Adenohypophysis formation in the zebrafish and its dependence on sonic hedgehog

Abstract

Formation of the adenohypophysis in mammalian embryos occurs via an invagination of the oral ectoderm to form Rathke's pouch, which becomes exposed to opposing dorsoventral gradients of signaling proteins governing specification of the different hormone-producing pituitary cell types. One signal promoting pituitary cell proliferation and differentiation to ventral cell types is Sonic hedgehog (Shh) from the oral ectoderm. To study pituitary formation and patterning in zebrafish, we cloned four cDNAs encoding different pituitary hormones, prolactin (prl), proopiomelancortin (pomc), thyroid stimulating hormone (tsh), and growth hormone (gh), and analyzed their expression patterns relative to that of the pituitary marker lim3. prl and pomc start to be expressed at the lateral edges of the lim3 expression domain, before pituitary cells move into the head. This indicates that patterning of the pituitary anlage and terminal differentiation of pituitary cells starts while cells are still organized in a placodal fashion at the anterior edge of the developing brain. Following the expression pattern of prl and pomc during development, we show that no pituitary-specific invagination equivalent to Rathke's pouch formation takes place. Rather, pituitary cells move inwards together with stomodeal cells during oral cavity formation, with medial cells of the placode ending up posterior and lateral cells ending up anterior, resulting in an anterior-posterior, rather than a dorsoventral, patterning of the adenohypophysis. Carrying out loss- and gain-of-function experiments, we show that Shh from the ventral diencephalon plays a crucial role during induction, patterning, and growth of the zebrafish adenohypophysis. The phenotypes are very similar to those obtained upon pituitary-specific inactivation or overexpression of Shh in mouse embryo, suggesting that the role of Shh during pituitary development has been largely conserved between fish and mice, despite the different modes of pituitary formation in the two vertebrate classes.

Thyroid and pituitary gland development from hatching through metamorphosis of a teleost flatfish, the Atlantic halibut

“…These studies further demonstrate that the pituitary cells in fish are derived from the anterior neural ridge and move inwards as a consequence of oral cavity formation (Glasgow et al 1997;Herzog et al 2003). In the present study, the Atlantic halibut pituitary cell ontogeny is found to be more like that of other temperate species, with endocrine cells being first detected in post-hatch larvae.…”

“…Recent studies on pituitary induction and patterning in zebrafish embryos indicate that, in this species, endocrine cells develop prior to hatch (Herzog et al 2003;Sbrogna et al 2003). These studies further demonstrate that the pituitary cells in fish are derived from the anterior neural ridge and move inwards as a consequence of oral cavity formation (Glasgow et al 1997;Herzog et al 2003).…”

“…Recent studies on zebrafish (Danio rerio) indicate that teleosts do not form a Rathke's pouch. Rather, the AH develops from a primodeum of pituitary cells in the anterior neural ridge and moves, together with stomodeum cells, inwards in the process of oral cavity formation (Glasgow et al 1997;Herzog et al 2003;Sbrogna et al 2003;Chapman et al 2005). The architecture of the fish AH, including the pattern of cellular arrangement and the timing and order of the first appearance of endocrine cells, varies among different groups and species (Yadav 1995).…”

“…In most teleost species, the endocrine cells of the pituitary develop at early larval stages and the detection of hormones by immunocytochemistry suggests that they are functional (Cambre et al 1990;Power and Canario 1992). However, in zebrafish, salmonids and ayu, somatotrophs, lactotrophs and somatolactotrophs develop prior to hatching (Herzog et al 2003;Sbrogna et al 2003). A number of studies also indicate that the apparent activity of various endocrine cells changes with different life stages (Cambre et al 1990;Power 1992).…”

Nusap1 is essential for neural crest cell migration in zebrafish

“…3, nusap1 was present in single-cell embryos, suggesting that it is a maternal gene. The zygotic expression was ubiquitous detected from the 1024 cell stage to mid-gastrulation stage , and the pattern in a salt and pepper manner implied its functions in cell cycle progression and proliferation by several experiences from large scale in situ screening work in other institutes (Herzog et al, 2003). After the somite formation, nusap1 transcripts were detected in forebrain, hindbrain, neural crest, blood island and proliferative cells .…”