Urocortin3 mediates somatostatin-dependent negative feedback control of insulin secretion (original) (raw)

• Lin, H.V. & Accili, D. Hormonal regulation of hepatic glucose production in health and disease. Cell Metab. 14, 9–19 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Leto, D. & Saltiel, A.R. Regulation of glucose transport by insulin: traffic control of GLUT4. Nat. Rev. Mol. Cell Biol. 13, 383–396 (2012).
  Article CAS PubMed Google Scholar
• Ramnanan, C.J., Edgerton, D.S., Kraft, G. & Cherrington, A.D. Physiologic action of glucagon on liver glucose metabolism. Diabetes Obes. Metab. 13 (suppl. 1), 118–125 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, Q. et al. Role of KATP channels in glucose-regulated glucagon secretion and impaired counterregulation in type 2 diabetes. Cell Metab. 18, 871–882 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Taborsky, G.J. Jr., Smith, P.H. & Porte, D. Jr. Interaction of somatostatin with the A and B cells of the endocrine pancreas. Metabolism 27, 1299–1302 (1978).
  Article CAS PubMed Google Scholar
• Caicedo, A. Paracrine and autocrine interactions in the human islet: more than meets the eye. Semin. Cell Dev. Biol. 24, 11–21 (2013).
  Article CAS PubMed Google Scholar
• Patel, Y.C. Somatostatin and its receptor family. Front. Neuroendocrinol. 20, 157–198 (1999).
  Article CAS PubMed Google Scholar
• Salehi, A., Qader, S.S., Grapengiesser, E. & Hellman, B. Pulses of somatostatin release are slightly delayed compared with insulin and antisynchronous to glucagon. Regul. Pept. 144, 43–49 (2007).
  Article CAS PubMed Google Scholar
• Schuit, F.C., Derde, M.P. & Pipeleers, D.G. Sensitivity of rat pancreatic A and B cells to somatostatin. Diabetologia 32, 207–212 (1989).
  Article CAS PubMed Google Scholar
• Unger, R.H. & Cherrington, A.D. Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. J. Clin. Invest. 122, 4–12 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Braun, M. et al. Somatostatin release, electrical activity, membrane currents and exocytosis in human pancreatic delta cells. Diabetologia 52, 1566–1578 (2009).
  Article CAS PubMed Google Scholar
• Barden, N., Alvarado-Urbina, G., Cote, J.P. & Dupont, A. Cyclic AMP-dependent stimulation of somatostatin secretion by isolated rat islets of Langerhans. Biochem. Biophys. Res. Commun. 71, 840–844 (1976).
  Article CAS PubMed Google Scholar
• Ipp, E. et al. Release of immunoreactive somatostatin from the pancreas in response to glucose, amino acids, pancreozymin-cholecystokinin, and tolbutamide. J. Clin. Invest. 60, 760–765 (1977).
  Article CAS PubMed PubMed Central Google Scholar
• Schauder, P. et al. Somatostatin and insulin release from isolated rat pancreatic islets stimulated by glucose. FEBS Lett. 68, 225–227 (1976).
  Article CAS PubMed Google Scholar
• Patton, G.S. et al. Pancreatic immunoreactive somatostatin release. Proc. Natl. Acad. Sci. USA 74, 2140–2143 (1977).
  Article CAS PubMed PubMed Central Google Scholar
• Hauge-Evans, A.C. et al. Somatostatin secreted by islet delta-cells fulfills multiple roles as a paracrine regulator of islet function. Diabetes 58, 403–411 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Göpel, S.O., Kanno, T., Barg, S. & Rorsman, P. Patch-clamp characterisation of somatostatin-secreting -cells in intact mouse pancreatic islets. J. Physiol. (Lond.) 528, 497–507 (2000).
  Article Google Scholar
• Vieira, E., Salehi, A. & Gylfe, E. Glucose inhibits glucagon secretion by a direct effect on mouse pancreatic alpha cells. Diabetologia 50, 370–379 (2007).
  Article CAS PubMed Google Scholar
• Li, C. et al. Urocortin III is expressed in pancreatic beta-cells and stimulates insulin and glucagon secretion. Endocrinology 144, 3216–3224 (2003).
  Article CAS PubMed Google Scholar
• van der Meulen, T. et al. Urocortin 3 marks mature human primary and embryonic stem cell-derived pancreatic alpha and beta cells. PLoS ONE 7, e52181 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Benner, C. et al. The transcriptional landscape of mouse beta cells compared to human beta cells reveals notable species differences in long non-coding RNA and protein-coding gene expression. BMC Genomics 15, 620 (2014).
  Article PubMed PubMed Central Google Scholar
• Huising, M.O. & Vale, W.W. Corticotropin-releasing hormone and urocortins: binding proteins and receptors. in Encyclopedia of Neuroscience (ed. Squire, L.R.) 231–237 (Academic Press, Oxford, 2009).
• Hsu, S.Y. & Hsueh, A.J. Human stresscopin and stresscopin-related peptide are selective ligands for the type 2 corticotropin-releasing hormone receptor. Nat. Med. 7, 605–611 (2001).
  Article CAS PubMed Google Scholar
• Lewis, K. et al. Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc. Natl. Acad. Sci. USA 98, 7570–7575 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• van der Meulen, T. & Huising, M.O. Maturation of stem cell-derived beta cells guided by the expression of urocortin 3. Rev. Diabet. Stud. 11, 115–132 (2014).
  Article PubMed PubMed Central Google Scholar
• Blum, B. et al. Functional beta-cell maturation is marked by an increased glucose threshold and by expression of urocortin 3. Nat. Biotechnol. 30, 261–264 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Li, C., Chen, P., Vaughan, J., Lee, K.F. & Vale, W. Urocortin 3 regulates glucose-stimulated insulin secretion and energy homeostasis. Proc. Natl. Acad. Sci. USA 104, 4206–4211 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Huising, M.O. et al. Glucocorticoids differentially regulate the expression of CRFR1 and CRFR2α in MIN6 insulinoma cells and rodent islets. Endocrinology 152, 138–150 (2011).
  Article CAS PubMed Google Scholar
• Zhang, J., McKenna, L.B., Bogue, C.W. & Kaestner, K.H. The diabetes gene Hhex maintains delta cell differentiation and islet function. Genes Dev. 28, 829–834 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Artner, I. et al. MafA and MafB regulate genes critical to beta-cells in a unique temporal manner. Diabetes 59, 2530–2539 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Bale, T.L. et al. Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nat. Genet. 24, 410–414 (2000).
  Article CAS PubMed Google Scholar
• Rivier, J. et al. Potent and long-acting corticotropin releasing factor (CRF) receptor 2 selective peptide competitive antagonists. J. Med. Chem. 45, 4737–4747 (2002).
  Article CAS PubMed Google Scholar
• Rorsman, P. & Braun, M. Regulation of insulin secretion in human pancreatic islets. Annu. Rev. Physiol. 75, 155–179 (2013).
  Article CAS PubMed Google Scholar
• Rozzo, A., Meneghel-Rozzo, T., Delakorda, S.L., Yang, S.B. & Rupnik, M. Exocytosis of insulin: in vivo maturation of mouse endocrine pancreas. Ann. NY Acad. Sci. 1152, 53–62 (2009).
  Article CAS PubMed Google Scholar
• Nygaard, E.B., Moller, C.L., Kievit, P., Grove, K.L. & Andersen, B. Increased fibroblast growth factor 21 expression in high-fat diet-sensitive non-human primates (Macaca mulatta). Int. J. Obes. (Lond) 38, 183–191 (2014).
  Article CAS Google Scholar
• Yang, Y.H. et al. Paracrine signalling loops in adult human and mouse pancreatic islets: netrins modulate beta cell apoptosis signalling via dependence receptors. Diabetologia 54, 828–842 (2011).
  Article CAS PubMed Google Scholar
• Rodriguez-Diaz, R. et al. Alpha cells secrete acetylcholine as a non-neuronal paracrine signal priming beta cell function in humans. Nat. Med. 17, 888–892 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Xu, E. et al. Intra-islet insulin suppresses glucagon release via GABA-GABAA receptor system. Cell Metab. 3, 47–58 (2006).
  Article CAS PubMed Google Scholar
• Yang, Y.H., Manning Fox, J.E., Zhang, K.L., MacDonald, P.E. & Johnson, J.D. Intraislet SLIT-ROBO signaling is required for beta-cell survival and potentiates insulin secretion. Proc. Natl. Acad. Sci. USA 110, 16480–16485 (2013).
  Article PubMed PubMed Central Google Scholar
• Ohtani, O., Ushiki, T., Kanazawa, H. & Fujita, T. Microcirculation of the pancreas in the rat and rabbit with special reference to the insulo-acinar portal system and emissary vein of the islet. Arch. Histol. Jpn. 49, 45–60 (1986).
  Article CAS PubMed Google Scholar
• Liu, Y.M., Guth, P.H., Kaneko, K., Livingston, E.H. & Brunicardi, F.C. Dynamic in vivo observation of rat islet microcirculation. Pancreas 8, 15–21 (1993).
  Article CAS PubMed Google Scholar
• Murakami, T. et al. The insulo-acinar portal and insulo-venous drainage systems in the pancreas of the mouse, dog, monkey and certain other animals: a scanning electron microscopic study of corrosion casts. Arch. Histol. Cytol. 56, 127–147 (1993).
  Article CAS PubMed Google Scholar
• Bonner-Weir, S. & Orci, L. New perspectives on the microvasculature of the islets of Langerhans in the rat. Diabetes 31, 883–889 (1982).
  Article CAS PubMed Google Scholar
• Stagner, J.I., Samols, E. & Bonner-Weir, S. beta-alpha-delta pancreatic islet cellular perfusion in dogs. Diabetes 37, 1715–1721 (1988).
  Article CAS PubMed Google Scholar
• Samols, E. & Stagner, J.I. Islet somatostatin–microvascular, paracrine, and pulsatile regulation. Metabolism 39, 55–60 (1990).
  Article CAS PubMed Google Scholar
• Nyman, L.R. et al. Real-time, multidimensional in vivo imaging used to investigate blood flow in mouse pancreatic islets. J. Clin. Invest. 118, 3790–3797 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Benninger, R.K., Zhang, M., Head, W.S., Satin, L.S. & Piston, D.W. Gap junction coupling and calcium waves in the pancreatic islet. Biophys. J. 95, 5048–5061 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Ravier, M.A. et al. Loss of connexin36 channels alters beta-cell coupling, islet synchronization of glucose-induced Ca2+ and insulin oscillations, and basal insulin release. Diabetes 54, 1798–1807 (2005).
  Article CAS PubMed Google Scholar
• Head, W.S. et al. Connexin-36 gap junctions regulate in vivo first- and second-phase insulin secretion dynamics and glucose tolerance in the conscious mouse. Diabetes 61, 1700–1707 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Jørgensen, M.C. et al. An illustrated review of early pancreas development in the mouse. Endocr. Rev. 28, 685–705 (2007).
  Article CAS PubMed Google Scholar
• Herrera, P.L. et al. Embryogenesis of the murine endocrine pancreas; early expression of pancreatic polypeptide gene. Development 113, 1257–1265 (1991).
  CAS PubMed Google Scholar
• Gromada, J., Franklin, I. & Wollheim, C.B. Alpha-cells of the endocrine pancreas: 35 years of research but the enigma remains. Endocr. Rev. 28, 84–116 (2007).
  Article CAS PubMed Google Scholar
• Unger, R.H. & Orci, L. Paracrinology of islets and the paracrinopathy of diabetes. Proc. Natl. Acad. Sci. USA 107, 16009–16012 (2010).
  Article PubMed PubMed Central Google Scholar
• Huising, M.O. et al. CRFR1 is expressed on pancreatic beta cells, promotes beta cell proliferation, and potentiates insulin secretion in a glucose-dependent manner. Proc. Natl. Acad. Sci. USA 107, 912–917 (2010).
  Article PubMed Google Scholar
• Huising, M.O. et al. Residues of corticotropin releasing factor-binding protein (CRF-BP) that selectively abrogate binding to CRF but not to urocortin 1. J. Biol. Chem. 283, 8902–8912 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Asfari, M. et al. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130, 167–178 (1992).
  Article CAS PubMed Google Scholar
• Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Herrera, P.L. Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127, 2317–2322 (2000).
  CAS PubMed Google Scholar
• Srinivas, S. et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Reubi, J.C. et al. SST3-selective potent peptidic somatostatin receptor antagonists. Proc. Natl. Acad. Sci. USA 97, 13973–13978 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Cescato, R. et al. Design and in vitro characterization of highly sst2-selective somatostatin antagonists suitable for radiotargeting. J. Med. Chem. 51, 4030–4037 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
  Article CAS PubMed Google Scholar
• Quinlan, A.R. & Hall, I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57–74 (2012).
• Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Brazeau, P. et al. Hypothalamic polypeptide that inhibits the secretion of immunoreactive pituitary growth hormone. Science 179, 77–79 (1973).
  Article CAS PubMed Google Scholar
• Vale, W., Rivier, J., Ling, N. & Brown, M. Biologic and immunologic activities and applications of somatostatin analogs. Metabolism 27, 1391–1401 (1978).
  Article CAS PubMed Google Scholar
• Vaughan, J.M. et al. Detection and purification of inhibin using antisera generated against synthetic peptide fragments. Methods Enzymol. 168, 588–617 (1989).
  Article CAS PubMed Google Scholar
• Padmanabhan, K., Eddy, W.F. & Crowley, J.C. A novel algorithm for optimal image thresholding of biological data. J. Neurosci. Methods 193, 380–384 (2010).
  Article PubMed Google Scholar