Cell and Tissue Research

, Volume 327, Issue 3, pp 521–528 | Cite as

Calcitonin is expressed in the chicken pituitary gland: influence of gonadal steroids and sexual maturation

  • Sreenivasa R. Maddineni
  • Susan M. Krzysik-Walker
  • Olga M. Ocón-Grove
  • Susan M. Motch
  • Gilbert L. HendricksIII
  • Ramesh Ramachandran
Regular Article
First Online:
Received:
Accepted:

Abstract

Calcitonin (CT) is primarily produced by the thyroid C cells in mammals or by the ultimobranchial gland in chickens. CT is also expressed by the pituitary gland in rats in which it functions as a paracrine factor causing decreased lactotroph proliferation and prolactin (PRL) secretion. Gonadal steroids influence CT expression in the rat pituitary gland. However, the expression of the CT gene in the pituitary gland of chickens or of any other avian species has not previously been reported. We have tested the hypotheses that CT is expressed in the chicken pituitary gland, and that its expression is influenced by sexual maturation or in response to ovarian steroid administration. We have detected robust expression of CT cDNA in the chicken pituitary gland by reverse transcription/polymerase chain reaction (PCR). The sequence of the pituitary-derived CT cDNA is identical to that of the ultimobranchial gland. CT-immunoreactive (ir) cells have been observed throughout the anterior pituitary gland by confocal microscopy. Many of the PRL-ir cells show co-localization with CT-ir cells. Quantitative real-time PCR analysis has revealed an inverse relationship between the quantities of PRL mRNA and CT mRNA in the pituitary gland: sexually mature hens contain lower amounts of CT mRNA but larger quantities of PRL mRNA compared with sexually immature chickens. Estradiol and/or progesterone treatment of sexually immature chickens leads to a significant decrease in the quantity of pituitary CT mRNA relative to that in the vehicle-treated chickens. We conclude that pituitary CT plays an important paracrine/autocrine role in the control of lactotroph function and PRL secretion in the chicken.

Keywords

Prolactin Lactotrophs Progesterone Estradiol Ovary Chicken (Leghorn) 
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Notes

Acknowledgements

We wish to thank Dr. Luc Berghman for the gift of anti-chicken PRL antibody and the staff at the Huck Institute of Life Sciences, The Pennsylvania State University for their help regarding confocal microscopy.

References

  1. Berghman LR, Grauwels L, Vanhamme L, Proudman JA, Foidart A, Balthazart J, Vandesande F (1992) Immunocytochemistry and immunoblotting of avian prolactins using polyclonal and monoclonal antibodies toward a synthetic fragment of chicken prolactin. Gen Comp Endocrinol 85:346–357PubMedCrossRefGoogle Scholar
  2. Bucht E, Telenius-Berg M, Lundell G, Sjoberg HE (1986) Immunoextracted calcitonin in milk and plasma from totally thyroidectomized women. Evidence of monomeric calcitonin in plasma during pregnancy and lactation. Acta Endocrinol (Copenh) 113:529–535Google Scholar
  3. Clark MS, Bendell L, Power DM, Warner S, Elgar G, Ingleton PM (2002) Calcitonin: characterisation and expression in a teleost fish, Fugu rubripes. J Mol Endocrinol 28:111–123PubMedCrossRefGoogle Scholar
  4. Copp DH, Cameron EC (1961) Demonstration of a hypocalcemic factor (calcitonin) in commercial parathyroid extract. Science 134:2038PubMedCrossRefGoogle Scholar
  5. Copp DH, Cockcroft DW, Kueh Y (1967) Ultimobranchial origin of calcitonin. Hypocalcemic effect of extracts from chicken glands. Can J Physiol Pharmacol 45:1095–1099PubMedGoogle Scholar
  6. Chronwall BM, Sands SA, Li Z, Shah GV (1996) Calcitonin-like peptide containing gonadotrophs are juxtaposed to cup-shaped lactotrophs. Endocr J 4:27–33Google Scholar
  7. Deftos LJ, Burton D, Catherwood BD, Bone HG, Parthemore JG, Guillemin R, Watkins WB, Moore RY (1978) Demonstration by immunoperoxidase histochemistry of calcitonin in the anterior lobe of the rat pituitary. J Clin Endocrinol Metab 47:457–460PubMedCrossRefGoogle Scholar
  8. Deftos LJ, Burton DW, Watkins WB, Catherwood BD (1980) Immunohistological studies of artiodactyl and teleost pituitaries with antisera to calcitonin. Gen Comp Endocrinol 42:9–18PubMedCrossRefGoogle Scholar
  9. Ding YQ, Zhu LJ, Bagchi MK, Bagchi IC (1994) Progesterone stimulates calcitonin gene expression in the uterus during implantation. Endocrinology 135:2265–2274PubMedCrossRefGoogle Scholar
  10. Dunn IC, Lewis PD, Wilson PW, Sharp PJ (2003) Acceleration of maturation of FSH and LH responses to photostimulation in prepubertal domestic hens by oestrogen. Reproduction 126:217–225PubMedCrossRefGoogle Scholar
  11. Flynn JJ, Margules DL, Cooper CW (1981) Presence of immunoreactive calcitonin in the hypothalamus and pituitary lobes of rats. Brain Res Bull 6:547–549PubMedCrossRefGoogle Scholar
  12. Galan Galan F, Rogers RM, Girgis SI, MacIntyre I (1981) Immunoreactive calcitonin in the central nervous system of the pigeon. Brain Res 212:59–66PubMedCrossRefGoogle Scholar
  13. Hidaka Y, Suzuki M (2004) Identification and tissue distribution of mRNAs encoding salmon-type calcitonins-IV and -V in the rainbow trout. J Mol Endocrinol 32:963–974PubMedCrossRefGoogle Scholar
  14. Kansaku N, Shimada K, Terada O, Saito N (1994) Prolactin, growth hormone, and luteinizing hormone-beta subunit gene expression in the cephalic and caudal lobes of the anterior pituitary gland during embryogenesis and different reproductive stages in the chicken. Gen Comp Endocrinol 96:197–205PubMedCrossRefGoogle Scholar
  15. Kumar S, Zhu LJ, Polihronis M, Cameron ST, Baird DT, Schatz F, Dua A, Ying YK, Bagchi MK, Bagchi IC (1998) Progesterone induces calcitonin gene expression in human endometrium within the putative window of implantation. J Clin Endocrinol Metab 83:4443–4450PubMedCrossRefGoogle Scholar
  16. Lanuza E, Davies DC, Landete JM, Novejarque A, Martinez-Garcia F (2000) Distribution of CGRP-like immunoreactivity in the chick and quail brain. J Comp Neurol 421:515–532PubMedCrossRefGoogle Scholar
  17. Lasmoles F, Jullienne A, Day F, Minvielle S, Milhaud G, Moukhtar MS (1985) Elucidation of the nucleotide sequence of chicken calcitonin mRNA: direct evidence for the expression of a lower vertebrate calcitonin-like gene in man and rat. EMBO J 4:2603–2607PubMedGoogle Scholar
  18. Li Z, Shah GV (1995) Estrogen attenuates expression of calcitonin-like immunoreactivity in the anterior pituitary gland. Endocr J 3:452–459Google Scholar
  19. Linscheid P, Seboek D, Nylen ES, Langer I, Schlatter M, Becker KL, Keller U, Muller B (2003) In vitro and in vivo calcitonin I gene expression in parenchymal cells: a novel product of human adipose tissue. Endocrinology 144:5578–5584PubMedCrossRefGoogle Scholar
  20. Liu HK, Bacon WL (2005) Changes in egg production rate induced by progesterone injection in broiler breeder hens. Poultry Sci 84:321–327Google Scholar
  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  22. Mikami S, Yamada S (1984) Immunohistochemistry of the hypothalamic neuropeptides and anterior pituitary cells in the Japanese quail. J Exp Zool 232:405–417PubMedCrossRefGoogle Scholar
  23. Muller B, White JC, Nylen ES, Snider RH, Becker KL, Habener JF (2001) Ubiquitous expression of the calcitonin-I gene in multiple tissues in response to sepsis. J Clin Endocrinol Metab 86:396–404PubMedCrossRefGoogle Scholar
  24. Ogawa H, Takahashi T, Kuwayama T, Kawashima M (2003) Presence of calcitonin receptors in shell gland of the guineafowl and changes in binding property during an oviposition cycle. Poultry Sci 82:1302–1306Google Scholar
  25. Pearse AG (1966) Common cytochemical properties of cells producing polypeptide hormones, with particular reference to calcitonin and the thyroid C cells. Vet Rec 79:587–590PubMedGoogle Scholar
  26. Perez Cano R, Girgis SI, Galan Galan F, MacIntyre I (1982) Identification of both human and salmon calcitonin-like molecules in birds suggesting the existence of two calcitonin genes. J Endocrinol 92:351–355PubMedGoogle Scholar
  27. Ren Y, Chien J, Sun YP, Shah GV (2001) Calcitonin is expressed in gonadotropes of the anterior pituitary gland: its possible role in paracrine regulation of lactotrope function. J Endocrinol 171:217–228PubMedCrossRefGoogle Scholar
  28. Ren Y, Sun YP, Shah GV (2003) Calcitonin inhibits prolactin promoter activity in rat pituitary GGH3 cells: evidence for involvement of p42/44 mitogen-activated protein kinase in calcitonin action. Endocrine 20:13–22PubMedCrossRefGoogle Scholar
  29. Russwurm S, Stonans I, Stonane E, Wiederhold M, Luber A, Zipfel PF, Deigner HP, Reinhart K (2001) Procalcitonin and CGRP-1 mRNA expression in various human tissues. Shock 16:109–112PubMedGoogle Scholar
  30. Shah GV, Deftos LJ, Crowley WR (1993) Synthesis and release of calcitonin-like immunoreactivity by anterior pituitary cells: evidence for a role in paracrine regulation of prolactin secretion. Endocrinology 132:1367–1372PubMedCrossRefGoogle Scholar
  31. Shah GV, Pedchenko V, Stanley S, Li Z, Samson WK (1996) Calcitonin is a physiological inhibitor of prolactin secretion in ovariectomized female rats. Endocrinology 137:1814–1822PubMedCrossRefGoogle Scholar
  32. Shah GV, Epand RM, Orlowski RC (1988) Calcitonin inhibition of prolactin secretion in isolated rat pituitary cells. J Endocrinol 116:279–286PubMedCrossRefGoogle Scholar
  33. Shah GV, Chien J, Sun YP, Puri S, Ravindra R (1999) Calcitonin inhibits anterior pituitary cell proliferation in the adult female rat. Endocrinology 140:4281–4291PubMedCrossRefGoogle Scholar
  34. Sheward WJ, Lutz EM, Harmar AJ (1994) The expression of the calcitonin receptor gene in the brain and pituitary gland of the rat. Neurosci Lett 181:31–34PubMedCrossRefGoogle Scholar
  35. Shimada K, Ishida H, Sato K, Seo H, Matsui N (1991) Expression of prolactin gene in incubating hens. J Reprod Fertil 91:147–154PubMedCrossRefGoogle Scholar
  36. Sjoberg HE, Arver S, Bucht E (1980) High concentration of immunoreactive calcitonin of prostatic origin in human semen. Acta Physiol Scand 110:101–102PubMedGoogle Scholar
  37. Sun YP, Lee TJ, Shah GV (2002) Calcitonin expression in rat anterior pituitary gland is regulated by ovarian steroid hormones. Endocrinology 143:4056–4064PubMedCrossRefGoogle Scholar
  38. Tschopp FA, Henke H, Petermann JB, Tobler PH, Janzer R, Hokfelt T, Lundberg JM, Cuello C, Fischer JA (1985) Calcitonin gene-related peptide and its binding sites in the human central nervous system and pituitary. Proc Natl Acad Sci USA 82:248–252PubMedCrossRefGoogle Scholar
  39. Tverberg LA, Gustafson MF, Scott TL, Arzumanova IV, Provost ER, Yan AW, Rawie SA (2000) Induction of calcitonin and calcitonin receptor expression in rat mammary tissue during pregnancy. Endocrinology 141:3696–3702PubMedCrossRefGoogle Scholar
  40. Wang YQ, Yuan R, Sun YP, Lee TJ, Shah GV (2003) Antiproliferative action of calcitonin on lactotrophs of the rat anterior pituitary gland: evidence for the involvement of transforming growth factor beta 1 in calcitonin action. Endocrinology 144:2164–2171PubMedCrossRefGoogle Scholar
  41. Wong EA, Ferrin NH, Silsby JL, Halawani ME el (1991) Cloning of a turkey prolactin cDNA: expression of prolactin mRNA throughout the reproductive cycle of the domestic turkey (Meleagris gallopavo). Gen Comp Endocrinol 83:18–26PubMedCrossRefGoogle Scholar
  42. Yasuoka T, Kawashima M, Takahashi T, Tatematsu N, Tanaka K (1998) Calcitonin receptor binding properties in bone and kidney of the chicken during the oviposition cycle. J Bone Miner Res 13:1412–1419PubMedCrossRefGoogle Scholar
  43. Yuan R, Kulkarni T, Wei F, Shah GV (2005) Targeted overexpression of calcitonin in gonadotrophs of transgenic mice leads to chronic hypoprolactinemia. Mol Cell Endocrinol 229:193–203PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Sreenivasa R. Maddineni
    • 1
  • Susan M. Krzysik-Walker
    • 1
  • Olga M. Ocón-Grove
    • 1
  • Susan M. Motch
    • 1
  • Gilbert L. HendricksIII
    • 1
  • Ramesh Ramachandran
    • 1
  1. 1.Department of Poultry ScienceThe Pennsylvania State UniversityUniversity ParkUSA

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