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Classical studies in amphibians have concluded that the endocrine pituitary and pars intermedia are derived from epithelial buccal epidermis and do not require the infundibulum for their induction. These studies also assumed that the pituitary is not subsequently determined by infundibular induction. Our extirpation, auto-transplantation and immunohistochemical studies with Xenopus laevis were initiated to investigate early presumptive pituitary development. These studies were conducted especially with reference to the pars intermedia melanotrope cell's induction, and its production and release of α-melanophore stimulating hormone (α-MSH) from the precursor protein proopiomelanocortin (POMC). Auto-transplantation studies demonstrated that the pituitary POMC-producing cells are determined at a stage prior to pituitary-infundibular contact. The results of experiments involving the extirpation of the presumptive infundibulum also indicated that the infundibulum is not essential for the differentiation of POMC-producing cells. We also demonstrated that early pituitary development involves adherence to the prechiasmatic area of the diencephalon with the pituitary placode growing in a posterior direction toward the infundibulum where contact occurs at Xenopus stage 39/40. Overall, our studies provide a model for early tissue relations among presumptive pituitary, suprachiasmatic nucleus, pars tuberalis and infundibulum during neurulation and later neural tube stages of development. It is hypothesized that the overlying chiasmatic area suppresses pituitary differentiation.
Fig. 1.
Stage 15 extirpation of the presumptive pituitary area. At stage 15 the presumptive pituitary (or organ) field (black and surrounding gray area) was extirpated from neural plate embryos. According to Jacobson [10], tissue organ fields extend beyond the tissue that eventually becomes part of the organ (pituitary in this case). The field area therefore includes the black area which is the tissue that maps to within the pituitary, and also includes the surrounding (gray area) which is capable of becoming pituitarytissue. This outer (gray) area also contains part of the retinal or eye field (Eagleson and Harris, 1990). After operations these animals were allowed to develop on black background under constant illumination until they reached stage 41/42. Neural plate embryos are 1 mm in diameter. (A) Tail melanophores of presumptive stage 42 animal that had undergone extirpation. Scale bar = 1 mm. (B) Normal relationship of the infundibulum and the pituitary is illustrated with this normal stage 41/42 tadpole. Scale bar = 200 μm. (C) Stage 42 tadpolebrain of an animal that had its presumptive pituitary extirpated at stage 15. This animal lacks a pituitary gland (arrow tip indicates the site where the pituitary should have been. Note the normal infundibulum (inf); N, notochord; oc, optic chiasma; pit, pituitary. Scale bar = 200 μm.
Fig. 2.
Auto-transplantation of the presumptive pituitary area. At stage 15 the presumptive pituitary area was auto-transplanted to the future tail region of the same embryo. (A) Arrow heads indicate examples of grafted tissue. The example at the top of the fig. has a more centrally restricted stage 15 graft inserted into the future tail. In the two lower examples, grafts included lateralANRtissue that contained some adjacent presumptive eyetissue (note lower two tadpoles grafts’ pigmented retinal epithelium within the graft). (B) A whole tadpole with an auto-transplanted graft (arrows). Scale bar = 150 μm. (C) The auto-transplanted graft exhibits immunoreactivity for α-MSH peptides (arrowheads). Cell nuclei counterstained with eosin-hematoxylin. Scale bar = 75 μm.
Fig. 3.
Stage 15 Extirpation of the presumptive suprachiasmatic nucleus area. This tissue included a small area (darkened area) of the neural plate that normally was contiguous with the ANR. (A) Stage 42 tadpoles without the presumptive SCN and grown on a white background exhibited high tailmelanophore indices (MIs) in tail melanophores. (B) Sagittal section of the brain of a stage 42 tadpole with the presumptive SCN extirpated. Posterior displacement of the (unattached) pituitary was often observed for these operated tadpoles. oc, optic chiasma; pit, pituitary. Scale bar = 150 μm.
Fig. 4.
(A) Stage 15 Extirpation of the presumptive infundibulum area. This extirpation operation included tissue more centrally located within the neural plate and posterior to the presumptive SCNtissue (darkened area). (B) Stage 42 tadpoles without the infundibulum exhibited dark tails with high tail MIs even if grown on a white background. (C) Sagittal section of the brain of a stage 42 tadpole with the presumptive infundibulum removed. In most cases the pituitary is directly attached to the diencephalon and the brain lacks an infundibulum. oc, optic chiasma; pit, pituitary. Asterisk indicates where infundibulum should be located. Scale bar = 150 μm.
Fig. 6.
Schematic representation of the stages of early development of the pituitary and hypothalamic areas of Xenopus laevis. Blue denotes the presumptive magnocellular area. Red represents the presumptive pituitary. Yellow indicates the presumptive prechiasmatic area, and green represents the presumptive infundibulum. (For a detailed neural plate map consult Eagleson and Harris, 1990). Stage 15 (frontal view) neural plate embryo. Stage 19 (frontal view). Neural folds have uplifted and enfolded all but the presumptive pituitary area. Stage 25 (mid-sagittal view). All neural and pituitary structures have been full enveloped by overlying ectoderm. The presumptive pituitary is tightly adhered to the chiasmatic ridge region (along the midline). The presumptive suprachiasmatic area has a more medial location than the more lateral presumptive magnocellular area. Stage 35/36 (mid-sagittal view).Expansion and growth of the brain and optic chiasma repositions the presumptive pituitary to a more rostral location as it remains adhered to the extending diencephalon. The suprachiasmatic (yellow) and magnocellular areas assume more central locations due to diencephalic expansion and proliferation. Stage 39/40 (mid-sagittal view) the presumptive pituitary grows into a rostro-posterior direction, making contact with the infundibulum. N, notochord (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article).
