Na+ current properties in islet α- and β-cells reflect cell-specific Scn3a and Scn9a expression

Journal of Physiology

Volumn 592, Issue 21, 2014, Pages 4677-4696

  Zhang, Quan ^a   Chibalina, Margarita V ^a   Bengtsson, Martin ^a   Groschner, Lukas N ^a   Ramracheya, Reshma ^a   Rorsman, Nils J G ^a   Leiss, Veronika ^b,c   Nassar, Mohammed A ^d,e   Welling, Andrea ^b   Gribble, Fiona M ^f   Reimann, Frank ^f   Hofmann, Franz ^b   Wood, John N ^d   Ashcroft, Frances M ^a   Rorsman, Patrik ^a,g  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCAGON; INSULIN; SODIUM CHANNEL NAV1.3; SODIUM CHANNEL NAV1.7; SODIUM ION; GLUCOSE; ISOPROTEIN; NEUROTOXIN; PROTEIN SUBUNIT; SODIUM;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELL FUNCTION; CELL MEMBRANE POTENTIAL; CELL SPECIFICITY; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GLUCAGON RELEASE; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCN3A GENE; SCN9A GENE; SODIUM CURRENT; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PROTEIN SUBUNIT; SECRETION (PROCESS);

ANIMALS; GENE EXPRESSION REGULATION; GLUCAGON-SECRETING CELLS; GLUCOSE; HEK293 CELLS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NAV1.3 VOLTAGE-GATED SODIUM CHANNEL; NAV1.7 VOLTAGE-GATED SODIUM CHANNEL; NEUROTOXINS; PROTEIN ISOFORMS; PROTEIN SUBUNITS; SODIUM;

EID: 84924815340     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.274209     Document Type: Article

References (49)

1. Ashcroft F & Rorsman P (2004). Type 2 diabetes mellitus: not quite exciting enough? Hum Mol Genet 13(Spec No 1), R21-31.
2. Ashcroft FM & Rorsman P (2012). Diabetes mellitus and the β cell: the last ten years. Cell 148, 1160-1171.
3. Ashcroft FM & Rorsman P (2013). K-ATP channels and islet hormone secretion: new insights and controversies. Nat Rev Endocrinol 9, 660-669.
4. Bengtsson M, Stahlberg A, Rorsman P & Kubista M (2005). Gene expression profiling in single cells from the pancreatic islets of Langerhans reveals lognormal distribution of mRNA levels. Genome Res 15, 1388-1392.
5. Braun M, Ramracheya R, Amisten S, Bengtsson M, Moritoh Y, Zhang Q, Johnson PR & Rorsman P (2009). Somatostatin release, electrical activity, membrane currents and exocytosis in human pancreatic delta cells. Diabetologia 52, 1566-1578.
6. Braun M, Ramracheya R, Bengtsson M, Clark A,Walker JN, Johnson PR & Rorsman P (2010). Gamma-aminobutyric acid (GABA) is an autocrine excitatory transmitter in human pancreatic beta-cells. Diabetes 59, 1694-1701.
7. Braun M, Ramracheya R, Bengtsson M, Zhang Q, Karanauskaite J, Partridge C, Johnson PR & Rorsman P (2008). Voltage-gated ion channels in human pancreatic β-cells: electrophysiological characterization and role in insulin secretion. Diabetes 57, 1618-1628.
8. Catterall WA (2000). From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26, 13-25.
9. Catterall WA, Goldin AL &Waxman SG (2005). International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57, 397-409.
10. Chera S, Baronnier D, Cigliola V, Jensen JN, Gu G, Ghila L, Furuyama K, Thorel F, Gribble F, Reimann F & Herrera PL (2014). Diabetes recovery by age-dependent conversion of pancreatic δ-cells into insulin producers. Nature doi:10.1038/nature13633.
11. Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, Springell K, Karbani G, Jafri H, Mannan J, Raashid Y, Al-Gazali L, Hamamy H, Valente EM, Gorman S, Williams R, McHale DP,Wood JN, Gribble FM &Woods CG (2006). An SCN9A channelopathy causes congenital inability to experience pain. Nature 444, 894-898.
12. De Marinis YZ, Salehi A,Ward CE, Zhang Q, Abdulkader F, Bengtsson M, Braha O, Braun M, Ramracheya R, Amisten S, Habib AM, Moritoh Y, Zhang E, Reimann F, Rosengren AH, Shibasaki T, Gribble F, Renstrom E, Seino S, Eliasson L & Rorsman P (2010). GLP-1 inhibits and adrenaline stimulates glucagon release by differential modulation of N- and L-type Ca2+ channel-dependent exocytosis. CellMetab 11, 543-553.
13. v1.7-related pain syndromes. Adv Genet 63, 85-110.
14. Dunning BE, Foley JE & Ahren B (2005). Alpha cell function in health and disease: influence of glucagon-like peptide-1. Diabetologia 48, 1700-1713.
15. Ernst SJ, Aguilar-Bryan L & Noebels JL (2009). Sodium channel β1 regulatory subunit deficiency reduces pancreatic islet glucose-stimulated insulin and glucagon secretion. Endocrinology 150, 1132-1139.
16. Goldin AL, Barchi RL, Caldwell JH, Hofmann F, Howe JR, Hunter JC, Kallen RG, Mandel G, Meisler MH, Netter YB, Noda M, Tamkun MM, Waxman SG,Wood JN & Catterall WA (2000). Nomenclature of voltage-gated sodium channels. Neuron 28, 365-368.
17. Girard CA,Wunderlich FT, Shimomura K, Collins S, Kaizik S, Proks P, Abdulkader F, Clark A, Ball V, Zubcevic L, Bentley L, Clark R, Church C, Hugill A, Galvanovskis J, Cox R, Rorsman P, Bruning JC & Ashcroft FM. (2009). Expression of an activating mutation in the gene encoding the KATP channel subunit Kir6.2 in mouse pancreatic beta cells recapitulates neonatal diabetes. J Clin Invest 119, 80-90 doi:10.1172/JCI35772.
18. Gonoi T & Hille B (1987). Gating of Na channels - inactivation modifiers discriminate among models. J Gen Physiol 89, 253-274.
19. Gopel S, Kanno T, Barg S, Galvanovskis J & Rorsman P (1999). Voltage-gated and resting membrane currents recorded from β-cells in intact mouse pancreatic islets. J Physiol 521, 717-728.
20. Gopel S, Zhang Q, Eliasson L, Ma XS, Galvanovskis J, Kanno T, Salehi A & Rorsman P (2004). Capacitance measurements of exocytosis in mouse pancreatic α-, β- and δ-cells within intact islets of Langerhans. J Physiol 556, 711-726.
21. Gopel SO, Kanno T, Barg S & Rorsman P (2000a). Patch-clamp characterisation of somatostatin-secreting δ-cells in intact mouse pancreatic islets. J Physiol 528, 497-507.
22. + channels. J Physiol 528, 509-520.
23. Hauge-Evans AC, King AJ, Carmignac D, Richardson CC, Robinson IC, Low MJ, Christie MR, Persaud SJ & Jones PM (2009). Somatostatin secreted by islet δ-cells fulfills multiple roles as a paracrine regulator of islet function. Diabetes 58, 403-411.
24. Henquin JC & Meissner HP (1984). Significance of ionic fluxes and changes in membrane potential for stimulus-secretion coupling in pancreatic B-cells. Experientia 40, 1043-1052.
25. Herrera PL (2000). Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127, 2317-2322.
26. v1.7 sodium channels in mouse spinal sensory neurons. J Physiol 551, 741-750.
27. Hille B (2001). Ion Channels of Excitable Membranes. Sinauer Associates, Sunderland, MA.
28. ATP-channel modulation. J Physiol 545, 501-507.
29. Koopmann TT, Bezzina CR &Wilde AA (2006). Voltage-gated sodium channels: action players with many faces. Ann Med 38, 472-482.
30. + channel inactivation: a comparative study between pancreatic islet β-cells and adrenal chromaffin cells in rat. J Physiol 548, 191-202.
31. ATP channel-dependent pathway within α cells regulates glucagon release from both rodent and human islets of Langerhans. PLoS Biol 5, e143.
32. Misler S, Barnett DW, Gillis KD & Pressel DM (1992). Electrophysiology of stimulus-secretion coupling in human β-cells. Diabetes 41, 1221-1228.
33. v1.3 null mutant mice. Mol Pain 2, 33.
34. Nica AC, Ongen H, Irminger JC, Bosco D, Berney T, Antonarakis SE, Halban PA & Dermitzakis ET (2013). Cell-type, allelic, and genetic signatures in the human pancreatic beta cell transcriptome. Genome Res 23, 1554-1562.
35. v1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci U S A 101, 12706-12711 doi:10.1073/pnas.0404915101.
36. + currents in cultured mouse pancreatic B-cells. Pflugers Arch 411, 429-435.
37. Postic C, Shiota M, Niswender KD, Jetton TL, Chen Y, Moates JM, Shelton KD, Lindner J, Cherrington AD & Magnuson MA (1999). Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic β cell-specific gene knock-outs using Cre recombinase. J Biol Chem 274, 305-315.
38. Pressel DM & Misler S (1990). Sodium channels contribute to action potential generation in canine and human pancreatic islet B cells. J Membr Biol 116, 273-280.
39. Raj A, Peskin CS, Tranchina D, Vargas DY & Tyagi S (2006). Stochastic mRNA synthesis in mammalian cells. PLoS Biol 4, e309.
40. Ramracheya R,Ward C, Shigeto M, Walker JN, Amisten S, Zhang Q, Johnson PR, Rorsman P & Braun M (2010). Membrane potential-dependent inactivation of voltage-gated ion channels in α-cells inhibits glucagon secretion from human islets. Diabetes 59, 2198-2208.
41. Renstrom E, DingWG, Bokvist K & Rorsman P (1996). Neurotransmitter-induced inhibition of exocytosis in insulin-secreting β cells by activation of calcineurin. Neuron 17, 513-522.
42. Rocheleau JV, Remedi MS, Granada B, HeadWS, Koster JC, Nichols CG & Piston DW (2006). Critical role of gap junction coupled KATP channel activity for regulated insulin secretion. PLoS Biol 4, e26.
43. Rorsman P, Eliasson L, Kanno T, Zhang Q & Gopel S (2011). Electrophysiology of pancreatic beta-cells in intact mouse islets of Langerhans. Progr Biophys Mol Biol 107, 224-235.
44. Stahlberg A & Bengtsson M (2010). Single-cell gene expression profiling using reverse transcription quantitative real-time PCR. Methods 50, 282-288.
45. Strowski MZ, Kohler M, Chen HY, Trumbauer ME, Li Z, Szalkowski D, Gopal-Truter S, Fisher JK, Schaeffer JM, Blake AD, Zhang BB &Wilkinson HA (2003). Somatostatin receptor subtype 5 regulates insulin secretion and glucose homeostasis. Mol Endocrinol 17, 93-106.
46. Vignali S, Leiss V, Karl R, Hofmann F &Welling A (2006). Characterization of voltage-dependent sodium and calcium channels in mouse pancreatic A- and B-cells. J Physiol 572, 691-706.
47. Zhang Q, Bengtsson M, Partridge C, Salehi A, Braun M, Cox R, Eliasson L, Johnson PR, Renstrom E, Schneider T, Berggren PO, Gopel S, Ashcroft FM & Rorsman P. (2007). R-type Ca(2+)-channel-evoked CICR regulates glucose-induced somatostatin secretion. Nat Cell Biol 9, 453-460 doi:10.1038/ncb1563.
48. Zhang Q, Galvanovskis J, Abdulkader F, Partridge CJ, Gopel SO, Eliasson L & Rorsman P (2008). Cell coupling in mouse pancreatic β-cells measured in intact islets of Langerhans. Phil Trans R Soc A 366, 3503-3523.
49. ATP channels in glucose-regulated glucagon secretion and impaired counterregulation in type 2 diabetes. Cell Metab 18, 871-882.