High sensitivity of β-cell replication to the inhibitory effects of interleukin-1β: Modulation by adenoviral overexpression of IGF2 in rat islets

Journal of Endocrinology

Volumn 203, Issue 1, 2009, Pages 55-63

  Estilles, Elisabet ^a   Téllez, Noèlia ^a,b   Soler, Joan ^a,b,c   Montanya, Eduard ^a,b,c  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; INTERLEUKIN 1BETA; NITRITE; SOMATOMEDIN C; GLUCOSE; SOMATOMEDIN B;

ADENOVIRUS INFECTION; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DIVISION; CELL PROLIFERATION; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; MALE; MITOGENESIS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ADENOVIRUS; ANIMAL; GENE TRANSFER; LEWIS RAT; METABOLISM; PHYSIOLOGY;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; GENE TRANSFER TECHNIQUES; GLUCOSE; INSULIN-LIKE GROWTH FACTOR II; INSULIN-SECRETING CELLS; INTERLEUKIN-1BETA; MALE; RATS; RATS, INBRED LEW;

EID: 70349771376     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1677/JOE-09-0047     Document Type: Article

References (52)

1. Asfari M,Wei D, Noel M, Holthuizen PE & Czernichow P 1995 IGF-II gene expression in a rat insulin-producing β-cell line (INS-1) is regulated by glucose. Diabetologia 38 927-935.
2. Biarnés M, Montolio M, Nacher V, Raurell M, Soler J & Montanya E 2002 β-Cell death and mass in syngeneically transplanted islets exposed to short- and long-term hyperglycaemia. Diabetes 51 66-72. (Pubitemid 34517981)
3. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA & Butler PC 2003 B-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 52 102-110. (Pubitemid 36042113)
4. Butler AE, Galasso R, Meier JJ, Basu R, Rizza RA & Butler PC 2007 Modestly increased β-cell apoptosis but no increased β-cell replication in recent-onset type 1 diabetic patients who died of diabetic ketoacidosis. Diabetologia 50 2323-2331. (Pubitemid 47512399)
5. Castrillo A, Bodelón OG & Boscá L 2000 Inhibitory effect of IGF-1 on type 2 nitric oxide synthase expression in Ins-1 cells and protection against activation-dependent apoptosis. Involvement of phosphatidylinositol 3-kinase. Diabetes 49 209-217.
6. Darville MI & Eizirik DL 1998 Regulation by cytokines of the inducible nitric oxide synthase promoter in insulin-producing cells. Diabetologia 41 1101-1108. (Pubitemid 28394417)
7. Devendra D, Liu E & Eisenbarth GS 2004 Type 1 diabetes: recent developments. BMJ 328 750-754.
8. Donath MY, Gross DJ, Cerasi E & Kaiser N 1999 Hyperglycemia-induced β-cell apoptosis in pancreatic islets of Psammomys obesus during development of diabetes. Diabetes 48 738-744. (Pubitemid 29153072)
9. Dor Y, Brown J, Martinez OI & Melton DA 2004 Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429 41-46. (Pubitemid 38620543)
10. Eizirik DL & Mandrup-Poulsen T 2001 A choice of death. The signal transduction of immune-mediated β-cell apoptosis. Diabetologia 44 2115-2133.
11. Eizirik DL, Strandell E, Bendtzen K & Sandler S 1988 Functional characteristics of rat pancreatic islets maintained in culture after exposure to human interleukin 1. Diabetes 37 916-919. (Pubitemid 19043721)
12. Eizirik DL, Welsh M, Strandell E, Welsh N & Sandler S 1990 Interleukin-1β depletes insulin messenger ribonucleic acid and increses the heat shock protein hsp70 in mouse pancreatic islets without impairing the glucose metabolism. Endocrinology 127 2290-2297. (Pubitemid 20381760)
13. Giannoukakis N, Mi Z, Rudert WA, Gambotto A, Trucco M & Robbins P 2000 Prevention of β-cell dysfunction and apoptosis activation in human islets by adenoviral gene transfer of the insulin-like growth factor 1. Gene Therapy 7 2015-2022. (Pubitemid 32036767)
14. Hill DJ, Petrick J, Arany E, McDonald TJ & Delovitch TL 1999 Insulin-like growth factors prevent cytokine-mediated cell death in isolated islets of Langerhans from pre-diabetic non-obese diabetic mice. Journal of Endocrinology 161 153-165. (Pubitemid 29170202)
15. Hill DJ, Strutt B, Arany E, Zaina S, Coukell S & Graham CF 2000 Increased and persistent circulating insulin-like growth factor II in neonatal transgenic mice suppresses developmental apoptosis in the pancreatic islets. Endocrinology 141 1151-1157. (Pubitemid 32260458)
16. Hogg J, Han VKM, Clemmons DR & Hill DJ 1993 Interactions of nutrient, insulin-like growth factors (IGFs) and IGF binding proteins in the regulation of DNA synthesis by isolated fetal rat islets of Langerhans. Journal of Endocrinology 138 401-412. (Pubitemid 23343067)
17. Hoorens A, Van de Casteele M, Kloppel G & Pipeleers D 1996 Glucose promotes survival of rat pancreatic β-cells by activating synthesis of proteins which suppress a constitutive apoptotic program. Journal of Clinical Investigation 98 1568-1574. (Pubitemid 26327866)
18. Hügl SR,White MF & Rhodes CJ 1998 Insulin-like growth factor I (IGF-I)-stimulated pancreatic β-cell growth is glucose-dependent. Synergistic activation of insulin receptor substrate-mediated signal transduction pathways by glucose and IGF-I in INS-1 cells. Journal of Biological Chemistry 273 17771-17779.
19. Huotari MA, Palgi J & Otonkoski T 1998 Growth factor-mediated proliferation and differentiation of insulin-producing INS-1 and RINm5F cells: identification of betacelulin as a novel β-cell mitogen. Endocrinology 139 1494-1499. (Pubitemid 28513801)
20. Ilvemarski V, Jattela M, Saksela E & Voutilainen R 1993 Tumor necrosis factor-alpha and interferon-gamma inhibit insulin-like growth factor-II gene expression in human fetal adrenal cell cultures. Molecular and Cellular Endocrinology 91 59-65. (Pubitemid 23053807)
21. Larsen CM, Faulenbarch M, Vaag A, Volund A, Ehses JA, Seifert B, Mandrup-Poulsen T & Donath MY 2007 Interleukin-1-receptor antagonist in type 2 diabetes mellitus. New England Journal of Medicine 356 1517-1526. (Pubitemid 46588416)
22. Lin T,Wang DL, Nagpal ML & CahangW1994 Recombinant murine tumor necrosis factor alpha inhibits cholesterol side-chain cleavage cytochrome P450 and insulin-like growth factor-I gene expression in rat Leydig cells. Molecular and Cellular Endocrinology 101 111-119.
23. Lingohr MK, Briaud I, Dickson LM, McCuaig JF, Alarcon C, Wicksteed BL & Rhodes CJ 2006 Specific regulation of IRS-2 expression by glucose in rat primary pancreateic islet b-cells. Journal of Biological Chemistry 281 15884-15892. (Pubitemid 43848480)
24. Mabley JG, Belin V, John N & Green IC 1997 Insulin-like growth factor I reverses interleukin-1β inhibition of insulin secretion, induction of nitric oxide synthase and cytokine-mediated apoptosis in rat islets of Langerhans. FEBS Letters 417 235-238. (Pubitemid 27491740)
25. Maedler K, Spinas GA, Lehman R, Sergeev P,Weber M, Fontana A, Kaiser N & Donath MY 2001 Glucose induces β-cell apoptosis via upregulation of the Fas receptor in human islets. Diabetes 50 1683-1690. (Pubitemid 33641583)
26. Maedler K, Schumann DM, Sauter N, Ellingsgaard H, Bosco D, Baertschiger R, Iwakura Y, Oberholzer J,Wollheim CB, Gauthier BR et al. 2006 Low concentration of interleukin-1β induces FLICE-inhibitory protein-mediated β-cell proliferation in human pancreatic islets. Diabetes 55 2713-2722. (Pubitemid 44923669)
27. Mandrup-Poulsen T 1996 The role of interleukin-1 in the pathogenesis of insulin-dependent diabetes mellitus. Diabetologia 39 1005-1029.
28. Martin DM, Carlson R & Feldman EL 1993 Interferon-gamma inhibits DNA synthesis and insulin-like growth factor-II expression in human neuro-blastoma cells. Journal of Neuroscience Research 34 489-501. (Pubitemid 23110936)
29. Mathis D, Vence L & Benoist C 2001 β-Cell death during progression to diabetes. Nature 414 792-798.
30. Meier JJ, Butler AE, Saisho Y, Monchamp T, Galasso R, Bhushan A, Rizza RA & Butler PC 2008 β-Cell replication is the primary mechanism subserving the postnatal expansion of β-cell mass in humans. Diabetes 57 1584-1594.
31. Montanya E, Nacher V, Biarnés M & Soler J 2000 Linear correlation between β-cell mass and body weight throughout the lifespan in Lewis rats. Diabetes 49 1341-1346.
32. Montolio M, Biarnés M, Téllez N, Escoriza J, Soler J & Montanya E 2007 IL-1β and iNOS expression in early syngeneic islet transplantation. Journal of Endocrinology 192 171-179.
33. Nácher V, Raurell M, Merino JF, Aranda O, Soler J & Montana E 1996 β-Cell growth and mass are preserved in long-term syngeneic islet transplantation in streptozocin-induced diabetic Lewis rats. Diabetes 45 1541-1546. (Pubitemid 26357547)
34. Nir T, Melton DA & Dor Y 2007 Recovery from diabetes in mice by β-cell regeneration. Journal of Clinical Investigation 117 2553-2561. (Pubitemid 47494356)
35. Okada T, Liew CW, Hu J, Hinault C, Michael MD, Krtzfeldt J, Yin C, Holzenberger M, Stoffel M & Kulkarni RN 2007 Insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. PNAS 104 8977-8982. (Pubitemid 47175422)
36. Parnaud G, Bisco D, Berney T, Pattou F, Kerry-Conte J, Donath MY, Bruun C, Mandrup-Poulsen T, Billestrup N & Halban PA 2008 Proliferation of sorted human and rat β-cells. Diabetologia 51 91-100. (Pubitemid 50002201)
37. PersidskyMD& Baillie GS 1977 Fluorometric test of cell membrane integrity. Cryobiology 14 322-331.
38. Petrik J, Arany E, McDonald TJ & Hill DJ 1998 Apoptosis in the pancreatic islet cells of the neonatal rat is associated with a reduced expression of insulin-like growth factor II that may act as a survival factor. Endocrinology 139 2994-3004. (Pubitemid 28512413)
39. Petrik J, Pell JM, Arany E, McDonald TJ, Dean WL, ReikW& Hill DJ 1999a Overexpression of insulin-like growth factor-II in transgenic mice is associated with pancreatic islet cell hyperplasia. Endocrinology 140 2353-2363. (Pubitemid 30636477)
40. Petrik J, Reusens B, Arany E, Remacle C, Coelho C, Hoet JJ & Hill DJ 1999b A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 140 4861-4873. (Pubitemid 30666156)
41. Raile K, Berthold A, Banning U, Horn F, Pfeiffer G & Kiess W 2003 IGFs, basic FGF, and glucose modulate proliferation and apoptosis induced by IFNγ but not by IL-1β in rat INS-1E β-cells. Hormone and Metabolic Research 35 407-414. (Pubitemid 37378268)
42. Robitaille R, Dusseault J, Henley N, Rosenberg L & Hallé JP 2003 Insulin-like growth factor II allows prolonged blood glucose normalization with reduced islet cell mass transplantation. Endocrinology 144 3037-3045. (Pubitemid 36819906)
43. Saldeen J 2000 Cytokines induce both necrosis and apoptosis via a common Bcl-2-inhibitable pathway in rat insulin-producing cells. Endocrinology 141 2003-2010. (Pubitemid 32274349)
44. Scaglia L, Cahill CJ, Finegood DT & Bonner-Weir S 1997 Apotosis participates in the remodeling of the endocrine pancreas in the neonatal rat. Endocrinology 138 1736-1741. (Pubitemid 27137129)
45. Scarim AL, Heitmeier MR & Corbett JA 1997 Irreversible inhibition of metabolic function and islet destruction after a 36-hour exposure to interleukin-1β. Endocrinology 138 5301-5307.
46. Sjöholm Å 1991 Inhibition of fetal rat pancreatic β-cell replication by interleukin-1β in vitro is not mediated through pertussis toxin-sensitive G-proteins, a decrease in cyclic AMP, or protease activation. FEBS Letters 289 249-252.
47. Southern C, Schulster D & Green IC 1990 Inhibition of insulin secretion from rat islets of Langerhans by interleukin-6. An effect distinct from that of interleukin-1. Biochemical Journal 272 243-245.
48. Spinas GA, Palmer JP, Mandrup-Poulsen T, Andersen H, Nielsen JH & Nerup J 1988 The bimodal effect of interleukin 1 on rat pancreatic β-cells -stimulation followed by inhibition- depends upon dose, duration of exposure, and ambient glucose concentration. Acta Endocrinologica 119 307-311. (Pubitemid 18238834)
49. Swenne I 1982 The role of glucose in the in vitro regulation of cell cycle kinetics and proliferation of fetal pancreatic B-cells. Diabetes 31 754-760. (Pubitemid 12062863)
50. Téllez N, Montolio M, Biarnés M, Castaño E, Soler J & Montanya E 2005 Adenoviral overexpression of interleukin-1 receptor antagonist protein increases β-cell replication in rat pancreatic islets. Gene Therapy 12 120-128. (Pubitemid 40185915)
51. Téllez N, Montolio M, Estil.les E, Escoriza J, Soler J & Montanya E 2007 Adenoviral overproduction of interleukin-1 receptor antagonist increases β-cell replication and mass in syngeneically transplanted islets, and improves metabolic outcome. Diabetologia 50 602-611.
52. Vasavada RC, Gonzalez-Pertusa JA, Fujinaka Y, Fiaschi-Taesch N, Cozar-Castellano I & Garcia Ocaña A 2006 Growth factors and β-cell replication. International Journal of Biochemistry & Cell Biology 38 931-950.