Erythropoietin induces bone marrow and plasma fibroblast growth factor 23 during acute kidney injury

Kidney International

Volumn 93, Issue 5, 2018, Pages 1131-1141

  Toro, Luis ^a,b   Barrientos, Víctor ^a,c   León, Pablo ^a   Rojas, Macarena ^a   Gonzalez, Magdalena ^a   González Ibáñez, Alvaro ^c,d   Illanes, Sebastián ^e   Sugikawa, Keigo ^f   Abarzúa, Néstor ^a   Bascuñán, César ^a   Arcos, Katherine ^a   Fuentealba, Carlos ^a   Tong, Ana María ^b   Elorza, Alvaro A ^c,d   Pinto, María Eugenia ^b   Alzamora, Rodrigo ^a,g   Romero, Carlos ^b   Michea, Luis ^a,b,c  

^a UNIVERSITY OF CHILE   (Chile)

^b HOSPITAL CLÍNICO UNIVERSIDAD DE CHILE   (Chile)

^c Pontificia Universidad Católica de Chile   (Chile)

^d UNIVERSIDAD ANDRÉS BELLO   (Chile)

^e UNIVERSIDAD DE LOS ANDES   (Chile)

^f TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^g Universidad de Talca and Millennium Nucleus of Ion Channels Associated Diseases   (Chile)

Author keywords

acute kidney injury; bone; erythropoietin; FGF23; sepsis

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; FIBROBLAST GROWTH FACTOR 23; HOMODIMER; MESSENGER RNA; EPO PROTEIN, HUMAN; EPO PROTEIN, MOUSE; ERYTHROPOIETIN, RAT; FGF23 PROTEIN, RAT; FIBROBLAST GROWTH FACTOR; RECOMBINANT ERYTHROPOIETIN; RECOMBINANT PROTEIN;

ACUTE KIDNEY FAILURE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BONE MARROW CULTURE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ERYTHROID PRECURSOR CELL; HEMORRHAGIC SHOCK; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SEPSIS; AGONISTS; ANIMAL; BLOOD; BONE MARROW CELL; C57BL MOUSE; COMPLICATION; DISEASE MODEL; DRUG EFFECT; METABOLISM; PROSPECTIVE STUDY; SPRAGUE DAWLEY RAT; TIME FACTOR; UPREGULATION;

ACUTE KIDNEY INJURY; ANIMALS; BONE MARROW CELLS; DISEASE MODELS, ANIMAL; ERYTHROID PRECURSOR CELLS; ERYTHROPOIETIN; FIBROBLAST GROWTH FACTORS; HUMANS; MALE; MICE, INBRED C57BL; PROSPECTIVE STUDIES; RATS, SPRAGUE-DAWLEY; RECEPTORS, ERYTHROPOIETIN; RECOMBINANT PROTEINS; SEPSIS; SHOCK, HEMORRHAGIC; TIME FACTORS; UP-REGULATION;

EID: 85041044278     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1016/j.kint.2017.11.018     Document Type: Article

References (55)

1. Wolf, M., Update on fibroblast growth factor 23 in chronic kidney disease. Kidney Int 82 (2012), 737–747.
2. Erben, R.G., Andrukhova, O., FGF23-Klotho signaling axis in the kidney. Bone 100 (2017), 62–69.
3. Kuro-o, M., Moe, O.W., FGF23-αKlotho as a paradigm for a kidney-bone network. Bone 100 (2017), 4–18.
4. Erben, R.G., Andrukhova, O., FGF23 regulation of renal tubular solute transport. Curr Opin Nephrol Hypertens 24 (2015), 450–456.
5. Hum, J.M., O'Bryan, L., Smith, R.C., et al. Novel functions of circulating Klotho. Bone 100 (2017;17), 36–40.
6. Martin, A., David, V., Quarles, L.D., Regulation and function of the FGF23/klotho endocrine pathways. Physiol Rev 92 (2012), 131–155.
7. Yoshiko, Y., Wang, H., Minamizaki, T., et al. Mineralized tissue cells are a principal source of FGF23. Bone 40 (2007), 1565–1573.
8. Liu, S., Tang, W., Zhou, J., et al. Distinct roles for intrinsic osteocyte abnormalities and systemic factors in regulation of FGF23 and bone mineralization in Hyp mice. Am J Physiol Endocrinol Metab 293 (2007), E1636–E1644.
9. Liu, S., Pathogenic role of Fgf23 in Hyp mice. Am J Physiol Endocrinol Metab 291 (2006), E38–E49.
10. Coe, L.M., Madathil, S.V., Casu, C., et al. FGF-23 is a negative regulator of prenatal and postnatal erythropoiesis. J Biol Chem 289 (2014), 9795–9810.
11. Clinkenbeard, E.L., Cass, T.A., Ni, P., et al. Conditional deletion of murine Fgf23: Interruption of the normal skeletal responses to phosphate challenge and rescue of genetic hypophosphatemia. J Bone Miner Res 31 (2016), 1247–1257.
12. Susantitaphong, P., Cruz, D.N., Cerda, J., et al. World incidence of AKI: a meta-analysis. Clin J Am Soc Nephrol 8 (2013), 1482–1493.
13. Mehta, R.L., Kellum, J.A., Shah, S.V., et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit Care, 11, 2007, R31.
14. Bellomo, R., Kellum, J.A., Ronco, C., Acute kidney injury. Lancet 380 (2012), 756–766.
15. Thomas, M.E., Blaine, C., Dawnay, A., et al. The definition of acute kidney injury and its use in practice. Kidney Int 87 (2014), 62–73.
16. Liangos, O., Wald, R., O'Bell, J.W., et al. Epidemiology and outcomes of acute renal failure in hospitalized patients: a national survey. Clin J Am Soc Nephrol 1 (2006), 43–51.
17. Bagshaw, S.M., Lapinsky, S., Dial, S., et al. Acute kidney injury in septic shock: clinical outcomes and impact of duration of hypotension prior to initiation of antimicrobial therapy. Intensive Care Med 35 (2009), 871–881.
18. Bagasha, P., Nakwagala, F., Kwizera, A., et al. Acute kidney injury among adult patients with sepsis in a low-income country: clinical patterns and short-term outcomes. BMC Nephrol 16 (2015), 4–7.
19. Zhang, M., Hsu, R., Hsu, C.-Y., et al. FGF-23 and PTH levels in patients with acute kidney injury: a cross-sectional case series study. Ann Intensive Care, 1, 2011, 21.
20. Leaf, D.E., Wolf, M., Waikar, S.S., et al. FGF-23 levels in patients with AKI and risk of adverse outcomes. Clin J Am Soc Nephrol 7 (2012), 1217–1223.
21. Leaf, D.E., Christov, M., Jüppner, H., et al. Fibroblast growth factor 23 levels are elevated and associated with severe acute kidney injury and death following cardiac surgery. Kidney Int 89 (2016), 939–948.
22. Leaf, D.E., Wolf, M., Stern, L., Elevated FGF-23 in a patient with rhabdomyolysis-induced acute kidney injury. Nephrol Dial Transplant 25 (2010), 1335–1337.
23. Christov, M., Waikar, S.S., Pereira, R.C., et al. Plasma FGF23 levels increase rapidly after acute kidney injury. Kidney Int 84 (2013), 776–785.
24. Hanudel, M.R., Wesseling-Perry, K., Gales, B., et al. Effects of acute kidney injury and chronic hypoxemia on fibroblast growth factor 23 levels in pediatric cardiac surgery patients. Pediatr Nephrol 31 (2015), 661–669.
25. Neyra, J.A., Moe, O.W., Hu, M.C., Fibroblast growth factor 23 and acute kidney injury. Pediatr Nephrol 30 (2015), 1909–1918.
26. Bunn, H.F., Erythropoietin. Cold Spring Harb Perspect Med, 3, 2013, a011619.
27. Clinkenbeard, E.L., Hanudel, M.R., Stayrook, K.R., et al. Erythropoietin stimulates murine and human Fibroblast growth factor-23, revealing novel roles for bone and bone marrow. Haematologica 102 (2017), e427–e430.
28. Rabadi S, Udo I, Leaf DE, et al. Acute blood loss stimulates fibroblast growth factor 23 production [e-pub ahead of print]. Am J Physiol Renal Physiol. http://www.physiology.org/doi/10.1152/ajprenal.00081.2017.
29. Elliot, J.M., Virankabutra, T., Jones, S., et al. Erythropoietin mimics the acute phase response in critical illness. Crit Care 7 (2003), R35–R40.
30. Yamashita, T., Noiri, E., Hamasaki, Y., et al. Erythropoietin concentration in acute kidney injury is associated with insulin-like growth factor-binding protein-1. Nephrology (Carlton) 21 (2016), 693–699.
31. Giarratana, M.-C., Kobari, L., Lapillonne, H., et al. Ex vivo generation of fully mature human red blood cells from hematopoietic stem cells. Nat Biotechnol 23 (2004), 69–74.
32. Yamazaki, S., Souma, T., Hirano, I., et al. A mouse model of adult-onset anaemia due to erythropoietin deficiency. Nat Commun, 4, 2013, 1950.
33. Tan, C.C., Tan, L.H., Eckardt, K.-U., Erythropoietin production in rats with post-ischemic acute renal failure. Kidney Int 50 (1996), 1958–1964.
34. Ditting, T., Hilgers, K.F., Stetter, A., et al. Renal sympathetic nerves modulate erythropoietin plasma levels after transient hemorrhage in rats. Am J Physiol Renal Physiol 293 (2007), F1099–F1106.
35. Hultström, M., Neurohormonal interactions on the renal oxygen delivery and consumption in haemorrhagic shock-induced acute kidney injury. Acta Physiol (Oxf) 209 (2013), 11–25.
36. Wang, H., Guan, Y., Karamercan, M.A., et al. Resveratrol rescues kidney mitochondrial function following hemorrhagic shock. Shock 44 (2015), 173–180.
37. Lee, J.H., Jo, Y.H., Kim, K., et al. Effect of N-acetylcysteine (NAC) on acute lung injury and acute kidney injury in hemorrhagic shock. Resuscitation 84 (2013), 121–127.
38. Wu, W.-T., Lin, N.-T., Subeq, Y.-M., et al. Erythropoietin protects severe haemorrhagic shock-induced organ damage in conscious rats. Injury 41 (2010), 724–730.
39. Leaf, D.E., Jacob, K.A., Srivastava, A., et al. Fibroblast Growth Factor 23 Levels Associate with AKI and Death in Critical Illness. J Am Soc Nephrol 28 (2017), 1877–1885.
40. Dellinger, R.P., Levy, M.M., Carlet, J.M., et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Intensive Care Med 34 (2008), 17–60.
41. Wu, H., Liu, X., Jaenisch, R., et al. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83 (1995), 59–67.
42. Dumitriu, B., Patrick, M.R., Petschek, J.P., et al. Sox6 cell-autonomously stimulates erythroid cell survival, proliferation, and terminal maturation and is thereby an important enhancer of definitive erythropoiesis during mouse development. Blood 108 (2006), 1198–1207.
43. Pop, R., Shearstone, J.R., Shen, Q., et al. A key commitment step in erythropoiesis is synchronized with the cell cycle clock through mutual inhibition between PU.1 and S-phase progression. PLoS Biol, 8, 2010, e1000484.
44. Clinkenbeard, E.L., Farrow, E.G., Summers, L.J., et al. Neonatal iron deficiency causes abnormal phosphate metabolism by elevating FGF23 in normal and ADHR mice. J Bone Miner Res 29 (2014), 361–369.
45. Cokic, V.P., Bhattacharya, B., Beleslin-Cokic, B.B., et al. JAK-STAT and AKT pathway-coupled genes in erythroid progenitor cells through ontogeny. J Transl Med, 10, 2012, 116.
46. Cao, Y., Lathia, J.D., Eyler, C.E., et al. Erythropoietin receptor signaling through STAT3 is required for glioma stem cell maintenance. Genes Cancer 1 (2010), 50–61.
47. Tsuji, K., Maeda, T., Kawane, T., et al. Leptin stimulates fibroblast growth factor 23 expression in bone and suppresses renal 1alpha,25-dihydroxyvitamin D3 synthesis in leptin-deficient mice. J Bone Miner Res 25 (2010), 1711–1723.
48. Durant, L., Watford, W.T., Ramos, H.L., et al. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 32 (2010), 605–615.
49. Haussler, M.R., Whitfield, G.K., Kaneko, I., et al. The role of vitamin D in the FGF23, klotho, and phosphate bone-kidney endocrine axis. Rev Endocr Metab Disord 13 (2012), 57–69.
50. Mace, M.L., Gravesen, E., Hofman-Bang, J., et al. Key role of the kidney in the regulation of fibroblast growth factor 23. Kidney Int 88 (2015), 1304–1313.
51. Ito, N., Wijenayaka, A.R., Prideaux, M., et al. Regulation of FGF23 expression in IDG-SW3 osteocytes and human bone by pro-inflammatory stimuli. Mol Cell Endocrinol 399 (2015), 208–218.
52. Rossaint, J., Oehmichen, J., Van Aken, H., et al. FGF23 signaling impairs neutrophil recruitment and host defense during CKD. J Clin Invest 126 (2016), 962–974.
53. Wichterman, K.A., Baue, A.E., Chaudry, I.H., Sepsis and septic shock—a review of laboratory models and a proposal. J Surg Res 29 (1980), 189–201.
54. Steele, T.H., DeLuca, H.F., Influence of dietary phosphorus on renal phosphate reabsorption in the parathyroidectomized rat. J Clin Invest 57 (1976), 867–874.
55. Giani, J.F., Bernstein, K.E., Janjulia, T., et al. Salt sensitivity in response to renal injury requires renal angiotensin-converting enzyme. Hypertension 66 (2015), 534–542.