Signal transduction via TRPM3 channels in pancreatic β-cells

Journal of Molecular Endocrinology

Volumn 50, Issue 3, 2013, Pages

  Thiel, Gerald ^a   Müller, Isabelle ^a   Rössler, Oliver G ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Calcium signaling; Gene regulation; Pancreatic cell; Signal transduction; Steroids

Indexed keywords

4 AMINOBUTYRIC ACID; CALCIUM CHANNEL L TYPE; CALMODULIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOCHROME P450; GLUCOSE; HYDROXYSTEROID SULFOTRANSFERASE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID; NIFEDIPINE; PHOSPHOPROTEIN PHOSPHATASE; POTASSIUM CHANNEL; PREGNENOLONE SULFATE; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE; RAF PROTEIN; STEROID HORMONE; STEROID RECEPTOR; TRANSCRIPTION FACTOR PDX 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M3;

ALTERNATIVE RNA SPLICING; BINDING SITE; BIOSYNTHESIS; CONCENTRATION (PARAMETERS); CYTOSOL; DEPHOSPHORYLATION; EXOCYTOSIS; GENE EXPRESSION; HUMAN; INSULIN RELEASE; INTRACELLULAR SIGNALING; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; HUMANS; INSULIN-SECRETING CELLS; SIGNAL TRANSDUCTION; TRPM CATION CHANNELS;

EID: 84876719582     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-12-0237     Document Type: Review

References (59)

1. Andrali SS, Sampley ML, Vanderford NL & Özcan S 2008 Glucose regulation of insulin gene expression in pancreatic β-cells. Biochemical Journal 415 1-10. (doi:10.1042/BJ20081029)
2. Arnette D, Gibson TB, Lawrence MC, January B, Khoo S, McGlynn K, Vanderbilt CA & Cobb MH 2003 Regulation of ERK1 and ERK2 by glucose and peptide hormones in pancreatic b cells. Journal of Biological Chemistry 278 32517-32525. (doi:10.1074/jbc.M301174200)
3. Benes C, Roisin MP, Van Tan H, Creuzet C, Miyazaki J-i. & Fagard R 1998 Rapid activation and nuclear translocation of mitogen-activated protein kinases in response to physiological concentration of glucose in the MIN6 pancreatic b cell line. Journal of Biological Chemistry 273 15507-15513. (doi:10.1074/jbc.273.25.15507)
4. Benes C, Poitout V, Marie J-C, Martin-Perez J, Roisin M-P & Fagard R 1999 Mode of regulation of the extracellular signal-regulated kinases in the pancreatic β-cell line MIN6 and their implication in the regulation of insulin gene transcription. Biochemical Journal 340 219-225. (doi:10.1042/0264-6021:3400219)
5. Bernal-Mizrachi E, Wice B, Inoue H & Permutt MA 2000 Activation of serum response factor in the depolarization induction of Egr-1 transcription in pancreatic islet β-cells. Journal of Biological Chemistry 275 25681-25689. (doi:10.1074/jbc.M003424200)
6. Bernal-Mizrachi E, Wen W, Srinivasan S, Klenk A, Cohen D & Permutt MA 2001 Activation of Elk-1, an Ets transcription factor, by glucose and EGF treatment of insulinoma cells. American Journal of Physiology. Endocrinology and Metabolism 281 E1286-E1299.
7. Brissova M, Shiota M, Nicholson WE, Gannon M, Knobel SM, Piston DW, Wright CVE & Powers AC 2002 Reduction in pancreatic transcription factor PDX-1 impairs glucose-stimulated insulin secretion. Journal of Biological Chemistry 277 11225-11232. (doi:10.1074/jbc.M111272200)
8. Brixel LR, Monteilh-Zoller MK, Ingenbrandt CS, Fleig A, Penner R, Enklaar T, Zabel BU & Prawitt D 2010 TRPM5 regulates glucose-stimulated insulin secretion. Pflügers Archive: European Journal of Physiology 460 69-76. (doi:10.1007/s00424-010-0835-z)
9. Cao DS, Zhong L, Hsieh TH, Abooj M, Bishnoi M, Hughes L & Premkumar LS 2012 Expression of transient receptor potential anlyrin 1 (TRPA1) and its role in insulin release from rat pancreatic b cells. PLoS ONE 7 e38005. (doi:10.1371/journal.pone.0038005)
10. Chen L & Sokabe M 2005 Presynaptic modulation of synaptic transmission by pregnenolone sulfate as studied by opical recordings. Journal of Neurophysiology 94 4131-4144. (doi:10.1152/jn.00755.2004)
11. Chen L, Cai W, Chen L, Zhou R, Furuya K & Sokabe M 2010 Modulatory metaplasticity induced by pregnenolone sulfate in the rat hippocampus: a leftward shift in LTP/LTD-frequency curve. Hippocampus 20 499-512. (doi:10.1002/hipo.20718)
12. Ciurtin C, Majeed Y, Naylor J, Sukumar P, English AA, Emery P & Beech DJ 2010 TRPM3 channel stimulated by pregnenolone sulphate in synovial fibroblasts and negatively coupled to hyaluronan. BMC Musculoskeletal Disorders 11 111. (doi:10.1186/1471-2474-11-111)
13. 2+ oscillations in pancreatic islets correlates with impaired glucose tolerance in Trpm5K/K mice. PNAS 107 5208-5213. (doi:10.1073/pnas.0913107107)
14. Colsoul B, Vennekens R & Nilius B 2011 Transient receptor potential cation channels in pancreatic b cells. Review of Physiological and Biochemical Pharmacology 161 87-110. (doi:10.1007/112_2011_2)
15. Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M & Rosner MR 2003 Activation of Raf-1 signaling by protein kinase C through amechanism involving Raf kinase inhibitory protein. Journal of Biological Chemistry 278 13061-13068. (doi:10.1074/jbc.M210015200)
16. Duan L & Cobb MH 2010 Calcineurin increases glucose activation of ERK1/2 by reversing negative feedback. PNAS 107 22314-22319. (doi:10.1073/pnas.1016630108)
17. Eto K, Kaur V & Thomas MK 2006 Regulation of insulin gene transcription by the immediate early response gene Egr-1. Endocrinology 147 2923-2935. (doi:10.1210/en.2005-1336)
18. Eto K, Kaur V & Thomas MK 2007 Regulation of pancreatic duodenum homeobox-1 expression by early growth response-1. Journal of Biological Chemistry 282 5973-5983. (doi:10.1074/jbc.M607288200)
19. Frödin M, Sekine N, Roche E, Filloux C, Prentki M, Wollheim CB & Van Obberghen EV 1995 Glucose, other secretagogues, and nerve growth factor stimulate mitogen-activated protein kinase in the insulin-secreting b cell line, INS-1. Journal of Biological Chemistry 270 7882-7889. (doi:10.1074/jbc.270.14.7882)
20. Frühwald J, Camacho Londono J, Dembla S, Mannebach S, Lis A, Drews A, Wissenbach U, Oberwinkler J & Philipp SE 2012 Alternative splicing of a protein domain indispensable for function of transient receptor potential melastatin 3 (TRPM3) ion channels. Journal of Biological Chemistry 287 36663-36672. (doi:10.1074/jbc.M112.396663)
21. Glauser DA & Schlegel W 2007 Sequential actions of ERK1/2 on the AP-1 transcription factor allow temporal integration of metabolic signals in pancreatic b cells. FASEB Journal 21 3240-3249. (doi:10.1096/fj.06-7798com)
22. Glauser DA, Brun T, Gauthier BR & Schlegel W 2006 Transcriptional response of pancreatic b cells to metabolic stimulation: large scale identification of immediate-early and secondary response genes. BMC Molecular Biology 8 54. (doi:10.1186/1471-2199-8-54)
23. Grimm C, Kraft R, Sauerbruch S, Schulz G & Harteneck C 2003 Molecular and functional characterization of the melastatin-related cation channel TRPM3. Journal of Biological Chemistry 278 21493-21501. (doi:10.1074/jbc.M300945200)
24. Grimm C, Kraft R, Schultz G & Harteneck C 2005 Activation of the melastatin-related cation channel TRPM3 by D-erythro-sphingosine. Molecular Pharmacology 67 798-805. (doi:10.1124/mol.104.006734)
25. Halokovska B, Grycova L, Jirku M, Sulc M, Bumba L & Teisinger J 2012 Calmodulin and S100A1 protein interact with N terminus of TRPM3 channel. Journal of Biological Chemistry 287 16645-16655. (doi:10.1074/jbc.M112.350686)
26. Hara Y, Wakamori M, Ishii M, Maeno E, Nishida M, Yoshida T, Yamada H, Shimizu S, Mori E, Kudoh J et al. 2002 LTRPC2 Ca2C-permeable channel activated by changes in redox status confer susceptibility to cell death. Molecular Cell 9 163-173. (doi:10.1016/S1097-2765(01)00438-5)
27. Hige T, Fujiyoshi Y & Takahashi T 2006 Neurosteroid pregnenolone sulfate enhances glutamatergic synaptic transmission by facilitating presynaptic calcium currents at the calyx of Held of immature rats. European Journal of Neuroscience 24 1955-1966. (doi:10.1111/j.1460-9568.2006.05080.x)
28. Horak M, Vlcek K, Petrovic M, Chodounska H & Vyklicky L Jr 2004 Molecular mechanism of pregnenolone sulfate action at NR1/NR2B receptors. Journal of Neuroscience 24 10318-10325. (doi:10.1523/JNEUROSCI.2099-04.2004)
29. Islam MS 2011 TRP channels of islets. In: transient receptor potential channels. Advances in Experimental Medicine and Biology 704 811-830. (doi:10.1007/978-94-007-0265-3_42)
30. Jang MK, Mierke DF, Russek SJ & Farb DH 2004 A steroid modulatory domain on NR2B controls N-methyl-D-aspartate receptor proton sensitivity. PNAS 101 8198-8203. (doi:10.1073/pnas.0401838101)
31. Josefsen K, Sorensen LR, Buschard K & Birkenbach M 1999 Glucose induces early growth response gene (Egr-1) expression in pancreatic b cells. Diabetologia 42 195-203. (doi:10.1007/s001250051139)
32. Klose C, Straub I, Riehle M, Ranta F, Krautwurst D, Ullrich S, Mayerhof W & Harteneck C 2011 Fenamates as TRP channel blocker: mefenamic acid selectively blocks TRMP3. British Journal of Pharmacology 162 1757-1769. (doi:10.1111/j.1476-5381.2010.01186.x)
33. Kobayashi T, Washiyama K & Ikeda K 2009 Pregnenolone sulfate potentiates the inwardly rectifying K channel Kir2.3. PLoS ONE 4 e6311. (doi:10.1371/journal.pone.0006311)
34. Kolch W, Heidecker G, Kochs G, Hummel R, Vahidi H, Mischak H, Finkenzeller G, Marmé D & Rapp UR 1993 Protein kinase C a activates RAF-1 by direct phosphorylation. Nature 364 249-252. (doi:10.1038/364249a0)
35. Kostakis E, Jang MK, Russek SJ, Gibbs TT & Farb DH 2011 A steroid modulatory domain in NR2A collaborates with NR1 exon-5 to control NMDAR moduation by pregnenolone sulfate and protons. Journal of Neurochemistry 119 486-496. (doi:10.1111/j.1471-4159.2011. 07442.x)
36. Lee N, Chen J, Sun L, Wu S, Gray KR, Rich A, Huang M, Lin J-H, Feder JN, Janovitz EB et al. 2003 Expression and characterization of human transient receptor potential melastatin 3 (hTRPM3). Journal of Biological Chemistry 278 20890-20897. (doi:10.1074/jbc.M211232200)
37. Majeed Y, Agarwal AK, Naylor J, Seymour VAL, Jiang S, Muraki K, Fishwick CWG & Beech DJ 2010 Cis-isomerism and other chemical requirements of steroid agonists and partial agonists acting at TRPM3 channels. British Journal of Pharmacology 161 430-441. (doi:10.1111/j.1476-5381.2010.00892.x)
38. Majeed Y, Bahnasi Y, Seymour VAL, Wilson LA, Milligan CJ, Agarwal AK, Sukumar P, Naylor J & Beech DJ 2011 Rapid and contrasting effects of rosiglitazone on transient receptor potential TRPM3 and TRPM5 channels. Molecular Pharmacology 79 1023-1030. (doi:10.1124/mol.110.069922)
39. Majeed Y, Tumova S, Green BL, Seymour VAL, Woods DM, Agarwal AK, Naylor J, Jiang S, Picton HM, Porter KE et al. 2012 Pregnenolone sulphate-independent inhibition of TRM3 channels by progesterone. Cell Calcium 51 1-11. (doi:10.1016/j.ceca.2011.09.005)
40. Mayer SI & Thiel G 2009 Calcium influx into MIN6 insulinoma cells induces expression of Egr-1 involving extracellular signal-regulated protein kinase and the transcription factors Elk-1 and CREB. European Journal of Cell Biology 88 19-33. (doi:10.1016/j.ejcb.2008.07.002)
41. Mayer SI, Müller I, Mannebach S, Endo T & Thiel G 2011 Signal transduction of pregnenolone sulfate in insulinoma cells. Activation of Egr-1 expression involving TRPM3, voltage-gated calcium channels, ERK, and ternary complex factors. Journal of Biological Chemistry 286 10084-10096. (doi:10.1074/jbc.M110.202697)
42. Müller I, Endo T & Thiel G 2010 Regulation of AP-1 activity in glucose-stimulated insulinoma cells. Journal of Cellular Biochemistry 110 1481-1494. (doi:10.1002/jcb.22715)
43. 2 channels and transient receptor potential melastatin 3 channels. Molecular Pharmacology 80 1179-1189. (doi:10.1124/ mol.111.074781)
44. 2 signaling and gene transcription in glucose-stimulated insulinoma cells. Cell Calcium 52 137-151. (doi:10.1016/j.ceca.2012.05.003)
45. Müller I, Rössler OG, Wittig C, Menger MD & Thiel G 2012b Critical role of Egr transcription factors in regulating insulin biosynthesis, blood glucose homeostasis and islet size. Endocrinology 153 3040-3053. (doi:10.1210/en.2012-1064)
46. Nakajima-Nagata N, Sugai M, Sakurai T, Miyazaki J-i, Tabata Y & Shimizu A 2004 Pdx-1 enables insulin secretion by regulating synaptotagmin 1 gene expression. Biochemical and Biophysical Research Communications 318 631-635. (doi:10.1016/j.bbrc.2004.04.071)
47. Naylor J, Li J, Milligan CJ, Zeng F, Sukumar P, Hou B, Sedo A, Yuldasheva N, Majeed Y, Beri D et al. 2010 Pregnenolone sulphate- and cholesterolregulated channels coupled to vascular smooth muscle secretion and contraction. Circulation Research 106 1507-1515. (doi:10.1161/CIRCRESAHA.110.219329)
48. Oberwinkler J, Lis A, Giehl KM, Flockerzi V & Philipp SE 2005 Alternative splicing switches the divalent cation selectivity of TRPM3 channels. Journal of Biological Chemistry 280 22899-22906. (doi:10.1074/jbc.M503092200)
49. Shimizu C, Fulda H, Yanai H & Strott CA 2003 Conservation of the hydroxysteroid sulfotransferase SULT2B1 gene structure in the mouse: pre- and postnatal expression, kinetic analysis of isoforms, and comparison with prototypical SULT2A1. Endocrinology 144 1186-1193. (doi:10.1210/en.2002-221011)
50. Straub I, Mohr F, Konrad M, Philipp SE, Oberwinkler J & Schaefer M 2013 Citrus fruit and fabacea secondary metabolites potently and selectively block TRPM3. British Journal of Pharmacology 168 1835-1850. (doi:10.1111/bph.12076)
51. Thiel G, Mayer SI, Müller I, Stefano L & Rössler OG 2010 Egr-1 - a Ca2C-regulated transcription factor. Cell Calcium 47 397-403. (doi:10.1016/j.ceca.2010.02.005)
52. 2 sensor protein of stimulus-secretion coupling in pancreatic b cells. Biochemistry 46 14461-14467. (doi:10.1021/bi7016816)
53. Uchida K, Dezaki K, Damdindorj B, Inada H, Shiuchi T, Mori T, Yada T, Minokoshi Y & Tominaga M 2011 Lack of TRPM2 impaired insulin secretion and glucose metabolisms in mice. Diabetes 60 119-126. (doi:10.2337/db10-0276)
54. Vriens J, Owsianik G, Hofmann T, Philipp SE, Stab J, Chen X, Benoit M, Xue F, Janssens A, Kerselaers S et al. 2011 TRPM3 is a nociceptor channel involved in the detection of noxious heat. Neuron 70 482-494. (doi:10.1016/j.neuron.2011.02.051)
55. Wagner TFJ, Loch S, Lambert S, Straub I, Mannebach S, Mathar I, Düfer M, Lis A, Flockerzi V, Philipp SE et al. 2008 Transient receptor potential M3 channels are ionotropic steroid receptors in pancreatic b cells. Nature Cell Biology 10 1421-1430. (doi:10.1038/ncb1801)
56. Wang M 2011 Neurosteroids and GABA-A receptor function. Frontiers in Neuroendocrine Science 2 44. (doi:10.1111/bph.12076)
57. Wang Q, Cai K, Pang S, Wang T, Qi D, Zhu Q, Ni Z & Le Y 2008 Mechanisms of glucose-induced expression of pancreatic-derived factor in pancreatic β-cells. Endocrinology 149 672-680. (doi:10.1210/en.2007-0106)
58. Yang M, Chisholm JW, Soelaiman S & Shryock JC 2010 Sulfonylureas uncouple glucose-dependence for GPR40-mediated enhancement of insulin secretion from INS-1E cells. Molecular and Cellular Endocrinology 315 308-313. (doi:10.1016/j.mce.2009.09.033)
59. Zheng P 2009 Neuroactive steroid regulation of neurotransmitter release in the CNS: action, mechanism and possible significance. Progress in Neurobiology 89 134-152. (doi:10.1016/j.pneurobio.2009.07.001)