Rapid modulation of gene expression profiles in the telencephalon of male goldfish following exposure to waterborne sex pheromones

Lado, Wudu E.; Zhang, Dapeng; Mennigen, Jan A.; Zamora, Jacob M.; Popesku, Jason T.; Trudeau, Vance L.

doi:10.1016/j.ygcen.2013.06.015

Cited by 16 publications

(8 citation statements)

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“…In goldfish, four GABA A subunits (α 1, β 4, γ 1 and 2) were expressed at higher levels in the brains of sexually mature females [39]. Similarly, the GABA A receptor γ 2 subunit was expressed at higher levels in the brains of goldfish exposed to prostaglandin-F 2α (PGF 2α ) than in controls [40]. In the current study, the δ subunit was up-regulated in sexually mature males; this is intriguing given that the δ subunit appears to be involved in neurosteroid modulation of the GABA A receptor [41].…”

Section: Discussionmentioning

confidence: 99%

“…Ependymins are involved in synaptic changes during memory consolidation and regeneration of the optic nerve [47–49]. Changes in the levels of ependymin-II expression have been observed in the hypothalamus in goldfish at breeding season [39] and in the telencephalon following exposure to a female pheromone [40]. …”

Section: Discussionmentioning

confidence: 99%

“…In goldfish, CALM levels also change with reproductive status. During breeding season, CALM and calcium/calmodulin-dependant protein kinase 2 (CaMK2) levels are highest in the hypothalamus in female goldfish [39] and CALM levels are highest in the telencephalon of males following exposure to PGF 2α [40]. Sexual maturation alters the eel’s internal state and changes in the way the animal relates to its environment.…”

Section: Discussionmentioning

confidence: 99%

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Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation

et al. 2014

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BackgroundThe vertebrate brain plays a critical role in the regulation of sexual maturation and reproduction by integrating environmental information with developmental and endocrine status. The European eel Anguilla anguilla is an important species in which to better understand the neuroendocrine factors that control reproduction because it is an endangered species, has a complex life cycle that includes two extreme long distance migrations with both freshwater and seawater stages and because it occupies a key position within the teleost phylogeny. At present, mature eels have never been caught in the wild and little is known about most aspects of reproduction in A. anguilla. The goal of this study was to identify genes that may be involved in sexual maturation in experimentally matured eels. For this, we used microarrays to compare the gene expression profiles of sexually mature to immature males.ResultsUsing a false discovery rate of 0.05, a total of 1,497 differentially expressed genes were identified. Of this set, 991 were expressed at higher levels in brains (forebrain and midbrain) of mature males while 506 were expressed at lower levels relative to brains of immature males. The set of up-regulated genes includes genes involved in neuroendocrine processes, cell-cell signaling, neurogenesis and development. Interestingly, while genes involved in immune system function were down-regulated in the brains of mature males, changes in the expression levels of several receptors and channels were observed suggesting that some rewiring is occurring in the brain at sexual maturity.ConclusionsThis study shows that the brains of eels undergo major changes at the molecular level at sexual maturity that may include re-organization at the cellular level. Here, we have defined a set of genes that help to understand the molecular mechanisms controlling reproduction in eels. Some of these genes have previously described functions while many others have roles that have yet to be characterized in a reproductive context. Since most of the genes examined here have orthologs in other vertebrates, the results of this study will contribute to the body of knowledge concerning reproduction in vertebrates as well as to an improved understanding of eel biology.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-799) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation

et al. 2014

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“…ascension to dominance; [38]). In fish, pheromone reception can induce significant changes in neural activity through increased IEG expression within brain regions known to regulate social behaviors [19,[39][40][41][42]. In male goldfish, reception of female pheromones elicits significant changes in c-fos expression within the pre-optic area; specifically in neurons rich with androgen receptors [42].…”

Section: Discussionmentioning

confidence: 99%

Ready for a fight? The physiological effects of detecting an opponent's pheromone cues prior to a contest

Garcia

Williams

Sinderman

et al. 2015

Physiology & Behavior

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Reception of pheromone cues can elicit significant physiological (e.g. steroid hormone levels) changes in the recipient. These pheromone-induced physiological changes have been well documented for male-female interactions, but scarcely in same-sex interactions (male-male and female-female). We sought to address this dearth in the current literature and examine whether mangrove rivulus fish (Kryptolebias marmoratus) could detect and, ultimately, mount a physiological response to the pheromone signature of a potential, same-sex competitor. We examined steroid hormone levels in mangrove rivulus exposed to one of three treatments: 1) isolation, 2) exposure to pheromones of a size-matched partner, and 3) pheromone exposure to a size-matched opponent followed by a physical encounter with the opponent. We found that exposure to a competitor's pheromone cues elicited a significant increase in testosterone levels. Increases in testosterone were similar across genetically distinct lineages derived from geographically distinct populations. Further, testosterone levels were similar between individuals only exposed to pheromone cues and individuals exposed to both pheromone cues and a subsequent physical encounter. Our findings led us to generate a number of testable predictions regarding how mangrove rivulus utilize pheromone signals in social interactions, the molecular mechanisms linking social stimuli and hormonal responses, and the possible adaptive benefits of hormonal responsiveness to receiving a potential competitor's pheromone cues.

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“…The role of DHP as a pheromone is probably best understood in the goldfish Carassius auratus . Exposure to DHP, which is released by pre-ovulatory female, activates a population of neurones in ventral pre-optic area (POA) that plays important roles in reproduction, and triggers immediate increases in cGnRH mRNA level in the telencephalon, luteinizing hormone (LH) in the plasma and milt volume (Kobayashi et al, 2002; Lado et al, 2013; Kawai et al, 2014). Moreover, electro-olfactogram (EOG) recording studies have shown that olfactory response thresholds to pheromones including DHP vary with reproductive stages of the fish and it is likely that this sensitivity of the olfactory epithelium is controlled by the endocrine system (Irvine and Sorensen, 1993; Cardwell et al, 1995; Belanger et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Cloning and olfactory expression of progestin receptors in the Chinese black sleeper Bostrichthys sinensis

Zhang

Liu

Zhu

et al. 2016

General and Comparative Endocrinology

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Our previous studies suggested that 17α,20β-dihydroxy-4-pregnen-3-one (DHP), an oocyte maturation inducing progestin, also acts as a sex pheromone in Chinese black sleeper Bostrichthys sinensis, a fish species that inhabits intertidal zones and mates and spawns inside a muddy burrow. The electroolfactogram response to DHP increased during the breeding season. In the present study, we cloned the cDNAs of the nine progestin receptors (pgr, paqr5, 6, 7(a, b), 8, 9, pgrmc1, 2) from B. sinensis, analyzed their tissue distribution, and determined the expression in the olfactory rosette during the reproductive cycle in female and male fish. The deduced amino acid sequences of the nine progestin receptors share high sequence identities with those of other fish species and relatively lower homology with their mammalian counterparts, and phylogenetic analyses classified the nine B. sinensis progestin receptors into their respective progestin receptor groups. Tissue distribution of B. sinensis progestin receptors showed differential expression patterns, but all these nine genes were expressed in the olfactory rosette. Interestingly, paqr5 mRNA was found in the intermediate and basal parts of the olfactory epithelium but not in the central core using in situ hybridization, and its expression level was the highest in the olfactory rosette among the tissues examined. These results suggested Paqr5 may have an important role for transmitting progestin signaling in the olfactory system. The expression levels of paqr7a and paqr7b, pgr and pgrmc2 mRNA peaked around the mid meiotic stage, and that of paqr8 peaked at late meiotic stage in the olfactory rosette in males, while the olfactory expression of paqr5 decreased gradually as spermatogenesis progressed. In contrast, the expression of the progestin receptors did not change significantly during the development of the ovary in the olfactory rosette in females, except that of pgr. Interestingly, the changes of paqr8 expression in the olfactory rosette in males mirrored the changes of plasma DHP levels in females during the reproductive cycle, suggesting the Paqr8 may also be important for deciphering progestin signaling released by female. To our knowledge, this is the first time to demonstrate the presence of all known progestin receptors in a teleost olfactory rosette, and to show different expressions between the males and females during the reproductive cycle. This study provides the first evidence on changes of all purported progestin receptors during a reproductive cycle in teleost olfactory rosette, and suggests that distinct olfactory sensitivities to DHP may be due to the changes and compositions of each progestin receptor in B. sinensis.

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Rapid modulation of gene expression profiles in the telencephalon of male goldfish following exposure to waterborne sex pheromones

Cited by 16 publications

References 64 publications

Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation

Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation

Ready for a fight? The physiological effects of detecting an opponent's pheromone cues prior to a contest

Cloning and olfactory expression of progestin receptors in the Chinese black sleeper Bostrichthys sinensis

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