Top

Published in:

01-04-2021 | Cytokines | Original Article

Native and IgE-primed rat peritoneal mast cells exert pro-inflammatory activity and migrate in response to yeast zymosan upon Dectin-1 engagement

Authors: Paulina Żelechowska, Ewa Brzezińska-Błaszczyk, Sylwia Różalska, Justyna Agier, Elżbieta Kozłowska

Published in: Immunologic Research | Issue 2/2021

Abstract

Mast cells (MCs) play an essential role in host defense, primarily because of their location, their ability to pathogen destruction via several mechanisms, and the pattern recognition receptors they express. Even though most data is available regarding MC activation by various bacteria- or virus-derived molecules, those cells’ activity in response to constituents associated with fungi is not recognized enough. Our research aimed to address whether Saccharomyces cerevisiae-derived zymosan, i.e., β-(1,3)-glucan containing mannan particles, impacts MC activity aspects. Overall, the obtained results indicate that zymosan has the potential to elicit a pro-inflammatory response of rat peritoneal MCs. For the first time ever, we provided evidence that zymosan induces fully mature MC migration, even in the absence of extracellular matrix (ECM) proteins. Moreover, the zymosan-induced migratory response of MCs is almost entirely a result of directional migration, i.e., chemotaxis. We found that zymosan stimulates MCs to degranulate and generate lipid mediators (cysLTs), cytokines (IFN-α, IFN-β, IFN-γ, GM-CSF, TNF), and chemokine (CCL2). Zymosan also upregulated mRNA transcripts for several cytokines/chemokines with pro-inflammatory/immunoregulatory activity. Moreover, we documented that zymosan activates MCs to produce reactive oxygen species (ROS). Lastly, we established that the zymosan-induced MC response is mediated through activation of the Dectin-1 receptor. In general, our results strongly support the notion that MCs contribute to innate antifungal immunity and bring us closer to elucidate their role in host-pathogenic fungi interactions. Besides, provided findings on IgE-sensitized MCs appear to indicate that exposure to fungal zymosan could affect the severity of IgE-dependent disorders, including allergic ones.

Krystel-Whittemore M, Dileepan KN, Wood JG. Mast cell: a multi-functional master cell. Front Immunol. 2016;6:620. https://doi.org/10.3389/fimmu.2015.00620.CrossRefPubMedPubMedCentral

Mukai K, Tsai M, Saito H, Galli SJ. Mast cells as sources of cytokines, chemokines, and growth factors. Immunol Rev. 2018;282:121–50. https://doi.org/10.1111/imr.12634.CrossRefPubMedPubMedCentral

Dudeck A, Köberle M, Goldmann O, Meyer N, Dudeck J, Lemmens S, et al. Mast cells as protectors of health. J Allergy Clin Immunol. 2019;144:S4–18. https://doi.org/10.1016/j.jaci.2018.10.054.CrossRefPubMed

Weller CL, Collington SJ, Williams T, Lamb JR. Mast cells in health and disease. Clin Sci (Lond). 2011;120:473–84. https://doi.org/10.1042/CS20100459.CrossRef

Olivera A, Beaven MA, Metcalfe DD. Mast cells signal their importance in health and disease. J Allergy Clin Immunol. 2018;142:381–93. https://doi.org/10.1016/j.jaci.2018.01.034.CrossRefPubMed

Pastwińska J, Agier J, Dastych J, Brzezińska-Błaszczyk E. Mast cells as the strength of the inflammatory process. Pol J Pathol. 2017;68:187–96. https://doi.org/10.5114/pjp.2017.71526.CrossRefPubMed

Cardamone C, Parente R, Feo GD, Triggiani M. Mast cells as effector cells of innate immunity and regulators of adaptive immunity. Immunol Lett. 2016;178:10–4. https://doi.org/10.1016/j.imlet.2016.07.003.CrossRefPubMed

Urb M, Sheppard DC. The role of mast cells in the defence against pathogens. PLoS Pathog. 2012;8:e1002619. https://doi.org/10.1371/journal.ppat.1002619.CrossRefPubMedPubMedCentral

Trivedi NH, Guentzel MN, Rodriguez AR, Yu JJ, Forsthuber TG, Arulanandam BP. Mast cells: multitalented facilitators of protection against bacterial pathogens. Expert Rev Clin Immunol. 2013;9:129–38. https://doi.org/10.1586/eci.12.95.CrossRefPubMedPubMedCentral

10.

Marshall JS, Portales-Cervantes L, Leong E. Mast cell responses to viruses and pathogen products. Int J Mol Sci. 2019;20:4241. https://doi.org/10.3390/ijms20174241.CrossRefPubMedCentral

11.

Abraham SN, St John AL. Mast cell-orchestrated immunity to pathogens. Nat Rev Immunol. 2010;10:440–52. https://doi.org/10.1038/nri2782.CrossRefPubMedPubMedCentral

12.

Möllerherm H, von Köckritz-Blickwede M, Branitzki-Heinemann K. Antimicrobial activity of mast cells: role and relevance of extracellular DNA traps. Front Immunol. 2016;7:265. https://doi.org/10.3389/fimmu.2016.00265.CrossRefPubMedPubMedCentral

13.

Agier J, Pastwińska J, Brzezińska-Błaszczyk E. An overview of mast cell pattern recognition receptors. Inflamm Res. 2018;67:737–46. https://doi.org/10.1007/s00011-018-1164-5.CrossRefPubMedPubMedCentral

14.

Sandig H, Bulfone-Paus S. TLR signaling in mast cells: common and unique features. Front Immunol. 2012;3:185. https://doi.org/10.3389/fimmu.2012.00185.CrossRefPubMedPubMedCentral

15.

Gow NAR, Latge JP, Munro CA. The fungal cell wall: structure, biosynthesis, and function. Microbiol Spectr. 2017;5:1. https://doi.org/10.1128/microbiolspec.FUNK-0035-2016.CrossRef

16.

Brown GD, Gordon S. Fungal β-glucans and mammalian immunity. Immunity. 2003;19:311–5. https://doi.org/10.1016/s1074-7613(03)00233-4.CrossRefPubMed

17.

Camilli G, Tabouret G, Quintin J. The complexity of fungal β-glucan in health and disease: effects on the mononuclear phagocyte system. Front Immunol. 2018;9:673. https://doi.org/10.3389/fimmu.2018.00673.CrossRefPubMedPubMedCentral

18.

Kozłowska E, Brzezińska-Błaszczyk E, Rasmus P, Żelechowska P. Fungal β-glucans and mannan stimulate peripheral blood mononuclear cells to cytokine production in Syk-dependent manner. Immunobiology. 2020;225:151985. https://doi.org/10.1016/j.imbio.2020.151985.CrossRefPubMed

19.

McCurdy JD, Olynych TJ, Maher LH, Marshall JS. Cutting edge: distinct Toll-like receptor 2 activators selectively induce different classes of mediator production from human mast cells. J Immunol. 2003;170:1625–9. https://doi.org/10.4049/jimmunol.170.4.1625.CrossRefPubMed

20.

Olynych TJ, Jakeman DL, Marshall JS. Fungal zymosan induces leukotriene production by human mast cells through a dectin-1-dependent mechanism. J Allergy Clin Immunol. 2006;118:837–43. https://doi.org/10.1016/j.jaci.2006.06.008.CrossRefPubMed

21.

Yang Z, Marshall JS. Zymosan treatment of mouse mast cells enhances dectin-1 expression and induces dectin-1-dependent reactive oxygen species (ROS) generation. Immunobiology. 2009;214:321–30. https://doi.org/10.1016/j.imbio.2008.09.002.CrossRefPubMed

22.

Pinke KH, Lima HG, Cunha FQ, Lara VS. Mast cells phagocyte Candida albicans and produce nitric oxide by mechanisms involving TLR2 and Dectin-1. Immunobiology. 2016;221:220–7. https://doi.org/10.1016/j.imbio.2015.09.004.CrossRefPubMed

23.

Horsfield GI. The effect of compound 48/80 on the rat mast cell. J Pathol Bacteriol. 1965;90:599–605. https://doi.org/10.1002/path.1700900228.CrossRefPubMed

24.

Penzo D, Petronilli V, Angelin A, Cusan C, Colonna R, Scorrano L, et al. Arachidonic acid released by phospholipase A₂ activation triggers Ca²⁺-dependent apoptosis through the mitochondrial pathway. J Biol Chem. 2004;279:25219–25. https://doi.org/10.1074/jbc.M310381200.CrossRefPubMed

25.

Gao D, Li W. Structures and recognition modes of toll-like receptors. Proteins. 2017;85:3–9. https://doi.org/10.1002/prot.25179.CrossRefPubMed

26.

Żelechowska P, Różalska S, Wiktorska M, Brzezińska-Błaszczyk E, Agier J. Curdlan stimulates tissue mast cells to synthesize proinflammatory mediators, generate ROS, and migrate via Dectin-1 receptor. Cell Immunol. 2020;351:104079. https://doi.org/10.1016/j.cellimm.2020.104079.CrossRefPubMed

27.

Wierzbicki M, Brzezińska-Błaszczyk E. Diverse effects of bacterial cell wall components on mast cell degranulation, cysteinyl leukotriene generation and migration. Microbiol Immunol. 2009;53:694–703. https://doi.org/10.1111/j.1348-0421.2009.00174.x.CrossRefPubMed

28.

Chan CY, St John AL, Abraham SN. Plasticity in mast cell responses during bacterial infections. Curr Opin Microbiol. 2012;15:78–84. https://doi.org/10.1016/j.mib.2011.10.007.CrossRefPubMed

29.

Graham AC, Temple RM, Obar JJ. Mast cells and influenza a virus: association with allergic responses and beyond. Front Immunol. 2015;26:238. https://doi.org/10.3389/fimmu.2015.00238.CrossRef

30.

Makni-Maalej K, Chiandotto M, Hurtado-Nedelec M, Bedouhene S, Gougerot-Pocidalo MA, Dang PM, et al. Zymosan induces NADPH oxidase activation in human neutrophils by inducing the phosphorylation of p47phox and the activation of Rac2: involvement of protein tyrosine kinases, PI3Kinase, PKC, ERK1/2 and p38MAPkinase. Biochem Pharmacol. 2013;85:92–100. https://doi.org/10.1016/j.bcp.2012.10.010.CrossRefPubMed

31.

Peters-Golden M, Canetti C, Mancuso P, Coffey MJ. Leukotrienes: underappreciated mediators of innate immune responses. J Immunol. 2005;174:589–94. https://doi.org/10.4049/jimmunol.174.2.589.CrossRefPubMed

32.

Branco ACCC, Yoshikawa FSY, Pietrobon AJ, Sato MN. Role of histamine in modulating the immune response and inflammation. Mediat Inflamm. 2018;9524075:1–10. https://doi.org/10.1155/2018/9524075.CrossRef

33.

Honda K, Takaoka A, Taniguchi T. Type I Interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity. 2006;25:349–60. https://doi.org/10.1016/j.immuni.2006.08.009.CrossRefPubMed

34.

Antachopoulos C, Roilides E. Cytokines and fungal infections. Br J Haematol. 2005;129:583–96. https://doi.org/10.1111/j.1365-2141.2005.05498.x.CrossRefPubMed

35.

Pathakumari B, Liang G, Liu W. Immune defence to invasive fungal infections: a comprehensive review. Biomed Pharmacother. 2020;130:110550. https://doi.org/10.1016/j.biopha.2020.110550.CrossRefPubMed

36.

Vautier S, Sousa Mda G, Brown GD. C-type lectins, fungi and Th17 responses. Cytokine Growth Factor Rev. 2010;21:405–12. https://doi.org/10.1016/j.cytogfr.2010.10.001.CrossRefPubMedPubMedCentral

37.

Zelante T, De Luca A, D'Angelo C, Moretti S, Romani L. IL-17/Th17 in anti-fungal immunity: what’s new? Eur J Immunol. 2009;39:645–8. https://doi.org/10.1002/eji.200839102.CrossRefPubMed

38.

Tristão FSM, Rocha FA, Carlos D, Ketelut-Carneiro N, Souza COS, Milanezi CM, et al. Th17-inducing cytokines IL-6 and IL-23 are crucial for granuloma formation during experimental paracoccidioidomycosis. Front Immunol. 2017;8:949. https://doi.org/10.3389/fimmu.2017.00949.CrossRefPubMedPubMedCentral

39.

Zelante T, De Luca A, Bonifazi P, Montagnoli C, Bozza S, Moretti S, et al. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol. 2007;37:2695–706. https://doi.org/10.1002/eji.200737409.CrossRefPubMed

40.

Lee W, Su Kim H, Lee GR. Leukotrienes induce the migration of Th17 cells. Immunol Cell Biol. 2015;93:472–9. https://doi.org/10.1038/icb.2014.104.CrossRefPubMed

41.

Wang A, Wang Z, Cao Y, Cheng S, Chen H, Bunjhoo H, et al. CCL2/CCR2-dependent recruitment of Th17 cells but not Tc17 cells to the lung in a murine asthma model. Int Arch Allergy Immunol. 2015;166:52–62. https://doi.org/10.1159/000371764.CrossRefPubMed

42.

Mommert S, Gschwandtner M, Koether B, Gutzmer R, Werfel T. Human memory Th17 cells express a functional histamine H4 receptor. Am J Pathol. 2012;180:177–85. https://doi.org/10.1016/j.ajpath.2011.09.028.CrossRefPubMed

43.

Sparber F, LeibundGut-Landmann S. Interleukin-17 in antifungal immunity. Pathogens. 2019;8:54. https://doi.org/10.3390/pathogens8020054.CrossRefPubMedCentral

44.

To EE, O'Leary JJ, O'Neill LAJ, Vlahos R, Bozinovski S, Porter CJH, et al. Spatial properties of reactive oxygen species govern pathogen-specific immune system responses. Antioxid Redox Signal. 2020;32:982–92. https://doi.org/10.1089/ars.2020.8027.CrossRefPubMedPubMedCentral

45.

Yang Y, Bazhin AV, Werner J, Karakhanova S. Reactive oxygen species in the immune system. Int Rev Immunol. 2013;32:249–70. https://doi.org/10.3109/08830185.2012.755176.CrossRefPubMed

46.

Drummond RA, Brown GD. The role of Dectin-1 in the host defence against fungal infections. Curr Opin Microbiol. 2011;14:392–9. https://doi.org/10.1016/j.mib.2011.07.001.CrossRefPubMed

47.

Schorey JS, Lawrence C. The pattern recognition receptor Dectin-1: from fungi to mycobacteria. Curr Drug Targets. 2008;9:123–9. https://doi.org/10.2174/138945008783502430.CrossRefPubMedPubMedCentral

48.

Joo H, Upchurch K, Zhang W, Ni L, Li D, Xue Y, et al. Opposing roles of Dectin-1 expressed on human plasmacytoid dendritic cells and myeloid dendritic cells in Th2 polarization. J Immunol. 2015;195:1723–31. https://doi.org/10.4049/jimmunol.1402276.CrossRefPubMedPubMedCentral

49.

Lundberg K, Rydnert F, Broos S, Andersson M, Greiff L, Lindstedt M. C-type lectin receptor expression on human basophils and effects of allergen-specific immunotherapy. Scand J Immunol. 2016;84:150–7. https://doi.org/10.1111/sji.12457.CrossRefPubMed

50.

Kimura Y, Chihara K, Honjoh C, Takeuchi K, Yamauchi S, Yoshiki H, et al. Dectin-1-mediated signaling leads to characteristic gene expressions and cytokine secretion via spleen tyrosine kinase (Syk) in rat mast cells. J Biol Chem. 2014;289:31565–75. https://doi.org/10.1074/jbc.M114.581322.CrossRefPubMedPubMedCentral

51.

Ribbing C, Engblom C, Lappalainen J, Lindstedt K, Kovanen PT, Karlsson MA, et al. Mast cells generated from patients with atopic eczema have enhanced levels of granule mediators and an impaired Dectin-1 expression. Allergy. 2011;66:110–9. https://doi.org/10.1111/j.1398-9995.2010.02437.x.CrossRefPubMed

52.

Dillon S, Agrawal S, Banerjee K, Letterio J, Denning TL, Oswald-Richter K, et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Invest. 2006;116:916–28. https://doi.org/10.1172/JCI27203.CrossRefPubMedPubMedCentral

53.

Kerrigan AM, Brown GD. Syk-coupled C-type lectins in immunity. Trends Immunol. 2011;32:151–6. https://doi.org/10.1016/j.it.2011.01.002.CrossRefPubMedPubMedCentral

54.

Kashiwakura J, Otani IM, Kawakami T. Monomeric IgE and mast cell development, survival and function. Adv Exp Med Biol. 2011;716:29–46. https://doi.org/10.1007/978-1-4419-9533-9_3.CrossRefPubMed

55.

Yamada N, Matsushima H, Tagaya Y, Shimada S, Katz SI. Generation of a large number of connective tissue type mast cells by culture of murine fetal skin cells. J Invest Dermatol. 2003;121:1425–32. https://doi.org/10.1046/j.1523-1747.2003.12613.x.CrossRefPubMed

56.

Słodka A, Wiktorska M, Brzezińska-Błaszczyk E. IgE by itself affects mature rat mast cell preformed and de novo-synthesized mediator release and amplifies mast cell migratory response. PLoS One. 2013;8:e79286. https://doi.org/10.1371/journal.pone.0079286.CrossRefPubMedPubMedCentral

57.

Selander C, Engblom C, Nilsson G, Scheynius A, Andersson CL. TLR2/MyD88-dependent and -independent activation of mast cell IgE responses by the skin commensal yeast Malassezia sympodialis. J Immunol. 2009;182:4208–16. https://doi.org/10.4049/jimmunol.0800885.CrossRefPubMed

58.

Żelechowska P, Brzezińska-Błaszczyk E, Różalska S, Agier J, Kozłowska E. Mannan activates tissue native and IgE-sensitized mast cells to proinflammatory response and chemotaxis in TLR4-dependent manner. J Leukoc Biol. 2020. https://doi.org/10.1002/JLB.4A0720-452R.

59.

Armann J, von Mutius E. Do bacteria have a role in asthma development? Eur Respir J. 2010;3:469–71. https://doi.org/10.1183/09031936.00041410.CrossRef

60.

Edwards MR, Strong K, Cameron A, Walton RP, Jackson DJ, Johnston SL. Viral infections in allergy and immunology: how allergic inflammation influences viral infections and illness. J Allergy Clin Immunol. 2017;140:909–20. https://doi.org/10.1016/j.jaci.2017.07.025.CrossRefPubMedPubMedCentral

61.

Sakurai A, Yamaguchi N, Sonoyama K. Cell wall polysaccharides of Candida albicans induce mast cell degranulation in the gut. Biosci Microbiota Food Health. 2012;31:67–70. https://doi.org/10.12938/bmfh.31.67.CrossRefPubMedPubMedCentral

62.

Sato H, Kobayashi Y, Hattori A, Suzuki T, Shigekawa M, Jippo T. Inhibitory effects of water-soluble low-molecular-weight β-(1,3-1,6) D-glucan isolated from Aureobasidium pullulans 1A1 strain black yeast on mast cell degranulation and passive cutaneous anaphylaxis. Biosci Biotechnol Biochem. 2012;76:84–8. https://doi.org/10.1271/bbb.110536.CrossRefPubMed

Title: Native and IgE-primed rat peritoneal mast cells exert pro-inflammatory activity and migrate in response to yeast zymosan upon Dectin-1 engagement
Authors: Paulina Żelechowska
Ewa Brzezińska-Błaszczyk
Sylwia Różalska
Justyna Agier
Elżbieta Kozłowska
Publication date: 01-04-2021
Publisher: Springer US
Keyword: Cytokines
Published in: Immunologic Research / Issue 2/2021
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI: https://doi.org/10.1007/s12026-021-09183-7

At a glance: The STEP trials

Springer Medicine

Native and IgE-primed rat peritoneal mast cells exert pro-inflammatory activity and migrate in response to yeast zymosan upon Dectin-1 engagement

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2021

Association of interleukin-12B rs6887695 with susceptibility to allergic rhinitis

MyD88 and beyond: a perspective on MyD88-targeted therapeutic approach for modulation of host immunity

Iodoprophylaxis and thyroid autoimmunity: an update

Correction to: Postural orthostatic tachycardia syndrome (POTS) and other autonomic disorders after COVID-19 infection: a case series of 20 patients

Postural orthostatic tachycardia syndrome (POTS) and other autonomic disorders after COVID-19 infection: a case series of 20 patients

Potential role of viral infection and B cells as a linker between innate and adaptive immune response in systemic lupus erythematosus