Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Inflammation
Published in: Inflammation 6/2014

01-12-2014

Mast Cells Kill Candida albicans in the Extracellular Environment but Spare Ingested Fungi from Death

Authors: Elisa Trevisan, Francesca Vita, Nevenka Medic, Maria Rosa Soranzo, Giuliano Zabucchi, Violetta Borelli

Published in: Inflammation | Issue 6/2014

Login to get access

Abstract

Mast cells (MCs) reside in tissues that are common targets of Candida spp. infections, and can exert bactericidal activity, but little is known about their fungicidal activity. MCs purified from rat peritoneum (RPMC) and a clinical isolate of C. albicans, were employed. Ingestion was evaluated by flow cytometry (FACS) and optical microscopy. The killing activity was assayed by FACS analysis and by colony forming unit method. RPMC degranulation was evaluated by β-hexosaminidase assay and phosphatidylserine externalization by FACS. Phagocytosing RPMC were also analyzed by transmission electron microscopy. Herein, we show that the killing of C. albicans by RPMC takes place in the extracellular environment, very likely through secreted granular components. Ultrastructural analysis of the ingestion process revealed an unusual RPMC–C. albicans interaction that could allow fungal survival. Our findings indicate that MCs have a positive role in the defense mechanism against Candida infections and should be included among the cell types involved in host-defense against this pathogen.
Literature
1.
Brown, G.D., and M.G. Netea. 2007. Immunology of fungal infections. Dordrecht: Springer.CrossRef
2.
Smeekens, S.P., F.L. van de Veerdonk, B.J. Kullberg, and M.G. Netea. 2013. Genetic susceptibility to Candida infections. EMBO Molecular Medicine 5(6): 805–813.PubMedCentralPubMedCrossRef
3.
Gow, N.A., F.L. van de Veerdonk, A.J. Brown, and M.G. Netea. 2011. Candida albicans morphogenesis and host defence: Discriminating invasion from colonization. Nature Reviews Microbiology 10: 112–122.PubMedCentralPubMed
4.
Cheng, S.C., L.A. Joosten, B.J. Kullberg, and M.G. Netea. 2012. Interplay between Candida albicans and the mammalian innate host defense. Infection and Immunity 80(4): 1304–1313.PubMedCentralPubMedCrossRef
5.
Miramón, P., L. Kasper, and B. Hube. 2013. Thriving within the host: Candida spp. interactions with phagocytic cells. Medical Microbiology and Immunology 202: 183–195.PubMedCrossRef
6.
Kullberg, B.J., M.G. Netea, A.G. Vonk, and J.W. van der Meer. 1999. Modulation of neutrophil function in host defense against disseminated Candida albicans infection in mice. Immunology and Medical Microbiology 26: 299–307.PubMedCrossRef
7.
Fernández-Arenas, E., C.K. Bleck, C. Nombela, C. Gil, G. Griffiths, and R. Diez-Orejas. 2009. Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cellular Microbiology 11: 560–589.PubMedCrossRef
8.
Saluja, R., M. Metz, and M. Maurer. 2012. Role and relevance of mast cells in fungal infections. Frontiers in Immunology 3: 1–11.CrossRef
9.
10.
Frossi, B., M. De Carli, and C. Pucillo. 2004. The mast cell: An antenna of the microenvironment that directs the immune response. Journal of Leukocyte Biology 75: 579–585.PubMedCrossRef
11.
Hofmann, A.M., and S.N. Abraham. 2009. New roles for MC in modulating allergic reaction and immunity against pathogens. Current Opinion in Immunology 21: 679–686.PubMedCentralPubMedCrossRef
12.
St John, A.L., and S.N. Abraham. 2013. Innate immunity and its regulation by mast cells. Journal of Immunology 190: 4458–4463.CrossRef
13.
Féger, F., S. Varadaradjalou, Z. Gao, S.N. Abraham, and M. Arock. 2002. The role of mast cells in host defense and their subversion by bacterial pathogens. Trends in Immunology 23: 151–158.PubMedCrossRef
14.
Gekara, N.O., and S. Weiss. 2008. Mast cells initiate early anti-Listeria host defences. Cellular Microbiology 10: 225–236.PubMed
15.
Malaviya, R., N.J. Twesten, E.A. Ross, S.N. Abraham, and J.D. Pfeifer. 1996. Mast cells process bacterial Ags through a phagocytic route for class I MHC presentation to T cells. Journal of Immunology 156: 1490–1496.
16.
Suurmond, J., J. van Heemst, J. van Heiningen, A.L. Dorjée, M.W. Schilham, F.B. van der Beek, T.W. Huizinga, and A.J.R.E. Schuerwegh Toes. 2013. Communication between human mast cells and CD4(+) T cells through antigen-dependent interactions. European Journal of Immunology 43: 1758–1768.PubMedCrossRef
17.
Di Nardo, A., A. Vitiello, and R.L. Gallo. 2003. Cutting edge: Mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. Journal of Immunology 170: 2274–2278.CrossRef
18.
Den Hertog, A.L., J. van Marle, H.A. van Veen, W. Van't Hof, J.G. Bolscher, E.C. Veerman, and A.V. Nieuw Amerongen. 2005. Candidacidal effects of two antimicrobial peptides: Histatin 5 causes small membrane defects, but LL-37 causes massive disruption of the cell membrane. The Biochemical Journal 1: 689–695.
19.
Den Hertog, A.L., J. Van Marle, H.A. Van Veen, W. Van't Hof, J.G. Bolscher, E.C. Veerman, A.V. Nieuw Amerongen, P.W. Tsai, C.Y. Yang, H.T. Chang, and C.Y. Lan. 2011. Human antimicrobial peptide LL-37 inhibits adhesion of Candida albicans by interacting with yeast cell-wall carbohydrates. PloS One 14: e17755.
20.
von Köckritz-Blickwede, M., O. Goldmann, P. Thulin, K. Heinemann, A. Norrby-Teglund, M. Rohde, and E. Medina. 2008. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111: 3070–3080.CrossRef
21.
Malaviya, R., E.A. Ross, J.I. MacGregor, T. Ikeda, J.R. Little, B.A. Jakschik, and S.N. Abraham. 1994. Mast cell phagocytosis of FimH-expressing enterobacteria. Journal of Immunology 15(152): 1907–1914.
22.
Arock, M., E. Ross, R. Lai-Kuen, G. Averlant, Z. Gao, and S.N. Abraham. 1998. Phagocytic and tumor necrosis factor alpha response of human mast cells following exposure to gram-negative and gram-positive bacteria. Infection and Immunity 66: 6030–6034.PubMedCentralPubMed
23.
Wei, O.L., A. Hilliard, D. Kalman, and M. Sherman. 2005. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infection and Immunity 73: 1978–1985.PubMedCentralPubMedCrossRef
24.
Padawer, J., and G.J. Fruhman. 1968. Phagocytosis of zymosan particles by mast cells. Experientia 15(24): 471–472.CrossRef
25.
Padawer, J. 1971. Poxvirus phagocytosis in vivo: Electron microscopy of macrophages, mast cells, and leukocytes. Journal of the Reticuloendothelial Society 9: 23–41.PubMed
26.
Fruhman, G.J. 1973. In vitro ingestion of zymosan particles by mast cells. Journal of the Reticuloendothelial Society 13: 424–435.PubMed
27.
Malaviya, R., T. Ikeda, E.A. Ross, B.A. Jakschik, and S.N. Abraham. 1995. Bacteria–mast cell interactions in inflammatory disease. American Journal of Therapy 2: 787–792.CrossRef
28.
Sher, A., A. Hein, G. Moser, and J.P. Caulfield. 1979. Complement receptors promote the phagocytosis of bacteria by rat peritoneal mast cell. Laboratory Investigation 41: 490–499.PubMed
29.
Katz, H.R., M.B. Raizman, C.S. Gartner, H.C. Scott, A.C. Benson, and K.F. Austen. 1992. Secretory granule mediator release and generation of oxidative metabolites of arachidonic acid via Fc-IgG receptor bridging in mouse mast cells. Journal of Immunology 148: 868–871.
30.
Otani, I., D.H. Conrad, J.R. Carlo, D.M. Segal, and S. Ruddy. 1982. Phagocytosis by rat peritoneal mast cells: Independence of IgG Fc-mediated and C3-mediated signals. Journal of Immunology 129: 2109–2112.
31.
Baorto, D.M., Z. Gao, R. Malaviya, M.L. Dustin, A. van der Merwe, D.M. Lublin, and S.N. Abraham. 1997. Survival of FimH-expressing enterobacteria in macrophages relies on glycolipid traffic. Nature 389: 636–639.PubMedCrossRef
32.
Shin, J.S., Z. Gao, and S.N. Abraham. 1999. Bacteria–host cell interaction mediated by cellular cholesterol/glycolipid-enriched microdomains. Bioscience Reports 19: 421–432.PubMedCrossRef
33.
Shin, J.S., Z. Gao, and S.N. Abraham. 2000. Involvement of cellular caveolae in bacterial entry into mast cells. Science 289: 785–788.PubMedCrossRef
34.
Rosenkranz, A.R., A. Coxon, M. Maurer, M.F. Gurish, K.F. Austen, D.S. Friend, S.J. Galli, and T.N. Mayadas. 1998. Impaired mast cell development and innate immunity in Mac-1 (CD11b/CD18, CR3)-deficient mice. Journal of Immunology 15(161): 6463–6467.
35.
Olynych, T.J., D.L. Jakeman, and J.S. Marshall. 2006. Fungal zymosan induces leukotriene production by human mast cells through a dectin-1-dependent mechanism. The Journal of Allergy and Clinical Immunology 118: 837–843.PubMedCrossRef
36.
Malbec, O., and M. Daeron. 2007. The mast cells IgG receptors and their role in tissue inflammation. Immunological Reviews 217: 206–221.PubMedCrossRef
37.
38.
Suzuki, Y., T. Inoue, T. Yoshimaru, and C. Ra. 2008. Galectin-3 but not galectin-1 induces mast cell death by oxidative stress and mitochondrial permeability transition. Biochimica et Biophysica Acta 1783: 924–934.PubMedCrossRef
39.
Netea, M.G., and L. Maródi. 2010. Innate immune mechanisms for recognition and uptake of Candida species. Trends in Immunology 31: 346–353.PubMedCrossRef
40.
Pietrzak, A., M. Wierzbicki, M. Wiktorska, and E. Brzezińska-Błaszczyk. 2011. Surface TLR2 and TLR4 expression on mature rat mast cells can be affected by some bacterial components and proinflammatory cytokines. Mediators of Inflammation 2: 1–11.CrossRef
41.
Nosál, R. 1974. Histamine release from isolated rat mast cells due to glycoprotein from Candida albicans in vitro. Journal of Hygiene, Epidemiology, Microbiology, and Immunology 18(3): 377–378.PubMed
42.
Yamaguchi, N., R. Sugita, A. Miki, N. Takemura, J. Kawabata, J. Watanabe, and K. Sonoyama. 2006. Gastrointestinal Candida colonisation promotes sensitisation against food antigens by affecting the mucosal barrier in mice. Gut 55: 954–960.PubMedCentralPubMedCrossRef
43.
Medic, N., F. Vita, R. Abbate, M.R. Soranzo, S. Pacor, E. Fabbretti, V. Borelli, and G. Zabucchi. 2008. Mast cell activation by myelin through scavenger receptor. Journal of Neuroimmunology 200: 27–40.PubMedCrossRef
44.
Busetto, S., E. Trevisan, P. Patriarca, and R. Menegazzi. 2004. A single-step, sensitive flow cytofluorometric assay for the simultaneous assessment of membrane-bound and ingested Candida albicans in phagocytosing neutrophils. Cytometry 58: 201–206.PubMedCrossRef
45.
Borelli, V., F. Vita, M.R. Soranzo, E. Banfi, and G. Zabucchi. 2002. Ultrastructure of the interaction between Mycobacterium tuberculosis-H37Rv-containing phagosomes and the lysosomal compartment in human alveolar macrophages. Experimental and Molecular Pathology 73: 128–134.PubMedCrossRef
46.
Dri, P., M.R. Soranzo, R. Cramer, R. Menegazzi, V. Miotti, and P. Patriarca. 1985. Role of myeloperoxidase in respiratory burst of human polymorphonuclear leukocytes. Studies with myeloperoxidase-deficient subjects. Inflammation 9: 21–31.PubMedCrossRef
47.
Bjerknes, R. 1984. Flow cytometric assay for combined measurement of phagocytosis and intracellular killing of Candida albicans. Journal of Immunological Methods 72: 229–241.PubMedCrossRef
48.
Decleva, E., R. Menegazzi, S. Busetto, P. Patriarca, and P. Dri. 2006. Common methodology is inadequate for studies on the microbicidal activity of neutrophils. Journal of Leukocyte Biology 79: 87–94.PubMedCrossRef
49.
Menegazzi, R., R. Cramer, P. Patriarca, P. Scheurich, and P. Dri. 1994. Evidence that tumor necrosis factor alpha (TNF)-induced activation of neutrophil respiratory burst on biologic surfaces is mediated by the p55 TNF receptor. Blood 84: 287–293.PubMed
50.
Martin, S., I. Pombo, P. Poncet, B. David, M. Arock, and U. Blank. 2000. Immunologic stimulation of mast cells leads to the reversible exposure of phosphatidylserine in the absence of apoptosis. International Archives of Allergy and Immunology 123: 249–258.PubMedCrossRef
51.
Saresella, M., K. Roda, L. Speciale, D. Taramelli, E. Mendozzi, F. Guerini, and P. Ferrante. 1997. A rapid evaluation of phagocytosis and killing of Candida albicans by CD13+ leukocytes. Journal of Immunological Methods 210(2): 227–234.PubMedCrossRef
52.
Blank, U. 2011. The mechanisms of exocytosis in mast cells. Advances in Experimental Medicine and Biology 716: 107–122.PubMedCrossRef
53.
Swindle, E.J., and D.D. Metcalfe. 2007. The role of reactive oxygen species and nitric oxide in mast cell dependent inflammatory processes. Immunological Reviews 217: 186–205.PubMedCrossRef
54.
Marquis, G., S. Garzon, S. Montplaisir, H. Strykowski, and N. Benhamou. 1991. Histochemical and immunochemical study of the fate of Candida albicans inside human neutrophil phagolysosomes. Journal of Leukocyte Biology 50(6): 587–599.PubMed
55.
Busetto, S., E. Trevisan, E. Decleva, P. Dri, and R. Menegazzi. 2007. Chloride movements in human neutrophils during phagocytosis: Characterization and relationship to granule release. Journal of Immunology 15(179): 4110–4124.CrossRef
56.
Abel, J., O. Goldmann, C. Ziegler, C. Höltje, M.S. Smeltzer, A.L. Cheung, D. Bruhn, M. Rohde, and E. Medina. 2011. Staphylococcus aureus evades the extracellular antimicrobial activity of mast cells by promoting its own uptake. Journal of Innate Immunity 3: 495–507.PubMedCrossRef
Metadata
Title
Mast Cells Kill Candida albicans in the Extracellular Environment but Spare Ingested Fungi from Death
Authors
Elisa Trevisan
Francesca Vita
Nevenka Medic
Maria Rosa Soranzo
Giuliano Zabucchi
Violetta Borelli
Publication date
01-12-2014
Publisher
Springer US
Published in
Inflammation / Issue 6/2014
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-014-9951-9

Other articles of this Issue 6/2014

Inflammation 6/2014 Go to the issue

OriginalPaper

Preventive Effect of Chrysin on Bleomycin-Induced Lung Fibrosis in Rats

OriginalPaper

Tetrahydrocoptisine Protects Rats from LPS-Induced Acute Lung Injury

OriginalPaper

Inhibition of Macrophage Migration Inhibitory Factor Reduces Diabetic Nephropathy in Type II Diabetes Mice

OriginalPaper

Development of Asthmatic Response upon Bronchial Allergen Challenge Is Associated with Dynamic Changes of Interleukin-10-Producing and Interleukin-10-Responding CD4+ T Cells

OriginalPaper

Protein Malnutrition Alters Spleen Cell Proliferation and IL-2 and IL-10 Production by Affecting the STAT-1 and STAT-3 Balance

OriginalPaper

Dual Effects of Respiratory Syncytial Virus Infections on Airway Inflammation by Regulation of Th17/Treg Responses in Ovalbumin-Challenged Mice
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits