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Plasticity in ion channel expression underlies variation in hearing during reproductive cycles.

ABSTRACT: Sensory plasticity related to reproductive state, hormonal profiles, and experience is widespread among vertebrates, including humans. Improvements in audio-vocal coupling that heighten the detection of conspecifics are part of the reproductive strategy of many nonmammalian vertebrates. Although seasonal changes in hearing are known, molecular mechanisms determining this form of adult sensory plasticity remain elusive. Among both nonmammals and mammals, large-conductance, calcium-activated potassium (BK) channels underlie a primary outward current having a predominant influence on frequency tuning in auditory hair cells. We now report an example from fish showing that increased BK channel abundance can improve an individual's ability to hear vocalizations during the breeding season. Pharmacological manipulations targeting BK channels, together with measures of BK transcript abundance, can explain the seasonal enhancement of auditory hair cell sensitivity to the frequency content of calls. Plasticity in ion channel expression is a simple, evolutionarily labile solution for sculpting sensory bandwidth to maximize the detection of conspecific signals during reproductive cycles.

SUBMITTER: Rohmann KN

PROVIDER: S-EPMC3676172 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Plasticity in ion channel expression underlies variation in hearing during reproductive cycles.

Rohmann Kevin N KN Fergus Daniel J DJ Bass Andrew H AH

Current biology : CB 20130404 8

Sensory plasticity related to reproductive state, hormonal profiles, and experience is widespread among vertebrates, including humans. Improvements in audio-vocal coupling that heighten the detection of conspecifics are part of the reproductive strategy of many nonmammalian vertebrates. Although seasonal changes in hearing are known, molecular mechanisms determining this form of adult sensory plasticity remain elusive. Among both nonmammals and mammals, large-conductance, calcium-activated potas ...[more]

PMID: 23562266

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Project description:BackgroundWomen facing increased energetic demands in childhood commonly have altered adult ovarian activity and shorter reproductive lifespan, possibly comprising a strategy to optimize reproductive success. Here, we sought to understand the mechanisms of early-life programming of reproductive function, by integrating analysis of reproductive tissues in an appropriate mouse model with methylation analysis of proxy tissue DNA in a well-characterized population of Bangladeshi migrants in the UK. Bangladeshi women whose childhood was in Bangladesh were found to have later pubertal onset and lower age-matched ovarian reserve than Bangladeshi women who grew-up in England. Subsequently, we aimed to explore the potential relevance to the altered reproductive phenotype of one of the genes that emerged from the screens.ResultsOf the genes associated with differential methylation in the Bangladeshi women whose childhood was in Bangladesh as compared to Bangladeshi women who grew up in the UK, 13 correlated with altered expression of the orthologous gene in the mouse model ovaries. These mice had delayed pubertal onset and a smaller ovarian reserve compared to controls. The most relevant of these genes for reproductive function appeared to be SRD5A1, which encodes the steroidogenic enzyme 5α reductase-1. SRD5A1 was more methylated at the same transcriptional enhancer in mice ovaries as in the women's buccal DNA, and its expression was lower in the hypothalamus of the mice as well, suggesting a possible role in the central control of reproduction. The expression of Kiss1 and Gnrh was also lower in these mice compared to controls, and inhibition of 5α reductase-1 reduced Kiss1 and Gnrh mRNA levels and blocked GnRH release in GnRH neuronal cell cultures. Crucially, we show that inhibition of this enzyme in female mice in vivo delayed pubertal onset.ConclusionsSRD5A1/5α reductase-1 responds epigenetically to the environment and its downregulation appears to alter the reproductive phenotype. These findings help to explain diversity in reproductive characteristics and how they are shaped by early-life environment and reveal novel pathways that might be targeted to mitigate health issues caused by life-history trade-offs.

Dataset Information

Plasticity in ion channel expression underlies variation in hearing during reproductive cycles.

Publications

Plasticity in ion channel expression underlies variation in hearing during reproductive cycles.

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