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ORIGINAL RESEARCH

Differential Recognition of Sporothrix schenckii, Sporothrix brasiliensis, and Sporothrix globosa by Human Monocyte-Derived Macrophages and Dendritic Cells

, , & ORCID Icon
Pages 4817-4834 | Received 03 May 2023, Accepted 20 Jul 2023, Published online: 25 Jul 2023

References

  • de Beer ZW, Duong TA, Wingfield MJ. The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol. 2016;83:165–191. doi:10.1016/j.simyco.2016.07.001
  • de Beer ZW, Procter M, Wingfield MJ, Marincowitz S, Duong TA. Generic boundaries in the Ophiostomatales reconsidered and revised. Stud Mycol. 2022;101:57–120. doi:10.3114/sim.2022.101.02
  • Lopes-Bezerra LM, Mora-Montes HM, Zhang Y, et al. Sporotrichosis between 1898 and 2017: the evolution of knowledge on a changeable disease and on emerging etiological agents. Med Mycol. 2018;56(suppl_1):126–143. doi:10.1093/mmy/myx103
  • Chakrabarti A, Bonifaz A, Gutierrez-Galhardo MC, Mochizuki T, Li S. Global epidemiology of sporotrichosis. Med Mycol. 2015;53(1):3–14. doi:10.1093/mmy/myu062
  • Lopez-Romero E, Reyes-Montes MR, Perez-Torres A, et al. Sporothrix schenckii complex and sporotrichosis, an emerging health problem. Future Microbiol. 2011;6(1):85–102. doi:10.2217/fmb.10.157
  • Lv S, Hu X, Liu Z, Lin Y, Wu H, Li F. Clinical epidemiology of sporotrichosis in Jilin province, China (1990–2019): a series of 4969 cases. Infect Drug Resist. 2022;15:1753–1765. doi:10.2147/idr.S354380
  • Takenaka M, Sato S, Nishimoto K. Survey of 155 sporotrichosis cases examined in Nagasaki Prefecture from 1951 to 2007. Nihon Ishinkin Gakkai Zasshi. 2009;50(2):101–108. doi:10.3314/jjmm.50.101
  • Bongomin F, Adetona Fayemiwo S. Epidemiology of fungal diseases in Africa: a review of diagnostic drivers. Curr Med Mycol. 2021;7(1):63–70. doi:10.18502/cmm.7.1.6246
  • Barile F, Mastrolonardo M, Loconsole F, Rantuccio F. Cutaneous sporotrichosis in the period 1978–1992 in the province of Bari, Apulia, Southern Italy. Mycoses. 1993;36(5–6):181–185. doi:10.1111/j.1439-0507.1993.tb00747.x
  • Gold JA, Derado G, Mody RK, Benedict K. Sporotrichosis-associated hospitalizations, United States, 2000–2013. Emerg Infect Dis. 2016;22(10):1817–1820. doi:10.3201/eid2210.160671
  • Lopes-Bezerra LM, Mora-Montes HM, Bonifaz A. Sporothrix and Sporotrichosis. In: Mora-Montes HM, Lopes-Bezerra LM, editors. Current Progress in Medical Mycology. Cham: Springer; 2017:309–331.
  • Mora-Montes HM, Dantas Ada S, Trujillo-Esquivel E, de Souza Baptista AR, Lopes-Bezerra LM. Current progress in the biology of members of the Sporothrix schenckii complex following the genomic era. FEMS Yeast Res. 2015;15:6.
  • Orofino-Costa R, Macedo PM, Rodrigues AM, Bernardes-Engemann AR. Sporotrichosis: an update on epidemiology, etiopathogenesis, laboratory and clinical therapeutics. An Bras Dermatol. 2017;92(5):606–620. doi:10.1590/abd1806-4841.2017279
  • Queiroz-Telles F, Buccheri R, Benard G. Sporotrichosis in immunocompromised hosts. J Fungi. 2019;5(1):8. doi:10.3390/jof5010008
  • de Miranda LHM, Meli M, Conceição-Silva F, et al. Co-infection with feline retrovirus is related to changes in immunological parameters of cats with sporotrichosis. PLoS One. 2018;13(11):e0207644. doi:10.1371/journal.pone.0207644
  • Mora-Montes HM. Special Issue “Sporothrix and Sporotrichosis 2.0”. J Fungi. 2022;8(8):821. doi:10.3390/jof8080821
  • Nava-Pérez N, Neri-García LG, Romero-González OE, Terrones-Cruz JA, García-Carnero LC, Mora-Montes HM. Biological and clinical attributes of Sporothrix globosa, a causative agent of sporotrichosis. Infect Drug Resist. 2022;15:2067–2090. doi:10.2147/idr.s362099
  • Arrillaga-Moncrieff I, Capilla J, Mayayo E, et al. Different virulence levels of the species of Sporothrix in a murine model. Clin Microbiol Infect. 2009;15(7):651–655. doi:10.1111/j.1469-0691.2009.02824.x
  • Lozoya-Pérez NE, Clavijo-Giraldo DM, Martínez-Duncker I, et al. Influences of the culturing media in the virulence and cell wall of Sporothrix schenckii, Sporothrix brasiliensis, and Sporothrix globosa. J Fungi. 2020;6(4):323. doi:10.3390/jof6040323
  • Rodrigues AM, Gonçalves SS, de Carvalho JA, Borba-Santos LP, Rozental S, Camargo ZP. Current progress on epidemiology, diagnosis, and treatment of sporotrichosis and their future trends. J Fungi. 2022;8(8):776. doi:10.3390/jof8080776
  • Etchecopaz A, Toscanini MA, Gisbert A, et al. Sporothrix brasiliensis: a review of an emerging South American fungal pathogen, its related disease, presentation and spread in Argentina. J Fungi. 2021;7(3):170. doi:10.3390/jof7030170
  • Tamez-Castrellón AK, van der Beek SL, López-Ramírez LA, et al. Disruption of protein rhamnosylation affects the Sporothrix schenckii-host interaction. Cell Surf. 2021;7:100058. doi:10.1016/j.tcsw.2021.100058
  • Lionakis MS, Drummond RA, Hohl TM. Immune responses to human fungal pathogens and therapeutic prospects. Nat Rev Immunol. 2023;1–20. doi:10.1038/s41577-022-00826-w
  • Loh JT, Lam KP. Fungal infections: immune defense, immunotherapies and vaccines. Adv Drug Deliv Rev. 2023;196:114775. doi:10.1016/j.addr.2023.114775
  • Gómez-Gaviria M, Vargas-Macías AP, García-Carnero LC, Martínez-Duncker I, Mora-Montes HM. Role of protein glycosylation in interactions of medically relevant fungi with the host. J Fungi. 2021;7(10):875. doi:10.3390/jof7100875
  • Martínez-Álvarez JA, Pérez-García LA, Mellado-Mojica E, et al. Sporothrix schenckii sensu stricto and Sporothrix brasiliensis are differentially recognized by human peripheral blood mononuclear cells. Front Microbiol. 2017;8:843. doi:10.3389/fmicb.2017.00843
  • Villalobos-Duno HL, Barreto LA, Alvarez-Aular Á, et al. Comparison of cell wall polysaccharide composition and structure between strains of Sporothrix schenckii and Sporothrix brasiliensis. Front Microbiol. 2021;12:726958. doi:10.3389/fmicb.2021.726958
  • Lopes-Bezerra LM, Walker LA, Niño-Vega G, et al. Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers. PLoS Negl Trop Dis. 2018;12(3):e0006169–e0006169. doi:10.1371/journal.pntd.0006169
  • Lozoya-Pérez NE, Casas-Flores S, de Almeida JRF, et al. Silencing of OCH1 unveils the role of Sporothrix schenckii N-linked glycans during the host-fungus interaction. Infect Drug Resist. 2019;12:67–85. doi:10.2147/idr.S185037
  • Bezerra L. Sporothrix schenckii cell wall peptidorhamnomannans. Mini Review. Front Microbiol. 2011;2:243. doi:10.3389/fmicb.2011.00243
  • López-Ramírez LA, Martínez-Duncker I, Márquez-Márquez A, Vargas-Macías AP, Mora-Montes HM. Silencing of ROT2, the encoding gene of the endoplasmic reticulum glucosidase II, affects the cell wall and the Sporothrix schenckii-host interaction. J Fungi. 2022;8(11):1220. doi:10.3390/jof8111220
  • Castro RA, Kubitschek-Barreira PH, Teixeira PAC, et al. Differences in cell morphometry, cell wall topography and Gp70 expression correlate with the virulence of Sporothrix brasiliensis clinical isolates. PLoS One. 2013;8(10):e75656. doi:10.1371/journal.pone.0075656
  • Lloyd KO, Bitoon MA. Isolation and purification of a peptido-rhamnomannan from the yeast form of Sporothrix schenckii. Structural and immunochemical studies. J Immunol. 1971;107(3):663–671. doi:10.4049/jimmunol.107.3.663
  • García-Carnero LC, Salinas-Marín R, Lozoya-Pérez NE, et al. The Heat shock protein 60 and Pap1 participate in the Sporothrix schenckii-host interaction. J Fungi. 2021;7(11):960. doi:10.3390/jof7110960
  • Vargas-Macías AP, Gómez-Gaviria M, García-Carnero LC, Mora-Montes HM. Current models to study the Sporothrix-host interaction. Review. Front Fungal Biol. 2022;3:833111. doi:10.3389/ffunb.2022.833111
  • Ward RA, Vyas JM. The first line of defense: effector pathways of anti-fungal innate immunity. Curr Opin Microbiol. 2020;58:160–165. doi:10.1016/j.mib.2020.10.003
  • Alegranci P, de Abreu Ribeiro LC, Ferreira LS, et al. The predominance of alternatively activated macrophages following challenge with cell wall peptide-polysaccharide after prior infection with Sporothrix schenckii. Mycopathologia. 2013;176(1–2):57–65. doi:10.1007/s11046-013-9663-y
  • Franco Dde L, Nascimento RC, Ferreira KS, Almeida SR. Antibodies against Sporothrix schenckii enhance TNF-α production and killing by macrophages. Scand J Immunol. 2012;75(2):142–146. doi:10.1111/j.1365-3083.2011.02636.x
  • Carlos IZ, Sgarbi DB, Santos GC, Placeres MC. Sporothrix schenckii lipid inhibits macrophage phagocytosis: involvement of nitric oxide and tumour necrosis factor-alpha. Scand J Immunol. 2003;57(3):214–220. doi:10.1046/j.1365-3083.2003.01175.x
  • Tachibana T, Matsuyama T, Mitsuyama M. Involvement of CD4+ T cells and macrophages in acquired protection against infection with Sporothrix schenckii in mice. Med Mycol. 1999;37(6):397–404. doi:10.1046/j.1365-280x.1999.00239.x
  • Oda LM, Kubelka CF, Alviano CS, Travassos LR. Ingestion of yeast forms of Sporothrix schenckii by mouse peritoneal macrophages. Infect Immun. 1983;39(2):497–504. doi:10.1128/iai.39.2.497-504.1983
  • Huang L, Zhang J, Du W, et al. Chitin-rich heteroglycan from Sporothrix schenckii sensu stricto potentiates fungal clearance in a mouse model of sporotrichosis and promotes macrophages phagocytosis. BMC Microbiol. 2021;21(1):190. doi:10.1186/s12866-021-02243-w
  • Jellmayer JA, Ferreira LS, Manente FA, et al. Dectin-1 expression by macrophages and related antifungal mechanisms in a murine model of Sporothrix schenckii sensu stricto systemic infection. Microb Pathog. 2017;110:78–84. doi:10.1016/j.micpath.2017.06.025
  • Negrini Tde C, Ferreira LS, Alegranci P, et al. Role of TLR-2 and fungal surface antigens on innate immune response against Sporothrix schenckii. Immunol Invest. 2013;42(1):36–48. doi:10.3109/08820139.2012.719982
  • Sassá MF, Ferreira LS, Ribeiro LC, Carlos IZ. Immune response against Sporothrix schenckii in TLR-4-deficient mice. Mycopathologia. 2012;174(1):21–30. doi:10.1007/s11046-012-9523-1
  • Sassá MF, Saturi AE, Souza LF, Ribeiro LC, Sgarbi DB, Carlos IZ. Response of macrophage Toll-like receptor 4 to a Sporothrix schenckii lipid extract during experimental sporotrichosis. Immunology. 2009;128(2):301–309. doi:10.1111/j.1365-2567.2009.03118.x
  • Rossato L, Santos SSD, Ferreira LG, de Almeida SR. The importance of Toll-like receptor 4 during experimental Sporothrix brasiliensis infection. Med Mycol. 2019;57(4):489–495. doi:10.1093/mmy/myy048
  • Rossato L, Silvana Dos Santos S, Ferreira LG, Rogério de Almeida S. The impact of the absence of Toll-like receptor-2 during Sporothrix brasiliensis infection. J Med Microbiol. 2019;68(1):87–94. doi:10.1099/jmm.0.000876
  • Neves GWP, Wong SSW, Aimanianda V, et al. Complement-mediated differential immune response of human macrophages to Sporothrix species through interaction with their cell wall peptidorhamnomannans. Front Immunol. 2021;12:749074. doi:10.3389/fimmu.2021.749074
  • Song Y, Yao L, Zhen Y, et al. Sporothrix globosa melanin inhibits antigen presentation by macrophages and enhances deep organ dissemination. Braz J Microbiol. 2021;52(1):19–31. doi:10.1007/s42770-020-00345-7
  • Guan MQ, Yao L, Zhen Y, Song Y, Cui Y, Li SS. Melanin of Sporothrix globosa affects the function of THP-1 macrophages and modulates the expression of TLR2 and TLR4. Microb Pathog. 2021;159:105158. doi:10.1016/j.micpath.2021.105158
  • Uenotsuchi T, Takeuchi S, Matsuda T, et al. Differential induction of Th1-prone immunity by human dendritic cells activated with Sporothrix schenckii of cutaneous and visceral origins to determine their different virulence. Int Immunol. 2006;18(12):1637–1646. doi:10.1093/intimm/dxl097
  • Quinello C, Souza Ferreira L, Picolli I, et al. Sporothrix schenckii cell wall proteins-stimulated BMDCs are able to induce a Th1-prone cytokine profile in vitro. J Fungi. 2018;4(3):106. doi:10.3390/jof4030106
  • Verdan FF, Faleiros JC, Ferreira LS, et al. Dendritic cell are able to differentially recognize Sporothrix schenckii antigens and promote Th1/Th17 response in vitro. Immunobiology. 2012;217(8):788–794. doi:10.1016/j.imbio.2012.04.006
  • Kusuhara M, Qian H, Li X, et al. Mouse bone marrow-derived dendritic cells can phagocytize the Sporothrix schenckii, and mature and activate the immune response by secreting interleukin-12 and presenting antigens to T lymphocytes. J Dermatol. 2014;41(5):386–392. doi:10.1111/1346-8138.12472
  • Madrid H, Cano J, Gené J, Bonifaz A, Toriello C, Guarro J. Sporothrix globosa, a pathogenic fungus with widespread geographical distribution. Rev Iberoam Micol. 2009;26(3):218–222. doi:10.1016/j.riam.2009.02.005
  • Teixeira MM, de Almeida LG, Kubitschek-Barreira P, et al. Comparative genomics of the major fungal agents of human and animal sporotrichosis: Sporothrix schenckii and Sporothrix brasiliensis. BMC Genomics. 2014;15:943. doi:10.1186/1471-2164-15-943
  • Giosa D, Felice MR, Giuffrè L, et al. Transcriptome-wide expression profiling of Sporothrix schenckii yeast and mycelial forms and the establishment of the Sporothrix Genome DataBase. Microb Genom. 2020;6(10):mgen000445. doi:10.1099/mgen.0.000445
  • Giosa D, Giuffrè L, Felice MR, et al. P421 Whole-transcriptome analysis of Sporothrix brasiliensis grown in mold- and yeast-inducing conditions. Med Mycol. 2022;60(Supplement_1):myac072P421. doi:10.1093/mmy/myac072.P421
  • Trujillo-Esquivel E, Martínez-Álvarez JA, Clavijo-Giraldo DM, et al. The Sporothrix schenckii gene encoding for the ribosomal protein L6 has constitutive and stable expression and works as an endogenous control in gene expression analysis. Front Microbiol. 2017;8:1676. doi:10.3389/fmicb.2017.01676
  • Endres S, Ghorbani R, Lonnemann G, van der Meer JW, Dinarello CA. Measurement of immunoreactive interleukin-1 beta from human mononuclear cells: optimization of recovery, intrasubject consistency, and comparison with interleukin-1 alpha and tumor necrosis factor. Clin Immunol Immunopathol. 1988;49(3):424–438. doi:10.1016/0090-1229(88)90130-4
  • Perez-Garcia LA, Csonka K, Flores-Carreon A, et al. Role of protein glycosylation in Candida parapsilosis cell wall integrity and host interaction. Front Microbiol. 2016;7:306. doi:10.3389/fmicb.2016.00306
  • Cambi A, Gijzen K, de Vries IJM, et al. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur J Immunol. 2003;33(2):532–538. doi:10.1002/immu.200310029
  • Cambi A, Netea MG, Mora-Montes HM, et al. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J Biol Chem. 2008;283(29):20590–20599. doi:10.1074/jbc.M709334200
  • Hernandez-Chavez MJ, Franco B, Clavijo-Giraldo DM, Hernandez NV, Estrada-Mata E, Mora-Montes HM. Role of protein phosphomannosylation in the Candida tropicalis-macrophage interaction. FEMS Yeast Res. 2018. doi:10.1093/femsyr/foy053
  • Lozoya-Pérez NE, Casas-Flores S, Martínez-Álvarez JA, et al. Generation of Sporothrix schenckii mutants expressing the green fluorescent protein suitable for the study of host-fungus interactions. Fungal Biol. 2018;122:1023–1030. doi:10.1016/j.funbio.2018.07.004
  • Gonzalez-Hernandez RJ, Jin K, Hernandez-Chavez MJ, et al. Phosphomannosylation and the functional analysis of the extended Candida albicans MNN4-like gene family. Front Microbiol. 2017;8:2156. doi:10.3389/fmicb.2017.02156
  • Mora-Montes HM, Bates S, Netea MG, et al. A multifunctional mannosyltransferase family in Candida albicans determines cell wall mannan structure and host-fungus interactions. J Biol Chem. 2010;285(16):12087–12095. doi:10.1074/jbc.M109.081513
  • Estrada-Mata E, Navarro-Arias MJ, Perez-Garcia LA, et al. Members of the Candida parapsilosis complex and Candida albicans are differentially recognized by human peripheral blood mononuclear cells. Front Microbiol. 2015;6:1527. doi:10.3389/fmicb.2015.01527
  • Navarro-Arias MJ, Defosse TA, Dementhon K, et al. Disruption of protein mannosylation affects Candida guilliermondii cell wall, immune sensing, and virulence. Front Microbiol. 2016;7:1951. doi:10.3389/fmicb.2016.01951
  • Schwartz SN, Medoff G, Kobayashi GS, Kwan CN, Schlessinger D. Antifungal properties of polymyxin B and its potentiation of tetracycline as an antifungal agent. Antimicrob Agents Chemother. 1972;2(1):36–40. doi:10.1128/AAC.2.1.36
  • Cossarizza A, Chang H-D, Radbruch A, et al. Guidelines for the use of flow cytometry and cell sorting in immunological studies. Eur J Immunol. 2021:51(12);2708–3145. doi:10.1002/eji.202170126
  • Tamez-Castrellón AK, Romeo O, García-Carnero LC, Lozoya-Pérez NE, Mora-Montes HM. Virulence factors in Sporothrix schenckii, one of the causative agents of sporotrichosis. Curr Protein Pept Sci. 2020;21(3):295–312. doi:10.2174/1389203720666191007103004
  • Ruiz-Baca E, Mora-Montes HM, Lopez-Romero E, Toriello C, Mojica-Marin V, Urtiz-Estrada N. 2D-immunoblotting analysis of Sporothrix schenckii cell wall. Mem Inst Oswaldo Cruz. 2011;106(2):248–250. doi:10.1590/S0074-02762011000200021
  • Thomas CJ, Schroder K. Pattern recognition receptor function in neutrophils. Trends Immunol. 2013;34(7):317–328. doi:10.1016/j.it.2013.02.008
  • García-Carnero LC, Martínez-Duncker I, Gómez-Gaviria M, Mora-Montes HM. Differential recognition of clinically relevant Sporothrix species by human mononuclear cells. J Fungi. 2023;9(4):448. doi:10.3390/jof9040448
  • Bozza S, Perruccio K, Montagnoli C, et al. A dendritic cell vaccine against invasive aspergillosis in allogeneic hematopoietic transplantation. Blood. 2003;102(10):3807–3814. doi:10.1182/blood-2003-03-0748
  • Reid DM, Gow NAR, Brown GD. Pattern recognition: recent insights from Dectin-1. Curr Opin Immunol. 2009;21(1):30–37. doi:10.1016/j.coi.2009.01.003