wang, Q., Chen, L., Yan, X., & Gao, L. (2021) · Nanotechnology Reviews · doi:10.1515/ntrev-2021-0084 · Cited by 16
Chop, M., Ledo, C., Nicolao, M. C., Loos, J. A., Cumino, A. C., & Rodrígues, C. R. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1334211 · Cited by 16
“In eukaryotic cells, recognition of b - glucan motifs on the fungal cell wall by dectin-1 induces LC3 recruitment to phagosomes in macrophages (Tam et al., 2014).”
BackgroundLi, D., Bai, C., Zhang, Q., Li, Z., Shao, D., & Li, X. (2019) · The Journal of Microbiology · doi:10.1007/s12275-019-8298-1 · Cited by 15
Autophagy as an innate immunity response against pathogens: a Tango dance
Aguilera, M. O., Delgui, L. R., Reggiori, F., Romano, P. S., & Colombo, M. I. (2023) · FEBS Letters · doi:10.1002/1873-3468.14788 · Cited by 15
“…toll-like receptors (TLR1 – TLR2, the TLR2 – TLR6 and TLR4), immunoglobulin (Ig) receptors, and receptors mediating the clearance of cell corpses such as T cell immunoglobulin-and mucin domain-containing molecule-4 (TIM4), are involved in the recognition of LAPosome cargos [83,91,100,102,104,105].”
BackgroundZajta, E., Csonka, K., Tóth, A., Tiszlavicz, L., Németh, T., Orosz, A., Novák, Á., Csikós, M., Vágvölgyi, C., Mócsai, A., et al. (2021) · mBio · doi:10.1128/mbio.01608-21 · Cited by 16
“albicans in RAW cells (31, 47), our next step was testing if phagosome acidification following the phagocytosis of live C.”
BackgroundFungal Keratitis: Recent Advances in Diagnosis and Treatment
Suman, S., Kumar, A., Saxena, I., & Kumar, M. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.98411 · Cited by 13
“Autophagy can regulate IL-1β release in human primary macrophage to resist the fungal infection [50].”
BackgroundHuman intestinal epithelial cells can internalize luminal fungi via LC3-associated phagocytosis
Cohen‐Kedar, S., Barda, E. S., Rabinowitz, K. M., Keizer, D., Abu-Taha, H., Schwartz, S., Kaboub, K., Baram, L., Sadot, E., White, I. D., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1142492 · Cited by 12
“Frontiers in Immunology 10 In professional phagocytes, LAP of fungi enhances pathogen killing (35) (19), cytokine secretion (30)and promotes MHC class II recrui tment to the LAPosome for susta ined ant igen presentation (20).”
BackgroundInfluentialThe Carbohydrate Lectin Receptor Dectin-1 Mediates the Immune Response to Exserohilum rostratum
Reedy, J. L., Negoro, P. E., Feliu, M., Lord, A. K., Khan, N. S., Lukason, D. P., Wiederhold, N. P., Tam, J. M., Mansour, M. K., Patterson, T. F., et al. (2016) · Infection and Immunity · doi:10.1128/iai.00903-16 · Cited by 12
“Primary bone marrow-derived macrophages (BMDMs) from C57BL/6, Dectin-1 / , and MyD88/TRIF / mice were obtained as previously described (78).”
MethodSelf-citationThe roles of autophagy and mitophagy in corneal pathology: current knowledge and future perspectives
Ramachandran, R. A., Sanches, J. M., & Robertson, D. M. (2023) · Frontiers in Medicine · doi:10.3389/fmed.2023.1064938 · Cited by 11
Morita, M., Kajiye, M., Sakurai, C., Kubo, S., Takahashi, M., Kinoshita, D., Hori, N., & Hatsuzawa, K. (2020) · Biology Open · doi:10.1242/bio.051029 · Cited by 11
“Furthermore, LAP facilitates the maturation and bactericidal activity of phagosomes (Sanjuan et al., 2007; Huang et al., 2009; Tam et al., 2014); however, in some cases LAP rather suppresses the phagosome maturation and enhances the recruitment of major histocompatibility complex (MHC) class II molecules into phagosom…”
BackgroundA dynamically evolving war between autophagy and pathogenic microorganisms
Zheng, Q., Duan, L., Zhang, Y., Li, J., Zhang, S., & Wang, H. (2022) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b2100285 · Cited by 8
“Studies have found that the Dectin-1/Syk pathway mediates the occurrence of autophagy via ROS pro‐ duction, LC3-lipidation, and so on (Ma et al., 2012; Kyrmizi et al., 2013; Tam et al., 2014), which plays an important role in resisting fungal infection (Smeekens et al.”
BackgroundWhen the Phagosome Gets Leaky: Pore-Forming Toxin-Induced Non-Canonical Autophagy (PINCA)
Herb, M., Gluschko, A., Farid, A., & Krönke, M. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.834321 · Cited by 7
“LAP is induced by various surface receptors found on macrophages (Sanjuan et al., 2007; Ma et al., 2012; Tam et al., 2014; Gluschko et al., 2018; Hayashi et al., 2018) and results in the decoration of phagosomes with microtubule-associated protein 1 light chain-3 (LC3) family proteins, resulting in…”
BackgroundNeutrophil Engulfment in Cancer: Friend or Foe?
Lu, T., & Li, W. (2025) · Cancers · doi:10.3390/cancers17030384 · Cited by 8
“Additionally, macrophages utilize LAP to clear Candida albicans in a Dectin-1-dependent manner [126,127].”
Mycobacterial α-glucans hijack dectin-1 to facilitate intracellular bacterial survival
Torigoe, S., Salie, S., Keeton, R., Aylan, B., Appelmelk, B. J., Williams, D. L., Lowman, D. W., Sugiki, T., Matsumoto, S., Kawano, A., et al. (2026) · Science Immunology · doi:10.1126/sciimmunol.adw0732 · Cited by 6
“Whereas Dectin-1 can promote LC3B recruitment to fungal phagosomes (36), this receptor also induces activation of mTOR (4–6). mTOR blocks canonical autophagy pathways (37), and inhibition of this enzyme is known to be protective during mycobacterial infection (23).”
Luan, J., Zhang, Z., Wang, Q., Cui, L., Zhang, H., Zhang, Y., Peng, X., Zhao, G., & Lin, J. (2024) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.65.8.4 · Cited by 7
“40 We established the A. fumi-gatus infection model in vitro to verify the mechanism of fungal antigen-induced LAP in FK.”
MethodResultTranscriptomic Changes Predict Metabolic Alterations in LC3 Associated Phagocytosis in Aged Mice
Dhingra, A., Tobias, J. W., Philp, N. J., & Boesze‐Battaglia, K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076716 · Cited by 4
“In macrophages and other immune cells, defective LAP leads to increased inflammatory signaling and inflammatory cytokine production [3,99,100].”
BackgroundCastillo-Cruz, J., Palacios-Barreto, S., Mosso-Pani, M. A., Serna-Pérez, A. B., Rodríguez-Tovar, A. V., Serafín‐López, J., Castrejón-Jiménez, N. S., & García‐Pérez, B. E. (2025) · Microbial Pathogenesis · doi:10.1016/j.micpath.2025.107479 · Cited by 4
Sun, Y., Cui, X., & Zhang, Y. (2025) · Journal de Mycologie Médicale · doi:10.1016/j.mycmed.2025.101598 · Cited by 2
Li, Q., Zhao, F., Zhang, J., Yang, Y. N., Guo, Z., Wang, C., Yang, Q., Sun, Y., & Zhu, Z. (2022) · Journal of Immunology Research · doi:10.1155/2022/1481154 · Cited by 3
“A variety of receptors that activate LAP, such as TLRs and immunoglobulin (Ig) receptors, have been identified [15, 18, 21, 31, 32].”
Wong, S., Upadhyay, S., & Martinez, J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820538-9.00005-3 · Cited by 2
Xenophagy: Autophagy in Direct Pathogen Elimination
Jo, E., Kim, J. K., & Hwang, S. (2016) · Springer eBooks · doi:10.1007/978-3-319-30079-5_7 · Cited by 2
Reyne, E., Arrindell, J., Bestion, E., Mezouar, S., & Desnues, B. (2025) · Autophagy Reports · doi:10.1080/27694127.2025.2475527 · Cited by 1
Chronic Granulomatous Disease and Aspergillosis
Grimm, M. J., & Segal, B. H. (2017) · Springer eBooks · doi:10.1007/978-3-319-50842-9_4 · Cited by 1
Self-citationLi, D., Wang, L., Zhao, Z., Bai, C., & Li, X. (2023) · Immunology Letters · doi:10.1016/j.imlet.2023.09.006 · Cited by 1
Dectin-1 (CLEC7A, BGR, CLECSF12)
Asamaphan, P., Willment, J. A., & Brown, G. D. (2016) · Springer eBooks · doi:10.1007/978-4-431-56015-9_4 · Cited by 1
Host Autophagy in Antifungal Immunity
Nicola, A. M., Fabricant, S. A., Albuquerque, P., Felipe, M. S. S., & Casadevall, A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802936-7.00019-2 · Cited by 1
de Oliveira, G. P., de Sousa, H. R., Gorgonha, K. C. D. M., Borges, T. K. D. S., Rangel, K. T., Fabricant, S. A., Gustavo, F. C. K., Friaça, L. F., Neto, A. R., Hurtado, F. A., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.30.362681 · Cited by 1
“albicans and Aspergillus fumigatus has been 220 previously determined[21,22].”
BackgroundVancomycin impairs macrophage fungal killing by disrupting mitochondrial morphology and functionPreprint
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The NADPH oxidase-induced phagosomal environment of neutrophils and other phagocytes
Foote, J. R. (2019) · UCL Discovery (University College London)
A Candida parapsilosis in vivo fertőzés jellemzése: a sejtfal N-mannoziláció szerepe a virulenciában
Csonka, K. (2019) · SZTE Repository of Dissertations (University of Szeged) · doi:10.14232/phd.9954
LC3-associated phagocytosis in macrophage responses to Paracoccidioides spp.
de Oliveira, G. P., de Sousa, H. R., Gorgonha, K. C. D. M., Tomaz, L. L. M., Borges, T. K. D. S., Rangel, K. T., Fabricant, S. A., Gustafson, F. K., Albuquerque, L. F. F., Neto, A. R., et al. (2026) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/0074-02760250089
“2) and Table, the replication of previous studies (21) confirms our results.”
Réplication et séquestration du VIH-1 dans les macrophages
Lepont, L. (2020) · theses.fr (ABES) · doi:10.70675/40f6be5ez97e5z4043za0cdz0099a87dd935
Vancomycin disrupts mitochondrial morphology and function and impairs macrophage fungal killing
Bojang, E., Sheriff, L., Morris, E., Rouvray, S., Fu, M. S., Wellings, C., Abdissa, K., Stavrou, V., Clark, C., Southam, A. D., et al. (2026) · mBio · doi:10.1128/mbio.00580-26
“Previous work found that LC3 is readily recruited to C. albicans -containing phagosomes (14), and LC3-deficient macrophages are impaired in their C. albicans killing capacity and were more inflammatory, indicated by greater production of TNFα and IL-1β when stimulated with C. albicans yeast (25).”
From confrontation to co-adaptation: the dynamic dialogue of Candida albicans and macrophages
Miramón, P., Wilson, H. B., & Lorenz, M. C. (2026) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00191-22
“Importantly, NOX-derived ROS are required for LC3 recruitment, creating a functional coupling between oxidative burst and LAP-dependent maturation (193).”
Metadata
- Authors
- Tam, J. M., Mansour, M. K., Khan, N. S., Seward, M., Puranam, S., Tanne, A., Sokolovska, A., Becker, C. E., Acharya, M., Baird, M. A., Choi, A. M. K., Davidson, M. W., Segal, B. H., Lacy-Hulbert, A., Stuart, L. M., Xavier, R. J., & Vyas, J. M.
- Affiliations
- Harvard University (US)
- Tisch Cancer Institute (US)
- Massachusetts General Hospital (US)
- Broad Institute (US)
- Benaroya Research Institute (US)
- Florida State University (US)
- Weill Cornell Medicine (US)
- Roswell Park Comprehensive Cancer Center (US)
- Corresponding author
- Tam, Jenny M.
- ORCID
- Venue
- The Journal of Infectious Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-05-19
- Volume
- 210
- Issue
- 11
- Pages
- 1844-1854
- ISSN
- 0022-1899 (ISSN-L)
- 1537-6613
- PMC
- PMC4271056
- OpenAlex
- W2069844386
- Cited by
- 101
- References
- 48
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 5 · 2023: 7 · 2022: 6 · 2021: 9 · 2020: 10 · 2019: 14 · 2018: 12 · 2017: 9 · 2016: 12 · 2015: 6 · 2014: 1
- FWCI
- 7.07
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Infectious Diseases (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL055330)
- National Institute of Allergy and Infectious Diseases (R01AI092084, R01AI097519, R01AI079253)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- Dectin-1, LC3, autophagy, macrophages, Candida albicans, phagosome, fungal pathogen defense, Syk signaling, NADPH oxidase, reactive oxygen species, cytokine production, CARD9, Toll-like receptors
- MeSH terms
- Syk Kinase, Dectin-1, Animals, Candida albicans, Cell Line, Fungi, Macrophages, Microtubule-Associated Proteins, Models, Biological, Phagosomes, Phosphorylation, Protein-Tyrosine Kinases, Proteoglycans, Tumor Necrosis Factor-alpha, Signal Transduction, Interleukin-6, Reactive Oxygen Species, NADPH Oxidases, Lectins, C-Type, beta-Glucans, Intracellular Signaling Peptides and Proteins, Mice, CARD Signaling Adaptor Proteins, Interleukin-1beta
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