Abstract
Mammalian pituitaries exhibit a high degree of intercellular coordination; this enables them to mount large-scale coordinated responses to various physiological stimuli. This type of communication has not been adequately demonstrated in teleost pituitaries, which exhibit direct hypothalamic innervation and expression of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in distinct cell types. We found that in two fish species, namely tilapia and zebrafish, LH cells exhibit close cell–cell contacts and form a continuous network throughout the gland. FSH cells were more loosely distributed but maintained some degree of cell–cell contact by virtue of cytoplasmic processes. These anatomical differences also manifest themselves at the functional level as evidenced by the effect of gap-junction uncouplers on gonadotropin release. These substances abolished the LH response to gonadotropin-releasing hormone stimulation but did not affect the FSH response to the same stimuli. Dye transfer between neighboring LH cells provides further evidence for functional coupling. The two gonadotropins were also found to be differently packaged within their corresponding cell types. Our findings highlight the evolutionary origin of pituitary cell networks and demonstrate how the different levels of cell–cell coordination within the LH and FSH cell populations are reflected in their distinct secretion patterns.
Highlights
Of the two gonadotropins[16], differential interpretation of GnRH signaling frequency[17,18], differential response to activin/inhibin signaling[19,20,21] and a complex feedback mechanism involving gonadal steroids[15]
LH-producing cells were found to reside in tight clusters in peripheral parts of the proximal pars distalis (PPD) (Fig. 1a), whereas FSH-producing cells were located more dorsally, close to the dorsal projections of the pars nervosa (PN)[30]
Three-dimensional imaging of transgenic fish with labeled FSH cells revealed that the contacts between these cells were far less prominent than those observed in the LH cell population (Fig. 1b)
Summary
Of the two gonadotropins[16], differential interpretation of GnRH signaling frequency[17,18], differential response to activin/inhibin signaling[19,20,21] and a complex feedback mechanism involving gonadal steroids[15]. The high level of structural and functional conservation combined with these teleost-unique traits make fish an exceptionally valuable model for studying the function and evolution of the vertebrate reproductive axis. While several studies have investigated paracrine interactions in fish pituitaries[24,25,26,27], very few studies have examined direct cell-cell coupling in teleosts. We investigated anatomical and functional gonadotrope networks in the fish pituitary. We found anatomical contacts between fish gonadotropes and identified different degrees of coordination between LH and FSH cells, reflecting their anatomical architecture. These findings are discussed within their physiological context to provide new insights into the evolution and significance of pituitary networks in vertebrates
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