Skip to main content
Log in

Transient expression of the calcitonin receptor by enteric neurons of the embryonic and early post-natal mouse

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Calcitonin receptor-immunoreactivity (CTR-ir) was found in enteric neurons of the mouse gastrointestinal tract from embryonic day 13.5 (E13.5) to post-natal day 28 (P28). CTR-ir occurred in cell bodies in ganglia of the myenteric plexus extending from the esophagus to the colon and in nerve cells of the submucosal ganglia of the small and large intestines. CTR-ir was also found in vagal nerve trunks and mesenteric nerves. Counts in the ileal myenteric plexus revealed CTR-ir in 80% of neurons. CTR-ir was clearly evident in the cell bodies of enteric neurons by E15.5. The immunoreactivity reached maximum intensity between P1.5 and P12 but was weaker at P18 and barely detectable at P28. The receptor was detected in nerve processes in the intestine for only a brief period around E17.5, when it was present in one to two axonal processes per villus in the small intestine. In late gestation and soon after birth, CTR-ir was also evident in the mucosal epithelium. The perinatal expression of CTR within the ENS suggests that the calcitonin/CTR system may have a role in the maturation of enteric neurons. Signals may reach enteric neurons in milk, which contains high levels of calcitonin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson RB, Stewart AL, Young HM (2006) Phenotypes of neural-crest-derived cells in vagal and sacral pathways. Cell Tissue Res 323:11–25

    Article  PubMed  CAS  Google Scholar 

  • Becskei C, Riediger T, Zünd D, Wookey P, Lutz TA (2004) Immunohistochemical mapping of calcitonin receptors in the adult rat brain. Brain Res 1030:221–233

    Article  PubMed  CAS  Google Scholar 

  • Burns AJ, Roberts RR, Bornstein JC, Young HM (2009) Development of the enteric nervous system and its role in intestinal motility during fetal and early postnatal stages. Semin Pediatr Surg 18:196–205

    Article  PubMed  Google Scholar 

  • Dacquin R, Davey RA, Laplace C, Levasseur R, Morris HA, Goldring SR, Gebre-Medhin S, Galson DL, Zajac JD, Karsenty G (2004) Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J Cell Biol 164:509–514

    Article  PubMed  CAS  Google Scholar 

  • Fairman CL, Clagett Dame M, Lennon VA, Epstein ML (1995) Appearance of neurons in the developing chick gut. Dev Dyn 204:192–201

    Article  PubMed  CAS  Google Scholar 

  • Findlay DM (2006) Regulation of cell growth mediated by the calcitonin receptor. Cell Mol Biol 52:3–8

    PubMed  CAS  Google Scholar 

  • Fukada S-I, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, Takeda S (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25:2448–2459

    Article  PubMed  CAS  Google Scholar 

  • Gershon MD (2010) Developmental determinants of the independence and complexity of the enteric nervous system. Trends Neurosci 33:446–456

    Article  PubMed  CAS  Google Scholar 

  • Gnocchi VF, White RB, Ono Y, Ellis JA, Zammit PS (2009) Further Characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS One 4:e5205

    Article  PubMed  Google Scholar 

  • Hao MM, Young HM (2009) Development of enteric neuron diversity. J Cell Mol Med 13:1193–1210

    Article  PubMed  CAS  Google Scholar 

  • Hao MM, Moore RE, Roberts RR, Nguyen T, Furness JB, Anderson RB, Young HM (2010) The role of neural activity in the migration and differentiation of enteric neuron precursors. Neurogastroenterol Motil 22:e127–e137

    PubMed  CAS  Google Scholar 

  • Ismail PM, DeMayo FJ, Amato P, Lydon JP (2004) Progesterone induction of calcitonin expression in the murine mammary gland. J Endocrinol 180:287–295

    Article  PubMed  CAS  Google Scholar 

  • Jagger C, Gallagher A, Chambers T, Pondel M (1999) The porcine calcitonin receptor promoter directs expression of a linked reporter gene in a tissue and developmental specific manner in transgenic mice. Endocrinology 140:492–499

    Article  PubMed  CAS  Google Scholar 

  • Jagger C, Chambers T, Pondel M (2000) Transgenic mice reveal novel sites of calcitonin receptor gene expression during development. Biochem Biophys Res Commun 274:124–129

    Article  PubMed  CAS  Google Scholar 

  • Katafuchi T, Kikumoto K, Hamano K, Kangawa K, Matsuo H, Minamino N (2003) Calcitonin receptor-stimulating peptide, a new member of the calcitonin gene-related peptide family. J Biol Chem 278:12046–12054

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Zhu L-J, Polihronis M, Cameron ST, Baird DT, Schatz F, Dua A, Ying Y-K, Bagchi MK, Bagchi IC (1998) Progesterone induces calcitonin gene expression in human endometrium within the putative window of implantation. J Clin Endocrinol Metab 83:4443–4450

    Article  PubMed  CAS  Google Scholar 

  • Pácha J (2000) Development of intestinal transport function in mammals. Physiol Rev 80:1633–1667

    PubMed  Google Scholar 

  • Tikellis C, Xuereb L, Casley D, Brasier G, Cooper ME, Wookey PJ (2003) Calcitonin receptor isoforms expressed in the developing rat kidney. Kidney Int 63:416–426

    Article  PubMed  CAS  Google Scholar 

  • Tolcos M, Tikellis C, Rees S, Cooper M, Wookey P (2003) Ontogeny of calcitonin receptor mRNA and protein in the developing central nervous system of the rat. J Comp Neurol 456:29–38

    Article  PubMed  CAS  Google Scholar 

  • Tverberg LA, Gustavson 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 141:3696–3702

    Article  PubMed  CAS  Google Scholar 

  • Werner S, Widström A-M, Wahlberg V, Winberg J (1982) Immunoreactive calcitonin in maternal milk and serum in relation to prolactin and neurotensin. Early Hum Dev 6:77–82

    Article  PubMed  CAS  Google Scholar 

  • Woodrow JP, Sharpe CJ, Fudge NJ, Hoff AO, Gagel RF, Kovacs CS (2006) Calcitonin plays a critical role in regulating skeletal mineral metabolism during lactation. Endocrinol 147:4010–4012

    Article  CAS  Google Scholar 

  • Wookey PJ (2009) A review of calcitonin receptor expression in embryonic, foetal and adult tissues, with an hypothesis on the connection between expression during foetal development and disease. Open Zool J 2:53–61

    Article  CAS  Google Scholar 

  • Wookey PJ, Zulli A, Buxton BF, Hare DL (2008) Calcitonin receptor immunoreactivity associated with specific cell types in diseased radial and internal mammary arteries. Histopathology 52:605–612

    Article  PubMed  CAS  Google Scholar 

  • Wookey PJ, Zulli A, Hare DL (2009) The elevated expression of calcitonin receptor by cells recruited into the endothelial layer and neo-intima of atherosclerotic plaque. Histochem Cell Biol 132:181–189

    Article  PubMed  CAS  Google Scholar 

  • Zhu L-J, Cullinan-Bove K, Polihronis M, Bagchi MK, Bagchi IC (1998) Calcitonin is a progesterone-regulated marker that forecasts the receptive state of endometrium during implantation. Endocrinology 138:3923–3924

    Article  Google Scholar 

Download references

Acknowledgement

This work was supported by a grant from the National Health and Medical Research Council of Australia (grant number 566696).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John B. Furness.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wookey, P.J., Turner, K. & Furness, J.B. Transient expression of the calcitonin receptor by enteric neurons of the embryonic and early post-natal mouse. Cell Tissue Res 347, 311–317 (2012). https://doi.org/10.1007/s00441-011-1303-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-011-1303-6

Keywords

Navigation