Danio rerio as a model for studying reproductive risks associated with human exposure to polychlorinated biphenils: a systematic review

Cover Page

Cite item

Full Text

Abstract

This review presents the findings of a comprehensive investigation that involved a systematic search, critical analysis, and synthesis of scientific evidence regarding the impact of a broad range of persistent organic pollutants (POPs), including polychlorinated biphenyls (PCBs), on the reproductive functions, postembryonic survival, and morphofunctional development of offspring in the aquarium fish species Danio rerio, commonly known as Zebrafish. These fish are extensively utilized in experimental studies to simulate carcinogenic, mutagenic, and general toxic effects.

The literature search was conducted using Web of Science, Scopus, PubMed, and eLIBRARY.RU databases following the PRISMA 2020 recommendations. A total of 613 articles were identified, out of which 14 were selected for detailed analysis. Among them, 11 focused on assessing the impact of PCB exposure on the reproductive system of Danio rerio. Additionally, 8 articles reported on the results of studying the effects of parental exposure to PCBs on the viability and postembryonic development of their offspring. The adverse effects of PCBs, either alone or in combination with other POPs, have been studied to a lesser extent in male Danio rerio compared to females. Furthermore, the transmission of morphological and functional disorders to subsequent generations resulting from separate parental exposure to PCBs in both sexes, as well as the dose-response relationship, have not been adequately assessed based on the published works. Moreover, developmental disorders in offspring have mostly been studied for the first generation following parental exposure to mixtures of POPs and PCBs. The lack of such information hinders a proper evaluation of the transgenerational risk inheritance phenomenon, specifically regarding the transmission of morphological and functional disorders associated with progenitor exposure to PCBs and other environmental endocrine-disrupting pollutants.

The findings of this analysis can be used for planning experimental quantitative assessments, predicting, and preventing impairments to human reproductive health, and safeguarding the well-being of future generations.

About the authors

Dmitry A. Kotsur

Northern (Arctic) Federal University named after M.V. Lomonosov; N. Laverov Federal Center for Integrated Arctic Research

Author for correspondence.
Email: mitia.kotsur@yandex.ru
ORCID iD: 0000-0002-1216-9335
SPIN-code: 8124-3660
Scopus Author ID: 57210162204
ResearcherId: ABF-3591-2020

Cand. Sci. (Legal)

Russian Federation, 17 Northern Dvina embankment, 163002 Arkhangelsk; Arkhangelsk

Tatyana Yu. Sorokina

Northern (Arctic) Federal University named after M.V. Lomonosov

Email: t.sorokina@narfu.ru
ORCID iD: 0000-0002-4873-8747
SPIN-code: 1813-7323

Cand. Sci. (Legal)

Russian Federation, 17 Northern Dvina embankment, 163002 Arkhangelsk

Andrey S. Aksenov

Northern (Arctic) Federal University named after M.V. Lomonosov

Email: a.s.aksenov@narfu.ru
ORCID iD: 0000-0003-1013-1357
SPIN-code: 2267-4560

Cand. Sci. (Tech.), associate professor

Russian Federation, 17 Northern Dvina embankment, 163002 Arkhangelsk

Valery P. Chashchin

Northern (Arctic) Federal University named after M.V. Lomonosov; North-Western State Medical University named after I.I. Mechnikov; NSE University; Northwestern Scientific Center for Hygiene and Public Health

Email: valerych05@mail.ru
ORCID iD: 0000-0002-2600-0522
SPIN-code: 6989-1648

MD, Dr. Sci. (Med.), professor, head research associate, Institute of Ecology

Russian Federation, 17 Northern Dvina embankment, 163002 Arkhangelsk; Saint Petersburg; Moscow; Saint Petersburg

References

  1. Hu D, Hornbuckle KC. Inadvertent polychlorinated biphenyls in commercial paint pigments. Environ Sci Technol. 2010;44(8):2822–2827. doi: 10.1021/es902413k
  2. https://publications.iarc.fr/ [Internet]. Overall evaluations of carcinogenicity: an updating of IARC monographs volumes 1 to 42. In: IARC monographs on the evaluation of carcinogenic risks to humans. Supplement. 1987. Vol. 7 [cited 29 Jan 2023]. Available from: https://publications.iarc.fr/Book-And-Report-Series/Iarc-Monographs-Supplements/Overall-Evaluations-Of-Carcinogenicity-An-Updating-Of-IARC-Monographs-Volumes-1%E2%80%9342-1987
  3. Agency for Toxic Substances and Disease Registry. ATSDR case studies in environmental medicine. Polychlorinated biphenyls (PCBs) toxicity [Internet]. 2016. P. 90 [cited 10 Feb 2023]. Available from: https://www.atsdr.cdc.gov/csem/pcb/docs/pcb.pdf
  4. Hayes MA, Safe SH, Armstrong D, Cameron RG. Influence of cell proliferation on initiating activity of pure polychlorinated biphenyls and complex mixtures in resistant hepatocyte in vivo assays for carcinogenicity. J Natl Cancer Inst. 1985;74(5):1037–1041.
  5. Silberhorn EM, Glauert HP, Robertsson LW. Carcinogenicity of polyhalogenated biphenyls: PCBs and PBBs. Crit Rev Toxicol. 1990;20(6):440–496. doi: 10.3109/10408449009029331
  6. Tryphonas H, Luster MI, Schiffman G. Effect of chronic exposure of PCB (Aroclor 1254) on specific and nonspecific immune parameters in the rhesus (Macaca mulatta) monkeys. Fundam Appl Toxicol. 1991;16(4):639–648. doi: 10.1093/toxsci/16.4.773
  7. AMAP Assessment 2016: chemicals of emerging arctic concern. In: Arctic Monitoring and Assessment Programme (AMAP). Oslo: AMAP; 2017. P. xvi + 353 [cited 29 Jan 2023]. Available from: https://www.amap.no/documents/doc/amap-assessment-2016-chemicals-of-emerging-arctic-concern/1624
  8. UNEP, 2015 [Internet]. Expert Meeting on the Effectiveness Evaluation of Implementation of the Stockholm Convention for PCB and Sixth Meeting of the Advisory Committee of the PCB Elimination Network (PEN). In: Stockholm Convention on Persistent Organic Pollutants. Geneva; 2015:40 [cited 15 Jan 2023]. Available from: http://chm.pops.int/Implementation/IndustrialPOPs/PCB/Meetings/6thmeetingPENAdvisoryCommittee/tabid/4779/Default.aspx
  9. Nogales B, Moore ER, Llobet-Brossa E, et al. Combined use of 16S ribosomal DNA and 16S rRNA to study the bacterial community of polychlorinated biphenyl-polluted soil. Appl Environ Microbiol. 2001;67(4):1874–1884. doi: 10.1128/AEM.67.4.1874-1884.2001
  10. Di Lenola M, Caracciolo AB, Grenni P, et al. Effects of apirolio addition and alfalfa and compost treatments on the natural microbial community of a historically PCB-contaminated soil. Water Air Soil Pollution. 2018;229:143. doi: 10.1007/s11270-018-3803-4
  11. Lakhmanov D, Varakina Yu, Aksenov A, et al. Persistent organic pollutants (POPs) in fish consumed by the indigenous peoples from Nenets Autonomous Okrug. Environments. 2020;7(3):14. doi: 10.3390/environments7010003
  12. Varakina Y, Lakhmanov D, Aksenov A, et al. Concentrations of persistent organic pollutants in women’s serum in the European Arctic Russia. Toxics. 2021;9(1):12. doi: 10.3390/toxics9010006
  13. Tehrani R, Van AB. Hydroxylated polychlorinated biphenyls in the environment: sources, fate, and toxicities. Environ Sci Pollut Res Int. 2014;21(10):6334–6345. doi: 10.1007/s11356-013-1742-6
  14. He QL, Zhang L, Liu SZ. Effects of polychlorinated biphenyls on animal reproductive systems and epigenetic modifications. Bull Environ Contam Toxicol. 2021;107(3):398–405. doi: 10.1007/s00128-021-03285-6
  15. He QL, Wei XY, Han XY, et al. Effects of 2, 3', 4, 4', 5-pentachlorobiphenyl exposure during pregnancy on epigenetic imprinting and maturation of offspring's oocytes in mice. Arch Toxicol. 2019;93(9):2575–2592. doi: 10.1007/s00204-019-02529-z
  16. He QL, Lyu TQ, Zhang YT, Wang HQ, Zhou Q, Zhang JM, Liu YY, Li JS, Jiang LG, Cheng D, Ge ZJ, Liu SZ. Effects of intrauterine exposure to 2, 3', 4, 4', 5-pentachlorobiphenyl on the reproductive system and sperm epigenetic imprinting of male offspring. Journal of applied toxicology. 2020;40(10):1396–1409. doi: 10.1002/jat.3992
  17. Canadian Council on Animal Care Conseil canadien de protection des animaux. CCAC guidelines: Zebrafish and other small, warm-water laboratory fish. Ottawa: 2020. P. iv + 104 [cited: 21.12.2022]. Available from: https://ccac.ca/Documents/Standards/Guidelines/CCAC_Guidelines-Zebrafish_and_other_small_warm-water_laboratory_fish.pdf
  18. Belyaeva NF, Kashirtseva VN, Medvedeva NV, et al. Zebrafish as a model system for biomedical studies. Biochemistry (Moscow), Supplement Series B: Biomedical Chemistry. 2009;3(4):343–350. (In Russ). doi: 10.18097/PBMC20105601120
  19. Kozikova LV, Polteva EA, Lohmatova SA. Zebrafish (Danio rerio) — an object model for the study of developmental biology, and test-system for ecological risks. Genetika i razvedenie zhivotnyh. 2016;2:13–18. (In Russ).
  20. Xu H, Yang J, Wang Y, et al. Exposure to 17alpha-ethynylestradiol impairs reproductive functions of both male and female zebrafish (Danio rerio). Aquat Toxicol. 2008;88(1):1–8. doi: 10.1016/j.aquatox.2008.01.020
  21. Brion F, Tyler CR, Palazzi X, et al. Impacts of 17beta-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-, larval-, juvenile- and adult-life stages in zebrafish (Danio rerio). Aquat Toxicol. 2004;68(3):193–217. doi: 10.1016/j.aquatox.2004.01.022
  22. Liu H, Nie F-H, Lin HY, et al. Developmental toxicity, EROD, and CYP1A mRNA expression in zebrafish embryos exposed to dioxin-like PCB126. Environ Toxicol. 2016;31(2):201–210. doi: 10.1002/tox.22035
  23. Liu H, Gooneratne R, Huang X, et al. A rapid in vivo zebrafish model to elucidate oxidative stress mediated PCB126-induced apoptosis and developmental toxicity. Free Radic Biol Med. 2015;84:91–102. doi: 10.1016/j.freeradbiomed.2015.03.002
  24. Timme-Laragy AR, Sant KE, Rousseau ME, Dilorio PJ. Deviant development of pancreatic beta cells from embryonic exposure to PCB-126 in zebrafish. Comp Biochem Physiol C Toxicol Pharmacol. 2015;178:25–32. doi: 10.1016/j.cbpc.2015.08.012
  25. Zhang X, Hong Q, Yang L, et al. PCB1254 exposure contributes to the abnormalities of optomotor responses and influence of the photoreceptor cell development in zebrafish larvae. Ecotoxicol Environ Saf. 2015;118:133–138. doi: 10.1016/j.ecoenv.2015.04.026
  26. Ju L, Zhou Z, Jiang B, et al. MiR-21 is involved in skeletal deficiencies of zebrafish embryos exposed to polychlorinated biphenyls. Environ Sci Pollut Res Int. 2017;24(1):886–891. doi: 10.1007/s11356-016-7874-8
  27. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:71. doi: 10.1136/bmj.n71
  28. Pochinkova PA, Gorbatova MA, Narkevich AN, Grjibovski AM. Updated brief recommendations on writing and presenting systematic reviews: what’s new in PRISMA-2020 guidelines? Marine Medicine. 2022;8(2):88–101. (In Russ). doi: 10.22328/2413-5747-2022-8-2-88-101
  29. Billsson K, Westerlund L, Tysklind M, Olsson P-E. Developmental disturbances caused by polychlorinated biphenyls in zebrafish (Brachydanio rerio). Marine environmental research. 1998;46(1-5):461–464. doi: 10.1016/S0141-1136(97)00041-X
  30. Orn S, Andersson PL, Förlin L, et al. The impact on reproduction of an orally administered mixture of selected PCBs in zebrafish (Danio rerio). Arch Environ Contam Toxicol. 1998;35(1):52–57. doi: 10.1007/s002449900348
  31. Olsson PE, Westerlund L, Teh SJ, et al. Effects of maternal exposure to estrogen and PCB on different life stages of zebrafish (Danio rerio). Ambio. 1999;28(1):100–106.
  32. Westerlund L, Billsson K, Andersson PL, Tysklind M, Olsson PE. Early life-stage mortality in zebrafish (Danio rerio) following maternal exposure to polychlorinated biphenyls and estrogen. Environmental toxicology. 2000;19(6):1582–1588. doi: 10.1002/etc.5620190615
  33. Njiwa JR, Müller P, Klein R. Binary mixture of DDT and Arochlor1254: effects on sperm release by Danio rerio. Ecotoxicol Environ Saf. 2004;58(2):211–219. doi: 10.1016/j.ecoenv.2003.11.003
  34. Nourizadeh-Lillabadi R, Lyche JL, Almaas C, et al. Transcriptional regulation in liver and testis associated with developmental and reproductive effects in male Zebrafish exposed to natural mixtures of persistent organic pollutants (POP). J Toxicol Environ Health A. 2009;72(3-4):112–130. doi: 10.1080/15287390802537255
  35. Lyche JL, Nourizadeh-Lillabadi R, Almaas C, et al. Natural mixtures of persistent organic pollutants (pop) increase weight gain, advance puberty, and induce changes in gene expression associated with steroid hormones and obesity in female Zebrafish. J Toxicol Environ Health A. 2010;73(15):1032–1057. doi: 10.1080/15287394.2010.481618
  36. Berg V, Lyche JL, Karlsson C, et al. Accumulation and effects of natural mixtures of persistent organic pollutants (POP) in Zebrafish after two generations of exposure. J Toxicol Environ Health A. 2011;74(7-9):407–423. doi: 10.1080/15287394.2011.550455
  37. Daouk T, Larcher T, Roupsard F, et al. Long-term food-exposure of zebrafish to PCB mixtures mimicking some environmental situations induces ovary pathology and impairs reproduction ability. Aquat Toxicol. 2011;105(3-4):270–278. doi: 10.1016/j.aquatox.2011.06.021
  38. Kraugerud M, Doughty RW, Lyche JL, et al. Natural mixtures of persistent organic pollutants (POPs) suppress ovarian follicle development, liver vitellogenin immunostaining and hepatocyte proliferation in female zebrafish (Danio rerio). Aquat Toxicol. 2012;116-117:16–23. doi: 10.1016/j.aquatox.2012.02.031
  39. Horri K, Alfonso S, Cousin X, et al. Fish life-history traits are affected after chronic dietary exposure to an environmentally realistic marine mixture of PCBs and PBDEs. Sci Total Environ. 2018;610-611:531–545. doi: 10.1016/j.scitotenv.2017.08.083
  40. Quintaneiro C, Soares AMVM, Costa D, Monteiro MS. Effects of PCB-77 in adult zebrafish after exposure during early life stages. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2019;54(5):478–483. doi: 10.1080/10934529.2019.1568793
  41. Alfonso S, Blanc M, Joassard L, et al. Examining multi- and transgenerational behavioral and molecular alterations resulting from parental exposure to an environmental PCB and PBDE mixture. Aquat Toxicol. 2019;208:29–38. doi: 10.1016/j.aquatox.2018.12.021
  42. Blanc M, Alfonso S, Bégout ML, et al. An environmentally relevant mixture of polychlorinated biphenyls (PCBs) and polybrominated diphenylethers (PBDEs) disrupts mitochondrial function, lipid metabolism and neurotransmission in the brain of exposed Zebrafish and their unexposed F2 offspring. Sci Total Environ. 2021;754(1):142097. doi: 10.1016/j.scitotenv.2020.142097
  43. Arnoldsson K, Halden AN, Norrgren L, Haglund P. Retention and maternal transfer of environmentally relevant polybrominated dibenzo-p-dioxins and dibenzofurans, polychlorinated dibenzo-p-dioxins and dibenzofurans, and polychlorinated biphenyls in Zebrafish (Danio rerio) after dietary exposure. Environ Toxicol Chem. 2012;31(4):804–812. doi: 10.1002/etc.1750
  44. Tan Y, Sun D, Huang W, Cheng SH. Mechanical modeling of biological cells in microinjection. IEEE Trans Nanobioscience. 2008;7(4):257–266. doi: 10.1109/TNB.2008.2011852
  45. AMAP assessment 2015: human health in the Arctic. In: Arctic Monitoring and Assessment Programme (AMAP). Oslo; 2015. P. vii + 165 [cited 29 Jan 2023]. Available from: https://www.amap.no/documents/doc/Amapassessment-2015-Humanhealth-in-the-Arctic/1346
  46. Dudarev AA, Chupachin VS, Ivanova ZS, Lebedev GB. The blood levels of stable toxic substances in the native dwellers of coastal Chukotka and their children’s infection morbidity. Hygiene and Sanitation, Russian Journal. 2011;4:26–30. (In Russ).
  47. Dudarev AA, Chupakhin VS. Influence of exposure to persistent toxic substances (PTS) on pregnancy outcomes, gender ratio and menstrual status in indigenous females of Chukotka. Hygiene and Sanitation, Russian Journal. 2014;93(1):36–40. (In Russ).

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Flow chart of articles selection procedure.

Download (213KB)
Indexing metadata

Copyright (c) 2023 Eco-Vector

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
 


Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».