Abstract
The primordium of the mammalian adenohypophysis derived from Rathke’s pouch (RP) is known to be formed by oral ectoderm invagination. However, in the early phase of pituitary development, the detailed process by which the oral ectoderm develops into the adenohypophysis remains largely unknown. Using high-resolution non-radiolabeled in situ hybridization and the BrdU and TUNEL methods, we have examined the detailed expression pattern of factors involved in the formation of RP of chicken and the changes in the mitotic and apoptotic cell regions in RP. In the chicken embryo, Sonic hedgehog (Shh) mRNA was initially expressed in the stomodeal plate but not in the oral ectoderm. After prospective diencephalon had detached from the oral ectoderm, another Shh-expressing region appeared in the most rostral part of the recess. LIM homeobox gene 3 (Lhx3) mRNA first appeared in the anterior area of Rathke’s recess, and expression then spread to the caudal region. αGSU mRNA-expressing cells were observed at both ends of the Lhx3-expressing region, and thereafter the expression area moved to the posterior region. Furthermore, a close overlap was found between the proliferating region and Lhx3 mRNA-expressing area, and TUNEL-positive cells appeared in Seessel’s pouch derived from the foregut. Thus, the primordium of the pituitary gland corresponding to the Lhx3-expressing region is surrounded by the Shh-expressing region, which appears in two steps, and the mass growth and invagination of RP of chicken result from the coordination of the dorsal extension of the anterior region and the ventral extension of the posterior region of RP.
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References
Bach I, Rhodes SJ, Pearse RV 2nd, Heinzel T, Gloss B, Scully KM, Sawchenko PE, Rosenfeld MG (1995) P-Lim, a LIM homeodomain factor, is expressed during pituitary organ and cell commitment and synergizes with Pit-1. Proc Natl Acad Sci USA 92:2720–2724
Bumcrot DA, McMahon AP (1995) Somite differentiation. Sonic signals somites. Curr Biol 5:612–614
Burrows HL, Birkmeier TS, Seasholtz AF, Camper SA (1996) Targeted ablation of cells in the pituitary primordia of transgenic mice. Mol Endocrinol 10:1467–1477
Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11:3286–3305
Cordero D, Marcucio R, Hu D, Gaffield W, Tapadia M, Helms JA (2004) Temporal perturbations in sonic hedgehog signaling elicit the spectrum of holoprosencephaly phenotypes. J Clin Invest 114:485–494
Couly GF, Le Douarin NM (1985) Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm and prosencephalon. Dev Biol 110:422–439
Couly GF, Le Douarin NM (1987) Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic congenital abnormalities. Dev Biol 120:198–214
Daikoku S, Chikamori M, Adachi T, Maki Y (1982) Effect of basal diencephalon on the development of Rathke’s pouch in rats: a study in combined organ culture. Dev Biol 90:198–202
Daikoku S, Chikamori M, Adachi T, Okamura Y, Nishiyama T, Tsuruo Y (1983) Ontogenesis of hypothalamic immunoreactive ACTH cells in vivo and in vitro: role of Rathke’s pouch. Dev Biol 97:81–88
Eagleson GW, Jenks BG, Van Overbeeke AP (1986) The pituitary adrenocorticotropes originate from neural ridge tissue in Xenopus laevis. J Embryol Exp Morphol 95:1–4
Ellsworth BS, Egashira N, Haller JL, Butts DL, Cocquet J, Clay CM, Osamura RY, Camper SA (2006) FOXL2 in the pituitary: molecular, genetic, and developmental analysis. Mol Endocrinol 20:2796–2805
Ericson J, Norlin S, Jessell TM, Edlund T (1998) Integrated FGF and BMP signaling controls the progression of progenitor cell differentiation and the emergence of pattern in the embryonic anterior pituitary. Development 125:1005–1015
Gleiberman AS, Fedtsova NG, Rosenfeld MG (1999) Tissue interactions in the induction of anterior pituitary: role of the ventral diencephalon, mesenchyme, and notochord. Dev Biol 213:340–353
Hobert O, Westphal H (2000) Functions of LIM-homeobox genes. Trends Genet 16:75–83
Jackson SM, Gutierrez-Hartmann A, Hoeffler JP (1995) Upstream stimulatory factor, a basic-helix-loop-helix-zipper protein, regulates the activity of the alpha-glycoprotein hormone subunit gene in pituitary cells. Mol Endocrinol 9:278–291
Japon MA, Rubinsteine M, Low MJ (1994) In situ hybridization analysis of anterior pituitary hormone gene expression during fetal mouse development. J Histochem Cytochem 42:1117–1125
Johnson RL, Tabin CJ (1997) Molecular models for vertebrate limb development. Cell 90:979–990
Kameda Y, Miura M, Ohno S (2000) Expression of the common alpha-subunit mRNA of glycoprotein hormones during the chick pituitary organogenesis, with special reference to the pars tuberalis. Cell Tissue Res 299:71–80
Kawamura K, Kikuyama S (1995) Induction from posterior hypothalamus is essential for the development of the pituitary proopiomelacortin (POMC) cells of the toad (Bufo japonicus). Cell Tissue Res 279:233–239
Kawamura K, Kikuyama S (1998) Morphogenesis of the hypothalamus and hypophysis: their association, dissociation and reassociation before and after “Rathke”. Arch Histol Cytol 61:189–198
Kikuyama S, Inaco H, Jenks BG, Kawamura K (1993) Development of the ectopically transplanted primordium of epithelial hypophysis (anterior neural ridge) in Bufo japonicus embryo. J Exp Zool 266:216–220
Kouki T, Imai H, Aoto K, Eto K, Shioda S, Kawamura K, Kikuyama S (2001) Developmental origin of the rat adenohypophysis prior to the formation of Rathke’s pouch. Development 128:959–963
Lawrence PA, Struhl G (1996) Morphogens, compartments, and pattern: lessons from Drosophila? Cell 85:951–961
Maseki Y, Nakamura K, Iwasawa A, Zheng J, Inoue K, Sakai T (2004) Development of gonadotropes in the chicken embryonic pituitary gland. Zool Sci 21:435–444
Rathke H (1838) Über die Entstehung der Glandula pituitaria. Arch Anat Physiol Wiss Med 1838:482–485
Roberson MS, Schoderbek WE, Tremml G, Maurer RA (1994) Activation of the glycoprotein hormone alpha-subunit promoter by a LIM-homeodomain transcription factor. Mol Cell Biol 14:2985–2993
Sakata I, Tanaka T, Matsubara M, Yamazaki M, Tani S, Hayashi Y, Kangawa K, Sakai T (2002) Postnatal changes in ghrelin mRNA expression and in ghrelin-producing cells in the rat stomach. J Endocrinol 174:463–471
Sbrogna JL, Barresi MJ, Karlstrom RO (2003) Multiple roles for Hedgehog signaling in zebrafish pituitary development. Dev Biol 254:19–35
Schwind JL (1928) The development of the hypophysis cerebri of the albino rat. Am J Anat 41:295–319
Seessel A (1877) Zur Entwicklungsgeschichte des Vorderdarms. Arch Anat Physiol 1877:449–467
Sheng HZ, Zhadanov AB, Mosinger B Jr, Fujii T, Bertuzzi S, Grinberg A, Lee EJ, Huang SP, Mahon KA, Westphal H (1996) Specification of pituitary cell lineages by the LIM homeobox gene Lhx3. Science 272:1004–1007
Sheng HZ, Moriyama K, Yamashita T, Li H, Potter SS, Mahon KA, Westphal H (1997) Multistep control of pituitary organogenesis. Science 278:1809–1812
Simmons DM, Voss JW, Ingraham HA, Holloway JM, Broide RS, Rosenfeld MG, Swanson LW (1990) Pituitary cell phenotypes involve cell-specific Pit-1 mRNA translation and synergistic interactions with other classes of transcription factors. Genes Dev 4:695–711
Steger DJ, Hecht JH, Mellon PL (1994) GATA-binding proteins regulate the human gonadotropin alpha-subunit gene in the placenta and pituitary gland. Mol Cell Biol 14:5592–5602
Stoeckel ME, Hindelang C, Klein MJ, Poissonnier M, Felix JM (1993) Early expression of the glycoprotein hormone alpha subunit in the pars tuberalis of the rat pituitary grand during ontogenesis. Neuroendocrinology 58:616–624
Tanabe Y, Jessell TM (1996) Diversity and pattern in the developing spinal cord. Science 274:1115–1123
Thesleff I, Sharpe P (1997) Signalling networks regulating dental development. Mech Dev 67:111–123
Treier M, Rosenfeld MG (1996) The hypothalamic-pituitary axis: co-development of two organs. Curr Opin Cell Biol 8:833–843
Treier M, Gleiberman AS, O’Connell SM, Szeto DP, McMahon JA, McMahon AP, Rosenfeld MG (1998) Multistep signaling requirements for pituitary organogenesis in vivo. Genes Dev 12:1691–1704
Treier M, O’Connell S, Gleiberman A, Price J, Szeto DP, Burgess R, Chuang PT, McMahon AP, Rosenfeld MG (2001) Hedgehog signaling is required for pituitary gland development. Development 128:377–386
Tremblay JJ, Lanctôt C, Drouin J (1998) The pan-pituitary activator of transcription, Ptx1 (pituitary homeobox 1), acts in synergy with SF-1 and Pit1 and is an upstream regulator of the LIM-homeodomain gene Lim3/Lhx3. Mol Endocrinol 12:428–441
Watanabe YG (1982) Effects of brain and mesenchyme upon the cytogenesis of rat adenohypophysis in vitro. I. Differentiation of adrenocorticotropes. Cell Tissue Res 227:257–266
Zhang Y, Zhang Z, Zhao X, Yu X, Hu Y, Geronimo B, Fromm SH, Chen YP (2000) A new function of BMP4: dual role for BMP4 in regulation of Sonic hedgehog expression in the mouse tooth germ. Development 127:1431–1443
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Takagi, H., Nagashima, K., Inoue, M. et al. Detailed analysis of formation of chicken pituitary primordium in early embryonic development. Cell Tissue Res 333, 417–426 (2008). https://doi.org/10.1007/s00441-008-0647-z
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DOI: https://doi.org/10.1007/s00441-008-0647-z