Cell and Tissue Research

, Volume 328, Issue 1, pp 129–135

Expression of retinaldehyde dehydrogenase (RALDH)2 and RALDH3 but not RALDH1 in the developing anterior pituitary glands of rats

  • Ken Fujiwara
  • Fumihiko Maekawa
  • Motoshi Kikuchi
  • Shu Takigami
  • Toshihiko Yada
  • Takashi Yashiro
Regular Article

Abstract

Retinoic acid (RA) plays an important role in cell growth and tissue development and is also a regulating factor of pituitary function. However, whether RA is generated in the pituitary gland and plays a role as a paracrine and/or autocrine hormone is generally unknown. RA is synthesized from retinoids through oxidation processes. Dehydrogenases catalyzing the oxidation of retinal to RA are members of the retinaldehyde dehydrogenase (RALDH) family. In this study, we examined the expression of RALDH1, RALDH2, and RALDH3 mRNA in the rat embryonic pituitary gland. By in situ hybridization with digoxigenin-labeled cRNA probes, we detected mRNA expression for RALDH2 and RALDH3, but not RALDH1. The expression of RALDH2 and RALDH3 was located in Rathke’s pouch at embryonic day 12.5 (E12.5) and subsequently in the developing anterior pituitary gland. We also used quantitative real-time polymerase chain reaction to analyze RALDH2 and RALDH3 mRNA expression levels during the development of the pituitary gland. We found that pituitary RALDH2 and RALDH3 mRNA levels were high at E17.5 and decreased markedly after birth. Our study is the first to show that RALDH2 and RALDH3, but not RALDH1, are expressed in the embryonic anterior pituitary gland of the rat.

Keywords

Aanterior pituitary gland Retinoic acid RALDH Development In situ hybridization Rat (Wistar) 

References

  1. Cohen LE, Zanger K, Brue T, Wondisford FE, Radovick S (1999) Defective retinoic acid regulation of the Pit-1 gene enhancer: a novel mechanism of combined pituitary hormone deficiency. Mol Endocrinol 13:476–484PubMedCrossRefGoogle Scholar
  2. De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, Rosewell I, Dickson C (2000) An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127:483–492PubMedGoogle Scholar
  3. Dolle P, Ruberte E, Leroy P, Morriss-Kay G, Chambon P (1990) Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110:1133–1151PubMedGoogle Scholar
  4. Dolle P, Fraulob V, Kastner P, Chambon P (1994) Developmental expression of murine retinoid X receptor (RXR) genes. Mech Dev 45:91–104PubMedCrossRefGoogle Scholar
  5. Duester G (2000) Families of retinoid dehydrogenases regulating vitamin A function: production of visual pigment and retinoic acid. Eur J Biochem 267:4315–4324PubMedCrossRefGoogle Scholar
  6. 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 125:1005–1015PubMedGoogle Scholar
  7. Fan X, Molotkov A, Manabe S, Donmoyer CM, Deltour L, Foglio MH, Cuenca AE, Blaner WS, Lipton SA, Duester G (2003) Targeted disruption of Aldh1a1 (Raldh1) provides evidence for a complex mechanism of retinoic acid synthesis in the developing retina. Mol Cell Biol 23:4637–4648PubMedCrossRefGoogle Scholar
  8. Fujiwara K, Maruyama M, Usui K, Sakai T, Matsumoto H, Hinuma S, Kitada C, Inoue K (2003) Appearance of prolactin-releasing peptide-producing neurons in the area postrema of adrenalectomized rats. Neurosci Lett 338:127–130PubMedCrossRefGoogle Scholar
  9. Gagnon I, Duester G, Bhat PV (2002) Kinetic analysis of mouse retinal dehydrogenase type-2 (RALDH2) for retinal substrates. Biochim Biophys Acta 1596:156–162PubMedGoogle Scholar
  10. Graham CE, Brocklehurst K, Pickersgill RW, Warren MJ (2006) Characterization of retinaldehyde dehydrogenase 3. Biochem J 394:67–75PubMedCrossRefGoogle Scholar
  11. Lin SC, Li S, Drolet DW, Rosenfeld MG (1994) Pituitary ontogeny of the Snell dwarf mouse reveals Pit-1-independent and Pit-1-dependent origins of the thyrotrope. Development 120:515– 522PubMedGoogle Scholar
  12. Lin M, Zhang M, Abraham M, Smith SM, Napoli JL (2003) Mouse retinal dehydrogenase 4 (RALDH4), molecular cloning, cellular expression, and activity in 9-cis-retinoic acid biosynthesis in intact cells. J Biol Chem 278:9856–9861PubMedCrossRefGoogle Scholar
  13. Mic FA, Molotkov A, Fan X, Cuenca AE, Duester G (2000) RALDH3, a retinaldehyde dehydrogenase that generates retinoic acid, is expressed in the ventral retina, otic vesicle and olfactory pit during mouse development. Mech Dev 97:227–230PubMedCrossRefGoogle Scholar
  14. Mogi C, Goda H, Mogi K, Takaki A, Yokoyama K, Tomida M, Inoue K (2005) Multistep differentiation of GH-producing cells from their immature cells. J Endocrinol 184:41–50PubMedCrossRefGoogle Scholar
  15. Niederreither K, McCaffery P, Drager UC, Chambon P, Dolle P (1997) Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech Dev 62:67–78PubMedCrossRefGoogle Scholar
  16. Niederreither K, Fraulob V, Garnier JM, Chambon P, Dolle P (2002) Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech Dev 110:165–171PubMedCrossRefGoogle Scholar
  17. Palomino T, Barettino D, Aranda A (1998) Role of GHF-1 in the regulation of the rat growth hormone gene promoter by thyroid hormone and retinoic acid receptors. J Biol Chem 273:27541–27547PubMedCrossRefGoogle Scholar
  18. Ribes V, Wang Z, Dolle P, Niederreither K (2006) Retinaldehyde dehydrogenase 2 (RALDH2)-mediated retinoic acid synthesis regulates early mouse embryonic forebrain development by controlling FGF and sonic hedgehog signaling. Development 133:351–361PubMedCrossRefGoogle Scholar
  19. Sakata I, Nakamura K, Yamazaki M, Matsubara M, Hayashi Y, Kangawa K, Sakai T (2002) Ghrelin-producing cells exist as two types of cells, closed- and opened-type cells, in the rat gastrointestinal tract. Peptides 23:531–536PubMedCrossRefGoogle Scholar
  20. 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 4:695–711Google Scholar
  21. Takuma N, Sheng HZ, Furuta Y, Ward JM, Sharma K, Hogan BL, Pfaff SL, Westphal H, Kimura S, Mahon KA (1998) Formation of Rathke’s pouch requires dual induction from the diencephalon. Development 125:4835–4840PubMedGoogle Scholar
  22. 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 12:1691–1704PubMedGoogle Scholar
  23. 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 128:377–386PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Ken Fujiwara
    • 1
  • Fumihiko Maekawa
    • 2
  • Motoshi Kikuchi
    • 1
  • Shu Takigami
    • 1
  • Toshihiko Yada
    • 2
  • Takashi Yashiro
    • 1
  1. 1.Division of Histology and Cell Biology, Department of AnatomyJichi Medical University, School of MedicineTochigiJapan
  2. 2.Division of Integrative Physiology, Department of PhysiologyJichi Medical University, School of MedicineTochigiJapan

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