Functional significance of thermosensitive transient receptor potential melastatin channel 8 (TRPM8) expression in immortalized human corneal endothelial cells

Experimental Eye Research

Volumn 116, Issue , 2013, Pages 337-349

  Mergler, Stefan ^a   Mertens, Charlotte ^a   Valtink, Monika ^b   Reinach, Peter S ^c   Castelo Székely, Violeta ^a   Slavi, Nefeli ^c   Garreis, Fabian ^d   Abdelmessih, Suzette ^a   Türker, Ersal ^a   Fels, Gabriele ^a   Pleyer, Uwe ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

BCTC; CAP; CPZ; HCEC 12; Human corneal endothelium; Intracellular Ca2+; Planar patch clamp technique; Transient receptor potential melastatin 8 channel; TRPA; TRPM

Indexed keywords

CAPSAZEPINE; CINEOLE; MENTHOL; N (4 TERT BUTYLPHENYL) 4 (3 CHLORO 2 PYRIDINYL) 1 PIPERAZINECARBOXAMIDE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8;

ARTICLE; CELL IMMORTALIZATION; CONTROLLED STUDY; COOLING; CORNEA CELL; CORNEAL ENDOTHELIAL CELL; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; PATCH CLAMP; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROOM TEMPERATURE; TEMPERATURE STRESS;

BCTC; CAP; CAPSAICIN; CAPSAZEPINE; CPZ; HCEC-12; HUMAN CORNEAL ENDOTHELIUM; IMMORTALIZED HUMAN CORNEAL ENDOTHELIAL CELL LINE; INTRACELLULAR CA(2+); N-(4-TERT.BUTYL-PHENYL)-4-(3-CHLOROPYRIDIN-2-YL) TETRAHYDROPYRAZINE-1(2H)-CARBOXAMIDE; PLANAR PATCH-CLAMP TECHNIQUE; TRANSIENT RECEPTOR POTENTIAL ANKYRIN; TRANSIENT RECEPTOR POTENTIAL MELASTATIN; TRANSIENT RECEPTOR POTENTIAL MELASTATIN 8 CHANNEL; TRPA; TRPM;

CALCIUM; CELL LINE; ENDOTHELIUM, CORNEAL; GENE EXPRESSION REGULATION; HOT TEMPERATURE; HUMANS; PATCH-CLAMP TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; RNA; THERMOSENSING; TRPM CATION CHANNELS;

EID: 84886860266     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.10.003     Document Type: Article

References (44)

1. Bandell M., Dubin A.E., Petrus M.J., Orth A., Mathur J., Hwang S.W., Patapoutian A. High-throughput random mutagenesis screen reveals TRPM8 residues specifically required for activation by menthol. Nat. Neurosci. 2006, 9:493-500.
2. Bautista D.M., Siemens J., Glazer J.M., Tsuruda P.R., Basbaum A.I., Stucky C.L., Jordt S.E., Julius D. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 2007, 448:204-208.
3. Bednarz J., Teifel M., Friedl P., Engelmann K. Immortalization of human corneal endothelial cells using electroporation protocol optimized for human corneal endothelial and human retinal pigment epithelial cells. Acta Ophthalmol. Scand. 2000, 78:130-136.
4. Bednarz J., Weich H.A., Rodokanaki-von Schrenck A., Engelmann K. Expression of genes coding growth factors and growth factor receptors in differentiated and dedifferentiated human corneal endothelial cells. Cornea 1995, 14:372-381.
5. Behrendt H.J., Germann T., Gillen C., Hatt H., Jostock R. 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. 2004, 141:737-745.
6. Bonanno J.A. Molecular mechanisms underlying the corneal endothelial pump. Exp. Eye Res. 2012, 95:2-7.
7. Bruggemann A., Farre C., Haarmann C., Haythornthwaite A., Kreir M., Stoelzle S., George M., Fertig N. Planar patch clamp: advances in electrophysiology. Methods Mol. Biol. 2008, 491:165-176.
8. Bruggemann A., Stoelzle S., George M., Behrends J.C., Fertig N. Microchip technology for automated and parallel patch-clamp recording. Small 2006, 2:840-846.
9. Chuang H.H., Neuhausser W.M., Julius D. The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 2004, 43:859-869.
10. Crawford D.C., Moulder K.L., Gereau R.W., Story G.M., Mennerick S. Comparative effects of heterologous TRPV1 and TRPM8 expression in rat hippocampal neurons. PLoS. ONE 2009, 4:e8166.
11. Engelmann K., Bohnke M., Friedl P. Isolation and long-term cultivation of human corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 1988, 29:1656-1662.
12. Fonfria E., Murdock P.R., Cusdin F.S., Benham C.D., Kelsell R.E., McNulty S. Tissue distribution profiles of the human TRPM cation channel family. J.Recept. Signal. Transduct. Res. 2006, 26:159-178.
13. 2+ indicators with greatly improved fluorescence properties. J.Biol. Chem. 1985, 260:3440-3450.
14. Hirata H., Oshinsky M.L. Ocular dryness excites two classes of corneal afferent neurons implicated in basal tearing in rats: involvement of transient receptor potential channels. J.Neurophysiol. 2012, 107:1199-1209.
15. Kim S.H., Nam J.H., Park E.J., Kim B.J., Kim S.J., So I., Jeon J.H. Menthol regulates TRPM8-independent processes in PC-3 prostate cancer cells. Biochim. Biophys. Acta 2009, 1792:33-38.
16. Kobayashi K., Fukuoka T., Obata K., Yamanaka H., Dai Y., Tokunaga A., Noguchi K. Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J.Comp. Neurol. 2005, 493:596-606.
17. Kochukov M.Y., McNearney T.A., Fu Y., Westlund K.N. Thermosensitive TRP ion channels mediate cytosolic calcium response in human synoviocytes. Am. J. Physiol. Cell. Physiol. 2006, 291:C424-C432.
18. 2+ release from endoplasmic reticulum and Golgi. J.Biol. Chem. 2007, 282:3325-3336.
19. Malkia A., Pertusa M., Fernandez-Ballester G., Ferrer-Montiel A., Viana F. Differential role of the menthol-binding residue Y745 in the antagonism of thermally gated TRPM8 channels. Mol. Pain 2009, 5:62.
20. McKemy D.D. How cold is it? TRPM8 and TRPA1 in the molecular logic of cold sensation. Mol. Pain 2005, 1:16.
21. McKemy D.D., Neuhausser W.M., Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 2002, 416:52-58.
22. Mergler S., Cheng Y., Skosyrsky S., Garreis F., Pietrzak P., Kociok N., Dwarakanath A., Reinach P.S., Kakkassery V. Altered calcium regulation by thermo-sensitive transient receptor potential channels in etoposide-resistant WERI-Rb1 retinoblastoma cells. Exp. Eye Res. 2012, 94:157-173.
23. Mergler S., Dannowski H., Bednarz J., Engelmann K., Hartmann C., Pleyer U. Calcium influx induced by activation of receptor tyrosine kinases in SV40-transfected human corneal endothelial cells. Exp. Eye Res. 2003, 77:485-495.
24. 2+ influx by inhibiting L-type channel activity in cultured human corneal endothelial cells. Exp. Eye Res. 2005, 80:285-293.
25. Mergler S., Skrzypski M., Sassek M., Pietrzak P., Pucci C., Wiedenmann B., Strowski M.Z. Thermo-sensitive transient receptor potential vanilloid channel-1 regulates intracellular calcium and triggers chromogranin A secretion in pancreatic neuroendocrine BON-1 tumor cells. Cell Signal 2012, 24:233-246.
26. Mergler S., Strowski M.Z., Kaiser S., Plath T., Giesecke Y., Neumann M., Hosokawa H., Kobayashi S., Langrehr J., Neuhaus P., Plockinger U., Wiedenmann B., Grotzinger C. Transient receptor potential channel TRPM8 agonists stimulate calcium influx and neurotensin secretion in neuroendocrine tumor cells. Neuroendocrinology 2007, 85:81-92.
27. Mergler S., Valtink M., Coulson-Thomas V.J., Lindemann D., Reinach P.S., Engelmann K., Pleyer U. TRPV channels mediate temperature-sensing in human corneal endothelial cells. Exp. Eye Res. 2010, 90:758-770.
28. Milligan C.J., Li J., Sukumar P., Majeed Y., Dallas M.L., English A., Emery P., Porter K.E., Smith A.M., McFadzean I., Beccano-Kelly D., Bahnasi Y., Cheong A., Naylor J., Zeng F., Liu X., Gamper N., Jiang L.H., Pearson H.A., Peers C., Robertson B., Beech D.J. Robotic multiwell planar patch-clamp for native and primary mammalian cells. Nat. Protoc. 2009, 4:244-255.
29. Pan Z., Yang H., Reinach P.S. Transient receptor potential (TRP) gene superfamily encoding cation channels. Hum. Genom. 2011, 5:108-116.
30. Parra A., Madrid R., Echevarria D., del O.S., Morenilla-Palao C., Acosta M.C., Gallar J., Dhaka A., Viana F., Belmonte C. Ocular surface wetness is regulated by TRPM8-dependent cold thermoreceptors of the cornea. Nat. Med. 2010, 16:1396-1399.
31. Peier A.M., Moqrich A., Hergarden A.C., Reeve A.J., Andersson D.A., Story G.M., Earley T.J., Dragoni I., McIntyre P., Bevan S., Patapoutian A. ATRP channel that senses cold stimuli and menthol. Cell 2002, 108:705-715.
32. Peier A.M., Reeve A.J., Andersson D.A., Moqrich A., Earley T.J., Hergarden A.C., Story G.M., Colley S., Hogenesch J.B., McIntyre P., Bevan S., Patapoutian A. Aheat-sensitive TRP channel expressed in keratinocytes. Science 2002, 296:2046-2049.
33. Rawls S.M., Gomez T., Ding Z., Raffa R.B. Differential behavioral effect of the TRPM8/TRPA1 channel agonist icilin (AG-3-5). Eur. J. Pharmacol. 2007, 575:103-104.
34. Sandboe F.D., Medin W., Froslie K.F. Influence of temperature on corneas stored in culture medium. A comparative study using functional and morphological methods. Acta Ophthalmol. Scand 2003, 81:54-59.
35. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., Earley T.J., Hergarden A.C., Andersson D.A., Hwang S.W., McIntyre P., Jegla T., Bevan S., Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 2003, 112:819-829.
36. Tominaga M., Caterina M.J. Thermosensation and pain. J.Neurobiol. 2004, 61:3-12.
37. Valero M., Morenilla-Palao C., Belmonte C., Viana F. Pharmacological and functional properties of TRPM8 channels in prostate tumor cells. Pflugers Arch. 2011, 461:99-114.
38. Valtink M., Gruschwitz R., Funk R.H., Engelmann K. Two clonal cell lines of immortalized human corneal endothelial cells show either differentiated or precursor cell characteristics. Cells Tissues. Organs 2008, 187:286-294.
39. Voets T., Droogmans G., Wissenbach U., Janssens A., Flockerzi V., Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 2004, 430:748-754.
40. Voets T., Owsianik G., Nilius B. TRPM8. Handb. Exp. Pharmacol. 2007, 329-344.
41. Vriens J., Appendino G., Nilius B. Pharmacology of vanilloid transient receptor potential cation channels. Mol. Pharmacol. 2009, 75:1262-1279.
42. Weil A., Moore S.E., Waite N.J., Randall A., Gunthorpe M.J. Conservation of functional and pharmacological properties in the distantly related temperature sensors TRVP1 and TRPM8. Mol. Pharmacol. 2005, 68:518-527.
43. Xing H., Chen M., Ling J., Tan W., Gu J.G. TRPM8 mechanism of cold allodynia after chronic nerve injury. J.Neurosci. 2007, 27:13680-13690.
44. 2+ channel required for the survival of prostate cancer cells. Cancer Res. 2004, 64:8365-8373.