FSH1 regulates the phenotype and pathogenicity of the pathogenic dermatophyte Microsporum canis

Zhang,Furong; Tan,Can; Xu,Yu; Yang,Guoling

doi:10.3892/ijmm.2019.4355

FSH1 regulates the phenotype and pathogenicity of the pathogenic dermatophyte Microsporum canis

Authors:
- Furong Zhang
- Can Tan
- Yu Xu
- Guoling Yang
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Affiliations: Department of Dermatology, The First Affiliated Hospital of Dalian Medical University, Chengdu, Sichuan 11736, P.R. China, Department of Dermatology, Hospital of Anjing Town, Chengdu, Sichuan 11736, P.R. China
Published online on: September 27, 2019 https://doi.org/10.3892/ijmm.2019.4355
Pages: 2047-2056
Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Microsporum canis (M. canis) is a common pathogen that causes tinea capitis and is present worldwide. The incidence of M. canis infection, particularly tinea capitis, has been increasing in China. In our previous studies, family of serine hydrolases 1 (FSH1) was identified as a potential virulence factor in tinea capitis infection caused by M. canis. To determine the function of this gene in M. canis, FSH1 was knocked down using double‑stranded RNA interference mediated by Agrobacterium tumefaciens. Reverse transcription‑quantitative PCR analysis was used to confirm gene knockdown. Loss of FSH1 expression by RNAi resulted in a minor phenotype alteration, but M. canis pathogenicity in guinea pig cutaneous infection was decreased compared with the wild‑type strain. To the best of our knowledge, the present study is the first to demonstrate that FSH1 is associated with macroconidia septa formation and is an important contributor to M. canis virulence. These findings may advance the understanding of the function of the FSH1 gene and provide a foundation for future studies on macroconidia septa formation and pathogenicity of M. canis.

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1	Mao L, Zhang L, Li H, Chen W, Wang H, Wu S, Guo C, Lu A, Yang G, An L, et al: Pathogenic fungus Microsporum canis activates the NLRP3 inflammasome. Infect Immun. 82:882–892. 2014. View Article : Google Scholar : PubMed/NCBI
2	Yu J, Wan Z, Chen W, Wang W and Li R: Molecular typing study of the Microsporum canis strains isolated from an outbreak of tinea capitis in a school. Mycopathologia. 157:37–41. 2004. View Article : Google Scholar : PubMed/NCBI
3	Vermout S, Baldo A, Tabart J, Losson B and Mignon B: Secreted dipeptidyl peptidases as potential virulence factors for Microsporum canis. FEMS Immunol Med Microbiol. 54:299–308. 2008. View Article : Google Scholar : PubMed/NCBI
4	Brosh-Nissimov T, Ben-Ami R, Astman N, Malin A, Baruch Y and Galor I: An outbreak of Microsporum canis infection at a military base associated with stray cat exposure and person-to-person transmission. Mycoses. 61:472–476. 2018. View Article : Google Scholar : PubMed/NCBI
5	Hermoso de Mendoza M, Hermoso de Mendoza J, Alonso JM, Rey JM, Sanchez S, Martin R, Bermejo F, Cortes M, Benitez JM, Garcia WL and Garcia-Sanchez A: A zoonotic ringworm outbreak caused by a dysgonic strain of Microsporum canis from stray cats. Rev Iberoam Micol. 27:62–65. 2010. View Article : Google Scholar : PubMed/NCBI
6	Binder B, Lackner HK, Poessl BD, Propst E, Weger W, Smolle J and Ginter Hanselmayer G: Prevalence of tinea capitis in southeastern Austria between 1985 and 2008: Up-to-date picture of the current situation. Mycoses. 54:243–247. 2011. View Article : Google Scholar
7	Del Boz J, Crespo V, Rivas-Ruiz F and de Troya M: A 30-year survey of paediatric tinea capitis in southern Spain. J Eur Acad Dermatol Venereol. 25:170–174. 2011. View Article : Google Scholar
8	Costa M, Passos XS, Hasimoto e Souza LK, Miranda AT, Lemos Jde A, Oliveira JG Jr and Silva Mdo R: Epidemiology and etiology of dermatophytosis in Goiânia, GO, Brazil. Rev Soc Bras Med Trop. 35:19–22. 2002.In Portuguese. View Article : Google Scholar : PubMed/NCBI
9	Doss RW, El-Rifaie AA, Radi N and El-Sherif AY: Antimicrobial susceptibility of tinea capitis in children from Egypt. Indian J Dermatol. 63:155–159. 2018.PubMed/NCBI
10	Zhu M, Li L, Wang J, Zhang C, Kang K and Zhang Q: Tinea capitis in southeastern China: A 16-year survey. Mycopathologia. 169:235–239. 2010. View Article : Google Scholar
11	Li C and Liu W: Epidemiology of tinea capitis among children in China in recent years: A retrospective analysis. Chin J Mycol. 6:77–82. 2011.
12	Yin B, Xiao Y, Ran Y, Kang D, Dai Y and Lama J: Microsporum canis infection in three familial cases with tinea capitis and tinea corporis. Mycopathologia. 176:259–265. 2013. View Article : Google Scholar : PubMed/NCBI
13	Berg JC, Hamacher KL and Roberts GD: Pseudomycetoma caused by Microsporum canis in an immunosuppressed patient: A case report and review of the literature. J Cutan Pathol. 34:431–434. 2007. View Article : Google Scholar : PubMed/NCBI
14	Anemüller W, Baumgartner S and Brasch J: Atypical Microsporum canis variant in an immunosuppressed child. J Dtsch Dermatol Ges. 6:473–475. 2008.In English and German. View Article : Google Scholar
15	Brillowska-Dabrowska A, Michalek E, Saunte DM, Nielsen SS and Arendrup MC: PCR test for Microsporum canis identification. Med Mycol. 51:576–579. 2013. View Article : Google Scholar : PubMed/NCBI
16	Sharma R, de Hoog S, Presber W and Gräser Y: A virulent genotype of Microsporum canis is responsible for the majority of human infections. J Med Microbiol. 56:1377–1385. 2007. View Article : Google Scholar : PubMed/NCBI
17	Ayanbimpe GM, Taghir H, Diya A and Wapwera S: Tinea capitis among primary school children in some parts of central nigeria. Mycoses. 51:336–340. 2008. View Article : Google Scholar : PubMed/NCBI
18	Patel GA and Schwartz RA: Tinea capitis: Still an unsolved problem? Mycoses. 54:183–188. 2011. View Article : Google Scholar
19	Baldo A, Mathy A, Tabart J, Camponova P, Vermout S, Massart L, Maréchal F, Galleni M and Mignon B: Secreted subtilisin Sub3 from Microsporum canis is required for adherence to but not for invasion of the epidermis. Br J Dermatol. 162:990–997. 2010. View Article : Google Scholar
20	Băguţ ET, Baldo A, Mathy A, Cambier L, Antoine N, Cozma V and Mignon B: Subtilisin Sub3 is involved in adherence of Microsporum canis to human and animal epidermis. Vet Microbiol. 160:413–419. 2012. View Article : Google Scholar
21	Baldo A, Chevigné A, Dumez ME, Mathy A, Power P, Tabart J, Cambier L, Galleni M and Mignon B: Inhibition of the kerati-nolytic subtilisin protease Sub3 from Microsporum canis by its propeptide (proSub3) and evaluation of the capacity of proSub3 to inhibit fungal adherence to feline epidermis. Vet Microbiol. 159:479–484. 2012. View Article : Google Scholar : PubMed/NCBI
22	Shi Y, Niu Q, Yu X, Jia X, Wang J, Lin D and Jin Y: Assessment of the function of SUB6 in the pathogenic dermatophyte. Trichophyton mentagrophytes Med Mycol. 54:59–71. 2016.
23	Grumbt M, Monod M, Yamada T, Hertweck C, Kunert J and Staib P: Keratin degradation by dermatophytes relies on cysteine dioxygenase and a sulfite efflux pump. J Invest Dermatol. 133:1550–1555. 2013. View Article : Google Scholar : PubMed/NCBI
24	Mathy A, Baldo A, Schoofs L, Cambier L, Defaweux V, Tabart J, Maréchal F, Symoens F and Mignon B: Fungalysin and dipeptidyl-peptidase gene transcription in Microsporum canis strains isolated from symptomatic and asymptomatic cats. Vet Microbiol. 146:179–182. 2010. View Article : Google Scholar : PubMed/NCBI
25	Nakayashiki H: RNA silencing in fungi: Mechanisms and applications. FEBS Lett. 579:5950–5957. 2005. View Article : Google Scholar : PubMed/NCBI
26	Zhang FR, Zhang Y, Zhang ZY, Yang GL, Jing LJ and Bai YG: Analysis of the differentially expressed genes in Microsporum canis in inducing smooth skin and scalp tissue conditions. Clin Exp Dermatol. 36:896–902. 2011. View Article : Google Scholar : PubMed/NCBI
27	Gräser Y, EI Fari M, Vilgalys R, Kuijpers AF, De Hoog GS, Presber W and Tietz H: Phylogeny and taxonomy of the family arthrodermataceae (dermatophytes) using sequence analysis of the ribosomal ITS region. Med Mycol. 37:105–114. 1999. View Article : Google Scholar : PubMed/NCBI
28	Jackson CJ, Barton RC and Evans EG: Species identification and strain differentiation of dermatophyte fungi by analysis of ribosomal-DNA intergenic spacer regions. J Clin Microbiol. 37:931–936. 1999.PubMed/NCBI
29	Zhang Z, Hou B, Wu YZ, Wang Y, Liu X and Han S: Two component histidine kinase DRK1 is required for pathogenesis in sporothrix schenckii. Mol Med Rep. 17:721–728. 2018.
30	Zhang P, Xu B, Wang Y, Li Y, Qian Z, Tang S, Huan S and Ren S: Agrobacterium tumefaciens-mediated transformation as a tool for insertional mutagenesis in the fungus penicillium marneffei. Mycol Res. 112:943–949. 2008. View Article : Google Scholar : PubMed/NCBI
31	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar
32	Basma AA, Zuraini Z and Sasidharan SA: Transmission electron microscopy study of the diversity of Candida albicans cells induced by Euphorbia hirta L. Leaf extract in vitro Asian Pac J Trop Biomed. 1:20–22. 2011. View Article : Google Scholar
33	Wang F, Tao J, Qian Z, You S, Dong H, Shen H, Chen X, Tang S and Ren S: A histidine kinase PmHHK1 regulates polar growth, sporulation and cell wall composition in the dimorphic fungus Penicillium marneffei. Mycol Res. 113:915–923. 2009. View Article : Google Scholar : PubMed/NCBI
34	Jin XJ, Wang AP, Qiao JJ, Liu W, Wan J, Wang XH, Wu LS and Li RY: Establishment of an animal model of dermatophytosis and evaluation of the antifungal efficacy on dermatophytosis with this model. Chin J Dermatol. 42:125–128. 2009.In Chinese.
35	Silverman J and Muir WW III: A review of laboratory animal anesthesia with chloral hydrate and chloralose. Lab Anim Sci. 43:210–216. 1993.PubMed/NCBI
36	Olszewski J: Guinea pig as often object to otoneurological experimental examinations. Otolaryngol Pol. 61:838–841. 2007.In Polish. View Article : Google Scholar
37	Mao N, Gao Q, Hu H, Zhu T and Hao L: BPA disrupts the cardio-protection by 17β-oestradiol against ischemia/reperfusion injury in isolated guinea pig hearts. Steroids. 146:50–56. 2019. View Article : Google Scholar : PubMed/NCBI
38	Zhou Y, Song J, Wang YP, Zhang AM, Tan CY, Liu YH, Zhang ZP, Wang Y, Ma KT, Li L and Si JQ: Age-associated variation in the expression and function of TMEM16A calcium-activated chloride channels in the cochlear stria vascularis of guinea pigs. Mol Med Rep. 20:1593–1604. 2019.PubMed/NCBI
39	Vermout S, Tabart J, Baldo A, Monod M, Losson B and Mignon B: RNA silencing in the dermatophyte Microsporum canis. FEMS Microbiol Lett. 275:38–45. 2007. View Article : Google Scholar : PubMed/NCBI
40	Quevillon-Cheruel S, Leulliot N, Graille M, Hervouet N, Coste F, Bénédetti H, Zelwer C, Janin J and Van Tilbeurgh H: Crystal structure of yeast YHR049W/FSH1, a member of the serine hydrolase family. Protein Sci. 14:1350–1356. 2005. View Article : Google Scholar : PubMed/NCBI
41	Baxter SM, Rosenblum JS, Knutson S, Nelson MR, Montimurro JS, Di Gennaro JA, Speir JA, Burbaum JJ and Fetrow JS: Synergistic computational and experimental proteomics approaches for more accurate detection of active serine hydrolases in yeast. Mol Cell Proteomics. 3:209–225. 2004. View Article : Google Scholar
42	Gang L, Wei C, Yuqing T, Huarong T, Chater KF and Buttner MJ: A novel gene: sawD related to the differentiation of streptomyces ansochromogenes. Chin J Biotechnol. 15:195–202. 1999.
43	Greenberg JH, King RD, Krebs S and Field R: A quantitative dermatophyte infection model in the guinea pig-a parallel to the quantitated human infection model. J Invest Dermatol. 67:704–708. 1976. View Article : Google Scholar : PubMed/NCBI
44	Zhang X, Wang Y, Chi W, Shi Y, Chen S, Lin D and Jin Y: Metalloprotease genes of Trichophyton mentagrophytes are important for pathogenicity. Med Mycol. 52:36–45. 2014.