Tenebrio molitor as an Alternative Model to Analyze the Sporothrix Species Virulence

References

• 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):126–143.29538731
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• López-Romero E, Reyes-Montes Mdel R, Pérez-Torres A, et al. Sporothrix schenckii complex and sporotrichosis, an emerging health problem. Future Microbiol. 2011;6(1):85–102.21162638
   PubMed Web of Science ®Google Scholar
• Rossow JA, Queiroz-Telles F, Caceres DH, et al. A one health approach to combatting Sporothrix brasiliensis: narrative review of an emerging zoonotic fungal pathogen in South America. J Fungi (Basel). 2020;6:4.
   Google Scholar
• Han HS, Kano R. Feline sporotrichosis in Asia. Braz J Microbiol. 2020.
   Web of Science ®Google Scholar
• Rodrigues AM, Della Terra PP, Gremião ID, Pereira SA, Orofino-Costa R, de Camargo ZP. The threat of emerging and re-emerging pathogenic Sporothrix species. Mycopathologia. 2020;185(5):813–842.32052359
   PubMed Web of Science ®Google Scholar
• Queiroz-Telles F, Buccheri R, Benard G. Sporotrichosis in immunocompromised hosts. J Fungi (Basel). 2019;5(1):8.
   Google Scholar
• de Beer ZW, Duong TA, Wingfield MJ. The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol. 2016;83:165–191.27616802
   PubMed Web of Science ®Google Scholar
• Rodrigues AM, de Hoog GS, de Camargo ZP. Sporothrix species causing outbreaks in animals and humans driven by animal-animal transmission. PLoS Pathog. 2016;12(7):e1005638.27415796
   PubMed Web of Science ®Google Scholar
• Etchecopaz AN, Lanza N, Toscanini MA, et al. Sporotrichosis caused by Sporothrix brasiliensis in Argentina: case report, molecular identification and in vitro susceptibility pattern to antifungal drugs. J Mycol Med. 2020;30(1):100908.31732417
   PubMed Web of Science ®Google Scholar
• Gremião ID, Miranda LH, Reis EG, Rodrigues AM, Pereira SA. Zoonotic epidemic of sporotrichosis: cat to human transmission. PLoS Pathog. 2017;13(1):e1006077.28103311
   PubMed Web of Science ®Google Scholar
• Moussa TAA, Kadasa NMS, Al Zahrani HS, et al. Origin and distribution of Sporothrix globosa causing sapronoses in Asia. J Med Microbiol. 2017;66(5):560–569.28327256
   PubMed Web of Science ®Google Scholar
• Chakrabarti A, Bonifaz A, Gutierrez-Galhardo MC, Mochizuki T, Li S. Global epidemiology of sporotrichosis. Med Mycol. 2015;53(1):3–14.25526781
   PubMed Web of Science ®Google Scholar
• Camacho E, León-Navarro I, Rodríguez-Brito S, Mendoza M, Niño-Vega GA. Molecular epidemiology of human sporotrichosis in Venezuela reveals high frequency of Sporothrix globosa. BMC Infect Dis. 2015;15:94.25880588
   PubMed Web of Science ®Google Scholar
• Martinez-Alvarez JA, Perez-Garcia 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;8:843.28539922
   PubMed Web of Science ®Google Scholar
• 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;15:943.25351875
   PubMed Web of Science ®Google Scholar
• Silva-Bailão MG, de Sousa Lima P, Evangelista de Oliveira MM, et al. Comparative proteomics in the three major human pathogenic species of the genus Sporothrix. Microbes Infect. 2020.
   Web of Science ®Google Scholar
• Fernandes GF, dos Santos PO, Rodrigues AM, Sasaki AA, Burger E, de Camargo ZP. Characterization of virulence profile, protein secretion and immunogenicity of different Sporothrix schenckii sensu stricto isolates compared with S. globosa and S. brasiliensis species. Virulence. 2013;4(3):241–249.23324498
   PubMed Web of Science ®Google Scholar
• Huang L, Gao W, Giosa D, et al. Whole-genome sequencing and in silico analysis of two strains of Sporothrix globosa. Genome Biol Evol. 2016;8(11):3292–3296.27635048
   PubMed Web of Science ®Google Scholar
• Oliveira MME, Almeida-Paes R, Corrêa-Moreira D, et al. A case of sporotrichosis caused by different Sporothrix brasiliensis strains: mycological, molecular, and virulence analyses. Mem Inst Oswaldo Cruz. 2019;114:e190260–e190260.31644705
   PubMed Web of Science ®Google Scholar
• Batista-Duharte A, Téllez-Martínez D, Aparecida Jellmayer J, et al. Repeated exposition to mercury (ii) chloride enhances susceptibility to S. schenckii sensu stricto infection in mice. J Fingi (Basel). 2018;4(2):64.
   Google Scholar
• Della Terra PP, Rodrigues AM, Fernandes GF, Nishikaku AS, Burger E, de Camargo ZP. Exploring virulence and immunogenicity in the emerging pathogen Sporothrix brasiliensis. PLoS Negl Trop Dis. 2017;11(8):e0005903–e0005903.28854184
   PubMed Web of Science ®Google Scholar
• Cruz Choappa R, Pérez Gaete S, Rodríguez Badilla V, Vieille Oyarzo P, Opazo Sanchez H. Virulence of Sporothrix globosa in murine models. Rev Argent Microbiol. 2016;48(3):196–199.27566945
   PubMed Web of Science ®Google Scholar
• Castro RA, Kubitschek-Barreira PH, Teixeira PA, 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):e75656.24116065
   PubMed Web of Science ®Google Scholar
• Fernandes KSS, Mathews HL, Bezerra LML. Differences in virulence of Sporothrix schenckii conidia related to culture conditions and cell-wall components. J Med Microbiol. 1999;48(2):195–203.9989648
   PubMed Web of Science ®Google Scholar
• Almeida-Paes R, De oliveira LC, Oliveira MME, Gutierrez-Galhardo MC, Nosanchuk JD, Zancopé-Oliveira RM. Phenotypic characteristics associated with virulence of clinical isolates from the Sporothrix complex. Biomed Res Int. 2015;2015:212308.25961005
   PubMed Web of Science ®Google Scholar
• Kong X, Xiao T, Lin J, Wang Y, Chen HD. Relationships among genotypes, virulence and clinical forms of Sporothrix schenckii infection. Clin Microbiol Infect. 2006;12(11):1077–1081.17002606
   PubMed Web of Science ®Google Scholar
• 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):651–655.19624508
   PubMed Web of Science ®Google Scholar
• Teixeira PA, De castro RA, Nascimento RC, et al. Cell surface expression of adhesins for fibronectin correlates with virulence in. Sporothrix Schenckii Microbiology. 2009;155(Pt 11):3730–3738.19762444
   PubMed Web of Science ®Google Scholar
• Jacobsen ID. Galleria mellonella as a model host to study virulence of Candida. Virulence. 2014;5(2):237–239.24384470
   PubMed Web of Science ®Google Scholar
• Clavijo-Giraldo DM, Matinez-Alvarez JA, Lopes-Bezerra LM, et al. Analysis of Sporothrix schenckii sensu stricto and Sporothrix brasiliensis virulence in Galleria mellonella. J Microbiol Methods. 2016;122:73–77.26826293
   PubMed Web of Science ®Google Scholar
• Lozoya-Perez 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;12:67–85.30643435
   PubMed Web of Science ®Google Scholar
• Lozoya-Perez NE, Casas-Flores S, Martinez-Alvarez 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(10):1023–1030.30227928
   PubMed Web of Science ®Google Scholar
• Lozoya-Perez NE, Clavijo-Giraldo DM, Martinez-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 (Basel). 2020;6:4.
   Google Scholar
• Passos JS, Martino LC, Dartora VFC, Araujo GLB, Ishida K, Lopes LB. Development, skin targeting and antifungal efficacy of topical lipid nanoparticles containing itraconazole. Eur j Pharm Sci. 2020;149:105296.32151706
   PubMed Web of Science ®Google Scholar
• Martinez-Alvarez JA, Garcia-Carnero LC, Kubitschek-Barreira PH, et al. Analysis of some immunogenic properties of the recombinant Sporothrix schenckii Gp70 expressed in Escherichia coli. Future Microbiol. 2019;14:397–410.30854893
   PubMed Web of Science ®Google Scholar
• Desalermos A, Fuchs BB, Mylonakis E. Selecting an invertebrate model host for the study of fungal pathogenesis. PLOS Pathog. 2012;8(2):e1002451.22319439
   PubMed Web of Science ®Google Scholar
• de Souza PC, Morey AT, Castanheira GM, et al. Tenebrio molitor (Coleoptera: tenebrionidae) as an alternative host to study fungal infections. J Microbiol Methods. 2015;118:182–186.26453946
   PubMed Web of Science ®Google Scholar
• Tamez-Castrellon AK, Romeo O, Garcia-Carnero LC, Lozoya-Perez NE, Mora-Montes HM. Virulence factors in Sporothrix schenckii, one of the causative agents of sporotrichosis. Curr Protein Pept Sci. 2020;21(3):295–312.31589121
   PubMed Web of Science ®Google Scholar
• Canteri de Souza P, Custodio Caloni C, Wilson D, Sergio Almeida R. An invertebrate host to study fungal infections, mycotoxins and antifungal drugs: tenebrio molitor. J Fungi (Basel). 2018;4:4.
   Google Scholar
• Vigneron A, Jehan C, Rigaud T, Moret Y. Immune defenses of a beneficial pest: the mealworm beetle, Tenebrio molitor. Front Physiol. 2019;10:138.30914960
   PubMed Web of Science ®Google Scholar
• Mora-Montes HM, Robledo-Ortiz CI, Gonzalez-Sanchez LC, Lopez-Esparza A, Lopez-Romero E, Flores-Carreon A. Purification and biochemical characterisation of endoplasmic reticulum alpha1,2-mannosidase from Sporothrix Schenckiil. Mem Inst Oswaldo Cruz. 2010;105(1):79–85.20209334
   PubMed Web of Science ®Google Scholar
• Madrid H, Cano J, Gene J, Bonifaz A, Toriello C, Guarro J. Sporothrix globosa, a pathogenic fungus with widespread geographical distribution. Rev Iberoam Micol. 2009;26(3):218–222.19635441
   PubMed Web of Science ®Google Scholar
• Garcia-Carnero LC, Clavijo-Giraldo DM, Gomez-Gaviria M, et al. Early virulence predictors during the Candida species-Galleria mellonella Interaction. J Fungi (Basel). 2020;6:3.
   Google Scholar
• Gomez-Gaviria M, Lozoya-Perez NE, Staniszewska M, Franco B, Nino-Vega GA, Mora-Montes HM. Loss of Kex2 affects the Candida albicans cell wall and interaction with innate immune cells. J Fungi (Basel). 2020;6:2.
   Google Scholar
• 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;18:5.
   Web of Science ®Google Scholar
• 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;8:2156.29163439
   PubMed Web of Science ®Google Scholar
• 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;7:1951.27994582
   PubMed Web of Science ®Google Scholar
• Ludwig D, Barsa MC. Activity of dehydrogenase enzymes during the metamorphosis of the mealworm, Tenebrio molitor Linnaeus. Ann Entomol Soc Am. 1958;51(3):311–314.
   Google Scholar
• Ito T, Fraenkel G. The effect of nitrogen starvation on Tenebrio molitor L. J Insect Physiol. 1966;12(7):803–817.4308372
   PubMed Web of Science ®Google Scholar
• Eriksson T, Andere AA, Kelstrup H, Emery VJ, Picard CJ. The yellow mealworm (Tenebrio molitor) genome: a resource for the emerging insects as food and feed industry. J Insects Food Feed. 2020;6(5):445–455.
   Web of Science ®Google Scholar
• Bergin D, Brennan M, Kavanagh K. Fluctuations in haemocyte density and microbial load may be used as indicators of fungal pathogenicity in larvae of Galleria mellonella. Microb Infect. 2003;5(15):1389–1395.
   PubMed Web of Science ®Google Scholar
• Mesa-Arango AC, Forastiero A, Bernal-Martinez L, Cuenca-Estrella M, Mellado E, Zaragoza O. The non-mammalian host Galleria mellonella can be used to study the virulence of the fungal pathogen Candida tropicalis and the efficacy of antifungal drugs during infection by this pathogenic yeast. Med Mycol. 2013;51(5):461–472.23170962
   PubMed Web of Science ®Google Scholar
• Roy MC, Kim Y. Tolerance of the mealworm beetle, Tenebrio molitor, to an entomopathogenic nematode, Steinernema feltiae, at two infection foci, the intestine and the hemocoel. J Invertebr Pathol. 2020;174:107428.32553640
   PubMed Web of Science ®Google Scholar
• Lim S, Yun HK, Kang KM, Lee BL, Won R, Lee IH. Interactions between Mycoplasma pulmonis and immune systems in the mealworm beetle, Tenebrio molitor. Insect Biochem Mol Biol. 2019;114:103231.31479697
   PubMed Web of Science ®Google Scholar
• Valtonen TM, Viitaniemi H, Rantala MJ. Copulation enhances resistance against an entomopathogenic fungus in the mealworm beetle. Tenebrio Molitor Parasitology. 2010;137(6):985–989.20128944
   PubMed Web of Science ®Google Scholar
• Kan H, Kim CH, Kwon HM, et al. Molecular control of phenoloxidase-induced melanin synthesis in an insect. J Biol Chem. 2008;283(37):25316–25323.18628205
   PubMed Web of Science ®Google Scholar
• Kavanagh K, Sheehan G. The use of Galleria mellonella larvae to identify novel antimicrobial agents against fungal species of medical interest. J Fungi (Basel). 2018;4:3.
   Google Scholar
• Tamez-Castrellon AK, Romo-Lucio R, Martinez-Duncker I, Mora-Montes HM. Generation of a synthetic binary plasmid that confers resistance to nourseothricin for genetic engineering of Sporothrix schenckii. Plasmid. 2018;100:1–5.30236508
   PubMed Web of Science ®Google Scholar
• Moret Y. “Trans-generational immune priming”: specific enhancement of the antimicrobial immune response in the mealworm beetle Tenebrio Molitor. Proc Biol Sci. 2006;273(1592):1399–1405.16777729
   PubMed Web of Science ®Google Scholar
• Dhinaut J, Chogne M, Moret Y. Immune priming specificity within and across generations reveals the range of pathogens affecting evolution of immunity in an insect. J Anim Ecol. 2018;87(2):448–463.28239855
   PubMed Web of Science ®Google Scholar
• Krappmann S. CRISPR-Cas9, the new kid on the block of fungal molecular biology. Med Mycol. 2017;55(1):16–23.27811178
   PubMed Web of Science ®Google Scholar
• Rantala MJ, Dubovskiy IM, Pölkki M, Krama T, Contreras-Garduño J, Krams IA. Effect of juvenile hormone on resistance against entomopathogenic fungus Metarhizium robertsii differs between sexes. J Fungi (Basel). 2020;6(4):298.
   Google Scholar
• Bharadwaj A, Stafford KC 3rd. Potential of Tenebrio molitor (Coleoptera: tenebrionidae) as a bioassay probe for Metarhizium brunneum (Hypocreales: clavicipitaceae) activity against Ixodes scapularis (Acari: ixodidae). J Econ Entomol. 2011;104(6):2095–2098.22299376
   PubMed Web of Science ®Google Scholar
• Jirakkakul J, Roytrakul S, Srisuksam C, et al. Culture degeneration in conidia of Beauveria bassiana and virulence determinants by proteomics. Fungal Biol. 2018;122(2–3):156–171.29458719
   PubMed Web of Science ®Google Scholar
• Fornari G, Gomes RR, Degenhardt-Goldbach J, et al. A model for trans-kingdom pathogenicity in Fonsecaea agents of human chromoblastomycosis. Front Microbiol. 2018;9:2211.30356683
   PubMed Web of Science ®Google Scholar
• Kim MH, Joo CH, Cho MY, et al. Bacterial-injection-induced syntheses of N-beta-alanyldopamine and Dopa decarboxylase in the hemolymph of coleopteran insect, Tenebrio molitor larvae. Eur j Biochem. 2000;267(9):2599–2608.10785380
   PubMedGoogle Scholar
• Keshavarz M, Jo YH, Park KB, et al. TmDorX2 positively regulates antimicrobial peptides in Tenebrio molitor gut, fat body, and hemocytes in response to bacterial and fungal infection. Sci Rep. 2019;9:16878.31728023
   PubMed Web of Science ®Google Scholar
• Keshavarz M, Jo YH, Edosa TT, Bae YM, Han YS. TmPGRP-SA regulates antimicrobial response to bacteria and fungi in the fat body and gut of Tenebrio molitor. Int J Mol Sci. 2020;21(6):2113.
   Web of Science ®Google Scholar
• Rodrigues AM, Kubitschek-Barreira PH, Fernandes GF, de Almeida SR, Lopes-Bezerra LM, de Camargo ZP. Immunoproteomic analysis reveals a convergent humoral response signature in the Sporothrix schenckii complex. J Proteomics. 2015;115:8–22.25434489
   PubMed Web of Science ®Google Scholar
• de Almeida JRF, Jannuzzi GP, Kaihami GH, Breda LCD, Ferreira KS, de Almeida SR. An immunoproteomic approach revealing peptides from Sporothrix brasiliensis that induce a cellular immune response in subcutaneous sporotrichosis. Sci Rep. 2018;8(1):4192.29520092
   PubMed Web of Science ®Google Scholar
• Chen F, Jiang R, Wang Y, et al. Recombinant phage elicits protective immune response against systemic S. globosa infection in mouse model. Sci Rep. 2017;7:42024.28165018
   PubMed Web of Science ®Google Scholar