QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

The Journal of Neuroscience, March 7, 2007, 27(10):2435-2443; doi:10.1523/JNEUROSCI.5614-06.2007

This Article Full Text Full Text (PDF) Supplemental Data Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (13) Citing Articles via Google Scholar Google Scholar Articles by Hjerling-Leffler, J. Articles by Koltzenburg, M. Search for Related Content PubMed PubMed Citation Articles by Hjerling-Leffler, J. Articles by Koltzenburg, M.

 Previous Article  |  Next Article 

Development/Plasticity/Repair
Emergence of Functional Sensory Subtypes as Defined by Transient Receptor Potential Channel Expression

Jens Hjerling-Leffler,^1,2 Mona AlQatari,² Patrik Ernfors,¹ and Martin Koltzenburg²

¹Division of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, 171 77 Stockholm, Sweden, and ²University College London Institute of Child Health, University College London, London WC1N 1EH, United Kingdom

Correspondence should be addressed to Prof. Martin Koltzenburg, University College London Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK. Email: m.koltzenburg{at}ich.ucl.ac.uk

The existence of heterogeneous populations of dorsal root ganglion (DRG) neurons conveying different somatosensory information is the basis for the perception of touch, temperature, and pain. A differential expression of transient receptor potential (TRP) cation channels contributes to this functional heterogeneity. However, little is known about the development of functionally diverse neuronal subpopulations. Here, we use calcium imaging of acutely dissociated mouse sensory neurons and quantitative reverse transcription PCR to show that TRP cation channels emerge in waves, with the diversification of functional groups starting at embryonic day 12.5 (E12.5) and extending well into the postnatal life. Functional responses of voltage-gated calcium channels were present in DRG neurons at E11.5 and reached adult levels by E14.5. Responses to capsaicin, menthol, and cinnamaldehyde were first seen at E12.5, E16.5, and postnatal day 0 (P0), when the mRNA for TRP cation channel, subfamily V, member 1 (TRPV1), TRP cation channel, subfamily M, member 8 (TRPM8), and TRP cation channel, subfamily A, member 1 (TRPA1), respectively, was first detected. Cold-sensitive neurons were present before the expression or functional responses of TRPM8 or TRPA1. Our data support a lineage relationship in which TRPM8- and TRPA1-expressing sensory neurons derive from the population of TRPV1-expressing neurons. The TRPA1 subpopulation of neurons emerges independently in two distinct classes of nociceptors: around birth in the peptidergic population and after P14 in the nonpeptidergic class. This indicates that neurons with similar receptive properties can be generated in different sublineages at different developmental stages. This study describes for the first time the emergence of functional subtypes of sensory neurons, providing new insight into the development of nociception and thermoreception.

Key words: TRP cation channel; functional development; dorsal root ganglion; lineage relationship; mouse; sensory neuron

---

Received Aug. 27, 2006; revised Jan. 16, 2007; accepted Jan. 17, 2007.

Correspondence should be addressed to Prof. Martin Koltzenburg, University College London Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK. Email: m.koltzenburg{at}ich.ucl.ac.uk

This article has been cited by other articles:

				A. A. Romanovsky, M. C. Almeida, A. Garami, A. A. Steiner, M. H. Norman, S. F. Morrison, K. Nakamura, J. J. Burmeister, and T. B. Nucci The Transient Receptor Potential Vanilloid-1 Channel in Thermoregulation: A Thermosensor It Is Not Pharmacol. Rev., September 1, 2009; 61(3): 228 - 261. [Abstract] [Full Text] [PDF]

				F. A. Kullmann, M. A. Shah, L. A. Birder, and W. C. de Groat Functional TRP and ASIC-like channels in cultured urothelial cells from the rat Am J Physiol Renal Physiol, April 1, 2009; 296(4): F892 - F901. [Abstract] [Full Text] [PDF]

				O. Caspani and P. A. Heppenstall TRPA1 and Cold Transduction: An Unresolved Issue? J. Gen. Physiol., March 1, 2009; 133(3): 245 - 249. [Full Text] [PDF]

				Y. Karashima, K. Talavera, W. Everaerts, A. Janssens, K. Y. Kwan, R. Vennekens, B. Nilius, and T. Voets TRPA1 acts as a cold sensor in vitro and in vivo PNAS, January 27, 2009; 106(4): 1273 - 1278. [Abstract] [Full Text] [PDF]

				A. R. Light, R. W. Hughen, J. Zhang, J. Rainier, Z. Liu, and J. Lee Dorsal Root Ganglion Neurons Innervating Skeletal Muscle Respond to Physiological Combinations of Protons, ATP, and Lactate Mediated by ASIC, P2X, and TRPV1 J Neurophysiol, September 1, 2008; 100(3): 1184 - 1201. [Abstract] [Full Text] [PDF]

				O. Fajardo, V. Meseguer, C. Belmonte, and F. Viana TRPA1 Channels Mediate Cold Temperature Sensing in Mammalian Vagal Sensory Neurons: Pharmacological and Genetic Evidence J. Neurosci., July 30, 2008; 28(31): 7863 - 7875. [Abstract] [Full Text] [PDF]

				K. Schnizler, L. P. Shutov, M. J. Van Kanegan, M. A. Merrill, B. Nichols, G. S. McKnight, S. Strack, J. W. Hell, and Y. M. Usachev Protein Kinase A Anchoring via AKAP150 Is Essential for TRPV1 Modulation by Forskolin and Prostaglandin E2 in Mouse Sensory Neurons J. Neurosci., May 7, 2008; 28(19): 4904 - 4917. [Abstract] [Full Text] [PDF]

				C. Nassenstein, K. Kwong, T. Taylor-Clark, M. Kollarik, D. M. MacGlashan, A. Braun, and B. J. Undem Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs J. Physiol., March 15, 2008; 586(6): 1595 - 1604. [Abstract] [Full Text] [PDF]

				T. E. Taylor-Clark, B. J. Undem, D. W. MacGlashan Jr., S. Ghatta, M. J. Carr, and M. A. McAlexander Prostaglandin-Induced Activation of Nociceptive Neurons via Direct Interaction with Transient Receptor Potential A1 (TRPA1) Mol. Pharmacol., February 1, 2008; 73(2): 274 - 281. [Abstract] [Full Text] [PDF]

				Y. Liu, F.-C. Yang, T. Okuda, X. Dong, M. J. Zylka, C.-L. Chen, D. J. Anderson, R. Kuner, and Q. Ma Mechanisms of Compartmentalized Expression of Mrg Class G-Protein-Coupled Sensory Receptors J. Neurosci., January 2, 2008; 28(1): 125 - 132. [Abstract] [Full Text] [PDF]

				Y. Takashima, R. L. Daniels, W. Knowlton, J. Teng, E. R. Liman, and D. D. McKemy Diversity in the Neural Circuitry of Cold Sensing Revealed by Genetic Axonal Labeling of Transient Receptor Potential Melastatin 8 Neurons J. Neurosci., December 19, 2007; 27(51): 14147 - 14157. [Abstract] [Full Text] [PDF]

				C. Tuffereau, K. Schmidt, C. Langevin, F. Lafay, G. Dechant, and M. Koltzenburg The Rabies Virus Glycoprotein Receptor p75NTR Is Not Essential for Rabies Virus Infection J. Virol., December 15, 2007; 81(24): 13622 - 13630. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help