Oxygen tension regulates pancreatic β-cell differentiation through hypoxia-inducible factor 1β

Diabetes

Volumn 59, Issue 3, 2010, Pages 662-669

  Heinis, Mylène ^a   Simon, Marie Thérèse ^a   Ilc, Karine ^b   Mazure, Nathalie M ^b   Pouysségur, Jacques ^b   Scharfmann, Raphael ^a   Duvillié, Bertrand ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HES1 PROTEIN, RAT; HIF1A PROTEIN, RAT; HOMEODOMAIN PROTEIN; NERVE PROTEIN; NEUROG3 PROTEIN, RAT; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL HYPOXIA; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION; NONHUMAN; OXYGEN TENSION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ANOXIA; CYTOLOGY; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; ORGAN CULTURE TECHNIQUE; PANCREAS ISLET; PATHOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; RAT; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; NERVE TISSUE PROTEINS; ORGAN CULTURE TECHNIQUES; OXYGEN; PREGNANCY; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION;

EID: 77950344913     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0891     Document Type: Article

References (57)

1. Semenza GL. Life with oxygen. Science 2007;318:62-64
2. Semenza GL. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr Opin Genet Dev 1998;8:588-594 (Pubitemid 28477364)
3. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr: HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001;292: 464-468
4. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001;292: 468-472
5. Holmquist-Mengelbier L, Fredlund E, Lofstedt T, Noguera R, Navarro S, Nilsson H, Pietras A, Vallon-Christersson J, Borg A, Gradin K, Poellinger L, Pahlman S. Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell 2006;10:413-423
6. Rosenberger C, Mandriota S, Jurgensen JS, Wiesener MS, Horstrup JH, Frei U, Ratcliffe PJ, Maxwell PH, Bachmann S, Eckardt KU. Expression of hypoxia-inducible factor-1alpha and -2alpha in hypoxic and ischemic rat kidneys. J Am Soc Nephrol 2002;13:1721-1732
7. Tian H, McKnight SL, Russell DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev 1997;11:72-82 (Pubitemid 27043825)
8. Berra E, Ginouves A, Pouyssegur J. The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep 2006;7:41-45
9. Ginouves A, Ilc K, Macias N, Pouyssegur J, Berra E. PHDs overactivation during chronic hypoxia "desensitizes" HIFalpha and protects cells from necrosis. Proc Natl Acad Sci U S A 2008;105:4745-4750
10. Simon MC, Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 2008;9:285-296 (Pubitemid 351430845)
11. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 2005;9:617-628
12. Lin Q, Lee YJ, Yun Z. Differentiation arrest by hypoxia. J Biol Chem 2006;281:30678-30683
13. Diez H, Fischer A, Winkler A, Hu CJ, Hatzopoulos AK, Breier G, Gessler M. Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Exp Cell Res 2007;313: 1-9 (Pubitemid 44958449)
14. Deutsch G, Jung J, Zheng M, Lora J, Zaret KS. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 2001;128:871-881 (Pubitemid 32288198)
15. Hebrok M, Kim SK, Melton DA. Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes Dev 1998;12:1705-1713 (Pubitemid 28299520)
16. Kim SK, Hebrok M, Melton DA. Pancreas development in the chick embryo. Cold Spring Harb Symp Quant Biol 1997;62:377-383
17. Lammert E, Cleaver O, Melton D. Induction of pancreatic differentiation by signals from blood vessels. Science 2001;294:564-567 (Pubitemid 32999547)
18. Scharfmann R. Control of early development of the pancreas in rodents and humans: implications of signals from the mesenchyme. Diabetologia 2000;43:1083-1092
19. Ahlgren U, Jonsson J, Edlund H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 1996;122:1409-1416 (Pubitemid 26159631)
20. Collombat P, Hecksher-Sorensen J, Serup P, Mansouri A. Specifying pancreatic endocrine cell fates. Mech Dev 2006;123:501-512 (Pubitemid 44176347)
21. Gradwohl G, Dierich A, LeMeur M, Guillemot F. Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 2000;97:1607-1611 (Pubitemid 30118489)
22. Gittes GK, Galante PE, Hanahan D, Rutter WJ, Debase HT. Lineage-specific morphogenesis in the developing pancreas: role of mesenchymal factors. Development 1996;122:439-447 (Pubitemid 26054133)
23. Miralles F, Czernichow P, Scharfmann R. Follistatin regulates the relative proportions of endocrine versus exocrine tissue during pancreatic development. Development 1998;125:1017-1024 (Pubitemid 28171196)
24. Attali M, Stetsyuk V, Basmaciogullari A, Aiello V, Zanta-Boussif MA, Duvillie B, Scharfmann R. Control of β-cell differentiation by the pancreatic mesenchyme. Diabetes 2007;56:1248-1258 (Pubitemid 46715605)
25. Jensen J, Pedersen EE, Galante P, Hald J, Heller RS, Ishibashi M, Kageyama R, Guillemot F, Serup P, Madsen OD. Control of endodermal endocrine development by Hes-1. Nat Genet 2000;24:36-44
26. Duvillie B, Attali M, Aiello V, Quemeneur E, Scharfmann R. Label-retaining cells in the rat pancreas: location and differentiation potential in vitro. Diabetes 2003;52:2035-2042 (Pubitemid 36919796)
27. Guillemain G, Filhoulaud G, Da Silva-Xavier G, Rutter GA, Scharfmann R. Glucose is necessary for embryonic pancreatic endocrine cell differentiation. J Biol Chem 2007;282:15228-15237 (Pubitemid 47093387)
28. Irwin R, LaPres JJ, Kinser S, McCabe LR. Prolyl-hydroxylase inhibition and HIF activation in osteoblasts promotes an adipocytic phenotype. J Cell Biochem 2007;100:762-772 (Pubitemid 46180537)
29. Baader E, Tschank G, Baringhaus KH, Burghard H, Gunzler V. Inhibition of prolyl 4-hydroxylase by oxalyl amino acid derivatives in vitro, in isolated microsomes and in embryonic chicken tissues. Biochem J 1994;300:525-530 (Pubitemid 24167913)
30. McCaffrey TA, Pomerantz KB, Sanborn TA, Spokojny AM, Du B, Park MH, Folk JE, Lamberg A, Kivirikko KI, Falcone DJ, et al. Specific inhibition of eIF-5A and collagen hydroxylation by a single agent: antiproliferative and fibrosuppressive effects on smooth muscle cells from human coronary arteries. J Clin Invest 1995;95:446-455
31. Warnecke C, Griethe W, Weidemann A, Jurgensen JS, Willam C, Bachmann S, Ivashchenko Y, Wagner I, Frei U, Wiesener M, Eckardt KU. Activation of the hypoxia-inducible factor-pathway and stimulation of angiogenesis by application of prolyl hydroxylase inhibitors. Faseb J 2003;17:1186-1188
32. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. Embo J 1999;18:2196-2207
33. Hald J, Hjorth JP, German MS, Madsen OD, Serup P, Jensen J. Activated Notch1 prevents differentiation of pancreatic acinar cells and attenuate endocrine development. Dev Biol 2003;260:426-437
34. Ahnfelt-Ronne J, Hald J, Bodker A, Yassin H, Serup P, Hecksher-Sorensen J. Preservation of proliferating pancreatic progenitor cells by Delta-Notch signaling in the embryonic chicken pancreas. BMC Dev Biol 2007;7:63
35. Duvillie B, Attali M, Bounacer A, Ravassard P, Basmaciogullari A, Scharfmann R. The mesenchyme controls the timing of pancreatic β-cell differentiation. Diabetes 2006;55:582-589
36. Brahimi-Horn MC, Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett 2007;581:3582-3591
37. Cantley J, Selman C, Shukla D, Abramov AY, Forstreuter F, Esteban MA, Claret M, Lingard SJ, Clements M, Harten SK, Asare-Anane H, Batterham RL, Herrera PL, Persaud SJ, Duchen MR, Maxwell PH, Withers DJ. Deletion of the von Hippel-Lindau gene in pancreatic beta cells impairs glucose homeostasis in mice. J Clin Invest 2009;119:125-135
38. Flamme I, Frohlich T, von Reutern M, Kappel A, Damert A, Risau W. HRF, a putative basic helix-loop-helix-PAS-domain transcription factor is closely related to hypoxia-inducible factor-1 alpha and developmentally expressed in blood vessels. Mech Dev 1997;63:51-60
39. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci U S A 1997;94:4273-4278
40. Yun Z, Maecker HL, Johnson RS, Giaccia AJ. Inhibition of PPAR gamma 2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev Cell 2002;2:331-341
41. Yochim JM, Mitchell JA. Intrauterine oxygen tension in the rat during progestation: its possible relation to carbohydrate metabolism and the regulation of nidation. Endocrinology 1968;83:706-713
42. Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992;80:283-285
43. Fraker CA, Alvarez S, Papadopoulos P, Giraldo J, Gu W, Ricordi C, Inverardi L, Dominguez-Bendala J. Enhanced oxygenation promotes beta-cell differentiation in vitro. Stem Cells 2007;25:3155-3164
44. Provot S, Zinyk D, Gunes Y, Kathri R, Le Q, Kronenberg HM, Johnson RS, Longaker MT, Giaccia AJ, Schipani E. Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development. J Cell Biol 2007;177:451-464
45. Gunton JE, Kulkarni RN, Yim S, Okada T, Hawthorne WJ, Tseng YH, Roberson RS, Ricordi C, O'Connell PJ, Gonzalez FJ, Kahn CR. Loss of ARNT/HIF1beta mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 2005;122:337-349
46. Puri S, Cano DA, Hebrok M. A role for von Hippel-Lindau protein in pancreatic β-cell function. Diabetes 2009;58:433-441
47. Zehetner J, Danzer C, Collins S, Eckhardt K, Gerber PA, Ballschmieter P, Galvanovskis J, Shimomura K, Ashcroft FM, Thorens B, Rorsman P, Krek W. PVHL is a regulator of glucose metabolism and insulin secretion in pancreatic beta cells. Genes Dev 2008;22:3135-3146
48. Bhushan A, Itoh N, Kato S, Thiery JP, Czernichow P, Bellusci S, Scharfmann R. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001;128:5109-5117
49. Miralles F, Czernichow P, Ozaki K, Itoh N, Scharfmann R. Signaling through fibroblast growth factor receptor 2b plays a key role in the development of the exocrine pancreas. Proc Natl Acad Sci U S A 1999;96:6267-6272
50. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002;129:2447-2457
51. Dahlqvist C, Blokzijl A, Chapman G, Falk A, Dannaeus K, Ibanez CF, Lendahl U. Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 2003;130:6089-6099
52. Cras-Meneur C, Li L, Kopan R, Permutt MA. Presenilins, Notch dose control the fate of pancreatic endocrine progenitors during a narrow developmental window. Genes Dev 2009;23:2088-2101
53. Miettinen PJ, Huotari M, Koivisto T, Ustinov J, Palgi J, Rasilainen S, Lehtonen E, Keski-Oja J, Otonkoski T. Impaired migration and delayed differentiation of pancreatic islet cells in mice lacking EGF-receptors. Development 2000;127:2617-2627
54. Kritzik MR, Krahl T, Good A, Gu D, Lai C, Fox H, Sarvetnick N. Expression of ErbB receptors during pancreatic islet development and regrowth. J Endocrinol 2000;165:67-77
55. Cras-Meneur C, Elghazi L, Czernichow P, Scharfmann R. Epidermal growth factor increases undifferentiated pancreatic embryonic cells in vitro: a balance between proliferation and differentiation. Diabetes 2001;50:1571-1579
56. Miralles F, Lamotte L, Couton D, Joshi RL. Interplay between FGF10 and Notch signalling is required for the self-renewal of pancreatic progenitors. Int J Dev Biol 2006;50:17-26
57. Cejudo-Martin P, Johnson RS. A new notch in the HIF belt: how hypoxia impacts differentiation. Dev Cell 2005;9:575-576