Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-20T01:31:53.472Z Has data issue: false hasContentIssue false
  • English
  • Français

Transient Receptor Potential (TRP) Channels in the Brain: the Good and the Ugly

Published online by Cambridge University Press:  02 May 2012

Bernd Nilius
Bernd Nilius
Affiliation:
Department Molecular Cell Biology, Laboratory of Ion Channel Research, KU Leuven, Campus Gasthuisberg, Herestraat 49, bus 802, B-3000 Leuven, Belgium. Email: Bernd.Nilius@med.kuleuven.be
Get access Rights & Permissions [Opens in a new window]

Abstract

The ‘transient receptor potential’ (TRP) multigene family encodes sixspan membrane proteins that function as ion channels in mostly tetrameric structures. Members of this family are conserved from yeast, worm, fly to invertebrate, vertebrate and man. These channels have been stigmatized to function only as cell sensors occupied by sensory function. It turns out that TRP channels fulfil a plethora of cellular functions, including non-sensory functions in our brain. This short paper will highlight the advent of novel ion channels in the brain serving different functions and being significantly involved in the genesis of multiple diseases. We will certainly witness a plethora of the novel roles of this protein family in physiological and pathophysiological functions in our central nervous system.

Type
Brains and Robots
Information
European Review , Volume 20 , Issue 3 , 02 May 2012 , pp. 343 - 355
Copyright
Copyright © Academia Europaea 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Damann, N., Voets, T. and Nilius, B. (2008) TRPs in our senses. Current Biology, 18, pp. R880–R889.CrossRefGoogle ScholarPubMed
2.Nilius, B., Owsianik, G., Voets, T. and Peters, J. A. (2007) Transient receptor potential channels in disease. Physiological Reviews, 87, pp. 165–217.CrossRefGoogle ScholarPubMed
3.Gasperini, R. J., Choi-Lundberg, D., Thompson, M. J., Mitchell, C. B. and Foa, L. (2009) Homer regulates calcium signalling in growth cone turning. Neural Development, 4, p. 29.CrossRefGoogle ScholarPubMed
4.Gokce, O., Runne, H., Kuhn, A. and Luthi-Carter, R. (2009) Short-term striatal gene expression responses to brain-derived neurotrophic factor are dependent on MEK and ERK activation. PLoS ONE, 4, e5292.CrossRefGoogle ScholarPubMed
5.Huang, W. C., Young, J. S. and Glitsch, M. D. (2007) Changes in TRPC channel expression during postnatal development of cerebellar neurons. Cell Calcium, 42, pp. 1–10.CrossRefGoogle ScholarPubMed
6.Zhang, Z., Reboreda, A., Alonso, A., Barker, P. A. and Seguela, P. (2011) TRPC channels underlie cholinergic plateau potentials and persistent activity in entorhinal cortex. Hippocampus, 24, pp. 269–283.Google Scholar
7.Greka, A., Navarro, B., Oancea, E., Duggan, A. and Clapham, D. E. (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nature Neuroscience, 6, pp. 837–845.CrossRefGoogle ScholarPubMed
8.Moran, M. M., Xu, H. and Clapham, D. E. (2004) TRP ion channels in the nervous system. Current Opinion in Neurobiology, 14, pp. 362–369.CrossRefGoogle ScholarPubMed
9.Bezzerides, V. J., Ramsey, I. S., Kotecha, S., Greka, A. and Clapham, D. E. (2004) Rapid vesicular translocation and insertion of TRP channels. Nature Cell Biology, 6, pp. 709–720.CrossRefGoogle ScholarPubMed
10.Wen, Z. et al. (2007) BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. Journal of Cell Biology, 178, pp. 107–119.CrossRefGoogle ScholarPubMed
11.Hutchins, B. I., Li, L. and Kalil, K. (2011) Wnt/calcium signaling mediates axon growth and guidance in the developing corpus callosum. Developmental Neurobiology, 71, pp. 269–283.CrossRefGoogle ScholarPubMed
12.Li, L., Hutchins, B. I. and Kalil, K. (2010) Wnt5a induces simultaneous cortical axon outgrowth and repulsive turning through distinct signaling mechanisms. Science Signalling, 3, pt2.Google ScholarPubMed
13.Li, Y., Calfa, G., Inoue, T., Amaral, M. D. and Pozzo-Miller, L. (2010) Activity-dependent release of endogenous BDNF from mossy fibres evokes a TRPC3 current and Ca2+ elevation in CA3 pyramidal neurons. Journal of Neurophysiology, 103.CrossRefGoogle ScholarPubMed
14.Hartmann, J. et al. (2008) TRPC3 channels are required for synaptic transmission and motor coordination. Neuron, 59, pp. 392–398.CrossRefGoogle ScholarPubMed
15.Zhou, J. et al. (2008) Critical role of TRPC6 channels in the formation of excitatory synapses. Nature Neuroscience, 11, pp. 741–743.CrossRefGoogle ScholarPubMed
16.Beis, D., Schwarting, R. K. and Dietrich, A. (2011) Evidence for a supportive role of classical transient receptor potential 6 (TRPC6) in the exploration behavior of mice. Physiological Behavior, 102, pp. 245–250.CrossRefGoogle ScholarPubMed
17.Musella, A. et al. Transient receptor potential vanilloid 1 channels control acetylcholine/2-arachidonoylglicerol coupling in the striatum. Neuroscience, 167, pp. 864–871.CrossRefGoogle Scholar
18.Peng, Y. R. et al. (2010) Postsynaptic spiking homeostatically induces cell-autonomous regulation of inhibitory inputs via retrograde signaling. Journal of Neuroscience, 30, pp. 16220–16231.CrossRefGoogle ScholarPubMed
19.Goswami, C., Schmidt, H. and Hucho, F. (2007) TRPV1 at nerve endings regulates growth cone morphology and movement through cytoskeleton reorganization. FEBS Journal, 274, pp. 760–772.CrossRefGoogle ScholarPubMed
20.Musella, A. et al. (2008) TRPV1 channels facilitate glutamate transmission in the striatum. Molecular and Cellular Neuroscience, 40, pp. 89–97.CrossRefGoogle ScholarPubMed
21.Edwards, J. G. et al. (2011) A novel non-CB1/TRPV1 endocannabinoid-mediated mechanism depresses excitatory synapses on hippocampal CA1 interneurons. Hippocampus, 22, pp. 209–221.CrossRefGoogle Scholar
22.Grueter, B. A., Brasnjo, G. and Malenka, R. C. (2010) Postsynaptic TRPV1 triggers cell-type specific LTD in the nucleus accumbens. Nature Neuroscience, 13, pp. 1519–1525.CrossRefGoogle ScholarPubMed
23.Chávez, A. E., Chiu, C. Q. and Castillo, P. E. (2010) TRPV1 activation by endogenous anandamide triggers postsynaptic LTD in dentate gyrus. Nature Neuroscience, 13, pp. 1511–1518.CrossRefGoogle ScholarPubMed
24.Shibasaki, K., Murayama, N., Ono, K., Ishizaki, Y. and Tominaga, M. (2010) TRPV2 enhances axon outgrowth through its activation by membrane stretch in developing sensory and motor neurons. Journal of Neuroscience, 30, pp. 4601–4612.CrossRefGoogle ScholarPubMed
25.Olah, M. E. et al. (2009) Ca2+-dependent induction of TRPM2 currents in hippocampal neurons. Journal of Physiology, 587, pp. 965–979.CrossRefGoogle ScholarPubMed
26.Freestone, P. S. et al. (2009) Acute action of rotenone on nigral dopaminergic neurons – involvement of reactive oxygen species and disruption of Ca homeostasis. European Journal of Neuroscience, 30, pp. 849–859.CrossRefGoogle Scholar
27.Lee, K. H. et al. (2010) Pregnenolone sulfate enhances spontaneous glutamate release by inducing presynaptic Ca2+-induced Ca2+ release. Neuroscience, 171, pp. 106–116.CrossRefGoogle ScholarPubMed
28.Zamudio-Bulcock, P. A. and Valenzuela, C. F. (2011) Pregnenolone sulfate increases glutamate release at neonatal climbing fiber-to-purkinje cell synapses. Neuroscience, 175, pp. 24–36.CrossRefGoogle ScholarPubMed
29.Rubin, J. E., Hayes, J. A., Mendenhall, J. L. and Del Negro, C. A. (2009) Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations. Proceedings of the National Academy of Science USA, 106, pp. 2939–2944.CrossRefGoogle ScholarPubMed
30.Szydlowska, K. and Tymianski, M. (2010) Calcium, ischemia and excitotoxicity. Cell Calcium, 47, pp. 122–129.CrossRefGoogle ScholarPubMed
31.Selvaraj, S., Sun, Y. and Singh, B.B. (2010) TRPC channels and their implication in neurological diseases. CNS Neurological Disorder Drug Targets, 9, pp. 94–104.CrossRefGoogle ScholarPubMed
32.Narayanan, K. L., Irmady, K., Subramaniam, S., Unsicker, K. and von Bohlen Und Halbach, O. (2008) Evidence that TRPC1 is involved in hippocampal glutamate-induced cell death. Neuroscience Letters, 446, pp. 117–122.CrossRefGoogle ScholarPubMed
33.Amaral, M. D., Chapleau, C. A. and Pozzo-Miller, L. (2007) Transient receptor potential channels as novel effectors of brain-derived neurotrophic factor signaling: potential implications for Rett syndrome. Pharmacology Therapeutics, 113, pp. 394–409.CrossRefGoogle ScholarPubMed
34.Becker, E. B. E. et al. (2009) A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proceedings of the National Academy of Science (USA), 106, pp. 6706–6711.CrossRefGoogle ScholarPubMed
35.Trebak, M. (2010) The puzzling role of TRPC3 channels in motor coordination. Pflugers Archiv. European Journal of Physiology, 459, pp. 369–375.CrossRefGoogle ScholarPubMed
36.Adachi, N. et al. (2008) Enzymological analysis of mutant protein kinase Cgamma causing spinocerebellar ataxia type 14 and dysfunction in Ca2+ homeostasis. Journal of Biological Chemistry, 283, pp. 19854–19863.CrossRefGoogle ScholarPubMed
37.Zhou, F. W., Matta, S. G. and Zhou, F. M. (2008) Constitutively active TRPC3 channels regulate basal ganglia output neurons. Journal of Neuroscience, 28, pp. 473–482.CrossRefGoogle ScholarPubMed
38.Tai, C., Himes, D. J. and MacVicar, B. A. (2009) Translocation of TRPC5 channels contributes to cholinergic-induced plateau potential in epilepsy. Journal of Neurochemistry, 109, pp. 277–278 Supplement 1.Google Scholar
39.Fu, M., Xie, Z. and Zuo, H. (2009) TRPV1: a potential target for antiepileptogenesis. Medical Hypotheses, 73, pp. 100–102.CrossRefGoogle ScholarPubMed
40.Gibson, H. E., Edwards, J. G., Page, R. S., Van Hook, M. J. and Kauer, J. A. (2008) TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron, 57, pp. 746–759.CrossRefGoogle ScholarPubMed
41.Alter, B. J. and Gereau, R. W. T. (2008) Hotheaded: TRPV1 as mediator of hippocampal synaptic plasticity. Neuron, 57, pp. 629–631.CrossRefGoogle ScholarPubMed
42.Chen, X. et al. (2010) The modulation of TRPM7 currents by nafamostat mesilate depends directly upon extracellular concentrations of divalent cations. Molecular Brain, 3 p. 38.CrossRefGoogle ScholarPubMed
43.Cevik, S. et al. (2010) Joubert syndrome Arl13b functions at ciliary membranes and stabilizes protein transport in Caenorhabditis elegans. Journal of Cell Biology, 188, pp. 953–969.CrossRefGoogle ScholarPubMed
44.Bach, G. (2005) Mucolipin 1: endocytosis and cation channel-a review. Pflugers Archiv. European Journal of Physiology, 451, pp. 313–317.CrossRefGoogle ScholarPubMed
45.Bach, G., Zeevi, D. A., Frumkin, A. and Kogot-Levin, A. (2010) Mucolipidosis type IV and the mucolipins. Biochemical Society Transactions, 38, pp. 1432–1435.CrossRefGoogle ScholarPubMed
46.Kiselyov, K., Yamaguchi, S., Lyons, C. W. and Muallem, S. (2010) Aberrant Ca(2+) handling in lysosomal storage disorders. Cell Calcium, 47, pp. 103–111.CrossRefGoogle Scholar
47.Miedel, M. T. et al. (2008) Membrane traffic and turnover in TRP-ML1-deficient cells: a revised model for mucolipidosis type IV pathogenesis. Journal of Experimental Medicine, 205, pp. 1477–1490.CrossRefGoogle Scholar
48.Venkatachalam, K. et al. (2008) Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell, 135, pp. 838–851.CrossRefGoogle Scholar
49.Venugopal, B. et al. (2009) Chaperone-mediated autophagy is defective in mucolipidosis type IV. Journal of Cell Physiology, 219, pp. 344–353.CrossRefGoogle ScholarPubMed
50.Dong, X.-P. et al. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature, 455, pp. 992–996.CrossRefGoogle Scholar
51.Plato, C. C. et al. (2002) ALS and PDC of Guam: forty-year follow-up. Neurology, 58, pp. 765–773.CrossRefGoogle ScholarPubMed
52.Plato, C. C. et al. (2003) Amyotrophic lateral sclerosis and parkinsonism-dementia complex of Guam: changing incidence rates during the past 60 years. American Journal of Epidemiology, 157, pp. 149–157.CrossRefGoogle ScholarPubMed
53.Hermosura, M. C. et al. (2005) A TRPM7 variant shows altered sensitivity to magnesium that may contribute to the pathogenesis of two Guamanian neurodegenerative disorders. Proceedings of the National Academy of Science USA, 102, pp. 11510–11515.CrossRefGoogle Scholar
54.McNulty, S. and Fonfria, E. (2005) The role of TRPM channels in cell death. Pflügers Archiv. European Journal of Physiology, 451, pp. 235–242.CrossRefGoogle ScholarPubMed
55.Li, S., Gosling, M., Poll, C. T., Westwick, J. and Cox, B. (2005) Therapeutic scope of modulation of non-voltage-gated cation channels. Drug Discoveries Today, 10, pp. 129–137.CrossRefGoogle ScholarPubMed
56.Li, S., Westwick, J., Cox, B. and Poll, C. T. (2004) TRP channels as drug targets. Novartis Found Symposium, 258, pp. 204–213; discussion 213–221, 263–266.CrossRefGoogle ScholarPubMed
57.Hermosura, M. et al. (2008) Altered functional properties of a TRPM2 variant in Guamanian ALS and PD. Proceedings of the National Academy of Science (USA), 105, pp. 18029–18034.CrossRefGoogle ScholarPubMed
58.Hermosura, M. C. and Garruto, R. M. (2007) TRPM7 and TRPM2-candidate susceptibility genes for Western Pacific ALS and PD? Biochim Biophys Acta, 1772, pp. 822–835.CrossRefGoogle ScholarPubMed
59.Landman, N. et al. (2006) Presenilin mutations linked to familial Alzheimer's disease cause an imbalance in phosphatidylinositol 4,5-bisphosphate metabolism. Proceedings of the National Academy of Science USA, 103, pp. 19524–19529.CrossRefGoogle ScholarPubMed
60.Lepichon, J. B., Bittel, D. C., Graf, W. D. and Yu, S. A. (2010) 15q13.3 homozygous microdeletion associated with a severe neurodevelopmental disorder suggests putative functions of the TRPM1, CHRNA7, and other homozygously deleted genes. American Journal of Medical Genetics A, 152A, pp. 1300–1304.CrossRefGoogle ScholarPubMed
61.Fernandez-Ruiz, J., Hernandez, M. and Ramos, J. A. (2010) Cannabinoid-dopamine interaction in the pathophysiology and treatment of CNS disorders. CNS Neuroscience & Therapeutics, 16, pp. e72–91.CrossRefGoogle ScholarPubMed
62.Moussaieff, A. et al. (2008) Incensole acetate, an incense component, elicits psychoactivity by activating TRPV3 channels in the brain. Faseb Journal, 22, pp. 3024–3034.CrossRefGoogle ScholarPubMed
63.Leuner, K. et al. (2007) Hyperforin – a key constituent of St. John's wort specifically activates TRPC6 channels. Faseb Journal, 21, pp. 4101–4111.Google Scholar
64.Griffith, T. N., Varela-Nallar, L. and Dinamarcaand N. Inestrosa, M. C. (2010) Neurobiological effects of hyperforin and its potential in Alzheimer's disease therapy. Current Medical Chemistry, 17, pp. 391–406.CrossRefGoogle ScholarPubMed
65.Aita, V. M. et al. (1999) A comprehensive linkage analysis of chromosome 21q22 supports prior evidence for a putative bipolar affective disorder locus. American Journal of Human Genetics, 64, pp. 210–217.CrossRefGoogle ScholarPubMed
66.Uemura, T., Kudoh, J., Noda, S., Kanba, S. and Shimizu, N. (2005) Characterization of human and mouse TRPM2 genes: identification of a novel N-terminal truncated protein specifically expressed in human striatum. Biochemical and Biophysical Research Communications, 328, pp. 1232–1243.CrossRefGoogle ScholarPubMed
67.Xu, C. et al. (2006) Association of the putative susceptibility gene, transient receptor potential protein melastatin type 2, with bipolar disorder. American Journal of Medical Genetics B Neuropsychiatric Genetics, 141, pp. 36–43.Google Scholar
68.Xu, C. et al. (2009) TRPM2 variants and bipolar disorder risk: confirmation in a family-based association study. Bipolar Disorder, 11, pp. 1–10.CrossRefGoogle Scholar
69.Chahl, L. A. (2007) TRP's: links to schizophrenia? Biochimica et Biophysica Acta, 1772, pp. 968–977.CrossRefGoogle ScholarPubMed
70.Cook, N. L., Vink, R., Helps, S. C., Manavis, J. and van den Heuvel, C. (2010) Transient receptor potential melastatin 2 expression is increased following experimental traumatic brain injury in rats. Journal of Molecular Neuroscience, 42, pp. 192–199.CrossRefGoogle ScholarPubMed
71.Simard, J. M., Kahle, K. T. and Gerzanich, V. (2010) Molecular mechanisms of microvascular failure in central nervous system injury-synergistic roles of NKCC1 and SUR1/TRPM4. Journal of Neurosurgery, 113, pp. 622–629.CrossRefGoogle ScholarPubMed
72.Gerzanich, V. et al. (2000) De novo expression of TRPM4 initiates secondary hemorrhage in spinal cord injury. Nature Medicine, 15, pp. 185–191.CrossRefGoogle Scholar
73.Rempe, D. A., Takano, T. and Nedergaard, M. (2009) TR(I)Pping towards treatment for ischemia. Nature Neuroscience, 12, pp. 1215–1216.CrossRefGoogle ScholarPubMed
74.Sun, H. S. et al. (2009) Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat Neuroscience, 12, pp. 1300–1307.CrossRefGoogle ScholarPubMed
75.Cook, N. L., Van Den Heuvel, C. and Vink, R. (2009) Are the transient receptor potential melastatin (TRPM) channels important in magnesium homeostasis following traumatic brain injury? Magnesium Research, 22, pp. 225–234.Google ScholarPubMed
76.Romero, J. R., Ridker, P. and Zee, R. Y. (2009) Gene variation of the transient receptor potential cation channel, subfamily m, member 7 (TRPM7), and risk of incident ischemic stroke. prospective, nested, case-control study. Stroke, 64, pp. 791–797.Google Scholar