Deletion of iron regulatory protein 1 causes polycythemia and pulmonary hypertension in mice through translational derepression of HIF2α

Cell Metabolism

Volumn 17, Issue 2, 2013, Pages 271-281

  Ghosh, Manik C ^a   Zhang, De Liang ^a   Jeong, Suh Young ^a   Kovtunovych, Gennadiy ^a   Ollivierre Wilson, Hayden ^a   Noguchi, Audrey ^b   Tu, Tiffany ^a   Senecal, Thomas ^a   Robinson, Gabrielle ^a   Crooks, Daniel R ^a   Tong, Wing Hang ^a   Ramaswamy, Kavitha ^a   Singh, Anamika ^a   Graham, Brian B ^c   Tuder, Rubin M ^c   Yu, Zu Xi ^b   Eckhaus, Michael ^d   Lee, Jaekwon ^e   Springer, Danielle A ^b   Rouault, Tracey A ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 2ALPHA; IRON REGULATORY PROTEIN 1;

ABDOMINAL BLEEDING; ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; ENDOTHELIUM CELL; GENE DELETION; GENE TARGETING; HEMATOCRIT; IRON RESTRICTION; LUNG ALVEOLUS CELL; MOUSE; NONHUMAN; POLYCYTHEMIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; TRANSLATION REGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DIET; ENDOTHELIAL CELLS; ENDOTHELIN-1; ERYTHROPOIETIN; GASTROINTESTINAL HEMORRHAGE; GENE DELETION; HEMATOPOIESIS, EXTRAMEDULLARY; HYPERTENSION, PULMONARY; IRON; IRON REGULATORY PROTEIN 1; IRON REGULATORY PROTEIN 2; LONGEVITY; MICE; MODELS, BIOLOGICAL; NERVE DEGENERATION; ORGAN SPECIFICITY; POLYCYTHEMIA; PROTEIN BIOSYNTHESIS; TRANSCRIPTIONAL ACTIVATION;

EID: 84873338684     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.12.016     Document Type: Article

References (37)

1. A. Bigham, M. Bauchet, D. Pinto, X. Mao, J.M. Akey, R. Mei, S.W. Scherer, C.G. Julian, M.J. Wilson, and D. López Herráez Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data PLoS Genet. 6 2010 e1001116 10.1371/journal.pgen.1001116
2. J. Bond, D.P. Gale, T. Connor, S. Adams, J. de Boer, D.M. Gascoyne, O. Williams, P.H. Maxwell, and P.J. Ancliff Dysregulation of the HIF pathway due to VHL mutation causing severe erythrocytosis and pulmonary arterial hypertension Blood 117 2011 3699 3701
3. K. Brusselmans, V. Compernolle, M. Tjwa, M.S. Wiesener, P.H. Maxwell, D. Collen, and P. Carmeliet Heterozygous deficiency of hypoxia-inducible factor-2alpha protects mice against pulmonary hypertension and right ventricular dysfunction during prolonged hypoxia J. Clin. Invest. 111 2003 1519 1527
4. S.S. Cooperman, E.G. Meyron-Holtz, H. Olivierre-Wilson, M.C. Ghosh, J.P. McConnell, and T.A. Rouault Microcytic anemia, erythropoietic protoporphyria, and neurodegeneration in mice with targeted deletion of iron-regulatory protein 2 Blood 106 2005 1084 1091
5. J. Dupuy, A. Volbeda, P. Carpentier, C. Darnault, J.M. Moulis, and J.C. Fontecilla-Camps Crystal structure of human iron regulatory protein 1 as cytosolic aconitase Structure 14 2006 129 139
6. F. Formenti, D. Constantin-Teodosiu, Y. Emmanuel, J. Cheeseman, K.L. Dorrington, L.M. Edwards, S.M. Humphreys, T.R. Lappin, M.F. McMullin, and C.J. McNamara Regulation of human metabolism by hypoxia-inducible factor Proc. Natl. Acad. Sci. USA 107 2010 12722 12727
7. D.P. Gale, S.K. Harten, C.D. Reid, E.G. Tuddenham, and P.H. Maxwell Autosomal dominant erythrocytosis and pulmonary arterial hypertension associated with an activating HIF2 alpha mutation Blood 112 2008 919 921
8. B. Galy, D. Ferring, B. Minana, O. Bell, H.G. Janser, M. Muckenthaler, K. Schümann, and M.W. Hentze Altered body iron distribution and microcytosis in mice deficient in iron regulatory protein 2 (IRP2) Blood 106 2005 2580 2589
9. M.C. Ghosh, W.H. Tong, D. Zhang, H. Ollivierre-Wilson, A. Singh, M.C. Krishna, J.B. Mitchell, and T.A. Rouault Tempol-mediated activation of latent iron regulatory protein activity prevents symptoms of neurodegenerative disease in IRP2 knockout mice Proc. Natl. Acad. Sci. USA 105 2008 12028 12033
10. B.B. Graham, M.M. Mentink-Kane, H. El-Haddad, S. Purnell, L. Zhang, A. Zaiman, E.F. Redente, D.W. Riches, P.M. Hassoun, and A. Bandeira Schistosomiasis-induced experimental pulmonary hypertension: role of interleukin-13 signaling Am. J. Pathol. 177 2010 1549 1561
11. M.W. Hentze, M.U. Muckenthaler, B. Galy, and C. Camaschella Two to tango: regulation of Mammalian iron metabolism Cell 142 2010 24 38
12. M.M. Hickey, J.C. Lam, N.A. Bezman, W.K. Rathmell, and M.C. Simon von Hippel-Lindau mutation in mice recapitulates Chuvash polycythemia via hypoxia-inducible factor-2 alpha signaling and splenic erythropoiesis J. Clin. Invest. 117 2007 3879 3889
13. M.M. Hickey, T. Richardson, T. Wang, M. Mosqueira, E. Arguiri, H. Yu, Q.C. Yu, C.C. Solomides, E.E. Morrisey, and T.S. Khurana The von Hippel-Lindau Chuvash mutation promotes pulmonary hypertension and fibrosis in mice J. Clin. Invest. 120 2010 827 839
14. S.Y. Jeong, and S. David Age-related changes in iron homeostasis and cell death in the cerebellum of ceruloplasmin-deficient mice J. Neurosci. 26 2006 9810 9819
15. W.G. Kaelin Jr., and P.J. Ratcliffe Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway Mol. Cell 30 2008 393 402
16. H. Kim, H.Y. Son, S.M. Bailey, and J. Lee Deletion of hepatic Ctr1 reveals its function in copper acquisition and compensatory mechanisms for copper homeostasis Am. J. Physiol. Gastrointest. Liver Physiol. 296 2009 G356 G364
17. T. LaVaute, S. Smith, S. Cooperman, K. Iwai, W. Land, E. Meyron-Holtz, S.K. Drake, G. Miller, M. Abu-Asab, and M. Tsokos Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice Nat. Genet. 27 2001 209 214
18. D.G. MacArthur, S. Balasubramanian, A. Frankish, N. Huang, J. Morris, K. Walter, L. Jostins, L. Habegger, J.K. Pickrell, S.B. Montgomery 1000 Genomes Project Consortium A systematic survey of loss-of-function variants in human protein-coding genes Science 335 2012 823 828
19. A.J. Majmundar, W.J. Wong, and M.C. Simon Hypoxia-inducible factors and the response to hypoxic stress Mol. Cell 40 2010 294 309
20. E.G. Meyron-Holtz, M.C. Ghosh, K. Iwai, T. LaVaute, X. Brazzolotto, U.V. Berger, W. Land, H. Ollivierre-Wilson, A. Grinberg, P. Love, and T.A. Rouault Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis EMBO J. 23 2004 386 395
21. E.G. Meyron-Holtz, M.C. Ghosh, and T.A. Rouault Mammalian tissue oxygen levels modulate iron-regulatory protein activities in vivo Science 306 2004 2087 2090
22. X. Pan, N. Suzuki, I. Hirano, S. Yamazaki, N. Minegishi, and M. Yamamoto Isolation and characterization of renal erythropoietin-producing cells from genetically produced anemia mice PLoS ONE 6 2011 e25839 10.1371/journal.pone. 0025839
23. M.J. Percy, Q. Zhao, A. Flores, C. Harrison, T.R. Lappin, P.H. Maxwell, M.F. McMullin, and F.S. Lee A family with erythrocytosis establishes a role for prolyl hydroxylase domain protein 2 in oxygen homeostasis Proc. Natl. Acad. Sci. USA 103 2006 654 659
24. T.A. Rouault The role of iron regulatory proteins in mammalian iron homeostasis and disease Nat. Chem. Biol. 2 2006 406 414
25. C.A. Sable, Z.Y. Aliyu, N. Dham, M. Nouraie, V. Sachdev, S. Sidenko, G.Y. Miasnikova, L.A. Polyakova, A.I. Sergueeva, and D.J. Okhotin Pulmonary artery pressure and iron deficiency in patients with upregulation of hypoxia sensing due to homozygous VHL(R200W) mutation (Chuvash polycythemia) Haematologica 97 2012 193 200
26. A.A. Salahudeen, J.W. Thompson, J.C. Ruiz, H.W. Ma, L.N. Kinch, Q. Li, N.V. Grishin, and R.K. Bruick An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis Science 326 2009 722 726
27. M. Sanchez, B. Galy, M.U. Muckenthaler, and M.W. Hentze Iron-regulatory proteins limit hypoxia-inducible factor-2alpha expression in iron deficiency Nat. Struct. Mol. Biol. 14 2007 420 426
28. G.L. Semenza Hypoxia-inducible factors in physiology and medicine Cell 148 2012 399 408
29. D. Shao, J.E. Park, and S.J. Wort The role of endothelin-1 in the pathogenesis of pulmonary arterial hypertension Pharmacol. Res. 63 2011 504 511
30. S.R. Smith, M.C. Ghosh, H. Ollivierre-Wilson, W. Hang Tong, and T.A. Rouault Complete loss of iron regulatory proteins 1 and 2 prevents viability of murine zygotes beyond the blastocyst stage of embryonic development Blood Cells Mol. Dis. 36 2006 283 287
31. T.G. Smith, J.T. Brooks, G.M. Balanos, T.R. Lappin, D.M. Layton, D.L. Leedham, C. Liu, P.H. Maxwell, M.F. McMullin, and C.J. McNamara Mutation of the von Hippel-Lindau gene alters human cardiopulmonary physiology Adv. Exp. Med. Biol. 605 2008 51 56
32. M. Sobczak, J. Dargatz, and M. Chrzanowska-Wodnicka Isolation and culture of pulmonary endothelial cells from neonatal mice J. Vis. Exp. 46 2010 2316 10.3791/2316
33. E. Thorin, and M. Clozel The cardiovascular physiology and pharmacology of endothelin-1 Adv. Pharmacol. 60 2010 1 26
34. A.A. Vashisht, K.B. Zumbrennen, X. Huang, D.N. Powers, A. Durazo, D. Sun, N. Bhaskaran, A. Persson, M. Uhlen, and O. Sangfelt Control of iron homeostasis by an iron-regulated ubiquitin ligase Science 326 2009 718 721
35. W.E. Walden, A.I. Selezneva, J. Dupuy, A. Volbeda, J.C. Fontecilla-Camps, E.C. Theil, and K. Volz Structure of dual function iron regulatory protein 1 complexed with ferritin IRE-RNA Science 314 2006 1903 1908
36. X. Yi, Y. Liang, E. Huerta-Sanchez, X. Jin, Z.X. Cuo, J.E. Pool, X. Xu, H. Jiang, N. Vinckenbosch, and T.S. Korneliussen Sequencing of 50 human exomes reveals adaptation to high altitude Science 329 2010 75 78
37. M. Zimmer, B.L. Ebert, C. Neil, K. Brenner, I. Papaioannou, A. Melas, N. Tolliday, J. Lamb, K. Pantopoulos, T. Golub, and O. Iliopoulos Small-molecule inhibitors of HIF-2a translation link its 5'UTR iron-responsive element to oxygen sensing Mol. Cell 32 2008 838 848