Dynamic Observation of Morphological Changes of in Pathogenic Molds Induced by the Antifungal Effects of Isavuconazole
The pathogenesis of invasive mycosis caused by filamentous fungi is closely associated with tissue damage resulting from hyphal elongation. The morphological changes that occur during hyphal cell death induced by antifungal drugs, however, have not been extensively investigated. In this study, we cu...
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| Published in | Nihon Ishinkin Gakkai Zasshi Vol. 64; no. 1; pp. 1 - 15 |
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| Main Authors | , , |
| Format | Journal Article |
| Language | Japanese |
| Published |
The Japanese Society for Medical Mycology
2023
一般社団法人 日本医真菌学会 |
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| Online Access | Get full text |
| ISSN | 2434-5229 2434-5237 |
| DOI | 10.11534/ishinkin.22-00022 |
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| Abstract | The pathogenesis of invasive mycosis caused by filamentous fungi is closely associated with tissue damage resulting from hyphal elongation. The morphological changes that occur during hyphal cell death induced by antifungal drugs, however, have not been extensively investigated. In this study, we cultured Aspergillus fumigatus and Rhizopus oryzae, two representative pathogenic molds, in the presence of isavuconazole and performed dynamic and detailed observations of morphological alterations in their hyphae. We observed cessation of hyphal elongation, degeneration of the cell membrane, and a continuous decrease in the fluidity of the intracellular matrix in both species. As evaluated by propidium iodide positivity, hyphal cell viability was reduced by 96.8% and 100% in A. fumigatus and R. oryzae, respectively. These results suggest that morphological changes in hyphae induced by isavuconazole result in cell death. |
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| AbstractList | The pathogenesis of invasive mycosis caused by filamentous fungi is closely associated with tissue damage resulting from hyphal elongation. The morphological changes that occur during hyphal cell death induced by antifungal drugs, however, have not been extensively investigated. In this study, we cultured Aspergillus fumigatus and Rhizopus oryzae, two representative pathogenic molds, in the presence of isavuconazole and performed dynamic and detailed observations of morphological alterations in their hyphae. We observed cessation of hyphal elongation, degeneration of the cell membrane, and a continuous decrease in the fluidity of the intracellular matrix in both species. As evaluated by propidium iodide positivity, hyphal cell viability was reduced by 96.8% and 100% in A. fumigatus and R. oryzae, respectively. These results suggest that morphological changes in hyphae induced by isavuconazole result in cell death.
糸状菌による侵襲性真菌症の病態には菌糸の伸長による組織傷害が深くかかわっている．しかし，抗真菌薬により菌糸の細胞死が誘導される過程で生ずる形態変化についてはほとんど解析されていない．本研究では，イサブコナゾール（ISCZ）存在下で代表的な病原糸状菌であるAspergillus fumigatus およびRhizopus oryzaeを培養し，両者における菌糸形態に関する動的かつ詳細な観察を行った．この結果，両糸状菌の菌糸がISCZの作用により伸長停止，細胞膜の変性および細胞内基質の流動性の連続的低下を起こすことを確認した．さらに両糸状菌でみられた菌糸の経時的な形態変化の終末像である不整膨化や細胞の壁構造の破綻は，伸長停止した菌糸先端部で生じた変性した微小器官の凝集による細胞内基質流路の狭窄・閉塞による局所的な内圧上昇に起因すると推定された．Propidium iodide陽性化率で評価した生存活性の消失率は，試験した菌株でA. fumigatus で96.8％，R. oryzaeでは100％であり，以上の変化はISCZにより細胞死に向かう過程で誘導されるものと考えられる． The pathogenesis of invasive mycosis caused by filamentous fungi is closely associated with tissue damage resulting from hyphal elongation. The morphological changes that occur during hyphal cell death induced by antifungal drugs, however, have not been extensively investigated. In this study, we cultured Aspergillus fumigatus and Rhizopus oryzae, two representative pathogenic molds, in the presence of isavuconazole and performed dynamic and detailed observations of morphological alterations in their hyphae. We observed cessation of hyphal elongation, degeneration of the cell membrane, and a continuous decrease in the fluidity of the intracellular matrix in both species. As evaluated by propidium iodide positivity, hyphal cell viability was reduced by 96.8% and 100% in A. fumigatus and R. oryzae, respectively. These results suggest that morphological changes in hyphae induced by isavuconazole result in cell death. |
| Author | Miyazaki, Shun Shibuya, Kazutoshi Tomita, Tsutomu |
| Author_FL | 宮﨑 俊 澁谷 和俊 富田 勉 |
| Author_FL_xml | – sequence: 1 fullname: 富田 勉 – sequence: 2 fullname: 宮﨑 俊 – sequence: 3 fullname: 澁谷 和俊 |
| Author_xml | – sequence: 1 fullname: Shibuya, Kazutoshi organization: Department of Surgical Pathology, Toho University Faculty School of Medicine – sequence: 1 fullname: Tomita, Tsutomu organization: Timelapse Vision Inc – sequence: 1 fullname: Miyazaki, Shun organization: Timelapse Vision Inc |
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| References | 17) Maertens JA, Raad II, Marr KA, et al: Isavuconazole versus voriconazole for primary treatment of invasive mould disease caused by Aspergillus and other filamentous fungi (SECURE): a phase 3, randomised-controlled, non-inferiority trial. Lancet 387: 760–769, 2016. 34）Hernández-González M, Bravo-Plaza I, Pinar M, de Los Ríos V, Arst HN Jr, Peñalva MA: Endocytic recycling via the TGN underlies the polarized hyphal mode of life. PLoS Genet 14: e1007291, 2018. 13) Spellberg B, Walsh TJ, Kontoyiannis DP, Edwards J Jr, Ibrahim AS: Recent advances in the management of mucormycosis: from bench to bedside. Clin Infect Dis 48: 1743–1751, 2009. 25) Rex JH, Alexander BD, Andes D, Arthington-Skaggs B, Brown SD, Chaturveli V, Espinel-Ingroff A, Ghannoum MA, Knapp CC, Motyl MR, Ostrosky-Zeichner L, Pfaller M, Sheehan DJ, Walsh TJ: Reference method for broth dilution antifungal susceptibility testing of filamentous fungi: Approved standard, 2nd ed. CSLI M38-A2. Clinical and Laboratory Standards Institute, 2008. 9) Jørgensen KM, Astvad KMT, Hare RK, Arendrup MC: EUCAST susceptibility testing of isavuconazole: MIC data for contemporary clinical mold and yeast isolates. Antimicrob Agents Chemother 63: e00073-19, 2019. 39) Roehm NW, Rodgers GH, Hatfield SM, Glasebrook AL: An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT. J Immunol Methods 142: 257–265, 1991. 26) Abràmoff MD, Magalhães PJ, Ram SJ: Image processing with imageJ. Biophotonics International 11: 36–42, 2004. 23) Natesan SK, Chandrasekar PH: Isavuconazole for the treatment of invasive aspergillosis and mucormycosis: current evidence, safety, efficacy, and clinical recommendations. Infect Drug Resist 9: 291–300, 2016. 8) Patterson TF, Thompson GR 3rd, Denning DW, et al: Practice guidelines for the diagnosis and management of aspergillosis: 2016 update by the Infectious Diseases Society of America. Clin Infect Dis 63: e1–e60, 2016. 40) Kuhn DM, Balkis M, Chandra J, Mukherjee PK, Ghannoum MA: Uses and limitations of the XTT assay in studies of Candida growth and metabolism. J Clin Microbiol 41: 506–508, 2003. 22) Risum M, Vestergaard MB, Weinreich UM, Helleberg M, Vissing NH, Jørgensen R: Therapeutic drug monitoring of isavuconazole: serum concentration variability and success rates for reaching target in comparison with voriconazole. Antibiotics (Basel) 10: 487, 2021. 33) Faoro F, Faccio A, Balestrini R: Contributions of ultrastructural studies to the knowledge of filamentous fungi biology and fungi-plant interactions. Front Fungal Biol 2: 805739, 2022. 6) 深在性真菌症のガイドライン作成委員会：深在性真菌症の診断・治療ガイドライン2014，pp.71–72，協和企画，東京，2014. 35) 溜池あかね，許斐麻美，佐藤眞美子，石島早苗，庭野吉己，大隅正子：抗真菌剤ラノコナゾールのTrichophyton rubrum発育菌糸細胞壁に及ぼす影響の電子顕微鏡学的研究．真菌誌37: 251–261, 1996. 4) 渋谷和俊，若山 恵，富田 勉，小澤英治，内田勝久，山口英世，直江史郎：ラット生体の腸間膜に接種したAspergillus fumigatusの組織侵襲過程に関する位相差顕微鏡による連続的観察．真菌誌34: 365–371, 1993. 30) Bossche HV: Biochemical targets for antifungal azole derivatives: hypothesis on the mode of action. In Current Topics in Medical Mycology (McGinnis MR ed), pp.313–351, Springer, New York, 1985. 27) Espinel-Ingroff A, Chowdhary A, Gonzalez GM, Lass-Flörl C, Martin-Mazuelos E, Meis J, Peláez T, Pfaller MA, Turnidge J: Multicenter study of isavuconazole MIC distributions and epidemiological cutoff values for Aspergillus spp. for the CLSI M38-A2 broth microdilution method. Antimicrob Agents Chemother 57: 3823–3828, 2013. 28) Vanden BH: Mode of action of pyridine, pyrimidine and azole antifungals. In Sterol biosynthesis inhibitors (Berg D, Plempel M ed), pp. 78–119, Ellis Horwood, Chichester, 1998. 29) Georgopapadakou NH, Walsh TJ: Antifungal agents: chemotherapeutic targets and immunologic strategies. Antimicrob Agents Chemother 40: 279–291, 1996. 14) Personett HA, Kayhart BM, Barreto EF, Tosh P, Dierkhising R, Mara K, Leung N: Renal recovery following liposomal amphotericin B-induced nephrotoxicity. Int J Nephrol 2019: 8629891, 2019. 11) Park BJ, Pappas PG, Wannemuehler KA, et al: Invasive non-Aspergillus mold infections in transplant recipients, United States, 2001–2006. Emerg Infect Dis 17: 1855–1864, 2011. 3) Cornely OA, Alastruey-Izquierdo A, Arenz D, et al: Global guideline for the diagnosis and management of mucormycosis: an initiative of the European Confederation of Medical Mycology in cooperation with the Mycoses Study Group Education and Research Consortium. Lancet Infect Dis 19: e405–e421, 2019. 24) Luo G, Gebremariam T, Lee H, Edwards JE Jr, Kovanda L, Ibrahim AS: Isavuconazole therapy protects immunosuppressed mice from mucormycosis. Antimicrob Agents Chemother 58: 2450–2453, 2014. 1) 神田善伸：血液疾患における侵襲性真菌症診療．日化療会誌62: 605–612, 2014. 12) Lewis RE, Lortholary O, Spellberg B, Roilides E, Kontoyiannis DP, Walsh TJ: How does antifungal pharmacology differ for mucormycosis versus aspergillosis? Clin Infect Dis 54 (suppl 1): S67–S72, 2012. 7) 木村俊一：血液領域における侵襲性アスペルギルス症. Med Mycol J 57: J77–J88, 2016. 32) 本山高幸, 堀内裕之, 高木正道：カビの細胞壁形成の分子生物学：キチンの合成・分解に関わる遺伝子を中心に．化学と生物 31: 807–816, 1993. 37) Geiβel B, Loiko V, Klugherz I, Zhu Z, Wagener N, Kurzai O, van den Hondel CAMJJ, Wagener J: Azole-induced cell wall carbohydrate patches kill Aspergillus fumigatus. Nat Commun 9: 3098, 2018. 38) Dengler WA, Schulte J, Berger DP, Mertelsmann R, Fiebig HH: Development of a propidium iodide fluorescence assay for proliferation and cytotoxicity assays. Anticancer Drugs 6: 522–532, 1995. 19) Marty FM, Ostrosky-Zeichner L, Cornely OA, et al: Isavuconazole treatment for mucormycosis: a single-arm open-label trial and case-control analysis. Lancet Infect Dis 16: 828–837, 2016. 5) Kume H, Yamazaki T, Togano T, Abe M, Tanuma H, Kawana S, Okudaira M: Epidemiology of visceral mycosis in autopsy case in Japan: comparison of the data from 1989, 1993, 1997, 2001, 2005 and 2007 in Annual of Pathological Autopsy Case in Japan. Med Mycol J 52: 117–127, 2011. 31) Ruge E, Korting HC, Borelli C: Current state of three-dimensional characterisation of antifungal targets and its use for molecular modelling in drug design. Int J Antimicrob Agents 26: 427–441, 2005. 36) 西山彌生：抗真菌薬の作用メカニズムと病原真菌の微細構造の変化. Med Mycol J 53: 233–239, 2012. 18) Arendrup MC, Jensen RH, Meletiadis J: In vitro activity of isavuconazole and comparators against clinical isolates of the Mucorales order. Antimicrob Agents Chemother 59: 7735–7742, 2015. 10) Jing R, Morrissey I, Xiao M, Sun TS, Zhang G, Kang W, Guo DW, Aram JA, Wang J, Utt EA, Wang Y, Xu YC: In vitro activity of isavuconazole and comparators against clinical isolates of molds from a multicenter study in China. Infect Drug Resist 15: 2101–2113, 2022. 16) Dagher H, Hachem R, Chaftari AM, Jiang Y, Ali S, Deeba R, Shah S, Raad I: Real-world use of isavuconazole as primary therapy for invasive fungal infections in high-risk patients with hematologic malignancy or stem cell transplant. J Fungi 8: 74, 2022. 20) Andes D, Kovanda L, Desai A, Kitt T, Zhao M, Walshc TJ: Isavuconazole concentration in real-world practice: consistency with results from clinical trials. Antimicrob Agents Chemother 62: e00585-18, 2018. 21) Kosmidis C, Otu A, Moore CB, Richardson MD, Rautemaa-Richardson R: Isavuconazole therapeutic drug monitoring during long-term treatment for chronic pulmonary aspergillosis. Antimicrob Agents Chemother 65: e01511-20, 2020. 15）CRESEMBA® [package insert]. Northbrook, IL: Astellas Pharma US, Inc. (High lights of prescribing information, Reference ID: 3712237) 2) 安藤常浩：呼吸器領域におけるアスペルギルス症に対する診療指針．日化療会誌62: 657–662, 2014. |
| References_xml | – reference: 16) Dagher H, Hachem R, Chaftari AM, Jiang Y, Ali S, Deeba R, Shah S, Raad I: Real-world use of isavuconazole as primary therapy for invasive fungal infections in high-risk patients with hematologic malignancy or stem cell transplant. J Fungi 8: 74, 2022. – reference: 4) 渋谷和俊，若山 恵，富田 勉，小澤英治，内田勝久，山口英世，直江史郎：ラット生体の腸間膜に接種したAspergillus fumigatusの組織侵襲過程に関する位相差顕微鏡による連続的観察．真菌誌34: 365–371, 1993. – reference: 1) 神田善伸：血液疾患における侵襲性真菌症診療．日化療会誌62: 605–612, 2014. – reference: 40) Kuhn DM, Balkis M, Chandra J, Mukherjee PK, Ghannoum MA: Uses and limitations of the XTT assay in studies of Candida growth and metabolism. J Clin Microbiol 41: 506–508, 2003. – reference: 20) Andes D, Kovanda L, Desai A, Kitt T, Zhao M, Walshc TJ: Isavuconazole concentration in real-world practice: consistency with results from clinical trials. Antimicrob Agents Chemother 62: e00585-18, 2018. – reference: 35) 溜池あかね，許斐麻美，佐藤眞美子，石島早苗，庭野吉己，大隅正子：抗真菌剤ラノコナゾールのTrichophyton rubrum発育菌糸細胞壁に及ぼす影響の電子顕微鏡学的研究．真菌誌37: 251–261, 1996. – reference: 3) Cornely OA, Alastruey-Izquierdo A, Arenz D, et al: Global guideline for the diagnosis and management of mucormycosis: an initiative of the European Confederation of Medical Mycology in cooperation with the Mycoses Study Group Education and Research Consortium. Lancet Infect Dis 19: e405–e421, 2019. – reference: 14) Personett HA, Kayhart BM, Barreto EF, Tosh P, Dierkhising R, Mara K, Leung N: Renal recovery following liposomal amphotericin B-induced nephrotoxicity. Int J Nephrol 2019: 8629891, 2019. – reference: 22) Risum M, Vestergaard MB, Weinreich UM, Helleberg M, Vissing NH, Jørgensen R: Therapeutic drug monitoring of isavuconazole: serum concentration variability and success rates for reaching target in comparison with voriconazole. Antibiotics (Basel) 10: 487, 2021. – reference: 10) Jing R, Morrissey I, Xiao M, Sun TS, Zhang G, Kang W, Guo DW, Aram JA, Wang J, Utt EA, Wang Y, Xu YC: In vitro activity of isavuconazole and comparators against clinical isolates of molds from a multicenter study in China. Infect Drug Resist 15: 2101–2113, 2022. – reference: 11) Park BJ, Pappas PG, Wannemuehler KA, et al: Invasive non-Aspergillus mold infections in transplant recipients, United States, 2001–2006. Emerg Infect Dis 17: 1855–1864, 2011. – reference: 25) Rex JH, Alexander BD, Andes D, Arthington-Skaggs B, Brown SD, Chaturveli V, Espinel-Ingroff A, Ghannoum MA, Knapp CC, Motyl MR, Ostrosky-Zeichner L, Pfaller M, Sheehan DJ, Walsh TJ: Reference method for broth dilution antifungal susceptibility testing of filamentous fungi: Approved standard, 2nd ed. CSLI M38-A2. Clinical and Laboratory Standards Institute, 2008. – reference: 2) 安藤常浩：呼吸器領域におけるアスペルギルス症に対する診療指針．日化療会誌62: 657–662, 2014. – reference: 18) Arendrup MC, Jensen RH, Meletiadis J: In vitro activity of isavuconazole and comparators against clinical isolates of the Mucorales order. Antimicrob Agents Chemother 59: 7735–7742, 2015. – reference: 27) Espinel-Ingroff A, Chowdhary A, Gonzalez GM, Lass-Flörl C, Martin-Mazuelos E, Meis J, Peláez T, Pfaller MA, Turnidge J: Multicenter study of isavuconazole MIC distributions and epidemiological cutoff values for Aspergillus spp. for the CLSI M38-A2 broth microdilution method. Antimicrob Agents Chemother 57: 3823–3828, 2013. – reference: 29) Georgopapadakou NH, Walsh TJ: Antifungal agents: chemotherapeutic targets and immunologic strategies. Antimicrob Agents Chemother 40: 279–291, 1996. – reference: 17) Maertens JA, Raad II, Marr KA, et al: Isavuconazole versus voriconazole for primary treatment of invasive mould disease caused by Aspergillus and other filamentous fungi (SECURE): a phase 3, randomised-controlled, non-inferiority trial. Lancet 387: 760–769, 2016. – reference: 37) Geiβel B, Loiko V, Klugherz I, Zhu Z, Wagener N, Kurzai O, van den Hondel CAMJJ, Wagener J: Azole-induced cell wall carbohydrate patches kill Aspergillus fumigatus. Nat Commun 9: 3098, 2018. – reference: 34）Hernández-González M, Bravo-Plaza I, Pinar M, de Los Ríos V, Arst HN Jr, Peñalva MA: Endocytic recycling via the TGN underlies the polarized hyphal mode of life. PLoS Genet 14: e1007291, 2018. – reference: 9) Jørgensen KM, Astvad KMT, Hare RK, Arendrup MC: EUCAST susceptibility testing of isavuconazole: MIC data for contemporary clinical mold and yeast isolates. Antimicrob Agents Chemother 63: e00073-19, 2019. – reference: 28) Vanden BH: Mode of action of pyridine, pyrimidine and azole antifungals. In Sterol biosynthesis inhibitors (Berg D, Plempel M ed), pp. 78–119, Ellis Horwood, Chichester, 1998. – reference: 24) Luo G, Gebremariam T, Lee H, Edwards JE Jr, Kovanda L, Ibrahim AS: Isavuconazole therapy protects immunosuppressed mice from mucormycosis. Antimicrob Agents Chemother 58: 2450–2453, 2014. – reference: 23) Natesan SK, Chandrasekar PH: Isavuconazole for the treatment of invasive aspergillosis and mucormycosis: current evidence, safety, efficacy, and clinical recommendations. Infect Drug Resist 9: 291–300, 2016. – reference: 32) 本山高幸, 堀内裕之, 高木正道：カビの細胞壁形成の分子生物学：キチンの合成・分解に関わる遺伝子を中心に．化学と生物 31: 807–816, 1993. – reference: 36) 西山彌生：抗真菌薬の作用メカニズムと病原真菌の微細構造の変化. Med Mycol J 53: 233–239, 2012. – reference: 13) Spellberg B, Walsh TJ, Kontoyiannis DP, Edwards J Jr, Ibrahim AS: Recent advances in the management of mucormycosis: from bench to bedside. Clin Infect Dis 48: 1743–1751, 2009. – reference: 7) 木村俊一：血液領域における侵襲性アスペルギルス症. Med Mycol J 57: J77–J88, 2016. – reference: 39) Roehm NW, Rodgers GH, Hatfield SM, Glasebrook AL: An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT. J Immunol Methods 142: 257–265, 1991. – reference: 8) Patterson TF, Thompson GR 3rd, Denning DW, et al: Practice guidelines for the diagnosis and management of aspergillosis: 2016 update by the Infectious Diseases Society of America. Clin Infect Dis 63: e1–e60, 2016. – reference: 12) Lewis RE, Lortholary O, Spellberg B, Roilides E, Kontoyiannis DP, Walsh TJ: How does antifungal pharmacology differ for mucormycosis versus aspergillosis? Clin Infect Dis 54 (suppl 1): S67–S72, 2012. – reference: 31) Ruge E, Korting HC, Borelli C: Current state of three-dimensional characterisation of antifungal targets and its use for molecular modelling in drug design. Int J Antimicrob Agents 26: 427–441, 2005. – reference: 26) Abràmoff MD, Magalhães PJ, Ram SJ: Image processing with imageJ. Biophotonics International 11: 36–42, 2004. – reference: 5) Kume H, Yamazaki T, Togano T, Abe M, Tanuma H, Kawana S, Okudaira M: Epidemiology of visceral mycosis in autopsy case in Japan: comparison of the data from 1989, 1993, 1997, 2001, 2005 and 2007 in Annual of Pathological Autopsy Case in Japan. Med Mycol J 52: 117–127, 2011. – reference: 6) 深在性真菌症のガイドライン作成委員会：深在性真菌症の診断・治療ガイドライン2014，pp.71–72，協和企画，東京，2014. – reference: 38) Dengler WA, Schulte J, Berger DP, Mertelsmann R, Fiebig HH: Development of a propidium iodide fluorescence assay for proliferation and cytotoxicity assays. 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| Title | Dynamic Observation of Morphological Changes of in Pathogenic Molds Induced by the Antifungal Effects of Isavuconazole |
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