Prolyl-4-hydroxylase 2 and 3 coregulate murine erythropoietin in brain pericytes

Blood

Volumn 128, Issue 21, 2016, Pages 2550-2560

  Urrutia, Andres A ^a   Afzal, Aqeela ^a   Nelson, Jacob ^a   Davidoff, Olena ^a,b   Gross, Kenneth W ^c   Haase, Volker H ^a,b,d  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; ERYTHROPOIETIN; MOLECULAR MARKER; NEURAL GLIAL ANTIGEN 2; OXYGEN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL 4 HYDROXYLASE 2; PROLYL 4 HYDROXYLASE 3; UNCLASSIFIED DRUG; EGLN1 PROTEIN, MOUSE; HIF-2 PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; PHD3 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN HYPOXIA; BRAIN PERICYTE; CONTROLLED STUDY; FEMALE; GENE TARGETING; GENETIC TRANSCRIPTION; HORMONE SYNTHESIS; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; ANIMAL; BIOSYNTHESIS; BRAIN; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PERICYTE; TRANSGENIC MOUSE;

ANIMALS; BRAIN; ERYTHROPOIETIN; GENE EXPRESSION REGULATION; HYPOXIA, BRAIN; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; MICE; MICE, TRANSGENIC; PERICYTES; PROCOLLAGEN-PROLINE DIOXYGENASE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 85014989961     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-05-713545     Document Type: Article

References (67)

1. Franke K, Gassmann M, Wielockx B. Erythrocytosis: the HIF pathway in control. Blood. 2013;122(7):1122-1128.
2. Koury MJ, Haase VH. Anaemia in kidney disease: harnessing hypoxia responses for therapy. Nat Rev Nephrol. 2015;11(7):394-410.
3. Obara N, Suzuki N, Kim K, Nagasawa T, Imagawa S, Yamamoto M. Repression via the GATA box is essential for tissue-specific erythropoietin gene expression. Blood. 2008;111(10):5223-5232.
4. Kobayashi H, Liu Q, Binns TC, et al. Distinct subpopulations of FOXD1 stroma-derived cells regulate renal erythropoietin. J Clin Invest. 2016;126(5):1926-1938.
5. Asada N, Takase M, Nakamura J, et al. Dysfunction of fibroblasts of extrarenal origin underlies renal fibrosis and renal anemia in mice. J Clin Invest. 2011;121(10):3981-3990.
6. Marti HH, Wenger RH, Rivas LA, et al. Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci. 1996;8(4):666-676.
7. Jelkmann W. Erythropoietin after a century of research: younger than ever. Eur J Haematol. 2007;78(3):183-205.
8. Minamishima YA, Kaelin WG Jr. Reactivation of hepatic EPO synthesis in mice after PHD loss. Science. 2010;329(5990):407.
9. Haase VH. Regulation of erythropoiesis by hypoxia-inducible factors. Blood Rev. 2013;27(1):41-53.
10. Tojo Y, Sekine H, Hirano I, et al. Hypoxia signaling cascade for erythropoietin production in hepatocytes. Mol Cell Biol. 2015;35(15):2658-2672.
11. Bernaudin M, Marti HH, Roussel S, et al. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab. 1999;19(6):643-651.
12. Bernaudin M, Bellail A, Marti HH, et al. Neurons and astrocytes express EPO mRNA: oxygen-sensing mechanisms that involve the redox-state of the brain. Glia. 2000;30(3):271-278.
13. Weidemann A, Kerdiles YM, Knaup KX, et al. The glial cell response is an essential component of hypoxia-induced erythropoiesis in mice. J Clin Invest. 2009;119(11):3373-3383.
14. Winkler EA, Bell RD, Zlokovic BV. Central nervous system pericytes in health and disease. Nat Neurosci. 2011;14(11):1398-1405.
15. Zhu X, Bergles DE, Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development. 2008;135(1):145-157.
16. Hill RA, Tong L, Yuan P, Murikinati S, Gupta S, Grutzendler J. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron. 2015;87(1):95-110.
17. Hartmann DA, Underly RG, Grant RI, Watson AN, Lindner V, Shih AY. Pericyte structure and distribution in the cerebral cortex revealed by high-resolution imaging of transgenic mice. Neurophotonics. 2015;2(4):041402.
18. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21(2):193-215.
19. Simon C, Lickert H, Götz M, Dimou L. Sox10-iCreERT2 : a mouse line to inducibly trace the neural crest and oligodendrocyte lineage. Genesis. 2012;50(6):506-515.
20. Mikawa T, Gourdie RG. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol. 1996;174(2):221-232.
21. Wilm B, Ipenberg A, Hastie ND, Burch JB, Bader DM. The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development. 2005;132(23):5317-5328.
22. Que J, Wilm B, Hasegawa H, Wang F, Bader D, Hogan BL. Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc Natl Acad Sci USA. 2008;105(43):16626-16630.
23. Asahina K, Zhou B, Pu WT, Tsukamoto H. Septum transversum-derived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology. 2011;53(3):983-995.
24. Scortegagna M, Morris MA, Oktay Y, Bennett M, Garcia JA. The HIF family member EPAS1/HIF-2alpha is required for normal hematopoiesis in mice. Blood. 2003;102(5):1634-1640.
25. Rankin EB, Biju MP, Liu Q, et al. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest. 2007;117(4):1068-1077.
26. 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.
27. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30(4):393-402.
28. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE. 2005;2005(306):re12.
29. Prabhakar NR, Semenza GL. Oxygen sensing and homeostasis. Physiology (Bethesda). 2015;30(5):340-348.
30. Epstein AC, Gleadle JM, McNeill LA, et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell. 2001;107(1):43-54.
31. Jaakkola P, Mole DR, Tian YM, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 2001;292(5516):468-472.
32. Ivan M, Kondo K, Yang H, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001;292(5516):464-468.
33. Hon WC, Wilson MI, Harlos K, et al. Structural basis for the recognition of hydroxyproline in HIF-1 alpha by pVHL. Nature. 2002;417(6892):975-978.
34. Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol. 2006;26(22):8336-8346.
35. 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.
36. 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.
37. Farsijani NM, Liu Q, Kobayashi H, et al. Renal epithelium regulates erythropoiesis via HIF-dependent suppression of erythropoietin. J Clin Invest. 2016;126(4):1425-1437.
38. Stallcup WB. The NG2 proteoglycan: past insights and future prospects. J Neurocytol. 2002;31(6-7):423-435.
39. Ozerdem U, Grako KA, Dahlin-Huppe K, Monosov E, Stallcup WB. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn. 2001;222(2):218-227.
40. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci. 2009;10(1):9-22.
41. Tan CC, Eckardt KU, Firth JD, Ratcliffe PJ. Feedback modulation of renal and hepatic erythropoietin mRNA in response to graded anemia and hypoxia. Am J Physiol. 1992;263(3 Pt 2):F474-F481.
42. Kunisaki Y, Bruns I, Scheiermann C, et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature. 2013;502(7473):637-643.
43. Nishiyama A, Suzuki R, Zhu X. NG2 cells (polydendrocytes) in brain physiology and repair. Front Neurosci. 2014;8:133.
44. Winkler EA, Bell RD, Zlokovic BV. Pericyte-specific expression of PDGF beta receptor in mouse models with normal and deficient PDGF beta receptor signaling. Mol Neurodegener. 2010;5:32.
45. Hall CN, Reynell C, Gesslein B, et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature. 2014;508(7494):55-60.
46. Rabie T, Kunze R, Marti HH. Impaired hypoxic response in senescent mouse brain. Int J Dev Neurosci. 2011;29(6):655-661.
47. Takeda K, Aguila HL, Parikh NS, et al. Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood. 2008;111(6):3229-3235.
48. Franke K, Kalucka J, Mamlouk S, et al. HIF-1α is a protective factor in conditional PHD2-deficient mice suffering from severe HIF-2α-induced excessive erythropoiesis. Blood. 2013;121(8):1436-1445.
49. Appelhoff RJ, Tian YM, Raval RR, et al. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem. 2004;279(37):38458-38465.
50. Minamishima YA, Moslehi J, Padera RF, Bronson RT, Liao R, Kaelin WG Jr. A feedback loop involving the Phd3 prolyl hydroxylase tunes the mammalian hypoxic response in vivo. Mol Cell Biol. 2009;29(21):5729-5741.
51. Brines ML, Ghezzi P, Keenan S, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA. 2000;97(19):10526-10531.
52. Ehrenreich H, Degner D, Meller J, et al. Erythropoietin: a candidate compound for neuroprotection in schizophrenia. Mol Psychiatry. 2004;9(1):42-54.
53. Brines M, Cerami A. Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci. 2005;6(6):484-494.
54. Chavez JC, Baranova O, Lin J, Pichiule P. The transcriptional activator hypoxia inducible factor 2 (HIF-2/EPAS-1) regulates the oxygen-dependent expression of erythropoietin in cortical astrocytes. J Neurosci. 2006;26(37):9471-9481.
55. Daneman R, Zhou L, Kebede AA, Barres BA. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature. 2010;468(7323):562-566.
56. Armulik A, Genové G,Mäe M, et al. Pericytes regulate the blood-brain barrier. Nature. 2010;468(7323):557-561.
57. Rasmussen P, Nordsborg N, Taudorf S, et al. Brain and skin do not contribute to the systemic rise in erythropoietin during acute hypoxia in humans. FASEB J. 2012;26(5):1831-1834.
58. Ganong WF. Circumventricular organs: definition and role in the regulation of endocrine and autonomic function. Clin Exp Pharmacol Physiol. 2000;27(5-6):422-427.
59. Bauer AT, Bürgers HF, Rabie T, Marti HH. Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J Cereb Blood Flow Metab. 2010;30(4):837-848.
60. Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain. 2002;125(Pt 11):2549-2557.
61. Souma T, Nezu M, Nakano D, et al. Erythropoietin Synthesis in Renal Myofibroblasts Is Restored by Activation of Hypoxia Signaling. J Am Soc Nephrol. 2016;27(2):428-438.
62. Pietras A, Gisselsson D, Ora I, et al. High levels of HIF-2alpha highlight an immature neural crest-like neuroblastoma cell cohort located in a perivascular niche. J Pathol. 2008;214(4):482-488.
63. Pietras A, Hansford LM, Johnsson AS, et al. HIF-2alpha maintains an undifferentiated state in neural crest-like human neuroblastoma tumor-initiating cells. Proc Natl Acad Sci USA. 2009;106(39):16805-16810.
64. 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.
65. Albiero E, Ruggeri M, Fortuna S, et al. Isolated erythrocytosis: study of 67 patients and identification of three novel germ-line mutations in the prolyl hydroxylase domain protein 2 (PHD2) gene. Haematologica. 2012;97(1):123-127.
66. Lorenzo FR, Huff C, Myllymäki M, et al. A genetic mechanism for Tibetan high-altitude adaptation. Nat Genet. 2014;46(9):951-956.
67. Bigham AW, Lee FS. Human high-altitude adaptation: forward genetics meets the HIF pathway. Genes Dev. 2014;28(20):2189-2204.