Skip to main content
Log in

Heterogeneous distribution of TRPC proteins in the embryonic cortex

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

The present study was initiated to gain some information about the tissue distribution of transient receptor potential proteins of C-type (TRPC), a family of voltage-independent cation channels, at the beginning of neurogenesis in the telencephalon of embryonic mice. The mRNAs of all known TRPCs (TRPC1–TRPC7) could be found in the cortex at E13. TRPC1, TRPC3 and TRPC5 were the main isoforms, whereas the mRNAs for TRPC2, TRPC4, TRPC6 and TRPC7 were less abundant. The distribution throughout the cortical wall of TRPC1, TRPC3 and TRPC6 was studied by means of immuno-histochemistry. The data collected pointed to a heterogeneous expression of the channels. Three groups were identified. The first one comprises TRPC1, specifically found in the preplate but only in some post-mitotic neurons. It was mainly observed in a subset of cells distinct from the Cajal-Retzius cells. The second group is composed of TRPC3. It was found in non-neuronal cells and also in dividing (5-bromo-2′-deoxyuridine-positive) cells, indicating that TRPC3 is present in precursor cells. The third group contains TRPC6 detected in neuronal and in dividing non-neuronal cells. Double immunostaining experiments showed that TRPC3-positive cells also express TRPC6. Collectively, this report highlights a specific TRPC expression pattern in the immature cortical wall.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bouron A, Altafaj X, Boisseau S, De Waard M (2005) A store-operated Ca2+ influx activated in response to the depletion of thapsigargin-sensitive Ca2+ stores is developmentally regulated in embryonic cortical neurons from mice. Brain Res Dev Brain Res 159:64–71

    Article  PubMed  CAS  Google Scholar 

  • Bouron A, Boisseau S, De Waard M, Peris L (2006) Differential down-regulation of voltage-gated calcium channel currents by glutamate and BDNF in embryonic cortical neurons. Eur J Neurosci 24:699–708

    Article  PubMed  Google Scholar 

  • Faure AV, Grunwald D, Moutin MJ, Hilly M, Mauger JP, Marty I, De Waard M, Villaz M, Albrieux M (2001) Developmental expression of the calcium release channels during early neurogenesis of the mouse cerebral cortex. Eur J Neurosci 14:1613–1622

    Article  PubMed  CAS  Google Scholar 

  • Fowler MA, Sidiropoulou K, Ozkan ED, Phillips CW, Cooper DC (2007) Corticolimbic expression of TRPC4 and TRPC5 channels in the rodent brain. PLoS ONE 2:e573

    Article  PubMed  Google Scholar 

  • Fusco FR, Martorana A, Giampa C, De March Z, Vacca F, Tozzi A, Longone P, Piccirilli S, Paolucci S, Sancesario G, Mercuri NB, Bernardi G (2004) Cellular localization of TRPC3 channel in rat brain: preferential distribution to oligodendrocytes. Neurosci Lett 365:137–142

    Article  PubMed  CAS  Google Scholar 

  • Garcia RL, Schilling WP (1997) Differential expression of mammalian TRP homologues across tissues and cell lines. Biochem Biophys Res Commun 239:279–283

    Article  PubMed  CAS  Google Scholar 

  • Ghosh A, Greenberg ME (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268:239–247

    Article  PubMed  CAS  Google Scholar 

  • Goel M, Sinkins WG, Schilling WP (2002) Selective association of TRPC channel subunits in rat brain synaptosomes. J Biol Chem 277(50):48303–48310

    Article  PubMed  CAS  Google Scholar 

  • Gotz M, Hartfuss E, Malatesta P (2002) Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res Bull 57:777–788

    Article  PubMed  Google Scholar 

  • Greka A, Navarro B, Oancea E, Duggan A, Clapham DE (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 6:837–845

    Article  PubMed  CAS  Google Scholar 

  • Grimaldi M, Maratos M, Verma A (2003) Transient receptor potential channel activation causes a novel form of [Ca 2+]I oscillations and is not involved in capacitative Ca 2+ entry in glial cells. J Neurosci 23:4737–4745

    PubMed  CAS  Google Scholar 

  • Hartfuss E, Galli R, Heins N, Gotz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30

    Article  PubMed  CAS  Google Scholar 

  • Haydar TF, Bambrick LL, Krueger BK, Rakic P (1999) Organotypic slice cultures for analysis of proliferation, cell death, and migration in the embryonic neocortex. Brain Res Brain Res Protoc 4:425–437

    Article  PubMed  CAS  Google Scholar 

  • Hui H, McHugh D, Hannan M, Zeng F, Xu SZ, Khan SU, Levenson R, Beech DJ, Weiss JL (2006) Calcium-sensing mechanism in TRPC5 channels contributing to retardation of neurite outgrowth. J Physiol 572:165–172

    PubMed  CAS  Google Scholar 

  • Jia Y, Zhou J, Tai Y, Wang Y (2007) TRPC channels promote cerebellar granule neuron survival. Nat Neurosci 10:559–567

    Article  PubMed  CAS  Google Scholar 

  • Komuro H, Rakic P (1992) Selective role of N-type calcium channels in neuronal migration. Science 257:806–809

    Article  PubMed  CAS  Google Scholar 

  • Kriegstein AR, Noctor SC (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 27:392–399

    Article  PubMed  CAS  Google Scholar 

  • Kunert-Keil C, Bisping F, Kruger J, Brinkmeier H (2006) Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics 7:159

    Article  PubMed  Google Scholar 

  • Li HS, Xu XZ, Montell C (1999) Activation of a TRPC3-dependent cation current through the neurotrophin BDNF. Neuron 24:261–273

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, Yuan XB (2005) Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434:894–898

    Article  PubMed  CAS  Google Scholar 

  • Menezes JR, Luskin MB (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 14:5399–5416

    PubMed  CAS  Google Scholar 

  • Messersmith EK, Feller MB, Zhang H, Shatz CJ (1997) Migration of neocortical neurons in the absence of functional NMDA receptors. Mol Cell Neurosci 9:347–357

    Article  PubMed  CAS  Google Scholar 

  • Minke B, Cook B (2002) TRP channel proteins and signal transduction. Physiol Rev 82:429–472

    PubMed  CAS  Google Scholar 

  • Mizuno N, Kitayama S, Saishin Y, Shimada S, Morita K, Mitsuhata C, Kurihara H, Dohi T (1999) Molecular cloning and characterization of rat trp homologues from brain. Brain Res Mol Brain Res 64:41–51

    Article  PubMed  CAS  Google Scholar 

  • Mwanjewe J, Grover AK (2004) Role of transient receptor potential canonical 6 (TRPC6) in non-transferrin-bound iron uptake in neuronal phenotype PC12 cells. Biochem J 378:975–982

    Article  PubMed  CAS  Google Scholar 

  • Nasman J, Bart G, Larsson K, Louhivuori L, Peltonen H, Akerman KE (2006) The orexin OX1 receptor regulates Ca2+ entry via diacylglycerol-activated channels in differentiated neuroblastoma cells. J Neurosci 26:10658–10666

    Article  PubMed  CAS  Google Scholar 

  • Pizzo P, Burgo A, Pozzan T, Fasolato C (2001) Role of capacitative calcium entry on glutamate-induced calcium influx in type-I rat cortical astrocytes. J Neurochem 79:98–109

    Article  PubMed  CAS  Google Scholar 

  • Pla AF, Maric D, Brazer SC, Giacobini P, Liu X, Chang YH, Ambudkar IS, Barker JL (2005) Canonical transient receptor potential 1 plays a role in basic fibroblast growth factor (bFGF)/FGF receptor-1-induced Ca2+ entry and embryonic rat neural stem cell proliferation. J Neurosci 25:2687–2701

    Article  CAS  Google Scholar 

  • Platel JC, Boisseau S, Dupuis A, Brocard J, Poupard A, Savasta M, Villaz M, Albrieux M (2005) Na+ channel-mediated Ca2+ entry leads to glutamate secretion in mouse neocortical preplate. Proc Natl Acad Sci USA 102:19174–19179

    Article  PubMed  CAS  Google Scholar 

  • Putney JW (2005) Physiological mechanisms of TRPC activation. Pflugers Arch 451:29–34

    Article  PubMed  CAS  Google Scholar 

  • Rakic P, Komuro H (1995) The role of receptor/channel activity in neuronal cell migration. J Neurobiol 26:299–315

    Article  PubMed  CAS  Google Scholar 

  • Shim S, Goh EL, Ge S, Sailor K, Yuan JP, Roderick HL, Bootman MD, Worley PF, Song H, Ming GL (2005) XTRPC1-dependent chemotropic guidance of neuronal growth cones. Nat Neurosci 8:730–735

    Article  PubMed  CAS  Google Scholar 

  • Sossey-Alaoui K, Lyon JA, Jones L, Abidi FE, Hartung AJ, Hane B, Schwartz CE, Stevenson RE, Srivastava AK (1999) Molecular cloning and characterization of TRPC5 (HTRP5), the human homologue of a mouse brain receptor-activated capacitative Ca2+ entry channel. Genomics 60:330–340

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Nowakowski RS, Caviness VS Jr (1995) Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci 15:6058–6068

    PubMed  CAS  Google Scholar 

  • Tesfai Y, Brereton HM, Barritt GJ (2001) A diacylglycerol-activated Ca2+ channel in PC12 cells (an adrenal chromaffin cell line) correlates with expression of the TRP-6 (transient receptor potential) protein. Biochem J 358:717–726

    Article  PubMed  CAS  Google Scholar 

  • Vazquez G, Wedel BJ, Aziz O, Trebak M, Putney JW Jr (2004) The mammalian TRPC cation channels. Biochim Biophys Acta 1742:21–36

    Article  PubMed  CAS  Google Scholar 

  • von Bohlen Und Halbach O, Hinz U, Unsicker K, Egorov AV (2005) Distribution of TRPC1 and TRPC5 in medial temporal lobe structures of mice. Cell Tissue Res 322:201–206

    Article  PubMed  Google Scholar 

  • Wang GX, Poo MM (2005) Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434:898–904

    Article  PubMed  CAS  Google Scholar 

  • Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci USA 92:9652–9656

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Zagranichnaya TK, Gurda GT, Eves EM, Villereal ML (2004) A TRPC1/TRPC3-mediated increase in store-operated calcium entry is required for differentiation of H19-7 hippocampal neuronal cells. J Biol Chem 279:43392–43402

    Article  PubMed  CAS  Google Scholar 

  • Zitt C, Halaszovich CR, Luckhoff A (2002) The TRP family of cation channels: probing and advancing the concepts on receptor-activated calcium entry. Prog Neurobiol 66:243–264

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank D. Grunwald for his help with the Leica scanning confocal microscope (iRTSV, CEA, Grenoble) and L. Lemonnier for helpful comments. This study was supported by a grant from 1’Agence Nationale de la Recherche (ANR).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexandre Bouron.

Additional information

S. Boisseau and C. Kunert-Keil have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary data (DOC 1083 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boisseau, S., Kunert-Keil, C., Lucke, S. et al. Heterogeneous distribution of TRPC proteins in the embryonic cortex. Histochem Cell Biol 131, 355–363 (2009). https://doi.org/10.1007/s00418-008-0532-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-008-0532-6

Keywords

Navigation