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Article ; Online: The role of DNA methylation on gene expression in the vertebrae of ancestrally benzo[a]pyrene exposed F1 and F3 male medaka.

Wan, Teng / Mo, Jiezhang / Au, Doris Wai-Ting / Qin, Xian / Tam, Nathan Yi-Kan / Kong, Richard Yuen-Chong / Seemann, Frauke

Epigenetics

2023 Volume 18, Issue 1, Page(s) 2222246

Abstract: Benzo[a]pyrene (BaP) is ubiquitously present in the aquatic environment and has been identified as a bone toxicant. Previous studies have demonstrated that ancestral BaP exposure can cause transgenerational bone deformities in fish. Transgenerational ... ...

Abstract	Benzo[a]pyrene (BaP) is ubiquitously present in the aquatic environment and has been identified as a bone toxicant. Previous studies have demonstrated that ancestral BaP exposure can cause transgenerational bone deformities in fish. Transgenerational effects are thought to be caused by heritable epigenetic changes, such as DNA methylation, histone modification, and non-coding RNAs. To investigate the role of DNA methylation in BaP-induced transgenerational skeletal deformities and the related transcriptomic changes in deformed vertebrae, we examined the vertebrae of male F1 and F3 medaka fish using high-throughput RNA sequencing (RNA-seq) and whole-genome bisulphite sequencing (WGBS). The histological results revealed that osteoblast numbers at the vertebral bone decreased in the BaP-derived F1 and F3 adult males in comparison with the control group. Differentially methylated genes (DMGs) associated with osteoblastogenesis (F1 and F3), chondrogenesis (F1 and F3), and osteoclastogenesis (F3) were identified. However, RNA-seq data did not support the role of DNA methylation in the regulation of genes involved in skeletogenesis since there was very little correlation between the level of differential methylation and gene expression profiles related to skeletogenesis. Although DNA methylation plays a major role in the epigenetic regulation of gene expression, the dysregulation of vertebral gene expression patterns observed in the current study is most likely to be mediated by histone modification and miRNAs. Notably, RNA-seq and WGBS data indicated that genes related to nervous system development are more sensitive to ancestral BaP exposure, indicating a more complex transgenerational phenotype in response to ancestral BaP exposure.
MeSH term(s)	Animals ; Male ; DNA Methylation ; Epigenesis, Genetic ; Benzo(a)pyrene/toxicity ; Oryzias/genetics ; Spine ; MicroRNAs ; Gene Expression
Chemical Substances	Benzo(a)pyrene (3417WMA06D) ; MicroRNAs
Language	English
Publishing date	2023-06-16
Publishing country	United States
Document type	Journal Article
ISSN	1559-2308
ISSN (online)	1559-2308
DOI	10.1080/15592294.2023.2222246
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Article: Benzo[a]pyrene osteotoxicity and the regulatory roles of genetic and epigenetic factors: A review

Mo, Jiezhang / Au, Doris Wai-Ting / Guo, Jiahua / Winkler, Christoph / Kong, Richard Yuen-Chong / Seemann, Frauke

Critical reviews in environmental science and technology. 2022 Sept. 17, v. 52, no. 18

2022

Abstract: As a ubiquitous environmental pollutant, benzo[a]pyrene (BaP) has been extensively studied for over 80 years. While much research has focused on its genotoxic and carcinogenic effects, considerably less attention has been paid to the osteotoxicity of BaP. ...

Abstract	As a ubiquitous environmental pollutant, benzo[a]pyrene (BaP) has been extensively studied for over 80 years. While much research has focused on its genotoxic and carcinogenic effects, considerably less attention has been paid to the osteotoxicity of BaP. Notably, environmental exposure to BaP is associated with skeletal malformation and bone impairment. Recent studies indicated that ancestral BaP exposure can cause transgenerational osteotoxicity in the unexposed F3 offspring. The consequences of environmental BaP/PAH pollution are thus likely to be severe and require re-assessment. We have reviewed the research status of BaP osteotoxicity, and a summary of genetic and epigenetic factors in the regulation of bone metabolism is provided as the basis for elucidating the mechanisms underlying transgenerational BaP osteotoxicity. Based on published studies on this topic, we propose that the transgenerational inheritance of osteotoxicity in fish induced by ancestral BaP exposure is mediated via epigenetically dysregulated bone miRNAs/genes. Two possible epigenetic regulatory circuits of BaP on bone miRNAs and genes are proposed: (i) bone miRNAs are dysregulated via altered DNA methylation and/or histone modifications, affecting target gene expression/activity; (ii) dysregulation of bone genes through altered DNA methylation and/or histone modifications. Our proposed mode of action (MOA) intends to serve as a basis for hypothesis testing in further in-depth studies. We emphasize that future works must verify the proposed MOA to assess its human relevance, and to decipher the underlying mechanism(s) of transgenerational BaP osteotoxicity.
Keywords	DNA methylation ; abnormal development ; bone metabolism ; carcinogenicity ; environmental exposure ; epigenetics ; fish ; gene expression ; histones ; humans ; mechanism of action ; microRNA ; mutagens ; pollutants ; pollution ; progeny ; technology
Language	English
Dates of publication	2022-0917
Size	p. 3244-3282.
Publishing place	Taylor & Francis
Document type	Article
ZDB-ID	2030115-7
ISSN	1547-6537 ; 1064-3389
ISSN (online)	1547-6537
ISSN	1064-3389
DOI	10.1080/10643389.2021.1915052
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Article ; Online: Assessment of parental benzo[a]pyrene exposure-induced cross-generational neurotoxicity and changes in offspring sperm DNA methylome in medaka fish.

Wan, Teng / Au, Doris Wai-Ting / Mo, Jiezhang / Chen, Lianguo / Cheung, Kwok-Ming / Kong, Richard Yuen-Chong / Seemann, Frauke

Environmental epigenetics

2022 Volume 8, Issue 1, Page(s) dvac013

Abstract: Previous studies have revealed that DNA methylation changes could serve as potential genomic markers for environmental benzo[a]pyrene (BaP) exposure and intergenerational inheritance of various physiological impairments (e.g. obesity and reproductive ... ...

Abstract	Previous studies have revealed that DNA methylation changes could serve as potential genomic markers for environmental benzo[a]pyrene (BaP) exposure and intergenerational inheritance of various physiological impairments (e.g. obesity and reproductive pathologies). As a typical aromatic hydrocarbon pollutant, direct BaP exposure has been shown to induce neurotoxicity. To unravel the inheritance mechanisms of the BaP-induced bone phenotype in freshwater medaka, we conducted whole-genome bisulfite sequencing of F1 sperm and identified 776 differentially methylated genes (DMGs). Ingenuity pathway analysis revealed that DMGs were significantly enriched in pathways associated with neuronal development and function. Therefore, it was hypothesized that parental BaP exposure (1 μg/l, 21 days) causes offspring neurotoxicity. Furthermore, the possibility for sperm methylation as an indicator for a neurotoxic phenotype was investigated. The F0 adult brains and F1 larvae were analyzed for BaP-induced direct and inherited toxicity. Acetylcholinesterase activity was significantly reduced in the larvae, together with decreased swimming velocity. Molecular analysis revealed that the marker genes associated with neuron development and growth (
Language	English
Publishing date	2022-05-27
Publishing country	England
Document type	Journal Article
ZDB-ID	2831217-X
ISSN	2058-5888 ; 2058-5888
ISSN (online)	2058-5888
ISSN	2058-5888
DOI	10.1093/eep/dvac013
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Article: Transgenerational bone toxicity in F3 medaka (Oryzias latipes) induced by ancestral benzo[a]pyrene exposure: Cellular and transcriptomic insights

Mo, Jiezhang / Wan, Miles Teng / Au, Doris Wai-Ting / Shi, Jingchun / Tam, Nathan / Qin, Xian / Cheung, Napo K.M. / Lai, Keng Po / Winkler, Christoph / Kong, Richard Yuen-Chong / Seemann, Frauke

Journal of environmental sciences (China). 2022 Apr. 29,

2022

Abstract: Benzo[a]pyrene (BaP), a ubiquitous pollutant, raises environmental health concerns due to induction of bone toxicity in the unexposed offspring. Exposure of F0 ancestor medaka (Oryzias latipes) to 1 μg/L BaP for 21 days causes reduced vertebral bone ... ...

Abstract	Benzo[a]pyrene (BaP), a ubiquitous pollutant, raises environmental health concerns due to induction of bone toxicity in the unexposed offspring. Exposure of F0 ancestor medaka (Oryzias latipes) to 1 μg/L BaP for 21 days causes reduced vertebral bone thickness in the unexposed F3 male offspring. To reveal the inherited modifications, osteoblast (OB) abundance and molecular signaling pathways of transgenerational BaP-induced bone thinning were assessed. Histomorphometric analysis showed a reduction in OB abundance. Analyses of the miRNA and mRNA transcriptomes revealed the dysregulation of Wnt signaling (frzb/ola-miR-1–3p, sfrp5/ola-miR-96–5p/miR-455–5p) and bone morphogenetic protein (Bmp) signaling (bmp3/ola-miR-96–5p/miR-181b-5p/miR-199a-5p/miR-205–5p/miR-455–5p). Both pathways are major indicators of impaired bone formation, while the altered Rank signaling in osteoclasts (c-fos/miR-205–5p) suggests a potentially augmented bone resorption. Interestingly, a typical BaP-responsive pathway, the Nrf2-mediated oxidative stress response (gst/ola-miR-181b-5p/miR-199a-5p/miR-205), was also affected. Moreover, mRNA levels of epigenetic modification enzymes (e.g., hdac6, hdac7, kdm5b) were found dysregulated. The findings indicated that epigenetic factors (e.g., miRNAs, histone modifications) may directly regulate the expression of genes associated with transgenerational BaP bone toxicity and warrants further studies. The identified candidate genes and miRNAs may serve as potential biomarkers for BaP-induced bone disease and as indicators of historic exposures in wild fish for conservation purposes.
Keywords	Oryzias latipes ; ancestry ; biomarkers ; bone formation ; bone morphogenetic proteins ; bone resorption ; environmental health ; epigenetics ; histones ; males ; microRNA ; osteoblasts ; osteoclasts ; oxidative stress ; pollutants ; progeny ; stress response ; toxicity ; transcriptome ; transcriptomics ; wild fish ; China
Language	English
Dates of publication	2022-0429
Publishing place	Elsevier B.V.
Document type	Article
Note	Pre-press version
ZDB-ID	1092300-7
ISSN	1878-7320 ; 1001-0742
ISSN (online)	1878-7320
ISSN	1001-0742
DOI	10.1016/j.jes.2022.04.051
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Article: Transgenerational bone toxicity in F3 medaka (Oryzias latipes) induced by ancestral benzo[a]pyrene exposure: Cellular and transcriptomic insights.

Mo, Jiezhang / Wan, Miles Teng / Au, Doris Wai-Ting / Shi, Jingchun / Tam, Nathan / Qin, Xian / Cheung, Napo K M / Lai, Keng Po / Winkler, Christoph / Kong, Richard Yuen-Chong / Seemann, Frauke

Journal of environmental sciences (China)

2022 Volume 127, Page(s) 336–348

Abstract: Benzo[a]pyrene (BaP), a ubiquitous pollutant, raises environmental health concerns due to induction of bone toxicity in the unexposed offspring. Exposure of F0 ancestor medaka (Oryzias latipes) to 1 µg/L BaP for 21 days causes reduced vertebral bone ... ...

Abstract	Benzo[a]pyrene (BaP), a ubiquitous pollutant, raises environmental health concerns due to induction of bone toxicity in the unexposed offspring. Exposure of F0 ancestor medaka (Oryzias latipes) to 1 µg/L BaP for 21 days causes reduced vertebral bone thickness in the unexposed F3 male offspring. To reveal the inherited modifications, osteoblast (OB) abundance and molecular signaling pathways of transgenerational BaP-induced bone thinning were assessed. Histomorphometric analysis showed a reduction in OB abundance. Analyses of the miRNA and mRNA transcriptomes revealed the dysregulation of Wnt signaling (frzb/ola-miR-1-3p, sfrp5/ola-miR-96-5p/miR-455-5p) and bone morphogenetic protein (Bmp) signaling (bmp3/ola-miR-96-5p/miR-181b-5p/miR-199a-5p/miR-205-5p/miR-455-5p). Both pathways are major indicators of impaired bone formation, while the altered Rank signaling in osteoclasts (c-fos/miR-205-5p) suggests a potentially augmented bone resorption. Interestingly, a typical BaP-responsive pathway, the Nrf2-mediated oxidative stress response (gst/ola-miR-181b-5p/miR-199a-5p/miR-205), was also affected. Moreover, mRNA levels of epigenetic modification enzymes (e.g., hdac6, hdac7, kdm5b) were found dysregulated. The findings indicated that epigenetic factors (e.g., miRNAs, histone modifications) may directly regulate the expression of genes associated with transgenerational BaP bone toxicity and warrants further studies. The identified candidate genes and miRNAs may serve as potential biomarkers for BaP-induced bone disease and as indicators of historic exposures in wild fish for conservation purposes.
MeSH term(s)	Animals ; Male ; Oryzias/physiology ; Benzo(a)pyrene/toxicity ; Benzo(a)pyrene/analysis ; Benzo(a)pyrene/metabolism ; Transcriptome ; Water Pollutants, Chemical/analysis ; RNA, Messenger ; MicroRNAs/metabolism
Chemical Substances	Benzo(a)pyrene (3417WMA06D) ; Water Pollutants, Chemical ; RNA, Messenger ; MicroRNAs
Language	English
Publishing date	2022-05-10
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	1092300-7
ISSN	1878-7320 ; 1001-0742
ISSN (online)	1878-7320
ISSN	1001-0742
DOI	10.1016/j.jes.2022.04.051
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Article ; Online: Multigenerational Impacts of Benzo[

Mo, Jiezhang / Au, Doris Wai-Ting / Wan, Miles Teng / Shi, Jingchun / Zhang, Ge / Winkler, Christoph / Kong, Richard Yuen-Chong / Seemann, Frauke

Environmental science & technology

2020 Volume 54, Issue 19, Page(s) 12271–12284

Abstract: Ancestral benzo[ ...

Abstract	Ancestral benzo[
MeSH term(s)	Animals ; Benzo(a)pyrene/toxicity ; Calcification, Physiologic ; Male ; Oryzias ; Osteoblasts ; Osteogenesis ; Water Pollutants, Chemical/toxicity
Chemical Substances	Water Pollutants, Chemical ; Benzo(a)pyrene (3417WMA06D)
Language	English
Publishing date	2020-09-14
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1520-5851
ISSN (online)	1520-5851
DOI	10.1021/acs.est.0c02416
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Article: Multigenerational Impacts of Benzo[a]pyrene on Bone Modeling and Remodeling in Medaka (Oryzias latipes)

Mo, Jiezhang / Au, Doris Wai-Ting / Wan, Miles Teng / Shi, Jingchun / Zhang, Ge / Winkler, Christoph / Kong, Richard Yuen-Chong / Seemann, Frauke

Environmental science & technology. 2020 Aug. 25, v. 54, no. 19

2020

Abstract: Ancestral benzo[a]pyrene (BaP) (1 μg/L, 21 days) exposure has previously been shown to cause skeletal deformities in medaka (Oryzias latipes) larvae in the F1–F3 generation. However, when and how this deformity is induced during bone development remain ... ...

Abstract	Ancestral benzo[a]pyrene (BaP) (1 μg/L, 21 days) exposure has previously been shown to cause skeletal deformities in medaka (Oryzias latipes) larvae in the F1–F3 generation. However, when and how this deformity is induced during bone development remain to be elucidated. The col10a1:nlGFP/osx:mCherry double transgenic medaka model was employed to determine the temporal and spatial changes of col10a1:nlGFP- positive osteochondral progenitor cells (OPCs) and osx:mCherry-positive premature osteoblasts (POBs) [8 days postfertilization (dpf)–31 dpf] in combination with changes in bone mineralization at the tissue level. Ancestral BaP exposure delayed the development of col10a1:nlGFP- and osx:mCherry-positive osteoblasts and reduced the abundance of col10a1:nlGFP-positive osteoblast progenitors and col10a1:nlGFP/osx:mCherry double-positive premature osteoblasts during critical windows of early vertebral bone formation, associated with reduced bone mineralization in embryos (14 dpf) and larvae (31 dpf), compressed vertebral segments in larvae (31 dpf), and reduced bone thickness in adult male medaka (6 months old) of the F1–F3 generations. Both Col10a1:nlGFP and osx:mCherry were identified as potential targets of epigenetic modifications underlying the transgenerational inheritance of BaP bone toxicity. The present study provides novel knowledge of the underlying mechanisms of transgenerational toxicity of BaP at the cellular level.
Keywords	Oryzias latipes ; adults ; bone mineralization ; environmental science ; epigenetics ; genetically modified organisms ; males ; models ; osteoblasts ; skeletal development ; technology ; toxicity
Language	English
Dates of publication	2020-0825
Size	p. 12271-12284.
Publishing place	American Chemical Society
Document type	Article
Note	NAL-AP-2-clean
ISSN	1520-5851
DOI	10.1021/acs.est.0c02416
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Article: Hypoxia causes sex-specific hepatic toxicity at the transcriptome level in marine medaka (Oryzias melastigma)

Lai, Keng Po / Tam, Nathan / Wang, Simon Yuan / Lin, Xiao / Chan, Ting Fung / Au, Doris Wai Ting / Wu, Rudolf Shiu Sun / Kong, Richard Yuen Chong

Aquatic toxicology. 2020 July, v. 224

2020

Abstract: Hypoxia, a low environmental oxygen level, is a common problem in the ocean globally. Hypoxia has been known to cause disruption to the endocrine system of marine organisms in both laboratory and field studies. Our previous studies have demonstrated the ... ...

Abstract	Hypoxia, a low environmental oxygen level, is a common problem in the ocean globally. Hypoxia has been known to cause disruption to the endocrine system of marine organisms in both laboratory and field studies. Our previous studies have demonstrated the sex-specific response to hypoxia in the neural and reproductive systems of marine fish. In the current report, we aim to study the sex-specific hepatic response of fish at the transcriptome level to hypoxic stress. By using a comparative transcriptome analysis, followed by a systematic bioinformatics analysis including Database for Annotation, Visualization and Integrated Discovery (DAVID) and Ingenuity Pathway Analysis (IPA), we found that hypoxia altered expression of genes related to cell proliferation and apoptosis of hepatocytes, which are associated with human pathologies, such as liver inflammation hepatic steatosis and steatohepatitis. Furthermore, we observed sex-specific responses in the livers of fish through different cell signaling pathways. In female fish, hypoxia causes dysregulation of expression of genes related to impairment in endoplasmic reticulum structure and liver metabolism. In male fish, genes associated with redox homeostasis and fatty acid metabolism were altered by hypoxic stress. The findings of this study support the notion that hypoxia could cause sex-specific changes (hepatic toxicity and changes) in marine fish.
Keywords	Oryzias melastigma ; apoptosis ; bioinformatics ; cell proliferation ; databases ; endocrine system ; endoplasmic reticulum ; fatty acid metabolism ; fatty liver ; females ; hepatocytes ; homeostasis ; humans ; hypoxia ; inflammation ; liver ; males ; marine fish ; oxygen ; toxicity ; toxicology ; transcriptome ; transcriptomics
Language	English
Dates of publication	2020-07
Publishing place	Elsevier B.V.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	782699-0
ISSN	1879-1514 ; 0166-445X
ISSN (online)	1879-1514
ISSN	0166-445X
DOI	10.1016/j.aquatox.2020.105520
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Article: Modulation of telomerase activity in fish muscle by biological and environmental factors.

Peterson, Drew Ryan / Mok, Helen Oi Lam / Au, Doris Wai Ting

Comparative biochemistry and physiology. Toxicology & pharmacology : CBP

2015 Volume 178, Page(s) 51–59

Abstract: Telomerase expression has long been linked to promotion of tumor growth and cell proliferation in mammals. Interestingly, telomerase activity (TA) has been detected in skeletal muscle for a variety of fish species. Despite this being a unique feature in ... ...

Abstract	Telomerase expression has long been linked to promotion of tumor growth and cell proliferation in mammals. Interestingly, telomerase activity (TA) has been detected in skeletal muscle for a variety of fish species. Despite this being a unique feature in fish, very few studies have investigated the potential role of TA in muscle. The present study was set to prove the concepts that muscle telomerase in fish is related to body growth, and more specifically, to muscle cell proliferation and apoptosis in vivo. Moreover, muscle TA can be influenced by biotic factors and modulated by environmental stress. Using three fish species, mangrove red snapper (Lutjanus argentimaculatus), orange-spotted grouper (Epinephelus coioides), and marine medaka (Oryzias melastigma), the present work reports for the first time that fish muscle TA was sensitive to the environmental stresses of starvation, foodborne exposure to benzo[a]pyrene, and hypoxia. In marine medaka, muscle TA was coupled with fish growth during early life stages. Upon sexual maturation, muscle TA was confounded by sex (female>male). Muscle TA was significantly correlated with telomerase reverse transcriptase (TERT) protein expression (Pearson correlation r=0.892; p≤0.05), which was coupled with proliferating cell nuclear antigen (PCNA) cell proliferation, but not associated with apoptosis (omBax/omBcl2 ratio) in muscle tissue. The results reported here have bridged the knowledge gap between the existence and function of telomerase in fish muscle. The underlying regulatory mechanisms of muscle TA in fish warrant further exploration for comparison with telomerase regulation in mammals.
MeSH term(s)	Animals ; Apoptosis/physiology ; Cell Proliferation/physiology ; Environment ; Female ; Fishes/metabolism ; Fishes/physiology ; Male ; Muscles/metabolism ; Proliferating Cell Nuclear Antigen/metabolism ; Telomerase/metabolism
Chemical Substances	Proliferating Cell Nuclear Antigen ; Telomerase (EC 2.7.7.49)
Language	English
Publishing date	2015-09-21
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	189285-x
ISSN	1532-0456 ; 0306-4492 ; 0742-8413
ISSN	1532-0456 ; 0306-4492 ; 0742-8413
DOI	10.1016/j.cbpc.2015.09.004
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Article: The development of cellular immune defence in marine medaka Oryzias melastigma.

Seemann, Frauke / Peterson, Drew Ryan / Chiang, Michael Wai Lun / Au, Doris Wai Ting

Comparative biochemistry and physiology. Toxicology & pharmacology : CBP

2017 Volume 199, Page(s) 81–89

Abstract: Environmentally induced alterations of the immune system during sensitive developmental stages may manifest as abnormalities in immune organ configuration and/or immune cell differentiation. These not only render the early life stages more vulnerable to ... ...

Abstract	Environmentally induced alterations of the immune system during sensitive developmental stages may manifest as abnormalities in immune organ configuration and/or immune cell differentiation. These not only render the early life stages more vulnerable to pathogens, but may also affect the adult immune competence. Knowledge of these sensitive periods in fish would provide an important prognostic/diagnostic tool for aquatic risk assessment of immunotoxicants. The marine medaka Oryzias melastigma is an emerging seawater fish model for immunotoxicology. Here, the presence and onset of four potentially sensitive periods during the development of innate and adaptive cellular immune defence were revealed in O. melastigma: 1.) initiation of phagocyte differentiation, 2.) migration and expansion of lymphoid progenitor cells, 3.) colonization of immune organs through lymphocyte progenitors and 4.) establishment of immune competence in the thymus. By using an established bacterial resistance assay for O. melastigma, larval immune competence (from newly hatched 1dph to 14dph) was found concomitantly increased with advanced thymus development and the presence of mature T-lymphocytes. A comparison between the marine O. melastigma and the freshwater counterpart Oryzias latipes disclosed a disparity in the T-lymphocyte maturation pattern, resulting in differences in the length of T-lymphocyte maturation. The results shed light on a potential difference between seawater and freshwater medaka in their sensitivity to environmental immunotoxicants. Further, medaka immune system development was compared and contrasted to economically important fish. The present study has provided a strong scientific basis for advanced investigation of critical windows for immune system development in fish.
MeSH term(s)	Animals ; Aquaculture ; Bacterial Load ; Cell Differentiation ; Edwardsiella tarda/growth & development ; Edwardsiella tarda/immunology ; Edwardsiella tarda/isolation & purification ; Embryo, Nonmammalian/cytology ; Embryo, Nonmammalian/immunology ; Embryo, Nonmammalian/microbiology ; Embryonic Development ; Gene Expression Regulation, Developmental ; Head Kidney/cytology ; Head Kidney/growth & development ; Head Kidney/immunology ; Head Kidney/microbiology ; Immunity, Cellular ; Immunity, Innate ; Immunocompetence ; In Situ Hybridization/veterinary ; Larva/cytology ; Larva/growth & development ; Larva/immunology ; Larva/microbiology ; Lymphoid Progenitor Cells/cytology ; Lymphoid Progenitor Cells/immunology ; Lymphoid Progenitor Cells/microbiology ; Morphogenesis ; Oryzias/embryology ; Oryzias/growth & development ; Oryzias/immunology ; Oryzias/microbiology ; Phagocytes/cytology ; Phagocytes/immunology ; Phagocytes/microbiology ; Species Specificity ; Spleen/cytology ; Spleen/growth & development ; Spleen/immunology ; Spleen/microbiology ; Survival Analysis ; T-Lymphocytes/cytology ; T-Lymphocytes/immunology ; T-Lymphocytes/microbiology ; Thymus Gland/cytology ; Thymus Gland/growth & development ; Thymus Gland/immunology ; Thymus Gland/microbiology
Language	English
Publishing date	2017-09
Publishing country	United States
Document type	Comparative Study ; Journal Article
ZDB-ID	189285-x
ISSN	1532-0456 ; 0306-4492 ; 0742-8413
ISSN	1532-0456 ; 0306-4492 ; 0742-8413
DOI	10.1016/j.cbpc.2017.03.010
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