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

Molecular and Cellular Endocrinology

Volumn 436, Issue , 2016, Pages 102-113

  Khan, Dawood ^a   Vasu, Srividya ^a   Moffett, R Charlotte ^a   Irwin, Nigel ^a   Flatt, Peter R ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

Apoptosis; Beta cell; Diabetes; NPYR; Peptide YY (PYY); Proliferation

Indexed keywords

ALANINE; CYCLIC AMP; GLUCAGON; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; HYDROCORTISONE; MESSENGER RNA; NEUROPEPTIDE Y RECEPTOR; PEPTIDE YY; PEPTIDE YY [3-36]; SOMATOSTATIN; STREPTOZOCIN; CALCIUM; INSULIN; PANCREAS POLYPEPTIDE; PROTECTIVE AGENT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE POTENTIAL; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; FOOD INTAKE; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN RELEASE; INSULIN RESISTANCE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; FEEDING BEHAVIOR; GENETICS; GLUCOSE TOLERANCE TEST; INTRACELLULAR SPACE; MEMBRANE POTENTIAL; METABOLISM; SECRETION (PROCESS);

ANIMALS; APOPTOSIS; CALCIUM; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DNA DAMAGE; FEEDING BEHAVIOR; GLUCAGON; GLUCOSE TOLERANCE TEST; HUMANS; HYDROCORTISONE; INSULIN; INSULIN-SECRETING CELLS; INTRACELLULAR SPACE; MALE; MEMBRANE POTENTIALS; MICE, INBRED C57BL; PANCREATIC POLYPEPTIDE; PEPTIDE YY; PROTECTIVE AGENTS; RECEPTORS, NEUROPEPTIDE Y; RNA, MESSENGER; SOMATOSTATIN; STREPTOZOCIN;

EID: 84979790103     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2016.07.020     Document Type: Article

References (67)

1. Ali-Rachedi, A., Varndell, I., Adrian, T., Gapp, D., Van Noorden, S., Bloom, S., Polak, J., Peptide YY (PYY) immunoreactivity is co-stored with glucagon-related immunoreactants in endocrine cells of the gut and pancreas. Histochemistry 80 (1984), 487–491.
2. Amisten, S., Salehi, A., Rorsman, P., Jones, P.M., Persaud, S.J., An atlas and functional analysis of G-protein coupled receptors in human islets of langerhans. Pharmacol. Ther. 139 (2013), 359–391.
3. Baeuerle, P.A., Baltimore, D., NF-κB: ten years after. Cell 87 (1996), 13–20.
4. Baggio, L.L., Drucker, D.J., Biology of incretins: GLP-1 and GIP. Gastroenterol 132 (2007), 2131–2157.
5. Batterham, R.L., Bloom, S.R., The gut hormone Peptide YY regulates appetite. Ann. N. Y. Acad. Sci. 994 (2003), 162–168.
6. Batterham, R.L., Cowley, M.A., Small, C.J., et al. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418 (2002), 650–654.
7. Bernardo, A.S., Hay, C.W., Docherty, K., Pancreatic transcription factors and their role in the birth, life and survival of the pancreatic β cell. Mol. Cell. Endocrinol. 294 (2008), 1–9.
8. Boey, D., Sainsbury, A., Herzog, H., The role of Peptide YY in regulating glucose homeostasis. Peptides 28 (2007), 390–395.
9. Boey, D., Lin, S., Karl, T., et al. Peptide YY ablation in mice leads to the development of hyperinsulinaemia and obesity. Diabetologia 49 (2006), 1360–1370.
10. Böttcher, G., Ekblad, E., Ekman, R., Håkanson, R., Sundler, F., Peptide YY: a neuropeptide in the gut. immunocytochemical and immunochemical evidence. Neuroscience 55 (1993), 281–290.
11. Böttcher, G., Ahren, B., Lundquist, I., Sundler, F., Peptide YY: intrapancreatic localization and effects on insulin and glucagon secretion in the mouse. Pancreas 4 (1989), 282–288.
12. Brown, R.J., Rother, K.I., Effects of beta-cell rest on beta-cell function: a review of clinical and preclinical data. Pediatr. Diabetes 9 (2008), 14–22.
13. Campbell, J.E., Drucker, D.J., Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab. 17 (2013), 819–837.
14. Chandarana, K., Gelegen, C., Irvine, E.E., et al. Peripheral activation of the Y2-receptor promotes secretion of GLP-1 and improves glucose tolerance. Mol. Metab. 2 (2013), 142–152.
15. Chung, C., Levine, F., Adult pancreatic alpha-cells: a new source of cells for beta-cell regeneration. Rev. Diabet. Stud. 7 (2010), 124–131.
16. Eizirik, D.L., Mandrup-Poulsen, T., A choice of death–the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia 44 (2001), 2115–2133.
17. Flatt, P.R., Bailey, C.J., Plasma glucose and insulin response to glucagon and arginine in Aston ob/ob mice: evidence for a selective defect in glucose-mediated insulin release. Horm. Metab. Res. 14 (1982), 127–130.
18. Fujita, Y., Wideman, R.D., Asadi, A., Yang, G.K., Baker, R., Webber, T., Zhang, T., Wang, R., Ao, Z., Warnock, G.L., Glucose-dependent insulinotropic polypeptide is expressed in pancreatic islet α-cells and promotes insulin secretion. Gastroenterology 138 (2010), 1966–1975.
19. Grandt, D., Schimiczek, M., Beglinger, C., Layer, P., Goebell, H., Eysselein, V., Reeve, J., Two molecular forms of Peptide YY (PYY) are abundant in human blood: characterization of a radioimmunoassay recognizing PYY 1–36 and PYY 3–36. Reg. Pept. 51 (1994), 151–159.
20. Grandt, D., Teyssen, S., Schimiczek, M., et al. Novel generation of hormone receptor specificity by amino terminal processing of Peptide YY. Biochem. Biophys. Res. Comm. 186 (1992), 1299–1306.
21. Greeley, G.H. Jr., Lluis, F., Gomez, G., Ishizuka, J., Holland, B., Thompson, J.C., Peptide YY antagonizes beta-adrenergic-stimulated release of insulin in dogs. Am. J. Physiol. 254 (1988), E513–E517.
22. Green, A.D., Vasu, S., McClenaghan, N.H., Flatt, P.R., Pseudoislet formation enhances gene expression, insulin secretion and cytoprotective mechanisms of clonal human insulin-secreting 1.1B4 cells. Pflugers Arch. 467 (2015), 2219–2228.
23. Hamid, M., McCluskey, J.T., McClenaghan, N.H., Flatt, P.R., Comparison of the secretory properties of four insulin-secreting cell lines. Endocr. Res. 28 (2002), 35–47.
24. Hansel, D.E., Eipper, B.A., Ronnett, G.V., Neuropeptide Y functions as a neuroproliferative factor. Nature 410 (2001), 940–944.
25. Hansen, A., Bödvarsdottir, T., Nordestgaard, D., et al. Upregulation of alpha cell glucagon-like peptide 1 (GLP-1) in psammomys obesus—an adaptive response to hyperglycaemia?. Diabetologia 54 (2011), 1379–1387.
26. Heller, R.S., Aponte, G.W., Intra-islet regulation of hormone secretion by glucagon-like peptide-1-(7–36) amide. Am. J. Physiol. 269 (1995), G852–G860.
27. Howell, O.W., Silva, S., Scharfman, H.E., et al. Neuropeptide Y is important for basal and seizure-induced precursor cell proliferation in the hippocampus. Neurobiol. Dis. 26 (2007), 174–188.
28. Karra, E., Chandarana, K., Batterham, R.L., The role of Peptide YY in appetite regulation and obesity. J. Physiol. 587 (2009), 19–25.
29. Kazanjian, K.K., Towfigh, S., McFadden, D.W., Peptide YY exhibits a mitogenic effect on pancreatic cells while improving acute pancreatitis in vitro. J. Surg. Res. 114 (2003), 95–99.
30. Lees Murdock, D.J., Barnett, Y.A., Barnett, C.R., DNA damage and cytotoxicity in pancreatic beta-cells expressing human CYP2E1. Biochem. Pharmacol. 68 (2004), 523–530.
31. Mannon, P.J., Peptide YY as a growth factor for intestinal epithelium. Peptides 23 (2002), 383–388.
32. Marchetti, P., Lupi, R., Bugliani, M., et al. A local glucagon-like peptide 1 (GLP-1) system in human pancreatic islets. Diabetologia 55 (2012), 3262–3272.
33. Masur, K., Tibaduiza, E.C., Chen, C., Ligon, B., Beinborn, M., Basal receptor activation by locally produced glucagon-like peptide-1 contributes to maintaining beta-cell function. Mol. Endocrinol. 19 (2005), 1373–1382.
34. McClenaghan, N.H., Barnett, C.R., Ah-Sing, E., et al. Characterization of a novel glucose-responsive insulin-secreting cell line, BRIN-BD11, produced by electrofusion. Diabetes 45 (1996), 1132–1140.
35. McCluskey, J.T., Hamid, M., Guo-Parke, H., McClenaghan, N.H., Gomis, R., Flatt, P.R., Development and functional characterization of insulin-releasing human pancreatic beta cell lines produced by electrofusion. J. Biol. Chem. 286 (2011), 21982–21992.
36. Medeiros, M.D., Turner, A.J., Processing and metabolism of Peptide-YY: pivotal roles of dipeptidylpeptidase-IV, aminopeptidase-P, and endopeptidase-24.11. Endocrinology 134 (1994), 2088–2094.
37. Miguel, J.C., Patterson, S., Abdel-Wahab, Y.H., Mathias, P.C., Flatt, P.R., Time-correlation between membrane depolarization and intracellular calcium in insulin secreting BRIN-BD11 cells: studies using FLIPR. Cell Calcium 36 (2004), 43–50.
38. Moffett, R.C., Irwin, N., Francis, J.M.E., Flatt, P.R., Alterations of glucose-dependent insulinotropic polypeptide and expression of genes involved in mammary gland and adipose tissue lipid metabolism during pregnancy and lactation. PLoS One, 8, 2013, e78560.
39. Moffett, R.C., Vasu, S., Thorens, B., Drucker, D.J., Flatt, P.R., Incretin receptor null mice reveal key role of GLP-1 but not GIP in pancreatic beta-cell adaptation to pregnancy. PloS One, 9, 2014, e96863.
40. Moffett, R.C., Vasu, S., Flatt, P.R., Functional GIP receptors play a major role in islet compensatory response to high fat feeding in mice. Biochim. Biophys. Acta 1850 (2015), 1206–1214.
41. Morgan, D., Small, C., Abusnana, S., et al. The NPY Y1 receptor antagonist BIBP 3226 blocks NPY induced feeding via a non-specific mechanism. Reg. Pept. 75 (1998), 377–382.
42. Mulder, H., Myrsen-Axcrona, U., Gebre-Medhin, S., Ekblad, E., Sundler, F., Expression of non-classical islet hormone-like peptides during the embryonic development of the pancreas. Microsc. Res. Tech., 433, 1998 13–321.
43. Murphy, K.G., Bloom, S.R., Gut hormones and the regulation of energy homeostasis. Nature 444 (2006), 854–859.
44. Myrsen-Axcrona, U., Ekblad, E., Sundler, F., Developmental expression of NPY, PYY and PP in the rat pancreas and their coexistence with islet hormones. Reg. Pept. 68 (1997), 165–175.
45. Nieuwenhuizen, A., Karlsson, S., Fridolf, T., Ahren, B., Mechanisms underlying the insulinostatic effect of Peptide YY in mouse pancreatic islets. Diabetologia 37 (1994), 871–878.
46. Omar, B.A., Liehua, L., Yamada, Y., Seino, Y., Marchetti, P., Ahrén, B., Dipeptidyl peptidase 4 (DPP-4) is expressed in mouse and human islets and its activity is decreased in human islets from individuals with type 2 diabetes. Diabetologia 57 (2014), 1876–1883.
47. Pathak, V., Vasu, S., Gault, V.A., Flatt, P.R., Irwin, N., Sequential induction of beta cell rest and stimulation using stable GIP inhibitor and GLP-1 mimetic peptides improves metabolic control in C57BL/KsJ db/db mice. Diabetologia 58 (2015), 2144–2153.
48. Persaud, S.J., Bewick, G.A., Peptide YY: more than just an appetite regulator. Diabetologia 57 (2014), 1762–1769.
49. Pittner, R.A., Moore, C.X., Bhavsar, S.P., et al. Effects of PYY[3-36] in rodent models of diabetes and obesity. Int. J. Obes. 28 (2004), 963–971.
50. Ramracheya, R.D., McCulloch, L.J., Clark, A., et al. PYY-dependent restoration of impaired insulin and glucagon secretion in type 2 diabetes following Roux-En-Y gastric bypass surgery. Cell Rep. 15 (2016), 944–950.
51. Rombout, J.H., Abad, M.E., Binkhorst, F.M., Taverne-Thiele, J.J., Coexistence of pancreatic polypeptide (PP)-and glucagon-immunoreactivity in pancreatic endocrine cells of mouse. Histochemistry 87 (1987), 1–6.
52. Sam, A.H., Gunner, D.J., King, A., et al. Selective ablation of Peptide YY cells in adult mice reveals their role in beta-cell survival. Gastroenterology 143 (2012), 459–468.
53. Shi, Y.C., Hämmerle, C.M., Lee, I.C., et al. Adult-onset PYY overexpression in mice reduces food intake and increases lipogenic capacity. Neuropeptides 46 (2012), 173–182.
54. Shi, Y.C., Loh, K., Bensellam, M., et al. Pancreatic PYY is critical in the control of insulin secretion and glucose homeostasis in female mice. Endocrinology 156 (2015), 3122–3136.
55. Szecowka, J., Tatemoto, K., Rajamäki, G., Efendić, S., Effects of PYY and PP on endocrine pancreas. Acta Physiol. Scand. 119 (1983), 123–126.
56. Tatemoto, K., Mutt, V., Isolation of two novel candidate hormones using a chemical method for finding naturally occurring polypeptides. Nature 285 (1980), 417–418.
57. Thiriet, N., Deng, X., Solinas, M., et al. Neuropeptide Y protects against methamphetamine-induced neuronal apoptosis in the mouse striatum. J. Neurosci. 25 (2005), 5273–5279.
58. Thorens, B., The required beta cell research for improving treatment of type 2 diabetes. J. Int. Med. 274 (2013), 203–214.
59. Unger, R., Dobbs, R., Orci, L., Insulin, glucagon, and somatostatin secretion in the regulation of metabolism. Ann. Rev. Physiol. 40 (1978), 307–343.
60. Upchurch, B.H., Aponte, G.W., Leiter, A.B., Expression of Peptide YY in all four islet cell types in the developing mouse pancreas suggests a common Peptide YY-producing progenitor. Development 120 (1994), 245–252.
61. Vasu, S., Moffett, R.C., Thorens, B., Flatt, P.R., Role of endogenous GLP-1 and GIP in beta-cell compensatory responses to insulin resistance and cellular stress. PloS One, 9, 2014, e101005.
62. Vasu, S., Moffett, R.C., McCluskey, J.T., Hamid, M.H., Irwin, N., Flatt, P.R., Beneficial effects of parenteral GLP-1 delivery by cell therapy in insulin-deficient streptozotocin diabetic mice. Gene Ther. 20 (2013), 1077–1084.
63. Wierup, N., Sundler, F., Heller, R.S., The islet ghrelin cell. J. Mol. Endocrinol. 52 (2014), R35–R49.
64. Whalley, N.M., Pritchard, L.E., Smith, D.M., White, A., Processing of proglucagon to GLP-1 in pancreatic alpha-cells: is this a paracrine mechanism enabling GLP-1 to act on beta-cells?. J. Endocrinol. 211 (2011), 99–106.
65. Wittmann, W., Loacker, S., Kapeller, I., Herzog, H., Schwarzer, C., Y1-receptors regulate the expression of Y2-receptors in distinct mouse forebrain areas. Neuroscience 136 (2005), 241–250.
66. Yada, T., Damdindorj, B., Rita, R., et al. Ghrelin signalling in β-cells regulates insulin secretion and blood glucose. Diabetes Obes. Metab. 16 (2014), 111–117.
67. Zambello, E., Zanetti, L., Hédou, G.F., et al. Neuropeptide Y-Y2 receptor knockout mice: influence of genetic background on anxiety-related behaviors. Neuroscience 176 (2011), 420–430.