Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The dusky grouper Epinephelus marginatus is a protogynous hermaphrodite fish, that maintains high levels of plasma steroids as juveniles, as substrates for sex inversion. These fish are exposed to marine pollution from oil spills during cargo handling. Polycyclic aromatic hydrocarbons (PAHs), such as phenanthrene (Phe), are the main crude oil components and are toxic to fish, acting as endocrine disruptors (ED). This is the first study that investigated impacts of Phe as an ED in E. marginatus juveniles. An in vivo sublethal exposure (96 h) to Phe was carried out at two concentrations (0.1 mg/L and 1 mg/L); exposure to the vehicle (ethanol; ETOH) was also performed. Plasma levels of 17β-estradiol (E 2 ), testosterone (T) and 11-ketotestosterone (11-KT) were measured by ELISA. Gonads, liver and spleen were processed for histological analysis. In an in vitro bioassay, gonad fragments were incubated with Phe (8.91 mg/L) or ETOH. Steroid levels in the culture media were measured by ELISA. The in vivo exposure to Phe triggered an increase of the area of the hepatocytes, increased number of melanomacrophagic centers and hemosiderosis in the spleen; ETOH induced similar effects on spleen. E 2 and T levels did not change in plasma or in vitro media. In plasma, ETOH decreased 11-KT levels. Phenanthrene sharply reduced 11-KT levels in vitro. Although in vivo bioassay results were not unequivocal owing to ethanol effects, Phe might disrupt steroidogenesis in juvenile grouper, possibly causing dysfunctions during sex change and gonadal maturity, considering the importance of 11-KT in developing ovaries. © 2017 Elsevier Inc.

Registro:

Documento: Artículo
Título:Endocrine disruption of phenanthrene in the protogynous dusky grouper Epinephelus marginatus (Serranidae: Perciformes)
Autor:de Campos, M.F.; Lo Nostro, F.L.; Da Cuña, R.H.; Moreira, R.G.
Filiación:Laboratório de Metabolismo e Reprodução de Organismos Aquáticos, Dep. de Fisiologia, Instituto de Biociências, Universidade de São Paulo, Brazil
Centro de Biologia Marinha (CEBIMar), Universidade de São Paulo, Brazil
Laboratorio de Ecotoxicología Acuática, Dept. de Biodiversidad y Biologia Experimental, FCEN, Universidad de Buenos Aires & IBBEA, CONICET-UBA, Argentina
Palabras clave:Acute toxicity; Gonadal steroids; PAH; Protogynous hermaphroditism; 11 oxotestosterone; alcohol; estradiol; phenanthrene; testosterone; estradiol; phenanthrene; phenanthrene derivative; animal cell; animal experiment; animal tissue; Article; concentration (parameters); controlled study; drug effect; endocrine disease; enzyme linked immunosorbent assay; Epinephelus; Epinephelus marginatus; exposure; hemosiderosis; histology; hormone blood level; in vitro study; in vivo study; juvenile animal; LC50; nonhuman; priority journal; spleen hemosiderosis; steroidogenesis; animal; female; male; metabolism; sex determination process; Animals; Estradiol; Female; Male; Phenanthrenes; Sex Determination Processes
Año:2018
Volumen:257
Página de inicio:255
Página de fin:263
DOI: http://dx.doi.org/10.1016/j.ygcen.2017.06.020
Título revista:General and Comparative Endocrinology
Título revista abreviado:Gen. Comp. Endocrinol.
ISSN:00166480
CODEN:GCENA
CAS:11 oxotestosterone, 564-35-2; alcohol, 64-17-5; estradiol, 50-28-2; phenanthrene, 85-01-8; testosterone, 58-22-0; Estradiol; phenanthrene; Phenanthrenes
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00166480_v257_n_p255_deCampos

Referencias:

  • Agius, C., Roberts, R.J., Melano-macrophage centres and their role in fish pathology (2003) J. Fish Dis., 26, pp. 499-509
  • Barreiros, J.P., Sexual inversion in Epinephelus marginatus (Lowe, 1834) (Pisces: Serranidae, Epinephelinae) (1998) Rev. Port. Zoot., 5, pp. 81-90
  • Bhandari, R.K., Komuro, H., Nakamura, S., Higa, M., Nakamura, M., Gonadal restructuring and correlative steroid hormone profiles during natural sex change in protogynous honeycomb grouper (Epinephelus merra) (2003) Zoolog. Sci., 20, pp. 1399-1404
  • Bhanu, S.V., Philip, B., Effect of ethanol on branchial adenosine triphosphatases in Oreochromismossambicus(Peters) (2011) Toxicol. Int., 18, pp. 27-30
  • Black, J.A., Birge, W.J., Westerman, A.G., Francis, P.C., Comparative aquatic toxicology of aromatic hydrocarbons (1983) Fundam. Appl. Toxicol., 3, pp. 353-358
  • Borg, B., Androgens in teleost fishes (1994) Comp. Biochem. Physiol., 109C, pp. 219-245
  • Camus, L., Jones, M.B., Borseth, J.F., Grosvik, B.E., Regoli, F., Depledge, M.H., Total oxyradical scavenging capacity and cell membrane stability of haemocytes of the Arctic scallop, Chlamysislandicus, following benzo(a)pyrene exposure (2002) Mar. Environ. Res., 54, pp. 425-430
  • Carvalho, P.S., Kalil, D.D.C.B., Novelli, G.A., Bainy, A.C., Fraga, A.P.M., Effects of naphthalene and phenanthrene on visual and prey capture endpoints during early stages of the dourado Salminus brasiliensis (2008) Mar. Environ. Res., 66, pp. 205-207
  • CETESB, COMPANHIA DE TECNOLOGIA DE SANEAMENTO AMBIENTAL, Monitoramento de águas costeiras: Litoral Norte em Relatório de Qualidade das Águas Litorâneas no Estado de São Paulo (2004), pp. 273-331. , Balneabilidade das Praias; Cornish, A., Harmelin-Vivien, M., (2004) Epinephelus marginatus, , www.iucnredlist.org, IUCN.IUCN Red List of Threatened Species
  • Divers, S.L., Mcquillan, H.J., Matsubara, H., Todo, T., Lokman, P.M., Effects of reproductive stage and 11-ketotestosterone on LPL mRNA levels in the ovary of the shortfinned eel (2010) J. Lipid Res., 51, pp. 3250-3258
  • Doerffer, J.W., Oil Spill Response in the Marine Environment (2013), Elsevier Pergamon; Endo, T., Todo, T., Lokman, P.M., Kudo, H., Ijiri, S., Adachi, S., Yamauchi, K., Androgens and very low density lipoprotein are essential for the growth of previtellogenic oocytes from Japanese eel, Anguilla japonica, in vitro (2011) Biol. Reprod., 84, pp. 816-825
  • Evans, D.R., Rice, S.P., Effects of oil on marine ecosystems: a review for administrators and policy makers (1974) Fish. Bull., 72, pp. 625-638
  • Figueiredo, J.L., Menezes, N.A., Manual de peixes marinhos do sudeste do Brasil III. Teleostei (2) (1980), p. 90. , Museu de Zoologia da Universidade de São Paulo São Paulo; Finney, D.J., Probit Analysis (1971), p. 333. , Cambridge University Press London; Fournie, J.W., Summers, J.K., Courtney, L.A., Engle, V.D., Blazer, V.S., Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments (2001) J. Aquat. Anim. Health, 13, pp. 105-116
  • Garcia, C.E.O., Araújo, B.C., Mello, P.H., Narcizo, A.M., Rodrigues-Filho, J.A., Medrado, A.T., Zampieri, R.A., Moreira, R.G., Involvement of pituitary gonadotropins, gonadal steroids and breeding season in sex change of protogynous dusky grouper, Epinephelus marginatus (Teleostei: Serranidae), induced by a non-steroidal aromatase inhibitor (2013) Gen. Comp. Endocrinol., 190, pp. 170-180
  • Genten, F., Terwinghe, E., Danguy, A., Atlas of Fish Histology (2009), Science Publishers Enfield, NH, USA; Geraudie, P., Nahrgang, J., Forget-Leray, J., Minier, C., Camus, L., In vivo effects of environmental concentrations of produced water on the reproductive function of polar cod (Boreogadus saida) (2014) J. Toxicol. Environ. Health, 77A, pp. 557-573
  • Goodbred, S.L., Gilliom, R.J., Gross, T.S., Denslow, N.P., Bryant, W.L., Schoeb, T.R., (1997), pp. 96-627. , Reconnaissance of 17B-estradiol, 11-ketotestosterone, vitellogenin, and gonad histopathology in common carp of United States streams: Potential for contaminant-induced endocrine disruption. US Geological Survey Open-File Report, Sacramento, CA, USA; Han, Z.X., Wang, J.H., Lv, W.Z., Min, L., Multibiomarker approaches in common carp to assess the effects of phenanthrene (2010) Synth. React. Inorg. Metal-Org. Nano-Metal Chem., 40, pp. 257-265
  • Harmelin, J.G., Harmelin-Vivien, M., A review on habitat, diet and growth of the dusky grouper Epinephelus marginatus (Lowe, 1834) (1999) Mar. Life, 9, pp. 11-20
  • Heemstra, P.C., Randall, J.E., FAO species catalogue. Groupers of the world (Family Serranidae, Subfamily Epinephelinae): an annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper, and lyretail species known to date (1993) FAO Fish Synops., 16 (125)
  • Heppell, S.A., Seasonal fluctuations in androgen levels in females of the hermaphroditic gag, Mycteroperca microlepis, with an emphasis on juvenile animals (2005) Comp. Biochem. Physiol., 142A, pp. 84-91
  • Hibiya, T., Yokote, M., Oguri, M., Sato, H., Takashima, F., Aida, K., An Atlas of Fish Histology. Normal and Pathological Features (1982), p. 147; Jee, J.H., Kim, S.G., Kang, J.C., Effects of phenanthrene on growth and basic physiological functions of the olive flounder, Paralichthys olivaceus (2004) J. Exp. Mar. Biol. Ecol., 304, pp. 123-136
  • Karami, A., Romano, N., Hamzah, H., Simpson, S.L., Yap, C.K., Acute phenanthrene toxicity to juvenile diploid and triploid African catfish (Clarias gariepinus): molecular, biochemical, and histopathological alterations (2016) Environ. Pollut., 212, pp. 155-165
  • Kennedy, C.J., Smyth, K.R., Disruption of the rainbow trout reproductive endocrine axis by the polycyclic aromatic hydrocarbon benzo[a]pyrene (2015) Gen. Comp. Endocrinol., 219, pp. 102-111
  • Lister, A., Nero, V., Farwell, A., Dixon, D.G., Van Der Kraak, G., Reproductive and stress hormone levels in goldfish (Carassius auratus) exposed to oil sands process-affected water (2008) Aquat. Toxicol., 87, pp. 170-177
  • Liu, X., Ji, K., Choi, K., Endocrine disruption potentials of organophosphate flame retardants and related mechanisms in H295R and MVLN cell lines and in zebrafish (2012) Aquat. Toxicol., 114, pp. 173-181
  • Lo Nostro, F., Grier, H., Andreone, L., Guerrero, G.A., Involvement of the gonadal germinal epithelium during sex reversal and seasonal testicular cycling in the protogynous swamp eel, Synbranchus marmoratus Bloch 1795 (Teleostei, Synbranchidae) (2003) J. Morphol., 257, pp. 107-126
  • Lohmann, R., Klanova, J., Pribylova, P., Liskova, H., Yonis, S., Bollinger, K., PAHs on a west-to-east transect across the tropical Atlantic Ocean (2013) Environ. Sci. Technol., 47, pp. 2570-2578
  • Lokman, P.M., Vermeulen, G.J., Lambert, J.G., Young, G., Gonad histology and plasma steroid profiles in wild New Zealand freshwater eels (Anguilla dieffenbachia and A. australis) before and at the onset of the natural spawning migration. I. Females (1998) Fish Physiol. Biochem., 19, pp. 325-338
  • Lokman, P.M., Harris, B., Kusakabe, M., Kime, D.E., Schulz, R.W., Adachi, S., Young, G., 11-Oxygenated androgens in female teleosts: prevalence, abundance, and life history implications (2002) Gen. Comp. Endocrinol., 129, pp. 1-12
  • Lokman, P.M., George, K.A., Divers, S.L., Algie, M., Young, G., 11-Ketotestosterone and IGF-I increase the size of previtellogenic oocytes from shortfinned eel, Anguilla australis, in vitro (2007) Reproduction, 133, pp. 955-967
  • Machado, A.A.S., Hoff, M.L.M., Klein, R.D., Cordeiro, G.J., Avila, J.M.L., Costa, P.G., Bianchini, A., Oxidative stress and DNA damage responses to phenanthrene exposure in the estuarine guppy Poecilia vivipara (2014) Mar. Environ. Res., 98, pp. 96-105
  • Maqbool, F., Mostafalou, S., Bahadar, H., Abdollahi, M., Review of endocrine disorders associated with environmental toxicants and possible involved mechanisms (2016) Life Sci., 145, pp. 265-273
  • Martin-Skilton, R., Thibaut, R., Porte, C., Endocrine alteration in juvenile cod and turbot exposed to dispersed crude oil and alkylphenols (2006) Aquat. Toxicol., 78, pp. S57-S64
  • Maskaoui, K., Zhou, J.L., Hong, H.S., Zhang, Z.L., Contamination by polycyclic aromatic hydrocarbons in the Jiulong River Estuary and Western Xiamen Sea, China (2002) Environ. Pollut., 118, pp. 109-112
  • Matthiessen, P., Johnson, I., Implications of research on endocrine disruption for the environmental risk assessment, regulation and monitoring of chemicals in the European Union (2007) Environ. Pollut., 146, pp. 9-18
  • Meador, J.P., Stein, J.E., Reichert, W.L., Varanasi, U., Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms (1995) Rev. Environ. Contam. Toxicol., 143, pp. 79-165
  • Medeiros, P.M., Bícego, M.C., Investigation of natural and anthropogenic hydrocarbon inputs in sediments using geochemical markers. II. São Sebastião, SP––Brazil (2004) Mar. Pollut. Bull., 49, pp. 892-899
  • Monteiro, P.R.R., Reis-Henriques, M.A., Coimbra, J., Polycyclic aromatic hydrocarbons inhibit in vitro ovarian steroidogenesis in the flounder (Platichthys flesusL.) (2000) Aquat. Toxicol., 48, pp. 549-559
  • Monteiro, P.R.R., Reis-Henriques, M.A., Coimbra, J., Plasma steroid levels in female flounder (Platichthys flesus) after chronic dietary exposure to single polycyclic aromatic hydrocarbons (2000) Mar. Environ. Res., 49, pp. 453-467
  • Nicolas, J.M., Vitellogenesis in fish and the effects of polycyclic aromatic hydrocarbon contaminants (1999) Aquat. Toxicol., 45, pp. 77-90
  • Ozaki, Y., Higuchi, M., Miura, C., Yamaguchi, S., Tozawa, Y., Miura, T., Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis (2006) Endocrinology, 147, pp. 5139-5146
  • Pankhurst, N.W., Van Der Kraak, G., Effects of stress on reproduction and growth of fish (1997) Fish Stress and Health in Aquaculture, pp. 73-93. , G.K. Iwama A.D. Pickering J.P. Sumpter C.B. Schreck Cambridge Univ. Press Cambridge
  • Pasqualotto, F.F., Lucon, A.M., Sobreiro, B.P., Pasqualotto, E.B., Arap, S., Effects of medical therapy, alcohol, smoking, and endocrine disruptors on male infertility (2004) Rev. Hosp. Clín. Med. São Paulo, 59, pp. 375-382
  • Roberts, B.J., Shoaf, S.E., Song, B.J., Rapid changes in cytochrome P4502E1 (CYP2E1) activity and other P450 isozymes following ethanol withdrawal in rats (1995) Biochem. Pharmacol., 49, pp. 1665-1673
  • Rodrigues-Filho, J.A., Alterações morfológicas e hormonais das gônadas e da hipófise da garoupa Epinephelus marginatus (Teleostei: Serranidae) durante a inversão sexual (2010), (Master's dissertation) University of São Paulo São Paulo; Rodrigues-Filho, J.A., Sanches, E.G., Garcia, C.E.O., Pannuti, C.V., Sebastini, E.F., Moreira, R.G., Threatened fishes of the world: Epinephelus marginatus (Lowe, 1834) (Serranidae: Epinephelinae) (2009) Environ. Biol. Fish., 85, pp. 301-302
  • Rohr, D.H., Lokman, P.M., Davie, P.S., Young, G., 11-Ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla australis (2001) Comp. Biochem. Physiol., 130, pp. 701-714
  • Roy, L.A., Steinert, S., Bay, S.M., Greenstein, D., Sapozhnikova, Y., Bawardi, O., Leifer, I., Schlenk, D., Biochemical effects of petroleum exposure in hornyhead turbot (Pleuronichthysverticalis) exposed to a gradient of sediments collected from a natural petroleum seep in CA, USA (2003) Aquat. Toxicol., 65, pp. 159-169
  • Salvo, L.M., Severino, D., De Assis, H.C.S., Da Silva, J.R.M., Photochemical degradation increases polycyclic aromatic hydrocarbon (PAH) toxicity to the grouper Epinephelus marginatus as assessed by multiple biomarkers (2016) Chemosphere, 144, pp. 540-547
  • Senthilkumaran, B., Pesticide-and sex steroid analogue-induced endocrine disruption differentially targets hypothalamo–hypophyseal–gonadal system during gametogenesis in teleosts – a review (2015) Gen. Comp. Endocrinol., 219, pp. 136-142
  • Setiawan, A.N., Ozaki, Y., Shoae, A., Kazeto, Y., Lokman, P.M., Androgen-specific regulation of FSH signalling in the previtellogenic ovary and pituitary of the New Zealand shortfinned eel, Anguilla australis (2012) Gen. Comp. Endocrinol., 176, pp. 132-143
  • Sluka, R., Chiappone, M., Sullivan, K.M., Comparison of juvenile grouper populations in southern Florida and the central Bahamas (1994) Bull. Mar. Sci., 54, pp. 871-880
  • Stegeman, J.J., Lech, J.J., Cytochrome P-450 monooxygenase systems in aquatic species: carcinogen metabolism and biomarkers for carcinogen and pollutant exposure (1991) Environ. Health Perspect., 90, pp. 101-109
  • Takashima, F., Hibiya, T., An Atlas of Fish Histology: Normal and Pathological Features (1995), Kodanska Tokyo, Japan; Thiyagarajah, A., Hartley, W.R., Abdelghani, A., Hepatic hemosiderosis in buffalo fish (Ictiobus spp.) (1998) Mar. Environ. Res., 46, pp. 203-207
  • Thomas, P., Reproductive endocrine function in female Atlantic croaker exposed to pollutants (1988) Mar. Environ. Res., 24, pp. 179-183
  • Tyler, C., Jobling, S., Sumpter, J.P., Endocrine disruption in wildlife: a critical review of the evidence (1998) Crit. Rev. Toxicol., 28, pp. 319-361
  • EPA, U.S., United States Environmental Protection Agency, , https://www3.epa.gov
  • Veintemilla, C.A.C., Impactos do fenantreno sobre o tambaqui Colossoma macropomum Cuvier, 1818: CL50, crescimento e hematologia (2006), (Master's dissertation) Instituto Nacional de Pesquisa da Amazônia (INPA) Manaus; Walker, M.K., Peterson, R.E., Potencies of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners, relative to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin, for producing early life stage mortality in rainbow trout (Oncorhynchus mykiss) (1991) Aquat. Toxicol., 21, pp. 219-237
  • Wolke, R.E., Piscine macrophage aggregates: a review (1992) Annu. Rev. Fish Dis., 2, pp. 91-108
  • Zagatto, A.P., Bertoletti, E., Ecotoxicologia Aquática - Princípios e Aplicações (2008), São Carlos, Brazil

Citas:

---------- APA ----------
de Campos, M.F., Lo Nostro, F.L., Da Cuña, R.H. & Moreira, R.G. (2018) . Endocrine disruption of phenanthrene in the protogynous dusky grouper Epinephelus marginatus (Serranidae: Perciformes). General and Comparative Endocrinology, 257, 255-263.
http://dx.doi.org/10.1016/j.ygcen.2017.06.020
---------- CHICAGO ----------
de Campos, M.F., Lo Nostro, F.L., Da Cuña, R.H., Moreira, R.G. "Endocrine disruption of phenanthrene in the protogynous dusky grouper Epinephelus marginatus (Serranidae: Perciformes)" . General and Comparative Endocrinology 257 (2018) : 255-263.
http://dx.doi.org/10.1016/j.ygcen.2017.06.020
---------- MLA ----------
de Campos, M.F., Lo Nostro, F.L., Da Cuña, R.H., Moreira, R.G. "Endocrine disruption of phenanthrene in the protogynous dusky grouper Epinephelus marginatus (Serranidae: Perciformes)" . General and Comparative Endocrinology, vol. 257, 2018, pp. 255-263.
http://dx.doi.org/10.1016/j.ygcen.2017.06.020
---------- VANCOUVER ----------
de Campos, M.F., Lo Nostro, F.L., Da Cuña, R.H., Moreira, R.G. Endocrine disruption of phenanthrene in the protogynous dusky grouper Epinephelus marginatus (Serranidae: Perciformes). Gen. Comp. Endocrinol. 2018;257:255-263.
http://dx.doi.org/10.1016/j.ygcen.2017.06.020