Ancestral benzo[a]pyrene exposure affects bone integrity in F3 adult fish (Oryzias latipes)

Frauke Seemann; Chang Bum Jeong; Ge Zhang; Miles Teng Wan; Baosheng Guo; Drew Ryan Peterson; Jae Seong Lee; Doris Wai Ting Au

doi:10.1016/j.aquatox.2016.12.018

Ancestral benzo[a]pyrene exposure affects bone integrity in F3 adult fish (Oryzias latipes)

Frauke Seemann, Chang Bum Jeong, Ge Zhang, Miles Teng Wan, Baosheng Guo, Drew Ryan Peterson, Jae Seong Lee, Doris Wai Ting Au^*

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › peer-review

28 Citations (Scopus)

Abstract

Benzo[a]pyrene (BaP) at an environmentally relevant concentration (1 μg/L) has previously been shown to affect bone development in a transgenerational manner in F3 medaka (Oryzias latipes) larvae (17 dph). Here, we provide novel histomorphometric data demonstrating that the impaired bone formation at an early life stage is not recoverable and can result in a persistent transgenerational impairment of bone metabolism in F3 adult fish. A decrease in bone thickness and the occurrence of microcracks in ancestrally BaP-treated adult male fish (F3) were revealed by MicroCt measurement and histopathological analysis. The expression of twenty conserved bone miRNAs were screened in medaka and their relative expression (in the F3 ancestral BaP treatment vs the F3 control fish) were determined by quantitative real-time PCR. Attempt was made to link bone miRNA expression with the potential target bone mRNA expression in medaka. Five functional pairs of mRNA/miRNA were identified (Osx/miR-214, Col2a1b/miR-29b, Runx2/miR-204, Sox9b/miR-199a-3p, APC/miR-27b). Unique knowledge of bone-related miRNA expression in medaka in response to ancestral BaP-exposure in the F3 generation is presented. From the ecological risk assessment perspective, BaP needs to be regarded as a transgenerational skeletal toxicant which exerts a far-reaching impact on fish survival and fitness. Given that the underlying mechanisms of cartilage/bone formation are conserved between medaka and mammals, the results may also shed light on the potential transgenerational effect of BaP on skeletal disorders in mammals/humans.

Original language	English
Pages (from-to)	127-134
Number of pages	8
Journal	Aquatic Toxicology
Volume	183
DOIs	https://doi.org/10.1016/j.aquatox.2016.12.018
Publication status	Published - Feb 2017

Scopus Subject Areas

Aquatic Science
Health, Toxicology and Mutagenesis

User-Defined Keywords

Epigenetics
Osteoblast activity
Osteogenic miRNAs
Osterix
Polycyclic aromatic hydrocarbons
Transgenerational inheritance

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10.1016/j.aquatox.2016.12.018

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@article{e5fc563f7b6441eeba6f1f0824edb32c,

title = "Ancestral benzo[a]pyrene exposure affects bone integrity in F3 adult fish (Oryzias latipes)",

abstract = "Benzo[a]pyrene (BaP) at an environmentally relevant concentration (1 μg/L) has previously been shown to affect bone development in a transgenerational manner in F3 medaka (Oryzias latipes) larvae (17 dph). Here, we provide novel histomorphometric data demonstrating that the impaired bone formation at an early life stage is not recoverable and can result in a persistent transgenerational impairment of bone metabolism in F3 adult fish. A decrease in bone thickness and the occurrence of microcracks in ancestrally BaP-treated adult male fish (F3) were revealed by MicroCt measurement and histopathological analysis. The expression of twenty conserved bone miRNAs were screened in medaka and their relative expression (in the F3 ancestral BaP treatment vs the F3 control fish) were determined by quantitative real-time PCR. Attempt was made to link bone miRNA expression with the potential target bone mRNA expression in medaka. Five functional pairs of mRNA/miRNA were identified (Osx/miR-214, Col2a1b/miR-29b, Runx2/miR-204, Sox9b/miR-199a-3p, APC/miR-27b). Unique knowledge of bone-related miRNA expression in medaka in response to ancestral BaP-exposure in the F3 generation is presented. From the ecological risk assessment perspective, BaP needs to be regarded as a transgenerational skeletal toxicant which exerts a far-reaching impact on fish survival and fitness. Given that the underlying mechanisms of cartilage/bone formation are conserved between medaka and mammals, the results may also shed light on the potential transgenerational effect of BaP on skeletal disorders in mammals/humans.",

keywords = "Epigenetics, Osteoblast activity, Osteogenic miRNAs, Osterix, Polycyclic aromatic hydrocarbons, Transgenerational inheritance",

author = "Frauke Seemann and Jeong, {Chang Bum} and Ge Zhang and Wan, {Miles Teng} and Baosheng Guo and Peterson, {Drew Ryan} and Lee, {Jae Seong} and Au, {Doris Wai Ting}",

note = "Funding Information: The authors thank warmly K.L. Wong, K.K. Tan, H.M. Wong, J. Li, H. Nie, J.X. Li and H. Kang for technical assistance. The project was funded by the City University Grant (project no: 7004660), the Research Grant Council of the Hong Kong Special Administrative Region, China (project no: 9041943/CityU 160013) and the State Key Laboratory in Marine Pollution, City University of Hong Kong. The corresponding author was supported by the Brain Pool Fellowship, awarded by the Korean Federation of Science and Technology Societies.",

year = "2017",

month = feb,

doi = "10.1016/j.aquatox.2016.12.018",

language = "English",

volume = "183",

pages = "127--134",

journal = "Aquatic Toxicology",

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publisher = "Elsevier",

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T1 - Ancestral benzo[a]pyrene exposure affects bone integrity in F3 adult fish (Oryzias latipes)

AU - Seemann, Frauke

AU - Jeong, Chang Bum

AU - Zhang, Ge

AU - Wan, Miles Teng

AU - Guo, Baosheng

AU - Peterson, Drew Ryan

AU - Lee, Jae Seong

AU - Au, Doris Wai Ting

N1 - Funding Information: The authors thank warmly K.L. Wong, K.K. Tan, H.M. Wong, J. Li, H. Nie, J.X. Li and H. Kang for technical assistance. The project was funded by the City University Grant (project no: 7004660), the Research Grant Council of the Hong Kong Special Administrative Region, China (project no: 9041943/CityU 160013) and the State Key Laboratory in Marine Pollution, City University of Hong Kong. The corresponding author was supported by the Brain Pool Fellowship, awarded by the Korean Federation of Science and Technology Societies.

PY - 2017/2

Y1 - 2017/2

N2 - Benzo[a]pyrene (BaP) at an environmentally relevant concentration (1 μg/L) has previously been shown to affect bone development in a transgenerational manner in F3 medaka (Oryzias latipes) larvae (17 dph). Here, we provide novel histomorphometric data demonstrating that the impaired bone formation at an early life stage is not recoverable and can result in a persistent transgenerational impairment of bone metabolism in F3 adult fish. A decrease in bone thickness and the occurrence of microcracks in ancestrally BaP-treated adult male fish (F3) were revealed by MicroCt measurement and histopathological analysis. The expression of twenty conserved bone miRNAs were screened in medaka and their relative expression (in the F3 ancestral BaP treatment vs the F3 control fish) were determined by quantitative real-time PCR. Attempt was made to link bone miRNA expression with the potential target bone mRNA expression in medaka. Five functional pairs of mRNA/miRNA were identified (Osx/miR-214, Col2a1b/miR-29b, Runx2/miR-204, Sox9b/miR-199a-3p, APC/miR-27b). Unique knowledge of bone-related miRNA expression in medaka in response to ancestral BaP-exposure in the F3 generation is presented. From the ecological risk assessment perspective, BaP needs to be regarded as a transgenerational skeletal toxicant which exerts a far-reaching impact on fish survival and fitness. Given that the underlying mechanisms of cartilage/bone formation are conserved between medaka and mammals, the results may also shed light on the potential transgenerational effect of BaP on skeletal disorders in mammals/humans.

AB - Benzo[a]pyrene (BaP) at an environmentally relevant concentration (1 μg/L) has previously been shown to affect bone development in a transgenerational manner in F3 medaka (Oryzias latipes) larvae (17 dph). Here, we provide novel histomorphometric data demonstrating that the impaired bone formation at an early life stage is not recoverable and can result in a persistent transgenerational impairment of bone metabolism in F3 adult fish. A decrease in bone thickness and the occurrence of microcracks in ancestrally BaP-treated adult male fish (F3) were revealed by MicroCt measurement and histopathological analysis. The expression of twenty conserved bone miRNAs were screened in medaka and their relative expression (in the F3 ancestral BaP treatment vs the F3 control fish) were determined by quantitative real-time PCR. Attempt was made to link bone miRNA expression with the potential target bone mRNA expression in medaka. Five functional pairs of mRNA/miRNA were identified (Osx/miR-214, Col2a1b/miR-29b, Runx2/miR-204, Sox9b/miR-199a-3p, APC/miR-27b). Unique knowledge of bone-related miRNA expression in medaka in response to ancestral BaP-exposure in the F3 generation is presented. From the ecological risk assessment perspective, BaP needs to be regarded as a transgenerational skeletal toxicant which exerts a far-reaching impact on fish survival and fitness. Given that the underlying mechanisms of cartilage/bone formation are conserved between medaka and mammals, the results may also shed light on the potential transgenerational effect of BaP on skeletal disorders in mammals/humans.

KW - Epigenetics

KW - Osteoblast activity

KW - Osteogenic miRNAs

KW - Osterix

KW - Polycyclic aromatic hydrocarbons

KW - Transgenerational inheritance

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DO - 10.1016/j.aquatox.2016.12.018

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AN - SCOPUS:85008222861

SN - 0166-445X

VL - 183

SP - 127

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JO - Aquatic Toxicology

JF - Aquatic Toxicology

ER -

Ancestral benzo[a]pyrene exposure affects bone integrity in F3 adult fish (Oryzias latipes)

Abstract

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