Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages

Sonia M. Johns, Nancy D. Denslow, Michael D. Kane, Karen Watanabe-Sailor, Edward F. Orlando, Maria S. Sepúlveda

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

Endocrine disrupting chemicals (EDCs) are known to contaminate aquatic environments and alter the growth and reproduction of organisms. The objective of this study was to evaluate the sensitivity and utility of fathead minnow (Pimephales promelas) early life-stages as a model to measure effects of estrogenic and antiestrogenic EDCs on physiological and gene expression endpoints relative to growth and reproduction. Embryos (<24-h postfertilization, hpf) were exposed to a potent estrogen (17α-ethinyl estradiol, EE2, 2, 10, and 50 ng L-1); a weak estrogen (mycotoxin zearalenone, ZEAR, same concentrations as above); an antiestrogen (ZM 189, 154; 40, 250, and 1000 ng L-1); and to mixtures of EE2 and ZM until swim-up stage (∼170 hpf). Exposure to all concentrations of ZEAR and to the lowest concentration of ZM resulted in increased body sizes, whereas high concentrations of EE2 decreased body sizes. There was a significant increase in the frequency of abnormalities (mostly edema) in larvae exposed to all concentrations of EE2, and high ZEAR, and EE2 + ZM mixture groups. Expression of growth hormone was upregulated by most of the conditions tested. Exposure to 50 ng L-1 ZEAR caused an induction of insulin-like growth factor 1, whereas exposure to 40 ng L-1 ZM caused a downregulation of this gene. Expression of steroidogenic acute regulatory protein gene was significantly upregulated after exposure to all concentrations of EE2 and luteinizing hormone expression increased significantly in response to all treatments tested. As expected, EE2 induced vitellogenin expression; however, ZEAR also induced expression of this gene to similar levels compared to EE2. Overall, exposure to EE2 + ZM mixture resulted in a different expression pattern compared to single exposures. The results of this study suggest that an early life stage 7-day exposure is sufficient to recognize and evaluate effects of estrogenic compounds on gene expression in this fish model.

Original languageEnglish (US)
Pages (from-to)195-206
Number of pages12
JournalEnvironmental Toxicology
Volume26
Issue number2
DOIs
StatePublished - Apr 2011
Externally publishedYes

Fingerprint

Cyprinidae
Estrogen Receptor Modulators
Gene expression
gene expression
Endocrine Disruptors
Estrogens
Genes
Body Size
Gene Expression
Reproduction
Zearalenone
Vitellogenins
Ethinyl Estradiol
Mycotoxins
Somatomedins
Regulator Genes
Growth
Luteinizing Hormone
Fish
Growth Hormone

Keywords

  • Early life-stages
  • EE2
  • Endocrine disrupting chemicals
  • Zearalanone

ASJC Scopus subject areas

  • Health, Toxicology and Mutagenesis
  • Toxicology
  • Management, Monitoring, Policy and Law

Cite this

Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages. / Johns, Sonia M.; Denslow, Nancy D.; Kane, Michael D.; Watanabe-Sailor, Karen; Orlando, Edward F.; Sepúlveda, Maria S.

In: Environmental Toxicology, Vol. 26, No. 2, 04.2011, p. 195-206.

Research output: Contribution to journalArticle

Johns, Sonia M. ; Denslow, Nancy D. ; Kane, Michael D. ; Watanabe-Sailor, Karen ; Orlando, Edward F. ; Sepúlveda, Maria S. / Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages. In: Environmental Toxicology. 2011 ; Vol. 26, No. 2. pp. 195-206.
@article{a0dc956fa4624aa7ad1dbc99240c0046,
title = "Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages",
abstract = "Endocrine disrupting chemicals (EDCs) are known to contaminate aquatic environments and alter the growth and reproduction of organisms. The objective of this study was to evaluate the sensitivity and utility of fathead minnow (Pimephales promelas) early life-stages as a model to measure effects of estrogenic and antiestrogenic EDCs on physiological and gene expression endpoints relative to growth and reproduction. Embryos (<24-h postfertilization, hpf) were exposed to a potent estrogen (17α-ethinyl estradiol, EE2, 2, 10, and 50 ng L-1); a weak estrogen (mycotoxin zearalenone, ZEAR, same concentrations as above); an antiestrogen (ZM 189, 154; 40, 250, and 1000 ng L-1); and to mixtures of EE2 and ZM until swim-up stage (∼170 hpf). Exposure to all concentrations of ZEAR and to the lowest concentration of ZM resulted in increased body sizes, whereas high concentrations of EE2 decreased body sizes. There was a significant increase in the frequency of abnormalities (mostly edema) in larvae exposed to all concentrations of EE2, and high ZEAR, and EE2 + ZM mixture groups. Expression of growth hormone was upregulated by most of the conditions tested. Exposure to 50 ng L-1 ZEAR caused an induction of insulin-like growth factor 1, whereas exposure to 40 ng L-1 ZM caused a downregulation of this gene. Expression of steroidogenic acute regulatory protein gene was significantly upregulated after exposure to all concentrations of EE2 and luteinizing hormone expression increased significantly in response to all treatments tested. As expected, EE2 induced vitellogenin expression; however, ZEAR also induced expression of this gene to similar levels compared to EE2. Overall, exposure to EE2 + ZM mixture resulted in a different expression pattern compared to single exposures. The results of this study suggest that an early life stage 7-day exposure is sufficient to recognize and evaluate effects of estrogenic compounds on gene expression in this fish model.",
keywords = "Early life-stages, EE2, Endocrine disrupting chemicals, Zearalanone",
author = "Johns, {Sonia M.} and Denslow, {Nancy D.} and Kane, {Michael D.} and Karen Watanabe-Sailor and Orlando, {Edward F.} and Sep{\'u}lveda, {Maria S.}",
year = "2011",
month = "4",
doi = "10.1002/tox.20545",
language = "English (US)",
volume = "26",
pages = "195--206",
journal = "Environmental Toxicology",
issn = "1520-4081",
publisher = "John Wiley and Sons Inc.",
number = "2",

}

TY - JOUR

T1 - Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages

AU - Johns, Sonia M.

AU - Denslow, Nancy D.

AU - Kane, Michael D.

AU - Watanabe-Sailor, Karen

AU - Orlando, Edward F.

AU - Sepúlveda, Maria S.

PY - 2011/4

Y1 - 2011/4

N2 - Endocrine disrupting chemicals (EDCs) are known to contaminate aquatic environments and alter the growth and reproduction of organisms. The objective of this study was to evaluate the sensitivity and utility of fathead minnow (Pimephales promelas) early life-stages as a model to measure effects of estrogenic and antiestrogenic EDCs on physiological and gene expression endpoints relative to growth and reproduction. Embryos (<24-h postfertilization, hpf) were exposed to a potent estrogen (17α-ethinyl estradiol, EE2, 2, 10, and 50 ng L-1); a weak estrogen (mycotoxin zearalenone, ZEAR, same concentrations as above); an antiestrogen (ZM 189, 154; 40, 250, and 1000 ng L-1); and to mixtures of EE2 and ZM until swim-up stage (∼170 hpf). Exposure to all concentrations of ZEAR and to the lowest concentration of ZM resulted in increased body sizes, whereas high concentrations of EE2 decreased body sizes. There was a significant increase in the frequency of abnormalities (mostly edema) in larvae exposed to all concentrations of EE2, and high ZEAR, and EE2 + ZM mixture groups. Expression of growth hormone was upregulated by most of the conditions tested. Exposure to 50 ng L-1 ZEAR caused an induction of insulin-like growth factor 1, whereas exposure to 40 ng L-1 ZM caused a downregulation of this gene. Expression of steroidogenic acute regulatory protein gene was significantly upregulated after exposure to all concentrations of EE2 and luteinizing hormone expression increased significantly in response to all treatments tested. As expected, EE2 induced vitellogenin expression; however, ZEAR also induced expression of this gene to similar levels compared to EE2. Overall, exposure to EE2 + ZM mixture resulted in a different expression pattern compared to single exposures. The results of this study suggest that an early life stage 7-day exposure is sufficient to recognize and evaluate effects of estrogenic compounds on gene expression in this fish model.

AB - Endocrine disrupting chemicals (EDCs) are known to contaminate aquatic environments and alter the growth and reproduction of organisms. The objective of this study was to evaluate the sensitivity and utility of fathead minnow (Pimephales promelas) early life-stages as a model to measure effects of estrogenic and antiestrogenic EDCs on physiological and gene expression endpoints relative to growth and reproduction. Embryos (<24-h postfertilization, hpf) were exposed to a potent estrogen (17α-ethinyl estradiol, EE2, 2, 10, and 50 ng L-1); a weak estrogen (mycotoxin zearalenone, ZEAR, same concentrations as above); an antiestrogen (ZM 189, 154; 40, 250, and 1000 ng L-1); and to mixtures of EE2 and ZM until swim-up stage (∼170 hpf). Exposure to all concentrations of ZEAR and to the lowest concentration of ZM resulted in increased body sizes, whereas high concentrations of EE2 decreased body sizes. There was a significant increase in the frequency of abnormalities (mostly edema) in larvae exposed to all concentrations of EE2, and high ZEAR, and EE2 + ZM mixture groups. Expression of growth hormone was upregulated by most of the conditions tested. Exposure to 50 ng L-1 ZEAR caused an induction of insulin-like growth factor 1, whereas exposure to 40 ng L-1 ZM caused a downregulation of this gene. Expression of steroidogenic acute regulatory protein gene was significantly upregulated after exposure to all concentrations of EE2 and luteinizing hormone expression increased significantly in response to all treatments tested. As expected, EE2 induced vitellogenin expression; however, ZEAR also induced expression of this gene to similar levels compared to EE2. Overall, exposure to EE2 + ZM mixture resulted in a different expression pattern compared to single exposures. The results of this study suggest that an early life stage 7-day exposure is sufficient to recognize and evaluate effects of estrogenic compounds on gene expression in this fish model.

KW - Early life-stages

KW - EE2

KW - Endocrine disrupting chemicals

KW - Zearalanone

UR - http://www.scopus.com/inward/record.url?scp=79952757443&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79952757443&partnerID=8YFLogxK

U2 - 10.1002/tox.20545

DO - 10.1002/tox.20545

M3 - Article

VL - 26

SP - 195

EP - 206

JO - Environmental Toxicology

JF - Environmental Toxicology

SN - 1520-4081

IS - 2

ER -