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Brain Aromatase in the guppy, Poecilia reticulata: Distribution, control and role in behaviour
Stockholm University, Faculty of Science, Department of Zoology. (Håkan Olsén)
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Oestrogens are produced by aromatisation of androgens by the aromatase enzyme. In the vertebrate brain this synthesis has vital functions in nerve protection, cell proliferation and nerve development during injury respectively brain development. Brain oestrogens are also crucial in activating certain reproductive and aggressive behaviours in mammals and birds. Teleosts have remarkably high activity of brain aromatase (bAA) compared to mammals and birds; 100-1000 times higher in brain regions like the hypothalamus, pre-optic area and optic tectum. The role of brain oestrogens in teleost behaviour is, however, less clear than in e.g. songbirds and rodents. This thesis studies the potential role of brain aromatase and brain oestrogens in the reproductive behaviour of the guppy male (Poecilia reticulata), how guppy brain aromatase responds to steroids and is distributed in the adult brain.

The thesis shows that male behaviour can be affected by brain aromatase. Reduction of bAA by aromatase inhibitor treatment reduced the sexual behaviours sigmoid display and gonopodium swinging (I) and oestrogen receptor blocking with an oestrogen antagonist reduced the number of successful mating attempts (II). The anatomical study (IV) showed that brain aromatase is distributed in areas of the adult guppy brain that are connected to reproductive control and behaviour in vertebrates.

Guppy bAA is stimulated by both androgens and oestrogens (III) but is more sensitive to oestrogens, especially in males, and could thus be used as an indicator of endocrine disruption at low concentrations found in the environment.

The thesis can also conclude that females possess more brain aromatase than males, and that although it is expressed in the same pattern throughout the brain in both genders the enzymatic activity is differently distributed between the sexes.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2009. , 41 p.
Series
Södertörn Doctoral Dissertations, ISSN 1652-7399 ; 36
Keyword [en]
Oestrogen production, behaviour, anatomy, endocrinology, bio markers, endocrine disruption
National Category
Microbiology
Research subject
Functional Zoomorphology
Identifiers
URN: urn:nbn:se:su:diva-26942ISBN: 978-91-86069-03-2 (print)ISBN: 978-91-7155-870-1 (print)OAI: oai:DiVA.org:su-26942DiVA: diva2:211967
Public defence
2009-05-26, MA624, Södertörns högskola, Alfred Nobels allé 7, Huddinge, 10:00 (English)
Opponent
Supervisors
Projects
Aromatase and androgens in fish reproductive behaviour
Available from: 2009-05-05 Created: 2009-04-20 Last updated: 2009-06-09Bibliographically approved
List of papers
1. Inhibition of cytochrome p450 brain aromatase reduces two male specific sexual behaviours in the male Endler guppy (Poecilia reticulata)
Open this publication in new window or tab >>Inhibition of cytochrome p450 brain aromatase reduces two male specific sexual behaviours in the male Endler guppy (Poecilia reticulata)
2006 (English)In: General and Comparative Endocrinology, ISSN 0016-6480, Vol. 147, no 3, 323-328 p.Article in journal (Refereed) Published
Abstract [en]

In mammalian and avian vertebrate groups, androgens act as controlling agents on male aggression and courtship behaviour by their conversion to oestrogens by cytochrome P450 aromatase in well-defined brain regions. Despite the fact that bony fishes have exceptionally high brain aromatase activity, little is known about it’s possible regulatory effects on the reproductive behaviours of teleosts. In this study, Endler guppy males (Poecilia reticulata) were subjected to 26–29 days of 24-h exposure to two different concentrations (15 and 100 μg/L) of the aromatase inhibitor fadrozole in the water. Compared with the control males, two of three courtship activities in males exposed to the higher concentration were reduced when they were paired with receptive stimulus females. Reduction in brain aromatase activity was confirmed in both exposed groups with the use of the tritiated water assay.

Place, publisher, year, edition, pages
Amsterdam, The Netherlands: Elsevier, 2006
Keyword
Brain aromatase; Teleost brain; Poecilia reticulata; Courtship behaviour
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-26902 (URN)10.1016/j.ygcen.2006.02.005 (DOI)
Projects
Aromatase and androgens in fish reproductive behaviour
Available from: 2009-04-20 Created: 2009-04-17 Last updated: 2009-06-09Bibliographically approved
2. Impacts of synthetic oestrogen and antioestrogen treatments on courtship and mating behaviours in male guppies (Poecilia reticulata)
Open this publication in new window or tab >>Impacts of synthetic oestrogen and antioestrogen treatments on courtship and mating behaviours in male guppies (Poecilia reticulata)
(English)Manuscript (Other academic)
Abstract [en]

Understanding the neuroendocrinological mechanisms behind reproductive behaviour is fundamental when studying endocrine disruption. Neuroestrogen production is a key step in the activation of reproductive behaviours among vertebrates. The actions of estrogens are transmitted through estrogen receptors (ERs) in distinct brain nuclei. Here we report alterations in reproductive behaviours in guppy males following 55-day food treatments with the antiestrogen fulvestrant (ICI) and the synthetic oestrogen 17α-ethinylestradiol (EE2). Male courtship and mating attempts were severely reduced in EE2 treated males after both 27-30 and 41-55 days of treatment when paired with females. ICI treatment gave a significant reduction in the frequency of sigmoid display behaviour after 27-30 days of treatment, and an almost 2.5-fold increase in gonopodium thrusting after 41-55 days of treatment. ICI treated males also decreased their frequency in successful mating attempts in comparison to the control males. The neurological effects of ICI were confirmed by Real Time-PCR analysis for brain aromatase and ERα gene expression. ICI treatment suppressed aromatase expression to 64% and stimulated ERα gene expression by over 300%. These results indicate that oestrogen action via ERs may play an important role for the complete display of male courtship and mating behaviour in the guppy. The results also suggest that local steroids are involved in regulating brain aromatase expression and that the negative effects of EE2 on sexual behaviour are linked via endocrine disruption of gonadal function.

Keyword
Brain aromatase, estrogen receptors, xenoestrogens, teleost reproduction, fulvestrant
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-26903 (URN)
Projects
Aromatase and androgens in fish reproductive behaviour
Available from: 2009-04-20 Created: 2009-04-17 Last updated: 2010-01-14Bibliographically approved
3. Effects on Guppy brain aromatase activity following short-term steroid and 4-Nonyl phenol exposures
Open this publication in new window or tab >>Effects on Guppy brain aromatase activity following short-term steroid and 4-Nonyl phenol exposures
2010 (English)In: Environmental Toxicology, ISSN 1520-4081, E-ISSN 1522-7278, Vol. 25, no 3, 261-271 p.Article in journal (Refereed) Accepted
Abstract [en]

Brain oestrogen production, performed by the enzyme aromatase, can be disrupted/affected in teleost fish exposed to endocrine disruptors found in polluted aquatic environments. The guppy (Poecilia reticulata) was previously studied and confirmed to suffer negative effects on reproductive behaviours following inhibition of the brain aromatase reaction. Here Adult guppies (Poecilia reticulata) of both genders were subjected to known endocrine disruptors: the androgen androstenedione (A), the synthetic oestrogen 17α-ethynylestradiol (EE2) and the oestrogenic surfactant 4-nonylphenol (NP), at high (50 μg/L) and at environmentally relevant concentrations (10 ng/L EE2, 5 μg/L NP and 0.7 μg/L A) for two weeks followed by measurements of brain aromatase activity (bAA). In the adult males, bAA was stimulated by A and EE2 at 50 μg/L. Female activity was also stimulated by the higher oestrogenic treatment. At environmentally relevant concentrations only the EE2 treatment affected bAA, and only in males. The alkylphenolic substance NP produced no effect in either of the experiments, not on males nor females. The results indicate that short-term steroid treatments have stimulatory effects on guppy brain aromatase even at concentrations that can be found in the environment. We thus suggest bAA of adult guppies to be a suitable bioindicator of endocrine disruptors.

Keyword
Teleost brain, endocrine disruption, bio-indicator, 17α-ethynylestradiol, androstenedione
National Category
Zoology
Research subject
Functional Zoomorphology; Ecotoxicology
Identifiers
urn:nbn:se:su:diva-26904 (URN)10.1002/tox.20494 (DOI)
Projects
Aromatase and androgens in fish reproductive behaviour
Available from: 2009-04-20 Created: 2009-04-17 Last updated: 2010-08-02Bibliographically approved
4. Cloning, sequencing and In situ localisation of guppy brain aromatase, cyp19b
Open this publication in new window or tab >>Cloning, sequencing and In situ localisation of guppy brain aromatase, cyp19b
(English)Manuscript (Other academic)
Abstract [en]

Oestrogens are biosynthesised by cytochrome p450-aromatase (Cyp19). Brain oestrogens serve several important functions of which nerve protection, cell proliferation, nerve development and behaviour control are a few. Teleost brain aromatase activity is exceptionally high (between 100-1000 times) compared to mammals and birds. We have successfully cloned and sequenced a 950 bp long partial fragment of the guppy CYP19B gene (PrCyp19b) derived from adult brain mRNA. Sequence alignment of translated amino acid sequence shows PrCYP19b having high sequence similarity to teleost brain aromatase. Anatomical distribution of PrCYP19b expression in adult guppy brains was studied using in situ-hybridisation with an antisense riboprobe synthesised from the cloned PrCYP19b gene. Expression of brain aromatase appeared at ventricular surfaces of the ventral telencephalic zones and the pre-optic area, in the hypothalamus, the pituitary gland, optic tectum and the cerebellum. This pattern is similar to previously reported distribution of brain aromatase in other teleosts. Measurement of brain aromatase activity in telencephalon, mesencephalon/diencephalon and rhombencephalon revealed female guppies producing the most oestrogens in mesencephalon/diencephalon, whereas males produces the most oestrogens in both telencephalon and mesencephalon/diencephalon. This indicates that brain oestrogen production is sexually dimorphic in the guppy and may serve different functions in the two genders.

Keyword
Brain aromatase, teleost brain, In Situ-hybridisation, anatomical distribution
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-26905 (URN)
Projects
Aromatase and androgens in fish reproductive behaviour
Available from: 2009-04-20 Created: 2009-04-17 Last updated: 2010-01-14Bibliographically approved

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