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Anionic Transporters and Channels in Pancreatic Islet Cells

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Abstract

After a brief description of the so-called consensus hypothesis for the mechanism of stimulus-secretion coupling in the process of glucose-induced insulin release, the present chapter, which deals with anionic transporters and channels in pancreatic islet cells, concerns mainly a second modality for the control of insulin secretion by the hexose. In such a perspective, it draws attention to the NBCe1 Na+/HCO3 − cotransporters, the volume-regulated anion channel hypothesis, the experimental model of extracellular hypotonicity, the possible role of NAD(P)H oxidase-derived H2O2 in the activation of volume-regulated anion channels in β-cells exposed to a hypotonic medium, the identity of the anions concerned by the volume-regulated anion channel hypothesis, the expression and function of anoctamin 1 in rodent and human pancreatic islet cells, the possible role of bicarbonate-activated soluble adenylyl cyclase, the identity and role of aquaporins in insulin-producing cells, and a proposed role for volume-regulated anion channels in glucagon secretion.

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References

  • Agre P (2004) Aquaporin water channels. Angew Chem Int Ed Engl 43:4278–4290

    Article  PubMed  CAS  Google Scholar 

  • Almaca J, Tian Y, Aldehni F, Ousingsawat J, Kongsuphol P, Rock JR, Harfe BD, Schreiber R, Kunzelmann K (2009) TMEM16A proteins produce volume regulated chloride currents that are reduced in mice lacking TMEM16A. J Biol Chem 284:28571–28578

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Beauwens R, Best L, Markadieu N, Crutzen R, Louchami K, Brown P, Yates AP, Malaisse WJ, Sener A (2006) Stimulus-secretion coupling of hypotonicity-induced insulin release in BRIN-BD11 cells. Endocrine 30:353–363

    Article  PubMed  CAS  Google Scholar 

  • Best L (1997) Glucose and a-ketoisocaproate induce transient inward currents in rat pancreatic β cells. Diabetologia 40:1–6

    Article  PubMed  CAS  Google Scholar 

  • Best L (1999) Cell-attached recordings of the volume-sensitive anion channel in rat pancreatic B cells. Biochim Biophys Acta 1419:248–256

    Article  PubMed  CAS  Google Scholar 

  • Best L (2000) Glucose-sensitive conductances in rat pancreatic β-cells: contribution to electrical activity. Biochim Biophys Acta 1468:311–319

    Article  PubMed  CAS  Google Scholar 

  • Best L (2002) Study of a glucose-activated anion-selective channel in rat pancreatic β-cells. Pflugers Arch 445:97–104

    Article  PubMed  CAS  Google Scholar 

  • Best L (2005) Glucose-induced electrical activity in rat pancreatic β-cells: dependence in intracellular chloride concentration. J Physiol (Lond) 568:137–144

    Article  CAS  Google Scholar 

  • Best L, Trebilcock R, Tomlinson S (1992) Lactate transport in insulin-secreting β-cells: contrast between rat islets and HIT-T15 insulinoma cells. Mol Cell Endocrinol 86:49–56

    Article  PubMed  CAS  Google Scholar 

  • Best L, Sheader EA, Brown PD (1996) A volume-activated anion conductance in insulin-secreting cells. Pflugers Arch 431:363–370

    Article  PubMed  CAS  Google Scholar 

  • Best L, Brown PD, Tomlinson S (1997) Anion fluxes, volume regulation and electrical activity in the mammalian β cell. Exp Physiol 82:957–966

    PubMed  CAS  Google Scholar 

  • Best L, Miley HE, Brown PD, Cook LJ (1999) Methylglyoxal causes swelling and activation of a volume-sensitive anion conductance in rat pancreatic β-cells. Membr Biol 167:65–71

    Article  CAS  Google Scholar 

  • Best L, Speake T, Brown PD (2001) Characterization of the volume-sensitive anion channel in rat pancreatic β-cells. Exp Physiol 86:145–150

    Article  PubMed  CAS  Google Scholar 

  • Best L, Brown PD, Yates AP, Perret J, Virreira M, Beauwens R, Malaisse WJ, Sener A, Delporte C (2009) Contrasting effects of glycerol and urea transport on rat pancreatic β-cell function. Cell Physiol Biochem 23:255–264

    Article  PubMed  CAS  Google Scholar 

  • Best L, Brown PD, Sener A, Malaisse WJ (2010a) Opposing effects of tenidap on the volume-regulated anion channel and KATP channel activity in rat pancreatic β-cells. Eur J Pharmacol 629:159–163

    Article  PubMed  CAS  Google Scholar 

  • Best L, Brown PD, Sener A, Malaisse WJ (2010b) Electrical activity in pancreatic islet cells: the VRAC hypothesis. Islets 2:59–64

    Article  PubMed  Google Scholar 

  • Blackard WG, Likuchi M, Rabinovitch A, Renold AE (1975) An effect of hypoosmolarity on insulin release in vitro. Am J Physiol 228:706–713

    PubMed  CAS  Google Scholar 

  • Boom A, Lybaert P, Pollet J-F, Jacobs P, Jijakli H, Golstein PE, Sener A, Malaisse WJ, Beauwens R (2007) Expression and localization of cystic fibrosis transmembrane conductance regulator in the endocrine pancreas. Endocrine 32:197–205

    Article  PubMed  CAS  Google Scholar 

  • Bukowiecki L, Trus M, Matschinsky FM, Freinkel N (1979) Alteration in pancreatic islet phosphate content during secretory stimulation with glucose. Biochim Biophys Acta 583:370–377

    Article  PubMed  CAS  Google Scholar 

  • Bulur N, Virreira M, Soyfoo MS, Louchami K, Delporte C, Perret J, Beauwens R, Malaisse WJ, Sener A (2009) Expression of the electrogenic Na+ -HCO3 – cotransporter NBCe1 in tumoral insulin-producing BRIN-BD11 cells. Cell Physiol Biochem 24:187–192

    Article  PubMed  CAS  Google Scholar 

  • Bulur N, Zhang Y, Malaisse WJ, Sener A (2010) Insulin release from isolated pancreatic islets, dispersed islet cells and tumoral insulin producing cells: a re-examination. Metab Funct Res Diab 3:20–24

    Google Scholar 

  • Bulur N, Crutzen R, Malaisse WJ, Sener A, Beauwens R, Golstein P (2013) Interaction between 3′,5′-cyclic monophosphate, volume-regulated anion channels and the Na+-HCO3 − cotransporter NBCe1 in the regulation of nutrient- and hypotonicity-induced insulin release from rat pancreatic islets and tumoral insulin-producing BRIN-BD11 cells. Mol Med Rep 7:1666–1672

    PubMed  CAS  Google Scholar 

  • Carpinelli AR, Malaisse WJ (1980) The stimulus-secretion coupling of glucose-induced insulin release. XLIV. A possible link between glucose metabolism and phosphate flush. Diabetologia 19:458–464

    Article  PubMed  CAS  Google Scholar 

  • Carpinelli AR, Malaisse WJ (1981) Regulation of 86Rb outflow from pancreatic islets. V. The dual effect of nutrient secretagogues. J Physiol (Lond) 315:143–156

    CAS  Google Scholar 

  • Casas S, Gomis R, Gribble FM, Altirriba J, Knuutila S, Novials A (2007) Impairment of the ubiquitin-proteasome pathway is a downstream endoplasmic reticulum stress response induced by extracellular human islet amyloid polypeptide and contributes to pancreatic β-cell apoptosis. Diabetes 56:2284–2294

    Article  PubMed  CAS  Google Scholar 

  • Cook DL, Hales CN (1984) Intracellular ATP directly blocks K+ channels in pancreatic β-cells. Nature 311:271–273

    Article  PubMed  CAS  Google Scholar 

  • Crutzen R, Shlyonsky V, Louchami K, Virreira M, Hupkens E, Boom A, Sener A, Malaisse WJ, Beauwens R (2012) Does NAD(P)H oxidase-derived H2O2 participate in hypotonicity-induced insulin release by activating VRAC in β-cells? Eur J Physiol 463:377–390

    Article  CAS  Google Scholar 

  • Davies SL, Roussa E, Le Rouzic P, Thevenod F, Alper SL, Best L, Brown PD (2004) Expression of K/Cl cotransporters in the a-cells of rat endocrine pancreas. Biochim Biophys Acta 1667:7–14

    Article  PubMed  CAS  Google Scholar 

  • Delporte C, Virreira M, Crutzen R, Louchami K, Sener A, Malaisse WJ, Beauwens R (2009) Functional role of aquaglyceroporin 7 expression in the pancreatic β-cell line BRIN-BD11. J Cell Physiol 221:424–429

    Article  PubMed  CAS  Google Scholar 

  • Freinkel N (1979) Phosphate translocation during secretory stimulation of pancreatic islets. In: Camerini-Davalos A, Hanover B (eds) Treatment of early diabetes. Plenum Press, New York, pp 71–77

    Chapter  Google Scholar 

  • Freinkel N, El Younsi C, Bonnar J, Dawson MC (1974) Rapid transient efflux of phosphate ions from pancreatic islets as an early action of insulin secretagogues. J Clin Invest 54:1179–1189

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Freinkel N, El Younsi C, Dawson RMC (1976) Insulin release and phosphate ion efflux from rat pancreatic islets induced by L-leucine and its nonmetabolizable analogue, 2-amino-bicyclo[2-2-1]heptane-2-carboxylic acid. Proc Natl Acad Sci USA 73:3403–3407

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gawenis LR, Bradford EM, Prasad V, Lorenz JN, Simpson JE, Charke LL, Woo AL, Grisham C, Sanford LP, Doetschman T, Miller ML, Shull GE (2007) Colonic anion secretory defects and metabolic acidosis in mice lacking the NBC1 Na+/HCO3 − cotransporter. J Biol Chem 282:9042–9052

    Article  PubMed  CAS  Google Scholar 

  • Hanzu FA, Gasa R, Bulur N, Lybaert P, Gomis R, Malaisse WJ, Beauwens R, Sener A (2012) Expression of TMEM16A and SLC4A4 in human pancreatic islets. Cell Physiol Biochem 29:61–64

    Article  PubMed  CAS  Google Scholar 

  • Henquin JC, Detimary P, Gembal M, Jonas JC, Shepherd RM, Warnotte C, Gilon P (1994) Aspects biophysiques du contrôle de la sécrétion d’insuline. Journées de Diabétologie de l’Hôtel-Dieu:21–32

    Google Scholar 

  • Huang F, Rock JR, Harfe BD, Cheng T, Huang X, Jan YN, Jan LY (2009) Studies on expression and function of the TMEM16A calcium-activated chloride channel. Proc Natl Acad Sci USA 106:21413–21418

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Li D-Q, Jing X, Salehi A, Collins SC, Hoppa MB, Rosengren AH, Zhang E, Lundquist I, Oloffson CS, Mörgerlin M, Eliasson L, Rorsman P, Renström E (2009) Suppression of sulfonylurea- and glucose-induced insulin secretion in vitro and in vivo in mice lacking the chloride transport protein CIC-3. Cell Metab 10:309–315

    Article  PubMed  Google Scholar 

  • Louchami K, Zhang Y, Beauwens R, Malaisse WJ, Sener A (2007) Is the glucose-induced phosphate flush in pancreatic islets attributable to gating of volume-sensitive anion channels? Endocrine 31:1–4

    Article  PubMed  CAS  Google Scholar 

  • Louchami K, Best L, Brown P, Virreira M, Hupkens E, Perret J, Devuyst O, Uchida S, Delporte C, Malaisse WJ, Beauwens R, Sener A (2012) A new role for aquaporin 7 in insulin secretion. Cell Physiol Biochem 29:65–74

    Article  PubMed  CAS  Google Scholar 

  • Majid A, Speake T, Best L, Brown PD (2001) Expression of the Na-K-2Cl cotransporter in and β cells isolated from the rat pancreas. Pflugers Arch 442:570–576

    Article  PubMed  CAS  Google Scholar 

  • Malaisse WJ, Orci L (1979) The role of the cytoskeleton in pancreatic β-cell function. In: Gabbiani G (ed) Methods of achievements in experimental pathology, vol 9. S. Karger, Basel, pp 112–136

    Google Scholar 

  • Malaisse WJ, Sener A, Koser M, Herchuelz A (1976) The stimulus-secretion coupling of glucose-induced insulin release. XXIV. The metabolism of α- and β-D-glucose in isolated islets. J Biol Chem 251:5936–5943

    PubMed  CAS  Google Scholar 

  • Malaisse WJ, Herchuelz A, Levy J, Sener A (1977) Calcium-antagonists and islet function. III. The possible site of action of verapamil. Biochem Pharmacol 26:735–740

    Article  PubMed  CAS  Google Scholar 

  • Malaisse WJ, Sener A, Herchuelz A, Hutton JC (1979a) Insulin release: the fuel hypothesis. Metabolism 28:373–386

    Article  PubMed  CAS  Google Scholar 

  • Malaisse WJ, Hutton JC, Kawazu S, Herchuelz A, Valverde I, Sener A (1979b) The stimulus-secretion coupling of glucose-induced insulin release. XXXV. The links between metabolic and cationic events. Diabetologia 16:331–341

    Article  PubMed  CAS  Google Scholar 

  • Malaisse WJ, Malaisse-Lagae F, Mayhew D (1967) A possible role for the adenylcyclase system in insulin secretion. J Clin Invest 46:1724–1734

    Google Scholar 

  • Malaisse WJ, Sener A, Welsh M, Malaisse-Lagae F, Hellerström C, Christophe J (1983) Mechanism of 3-phenylpyruvate-induced insulin release. Metabolic aspects. Biochem J 210:921–927

    PubMed  CAS  PubMed Central  Google Scholar 

  • Malaisse WJ, Zhang Y, Louchami K, Jijakli H (2004) Stimulation by D-glucose of 36Cl− efflux from prelabeled rat pancreatic islets. Endocrine 25:23–25

    Article  PubMed  CAS  Google Scholar 

  • Malaisse WJ, Best L, Beauwens R, Sener A (2008) Ionic determinants of the insulinotropic action of glucose: the anion channel hypothesis. Metab Funct Res Diab 1:2–6

    Google Scholar 

  • Malaisse WJ, Virreira M, Zhang Y, Crutzen R, Bulur N, Lybaert P, Golstein PE, Sener A, Beauwens R (2012) Role of anoctamin 1 (TMEM16A) as a volume regulated anion channel in insulin-producing cells. Diabetologia 55(Suppl 1):S204

    Google Scholar 

  • Malaisse WJ, Crutzen R, Bulur N, Virreira M, Rzajeva A, Golstein PE, Sener A, Beauwens R (2013) Effects of the inhibitor of anoctamin 1, tannic acid, on insulin-producing cells. Diabetologia 56(Suppl 1):S196

    Google Scholar 

  • Martins JR, Faria D, Kongsuphol P, Schreiber R, Kunzelmann K (2011) Anoctamin 6 is an essential component of the outwardly rectifying chloride channel. Proc Natl Acad Sci USA 108:18168–18172

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Matsumura K, Chang BH, Fujimiya M, Chen W, Kulkarni RN, Eguchi Y, Kimura H, Kojima H, Chan L (2007) Aquaporin 7 is a β-cell protein and regulator of intraislet glycerol content and glycerol kinase activity, β-cell mass, and insulin production and secretion. Mol Cell Biol 27:6026–6037

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • McClenaghan NH, Barnett CR, O’Harte FP, Flatt PR (1996) Mechanisms of amino acid-induced insulin secretion from the glucose-responsive BRIN-BD11 pancreatic β-cell line. J Endocrinol 151:349–357

    Article  PubMed  CAS  Google Scholar 

  • McGlasson L, Best L, Brown PD (2011) The glucokinase activator GKA50 causes an increase in cell volume and activation of volume-regulated anion channels in rat pancreatic β-cells. Mol Cell Endocrinol 342:48–53

    Article  PubMed  CAS  Google Scholar 

  • Miley HE, Sheader EA, Brown PD, Best L (1997) Glucose-induced swelling in rat pancreatic β-cells. J Physiol (Lond) 504:191–198

    Article  CAS  Google Scholar 

  • Muller-Berger S, Ducoudret O, Diakov A, Frömter E (2001) The renal Na-HCO3 − cotransporter expressed in Xenopus laevis oocytes: change in stoichiometry in response to elevation of cytosolic Ca2 concentrations. Pflugers Arch 442:718–728

    Article  PubMed  CAS  Google Scholar 

  • Namkung W, Phuan PW, Verkman AS (2011) TMEM16A inhibitors reveal TMEM16A as a minor component of calcium-activated chloride channel conductance in airway and intestinal epithelial cells. J Biol Chem 286:2365–2374

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Orci L, Malaisse WJ (1980) Hypothesis: single and chain release of insulin secretory granules is related to anionic transport at exocytotic sites. Diabetes 29:943–944

    Article  PubMed  CAS  Google Scholar 

  • Parker MD, Boron WF (2008) Sodium-coupled bicarbonate transporters. In: Alpern RJ, Hebert SC (eds) Seldin and Giebisch’s. The kidney physiology and pathophysiology. Elsevier Academic Press, Amsterdam, pp 1481–1497

    Google Scholar 

  • Ramos LS, Zippin JH, Kamenetsky M, Buck J, Levin LR (2008) Glucose and GLP-1 stimulate camp production via distinct adenylyl cyclases in INS-1E insulinoma cells. J Gen Physiol 132:329–338

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rojek A, Praetorius J, Froklaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327

    Article  PubMed  CAS  Google Scholar 

  • Schreiber R, Uliyakina I, Kongsuphol P, Warth R, Mirza M, Martins JR, Kunzelmann K (2010) Expression and function of epithelial anoctamins. J Biol Chem 285:7838–7845

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sehlin J (1978) Interrelationship between chloride fluxes in pancreatic islets and insulin release. Am J Physiol 235:E501–E508

    PubMed  CAS  Google Scholar 

  • Sener A, Malaisse WJ (1976) Measurement of lactic acid in nanomolar amounts. Reliability of such a method as an index of glycolysis in pancreatic islets. Biochem Med 15:34–41

    Article  PubMed  CAS  Google Scholar 

  • Sener A, Malaisse WJ (2012) Secretory, ionic and metabolic events in rat pancreatic islets deprived of extracellular NaHCO3. Metab Funct Res Diab 5:1–3

    Google Scholar 

  • Sener A, Malaisse-Lagae F, Malaisse WJ (1981) Stimulation of islet metabolism and insulin release by a nonmetabolizable amino acid. Proc Natl Acad Sci U S A 78:5460–5464

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sener A, Welsh M, Lebrun P, Garcia-Morales P, Saceda M, Malaisse-Lagae F, Herchuelz A, Valverde I, Hellerström C, Malaisse WJ (1983) Mechanism of 3-phenylpyruvate-induced insulin release. Secretory, ionic and oxidative aspects. Biochem J 210:913–919

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sener A, Jijakli H, Zahedi Asl S, Courtois P, Yates AP, Meuris S, Best LC, Malaisse WJ (2007) Possible role of carbonic anhydrase in rat pancreatic islets: enzymatic, secretory, metabolic, ionic, and electrical aspects. Am J Physiol 292:E1624–E1630

    CAS  Google Scholar 

  • Somers G, Blondel B, Orci L, Malaisse WJ (1979) Motile events in pancreatic endocrine cells. Endocrinology 104:255–264

    Article  PubMed  CAS  Google Scholar 

  • Somers G, Sener A, Devis G, Malaisse WJ (1980) The stimulus-secretion coupling of glucose-induced insulin release. XLV. The anion-osmotic hypothesis for exocytosis. Pflugers Arch 388:249–253

    Article  PubMed  CAS  Google Scholar 

  • Soyfoo MS, Bulur N, Virreira M, Louchami K, Lybaert P, Crutzen R, Perret J, Delporte C, Roussa E, Thevenod F, Best L, Yates AP, Malaisse WJ, Sener A, Beauwens R (2009) Expression of the electrogenic Na+ -HCO3 − cotransporters NBCe1-A and NBCe1-B in rat pancreatic islet cells. Endocrine 35:449–458

    Article  PubMed  CAS  Google Scholar 

  • Valverde I, Vandermeers A, Anjaneyulu R, Malaisse WJ (1979) Calmodulin activation of adenylate cyclase in pancreatic islets. Science 206:225–227

    Article  PubMed  CAS  Google Scholar 

  • Valverde I, Garcia-Morales P, Ghiglione M, Malaisse WJ (1983) The stimulus-secretion coupling of glucose-induced insulin release. LIII. Calcium-dependency of the cyclic AMP response to nutrient secretagogues. Horm Metab Res 15:62–68

    Article  PubMed  CAS  Google Scholar 

  • Virreira M, Malaisse WJ, Sener A, Beauwens R (2012) Expression of aquaporin isoforms in mouse pancreatic islets. Metab Funct Res Diab 5:27–28

    Google Scholar 

  • Zhao C, Wilson MC, Schuit F, Halestrap AP, Rutter GA (2001) Expression and distribution of lactate/monocarboxylate transporter isoforms in pancreatic islets and the exocrine pancreas. Diabetes 50:361–366

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Experimental Medicine, Université Libre de Bruxelles, B-1070, Brussels, Belgium

    Nurdan Bulur & Willy J. Malaisse

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  1. Nurdan Bulur
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  2. Willy J. Malaisse
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Correspondence to Willy J. Malaisse .

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  1. Department of Clinical Sciences and Education, Sodersjukhuset, Karolinska Institutet, Stockholm, Sweden

    Md. Shahidul Islam

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Bulur, N., Malaisse, W.J. (2015). Anionic Transporters and Channels in Pancreatic Islet Cells. In: Islam, M. (eds) Islets of Langerhans. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6686-0_41

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