IRP1 regulates erythropoiesis and systemic iron homeostasis by controlling HIF2α mRNA translation

Blood

Volumn 122, Issue 9, 2013, Pages 1658-1669

  Wilkinson, Nicole ^a   Pantopoulos, Kostas ^a  

^a not available   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; FERROPORTIN; HEPCIDIN; HYPOXIA INDUCIBLE FACTOR 2ALPHA; IRON; IRON REGULATORY PROTEIN 1; IRON REGULATORY PROTEIN 2; MESSENGER RNA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ERYTHROPOIESIS; EXTRAMEDULLARY HEMATOPOIESIS; FEMALE; HEMOSIDEROSIS; HOMEOSTASIS; IRON DEPLETION; IRON METABOLISM; IRON RESPONSIVE ELEMENT; JUVENILE; MACROPHAGE; MALE; MOUSE; NONHUMAN; POLYCYTHEMIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY MECHANISM; RETICULOCYTOSIS; RNA TRANSLATION; SPLENOMEGALY;

EID: 84888037689     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-03-492454     Document Type: Article

References (48)

1. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell. 2012;148(3):399-408.
2. Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer. 2012;12(1):9-22.
3. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30(4):393-402.
4. Sanchez M, Galy B, Muckenthaler MU, Hentze MW. Iron-regulatory proteins limit hypoxia-inducible factor-2alpha expression in iron deficiency. Nat Struct Mol Biol. 2007;14(5):420-426.
5. Wang J, Pantopoulos K. Regulation of cellular iron metabolism. Biochem J. 2011;434(3):365-381.
6. Salahudeen AA, Thompson JW, Ruiz JC, et al. An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science. 2009;326(5953):722-726.
7. Vashisht AA, Zumbrennen KB, Huang X, et al. Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science. 2009;326(5953):718-721.
8. Meyron-Holtz EG, Ghosh MC, Rouault TA. Mammalian tissue oxygen levels modulate iron-regulatory protein activities in vivo. Science. 2004;306(5704):2087-2090.
9. Ganz T, Nemeth E. Hepcidin and iron homeostasis. Biochim Biophys Acta. 2012;1823(9):1434-1443.
10. Zimmer M, Ebert BL, Neil C, et al. Small-molecule inhibitors of HIF-2a translation link its 5'UTR iron-responsive element to oxygen sensing. Mol Cell. 2008;32(6):838-848.
11. Kapitsinou PP, Liu Q, Unger TL, et al. Hepatic HIF-2 regulates erythropoietic responses to hypoxia in renal anemia. Blood. 2010;116(16):3039- 3048.
12. Galy B, Ferring D, Hentze MW. Generation of conditional alleles of the murine Iron Regulatory Protein (IRP)-1 and -2 genes. Genesis. 2005;43(4):181-188.
13. Gkouvatsos K, Wagner J, Papanikolaou G, Sebastiani G, Pantopoulos K. Conditional disruption of mouse HFE2 gene: maintenance of systemic iron homeostasis requires hepatic but not skeletal muscle hemojuvelin. Hepatology. 2011;54(5):1800-1807.
14. Maffettone C, Chen G, Drozdov I, Ouzounis C, Pantopoulos K. Tumorigenic properties of iron regulatory protein 2 (IRP2) mediated by its specific 73-amino acids insert. PLoS ONE. 2010;5(4):e10163.
15. Gandin V, Miluzio A, Barbieri AM, Beugnet A, Kiyokawa H, Marchisio PC, Biffo S. Eukaryotic initiation factor 6 is rate-limiting in translation, growth and transformation. Nature. 2008;455(7213):684-688.
16. Nasr Z, Robert F, Porco JA Jr, Muller WJ, Pelletier J. eIF4F suppression in breast cancer affects maintenance and progression. Oncogene. 2013;32(7):861-871.
17. 4-induced liver fibrosis in Hjv-/- mice, associated with an oxidative burst and precocious profibrogenic gene expression. PLoS ONE. 2011;6(9):e25138.
18. Fillebeen C, Chahine D, Caltagirone A, Segal P, Pantopoulos K. A phosphomimetic mutation at Ser-138 renders iron regulatory protein 1 sensitive to iron-dependent degradation. Mol Cell Biol. 2003;23(19):6973-6981.
19. Paliege A, Rosenberger C, Bondke A, et al. Hypoxia-inducible factor-2alpha-expressing interstitial fibroblasts are the only renal cells that express erythropoietin under hypoxia-inducible factor stabilization. Kidney Int. 2010;77(4):312-318.
20. Meyron-Holtz EG, Ghosh MC, Iwai K, et al. Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J. 2004;23(2):386-395.
21. Ang SO, Chen H, Hirota K, et al. Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia. Nat Genet. 2002;32(4):614-621.
22. Hickey MM, Lam JC, Bezman NA, Rathmell WK, Simon MC. von Hippel-Lindau mutation in mice recapitulates Chuvash polycythemia via hypoxia-inducible factor-2alpha signaling and splenic erythropoiesis. J Clin Invest. 2007;117(12):3879-3889.
23. Gordeuk VR, Miasnikova GY, Sergueeva AI, et al. Chuvash polycythemia VHLR200W mutation is associated with down-regulation of hepcidin expression. Blood. 2011;118(19):5278-5282.
24. Percy MJ, Zhao Q, Flores A, et al. A family with erythrocytosis establishes a role for prolyl hydroxylase domain protein 2 in oxygen homeostasis. Proc Natl Acad Sci USA. 2006;103(3):654-659.
25. Percy MJ, Furlow PW, Beer PA, Lappin TR, McMullin MF, Lee FS. A novel erythrocytosis-associated PHD2 mutation suggests the location of a HIF binding groove. Blood. 2007;110(6):2193-2196.
26. Ladroue C, Carcenac R, Leporrier M, et al. PHD2 mutation and congenital erythrocytosis with paraganglioma. N Engl J Med. 2008;359(25):2685-2692.
27. Percy MJ, Furlow PW, Lucas GS, Li X, Lappin TR, McMullin MF, Lee FS. A gain-of-function mutation in the HIF2A gene in familial erythrocytosis. N Engl J Med. 2008;358(2):162-168.
28. Takeda K, Aguila HL, Parikh NS, et al. Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood. 2008;111(6):3229-3235.
29. Minamishima YA, Moslehi J, Bardeesy N, Cullen D, Bronson RT, Kaelin WG Jr. Somatic inactivation of the PHD2 prolyl hydroxylase causes polycythemia and congestive heart failure. Blood. 2008;111(6):3236-3244.
30. Laitala A, Aro E, Walkinshaw G, et al. Transmembrane prolyl 4-hydroxylase is a fourth prolyl 4-hydroxylase regulating EPO production and erythropoiesis. Blood. 2012;120(16):3336-3344.
31. Semenza GL, Traystman MD, Gearhart JD, Antonarakis SE. Polycythemia in transgenic mice expressing the human erythropoietin gene. Proc Natl Acad Sci USA. 1989;86(7):2301-2305.
32. Cooperman SS, Meyron-Holtz EG, Olivierre- Wilson H, Ghosh MC, McConnell JP, Rouault TA. Microcytic anemia, erythropoietic protoporphyria, and neurodegeneration in mice with targeted deletion of iron-regulatory protein 2. Blood. 2005;106(3):1084-1091.
33. Galy B, Ferring D, Minana B, et al. Altered body iron distribution and microcytosis in mice deficient in iron regulatory protein 2 (IRP2). Blood. 2005;106(7):2580-2589.
34. Chen OS, Blemings KP, Schalinske KL, Eisenstein RS. Dietary iron intake rapidly influences iron regulatory proteins, ferritin subunits and mitochondrial aconitase in rat liver. J Nutr. 1998;128(3):525-535.
35. Davis MR, Shawron KM, Rendina E, Peterson SK, Lucas EA, Smith BJ, Clarke SL. Hypoxia inducible factor-2α is translationally repressed in response to dietary iron deficiency in Sprague-Dawley rats. J Nutr. 2011;141(9):1590- 1596.
36. Mastrogiannaki M, Matak P, Mathieu JR, Delga S, Mayeux P, Vaulont S, Peyssonnaux C. Hepatic hypoxia-inducible factor-2 downregulates hepcidin expression in mice through an erythropoietin-mediated increase in erythropoiesis. Haematologica. 2012;97(6):827-834.
37. Liu Q, Davidoff O, Niss K, Haase VH. Hypoxia-inducible factor regulates hepcidin via erythropoietin-induced erythropoiesis. J Clin Invest. 2012;122(12):4635-4644.
38. Mastrogiannaki M, Matak P, Keith B, Simon MC, Vaulont S, Peyssonnaux C. HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. J Clin Invest. 2009;119(5):1159-1166.
39. Shah YM, Matsubara T, Ito S, Yim SH, Gonzalez FJ. Intestinal hypoxia-inducible transcription factors are essential for iron absorption following iron deficiency. Cell Metab. 2009;9(2):152-164.
40. Nicolas G, Chauvet C, Viatte L, et al. The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest. 2002;110(7):1037-1044.
41. Huang H, Constante M, Layoun A, Santos MM. Contribution of STAT3 and SMAD4 pathways to the regulation of hepcidin by opposing stimuli. Blood. 2009;113(15):3593-3599.
42. Tanno T, Bhanu NV, Oneal PA, et al. High levels of GDF15 in thalassemia suppress expression of the iron regulatory protein hepcidin. Nat Med. 2007;13(9):1096-1101.
43. Wilkinson N, Pantopoulos K. IRP1-/- mice exhibit defects in glucose metabolism and erythropoiesis. In: 4th Congress of the International BioIron Society abstract book; May 22-26, 2011; Vancouver, BC, Canada. 2011:93-94.
44. Lipiński P, Styś A, Starzyński RR. Molecular insights into the regulation of iron metabolism during the prenatal and early postnatal periods. Cell Mol Life Sci. 2013;70(1):23-38.
45. Ghosh MC, Zhang DL, Jeong SY, et al. Deletion of iron regulatory protein 1 causes polycythemia and pulmonary hypertension in mice through translational derepression of HIF2α. Cell Metab. 2013;17(2):271-281.
46. Anderson SA, Nizzi CP, Chang YI, et al. The IRP1-HIF-2α axis coordinates iron and oxygen sensing with erythropoiesis and iron absorption. Cell Metab. 2013;17(2):282-290.
47. Smith TG, Brooks JT, Balanos GM, et al. Mutation of von Hippel-Lindau tumour suppressor and human cardiopulmonary physiology. PLoS Med. 2006;3(7):e290.
48. Hickey MM, Richardson T, Wang T, et al. The von Hippel-Lindau Chuvash mutation promotes pulmonary hypertension and fibrosis in mice. J Clin Invest. 2010;120(3):827-839.