Exposição aguda ao Bisfenol-A desencadeia um desequilíbrio superóxido-óxido nítrico e comprometimento da imunocompetência na minhoca Eisenia fetida

Autores

DOI:

https://doi.org/10.21527/2176-7114.2024.48.14558

Palavras-chave:

desreguladores endócrinos, genotoxicidade, estresse oxidativo, inflamação, apoptose, imunocompetência

Resumo

O bisfenol-A (BPA) é uma molécula desreguladora endócrina associada ao risco de diversas doenças crônicas não transmissíveis. Postulamos que o BPA desencadeia alterações oxidativas, alterando a imunocompetência e contribuindo para a disfunção fisiológica. Para avaliar os efeitos do BPA no sistema oxidativo e imunológico, minhocas californianas foram criadas em meio de cultura contendo diferentes concentrações de BPA por 24 horas e 72 horas. Celomócitos foram utilizados para avaliar os efeitos do BPA em marcadores oxidativos, proliferação celular e apoptose, e efeitos de imunocompetência foram investigados por ensaio de exposição a leveduras e modulação de genes relacionados à resposta imune. Baixas concentrações de BPA induziram proliferação de celomócitos, níveis desequilibrados de superóxido/NO, maior frequência de micronúcleos e apoptose. O BPA também induziu a superexpressão do gene Amp1 e uma baixa eficiência de captura de levedura morta. A associação entre danos no DNA e alterações no metabolismo imune inato pode estar relacionada à ação do BPA, que está associado ao risco de distúrbios fisiológicos e doenças crônicas não transmissíveis.

 

Referências

Abraham A, Chakraborty P. A review on sources and health impacts of bisphenol A. Rev Environ Health. 2020 Jun. 25;35(2):201-210.

Balistrieri A, Hobohm L, Srivastava T, Meier A, Corriden R. Alterations in human neutrophil function caused by bisphenol A. Am J Physiol-Cell Physiol. 2018 Nov. 1;315(5):C636-642.

Nowak K, Jabłońska E, Ratajczak-Wrona W. Neutrophils life under estrogenic and xenoestrogenic control. J Steroid Biochem Mol Biol. 2019 Feb.;186:203-211.

Ratajczak-Wrona W, Rusak M, Nowak K, Dabrowska M, Radziwon P, Jablonska E. Effect of bisphenol A on human neutrophils immunophenotype. Sci Rep. 2020 Feb. 20;10(1):3.083.

Ratajczak-Wrona W, Garley M, Rusak M, Nowak K, Czerniecki J, Wolosewicz K, et al. Sex-dependent dysregulation of human neutrophil responses by bisphenol A. Environ Health. 2021 Dec.;20(1):5.

Hugo Del Rio Araiza V. Bisphenol A, an endocrine-disruptor compund, that modulates the immune response to infections. Front Biosci. 2021;26(2):346-362.

Cimmino I, Oriente F, D’Esposito V, Liguoro D, Liguoro P, Ambrosio MR, et al. Low-dose Bisphenol-A regulates inflammatory cytokines through GPR30 in mammary adipose cells. J Mol Endocrinol. 2019 Nov.;63(4):273-283.

Kimber I. Bisphenol A and immunotoxic potential: A commentary. Regul Toxicol Pharmacol. 2017 Nov.;90:358-363.

Srinivas US, Tan BWQ, Vellayappan BA, Jeyasekharan AD. ROS and the DNA damage response in cancer. Redox Biol. 2019 Jul.;25:101084.

Zindel J, Kubes P. DAMPs, PAMPs, and LAMPs in Immunity and Sterile Inflammation. Annu Rev Pathol Mech Dis. 2020 Jan. 24;15(1):493-518.

Oliveira KMGD, Carvalho EHDS, Santos Filho RD, Sivek TW, Thá EL, Souza IRD, et al. Single and mixture toxicity evaluation of three phenolic compounds to the terrestrial ecosystem. J Environ Manage. 2021 Oct.;296:113226.

Novo M, Verdú I, Trigo D, Martínez-Guitarte JL. Endocrine disruptors in soil: Effects of bisphenol A on gene expression of the earthworm Eisenia fetida. Ecotoxicol Environ Saf. 2018 Apr.;150:159-167.

Homa J. Earthworm coelomocyte extracellular traps: structural and functional similarities with neutrophil NETs. Cell Tissue Res. 2018 Mar.;371(3):407-414.

Alves ADO, Weis GCC, Unfer TC, Assmann CE, Barbisan F, Azzolin VF, et al. Caffeinated beverages contribute to a more efficient inflammatory response: Evidence from human and earthworm immune cells. Food Chem Toxicol. 2019 Dec.;134:110809.

Cruz Jung IED, Assmann CE, Mastella MH, Barbisan F, Spilliari Ruaro RA, Roggia I, et al. Superoxide-anion triggers impairments of immune efficiency and stress response behaviors of Eisenia fetida earthworms. Chemosphere. 2021 Apr.;269:128712.

Pérez S, Rius-Pérez S. Macrophage Polarization and Reprogramming in Acute Inflammation: A Redox Perspective. Antioxidants (Basel). 2022 Jul. 19;11(7):1.394.

Wang W, Zhang J, Wu J, Yu R, Zhang Y, Sun L, et al. Acute Toxicity and Ecotoxicological Risk Assessment of Three Volatile Pesticide Additives on the Earthworm-Eisenia fetida. Int J Environ Res Public Health. 2021 Oct. 26;18(21):11.232.

Cho JH, Park CB, Yoon YG, Kim SC. Lumbricin I, a novel proline-rich antimicrobial peptide from the earthworm: purification, cDNA cloning and molecular characterization. Biochim Biophys Acta BBA - Mol Basis Dis. 1998 Oct.;1408(1):67-76.

Mo X, Qiao Y, Sun Z, Sun X, Li Y. Molecular toxicity of earthworms induced by cadmium contaminated soil and biomarkers screening. J Environ Sci. 2012 Aug.;24(8):1.504-1.510.

Škanta F, Roubalová R, Dvořák J, Procházková P, Bilej M. Molecular cloning and expression of TLR in the Eisenia andrei earthworm. Dev Comp Immunol. 2013 Dec.;41(4):694-702.

Morabito C, Rovetta F, Bizzarri M, Mazzoleni G, Fanò G, Mariggiò MA. Modulation of redox status and calcium handling by extremely low frequency electromagnetic fields in C2C12 muscle cells: A real-time, single-cell approach. Free Radic Biol Med. 2010 Feb. 15;48(4):579-589.

Choi WS, Shin PG, Lee JH, Kim GD. The regulatory effect of veratric acid on NO production in LPS-stimulated RAW264.7 macrophage cells. Cell Immunol. 2012 Dec.;280(2):164-170.

Jentzsch AM, Bachmann H, Fürst P, Biesalski HK. Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med. 1996 Jan.;20(2):251-256.

Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. [49] Determination of carbonyl content in oxidatively modified proteins. In: Methods in Enzymology [Internet]. Elsevier; 1990 [cited 2023 May. 29]. p. 464-478. Available from: https://linkinghub.elsevier.com/retrieve/pii/007668799086141H

Holland N, Bolognesi C, Kirschvolders M, Bonassi S, Zeiger E, Knasmueller S, et al. The micronucleus assay in human buccal cells as a tool for biomonitoring DNA damage: The HUMN project perspective on current status and knowledge gaps. Mutat Res Mutat Res. 2008 Jul.;659(1-2):93-108.

Troha K, Buchon N. Methods for the study of innate immunity in Drosophila melanogaster. WIREs Dev Biol [Internet]. 2019 Sept. [cited 2023 May. 29];8(5). Available from: https://onlinelibrary.wiley.com/doi/10.1002/wdev.344

Kim DH. Signaling in the innate immune response. WormBook. 2018 Aug. 16;1-35.

Ma Y, Liu H, Wu J, Yuan L, Wang Y, Du X, et al. The adverse health effects of bisphenol A and related toxicity mechanisms. Environ Res. 2019 Sept.;176:108575.

Jalal N, Surendranath AR, Pathak JL, Yu S, Chung CY. Bisphenol A (BPA) the mighty and the mutagenic. Toxicol Rep. 2018;5:76-84.

ANVISA. Bisfenol A [Internet]. [cited 2021 Dec 20]. Available from: Https://www.http://gov.br/anvisa/pt-br/setorregulado/regularizacao/alimentos/bisfenol-a

EFSA. Bisphenol A [Internet]. Available from: https://www.efsa.europa.eu/en/topics/topic/bisphenol#:~:text=Bisphenol%20A%20(BPA)%20is%20a,to%20manufacture%20plastics%20and%20resins.&text=EFSA%20published%20a%20comprehensive%20re,to%204%20%C2%B5g%2Fkg%20bw

Cimmino I, Fiory F, Perruolo G, Miele C, Beguinot F, Formisano P, et al. Potential Mechanisms of Bisphenol A (BPA) Contributing to Human Disease. Int J Mol Sci. 2020 Aug. 11;21(16):5761.

Furman D, Campisi J, Verdin E, Carrera-Bastos P, Targ S, Franceschi C, et al. Chronic inflammation in the etiology of disease across the life span. Nat Med. 2019 Dec.;25(12):1.822.

Babić S, Barišić J, Bielen A, Bošnjak I, Sauerborn Klobučar R, Ujević I, et al. Multilevel ecotoxicity assessment of environmentally relevant bisphenol A concentrations using the soil invertebrate Eisenia fetida. J Hazard Mater. 2016 Nov.;318:477-486.

Bilej M, De Baetselier P, Beschin A. Antimicrobial defense of the earthworm. Folia Microbiol (Praha). 2000 Aug.;45(4):283-300.

Homa J, Zorska A, Wesolowski D, Chadzinska M. Dermal exposure to immunostimulants induces changes in activity and proliferation of coelomocytes of Eisenia andrei. J Comp Physiol B. 2013 Apr.;183(3):313-322.

D. Varela C, Farhana A. Biochemistry, Superoxides. Treasure Island (Florida: StatPearls Publishing.

Galkina SI, Golenkina EA, Viryasova GM, Romanova YM, Sud’ina GF. Nitric Oxide in Life and Death of Neutrophils. Curr Med Chem. 2019 Nov. 19;26(31):5.764-5.780.

Homa J, Ortmann W, Kolaczkowska E. Conservative Mechanisms of Extracellular Trap Formation by Annelida Eisenia andrei: Serine Protease Activity Requirement. Palaniyar N, editor. PLOS ONE. 2016 Jul. 14;11(7):e0159031.

Tiwari D, Kamble J, Chilgunde S, Patil P, Maru G, Kawle D, et al. Clastogenic and mutagenic effects of bisphenol A: An endocrine disruptor. Mutat Res Toxicol Environ Mutagen. 2012 Mar.;743(1-2):83-90.

Wiesner J, Vilcinskas A. Antimicrobial peptides: The ancient arm of the human immune system. Virulence. 2010 Sept.;1(5):440-464.

Wang X, Li X, Sun Z. iTRAQ-based quantitative proteomic analysis of the earthworm Eisenia fetida response to Escherichia coli O157:H7. Ecotoxicol Environ Saf. 2018 Sep;160:60-66.

Mincarelli L, Tiano L, Craft J, Marcheggiani F, Vischetti C. Evaluation of gene expression of different molecular biomarkers of stress response as an effect of copper exposure on the earthworm EIsenia Andrei. Ecotoxicology. 2019 Oct.;28(8):938-948.

Kumar P, Kizhakkedathu J, Straus S. Antimicrobial Peptides: Diversity, Mechanism of Action and Strategies to Improve the Activity and Biocompatibility In Vivo. Biomolecules. 2018 Jan. 19;8(1):4.

Vijay K. Toll-like receptors in immunity and inflammatory diseases: Past, present, and future. Int Immunopharmacol. 2018 Jun.;59:391-412.

Navarro Pacheco NI, Roubalova R, Semerad J, Grasserova A, Benada O, Kofronova O, et al. In Vitro Interactions of TiO2 Nanoparticles with Earthworm Coelomocytes: Immunotoxicity Assessment. Nanomaterials. 2021 Jan. 19;11(1):250.

Collet SH, Picard-Hagen N, Lacroix MZ, Puel S, Viguié C, Bousquet-Melou A, et al. Allometric scaling for predicting human clearance of bisphenol A. Toxicol Appl Pharmacol. 2015 May.;284(3):323-329.

Downloads

Publicado

2024-02-21

Como Citar

Turra , B. O., da Cruz , I. B. M., Bonotto , N. C. de A., Teixeira, C. F., Mastella, M. ., Ferreira , W. C., Jung, I. E. da C., Musachio, E. A. S., Prigol, M., & Barbisan, F. (2024). Exposição aguda ao Bisfenol-A desencadeia um desequilíbrio superóxido-óxido nítrico e comprometimento da imunocompetência na minhoca Eisenia fetida. Revista Contexto &Amp; Saúde, 24(48), e14558. https://doi.org/10.21527/2176-7114.2024.48.14558

Edição

Seção

Artigo Original