Islet distribution of Peptide YY and its regulatory role in primary mouse islets and immortalised rodent and human beta-cell function and survival

Mol Cell Endocrinol. 2016 Nov 15:436:102-13. doi: 10.1016/j.mce.2016.07.020. Epub 2016 Jul 25.

Abstract

Recent evidence suggests that the classic gut peptide, Peptide YY (PYY), could play a fundamental role in endocrine pancreatic function. In the present study expression of PYY and its NPY receptors on mouse islets and immortalised rodent and human beta-cells was examined together with the effects of both major circulating forms of PYY, namely PYY(1-36) and PYY(3-36), on beta-cell function, murine islet adaptions to insulin deficiency/resistance, as well as direct effects on cultured beta-cell proliferation and apoptosis. In vivo administration of PYY(3-36), but not PYY(1-36), markedly (p < 0.05) decreased food intake in overnight fasted mice. Neither form of PYY affected glucose disposal or insulin secretion following an i.p. glucose challenge. However, in vitro, PYY(1-36) and PYY(3-36) inhibited (p < 0.05 to p < 0.001) glucose, alanine and GLP-1 stimulated insulin secretion from immortalised rodent and human beta-cells, as well as isolated mouse islets, by impeding alterations in membrane potential, [Ca(2+)]i and elevations of cAMP. Mice treated with multiple low dose streptozotocin presented with severe (p < 0.01) loss of beta-cell mass accompanied by notable increases (p < 0.001) in alpha and PP cell numbers. In contrast, hydrocortisone-induced insulin resistance increased islet number (p < 0.01) and beta-cell mass (p < 0.001). PYY expression was consistently observed in alpha-, PP- and delta-, but not beta-cells. Streptozotocin decreased islet PYY co-localisation with PP (p < 0.05) and somatostatin (p < 0.001), whilst hydrocortisone increased PYY co-localisation with glucagon (p < 0.05) in mice. More detailed in vitro investigations revealed that both forms of PYY augmented (p < 0.05 to p < 0.01) immortalised human and rodent beta-cell proliferation and protected against streptozotocin-induced cytotoxicity, to a similar or superior extent as the well characterised beta-cell proliferative and anti-apoptotic agent GLP-1. Taken together, these data highlight the significance and potential offered by modulation of pancreatic islet NPY receptor signalling pathways for preservation of beta-cell mass in diabetes.

Keywords: Apoptosis; Beta-cell; Diabetes; NPYR; Peptide YY (PYY); Proliferation.

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Calcium / metabolism
  • Cell Line
  • Cell Proliferation / genetics
  • Cell Survival / drug effects
  • Cells, Cultured
  • DNA Damage
  • Feeding Behavior
  • Glucagon / metabolism
  • Glucose Tolerance Test
  • Humans
  • Hydrocortisone / pharmacology
  • Insulin / metabolism
  • Insulin Secretion
  • Insulin-Secreting Cells / cytology*
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism*
  • Intracellular Space / metabolism
  • Male
  • Membrane Potentials / drug effects
  • Mice, Inbred C57BL
  • Pancreatic Polypeptide / metabolism
  • Peptide YY / genetics
  • Peptide YY / metabolism*
  • Protective Agents / pharmacology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Neuropeptide Y / genetics
  • Receptors, Neuropeptide Y / metabolism
  • Somatostatin / metabolism
  • Streptozocin

Substances

  • Insulin
  • Protective Agents
  • RNA, Messenger
  • Receptors, Neuropeptide Y
  • Peptide YY
  • Somatostatin
  • Pancreatic Polypeptide
  • Streptozocin
  • Glucagon
  • Calcium
  • Hydrocortisone