Skip to main content

Advertisement

SpringerLink
Log in

TRPM8 and prostate: a cold case?

  • Invited Review
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

While originally cloned from the prostate in 2001, transient receptor potential, melastatin member 8 (TRPM8) has since been identified as the cold/menthol receptor in the peripheral nervous system. This discovery has led to hundreds of studies regarding the role of this channel in pain and thermosensation phenomena, while relegating TRPM8 involvement in cancer to a secondary role. Despite these findings, there is growing evidence that TRPM8 should be carefully studied within the frame of carcinogenesis, especially in the prostate, where it is highly expressed and where many teams have confirmed variations in its expression during cancer progression. Its regulation by physiological factors, such as PSA and androgens, has proved that TRPM8 can exhibit an activity beyond that of a cold receptor, thus explaining how the channel can be activated in organs not exposed to temperature variations. With this review, we aim to provide a brief overview of the current knowledge regarding the complex roles of TRPM8 in prostate carcinogenesis and to show that this research path still represents a “hot” topic with potential clinical applications in the short term.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Asuthkar S, Demirkhanyan L, Sun X, Elustondo PA, Krishnan V, Baskaran P, Velpula KK, Thyagarajan B, Pavlov EV, Zakharian E (2015) The TRPM8 protein is a testosterone receptor: II. Functional evidence for an ionotropic effect of testosterone on TRPM8. J Biol Chem 290:2670–2688. https://doi.org/10.1074/jbc.M114.610873

    Article  PubMed  CAS  Google Scholar 

  2. Asuthkar S, Velpula KK, Elustondo PA, Demirkhanyan L, Zakharian E (2015) TRPM8 channel as a novel molecular target in androgen-regulated prostate cancer cells. Oncotarget 6:17221–17236. https://doi.org/10.18632/oncotarget.3948

    Article  PubMed  PubMed Central  Google Scholar 

  3. Asuthkar S, Demirkhanyan L, Mueting SR, Cohen A, Zakharian E (2017) High-throughput proteome analysis reveals targeted TRPM8 degradation in prostate cancer. Oncotarget 8:12877–12890. https://doi.org/10.18632/oncotarget.14178

    Article  PubMed  Google Scholar 

  4. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt S-E, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204–208. https://doi.org/10.1038/nature05910

    Article  PubMed  CAS  Google Scholar 

  5. Beck B, Bidaux G, Bavencoffe A, Lemonnier L, Thebault S, Shuba Y, Barrit G, Skryma R, Prevarskaya N (2007) Prospects for prostate cancer imaging and therapy using high-affinity TRPM8 activators. Cell Calcium 41:285–294. https://doi.org/10.1016/j.ceca.2006.07.002

    Article  PubMed  CAS  Google Scholar 

  6. Behrendt H-J, 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 141:737–745. https://doi.org/10.1038/sj.bjp.0705652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Bidaux G, Roudbaraki M, Merle C, Crepin A, Delcourt P, Slomianny C, Thebault S, Bonnal J-L, 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 12:367–382. https://doi.org/10.1677/erc.1.00969

    Article  PubMed  CAS  Google Scholar 

  8. Bidaux G, Flourakis M, Thebault S, Zholos A, Beck B, Gkika D, Roudbaraki M, Bonnal J-L, Mauroy B, Shuba Y, Skryma R, Prevarskaya N (2007) Prostate cell differentiation status determines transient receptor potential melastatin member 8 channel subcellular localization and function. J Clin Invest 117:1647–1657. https://doi.org/10.1172/JCI30168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Bidaux G, Beck B, Zholos A, Gordienko D, Lemonnier L, Flourakis M, Roudbaraki M, Borowiec A-S, Fernandez J, Delcourt P, Lepage G, Shuba Y, Skryma R, Prevarskaya N (2012) Regulation of activity of transient receptor potential melastatin 8 (TRPM8) channel by its short isoforms. J Biol Chem 287:2948–2962. https://doi.org/10.1074/jbc.M111.270256

    Article  PubMed  CAS  Google Scholar 

  10. Bidaux G, Borowiec A, Gordienko D, Beck B, Shapovalov GG, Lemonnier L, Flourakis M, Vandenberghe M, Slomianny C, Dewailly E, Delcourt P, Desruelles E, Ritaine A, Polakowska R, Lesage J, Chami M, Skryma R, Prevarskaya N (2015) Epidermal TRPM8 channel isoform controls the balance between keratinocyte proliferation and differentiation in a cold-dependent manner. Proc Natl Acad Sci U S A 112:E3345–E3354. https://doi.org/10.1073/pnas.1423357112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Bidaux G, Sgobba M, Lemonnier L, Borowiec A-S, Noyer L, Jovanovic S, Zholos AV, Haider S (2015) Functional and modeling studies of the transmembrane region of the TRPM8 channel. Biophys J 109:1840–1851. https://doi.org/10.1016/j.bpj.2015.09.027

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Bidaux G, Borowiec A-S, Dubois C, Delcourt P, Schulz C, Vanden Abeele F, Lepage G, Desruelles E, Bokhobza A, Dewailly E, Slomianny C, Roudbaraki M, Heliot L, Bonnal J-L, Mauroy B, Mariot P, Lemonnier L, Prevarskaya N (2016) Targeting of short TRPM8 isoforms induces 4TM-TRPM8-dependent apoptosis in prostate cancer cells. Oncotarget 7:29063–29080. https://doi.org/10.18632/oncotarget.8666

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bidaux G, Borowiec A-S, Prevarskaya N, Gordienko D (2016) Fine-tuning of eTRPM8 expression and activity conditions keratinocyte fate. Channels (Austin) 10:320–331. https://doi.org/10.1080/19336950.2016.1168551

    Article  Google Scholar 

  14. Bidaux G, Gordienko D, Shapovalov G, Farfariello V, Borowiec A-S, Iamshanova O, Lemonnier L, Gueguinou M, Guibon R, Fromont G, Paillard M, Gouriou Y, Chouabe C, Dewailly E, Gkika D, Lopez-Alvarado P, Carlos Menendez J, Heliot L, Slomianny C, Prevarskaya N (2018) 4TM-TRPM8 channels are new gatekeepers of the ER-mitochondria Ca(2+) transfer. Biochim Biophys Acta 1865:981–994. https://doi.org/10.1016/j.bbamcr.2018.04.007

    Article  PubMed  CAS  Google Scholar 

  15. Bodding M, Wissenbach U, Flockerzi V (2007) Characterisation of TRPM8 as a pharmacophore receptor. Cell Calcium 42:618–628. https://doi.org/10.1016/j.ceca.2007.03.005

    Article  PubMed  CAS  Google Scholar 

  16. Bourne HR, Sanders DA, McCormick F (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348:125–132. https://doi.org/10.1038/348125a0

    Article  PubMed  CAS  Google Scholar 

  17. 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 101:15494–15499. https://doi.org/10.1073/pnas.0406773101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Carmona G, Gottig S, Orlandi A, Scheele J, Bauerle T, Jugold M, Kiessling F, Henschler R, Zeiher AM, Dimmeler S, Chavakis E (2009) Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis. Blood 113:488–497. https://doi.org/10.1182/blood-2008-02-138438

    Article  PubMed  CAS  Google Scholar 

  19. Cheung WYW, Ha N-R, Suen MWH, Xu CL, Yang CWT (2007) Warming up the cold reception at a TRPM8 function. J Neurosci 27:7617–7618. https://doi.org/10.1523/JNEUROSCI.2353-07.2007

    Article  PubMed  CAS  Google Scholar 

  20. Chrzanowska-Wodnicka M, Kraus AE, Gale D, White GC 2nd, Vansluys J (2008) Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. Blood 111:2647–2656. https://doi.org/10.1182/blood-2007-08-109710

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Chuang H, Neuhausser WM, Julius D (2004) The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43:859–869. https://doi.org/10.1016/j.neuron.2004.08.038

    Article  PubMed  CAS  Google Scholar 

  22. Colburn RW, Lubin ML, Stone DJJ, Wang Y, Lawrence D, D’Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379–386. https://doi.org/10.1016/j.neuron.2007.04.017

    Article  PubMed  CAS  Google Scholar 

  23. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371–378. https://doi.org/10.1016/j.neuron.2007.02.024

    Article  PubMed  CAS  Google Scholar 

  24. Duncan D, Stewart F, Frohlich M, Urdal D (2009) Preclinical evaluation of the TRPM8 ion channel agonist D-3263 for benign prostatic hyperplasia. J Urol 181:503. https://doi.org/10.1016/S0022-5347(09)61422-1

    Article  Google Scholar 

  25. Facer P, Casula MA, Smith GD, Benham CD, Chessell IP, Bountra C, Sinisi M, Birch R, Anand P (2007) Differential expression of the capsaicin receptor TRPV1 and related novel receptors TRPV3, TRPV4 and TRPM8 in normal human tissues and changes in traumatic and diabetic neuropathy. BMC Neurol 7:11. https://doi.org/10.1186/1471-2377-7-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Fernandez JA, Skryma R, Bidaux G, Magleby KL, Scholfield CN, McGeown JG, Prevarskaya N, Zholos AV (2011) Voltage- and cold-dependent gating of single TRPM8 ion channels. J Gen Physiol 137:173–195. https://doi.org/10.1085/jgp.201010498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Fujimoto N, Akimoto Y, Suzuki T, Kitamura S, Ohta S (2006) Identification of prostatic-secreted proteins in mice by mass spectrometric analysis and evaluation of lobe-specific and androgen-dependent mRNA expression. J Endocrinol 190:793–803. https://doi.org/10.1677/joe.1.06733

    Article  PubMed  CAS  Google Scholar 

  28. Genova T, Grolez GP, Camillo C, Bernardini M, Bokhobza A, Richard E, Scianna M, Lemonnier L, Valdembri D, Munaron L, Philips MR, Mattot V, Serini G, Prevarskaya N, Gkika D, Pla AF (2017) TRPM8 inhibits endothelial cell migration via a non-channel function by trapping the small GTPase Rap1. J Cell Biol 216(7):2107–2130. https://doi.org/10.1083/jcb.201506024

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Geretti E, Leonard SC, Dumont N, Lee H, Zheng J, De Souza R, Gaddy DF, Espelin CW, Jaffray DA, Moyo V, Nielsen UB, Wickham TJ, Hendriks BS (2015) Cyclophosphamide-mediated tumor priming for enhanced delivery and antitumor activity of HER2-targeted liposomal doxorubicin (MM-302). Mol Cancer Ther 14:2060–2071. https://doi.org/10.1158/1535-7163.MCT-15-0314

    Article  PubMed  CAS  Google Scholar 

  30. Gkika D, Prevarskaya N (2011) TRP channels in prostate cancer: the good, the bad and the ugly? Asian J Androl 13:673–676. https://doi.org/10.1038/aja.2011.18

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gkika D, Mahieu F, Nilius B, Hoenderop JGJ, Bindels RJM (2004) 80K-H as a new Ca2+ sensor regulating the activity of the epithelial Ca2+ channel transient receptor potential cation channel V5 (TRPV5). J Biol Chem 279:26351–26357. https://doi.org/10.1074/jbc.M403801200

    Article  PubMed  CAS  Google Scholar 

  32. Gkika D, Topala CN, Chang Q, Picard N, Thebault S, Houillier P, Hoenderop JGJ, Bindels RJM (2006) Tissue kallikrein stimulates Ca(2+) reabsorption via PKC-dependent plasma membrane accumulation of TRPV5. EMBO J 25:4707–4716. https://doi.org/10.1038/sj.emboj.7601357

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Gkika D, Flourakis M, Lemonnier L, Prevarskaya N (2010) PSA reduces prostate cancer cell motility by stimulating TRPM8 activity and plasma membrane expression. Oncogene 29:4611–4616. https://doi.org/10.1038/onc.2010.210

    Article  PubMed  CAS  Google Scholar 

  34. Gkika D, Lemonnier L, Shapovalov G, Gordienko D, Poux C, Bernardini M, Bokhobza A, Bidaux G, Degerny C, Verreman K, Guarmit B, Benahmed M, de Launoit Y, Bindels RJM, Fiorio Pla A, Prevarskaya N (2015) TRP channel-associated factors are a novel protein family that regulates TRPM8 trafficking and activity. J Cell Biol 208:89–107. https://doi.org/10.1083/jcb.201402076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Grolez GP, Gkika D (2016) TRPM8 puts the chill on prostate cancer. Pharm Basel Switz 9. https://doi.org/10.3390/ph9030044

  36. Harteneck C, Gollasch M (2011) Pharmacological modulation of diacylglycerol-sensitive TRPC3/6/7 channels. Curr Pharm Biotechnol 12:35–41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Henshall SM, Afar DEH, 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 63:4196–4203

    PubMed  CAS  Google Scholar 

  38. Karashima Y, Damann N, Prenen J, Talavera K, Segal A, Voets T, Nilius B (2007) Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 27:9874–9884. https://doi.org/10.1523/JNEUROSCI.2221-07.2007

    Article  PubMed  CAS  Google Scholar 

  39. Kuhn FJP, Kuhn C, Luckhoff A (2009) Inhibition of TRPM8 by icilin distinct from desensitization induced by menthol and menthol derivatives. J Biol Chem 284:4102–4111. https://doi.org/10.1074/jbc.M806651200

    Article  PubMed  CAS  Google Scholar 

  40. Lafuente EM, van Puijenbroek AAFL, Krause M, Carman CV, Freeman GJ, Berezovskaya A, Constantine E, Springer TA, Gertler FB, Boussiotis VA (2004) RIAM, an Ena/VASP and profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell 7:585–595. https://doi.org/10.1016/j.devcel.2004.07.021

    Article  PubMed  CAS  Google Scholar 

  41. Lashinger ESR, Steiginga MS, Hieble JP, Leon LA, Gardner SD, Nagilla R, Davenport EA, Hoffman BE, Laping NJ, Su X (2008) AMTB, a TRPM8 channel blocker: evidence in rats for activity in overactive bladder and painful bladder syndrome. Am J Physiol Ren Physiol 295:F803–F810. https://doi.org/10.1152/ajprenal.90269.2008

    Article  CAS  Google Scholar 

  42. Liu B, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:1674–1681. https://doi.org/10.1523/JNEUROSCI.3632-04.2005

    Article  PubMed  CAS  Google Scholar 

  43. Macpherson LJ, Hwang SW, Miyamoto T, Dubin AE, Patapoutian A, Story GM (2006) More than cool: promiscuous relationships of menthol and other sensory compounds. Mol Cell Neurosci 32:335–343. https://doi.org/10.1016/j.mcn.2006.05.005

    Article  PubMed  CAS  Google Scholar 

  44. Mahieu F, Owsianik G, Verbert L, Janssens A, De Smedt H, Nilius B, Voets T (2007) TRPM8-independent menthol-induced Ca2+ release from endoplasmic reticulum and Golgi. J Biol Chem 282:3325–3336. https://doi.org/10.1074/jbc.M605213200

    Article  PubMed  CAS  Google Scholar 

  45. Maingret F, Patel AJ, Lesage F, Lazdunski M, Honore E (2000) Lysophospholipids open the two-pore domain mechano-gated K(+) channels TREK-1 and TRAAK. J Biol Chem 275:10128–10133

    Article  PubMed  CAS  Google Scholar 

  46. Malkia A, Madrid R, Meseguer V, de la Pena E, Valero M, Belmonte C, Viana F (2007) Bidirectional shifts of TRPM8 channel gating by temperature and chemical agents modulate the cold sensitivity of mammalian thermoreceptors. J Physiol 581:155–174. https://doi.org/10.1113/jphysiol.2006.123059

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Malkia A, Pertusa M, Fernandez-Ballester G, Ferrer-Montiel A, Viana F (2009) Differential role of the menthol-binding residue Y745 in the antagonism of thermally gated TRPM8 channels. Mol Pain 5:62. https://doi.org/10.1186/1744-8069-5-62

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Malkia A, Morenilla-Palao C, Viana F (2011) The emerging pharmacology of TRPM8 channels: hidden therapeutic potential underneath a cold surface. Curr Pharm Biotechnol 12:54–67

    Article  PubMed  CAS  Google Scholar 

  49. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58. https://doi.org/10.1038/nature719

    Article  PubMed  CAS  Google Scholar 

  50. Miller S, Rao S, Wang W, Liu H, Wang J, Gavva NR (2014) Antibodies to the extracellular pore loop of TRPM8 act as antagonists of channel activation. PLoS One 9:e107151. https://doi.org/10.1371/journal.pone.0107151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Morgan K, Sadofsky LR, Crow C, Morice AH (2014) Human TRPM8 and TRPA1 pain channels, including a gene variant with increased sensitivity to agonists (TRPA1 R797T), exhibit differential regulation by. Biosci Rep 34:469–478. https://doi.org/10.1042/BSR20140061

    Article  CAS  Google Scholar 

  52. Mukerji G, Yiangou Y, Corcoran SL, Selmer IS, Smith GD, Benham CD, Bountra C, Agarwal SK, Anand P (2006) Cool and menthol receptor TRPM8 in human urinary bladder disorders and clinical correlations. BMC Urol 6:6. https://doi.org/10.1186/1471-2490-6-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Patel R, Goncalves L, Newman R, Jiang FL, Goldby A, Reeve J, Hendrick A, Teall M, Hannah D, Almond S, Brice N, Dickenson AH (2014) Novel TRPM8 antagonist attenuates cold hypersensitivity after peripheral nerve injury in rats. J Pharmacol Exp Ther 349:47–55. https://doi.org/10.1124/jpet.113.211243

    Article  PubMed  CAS  Google Scholar 

  54. 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 108:705–715

    Article  PubMed  CAS  Google Scholar 

  55. Peng M, Wang Z, Yang Z, Tao L, Liu Q, Yi LU, Wang X (2015) Overexpression of short TRPM8 variant alpha promotes cell migration and invasion, and decreases starvation-induced apoptosis in prostate cancer LNCaP cells. Oncol Lett 10:1378–1384. https://doi.org/10.3892/ol.2015.3373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Prevarskaya N, Skryma R, Shuba Y (2018) Ion channels in cancer: are cancer hallmarks oncochannelopathies? Physiol Rev 98:559–621. https://doi.org/10.1152/physrev.00044.2016

    Article  PubMed  Google Scholar 

  57. Redondo PC, Rosado JA (2015) Store-operated calcium entry: unveiling the calcium handling signalplex. Int Rev Cell Mol Biol 316:183–226. https://doi.org/10.1016/bs.ircmb.2015.01.007

    Article  PubMed  Google Scholar 

  58. Reedquist KA, Ross E, Koop EA, Wolthuis RM, Zwartkruis FJ, van Kooyk Y, Salmon M, Buckley CD, Bos JL (2000) The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J Cell Biol 148:1151–1158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Reid RC, Yau M-K, Singh R, Hamidon JK, Reed AN, Chu P, Suen JY, Stoermer MJ, Blakeney JS, Lim J, Faber JM, Fairlie DP (2013) Downsizing a human inflammatory protein to a small molecule with equal potency and functionality. Nat Commun 4:2802. https://doi.org/10.1038/ncomms3802

    Article  PubMed  CAS  Google Scholar 

  60. Rohacs T, Lopes CMB, Michailidis I, Logothetis DE (2005) PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8:626–634. https://doi.org/10.1038/nn1451

    Article  PubMed  CAS  Google Scholar 

  61. 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 172:1175–1178. https://doi.org/10.1097/01.ju.0000134880.55119.cf

    Article  PubMed  CAS  Google Scholar 

  62. 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 112:819–829

    Article  PubMed  CAS  Google Scholar 

  63. Sweeney ZK, Minatti A, Button DC, Patrick S (2009) Small-molecule inhibitors of store-operated calcium entry. ChemMedChem 4:706–718. https://doi.org/10.1002/cmdc.200800452

    Article  PubMed  CAS  Google Scholar 

  64. 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 280:39423–39435. https://doi.org/10.1074/jbc.M503544200

    Article  PubMed  CAS  Google Scholar 

  65. 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 61:3760–3769

    PubMed  CAS  Google Scholar 

  66. Vanden Abeele F, Zholos A, Bidaux G, Shuba Y, Thebault S, Beck B, Flourakis M, Panchin Y, Skryma R, Prevarskaya N (2006) Ca2+-independent phospholipase A2-dependent gating of TRPM8 by lysophospholipids. J Biol Chem 281:40174–40182. https://doi.org/10.1074/jbc.M605779200

    Article  CAS  Google Scholar 

  67. Vincent F, Acevedo A, Nguyen MT, Dourado M, DeFalco J, Gustafson A, Spiro P, Emerling DE, Kelly MG, Duncton MAJ (2009) Identification and characterization of novel TRPV4 modulators. Biochem Biophys Res Commun 389:490–494. https://doi.org/10.1016/j.bbrc.2009.09.007

    Article  PubMed  CAS  Google Scholar 

  68. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748–754. https://doi.org/10.1038/nature02732

    Article  PubMed  CAS  Google Scholar 

  69. Voets T, Owsianik G, Janssens A, Talavera K, Nilius B (2007) TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat Chem Biol 3:174–182. https://doi.org/10.1038/nchembio862

    Article  PubMed  CAS  Google Scholar 

  70. Weil A, Moore SE, Waite NJ, Randall A, Gunthorpe MJ (2005) Conservation of functional and pharmacological properties in the distantly related temperature sensors TRVP1 and TRPM8. Mol Pharmacol 68:518–527. https://doi.org/10.1124/mol.105.012146

    Article  PubMed  CAS  Google Scholar 

  71. Xiao B, Dubin AE, Bursulaya B, Viswanath V, Jegla TJ, Patapoutian A (2008) Identification of transmembrane domain 5 as a critical molecular determinant of menthol sensitivity in mammalian TRPA1 channels. J Neurosci 28:9640–9651. https://doi.org/10.1523/JNEUROSCI.2772-08.2008

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Xu XZ, Moebius F, Gill DL, Montell C (2001) Regulation of melastatin, a TRP-related protein, through interaction with a cytoplasmic isoform. Proc Natl Acad Sci U S A 98:10692–10697. https://doi.org/10.1073/pnas.191360198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Yallapu MM, Khan S, Maher DM, Ebeling MC, Sundram V, Chauhan N, Ganju A, Balakrishna S, Gupta BK, Zafar N, Jaggi M, Chauhan SC (2014) Anti-cancer activity of curcumin loaded nanoparticles in prostate cancer. Biomaterials 35:8635–8648. https://doi.org/10.1016/j.biomaterials.2014.06.040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Yang Z-H, Wang X-H, Wang H-P, Hu L-Q (2009) Effects of TRPM8 on the proliferation and motility of prostate cancer PC-3 cells. Asian J Androl 11:157–165. https://doi.org/10.1038/aja.2009.1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Yee NS, Zhou W, Lee M (2010) Transient receptor potential channel TRPM8 is over-expressed and required for cellular proliferation in pancreatic adenocarcinoma. Cancer Lett 297:49–55. https://doi.org/10.1016/j.canlet.2010.04.023

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Yin Y, Wu M, Zubcevic L, Borschel WF, Lander GC, Lee S-Y (2018) Structure of the cold- and menthol-sensing ion channel TRPM8. Science 359:237–241. https://doi.org/10.1126/science.aan4325

    Article  PubMed  CAS  Google Scholar 

  77. Yu B, Tai HC, Xue W, Lee LJ, Lee RJ (2010) Receptor-targeted nanocarriers for therapeutic delivery to cancer. Mol Membr Biol 27:286–298. https://doi.org/10.3109/09687688.2010.521200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Yudin Y, Rohacs T (2012) Regulation of TRPM8 channel activity. Mol Cell Endocrinol 353:68–74. https://doi.org/10.1016/j.mce.2011.10.023

    Article  PubMed  CAS  Google Scholar 

  79. Yudin Y, Lutz B, Tao Y-X, Rohacs T (2016) Phospholipase C delta4 regulates cold sensitivity in mice. J Physiol 594:3609–3628. https://doi.org/10.1113/JP272321

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Zhang L, Barritt GJ (2004) Evidence that TRPM8 is an androgen-dependent Ca2+ channel required for the survival of prostate cancer cells. Cancer Res 64:8365–8373. https://doi.org/10.1158/0008-5472.CAN-04-2146

    Article  PubMed  CAS  Google Scholar 

  81. Zhang L, Barritt GJ (2006) TRPM8 in prostate cancer cells: a potential diagnostic and prognostic marker with a secretory function? Endocr Relat Cancer 13:27–38. https://doi.org/10.1677/erc.1.01093

    Article  PubMed  CAS  Google Scholar 

  82. Zhang L, Jones S, Brody K, Costa M, Brookes SJH (2004) Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. Am J Physiol Gastrointest Liver Physiol 286:G983–G991. https://doi.org/10.1152/ajpgi.00441.2003

    Article  PubMed  CAS  Google Scholar 

  83. Zhu G, Wang X, Yang Z, Cao H, Meng Z, Wang Y, Chen D (2011) Effects of TRPM8 on the proliferation and angiogenesis of prostate cancer PC-3 cells in vivo. Oncol Lett 2:1213–1217. https://doi.org/10.3892/ol.2011.410

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

Our work was supported by funds from INSERM, University Lille Nord de France, Ministère de l’Education Nationale, LabEx ICST, Ligue Contre le Cancer, Fondation ARC pour la recherche sur le cancer (PJA 20141202010), Agence Nationale pour la Recherche, the Region Hauts de France, SIRIC ONCOLille, Canceropole Nord Ouest, Association pour la Recherche sur les Tumeurs de la Prostate, and the Institut National du Cancer (INCa-PLBIO14-213).

Author information

Author notes

  1. Lucile Noyer, Guillaume P. Grolez, Dimitra Gkika and Loic Lemonnier contributed equally to this work.

Authors and Affiliations

  1. Inserm, U1003, Laboratory of Cell Physiology, University Lille Nord de France, 59655 Cedex, Villeneuve d’Ascq, France

    Lucile Noyer, Guillaume P. Grolez, Natalia Prevarskaya, Dimitra Gkika & Loic Lemonnier

  2. Laboratory of Excellence, Ion Channels Science and Therapeutics, Villeneuve d’Ascq, France

    Lucile Noyer, Guillaume P. Grolez, Natalia Prevarskaya, Dimitra Gkika & Loic Lemonnier

Authors
  1. Lucile Noyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guillaume P. Grolez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia Prevarskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dimitra Gkika
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loic Lemonnier
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L. N., G. G., N. P., D. G., and L. L. wrote the paper.

Corresponding author

Correspondence to Loic Lemonnier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Noyer, L., Grolez, G.P., Prevarskaya, N. et al. TRPM8 and prostate: a cold case?. Pflugers Arch - Eur J Physiol 470, 1419–1429 (2018). https://doi.org/10.1007/s00424-018-2169-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-018-2169-1

Keywords

Search

Navigation