Advertisement

Abstract

Originally cloned as a prostate-specific protein, TRPM8 is now best known as a cold- and menthol-activated channel implicated in thermosensation. In this chapter we provide a brief review of current knowledge concerning the biophysical properties, gating mechanisms, pharmacology and (patho)physiology of this TRP channel.

Keywords

Temperature sensing Voltage-dependent gating 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abe J, Hosokawa H, Sawada Y, Matsumura K, Kobayashi S (2005) Ca(2+)-dependent PKC activation mediates menthol-induced desensitization of transient receptor potential M8. Neurosci Lett 397:140–144PubMedCrossRefGoogle Scholar
  2. Andersson DA, Chase HW, Bevan S (2004) TRPM8 activation by menthol, icilin, and cold is differentially modulated by intracellular pH. J Neurosci 24:5364–5369PubMedCrossRefGoogle Scholar
  3. Babes A, Zorzon D, Reid G (2004) Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur J Neurosci 20:2276–2282PubMedCrossRefGoogle Scholar
  4. Behrendt HJ, Germann T, Gillen C, Hatt H, Jostock R (2004) Characterization of the mouse cold-menthol receptor TRPM8 and vanilloid receptor type-1 VR1 using a fluorometric imaging plate reader (FLIPR) assay. Br J Pharmacol 141:737–745PubMedCrossRefGoogle Scholar
  5. Bidaux G, Roudbaraki M, Merle C, Crepin A, Delcourt P, Slomianny C, Thebault S, Bonnal JL, Benahmed M, Cabon F, Mauroy B, Prevarskaya N (2005) Evidence for specific TRPM8 expression in human prostate secretory epithelial cells: functional androgen receptor requirement. Endocr Relat Cancer 12:367–382PubMedCrossRefGoogle Scholar
  6. Bilmen JG, Wootton LL, Godfrey RE, Smart OS, Michelangeli F (2002) Inhibition of SERCA Ca2+ pumps by 2-aminoethoxydiphenyl borate (2-APB). 2-APB reduces both Ca2+ binding and phosphoryl transfer from ATP, by interfering with the pathway leading to the Ca2+-binding sites. Eur J Biochem 269:3678–3687PubMedCrossRefGoogle Scholar
  7. Brauchi S, Orio P, Latorre R (2004) Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. Proc Natl Acad Sci U S A 101:15494–15499PubMedCrossRefGoogle Scholar
  8. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306–313PubMedCrossRefGoogle Scholar
  9. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D (2001) Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411:957–962PubMedCrossRefGoogle Scholar
  10. Chuang HH, Neuhausser WM, Julius D (2004) The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43:859–869PubMedCrossRefGoogle Scholar
  11. Chung MK, Lee H, Mizuno A, Suzuki M, Caterina MJ (2004) 2-Aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J Neurosci 24:5177–5182PubMedCrossRefGoogle Scholar
  12. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183–187PubMedCrossRefGoogle Scholar
  13. Fuessel S, Sickert D, Meye A, Klenk U, Schmidt U, Schmitz M, Rost AK, Weigle B, Kiessling A, Wirth MP (2003) Multiple tumor marker analyses (PSA, hK2, PSCA, trp-p8) in primary prostate cancers using quantitative RT-PCR. Int J Oncol 23:221–228PubMedGoogle Scholar
  14. Gavva NR, Klionsky L, Qu Y, Shi L, Tamir R, Edenson S, Zhang TJ, Viswanadhan VN, Toth A, Pearce LV, Vanderah TW, Porreca F, Blumberg PM, Lile J, Sun Y, Wild K, Louis JC, Treanor JJ (2004) Molecular determinants of vanilloid sensitivity in TRPV1. J Biol Chem 279:20283–20295PubMedCrossRefGoogle Scholar
  15. Henshall SM, Afar DE, Hiller J, Horvath LG, Quinn DI, Rasiah KK, Gish K, Willhite D, Kench JG, Gardiner-Garden M, Stricker PD, Scher HI, Grygiel JJ, Agus DB, Mack DH, Sutherland RL (2003) Survival analysis of genome-wide gene expression profiles of prostate cancers identifies new prognostic targets of disease relapse. Cancer Res 63:4196–4203PubMedGoogle Scholar
  16. Hoenderop JGJ, Voets T, Hoefs S, Weidema F, Prenen J, Nilius B, Bindels RJM (2003) Homo-and heterotetrameric architecture of the epithelial Ca2+ channels, TRPV5 and TRPV6. EMBO J 22:776–785PubMedCrossRefGoogle Scholar
  17. Hu HZ, Gu Q, Wang C, Colton CK, Tang J, Kinoshita-Kawada M, Lee LY, Wood JD, Zhu MX (2004) 2-Aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279:35741–35748PubMedCrossRefGoogle Scholar
  18. Hui K, Guo Y, Feng ZP (2005) Biophysical properties of menthol-activated cold receptor TRPM8 channels. Biochem Biophys Res Commun 333:374–382PubMedCrossRefGoogle Scholar
  19. Iwasaki H, Mori Y, Hara Y, Uchida K, Zhou H, Mikoshiba K (2001) 2-Aminoethoxydiphenyl borate (2-APB) inhibits capacitative calcium entry independently of the function of inositol 1,4,5-trisphosphate receptors. Receptors Channels 7:429–439PubMedGoogle Scholar
  20. Jerman JC, Brough SJ, Prinjha R, Harries MH, Davis JB, Smart D (2000) Characterization using FLIPR of rat vanilloid receptor (rVR1) pharmacology. Br J Pharmacol 130:916–922PubMedCrossRefGoogle Scholar
  21. Jordt SE, Julius D (2002) Molecularbasis for species-specific sensitivity to “hot” chilipeppers. Cell 108:421–430PubMedCrossRefGoogle Scholar
  22. Julius D, Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413:203–210PubMedCrossRefGoogle Scholar
  23. Liu B, Qin F (2005) Functional control of cold-and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:1674–1681PubMedCrossRefGoogle Scholar
  24. Maruyama T, Kanaji T, Nakade S, Kanno T, Mikoshiba K (1997) 2APB, 2-aminoethoxydiphenyl borate, a membrane-penetrable modulator of Ins(1,4,5)P3-induced Ca2+ release. J Biochem (Tokyo) 122:498–505PubMedGoogle Scholar
  25. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58PubMedCrossRefGoogle Scholar
  26. Missiaen L, Callewaert G, De Smedt H, Parys JB (2001) 2-Aminoethoxydiphenyl borate affects the inositol 1,4,5-trisphosphate receptor, the intracellular Ca2+ pump and the non-specific Ca2+ leak from the non-mitochondrial Ca2+ stores in permeabilized A7r5 cells. Cell Calcium 29:111–116PubMedCrossRefGoogle Scholar
  27. Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005:re3Google Scholar
  28. Montell C, Birnbaumer L, Flockerzi V, Bindels RJ, Bruford EA, Caterina MJ, Clapham DE, Harteneck C, Heller S, Julius D, Kojima I, Mori Y, Penner R, Prawitt D, Scharenberg AM, Schultz G, Shimizu N, Zhu MX (2002) A unified nomenclature for the superfamily of TRP cation channels. Mol Cell 9:229–231PubMedCrossRefGoogle Scholar
  29. Mustafa S, Oriowo M (2005) Cooling-induced contraction of the rat gastric fundus: mediation via transient receptor potential (TRP) cation channel TRPM8 receptor and Rho-kinase activation. Clin Exp Pharmacol Physiol 32:832–838PubMedCrossRefGoogle Scholar
  30. Nadler MJ, Hermosura MC, Inabe K, Perraud AL, Zhu Q, Stokes AJ, Kurosaki T, Kinet JP, Penner R, Scharenberg AM, Fleig A (2001) LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 411:590–595PubMedCrossRefGoogle Scholar
  31. Nealen ML, Gold MS, Thut PD, Caterina MJ (2003) TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90:515–520PubMedCrossRefGoogle Scholar
  32. Nilius B, Voets T, Peters J (2005a) TRP channels in disease. Sci STKE 2005:re8Google Scholar
  33. Nilius B, Prenen J, Janssens A, Owsianik G, Wang C, Zhu MX, Voets T (2005b) The selectivity filter of the cation channel TRPM4. J Biol Chem 280:22899–22906PubMedCrossRefGoogle Scholar
  34. Owsianik G, Talavera K, Voets T, Nilius B (2006) Permeation and selectivity of TRP channels. Annu Rev Physiol 68:685–717PubMedCrossRefGoogle Scholar
  35. Patapoutian A, Peier AM, Story GM, Viswanath V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4:529–539PubMedCrossRefGoogle Scholar
  36. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705–715PubMedCrossRefGoogle Scholar
  37. Premkumar LS, Ahern GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985–990PubMedCrossRefGoogle Scholar
  38. Premkumar LS, Raisinghani M, Pingle SC, Long C, Pimentel F (2005) Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. J Neurosci 25:11322–11329PubMedCrossRefGoogle Scholar
  39. Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300:1284–1288PubMedCrossRefGoogle Scholar
  40. Reid G (2005) Thermo TRP channels and cold sensing: what are they really up to? Pflugers Arch 451:250–263PubMedCrossRefGoogle Scholar
  41. Reid G, Flonta M (2001b) Cold transduction by inhibition of a background potassium conductance in rat primary sensory neurones. Neurosci Lett 297:171–174PubMedCrossRefGoogle Scholar
  42. Reid G, Flonta ML (2001a) Physiology. Cold current in thermoreceptive neurons. Nature 413:480PubMedCrossRefGoogle Scholar
  43. Rohacs T, Lopes CM, Michailidis I, Logothetis DE (2005) PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8:626–634PubMedCrossRefGoogle Scholar
  44. Schmitz C, Perraud AL, Johnson CO, Inabe K, Smith MK, Penner R, Kurosaki T, Fleig A, Scharenberg AM (2003) Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 114:191–200PubMedCrossRefGoogle Scholar
  45. Stein RJ, Santos S, Nagatomi J, Hayashi Y, Minnery BS, Xavier M, Patel AS, Nelson JB, Futrell WJ, Yoshimura N, Chancellor MB, De Miguel F (2004) Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract. J Urol 172:1175–1178PubMedCrossRefGoogle Scholar
  46. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829PubMedCrossRefGoogle Scholar
  47. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B (2005) Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022–1025PubMedCrossRefGoogle Scholar
  48. Thebault S, Lemonnier L, Bidaux G, Flourakis M, Bavencoffe A, Gordienko D, Roudbaraki M, Delcourt P, Panchin Y, Shuba Y, Skryma R, Prevarskaya N (2005) Novel role of cold/menthol-sensitive transient receptor potential melastatine family member 8 (TRPM8) in the activation of store-operated channels in LNCaP human prostate cancer epithelial cells. J Biol Chem 280:39423–39435PubMedCrossRefGoogle Scholar
  49. Tsavaler L, Shapero MH, Morkowski S, Laus R (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61:3760–3769PubMedGoogle Scholar
  50. Tsukimi Y, Mizuyachi K, Yamasaki T, Niki T, Hayashi F (2005) Cold response of the bladder in guinea pig: involvement of transient receptor potential channel, TRPM8. Urology 65:406–410PubMedCrossRefGoogle Scholar
  51. Valenzano KJ, Grant ER, Wu G, Hachicha M, Schmid L, Tafesse L, Sun Q, Rotshteyn Y, Francis J, Limberis J, Malik S, Whittemore ER, Hodges D (2003) N-(4-tertiarybutylphenyl)-4-(3-chloropyridin-2-yl)tetrahydropyrazine-1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties. I. In vitro characterization and pharmacokinetic properties. J Pharmacol Exp Ther 306:377–386PubMedCrossRefGoogle Scholar
  52. Viana F, de la Pena E, Belmonte C (2002) Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat Neurosci 5:254–260PubMedCrossRefGoogle Scholar
  53. Voets T, Prenen J, Fleig A, Vennekens R, Watanabe H, Hoenderop JG, Bindels RJ, Droogmans G, Penner R, Nilius B (2001) CaT1 and the calcium release-activated calcium channel manifest distinct pore properties. J Biol Chem 276:47767–47770PubMedGoogle Scholar
  54. Voets T, Janssens A, Droogmans G, Nilius B (2004a) Outer pore architecture of a Ca2+-selective TRP channel. J Biol Chem 279:15223–15230PubMedCrossRefGoogle Scholar
  55. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004b) The principle of temperature-dependent gating in cold-and heat-sensitive TRP channels. Nature 430:748–754PubMedCrossRefGoogle Scholar
  56. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B (2004) Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci U S A 101:396–401PubMedCrossRefGoogle Scholar
  57. Xu SZ, Zeng F, Lei M, Li J, Gao B, Xiong C, Sivaprasadarao A, Beech DJ (2005) Generation of functional ion-channel tools by E3 targeting. Nat Biotechnol 23:1289–1293PubMedCrossRefGoogle Scholar
  58. Yang XR, Lin MJ, McIntosh LS, Sham JS (2006) Functional expression of transient receptor potential melastatin-(TRPM) and vanilloid-related (TRPV) channels in pulmonary arterial and aortic smooth muscle. Am J Physiol Lung Cell Mol Physiol 290:L1267–L1276PubMedCrossRefGoogle Scholar
  59. Zhang L, Barritt GJ (2004) Evidence that TRPM8 is an androgen-dependent Ca2+ channel required for the survival of prostate cancer cells. Cancer Res 64:8365–8373PubMedCrossRefGoogle Scholar
  60. Zhang L, Jones S, Brody K, Costa M, Brookes SJ (2004) Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. Am J Physiol Gastrointest Liver Physiol 286:G983–991PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2007

Authors and Affiliations

  • T. Voets
    • 1
  • G. Owsianik
    • 1
  • B. Nilius
    • 1
  1. 1.Laboratory of PhysiologyKU LeuvenLeuvenBelgium

Personalised recommendations