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Azole계열 항곰팡이 물질의 양서류 독성: 총설

Effects of Azole Fungicide on Amphibian: Review

  • 박찬진 (한양대학교 자연과학대학 생명과학과) ;
  • 박용아 (한양대학교 자연과학대학 생명과학과) ;
  • 옥승석 (한양대학교 자연과학대학 생명과학과) ;
  • 계명찬 (한양대학교 자연과학대학 생명과학과)
  • Park, Chan Jin (Department of Life Science, College of Natural Sciences, Hanyang University) ;
  • Park, Yong Ah (Department of Life Science, College of Natural Sciences, Hanyang University) ;
  • Ok, Seung Seok (Department of Life Science, College of Natural Sciences, Hanyang University) ;
  • Gye, Myung Chan (Department of Life Science, College of Natural Sciences, Hanyang University)
  • 투고 : 2014.02.18
  • 심사 : 2014.03.11
  • 발행 : 2014.03.31

초록

양서류는 육상과 수상생태계를 연결하는 먹이사슬의 연결자로 진화적 생태적 지이를 갖는다. 양서류의 배아와 유생은 모체와 독립되어 수환경 내에서 초기발생 및 성장하기 때문에 수환경에 존재하는 다양한 화학물질에 직접적으로 노출될 수 있다. Azole계열 항곰팡이제는 농업 및 의료용으로 널리 사용되는 화학물질로서 농지, 하수처리장 등으로 부터 수계로 유입된다. 최근, 양서류에서 이러한 azole계 물질에 의한 기형유발, 내분비계장애 효과가 증가하고 있다. 본 소고에서는 azole계 물질의 양서류 독성을 파악하고 azole계 물질의 안전한 이용을 위한 가이드라인을 제공하고자 azole계열에 속하는 imidazole, triazole, thiazole, oxazole, pyrazole 항곰팡이 물질이 양서류의 발생, 분화, 생식 등에 미치는 영향에 대해 최근까지의 연구결과를 정리하였다.

Amphibians play a pivotal role in the ecosystem as a mediator between aquatic and terrestrial environment. Currently they are directly exposed to a variety of chemicals in the aquatic environment throughout their life cycle. Azole fungicides have been widely used in medical applications and agricultural activities. The direct exposure of azole fungicides causes an alarming situation for various ecosystem. Recently, teratogenesis and endocrine disruption by azole fungicides have been reported in amphibians. In an effort to provide the current information for amphibian toxicity of azole fungicides and to make the guidelines for safe usage of azole-based materials, the effects of azole fungicides including imidazole, triazole, thiazole, oxazole, and pyrazoleon on early development, differentiation and reproduction of amphibians were reviewed.

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참고문헌

  1. Ankley GT, KM Jensen, EJ Durhan, EA Makynen, BC Butterworth, MD Kahl, DL Villeneuve, A Linnum, LE Gray, M Cardon and VS Wilson. 2005. Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fatheadminnow (Pimephales promelas). Toxicol. Sci. 86:300-308. https://doi.org/10.1093/toxsci/kfi202
  2. Baltzinger M, M Ori, M Pasqualetti, I Nardi and FM Rijli. 2005. Hoxa2 knockdown in Xenopus results in hyoid to mandibular homeosis. Dev. Dyn. 234:858-867. https://doi.org/10.1002/dvdy.20567
  3. Battaglin W, M Sandstrom, K Kuivila, D Kolpin and M Meyer. 2011. Occurrence of azoxystrobin, propiconazole, and selected other fungicides in US streams, 2005-2006. Water Air Soil Pollut. 218:307-322. https://doi.org/10.1007/s11270-010-0643-2
  4. Bogi C, J Schwaiger, H Ferling, U Mallow, C Steineck, F Sinowatz, W Kalbfus, RD Negele, I Lutz and W Kloas. 2003. Endocrine effects of environmental pollution on Xenopus laevis and Rana temporaria. Environ. Res. 93:195-201. https://doi.org/10.1016/S0013-9351(03)00082-3
  5. Boyer R and CE Grue. 1995. The need for water quality criteria for frogs. J. Environ. Health Perspect. 103:352-357. https://doi.org/10.1289/ehp.95103352
  6. Cha HJ, M Byrom, PE Mead, AD Ellington, JB Wallingford and EM Marcotte. 2012. Evolutionarily repurposed networks reveal the well-known antifungal drug thiabendazole to be a novel vascular disrupting agent. PLoS Biol. 10:e1001379. https://doi.org/10.1371/journal.pbio.1001379
  7. Chardard D and C Dournon. 1999. Sex reversal by aromatase inhibitor treatment in the Newt pleurodeles waltl. J. Exp. Zool. 283:43-50. https://doi.org/10.1002/(SICI)1097-010X(19990101)283:1<43::AID-JEZ6>3.0.CO;2-G
  8. Choi MJ, SC Kim, AN Kim, HB Kwon and RS Ahn. 2007. Effect of endocrine disruptors on the oocyte maturation and ovulation in amphibiansm, Rana dybowskii. Integ. Biosci. 11:1-8. https://doi.org/10.1080/17386357.2007.9647309
  9. Di Renzo F, R Bacchetta, A Bizzo, E Giavini and E Menegola. 2011b. Is the amphibian X. laevis WEC a good alternative method to rodent WEC teratogenicity assay? The example of the three triazole derivative fungicides Triadimefon, Tebuconazole, Cyproconazole. Reprod. Toxicol. 32:220-226. https://doi.org/10.1016/j.reprotox.2011.05.001
  10. Di Renzo F, R Bacchetta, L Sangiorgio, A Bizzo and E Menegola. 2011a. The agrochemical fungicide triadimefon induces abnormalities in Xenopus laevis embryos. Reprod. Toxicol. 31:486-493. https://doi.org/10.1016/j.reprotox.2011.01.003
  11. Durston AJ, J van der Wees, WW Pijnappel, JG Schilthuis and SF Godsave. 1997. Retinoid signalling and axial patterning during early vertebrate embryogenesis. Cell. Mol. Life Sci. 53:339-349. https://doi.org/10.1007/PL00000610
  12. El-Mofty MM, AE Essawy, MH Shwaired and HM Abdel- Karim. 2000. The use of swiss albino mice and egyptian toads (Bufo regularis) as reliable biological test animals for screening chemicals and drugs which induce leukaemia in man. I: The effect of Nizoral (ketoconazole) on leucocytes of toads and mice. Pakistan J. Biol. Sci. 3:411-414. https://doi.org/10.3923/pjbs.2000.411.414
  13. Essawy AE, AH El-Zoheiry, MM El-Mofty, SF Helal and EM El-Bardan. 2005. Pathological changes of the blood cells in fluconazole treated toads. Science Asia 31:43-47. https://doi.org/10.2306/scienceasia1513-1874.2005.31.043
  14. Essawy AE, SF Helal, AH El-Zoheiry and EM El-Bardan 2010. Hepatotoxicity induced by antifungal drug fluconazole in the Toads (Bufo Regularis). J. Drug Metabol. Toxicol. 1: 106-109.
  15. Gallien L and M Durocher. 1957. Table chronologique du developpement chez Pleurodeles waltl. Bull. Biol. Fr. Belg. 91:97-114.
  16. Ghannoum MA and LB Rice. 1999. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12:501-517.
  17. Gianessi L and N Reigner. 2006. Pesticide use in US crop production 2002-With comparison to 1992 & 1997. Washington, D.C., CropLife Foundation. Available at http://www. croplifefoundation.org.
  18. Gosner K. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183-190.
  19. Groppelli S, R Pennati, F De Bernardi, E Menegola, E Giavini and C Sotgia. 2005. Teratogenic effects of two antifungal triazoles, triadimefon and triadimenol, on Xenopus laevis development: craniofacial defects. Aquat. Toxicol. 73:370-381. https://doi.org/10.1016/j.aquatox.2005.04.004
  20. Gulden M, A Turan and H Seibert. 1997. Substanzen mit endokriner Wirkung in Oberflachengewassern. UBA-Texte 1997, 46/97, Berlin. Umweltbundesamt.
  21. Gyllenhammar I, E Hanna, S Anneli, HL Richard, F Jerker and B Cecilia. 2009. Clotrimazole exposure modulates aromatase activity in gonads and brain during gonadal differentiation in xenopus tropicalis forgs. Aquat. Toxicol. 91:102-109. https://doi.org/10.1016/j.aquatox.2008.10.005
  22. Han KT, KS Lee, EK Lee, YJ Lee, KY Ko, DJ Won, JW Lee and SD Kwon. 2003. Pesticide residue survey and estimate intake amount of vegetables in Noeun wholesale market, Daejeon. Korean J. Environ. Agri. 22:210-214. https://doi.org/10.5338/KJEA.2003.22.3.210
  23. Hewitt HG. 1998. Fungicides in Crop Protection. CAB International. New York. pp. 60-86.
  24. Hoffmann F and W Kloas. 2010. An environmentally relevant endocrine-disrupting antiandrogen, vinclozolin, affects calling behavior of male Xenopus laevis. Horm. Behav. 58:653-659. https://doi.org/10.1016/j.yhbeh.2010.06.008
  25. Hooser EA, JB Belden, LM Smith and ST McMurry. 2012. Acute toxicity of three strobilurin fungicide formulations and their active ingredients to tadpoles. Ecotoxicology 21: 1458-1464. https://doi.org/10.1007/s10646-012-0899-y
  26. Hunt P, M Gulisano, M Cook, MH Sham, A Faiella, D Wilkinson, E Boncinelli and R Krumlauf. 1991. A distinct Hox code for the branchial region of vertebrate head. Nature 353: 861-864. https://doi.org/10.1038/353861a0
  27. Iwan J. 1988. Pflanzenschutzmittel in grund- und trinkwasserergebnisse einer untersuchung in der bundesrepublik deutschland. Gesunde Pflanzen 40:208-213.
  28. Just P, U Greulach, G Henze and D Rinne. 1995. Trace analysis of vinclozolin by gas chromatography with electrolytic conductivity detection and solid-phase extraction. Fresenius J. Anal. Chem. 352:385-387. https://doi.org/10.1007/BF00322237
  29. Kahle M, IJ Buerge, A Hauser, MD Muller and T Poiger. 2008. Azole fungicides: occurrence and fate in wastewater and surface waters. Environ. Sci. Technol. 42:7193-7200. https://doi.org/10.1021/es8009309
  30. Kelce WR and EM Wilson. 1997. Environmental antiandrogens: developmental effects, molecular mechanisms, and clinical implications. J. Mol. Med. JMM 75:198-207. https://doi.org/10.1007/s001090050104
  31. Kidd H and DR James. (eds) 1991. The Agrochemicals Handbook. Third Edition. Royal Society of Chemistry Information Services, Cambridge, UK (As Updated).
  32. Kim AN, RS Ahn and HB Kwon. 2006. Effects of Azoles on the in vitro follicular steroidogenesis in amphibians. Integ. Biosci. 10:203-209. https://doi.org/10.1080/17386357.2006.9647303
  33. Kloas W and I Lutz. 2006. Amphibians as model to study endocrine distupters. J. Chromatogr. A 1130:16-27. https://doi.org/10.1016/j.chroma.2006.04.001
  34. Lahr J. 1997. Ecotoxicology of organisms adapted to life in temporary freshwater ponds in arid and semi-arid regions. Arch. Environ. Contam. Toxicol. 32:50-57. https://doi.org/10.1007/s002449900154
  35. Lenkowski JR, G Sanchez-Bravo and KA McLaughlin. 2010. Low concentrations of atrazine, glyphosate, 2,4-dichlorophenoxyacetic acid, and triadimefon exposures have diverse effects on Xenopus laevis organ morphogenesis. J. Environ. Sci. 22:1305-1308. https://doi.org/10.1016/S1001-0742(09)60254-0
  36. Levy G, I Lutz, A Kruger, W von Tumpling and W Kloas. 2004. Retinol-binding protein as a biomarker to assess endocrinedisrupting compounds in the environment. Anal. Bioanal. Chem. 378:676-683. https://doi.org/10.1007/s00216-003-2341-z
  37. Loeffler IK, DL Stocum, JF Fallon and CU Meteyer. 2001. Leaping lopsided: a review of the current hypotheses regarding etiologies of limp malformations in frogs. Anat. Rec. 265:228-245. https://doi.org/10.1002/ar.10009
  38. Martini F, C Fernandez, LS Segundo, JV Tarazona and MV Pablos. 2010. Assessment of potential immunotoxic effects caused by cypermethrin, fluoxetine, and thiabendazole using heat shock protein 70 and interleukin-1$\beta$ mRNA expression in the anuran Xenopus laevis. Environ Toxicol. Chem. 29: 2536-2543. https://doi.org/10.1002/etc.313
  39. McKearin DM and DJ Shapiro. 1988. Persistent estrogen induction of hepatic Xenopus laevis serum retinol binding protein mRNA. J. Biol. Chem. 263:3261-3265.
  40. McKearin DM, MC Barton, MJ Keller and DJ Shapiro. 1987. Estrogen induces transcription of the Xenopus laevis serum retinol-binding protein gene. J. Biol. Chem. 262:4939-4942.
  41. Menegola E, ML Broccia, Di Renzo F, V Massa and E Giavini. 2005. Study on the common teratogenic pathway elicited by the fungicides triazole-derivatives. Toxicol. In Vitro 19: 737-748. https://doi.org/10.1016/j.tiv.2005.04.005
  42. Nieuwkoop PD and J Faber. 1956. Normal Table of Xenopus laevis. North-Holland Publishing Company, Amsterdam.
  43. Norkova R, JJ Dytrtova, M Jakl and D Schroder. 2012. Formation of tebuconazole complexes with cadmium (II) investigated by electrospray ionization mass spectrometry. Water Air Soil Pollut. 223:2633-2640. https://doi.org/10.1007/s11270-011-1055-7
  44. Olmstead AW, PA Kosian, JJ Krte and GW Holcombe. 2009. Sex reversal of the amphibian, Xenopus tropicalis, following larval exposure to an aromatase inhibitor. Aquat. Toxicol. 91:143-150. https://doi.org/10.1016/j.aquatox.2008.07.018
  45. Papis E, G Bernardini, R Gornati and M Prati. 2006. Triadimefon causes branchial arch malformations in Xenopus laevis embryos. Environ. Sci. Pollut. Res. Int. 13:251-255. https://doi.org/10.1065/espr2006.01.014
  46. Papis E, G Bernardini, R Gornati, E Menegola and M Prati. 2007. Gene expression in Xenopus laevis embryos after Triadimefon exposure. Gene Expr. Patterns 7:137-142. https://doi.org/10.1016/j.modgep.2006.06.003
  47. Pasqualetti M, M Ori, I Nardi and FM Rijli. 2000. Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus. Development 127:5367-5378.
  48. Readman JW, TA Albanis, D Barcel, S Galassi, J Tronczynski and GP Gabrielides. 1997. Fungicide contamination of Mediterranean estuarine waters: results from a MED POL pilot survey. Mar. Pollut. Bull. 34:259-263. https://doi.org/10.1016/S0025-326X(97)00101-X
  49. Rijli FM, A Gavalas and P Chambon. 1998. Segmentation and specification in the branchial region of the head: the role of the Hox selector genes. Int. J. Dev. Biol. 42:393-401.
  50. Roberts PH and KV Thomas. 2006. The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Sci. Total Environ. 356:143-153. https://doi.org/10.1016/j.scitotenv.2005.04.031
  51. Safrin S. 2009. Antiviral agents. In: Katzung BG, Masters SB, Trevor AJ, editors. Basic and clinical pharmacology. 11th ed. New York: McGraw-Hill. pp. 845-875.
  52. Sheehan DJ, CA Hitchcock and CM Sibley. 1999. Current and emerging azole antifungal agents. Clin. Microbiol. Rev. 12: 40-79.
  53. Smalling KL, GM Fellers, PM Kleeman and KM Kuivila. 2013. Accumulation of pesticides in Pacific chorus frogs (Pseudacris regilla) from California's Sierra Nevada Mountains, USA. Environ. Toxicol. Chem. 32:2026-2034. https://doi.org/10.1002/etc.2308
  54. Thomas KV and MJ Hilton. 2004. The occurrence of selected human pharmaceutical compounds in UK estuaries. Mar. Pollut. Bull. 49:436-444. https://doi.org/10.1016/j.marpolbul.2004.02.028
  55. Tietge JE, SJ Degitz, JT Haselman, BC Butterworth, JJ Korte, PA Kosian, AJ Lindberg-Livingston, EM Burgess, PE Blackshear and MW Hornung. 2013. Inhibition of the thyroid hormone pathway in Xenopus laevis by 2-mercaptobenzothiazole. Aquat. Toxicol. 126:128-136. https://doi.org/10.1016/j.aquatox.2012.10.013
  56. Trosken ER, K Scholz, RW Lutz, W Volkel, JA Zarn and WK Lutz. 2004. Comparative assessment of the inhibition of recombinant human CYP19 (aromatase) by azoles used in agriculture and as drugs for humans. Endocr. Res. 30:387-394. https://doi.org/10.1081/ERC-200035093
  57. Trosken ER, N Bittner and W Volkel. 2005. Quantitation of 13 azole fungicides in wine samples by liquid chromatographytandem mass spectrometry. J. Chromatogr. A. 1083:113-119. https://doi.org/10.1016/j.chroma.2005.06.020
  58. van Wyk JH, EJ Pool and AJ Leslie. 2003. The effects of antiandrogenic and estrogenic disrupting contaminants on breeding gland (nuptial pad) morphology, plasma testosterone levels, and plasma vitellogenin levels in male Xenopus laevis (African clawed frog). Arch. Environ. Contam. Toxicol. 44: 247-256. https://doi.org/10.1007/s00244-002-1161-z
  59. White JA, YD Guo, K Baetz, B Beckett-Jones, J Bonasoro, KE Hsu, FJ Dilworth, G Jones and M Petkovich. 1996. Identification of the retinoic acid-inducible all-trans-retinoic acid 4-hydroxylase. J. Biol. Chem. 271:29922-29927. https://doi.org/10.1074/jbc.271.47.29922
  60. Zarn JA, BJ Bruschweiler and JR Schlatter. 2003. Azole fungicides affect mammalian steroidogenesis by inhibiting sterol 14 alpha-demethylase and aromatase. Environ. Health Perspect. 111:255-261.