Transgenerational hypocortisolism and behavioral disruption are induced by the antidepressant fluoxetine in male zebrafish Danio rerio
The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disrup...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 115; no. 52; pp. E12435 - E12442 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
26.12.2018
|
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F₀). This effect persists for three consecutive generations in the unexposed descendants (F₁ to F₃) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish “adrenal”) to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F₀ and F₃ FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F₀ and F₃ generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F₀ to F₂ FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs. |
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| AbstractList | The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F
). This effect persists for three consecutive generations in the unexposed descendants (F
to F
) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish "adrenal") to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F
and F
FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F
and F
generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F
to F
FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs. The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F0). This effect persists for three consecutive generations in the unexposed descendants (F1 to F3) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish “adrenal”) to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F0 and F3 FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F0 and F3 generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F0 to F2 FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs. The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F₀). This effect persists for three consecutive generations in the unexposed descendants (F₁ to F₃) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish “adrenal”) to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F₀ and F₃ FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F₀ and F₃ generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F₀ to F₂ FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs. The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F0). This effect persists for three consecutive generations in the unexposed descendants (F1 to F3) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish "adrenal") to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F0 and F3 FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F0 and F3 generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F0 to F2 FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs.The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F0). This effect persists for three consecutive generations in the unexposed descendants (F1 to F3) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish "adrenal") to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F0 and F3 FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F0 and F3 generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F0 to F2 FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs. The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F 0 ). This effect persists for three consecutive generations in the unexposed descendants (F 1 to F 3 ) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish “adrenal”) to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F 0 and F 3 FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F 0 and F 3 generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F 0 to F 2 FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs. Due to the high incidence of depression during childbearing, antidepressants such as fluoxetine (FLX) are highly prescribed during pregnancy, yet the risks to offspring are unknown. We report that a 6-day FLX exposure during early zebrafish development induces hypocortisolism for at least three generations. Gene expression analysis indicates that pathways controlling cortisol synthesis are altered in the descendants in the third generation. This FLX-induced low-cortisol phenotype is more prominent in males and is associated with significantly reduced exploratory behaviors for two generations. This is an important demonstration that, in an animal model, even a brief ancestral exposure to a common antidepressant modifies the stress response and critical coping behaviors for several generations. The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor fluoxetine (FLX) is often the first line of treatment. Given that FLX readily crosses the placenta, a fetus may be susceptible to the disruptive effects of FLX during this highly plastic stage of development. Here, we demonstrate that a 6-day FLX exposure to a fetus-relevant concentration at a critical developmental stage suppresses cortisol levels in the adult zebrafish (F 0 ). This effect persists for three consecutive generations in the unexposed descendants (F 1 to F 3 ) without diminution and is more pronounced in males. We also show that the in vivo cortisol response of the interrenal (fish “adrenal”) to an i.p. injection of adrenocorticotropic hormone was also reduced in the males from the F 0 and F 3 FLX lineages. Transcriptomic profiling of the whole kidney containing the interrenal cells revealed that early FLX exposure significantly modified numerous pathways closely associated with cortisol synthesis in the male adults from the F 0 and F 3 generations. We also show that the low cortisol levels are linked to significantly reduced exploratory behaviors in adult males from the F 0 to F 2 FLX lineages. This may be a cause for concern given the high prescription rates of FLX to pregnant women and the potential long-term negative impacts on humans exposed to these therapeutic drugs. |
| Author | Trudeau, Vance L. St-Jacques, Antony D. Martyniuk, Chris J. Gagné, Rémi Yauk, Carole L. Moon, Thomas W. Vera-Chang, Marilyn N. |
| Author_xml | – sequence: 1 givenname: Marilyn N. surname: Vera-Chang fullname: Vera-Chang, Marilyn N. organization: Department of Biology, University of Ottawa, Ottawa, ON K1N 6N5, Canada – sequence: 2 givenname: Antony D. surname: St-Jacques fullname: St-Jacques, Antony D. organization: Department of Chemistry and Biomolecular Sciences, University of Ottawa, Ottawa, ON K1N 6N5, Canada – sequence: 3 givenname: Rémi surname: Gagné fullname: Gagné, Rémi organization: Environmental Health Science and Research Bureau, Health Canada, Ottawa, ON K1A 0K9, Canada – sequence: 4 givenname: Chris J. surname: Martyniuk fullname: Martyniuk, Chris J. organization: University of Florida Genetics Institute, University of Florida, Gainesville, FL 32611 – sequence: 5 givenname: Carole L. surname: Yauk fullname: Yauk, Carole L. organization: Environmental Health Science and Research Bureau, Health Canada, Ottawa, ON K1A 0K9, Canada – sequence: 6 givenname: Thomas W. surname: Moon fullname: Moon, Thomas W. organization: Department of Biology, University of Ottawa, Ottawa, ON K1N 6N5, Canada – sequence: 7 givenname: Vance L. surname: Trudeau fullname: Trudeau, Vance L. organization: Department of Biology, University of Ottawa, Ottawa, ON K1N 6N5, Canada |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30530669$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author contributions: M.N.V.-C., T.W.M., and V.L.T. designed research; M.N.V.-C. performed research; A.D.S.-J., R.G., C.J.M., C.L.Y., T.W.M., and V.L.T. contributed new reagents/analytic tools; M.N.V.-C., A.D.S.-J., and R.G. analyzed data; and M.N.V.-C. wrote the paper. Edited by Bruce McEwen, The Rockefeller University, New York, NY, and approved November 8, 2018 (received for review July 17, 2018) |
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| Snippet | The global prevalence of depression is high during childbearing. Due to the associated risks to the mother and baby, the selective serotonin reuptake inhibitor... Due to the high incidence of depression during childbearing, antidepressants such as fluoxetine (FLX) are highly prescribed during pregnancy, yet the risks to... |
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| SubjectTerms | Adrenocorticotropic hormone Adults Animals Antidepressants Antidepressive Agents - pharmacology Behavior, Animal - drug effects Biological Sciences Danio rerio Depressive Disorder Developmental stages Disruption Epigenetics Exposure Family Characteristics Female Fetuses Fluoxetine Fluoxetine - adverse effects Fluoxetine - pharmacology Human exposure Hydrocortisone - metabolism Male Males Maternal Exposure - adverse effects Maternal-Fetal Exchange - drug effects Mental depression Placenta PNAS Plus Postpartum depression Pregnancy Serotonin Serotonin uptake inhibitors Serotonin Uptake Inhibitors - pharmacology Side effects Stress, Psychological Zebrafish Zebrafish - metabolism Zebrafish - physiology Zebrafish Proteins - metabolism |
| Title | Transgenerational hypocortisolism and behavioral disruption are induced by the antidepressant fluoxetine in male zebrafish Danio rerio |
| URI | https://www.jstor.org/stable/26573982 https://www.ncbi.nlm.nih.gov/pubmed/30530669 https://www.proquest.com/docview/2162456375 https://www.proquest.com/docview/2155151692 https://pubmed.ncbi.nlm.nih.gov/PMC6310822 |
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