Paracoccidioides brasiliensis plasma membrane characterization by EPR spectroscopy and interactions with amphotericin B, miltefosine and nerolidol

References

• AbouLaila, M., Sivakumar, T., Yokoyama, N., & Igarashi, I. (2010). Inhibitory effect of terpene nerolidol on the growth of Babesia parasites. Parasitology International, 59(2), 278–282. https://doi.org/10.1016/j.parint.2010.02.006
   PubMed Web of Science ®Google Scholar
• Alonso, L., Cardoso, E. J. S., Mendanha, S. A., & Alonso, A. (2019a). Interactions of miltefosine with erythrocyte membrane proteins compared to those of ionic surfactants. Colloids and Surfaces B Biointerfaces, 180, 23–30. https://doi.org/10.1016/j.colsurfb.2019.04.040
   PubMed Web of Science ®Google Scholar
• Alonso, L., Cardoso, É. J. S., Gomes, R. S., Mendanha, S. A., Dorta, M. L., & Alonso, A. (2019b). Antileishmanial and cytotoxic activities of ionic surfactants compared to those of miltefosine. Colloids and Surfaces B Biointerfaces, 183, 110421. https://doi.org/10.1016/j.colsurfb.2019.110421
   PubMed Web of Science ®Google Scholar
• Alonso, L., de Paula, J. C., Baréa, P., Sarragiotto, M. H., Nakamura, T. U., Alonso, A., Fernandes, N. S., Lancheros, C. A. C., Volpato, H., Bidóia, D. L., & Nakamura, C. V. (2021a). Membrane dynamics in Leishmania amazonensis and antileishmanial activities of β-carboline derivatives. Biochimica Et Biophysica Acta. Biomembranes, 1863(1), 183473. https://doi.org/10.1016/j.bbamem.2020.183473
   PubMed Web of Science ®Google Scholar
• Alonso, L., Fernandes, K. S., Mendanha, S. A., Gonçalves, P. J., Gomes, R. S., Dorta, M. L., & Alonso, A. (2019c). In vitro antileishmanial and cytotoxic activities of nerolidol are associated with changes in plasma membrane dynamics. Biochimica Et Biophysica Acta. Biomembranes, 1861(6), 1049–1056. https://doi.org/10.1016/j.bbamem.2019.03.006
   PubMed Web of Science ®Google Scholar
• Alonso, L., Mendanha, S. A., Dorta, M. L., & Alonso, A. (2020a). Analysis of the interactions of amphotericin B with the leishmania plasma membrane using EPR spectroscopy. The Journal of Physical Chemistry B, 124(45), 10157–10165. https://doi.org/10.1021/acs.jpcb.0c07721
   PubMed Web of Science ®Google Scholar
• Alonso, L., Mendanha, S. A., Gomes, R. S., Dorta, M. L., & Alonso, A. (2021b). Comparative EPR spectroscopy analysis of amphotericin B and miltefosine interactions with Leishmania, erythrocyte and macrophage membranes. European Journal of Pharmaceutical Sciences, 163, 105859. https://doi.org/10.1016/j.ejps.2021.105859
   PubMed Web of Science ®Google Scholar
• Alonso, L., Menegatti, R., Gomes, R. S., Dorta, M. L., Luzin, R. M., Lião, L. M., & Alonso, A. (2020b). Antileishmanial activity of the chalcone derivative LQFM064 associated with reduced fluidity in the parasite membrane as assessed by EPR spectroscopy. European Journal of Pharmaceutical Sciences, 151, 105407. https://doi.org/10.1016/j.ejps.2020.105407
   PubMed Web of Science ®Google Scholar
• Alonso, L., Pimenta, L. K. L., Kipnis, A., & Alonso, A. (2022). Mycobacterium abscessus cell wall and plasma membrane characterization by EPR spectroscopy and effects of amphotericin B, miltefosine and nerolidol. Biochimica et Biophysica Acta Biomembranes, 1864(5), 183872. https://doi.org/10.1016/j.bbamem.2022.183872
   PubMed Web of Science ®Google Scholar
• Anderson, T. M., Clay, M. C., Cioffi, A. G., Diaz, K. A., Hisao, G. S., Tuttle, M. D., Nieuwkoop, A. J., Comellas, G., Maryum, N., Wang, S., Uno, B. E., Wildeman, E. L., Gonen, T., Rienstra, C. M., & Burke, M. D. (2014). Amphotericin forms an extramembranous and fungicidal sterol sponge. Nature Chemical Biology, 10(5), 400–406. https://doi.org/10.1038/nchembio.1496
   PubMed Web of Science ®Google Scholar
• Anjos, J. L. V. D., Neto, D. d S., & Alonso, A. (2007). Effects of 1,8-cineole on the dynamics of lipids and proteins of stratum corneum. International Journal of pharmaceutics, 345(1–2), 81–87. https://doi.org/10.1016/j.ijpharm.2007.05.041
   PubMed Web of Science ®Google Scholar
• Arruda, D., D'Alexandri, F., Katzin, A., & Uliana, S. (2005). Antileishmanial activity of the terpene Nerolidol. Antimicrobial Agents and Chemotherapy, 49(5), 1679–1687. https://doi.org/10.1128/AAC.49.5.1679-1687.2005
   PubMed Web of Science ®Google Scholar
• Barreto, T. L., Rossato, L., de Freitas, A. L. D., Meis, J. F., Lopes, L. B., Colombo, A. L., & Ishida, K. (2020). Miltefosine as an alternative strategy in the treatment of the emerging fungus Candida auris. International Journal of Antimicrobial Agents, 56(2), 106049. https://doi.org/10.1016/j.ijantimicag.2020.106049
   PubMed Web of Science ®Google Scholar
• Brummer, E., Castaneda, E., & Restrepo, A. (1993). Paracoccidioidomycosis: an update. Clinical Microbiology Reviews, 6(2), 89–117. https://doi.org/10.1128/CMR.6.2.89
   PubMed Web of Science ®Google Scholar
• Budil, D. E., Sanghyuk, L., Saxena, S., & Freed, J. H. (1996). Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm. Journal of Magnetic Resononace Series A, 120(2), 155–189. https://doi.org/10.1006/jmra.1996.0113
   Web of Science ®Google Scholar
• Camargos, H. S., Moreira, R. A., Mendanha, S. A., Fernandes, K. S., Dorta, M. L., & Alonso, A. (2014). Terpenes increase the lipid dynamics in the Leishmania plasma membrane at concentrations similar to their IC50 values. PLoS One, 9(8), e104429. https://doi.org/10.1371/journal.pone.0104429
   PubMed Web of Science ®Google Scholar
• Park, M. J., Gwak, K. S., Yang, I., Kim, K. W., Jeung, E. B., Chang, J. W., & Choi, I. G. (2009). Effect of citral, eugenol, nerolidol and alpha-terpineol on the ultrastructural changes of Trichophyton mentagrophytes. Fitoterapia, 80(5), 290–296. https://doi.org/10.1016/j.fitote.2009.03.007
   PubMed Web of Science ®Google Scholar
• de Curcio, J. S., Silva, M. G., Silva Bailão, M. G., Báo, S. N., Casaletti, L., Bailão, A. M., & de Almeida Soares, C. M. (2017). Identification of membrane proteome of Paracoccidioides lutzii and its regulation by zinc. Future Science OA, 3(4), FSO232. https://doi.org/10.4155/fsoa-2017-0044
   PubMedGoogle Scholar
• de Moura, D. F., Rocha, T. A., de Melo Barros, D., da Silva, M. M., Dos Santos Santana, M., Neta, B. M., Cavalcanti, I. M. F., Martins, R. D., & da Silva, M. V. (2021). Evaluation of the antioxidant, antibacterial, and antibiofilm activity of the sesquiterpene nerolidol. Archives of Microbiology, 203(7), 4303–4311. https://doi.org/10.1007/s00203-021-02377-5
   PubMed Web of Science ®Google Scholar
• do Carmo Silva, L., de Oliveira, A. A., de Souza, D. R., Barbosa, K. L. B., Freitas, E., Silva, K. S., Carvalho Júnior, M. A. B., Rocha, O. B., Lima, R. M., Santos, T. G., Soares, C. M. A., & Pereira, M. (2020a). Overview of antifungal drugs against Paracoccidioidomycosis: How do we start, where are we, and where are we going? Journal of Fungi, 6(4), 300. https://doi.org/10.3390/jof6040300
   Web of Science ®Google Scholar
• do Carmo Silva, L., Miranda, M. A. C. M., de Freitas, J. V., Ferreira, S. F. A., de Oliveira Lima, E. C., de Oliveira, C. M. A., Kato, L., Terezan, A. P., Rodriguez, A. F. R., Faria, F. S. E. D. V., de Almeida Soares, C. M., & Pereira, M. (2020b). Antifungal activity of Copaíba resin oil in solution and nanoemulsion against Paracoccidioides spp. Brazilian Journal of Microbiology, 51(1), 125–134. https://doi.org/10.1007/s42770-019-00201-3
   PubMed Web of Science ®Google Scholar
• Dorlo, T. P. C., Balasegaram, M., Beijnen, J. H., & de Vries, P. J. (2012). Miltefosine: A review of its pharmacology and therapeutic efficacy in the treatment of leishmaniasis. The Journal of Antimicrobial Chemotherapy, 67(11), 2576–2597. https://doi.org/10.1093/jac/dks275
   PubMed Web of Science ®Google Scholar
• dos Anjos, J. L., & Alonso, A. (2008). Terpenes increase the partitioning and molecular dynamics of an amphipathic spin label in stratum corneum membranes. International Journal of Pharmaceutics, 350(1–2), 103–112. https://doi.org/10.1016/j.ijpharm.2007.08.024
   PubMed Web of Science ®Google Scholar
• Eissa, M. M., El-Moslemany, R. M., Ramadan, A. A., Amer, E. I., El-Azzouni, M. Z., & El-Khordagui, L. K. (2015). Miltefosine lipid nanocapsules for single dose oral treatment of Schistosomiasis mansoni: A preclinical study. PLoS One, 10(11), e0141788. https://doi.org/10.1371/journal.pone.0141788
   PubMed Web of Science ®Google Scholar
• Fernandes, K. S., de Souza, P. E., Dorta, M. L., & Alonso, A. (2017). The cytotoxic activity of miltefosine against Leishmania and macrophages is associated with dynamic changes in plasma membrane proteins. Biochimica et Biophysica Acta Biomembranes, 1859(1), 1–9. https://doi.org/10.1016/j.bbamem.2016.10.008
   PubMed Web of Science ®Google Scholar
• Fleitas Martínez, O., Cardoso, M. H., Ribeiro, S. M., & Franco, O. L. (2019). Recent advances in anti-virulence therapeutic strategies with a focus on dismantling bacterial membrane microdomains, toxin neutralization, Quorum-Sensing interference and biofilm inhibition. Frontiers in Cellular and Infection Microbiology, 9, 74. https://doi.org/10.3389/fcimb.2019.00074
   PubMed Web of Science ®Google Scholar
• Fonseca Bezerra, C., de Alencar Júnior, J. G., de Lima Honorato, R., Dos Santos, A. T. L., Pereira da Silva, J. C., Silva, T. G. D., Leal, A. L. A. B., de Freitas, T. S., Vieira, T. A. T., Esmeraldo Rocha, J., Lima Sales, D., Barbosa Filho, J. M., Ribeiro de Sousa, G., Pinheiro, A. P., Ribeiro-Filho, J., Coutinho, H. D. M., Bezerra Morais-Braga, M. F., & da Silva, T. G. (2020). Antifungal properties of nerolidol-containing liposomes in association with fluconazole. Membranes (Basel), 10(9), 194. https://doi.org/10.3390/membranes10090194
   PubMed Web of Science ®Google Scholar
• Hoet, S., Stévigny, C., Hérent, M. F., & Quetin-Leclercq, J. (2006). Antitrypanosomal compounds from the leaf essential oil of Strychnos spinosa. Planta Medica, 5, 480–482.
   Google Scholar
• Johann, S., Oliveira, F. B., Siqueira, E. P., Cisalpino, P. S., Rosa, C. A., Alves, T. M., Zani, C. L., & Cota, B. B. (2012). Activity of compounds isolated from Baccharis dracunculifolia D.C. (Asteraceae) against Paracoccidioide brasiliensis. Medical Mycology. 8, 843–851.
   Google Scholar
• Kamiński, D. M. (2014). Recent progress in the study of the interactions of amphotericin B with cholesterol and ergosterol in lipid environments. European Biophysics Journal, 43(10–11), 453–467. https://doi.org/10.1007/s00249-014-0983-8
   PubMed Web of Science ®Google Scholar
• Kurad, D., Jeschke, G., & Marsh, D. (2003). Lipid membrane polarity profiles by high-field EPR. Biophysical Journal. 85(2), 1025–1033. https://doi.org/10.1016/S0006-3495(03)74541-X
   PubMed Web of Science ®Google Scholar
• Lacaz, C. S. (2018). Evolução histórica do conhecimento sobre a paracoccidioidomicose e seu agente etiológico, Paracoccidioides brasiliensis. Paracoccidioidomicose, 1–12. https://doi.org/10.1201/9781351075329-1
   Google Scholar
• Lee, S. J., Han, J. I., Lee, G. S., Park, M. J., Choi, I. G., Na, K. J., & Jeung, E. B. (2007). Antifungal effect of eugenol and nerolidol against Microsporum gypseum in a guinea pig model. Biological & Pharmaceutical Bulletin, 30(1), 184–188. https://doi.org/10.1248/bpb.30.184
   PubMed Web of Science ®Google Scholar
• Llull, D., Rivas, L., & García, E. (2007). In vitro bactericidal activity of the antiprotozoal drug miltefosine against Streptococcus pneumoniae and other pathogenic streptococci. Antimicrobial Agents and Chemotherapy, 51(5), 1844–1848. https://doi.org/10.1128/AAC.01428-06
   PubMed Web of Science ®Google Scholar
• Lorenzo-Morales, J., Khan, N. A., & Walochnik, J. (2015). An update on Acanthamoeba keratitis: Diagnosis, pathogenesis and treatment. Parasite (Paris, France), 22, 10. https://doi.org/10.1051/parasite/2015010
   PubMed Web of Science ®Google Scholar
• Marques, S. A. (2013). Paracoccidioidomycosis: epidemiological, clinical, diagnostic and treatment up-dating. Anais Brasileiros de Dermatologia, 88(5), 700–711. https://doi.org/10.1590/abd1806-4841.20132463
   PubMed Web of Science ®Google Scholar
• Maza, P. K., Straus, A. H., Toledo, M. S., Takahashi, H. K., & Suzuki, E. (2008). Interaction of epithelial cell membrane rafts with Paracoccidioides brasiliensis leads to fungal adhesion and Src-family kinase activation. Microbes and Infection, 10(5), 540–547. https://doi.org/10.1016/j.micinf.2008.02.004
   PubMed Web of Science ®Google Scholar
• Mendanha, S. A., & Alonso, A. (2015). Effects of terpenes on fluidity and lipid extraction in phospholipid membranes. Biophysical Chemistry, 198, 45–54. https://doi.org/10.1016/j.bpc.2015.02.001
   PubMed Web of Science ®Google Scholar
• Monforte, V., Ussetti, P., López, R., Gavaldà, J., Bravo, C., de Pablo, A., Pou, L., Pahissa, A., Morell, F., & Román, A. (2009). Nebulized liposomal amphotericin B prophylaxis for Aspergillus infection in lung transplantation: pharmacokinetics and safety. The Journal of Heart and Lung Transplantation, 28(2), 170–175. https://doi.org/10.1016/j.healun.2008.11.004
   PubMed Web of Science ®Google Scholar
• Moreira, A. P. V. (2008). Paracoccidioidomicose: Histórico, etiologia, epidemiologia, patogênese, formas clínicas, diagnóstico laboratorial e antígenos. Boletim Epidemiológico Paulista, 5, 11–24.
   Google Scholar
• Moreira, R. A., Mendanha, S. A., Fernandes, K. S., Matos, G. G., Alonso, L., Dorta, M. L., & Alonso, A. (2014). Miltefosine increases lipid and protein dynamics in Leishmania amazonensis membranes at concentrations similar to those needed for cytotoxicity activity. Antimicrobial Agents and Chemotherapy, 58(6), 3021–3028. https://doi.org/10.1128/AAC.01332-13
   PubMed Web of Science ®Google Scholar
• Pereira, A. O., Avila, J. M., Do Carmo, G., Siqueira, F. S., Campos, M. M. A., Back, D. F., Morel, A. F., & Dalcol, I. (2018). Chemical composition, antimicrobial and antimycobacterial activities of Aristolochia triangularis Cham. from Brazil. Industrial Crops and Products, 121, 461–467. https://doi.org/10.1016/j.indcrop.2018.05.052
   Web of Science ®Google Scholar
• Rossi, D. C. P., Spadari, C. C., Nosanchuk, J. D., Taborda, C. P., & Ishida, K. (2017). Miltefosine is fungicidal to Paracoccidioides Spp. yeast cells but subinhibitory concentrations induce melanisation. International Journal of Antimicrobial Agents, 49(4), 465–471. https://doi.org/10.1016/j.ijantimicag.2016.12.020
   PubMed Web of Science ®Google Scholar
• Saito, A. Y., Marin Rodriguez, A. A., Menchaca Vega, D. S., Sussmann, R. A. C., Kimura, E. A., & Katzin, A. M. (2016). Antimalarial activity of the terpene nerolidol. International Journal of Antimicrobial Agents, 48(6), 641–646. https://doi.org/10.1016/j.ijantimicag.2016.08.017
   PubMed Web of Science ®Google Scholar
• Shikanai-Yasuda, M. A., Mendes, R. P., Colombo, A. L., Queiroz-Telles, F., Kono, A. S. G., Paniago, A. M. M., Nathan, A., Valle, A. C. F. D., Bagagli, E., Benard, G., Ferreira, M. S., Teixeira, M. M., Silva-Vergara, M. L., Pereira, R. M., Cavalcante, R. S., Hahn, R., Durlacher, R. R., Khoury, Z., Camargo, Z. P., Moretti, M. L., & Martinez, R. (2017). Brazilian guidelines for the clinical management of paracoccidioidomycosis. Revista da Sociedade Brasileira de Medicina Tropical, 50(5), 715–740. https://doi.org/10.1590/0037-8682-0230-2017
   PubMed Web of Science ®Google Scholar
• Silva, L. C., Neves, B. J., Gomes, M. N., Melo-Filho, C. C., Soares, C. M., Andrade, C. H., & Pereira, M. (2018). Computer-aided identification of novel anti-paracoccidioidomycosis compounds. Future Microbiology, 13, 1523–1535. https://doi.org/10.2217/fmb-2018-0175
   PubMed Web of Science ®Google Scholar
• Stone, N. R., Bicanic, T., Salim, R., & Hope, W. (2016). Liposomal amphotericin B (AmBisome(®)): A review of the pharmacokinetics, pharmacodynamics, clinical experience and future directions. Drugs, 76(4), 485–500. https://doi.org/10.1007/s40265-016-0538-7
   PubMed Web of Science ®Google Scholar
• Takahagi-Nakaira, E., Sugizaki, M., & Peraçoli, M. (2009). Microdilution procedure for antifungal susceptibility testing of Paracoccidioides brasiliensis to amphotericin b and itraconazole. Journal of Venomous Animals and Toxins Including Tropical Diseases, 15(4), 718–731. https://doi.org/10.1590/S1678-91992009000400010
   Web of Science ®Google Scholar
• Thomas, N. S., & Panchagnula, R. (2003). Transdermal delivery of zidovudine: Effect of vehicles on permeation across rat skin and their mechanism of action. European Journal of Pharmaceutical Sciences. 18(1), 71–79. https://doi.org/10.1016/S0928-0987(02)00242-7
   PubMed Web of Science ®Google Scholar
• Travassos, L. R., Taborda, C. P., & Colombo, A. L. (2008). Treatment options for paracoccidioidomycosis and new strategies investigated. Expert Review of Anti-Infective Therapy, 6(2), 251–262. https://doi.org/10.1586/14787210.6.2.251
   PubMed Web of Science ®Google Scholar
• Widmer, F., Wright, L. C., Obando, D., Handke, R., Ganendren, R., Ellis, D. H., & Sorrell, T. C. (2006). Hexadecylphosphocholine (miltefosine) has broad-spectrum fungicidal activity and is efficacious in a mouse model of Cryptococcosis. Antimicrobial Agents and Chemotherapy, 50(2), 414–421. https://doi.org/10.1128/AAC.50.2.414-421.2006
   PubMed Web of Science ®Google Scholar