Effect of Fonsecaea monophora on the Polarization of THP-1 Cells to Macrophages

Abstract

Background

Chromoblastomycosis is a chronic, progressive fungal disease of the skin and subcutaneous tissue caused by a unique group of dematiaceous fungi. Fonsecaea monophora, a new species distinct from Fonsecaea pedrosoi strains, is the main pathogen responsible for chromoblastomycosis in south China. Macrophages can be polarized into two categories: classically activated and alternatively activated.

Objectives

Little is known about the relationship between F. monophora and macrophage polarization. This study aimed to study the effect of F. monophora on the polarization of THP-1 cells to macrophages.

Methods

We established coculture systems of F. monophora and THP-1-derived macrophages in different activation states.

Results

F. monophora enhanced the phagocytosis by macrophages in the initially activated state and weakened the phagocytosis by classically activated macrophages without affecting that by alternatively activated macrophages. Classically activated macrophages had the strongest killing effect on F. monophora, while the initially activated macrophages had the weakest. The pathogen could not be rapidly cleared by any type of macrophage. F. monophora promoted the expression of proinflammatory cytokines and inhibited that of anti-inflammatory cytokines.

Conclusions

F. monophora promoted the polarization of THP-1 cells to classically activated macrophages and inhibited that of THP-1 cells to alternatively activated macrophages.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Queiroz-Telles F, de Hoog S, Santos DW, et al. Chromoblastomycosis. Clin Microbiol Rev. 2017;30:233–76.

    CAS  Article  Google Scholar 

  2. 2.

    Lu S, Lu C, Zhang J, Hu Y, Li X, Xi L. Chromoblastomycosis in Mainland China: a systematic review on clinical characteristics. Mycopathologia. 2013;175:489–95.

    Article  Google Scholar 

  3. 3.

    Liu ZH, Xia XJ. Successful sequential treatment with itraconazole and ALA-PDT for chromoblastomycosis because of Alternaria alternata. Dermatol Ther. 2014;27:357–60.

    Article  Google Scholar 

  4. 4.

    de Sousa MG, Belda WJ, Spina R, et al. Topical application of imiquimod as a treatment for chromoblastomycosis. Clin Infect Dis. 2014;58:1734–7.

    Article  Google Scholar 

  5. 5.

    Zhang J, Xi L, Lu C, et al. Successful treatment for chromoblastomycosis caused by Fonsecaea monophora: a report of three cases in Guangdong, China. Mycoses. 2009;52:176–81.

    Article  Google Scholar 

  6. 6.

    Bonifaz A, Davoudi MM, de Hoog GS, et al. Severe disseminated phaeohyphomycosis in an immunocompetent patient caused by Veronaea botryosa. Mycopathologia. 2013;175:497–503.

    Article  Google Scholar 

  7. 7.

    Queiroz-Telles F, Esterre P, Perez-Blanco M, Vitale RG, Salgado CG, Bonifaz A. Chromoblastomycosis: an overview of clinical manifestations, diagnosis and treatment. Med Mycol. 2009;47:3–15.

    Article  Google Scholar 

  8. 8.

    Jiang M, Cai W, Zhang J, et al. Melanization of a meristematic mutant of Fonsecaea monophora increase the pathogenesis in a BALB/c mice infection model. Med Mycol. 2018;56:979–86.

    CAS  PubMed  Google Scholar 

  9. 9.

    De Guzman L, Perlman DC, Hubbard CE. Septic arthritis and osteomyelitis due to the chromoblastomycosis agent Fonsecaea pedrosoi. Am J Orthop (Belle Mead NJ). 2012;41:328–31.

    Google Scholar 

  10. 10.

    Kondo M, Hiruma M, Nishioka Y, et al. A case of chromomycosis caused by Fonsecaea pedrosoi and a review of reported cases of dematiaceous fungal infection in Japan. Mycoses. 2005;48:221–5.

    CAS  Article  Google Scholar 

  11. 11.

    Queiroz-Telles F, Santos DW. Challenges in the therapy of chromoblastomycosis. Mycopathologia. 2013;175:477–88.

    Article  Google Scholar 

  12. 12.

    Ameen M. Chromoblastomycosis: clinical presentation and management. Clin Exp Dermatol. 2009;34:849–54.

    CAS  Article  Google Scholar 

  13. 13.

    Xi L, Lu C, Sun J, et al. Chromoblastomycosis caused by a meristematic mutant of Fonsecaea monophora. Med Mycol. 2009;47:77–80.

    Article  Google Scholar 

  14. 14.

    Takei H, Goodman JC, Powell SZ. Cerebral phaeohyphomycosis caused by ladophialophora bantiana and Fonsecaea monophora: report of three cases. Clin Neuropathol. 2007;26:21–7.

    CAS  Article  Google Scholar 

  15. 15.

    Surash S, Tyagi A, De Hoog GS, Zeng JS, Barton RC, Hobson RP. Cerebral phaeohyphomycosis caused by Fonsecaea monophora. Med Mycol. 2005;43:465–72.

    CAS  Article  Google Scholar 

  16. 16.

    Doymaz MZ, Seyithanoglu MF, Hakyemez I, Gultepe BS, Cevik S, Aslan T. A case of cerebral phaeohyphomycosis caused by Fonsecaea monophora, a neurotropic dematiaceous fungus, and a review of the literature. Mycoses. 2015;58:187–92.

    Article  Google Scholar 

  17. 17.

    Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010;11:889–96.

    CAS  Article  Google Scholar 

  18. 18.

    Verreck FA, de Boer T, Langenberg DM, et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci USA. 2004;101:4560–5.

    CAS  Article  Google Scholar 

  19. 19.

    Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol. 2009;27:451–83.

    CAS  Article  Google Scholar 

  20. 20.

    Wang N, Liang H, Zen K. Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front Immunol. 2014;5:614.

    PubMed  PubMed Central  Google Scholar 

  21. 21.

    Reales-Calderon JA, Aguilera-Montilla N, Corbi AL, Molero G, Gil C. Proteomic characterization of human proinflammatory M1 and anti-inflammatory M2 macrophages and their response to Candida albicans. Proteomics. 2014;14:1503–18.

    CAS  Article  Google Scholar 

  22. 22.

    Bhatia S, Fei M, Yarlagadda M, et al. Rapid host defense against Aspergillus fumigatus involves alveolar macrophages with a predominance of alternatively activated phenotype. PLoS ONE. 2011;6:e15943.

    CAS  Article  Google Scholar 

  23. 23.

    Dai X, Mao C, Lan X, et al. Acute Penicillium marneffei infection stimulates host M1/M2a macrophages polarization in BALB/C mice. BMC Microbiol. 2017;17:177.

    Article  Google Scholar 

  24. 24.

    Hardison SE, Herrera G, Young ML, Hole CR, Wozniak KL, Wormley FL. Protective immunity against pulmonary cryptococcosis is associated with STAT1-mediated classical macrophage activation. J Immunol. 2012;189:4060–8.

    CAS  Article  Google Scholar 

  25. 25.

    Leopold Wager CM, Wormley FL. Classical versus alternative macrophage activation: the Ying and the Yang in host defense against pulmonary fungal infections. Mucosal Immunol. 2014;7:1023–35.

    CAS  Article  Google Scholar 

  26. 26.

    Flesch IE, Schwamberger G, Kaufmann SH. Fungicidal activity of IFN-gamma-activated macrophages. Extracellular killing of Cryptococcus neoformans. J Immunol. 1989;142:3219–24.

    CAS  PubMed  Google Scholar 

  27. 27.

    Hardison SE, Ravi S, Wozniak KL, Young ML, Olszewski MA, Wormley FJ. Pulmonary infection with an interferon-gamma-producing Cryptococcus neoformans strain results in classical macrophage activation and protection. Am J Pathol. 2010;176:774–85.

    CAS  Article  Google Scholar 

  28. 28.

    Zhang Y, Wang F, Tompkins KC, et al. Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. Am J Pathol. 2009;175:2489–500.

    CAS  Article  Google Scholar 

  29. 29.

    Arora S, Hernandez Y, Erb-Downward JR, McDonald RA, Toews GB, Huffnagle GB. Role of IFN-gamma in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis. J Immunol. 2005;174:6346–56.

    CAS  Article  Google Scholar 

  30. 30.

    Muller U, Stenzel W, Kohler G, et al. IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans. J Immunol. 2007;179:5367–77.

    Article  Google Scholar 

  31. 31.

    Saeed S, Quintin J, Kerstens HH, et al. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science. 2014;345:1251086.

    Article  Google Scholar 

  32. 32.

    Das A, Sinha M, Datta S, et al. Monocyte and macrophage plasticity in tissue repair and regeneration. Am J Pathol. 2015;185:2596–606.

    CAS  Article  Google Scholar 

  33. 33.

    Sicari BM, Dziki JL, Siu BF, Medberry CJ, Dearth CL, Badylak SF. The promotion of a constructive macrophage phenotype by solubilized extracellular matrix. Biomaterials. 2014;35:8605–12.

    CAS  Article  Google Scholar 

  34. 34.

    Wüthrich M, Deepe GS, Klein B. Adaptive immunity to fungi. Annu Rev Immunol. 2012;30:115–48.

    Article  Google Scholar 

  35. 35.

    Nandakumar V, Hebrink D, Jenson P, Kottom T, Limper AH. Differential macrophage polarization from pneumocystis in immunocompetent and immunosuppressed hosts: potential adjunctive therapy during pneumonia. Infect Immun. 2017;85:3.

    Article  Google Scholar 

  36. 36.

    Deckman JM, Kurkjian CJ, McGillis JP, et al. Pneumocystis infection alters the activation state of pulmonary macrophages. Immunobiology. 2017;222:188–97.

    CAS  Article  Google Scholar 

  37. 37.

    Rozental S, Alviano CS, de Souza W. The in vitro susceptibility of Fonsecaea pedrosoi to activated macrophages. Mycopathologia. 1994;126:85–91.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the National Natural Science Foundation of China (No. 81571970).

Author information

Affiliations

Authors

Contributions

JZ, LX, JQ conceived of or designed study; JQ, MS performed research; JQ, MS analyzed data; JZ contributed new methods or models; JQ wrote the paper.

Corresponding author

Correspondence to Junmin Zhang.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical Statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Celia Maria de Almeida Soares.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Supplementary material 2 (DOCX 1840 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Qin, J., Zhang, J., Shi, M. et al. Effect of Fonsecaea monophora on the Polarization of THP-1 Cells to Macrophages. Mycopathologia 185, 467–476 (2020). https://doi.org/10.1007/s11046-020-00444-x

Download citation

Keywords

  • Chromoblastomycosis
  • Fonsecaea monophora
  • THP-1
  • Polarization
  • Macrophages