Distinct subpopulations of FOXD1 stroma-derived cells regulate renal erythropoietin

Journal of Clinical Investigation

Volumn 126, Issue 5, 2016, Pages 1926-1938

  Kobayashi, Hanako ^a,b   Liu, Qingdu ^a,b   Binns, Thomas C ^b   Urrutia, Andres A ^b   Davidoff, Olena ^a,b   Kapitsinou, Pinelopi P ^b,h   Pfaff, Andrew S ^b   Olauson, Hannes ^c   Wernerson, Annika ^c,d   Fogo, Agnes B ^b   Fong, Guo Hua ^e   Gross, Kenneth W ^f   Haase, Volker H ^a,b,g  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c Division of Geriatric Medicine   (Sweden)

^d KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^e UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^f ROSWELL PARK CANCER INSTITUTE   (United States)

^g VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; ERYTHROPOIETIN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN FOXD1; PROTEIN HIF 2; PROTEIN PHD1; PROTEIN PHD2; PROTEIN PHD3; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; EGLN1 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXD1 PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; PHD1 PROTEIN, MOUSE; PHD3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LINEAGE; CELL SUBPOPULATION; HETEROZYGOSITY; HYPOXIA; KIDNEY INTERSTITIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; STROMA CELL; ANIMAL; BIOSYNTHESIS; GENETICS; KIDNEY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; VASCULARIZATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; ERYTHROPOIETIN; FORKHEAD TRANSCRIPTION FACTORS; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; KIDNEY; MICE; MICE, KNOCKOUT; PROCOLLAGEN-PROLINE DIOXYGENASE; STROMAL CELLS;

EID: 84988468588     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI83551     Document Type: Article

References (54)

1. Koury MJ, Haase VH. Anaemia in kidney disease: harnessing hypoxia responses for therapy. Nat Rev Nephrol. 2015;11(7):394-410.
2. Scortegagna M, Morris MA, Oktay Y, Bennett M, Garcia JA. The HIF family member EPAS1/ HIF-2α is required for normal hematopoiesis in mice. Blood. 2003;102(5):1634-1640.
3. Kapitsinou PP, et al. Hepatic HIF-2 regulates erythropoietic responses to hypoxia in renal anemia. Blood. 2010;116(16):3039-3048.
4. Semenza GL. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Annu Rev Pathol. 2014;9:47-71.
5. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30(4):393-402.
6. Koury ST, Bondurant MC, Koury MJ. Localization of erythropoietin synthesizing cells in murine kidneys by in situ hybridization. Blood. 1988;71(2):524-527.
7. Bachmann S, Le Hir M, Eckardt KU. Co-localization of erythropoietin mRNA and ecto-5?-nucleotidase immunoreactivity in peritubular cells of rat renal cortex indicates that fibroblasts produce erythropoietin. J Histochem Cytochem. 1993;41(3):335-341.
8. Obara N, et al. Repression via the GATA box is essential for tissue-specific erythropoietin gene expression. Blood. 2008;111(10):5223-5232.
9. Paliege A, et al. Hypoxia-inducible factor-2αexpressing interstitial fibroblasts are the only renal cells that express erythropoietin under hypoxia-inducible factor stabilization. Kidney Int. 2010;77(4):312-318.
10. Smith SW, Chand S, Savage CO. Biology of the renal pericyte. Nephrol Dial Transplant. 2012;27(6):2149-2155.
11. Gomez IG, Duffield JS. The FOXD1 lineage of kidney perivascular cells and myofibroblasts: functions and responses to injury. Kidney Int Suppl. 2014;4(1):26-33.
12. Koury ST, Koury MJ, Bondurant MC, Caro J, Graber SE. Quantitation of erythropoietin-producing cells in kidneys of mice by in situ hybridization: correlation with hematocrit, renal erythropoietin mRNA, and serum erythropoietin concentration. Blood. 1989;74(2):645-651.
13. Kaissling B, Spiess S, Rinne B, Le Hir M. Effects of anemia on morphology of rat renal cortex. Am J Physiol. 1993;264(4 pt 2):F608-F617.
14. Asada N, et al. Dysfunction of fibroblasts of extrarenal origin underlies renal fibrosis and renal anemia in mice. J Clin Invest. 2011;121(10):3981-3990.
15. Humphreys BD, et al. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol. 2010;176(1):85-97.
16. Kobayashi A, et al. Identification of a multipotent self-renewing stromal progenitor population during mammalian kidney organogenesis. Stem Cell Reports. 2014;3(4):650-662.
17. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007;45(9):593-605.
18. Zeigler BM, Vajdos J, Qin W, Loverro L, Niss K. A mouse model for an erythropoietin-deficiency anemia. Dis Model Mech. 2011;3(11-12):763-772.
19. Takeda K, et al. Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood. 2008;111(6):3229-3235.
20. Minamishima YA, et al. Somatic inactivation of the PHD2 prolyl hydroxylase causes polycythemia and congestive heart failure. Blood. 2008;111(6):3236-3244.
21. Minamishima YA, Kaelin WG Jr. Reactivation of hepatic EPO synthesis in mice after PHD loss. Science. 2010;329(5990):407.
22. Querbes W, et al. Treatment of erythropoietin deficiency in mice with systemically administered siRNA. Blood. 2012;120(9):1916-1922.
23. Tojo Y, et al. Hypoxia signaling cascade for erythropoietin production in hepatocytes. Mol Cell Biol. 2015;35(15):2658-2672.
24. Liu J, et al. Cell-specific translational profiling in acute kidney injury. J Clin Invest. 2014;124(3):1242-1254.
25. Pan X, et al. Isolation and characterization of renal erythropoietin-producing cells from genetically produced anemia mice. PLoS One. 2011;6(10):e25839.
26. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21(2):193-215.
27. Lin SL, Kisseleva T, Brenner DA, Duffield JS. Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol. 2008;173(6):1617-1627.
28. Souma T, et al. Erythropoietin synthesis in renal myofibroblasts is restored by activation of hypoxia signaling. J Am Soc Nephrol. 2016;27(2):428-438.
29. Souma T, et al. Plasticity of renal erythropoietinproducing cells governs fibrosis. J Am Soc Nephrol. 2013;24(10):1599-1616.
30. Blumberg A, Keller H, Marti HR. Effect of altitude on erythropoiesis and oxygen affinity in anaemic patients on maintenance dialysis. Eur J Clin Invest. 1973;3(2):93-97.
31. Bosman DR, et al. Erythropoietin response to hypoxia in patients with diabetic autonomic neuropathy and non-diabetic chronic renal failure. Diabet Med. 2002;19(1):65-69.
32. Bernhardt WM, et al. Inhibition of prolyl hydroxylases increases erythropoietin production in ESRD. J Am Soc Nephrol. 2010;21(12):2151-2156.
33. Brookhart MA, et al. The effect of altitude on dosing and response to erythropoietin in ESRD. J Am Soc Nephrol. 2008;19(7):1389-1395.
34. Fishbane S, Nissenson AR. The new FDA label for erythropoietin treatment: how does it affect hemoglobin target? Kidney Int. 2007;72(7):806-813.
35. Unger EF, Thompson AM, Blank MJ, Temple R. Erythropoiesis-stimulating agents - time for a reevaluation. N Engl J Med. 2010;362(3):189-192.
36. Vaziri ND, Zhou XJ. Potential mechanisms of adverse outcomes in trials of anemia correction with erythropoietin in chronic kidney disease. Nephrol Dial Transplant. 2009;24(4):1082-1088.
37. Weidemann A, et al. The glial cell response is an essential component of hypoxiainduced erythropoiesis in mice. J Clin Invest. 2009;119(11):3373-3383.
38. Rankin EB, et al. The HIF signaling pathway in osteoblasts directly modulates erythropoiesis through the production of EPO. Cell. 2012;149(1):63-74.
39. Kurt B, et al. Deletion of von Hippel-Lindau protein converts renin-producing cells into erythropoietin-producing cells. J Am Soc Nephrol. 2013;24(3):433-444.
40. Kurt B, Gerl K, Karger C, Schwarzensteiner I, Kurtz A. Chronic hypoxia-inducible transcription factor-2 activation stably transforms juxtaglomerular renin cells into fibroblast-like cells in vivo. J Am Soc Nephrol. 2015;26(3):587-596.
41. Kishore BK, Isaac J, Westenfelder C. Administration of poly-D-glutamic acid induces proliferation of erythropoietin-producing peritubular cells in rat kidney. Am J Physiol Renal Physiol. 2007;292(2):F749-F761.
42. Yamagishi S, et al. Vascular endothelial growth factor acts as a pericyte mitogen under hypoxic conditions. Lab Invest. 1999;79(4):501-509.
43. Rankin EB, et al. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest. 2007;117(4):1068-1077.
44. Kunze R, et al. Neuron-specific prolyl-4-hydroxylase domain 2 knockout reduces brain injury after transient cerebral ischemia. Stroke. 2012;43(10):2748-2756.
45. Appelhoff RJ, 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.
46. Minamishima YA, et al. A feedback loop involving the Phd3 prolyl hydroxylase tunes the mammalian hypoxic response in vivo. Mol Cell Biol. 2009;29(21):5729-5741.
47. Lubbers DW, Baumgartl H. Heterogeneities and profiles of oxygen pressure in brain and kidney as examples of the pO2 distribution in the living tissue. Kidney Int. 1997;51(2):372-380.
48. Takeda K, et al. Placental but not heart defects are associated with elevated hypoxia-inducible factor α levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol. 2006;26(22):8336-8346.
49. Gruber M, et al. Acute postnatal ablation of Hif-2α results in anemia. Proc Natl Acad Sci U S A. 2007;104(7):2301-2306.
50. Liu Q, Davidoff O, Niss K, Haase VH. Hypoxiainducible factor regulates hepcidin via erythropoietin-induced erythropoiesis. J Clin Invest. 2012;122(12):4635-4644.
51. Zhu X, Bergles DE, Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development. 2008;135(1):145-157.
52. Foo SS, et al. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell. 2006;124(1):161-173.
53. Kobayashi H, et al. Myeloid cell-derived hypoxiainducible factor attenuates inflammation in unilateral ureteral obstruction-induced kidney injury. J Immunol. 2012;188(10):5106-5115.
54. Wiesener MS, et al. Widespread hypoxiainducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J. 2003;17(2):271-273.