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Explorando os estresses oxidativo e nitrosativo contra fungos: um mecanismo subjacente à ação de tradicionais antifúngicos e um potencial novo alvo terapêutico na busca por indutores oriundos de fontes naturais
Exploring the oxidative and nitrosative stresses against fungi: an underlying mechanism beyond the action of traditional antifungal agents and a potential new therapeutic target in searching for inducers from natural sources
Explorando los estréses oxidativos y nitrosativos contra hongos: un mecanismo subyacente a la acción de los antifúngicos tradicionales y un potencial nuevo objetivo terapéutico en la búsqueda de inductores de fuentes naturales
DOI:
https://doi.org/10.15446/rcciquifa.v50n1.85504Palavras-chave:
Estresse oxidativo, Estresse nitrosativo, Fungos, Candida albicans, Antifúngico, Produtos naturais. (pt)Estrés oxidativo, Estrés nitrosativo, Hongos, Candida albicans, Antifúngico, Productos naturales. (es)
Oxidative stress, Nitrosative stress, Yeast, Candida albicans, Antifungal, Natural products (en)
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Objetivo: nesta revisão sistemática, nós avaliamos o link entre indutores de estresse oxidativo e/ou nitrosativo (EO/EN) com atividade antifúngica, através de uma ação direta sobre a célula fúngica e/ou modulando a resposta de fagócitos contra fungos de interesse médico (incluindo Candida spp., Cryptococcus spp. e Aspergillusspp.). Ainda, foram avaliadas as implicações clínicas deste evento bioquímico, bem como as perspectivas quanto à busca por novos compostos com atividade antifúngica, principalmente, os provenientes de fonte natural e, que explorem a indução de um EO ou EN como parte de seu mecanismo de ação. Metodologia: foram avaliados artigos, provenientes de diferentes bases de dados e publicados a qualquer período, acessados entre abril e junho de 2017, através da utilização de diferentes descritores. Resultados: primeiramente, estabelecemos as definições de EO/EN, como sendo aumento das concentrações de espécies reativas do oxigênio e/ou nitrogênio (ERO/ERN) quantificado diretamente e, provenientes de fontes fúngicas mitocondriais, Reação de Fenton, retículo endoplasmático ou outras não definidas, e excedendo a capacidade de defesa antioxidante do microrganismo (avaliados por análises de perfis transcriptômicos ou proteômicos ou metabolômicos ou níveis de atividade enzimática). Este aumento de ERO/ERN causando EO/EN é definido por tempo e condições que conduzem a sinalização de apoptose ou reais danos a biomoléculas com perda de função (peroxidação lipídica ou oxidação proteica ou danos ao DNA) e, consequentemente, gerando morte fúngica ou outro efeito antifúngico associado. Portanto, 64 artigos (apenas um publicado antes do ano 2000 e 50 entre 2007-2017) abordam que a indução de EO ou EN na célula fúngica é parte do mecanismo de ação de clássicos agentes antifúngicos (22 publicações), tais como azóis (fluconazol, itraconazol e miconazol), polienos (anfotericina B [AnB]) e equinocandinas (mica-fungina), assim como tal modulação redox tem sido reportada como um importante alvo terapêutico na busca por novos e promissores compostos naturais com atividade antifúngica (32 publicações), que tem respaldo pela grande variedade de indutores que podem provir da natureza. Ainda, compostos que também induzem o burstoxidativo de fagócitos, incluindo AnB, são potencializadores do efeito antifúngico in vivo. Além do efeito antifúngico contra células planctônicas, os efeitos dos EO ou EN sobre biofilmes fúngicos, também têm sido reportados. Tem sido firmado na literatura recente um claro link entre EO ou EN e a atividade antifúngica, tanto para aqueles agentes antifúngicos já utilizados na terapêutica em humanos, quanto para possíveis candidatos a fármaco. Portanto, a indução do EO ou EN como parte do mecanismo de ação de antifúngicos demonstra ser um importante alvo terapêutico, com perspectivas favoráveis sobre os desfechos na prática clínica.
Aim:In this systematic review, we evaluated the link between inducers of oxidative or nitrosative stresses (OS/NS) and antifungal activity against fungi of medical relevance (including Candida spp., Cryptococcus spp., and Aspergillus spp.), through a direct action on the fungal cell or modulating phagocyte response. Moreover, the clinical implications of this biochemical event, as well as the perspectives, were examined, highlighting the search for new compounds with antifungal activity, mainly those from natural sources and, which explores the induction of OS or NS as part of the mechanism of action. Methodology:Articles from different data-bases and published at any time were evaluated, between April and June 2017, and using different descriptors. Results:First, a definition of OS and NS was established in which an increase in reactive oxygen or nitrogen species (ROS/RNS, quantified directly and from mitochondrial, Fenton reaction, endoplasmic reticulum or other fungal sources) should exceed the antioxidant defense capacity of the microorganism (evaluated by transcriptomic or proteomic or metabolomic profiles or enzyme activity levels). These events, by time and conditions delimited, can lead to the signaling of apoptosis or an actual damage toward biomolecules (lipid peroxidation or protein oxidation or DNA damage) and, consequently, they can cause cell death or other associated antifungal effect. Therefore, 64 articles were found, of these, only one was published before 2000 and 50 between 2007-2017, reporting the induction of OS or NS directly into the fungal cell via an increase in ROS or RNS as part of the mechanism of action of classical antifungal agents (22 publications), such as: azoles (fluconazole, itraconazole, and micon-azole), polyenes (amphotericin B, [AnB]), and echinocandins (micafungin). This redox modulation has also been reported as an important therapeutic target in the search for new natural compounds with antifungal activity (32 publications), which is supported for the great variety of inducers from nature. Compounds that also induce the oxidative burst of phagocytes, including AnB, promote a combina-torial antifungal effect in vivo. In addition to the antifungal effect against plank-tonic cells, the relation between OS or NS and antifungal activity against fungal biofilms has also been reported. It has been established in the recent literature a clear link between OS or NS and antifungal effect, during the action of anti-fungal agents already used in the therapy in humans as well as for possible drug candidates. Thus, the induction of OS or NS as part of the mechanism of action proves to be an important therapeutic target with favorable perspectives on the outcomes in clinical practice.
Objetivo:esta revisión sistemática, evaluamos el vínculo entre los inductores de estrés oxidativo o nitrosativo (EO/EN) con actividad antifúngica, a través de una acción directa sobre las células fúngicas o modulando la respuesta de los fagocitos contra hongos de interés médico (incluyendo Candida spp., Cryptococcus spp. yAspergillus spp.). Aun así, se evaluaron las implicaciones clínicas de este evento bioquímico, así como las perspectivas con respecto a la búsqueda de nuevos compuestos con actividad antifúngica, principalmente los de fuentes naturales y que exploran la inducción de un EO o EN como parte de su mecanismo. Metodología:entre abril y junio de 2017, evaluamos artículos de diferentes bases de datos publicados en el cualquier período, utilizando diferentes descriptores. Resultados:primero, establecemos las definiciones de EO/EN, como el aumento en las concentraciones de especies reactivas de oxígeno o nitrógeno (ERO/ERN) direc-tamente cuantificadas y, provenientes de fuentes fúngicas mitocondriales, reacción de Fenton, retículo endoplásmicou otros no definido y que excede la capacidad de defensa antioxidante del microorganismo (evaluado por análisis de perfiles trans-criptómicos o proteómicos o metabólicos o niveles de actividad enzimática). Este aumento de ERO/ERN que causa EO/EN se define por el tiempo y las condi-ciones que conducen a la apoptosis o daño real a las biomoléculas con pérdida de función (peroxidación lipídica y/u oxidación de proteínas o daño al ADN) y, en consecuencia, provoca la muerte microbiana u otro efecto antifúngico asociado. Por lo tanto, 64 artículos (solo uno publicado antes del año 2000 y 50 entre 2007-2017) abordan que la inducción de EO o EN en la célula fúngica es parte del meca-nismo de acción de los agentes antifúngicos clásicos (22 publicaciones), como los azoles (fluconazol, itraconazol y miconazol), polienos (anfotericina B [AnB]) y equinocandinas (micafungina), así como dicha modulación redox se ha informado como un objetivo terapéutico importante en la búsqueda de compuestos naturales nuevos y prometedores con actividad antifúngica (32 publicaciones), que está respaldado por la amplia variedad de inductores que pueden provenir de la natu-raleza. Además, los compuestos que también inducen la explosión oxidativa de fagocitos, incluido AnB, son potenciadores del efecto antifúngico in vivo. Además del efecto antifúngico contra las células planctónicas, también se han informado los efectos de EO o EN en las biopelículas fúngicas. Se ha establecido un vínculo claro entre EO o EN y la actividad antifúngica en la literatura reciente, tanto para aquellos agentes antifúngicos ya utilizados en terapia en humanos, c omo para posi-bles candidatos a fármacos. Por lo tanto, la inducción de EO o EN como parte del mecanismo de acción de los antifúngicos es un objetivo terapéutico importante, con perspectivas favorables sobre los resultados en la práctica clínica.
Referências
R. Santamaría, L. Rizzetto, M. Bromley, et al., Systems biology of infectious diseases: a focus on fungal infections, Immunobiology, 216, 1212 (2011).
Centers for Disease Control and Prevention (CDC), Antibiotic Resistant Threats in the United States, 2013, 114 p., 2013.
P. Vandeputte, S. Ferrari, A.T. Coste, Antifungal Resistance and New Strategies to Control Fungal Infections, International Journal of Microbiology, 2012, 26 (2012).
G. F. Ferreira, L.M. Baltazar, J.R.A. Santos, et al., The role of oxidative and nitrosative bursts caused by azoles and amphotericin B against the fungal pathogen Cryptococcus gattii, J Antimicrob Chemother, 68, 1801 (2013).
A. Khan, A. Ahmad, F. Akhtar, et al., Induction of oxidative stress as a possible mechanism of the antifungal action of three phenylpropanoids, FEMS Yeast Res, 11, 114 (2011).
C.D. Mahl, C.S. Behling, F.S. Hackenhaar, et al., Induction of ROS generation by fluconazole in Candida glabrata: activation of antioxidant enzymes and oxidative DNA damage, Diagnostic Microbiology and Infectious Disease, 82, 203 (2015).
H. Tian, S. Qu, Y. Wang, et al., Calcium and oxidative stress mediate perillaldehyde-induced apoptosis in Candida albicans, Appl Microbiol Biotechnol, 101, 3335 (2017).
Z. Wang, Y. Shen, Antifungal compound honokiol triggers oxidative stress responsive signalling pathway and modulates central carbon metabolism, Mycology, 7, 124 (2016).
M. Sharma, R. Manoharlal, N. Puri, et al., Antifungal curcumin induces reactive oxygen species and triggers an early apoptosis but prevents hyphae development by targeting the global repressorTUP1 in Candida albicans, Biosci Rep, 30, 391 (2010).
D. Kobayashi, K. Kondo, N. Uehara, et al., Endogenous Reactive Oxygen Species Is an Important Mediator of Miconazole Antifungal Effect, Antimicrobial Agents and Chemotherapy, 46, 3113 (2002).
A.C. Mesa-Arango, L. Scorzoni, O. Zaragoza, It only takes one to do many jobs: Amphotericin B as antifungal and immunomodulatory drug, Frontiers in Microbiology, 3, 1 (2012).
J.P. Guirao-Abad, R. Sánchez-Fresneda, B. Alburquerque, et al., ROS formation is a differential contributory factor to the fungicidal action of Amphotericin B and Micafungin in Candida albicans, International Journal of Medical Microbiology, 307, 241 (2017).
A.J. Philips, I. Sudbery, M. Ramsdale, Apoptosis induced by enviromental stresses and amphothericin B in Candida albicans, Proc Natl Acad Sci USA, 100, 14327 (2003).
M.P. Brynildsen, J.A. Winkler, C.S. Spina, et al., Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production, Nature Biotechnology, 31, 160 (2013).
I. Albesa, M.C. Becerra, P.C. Battan, et al., Oxidative stress involved in the antibacterial action of different antibiotics, Biochem Biophys Res Commun, 317, 605 (2004).
I. Keren, Y. Wu, J. Inocencio, et al., Killing by Bactericidal Antibiotics Does Not Depend on Reactive Oxygen Species, Science, 339, 1213 (2013).
Y. Liu, J.A. Imlay, Cell Death from Antibiotics Without the Involvement of Reactive Oxygen Species, Science, 339, 1210 (2013).
D.J. Dwyer, P.A. Belenky, J.H. Yang, et al., Antibiotics induce redox-related physiological alterations as part of their lethality, Proc Natl Acad Sci USA, 111, E2100 (2014).
P. Belenky, D. Camacho, J. J. Collins, Fungicidal Drugs Induce a Common Oxidative Damage Cellular Death Pathway, Cell Reports, 3, 350 (2013).
A.J.P. Brown, K. Haynes, J. Quinn, Nitrosative and oxidative stress responses in fungal pathogenicity, Current Opinion in Microbiology, 12, 384 (2009).
H. Sies, Oxidative stress: a concept in redox biology and medicine, Redox Biology, 4, 180 (2015).
B.S. Hromatka, S.M. Noble, A.D. Johnson, Transcriptional Response of Candida albicans to Nitric Oxide and the Role of theYHB1Gene in Nitrosative Stress and Virulence, Molecular Biology of the Cell, 16, 4814 (2005).
D. Cánovas, J.F. Marcos, J. Strauss. Nitric oxide in fungi: is there NO light at the end of the tunnel?, Curr Genet, 62, 513 (2016).
Q. Yu, B. Zhang, J. Li, et al., Endoplasmic reticulum-derived reactive oxygen species (ROS) is involved in toxicity of cell wall stress to Candida albicans, Free Radical Biology and Medicine, 99, 572 (2016).
P. Avci, F. Freire, A. Banvolgyi, et al., Sodium ascorbate kills Candida albicans in vitro via iron-catalyzed Fenton reaction: importance of oxygenation and metabolism, Future Microbiol, 11, 1535 (2016).
J. H. Lee, I. Y. Choi, I. S. Kil, et al., Protective role of superoxide dismutases against ionizing radiation in yeast, Biochimica et Biophysica Acta, 1526, 191 (2001).
S. Paul, T.L. Doering, W.S. Moye-Rowley, Cryptococcus neoformans Yap1 is required for normal fluconazole and oxidative stress resistance, Fungal Genet Biol, 74, 1 (2015).
T. Rossignol, B. Kocsis, O. Bouquet, et al., Antifungal Activity of Fused Mannich Ketones Triggers an Oxidative Stress Response and Is Cap1-Dependent in Candida albicans, PLoS ONE, 8, e62142 (2013).
G. Bartosz, Reactive oxygen species: destroyers or messengers?, Biochemical Pharmacology, 77, 1303 (2009).
M. Ramsdale. Programmed cell death in pathogenic fungi, Biochimica et Biophysica Acta, 1783, 1369 (2008).
P.W-K. Tsang, A.P-K. Wong, H-P. Yang, et al., Purpurin Triggers Caspase-Independent Apoptosis in Candida dubliniensis Biofilms, PLoS ONE, 8, e86032 (2013).
A. Hamann, D. Brust, H.D. Osiewacz, Apoptosis pathways in fungal growth, development and ageing, Trends in Microbiology, 6, 276 (2008).
G. Farrugia, R. Balzan, Oxidative stress and programmed cell death in yeast, Frontiers, 2, 1 (2012).
A. Sharon, A. Finkelstein, N. Shlezinger, et al., Fungal apoptosis: function, genes and gene function, FEMS Microbiol Rev, 33, 833 (2009).
S.A. Mousavi, G.D. Robson, Oxidative and amphotericin B-mediated cell death in the opportunistic pathogen Aspergillus fumigatus is associated with an apoptotic-like phenotype, Microbiology, 150, 1937 (2004).
K. Kang, K.S. Wong, W.P. Fong, et al., Metergoline-induced cell death in Candida krusei, Fungal Biol, 115, 302 (2011).
J. Cheng, T.S. Park, L.C. Chio, et al., Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans, Mol Cell Biol, 23, 163 (2003).
J.H. Hwang, I.S. Hwang, Q.H. Liu, et al., (+)-medioresinol leads to intracellular ROS accumulation and mitochondria-mediated apoptotic cell death in Candida albicans, Biochimie, 94, 1784 (2012).
B.D. Dai, Y.Y. Cao, S. Huang, et al., Baicalein induces programmed cell death in Candida albicans, J Microbiol Biotechnol, 19, 803 (2009).
X.Z. Wu, W.Q. Chang, A.X. Cheng, et al., Plagiochin E, an antifungal active macrocyclic bis(bibenzyl), induced apoptosis in Candida albicans through a metacaspase-dependent apoptotic pathway, Biochimica et Biophysica Acta, 1800, 439 (2010).
X.Z. Wu, A.X. Cheng, L.M. Sun, et al., Plagiochin E, an antifungal bis(bibenzyl), exerts its antifungal activity through mitochondrial dysfunction-induced reactive oxygen species accumulation in Candida albicans, Biochimica et Biophysica Acta, 1790, 770 (2009).
I.S. Hwang, J. Lee, H.G. Jin, et al., Amentof lavone stimulates mitochondrial dysfunction and induces apoptotic cell death in Candida albicans, Mycopathologia, 173, 207 (2012).
C. Park, E.R. Woo, D.G. Lee, Antifungal effect with apoptotic mechanism(s) of Styraxjaponoside C, Biochem Biophys Res Commun, 390, 1255 (2009).
A.M. Aerts, D. Carmona-Gutierrez, S. Lefevre, et al., The antifungal plant defensin RsAFP2 from radish induces apoptosis in a metacaspase independent way in Candida albicans, FEBS Lett, 583, 2513 (2009).
E.O. Mello, S.F. Ribeiro, A.O. Carvalho et al., Antifungal activity of PvD1 defensin involves plasma membrane permeabilization, inhibition of medium acidification, and induction of ROS in fungi cells, Curr Microbiol, 62, 1209 (2011).
B. Hwang, J.S. Hwang, J. Lee, et al., The antimicrobial peptide, psacotheasin induces reactive oxygen species and triggers apoptosis in Candida albicans. Biochem Biophys Res Commun, 405, 267 (2011).
J. Cho, D.G. Lee. The antimicrobial peptide arenicin-1 promotes generation of reactive oxygen species and induction of apoptosis, Biochimica et Biophysica Acta, 1810, 1246 (2011).
J. Cho, D.G. Lee. Oxidative stress by antimicrobial peptide pleurocidin triggers apoptosis in Candida albicans, Biochimie, 93, 1873 (2011).
B. Hwang, J.S. Hwang, J. Lee, et al., Induction of yeast apoptosis by an antimicrobial peptide, Papiliocin, Biochem Biophys Res Commun, 408, 89 (2011).
C. Park, D.G. Lee, Melittin induces apoptotic features in Candida albicans, Biochem Biophys Res Commun, 394, 170 (2010).
A. Lupetti, A. Paulusma-Annema, S. Senesi, et al., Internal thiols and reactive oxygen species in candidacidal activity exerted by an N-terminal peptide of human lactoferrin, Antimicrobial Agents and Chemotherapy, 46, 1634 (2002).
E.J. Helmerhorst, R.F. Troxler, F.G. Oppenheim, The human salivary peptide histatin 5 exerts its antifungal activity through the formation of reactive oxygen species, Proc Natl Acad Sci USA, 98, 14637 (2001).
D. Wunder, J. Dong, D. Baev, et al., Human salivary histatin 5 fungicidal action does not induce programmed cell death pathways in Candida albicans, Antimicrobial Agents and Chemotherapy, 48, 110 (2004).
C.R. Silva, J.B.A. Neto, R.S. Campos, et al., Synergistic effect of the flavonoid Catechin, Quercetin, or Epigallocatechin Gallate with Fluconazole induces apoptosis in Candida tropicalis resistant to Fluconazole, Antimicrobial Agents and Chemotherapy, 58, 1468 (2015).
I. D. Podmore, H. R. Griffiths, K. E. Herbert, et al., Vitamin C exhibits pro-oxidant properties, Nature, 392, 559 (1998).
P. Liu, L. Luo, J. Guo, et al., Farnesol induces apoptosis and oxidative stress in the fungal pathogen Penicillium expansum, Mycologia, 102, 311 (2010).
Q. Gaofua, Z. Fayin, D. Peng, et al., Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway, Peptides, 31, 1978 (2010).
I.K. Maurya, S. Pathak, M. Sharma, et al., Antifungal activity of novel synthetic peptides by accumulation of reactive oxygen species (ROS) and disruption of cell wall against Candida albicans, Peptides, 32, 1732 (2011).
D.M. Arana, C. Nombela, J. Pla, Fluconazole at subinhibitory concentrations induces the oxidative- and nitrosative-responsive genes TRR1, GRE2 and YHB1, and enhances the resistance of Candida albicans to phagocytes, J Antimicrob Chemother, 65, 54 (2010).
M. Goswami, S.H. Mangoli, N. Jawali, Antibiotics and Antioxidants: Friends or Foes During Therapy?, Barc Newsletter, 323, 42 (2011).
C.E.B. Linhares, S.R. Giacomelli, D. Altenhofen, et al., Fluconazole and amphotericin-B resistance are associated with increased catalase and superoxide dismutase activity in Candida albicans and Candida dubliniensis, Rev Soc Bras Med Trop, 46, 752 (2013).
Y. Xu, Y. Wang, L. Yan, et al., Proteomic analysis reveals a synergistic mechanism of fluconazole and berberine against fluconazole-resistant Candida albicans, J Proteome Res, 8, 5296 (2009).
M.L. Sokol-Anderson, J. Brajtburg, G. Medoff, Amphotericin B-induced oxidative damage and killing of Candida albicans, J Infect Dis, 154, 76 (1986).
F. Sangalli-Leite, L. Scorzoni, A.C. Mesa-Arango, et al., Amphotericin B mediates killing in Cryptococcus neoformans through the induction of a strong oxidative burst, Microbes Infect, 13, 457 (2011).
B. Hao, S. Cheng, C.J. Clancy, et al., Caspofungin kills Candida albicans by causing both cellular apoptosis and necrosis, Antimicrobial Agents and Chemotherapy, 57, 326 (2013).
L. Yan, M. Li, Y. Cao, et al., The alternative oxidase of Candida albicans causes reduced fluconazole susceptibility, J Antimicrob Chemother, 64, 764 (2009).
K. Thevissen, K.R. Ayscough, A.M. Aerts, et al., Miconazole induces changes in actin cytoskeleton prior to reactive oxygen species induction in yeast, J Biol Chem, 282, 21592 (2007).
M.C. Rubio, I.R. de Ocariz, J. Gil, et al., Potential fungicidal effect of voriconazole against Candida spp., Int J Antimicrob Agents, 25, 264 (2005).
P.G. Sohnle, B.L. Hahn, M.D. Erdmann, Effect of Fluconazole on Viability of Candida albicans over Extended Periods of Time, Antimicrobial Agents and Chemotherapy, 40, 2622 (1996).
P.G. Sohnle, B.L. Hahn, Effect of Prolonged Fluconazole Treatment on Candida albicans in Diffusion Chambers Implanted into Mice, Antimicrobial Agents and Chemotherapy, 46, 3175 (2002).
A. Zida, S. Bamba, A. Yacouba, et al., Anti-Candida albicans natural products, sources of new antifungal drugs: A review, Journal of Medical Mycology, 27, 1 (2017).
W-Q. Chang, X-Z. Wu, A-X. Cheng, et al., Retigeric acid B exerts antifungal effect through enhanced reactive oxygen species and decreased cAMP, Biochimica et Biophysica Acta, 1810, 569 (2011).
A. Ostrosky-Zeichner, A. Casadevall, J.N. Galgiani, et al., An insight into the antifungal pipeline: selected new molecules and beyond, Nature Reviews Drug Discovery, 9, 719 (2010).
M-Z. Xing, X-Z. Zhang, Z-L. Sun, et al., Perylenequinones act as broad-spectrum fungicides by generation reactive oxygen species both in the dark and in the light, J Agric Food Chem, 51, 7722 (2003).
M.A. Peralta, M.A. da Silva, M.A. Ortega, et al., Usnic Acid Activity on Oxidative and Nitrosative Stress of Azole-Resistant Candida albicans Biofilm, Planta Med, 83, 326 (2017).
K-T. Liou, Y-C. Shen, C-F. Chen, et al., Honokiol protects rat brain from focal cerebral ischemia–reperfusion injury by inhibiting neutrophil infiltration and reactive oxygen species production, Brain Research, 992, 159 (2003).
Y. Fukuyama, K. Nakade, Y. Minoshima, et al., Neurotrophic Activity of Honokiol on the Cultures of Fetal Rat Cortical Neurons, Bioorganic & Medicinal Chemistry Letters, 12, 1163 (2002).
O.A.K. Khalil, O.M.M. de Faria Oliveira, J.C.R. Vellosa, et al., Curcumin antifungal and antioxidant activities are increased in the presence of ascorbic acid, Food Chemistry, 133,1001 (2012).
Z. Liao, Y. Yan, H. Dong, et al., Endogenous nitric oxide accumulation is involved in the antifungal activity of Shikonin against Candida albicans, Emerging Microbes & Infections, 5, e88 (2016).
M. Sharma, R. Manoharlal, A.S. Negi, et al., Synergistic anticandidal activity of pure polyphenol curcumin I in combination with azoles and polyenes generates reactive oxygen species leading to apoptosis, FEMS Yeast Res, 10, 570 (2010).
M. An, H. Shen, Y. Cao, et al., Allicin enhances the oxidative damage effect of amphotericin B against Candida albicans, Int J Antimicrob Agents, 33, 258 (2009).
J.H. Kim, N.C. Faria, M.L. Martins, et al., Enhancement of antimycotic activity of amphotericin B by targeting the oxidative stress response of Candida and Cryptococcus with natural dihydroxybenzaldehydes, Front Microbiol, 3, 261 (2012).
B. Halliwell, J.M.C. Gutteridge, Free radicals in biology and medicine. Fourth edition, Oxford University Press Inc., New York, EUA, 2007.
P. Wojtaszek, Oxidative burst: an early plant response to pathogen infection, Biochem J, 322, 681 (1997).
C. Bogdan, M. Röllinghoff, A. Diefenbach, Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity, Current Opinion in Immunology, 12, 64 (2000).
K-W. Wong, Jr W. R. Jacobs, Mycobacterium tuberculosis exploits human interferon γ to stimulate macrophage extracellular trap formation and necrosis, JID, 208, 109 (2013).
M.S. Cohen, R.E. Isturiz, H.L. Malech, et al., Fungal infection in chronic granulomatous disease. The importance of the phagocyte in defense against fungi, Am J Med, 71, 59 (1981).
Y. Sun, S. Yu, P. Sun, et al., Inactivation of Candida biofilms by nonthermal plasma and its enhancement for fungistatic effect of antifungal drugs, PLoS ONE, 7, e40629 (2012).
K. Fricke, I. Koban, H. Tresp, et al., Atmospheric pressure plasma. a high-performance tool for the efficient removal of biofilms, PLoS ONE, 7, e42539 (2012).
M.C. Andrade, A.P. Ribeiro, L.N. Dovigo, et al., Effect of different pre-irradiation times on curcumin-mediated photodynamic therapy against planktonic cultures and biofilms of Candida spp., Arch Oral Biol, 58, 200 (2013).
L.N. Dovigo, A.C. Pavarina, J.C. Carmello, et al., Susceptibility of clinical isolates of Candida to photodynamic effects of curcumin, Lasers Surg Med, 43, 927 (2011).
C.D. Cerdeira, M.R.P.L. Brigagão, M.L. Carli, et al., Low-level laser therapy stimulates the oxidative burst in human neutrophils and increases their fungicidal capacity, Journal of Biophotonics, 9, 1180 (2016).
E. Roilides, C.A. Lyman, J. Filioti, et al., Amphotericin B formulations exert additive antifungal activity in combination with pulmonary alveolar macrophages and poly-morphonuclear leukocytes against Aspergillus fumigatus, Antimicrobial Agents and Chemotherapy, 46, 1974 (2002).
M. Tohyama, K. Kawakami, A. Saito, Anticryptococcal effect of amphotericin B is mediated through macrophage production of nitric oxide, Antimicrobial Agents and Chemotherapy, 40, 1919 (1996).
A. Coste, M.D. Linas, S. Cassaing, et al., A sub-inhibitory concentration of amphotericin B enhances candidastatic activity of interferon-gamma- and interleukin-13-treated murine peritoneal macrophages, J Antimicrob Chemother, 49, 731 (2002).
H.A. Jr. Chapman, J. B. Jr. Hibbs, Modulation of macrophage tumoricidal capability by polyene antibiotics: support for membrane lipid as a regulatory determinant of macrophage function, Proc Natl Acad Sci USA., 75, 4349 (1978).
E. Wilson, L. Thorson, D. P. Speert, Enhancement of macrophage superoxide anion production by amphotericin B, Antimicrobial Agents and Chemotherapy, 35, 796 (1991).
I. Kos, M.J. Patterson, S. Znaidi, et al., Mechanisms Underlying the Delayed Activation of the Cap1Transcription Factor in Candida albicans following Combinatorial Oxidative and Cationic Stress Important for Phagocytic Potency, mBio, 7, e00331-16 (2016).
K.C. Hazen, G. Mandell, E. Coleman, et al., Infuence of fuconazole at subinhibitory concentrations on cell surface hydrophobicity and phagocytosis of Candida albicans, FEMS Microbiology Letters, 183, 89 (2000).
N. Delattin, B. Cammue, K. Thevissen, Reactive oxygen species-inducing antifungal agents and their activity against fungal biofilms, Future Med Chem, 6, 77 (2014).
D.H. Navarathna, J.M. Hornby, N. Hoerrmann, et al., Enhanced pathogenicity of Candida albicans pre-treated with subinhibitory concentrations of fluconazole in a mouse model of disseminated candidiasis, J Antimicrob Chemother, 56, 1156 (2005).
M.A. Kohanski, M.A. DePristo, J.J. Collins, Sub-lethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis, Mol Cell, 37, 311 (2010).
C.J. Seneviratne, Y. Wang, L. Jin, et al., Candida albicans biofilm formation is associated with increased anti-oxidative capacities, Proteomics, 8, 2936 (2008).
A. Bink, G. Govaert, D. Vandenbosch, et al., Transcription factor Efg1 contributes to the tolerance of Candida albicans biofilms against antifungal agents in vitro and in vivo, J Med Microbiol, 61, 813 (2012).
K. Cremer, K. Brucker, I. Staes, et al., Stimulation of superoxide production increases fungicidal action of miconazole against Candida albicans biofilms, Scientific Reports, 6, 27463 (2016).
I. E. François, K. Thevissen, K. Pellens, et al., Design and synthesis of a series of piperazine-1-carboxamidine derivatives with antifungal activity resulting from accumulation of endogenous reactive oxygen species, Chem Med Chem, 4,1714 (2009).
A. Shirai, S. Ueta, H. Maseda, et al., Action of reactive oxygen species in the antifungal mechanism of Gemini-pyridinium salts against yeast, Biocontrol Science, 17, 77 (2012).
J.D. Lambert, R.J. Elias, The antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention, Arch Biochem Biophys, 501, 65 (2010).
A.J. León-González, C. Auger, V.B. Schini-Kerth, Pro-oxidant activity of polyphenols and its implication on cancer chemoprevention and chemotherapy, Biochemical Pharmacology, 98, 371 (2015).
M. Narasimhan, N.S. Rajasekaran, Reductive potential. A savior turns stressor in protein aggregation cardiomyopathy, Biochimica et Biophysica Acta, 1852, 53 (2015).
A.C. Brewer, S.B. Mustafi, T.V.A. Murray, et al., Reductive Stress Linked to Small HSPs, G6PD, and Nrf2 Pathways in Heart Disease, Antioxidants & Redox Signaling, 18, 1114 (2013).
T. Roemer, D. Xu, S.B. Singh, et al., Confronting the challenges of natural product-based antifungal discovery, Chem Biol, 18, 148 (2011).
J.A. Imlay. Diagnosing oxidative stress in bacteria: not as easy as you might think, Curr Opin Microbiol, 24, 124 (2015).
G.Q. Li, F. Quan, T. Qu, et al., Sublethal vancomycin-induced ROS mediating antibiotic resistance in Staphylococcus aureus, Biosci Rep, 35, e00279 (2015).
K. Poole, Stress responses as determinants of antimicrobial resistance in Gram-negative bacteria, Trends Microbiol, 20, 227 (2012).
Y. Wu, M. Vulic, I. Keren, et al., Role of oxidative stress in persister tolerance, Antimicrobial Agents and Chemotherapy, 56, 4922 (2012).
M.A. Kohanski, M.A. DePristo, J.J. Collins, Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis, Mol Cell, 37, 311 (2010).
J. Jee, A. Rasouly, I. Shamovsky, et al., Rates and mechanisms of bacterial mutagenesis from maximum-depth sequencing, Nature, 534, 693 (2016).
W.L. Neeley, J.M. Essigmann, Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products, Chem Res Toxicol, 19, 491 (2006).
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1. Cláudio Daniel Cerdeira, Maísa R. P. L. Brigagão. (2024). Targeting Macrophage Polarization in Infectious Diseases: M1/M2 Functional Profiles, Immune Signaling and Microbial Virulence Factors. Immunological Investigations, , p.1. https://doi.org/10.1080/08820139.2024.2367682.
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