Surfactant protein D inhibits growth, alters cell surface polysaccharide exposure and immune activation potential of Aspergillus fumigatus
•Surfactant protein D (SP-D), a C-type lectin and a major humoral immune component in the human lung-alveoli, shows direct growth inhibitory effect on Aspergillus fumigatus, an airborne opportunistic fungal pathogen.•SP-D treatment modifies the surface architecture and cell wall polysaccharide expos...
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Published in | Cell surface (Amsterdam) Vol. 8; p. 100072 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier B.V
01.12.2022
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Abstract | •Surfactant protein D (SP-D), a C-type lectin and a major humoral immune component in the human lung-alveoli, shows direct growth inhibitory effect on Aspergillus fumigatus, an airborne opportunistic fungal pathogen.•SP-D treatment modifies the surface architecture and cell wall polysaccharide exposure on the A. fumigatus hyphae.•A. fumigatus hyphae grown in presence of SP-D stimulate significantly lower secretions of pro-inflammatory cytokine, but higher anti-inflammatory cytokine and chemokine secretions upon interaction with immune cells, compared to hyphae grown without SP-D.•Increased permeability of A. fumigatus hyphae upon SP-D treatment leads to a better efficacy of voriconazole, an antifungal drug that has its target in the fungal cytosol.
Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to Aspergillus fumigatus, an airborne fungal pathogen. Previously, we have demonstrated that surfactant protein D (SP-D), a major humoral component in human lung-alveoli, recognizes A. fumigatus conidial surface exposed melanin pigment. Through binding to melanin, SP-D opsonizes conidia, facilitates conidial phagocytosis, and induces the expression of protective pro-inflammatory cytokines in the phagocytic cells. In addition to melanin, SP-D also interacts with galactomannan (GM) and galactosaminogalactan (GAG), the cell wall polysaccharides exposed on germinating conidial surfaces. Therefore, we aimed at unravelling the biological significance of SP-D during the germination process. Here, we demonstrate that SP-D exerts direct fungistatic activity by restricting A. fumigatus hyphal growth. Conidial germination in the presence of SP-D significantly increased the exposure of cell wall polysaccharides chitin, α-1,3-glucan and GAG, and decreased β-1,3-glucan exposure on hyphae, but that of GM was unaltered. Hyphae grown in presence of SP-D showed positive immunolabelling for SP-D. Additionally, SP-D treated hyphae induced lower levels of pro-inflammatory cytokine, but increased IL-10 (anti-inflammatory cytokine) and IL-8 (a chemokine) secretion by human peripheral blood mononuclear cells (PBMCs), compared to control hyphae. Moreover, germ tube surface modifications due to SP-D treatment resulted in an increased hyphal susceptibility to voriconazole, an antifungal drug. It appears that SP-D exerts its anti-A. fumigatus functions via a range of mechanisms including hyphal growth-restriction, hyphal surface modification, masking of hyphal surface polysaccharides and thus altering hyphal immunostimulatory properties. |
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AbstractList | Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to
, an airborne fungal pathogen. Previously, we have demonstrated that surfactant protein D (SP-D), a major humoral component in human lung-alveoli, recognizes
conidial surface exposed melanin pigment. Through binding to melanin, SP-D opsonizes conidia, facilitates conidial phagocytosis, and induces the expression of protective pro-inflammatory cytokines in the phagocytic cells. In addition to melanin, SP-D also interacts with galactomannan (GM) and galactosaminogalactan (GAG), the cell wall polysaccharides exposed on germinating conidial surfaces. Therefore, we aimed at unravelling the biological significance of SP-D during the germination process. Here, we demonstrate that SP-D exerts direct fungistatic activity by restricting
hyphal growth. Conidial germination in the presence of SP-D significantly increased the exposure of cell wall polysaccharides chitin, α-1,3-glucan and GAG, and decreased β-1,3-glucan exposure on hyphae, but that of GM was unaltered. Hyphae grown in presence of SP-D showed positive immunolabelling for SP-D. Additionally, SP-D treated hyphae induced lower levels of pro-inflammatory cytokine, but increased IL-10 (anti-inflammatory cytokine) and IL-8 (a chemokine) secretion by human peripheral blood mononuclear cells (PBMCs), compared to control hyphae. Moreover, germ tube surface modifications due to SP-D treatment resulted in an increased hyphal susceptibility to voriconazole, an antifungal drug. It appears that SP-D exerts its anti-
functions via a range of mechanisms including hyphal growth-restriction, hyphal surface modification, masking of hyphal surface polysaccharides and thus altering hyphal immunostimulatory properties. Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to Aspergillus fumigatus, an airborne fungal pathogen. Previously, we have demonstrated that surfactant protein D (SP-D), a major humoral component in human lung-alveoli, recognizes A. fumigatus conidial surface exposed melanin pigment. Through binding to melanin, SP-D opsonizes conidia, facilitates conidial phagocytosis, and induces the expression of protective pro-inflammatory cytokines in the phagocytic cells. In addition to melanin, SP-D also interacts with galactomannan (GM) and galactosaminogalactan (GAG), the cell wall polysaccharides exposed on germinating conidial surfaces. Therefore, we aimed at unravelling the biological significance of SP-D during the germination process. Here, we demonstrate that SP-D exerts direct fungistatic activity by restricting A. fumigatus hyphal growth. Conidial germination in the presence of SP-D significantly increased the exposure of cell wall polysaccharides chitin, α-1,3-glucan and GAG, and decreased β-1,3-glucan exposure on hyphae, but that of GM was unaltered. Hyphae grown in presence of SP-D showed positive immunolabelling for SP-D. Additionally, SP-D treated hyphae induced lower levels of pro-inflammatory cytokine, but increased IL-10 (anti-inflammatory cytokine) and IL-8 (a chemokine) secretion by human peripheral blood mononuclear cells (PBMCs), compared to control hyphae. Moreover, germ tube surface modifications due to SP-D treatment resulted in an increased hyphal susceptibility to voriconazole, an antifungal drug. It appears that SP-D exerts its anti-A. fumigatus functions via a range of mechanisms including hyphal growth-restriction, hyphal surface modification, masking of hyphal surface polysaccharides and thus altering hyphal immunostimulatory properties. Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to Aspergillus fumigatus, an airborne fungal pathogen. Previously, we have demonstrated that surfactant protein D (SP-D), a major humoral component in human lung-alveoli, recognizes A. fumigatus conidial surface exposed melanin pigment. Through binding to melanin, SP-D opsonizes conidia, facilitates conidial phagocytosis, and induces the expression of protective pro-inflammatory cytokines in the phagocytic cells. In addition to melanin, SP-D also interacts with galactomannan (GM) and galactosaminogalactan (GAG), the cell wall polysaccharides exposed on germinating conidial surfaces. Therefore, we aimed at unravelling the biological significance of SP-D during the germination process. Here, we demonstrate that SP-D exerts direct fungistatic activity by restricting A. fumigatus hyphal growth. Conidial germination in the presence of SP-D significantly increased the exposure of cell wall polysaccharides chitin, α-1,3-glucan and GAG, and decreased β-1,3-glucan exposure on hyphae, but that of GM was unaltered. Hyphae grown in presence of SP-D showed positive immunolabelling for SP-D. Additionally, SP-D treated hyphae induced lower levels of pro-inflammatory cytokine, but increased IL-10 (anti-inflammatory cytokine) and IL-8 (a chemokine) secretion by human peripheral blood mononuclear cells (PBMCs), compared to control hyphae. Moreover, germ tube surface modifications due to SP-D treatment resulted in an increased hyphal susceptibility to voriconazole, an antifungal drug. It appears that SP-D exerts its anti-A. fumigatus functions via a range of mechanisms including hyphal growth-restriction, hyphal surface modification, masking of hyphal surface polysaccharides and thus altering hyphal immunostimulatory properties.Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to Aspergillus fumigatus, an airborne fungal pathogen. Previously, we have demonstrated that surfactant protein D (SP-D), a major humoral component in human lung-alveoli, recognizes A. fumigatus conidial surface exposed melanin pigment. Through binding to melanin, SP-D opsonizes conidia, facilitates conidial phagocytosis, and induces the expression of protective pro-inflammatory cytokines in the phagocytic cells. In addition to melanin, SP-D also interacts with galactomannan (GM) and galactosaminogalactan (GAG), the cell wall polysaccharides exposed on germinating conidial surfaces. Therefore, we aimed at unravelling the biological significance of SP-D during the germination process. Here, we demonstrate that SP-D exerts direct fungistatic activity by restricting A. fumigatus hyphal growth. Conidial germination in the presence of SP-D significantly increased the exposure of cell wall polysaccharides chitin, α-1,3-glucan and GAG, and decreased β-1,3-glucan exposure on hyphae, but that of GM was unaltered. Hyphae grown in presence of SP-D showed positive immunolabelling for SP-D. Additionally, SP-D treated hyphae induced lower levels of pro-inflammatory cytokine, but increased IL-10 (anti-inflammatory cytokine) and IL-8 (a chemokine) secretion by human peripheral blood mononuclear cells (PBMCs), compared to control hyphae. Moreover, germ tube surface modifications due to SP-D treatment resulted in an increased hyphal susceptibility to voriconazole, an antifungal drug. It appears that SP-D exerts its anti-A. fumigatus functions via a range of mechanisms including hyphal growth-restriction, hyphal surface modification, masking of hyphal surface polysaccharides and thus altering hyphal immunostimulatory properties. •Surfactant protein D (SP-D), a C-type lectin and a major humoral immune component in the human lung-alveoli, shows direct growth inhibitory effect on Aspergillus fumigatus, an airborne opportunistic fungal pathogen.•SP-D treatment modifies the surface architecture and cell wall polysaccharide exposure on the A. fumigatus hyphae.•A. fumigatus hyphae grown in presence of SP-D stimulate significantly lower secretions of pro-inflammatory cytokine, but higher anti-inflammatory cytokine and chemokine secretions upon interaction with immune cells, compared to hyphae grown without SP-D.•Increased permeability of A. fumigatus hyphae upon SP-D treatment leads to a better efficacy of voriconazole, an antifungal drug that has its target in the fungal cytosol. Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to Aspergillus fumigatus, an airborne fungal pathogen. Previously, we have demonstrated that surfactant protein D (SP-D), a major humoral component in human lung-alveoli, recognizes A. fumigatus conidial surface exposed melanin pigment. Through binding to melanin, SP-D opsonizes conidia, facilitates conidial phagocytosis, and induces the expression of protective pro-inflammatory cytokines in the phagocytic cells. In addition to melanin, SP-D also interacts with galactomannan (GM) and galactosaminogalactan (GAG), the cell wall polysaccharides exposed on germinating conidial surfaces. Therefore, we aimed at unravelling the biological significance of SP-D during the germination process. Here, we demonstrate that SP-D exerts direct fungistatic activity by restricting A. fumigatus hyphal growth. Conidial germination in the presence of SP-D significantly increased the exposure of cell wall polysaccharides chitin, α-1,3-glucan and GAG, and decreased β-1,3-glucan exposure on hyphae, but that of GM was unaltered. Hyphae grown in presence of SP-D showed positive immunolabelling for SP-D. Additionally, SP-D treated hyphae induced lower levels of pro-inflammatory cytokine, but increased IL-10 (anti-inflammatory cytokine) and IL-8 (a chemokine) secretion by human peripheral blood mononuclear cells (PBMCs), compared to control hyphae. Moreover, germ tube surface modifications due to SP-D treatment resulted in an increased hyphal susceptibility to voriconazole, an antifungal drug. It appears that SP-D exerts its anti-A. fumigatus functions via a range of mechanisms including hyphal growth-restriction, hyphal surface modification, masking of hyphal surface polysaccharides and thus altering hyphal immunostimulatory properties. • Surfactant protein D (SP-D), a C -type lectin and a major humoral immune component in the human lung-alveoli, shows direct growth inhibitory effect on Aspergillus fumigatus , an airborne opportunistic fungal pathogen. • SP-D treatment modifies the surface architecture and cell wall polysaccharide exposure on the A. fumigatus hyphae. • A. fumigatus hyphae grown in presence of SP-D stimulate significantly lower secretions of pro-inflammatory cytokine, but higher anti-inflammatory cytokine and chemokine secretions upon interaction with immune cells, compared to hyphae grown without SP-D. • Increased permeability of A. fumigatus hyphae upon SP-D treatment leads to a better efficacy of voriconazole, an antifungal drug that has its target in the fungal cytosol. Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to Aspergillus fumigatus , an airborne fungal pathogen. Previously, we have demonstrated that surfactant protein D (SP-D), a major humoral component in human lung-alveoli, recognizes A. fumigatus conidial surface exposed melanin pigment. Through binding to melanin, SP-D opsonizes conidia, facilitates conidial phagocytosis, and induces the expression of protective pro-inflammatory cytokines in the phagocytic cells. In addition to melanin, SP-D also interacts with galactomannan (GM) and galactosaminogalactan (GAG), the cell wall polysaccharides exposed on germinating conidial surfaces. Therefore, we aimed at unravelling the biological significance of SP-D during the germination process. Here, we demonstrate that SP-D exerts direct fungistatic activity by restricting A. fumigatus hyphal growth. Conidial germination in the presence of SP-D significantly increased the exposure of cell wall polysaccharides chitin, α-1,3-glucan and GAG, and decreased β-1,3-glucan exposure on hyphae, but that of GM was unaltered. Hyphae grown in presence of SP-D showed positive immunolabelling for SP-D. Additionally, SP-D treated hyphae induced lower levels of pro-inflammatory cytokine, but increased IL-10 (anti-inflammatory cytokine) and IL-8 (a chemokine) secretion by human peripheral blood mononuclear cells (PBMCs), compared to control hyphae. Moreover, germ tube surface modifications due to SP-D treatment resulted in an increased hyphal susceptibility to voriconazole, an antifungal drug. It appears that SP-D exerts its anti- A. fumigatus functions via a range of mechanisms including hyphal growth-restriction, hyphal surface modification, masking of hyphal surface polysaccharides and thus altering hyphal immunostimulatory properties. |
ArticleNumber | 100072 |
Author | Sorensen, Grith L. Wong, Sarah Sze Wah Kishore, Uday Bomme, Perrine Schlosser, Anders G. Aimanianda, Vishukumar Schiefermeier-Mach, Natalia Fontaine, Thierry Madan, Taruna Dellière, Sarah Perkhofer, Susanne Lechner, Lukas |
Author_xml | – sequence: 1 givenname: Sarah Sze Wah surname: Wong fullname: Wong, Sarah Sze Wah email: swong@pasteur.fr organization: Institut Pasteur, Université de Paris, CNRS, Unité de Mycologie Moléculaire, UMR2000, F-75015 Paris, France – sequence: 2 givenname: Sarah surname: Dellière fullname: Dellière, Sarah organization: Institut Pasteur, Université de Paris, CNRS, Unité de Mycologie Moléculaire, UMR2000, F-75015 Paris, France – sequence: 3 givenname: Natalia surname: Schiefermeier-Mach fullname: Schiefermeier-Mach, Natalia organization: Health University of Applied Sciences Tyrol/FH Gesundheit Tirol, Innrain 98, 6020 Innsbruck, Austria – sequence: 4 givenname: Lukas surname: Lechner fullname: Lechner, Lukas organization: Health University of Applied Sciences Tyrol/FH Gesundheit Tirol, Innrain 98, 6020 Innsbruck, Austria – sequence: 5 givenname: Susanne surname: Perkhofer fullname: Perkhofer, Susanne organization: Health University of Applied Sciences Tyrol/FH Gesundheit Tirol, Innrain 98, 6020 Innsbruck, Austria – sequence: 6 givenname: Perrine surname: Bomme fullname: Bomme, Perrine organization: Ultrastructural Bio Imaging Unit, C2RT, Institut Pasteur, Paris, France – sequence: 7 givenname: Thierry surname: Fontaine fullname: Fontaine, Thierry organization: Institut Pasteur, Université de Paris, INREA, USC2019, Unité Biologie et Pathogénicité Fongiques, F-75015 Paris, France – sequence: 8 givenname: Anders G. surname: Schlosser fullname: Schlosser, Anders G. organization: Department of Cancer and Inflammation Research, Institute of Molecular Medicine, University of Southern Denmark, Odense, Denmark – sequence: 9 givenname: Grith L. surname: Sorensen fullname: Sorensen, Grith L. organization: Department of Cancer and Inflammation Research, Institute of Molecular Medicine, University of Southern Denmark, Odense, Denmark – sequence: 10 givenname: Taruna surname: Madan fullname: Madan, Taruna organization: Department of Innate Immunity, ICMR-National Institute for Research in Reproductive and Child Health, Mumbai, India – sequence: 11 givenname: Uday surname: Kishore fullname: Kishore, Uday organization: Biosciences, College of Health, Medicine and Life Sciences, Brunel University London, Uxbridge, United Kingdom – sequence: 12 givenname: Vishukumar surname: Aimanianda fullname: Aimanianda, Vishukumar email: vkumar@pasteur.fr organization: Institut Pasteur, Université de Paris, CNRS, Unité de Mycologie Moléculaire, UMR2000, F-75015 Paris, France |
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Keywords | SP-D Polysaccharides IL Surfactant protein D GM Innate immunity GAG Aspergillus fumigatus PBMCs Pattern-recognition receptor Cell wall GAG:, Galactosaminogalactan GM:, Galactomannan PBMCs:, Peripheral blood mononuclear cells SP-D:, Surfactant protein-D IL:, Interleukin |
Language | English |
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Snippet | •Surfactant protein D (SP-D), a C-type lectin and a major humoral immune component in the human lung-alveoli, shows direct growth inhibitory effect on... Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to , an airborne fungal pathogen.... Humoral immunity plays a defensive role against invading microbes. However, it has been largely overlooked with respect to Aspergillus fumigatus, an airborne... • Surfactant protein D (SP-D), a C -type lectin and a major humoral immune component in the human lung-alveoli, shows direct growth inhibitory effect on... |
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SubjectTerms | Aspergillus fumigatus Cell wall Innate immunity Life Sciences Microbiology and Parasitology Mycology Pattern-recognition receptor Polysaccharides Surfactant protein D |
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Title | Surfactant protein D inhibits growth, alters cell surface polysaccharide exposure and immune activation potential of Aspergillus fumigatus |
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