Relationship between GFR, intact PTH, oxidized PTH, non-oxidized PTH as well as FGF23 in patients with CKD.


Journal

FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484

Informations de publication

Date de publication:
11 2020
Historique:
received: 17 03 2020
revised: 07 08 2020
accepted: 08 09 2020
pubmed: 24 9 2020
medline: 28 4 2021
entrez: 23 9 2020
Statut: ppublish

Résumé

Fibroblast growth factor 23 (FGF23) and parathyroid hormone (PTH) are regulators of renal phosphate excretion and vitamin D metabolism. In chronic kidney disease (CKD), circulating FGF23 and PTH concentrations progressively increase as renal function declines. Oxidation of PTH at two methionine residues (positions 8 and 18) causes a loss of function. The impact of n-oxPTH and oxPTH on FGF23 synthesis, however, and how n-oxPTH and oxPTH concentrations are affected by CKD, is yet unknown. The effects of oxidized and non-oxidized PTH 1-34 on Fgf23 gene expression were analyzed in UMR106 osteoblast-like cells. Furthermore, we investigated the relationship between n-oxPTH and oxPTH, respectively, with FGF23 in two independent patients' cohorts (620 children with CKD and 600 kidney transplant recipients). While n-oxPTH stimulated Fgf23 mRNA synthesis in vitro, oxidation of PTH in particular at Met8 led to a markedly weaker stimulation of Fgf23. The effect was even stronger when both Met8 and Met18 were oxidized. In both clinical cohorts, n-oxPTH-but not oxPTH-was significantly associated with FGF23 concentrations, independent of known confounding factors. Moreover, with progressive deterioration of kidney function, intact PTH (iPTH) and oxPTH increased substantially, whereas n-oxPTH increased only moderately. In conclusion, n-oxPTH, but not oxPTH, stimulates Fgf23 gene expression. The increase in PTH with decreasing GFR is mainly due to an increase in oxPTH in more advanced stages of CKD.

Identifiants

pubmed: 32964520
doi: 10.1096/fj.202000596R
doi:

Substances chimiques

FGF23 protein, human 0
Parathyroid Hormone 0
Fibroblast Growth Factors 62031-54-3
Fibroblast Growth Factor-23 7Q7P4S7RRE

Types de publication

Journal Article Observational Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

15269-15281

Informations de copyright

© 2020 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.

Références

Kuro-o M, Moe OW. FGF23-alpha Klotho as a paradigm for a kidney-bone network. Bone. 2017;100:4-18.
Krajisnik T, Bjorklund P, Marsell R, et al. Fibroblast growth factor-23 regulates parathyroid hormone and 1alpha-hydroxylase expression in cultured bovine parathyroid cells. J Endocrinol. 2007;195:125-131.
Isakova T., Cai X., Lee J., et al. Longitudinal FGF23 trajectories and mortality in patients with CKD. J Am Soc Nephrol. 2018;29:579-590.
Isakova T, Wahl P, Vargas GS, et al. Fibroblast growth factor 23 is elevated before parathyroid hormone and phosphate in chronic kidney disease. Kidney Int. 2011;79:1370-1378.
Graciolli FG, Neves KR, Barreto F, et al. The complexity of chronic kidney disease-mineral and bone disorder across stages of chronic kidney disease. Kidney Int. 2017;91:1436-1446.
Lavi-Moshayoff V, Wasserman G, Meir T, Silver J, Naveh-Many T. PTH increases FGF23 gene expression and mediates the high-FGF23 levels of experimental kidney failure: a bone parathyroid feedback loop. Am J Physiol Renal Physiol. 2010;299:F882-F889.
Masuyama R, Stockmans I, Torrekens S, et al. Vitamin D receptor in chondrocytes promotes osteoclastogenesis and regulates FGF23 production in osteoblasts. J Clin Invest. 2006;116:3150-3159.
David V, Martin A, Isakova T, et al. Inflammation and functional iron deficiency regulate fibroblast growth factor 23 production. Kidney Int. 2016;89:135-146.
Rodriguez-Ortiz ME, Lopez I, Munoz-Castaneda JR, et al. Calcium deficiency reduces circulating levels of FGF23. J Am Soc Nephrol. 2012;23:1190-1197.
Ferrari SL, Bonjour JP, Rizzoli R. Fibroblast growth factor-23 relationship to dietary phosphate and renal phosphate handling in healthy young men. J Clin Endocr Metab. 2005;90:1519-1524.
Feger M, Hase P, Zhang BB, et al. The production of fibroblast growth factor 23 is controlled by TGF ss 2. Sci Rep. 2017;7:4982.
Meir T, Durlacher K, Pan Z, et al. Parathyroid hormone activates the orphan nuclear receptor Nurr1 to induce FGF23 transcription. Kidney Int. 2014;86:1106-1115.
Hocher B, Oberthur D, Slowinski T, et al. Modeling of oxidized PTH (oxPTH) and non-oxidized PTH (n-oxPTH) receptor binding and relationship of oxidized to non-oxidized PTH in children with chronic renal failure, adult patients on hemodialysis and kidney transplant recipients. Kidney Blood Press Res. 2013;37:240-251.
Ursem SR, Vervloet MG, Hillebrand JJG, de Jongh RT, Heijboer AC. Oxidation of PTH: in vivo feature or effect of preanalytical conditions? Clin Chem Lab Med. 2018;56:249-255.
Hocher B, Armbruster FP, Stoeva S, et al. Measuring parathyroid hormone (PTH) in patients with oxidative stress-do we need a fourth generation parathyroid hormone assay? PLoS One. 2012;7:e40242.
Panah F, Ghorbanihaghjo A, Argani H, Zarmehri MA, Ahmad SNS. Ischemic acute kidney injury and klotho in renal transplantation. Clin Biochem. 2018;55:3-8.
Querfeld U, Anarat A, Bayazit AK, et al. The Cardiovascular Comorbidity in Children with Chronic Kidney Disease (4C) study: objectives, design, and methodology. Clin J Am Soc Nephrol. 2010;5:1642-1648.
Schwartz GJ, Munoz A, Schneider MF, et al. New equations to estimate GFR in children with CKD. J Am Soc Nephrol. 2009;20:629-637.
Bär L, Hase P, Föller M. PKC regulates the production of fibroblast growth factor 23 (FGF23). PLOS ONE. 2019:14(3):e0211309. http://dx.doi.org/10.1371/journal.pone.0211309.
Lowik CW, van der Pluijm G, Bloys H, et al. Parathyroid hormone (PTH) and PTH-like protein (PLP) stimulate interleukin-6 production by osteogenic cells: a possible role of interleukin-6 in osteoclastogenesis. Biochem Biophys Res Commun. 1989;162:1546-1552.
Greenfield EM, Gornik SA, Horowitz MC, Donahue HJ, Shaw SM. Regulation of cytokine expression in osteoblasts by parathyroid hormone: rapid stimulation of interleukin-6 and leukemia inhibitory factor mRNA. J Bone Miner Res. 1993;8:1163-1171.
Sakagami Y, Girasole G, Yu XP, Boswell HS, Manolagas SC. Stimulation of interleukin-6 production by either calcitonin gene-related peptide or parathyroid hormone in two phenotypically distinct bone marrow-derived murine stromal cell lines. J Bone Miner Res. 1993;8:811-816.
Keller H, Kneissel M. SOST is a target gene for PTH in bone. Bone. 2005;37:148-158.
Rhee Y, Allen MR, Condon K, et al. PTH receptor signaling in osteocytes governs periosteal bone formation and intracortical remodeling. J Bone Miner Res. 2011;26:1035-1046.
Kramer I, Loots GG, Studer A, Keller H, Kneissel M. Parathyroid hormone (PTH)-induced bone gain is blunted in SOST overexpressing and deficient mice. J Bone Miner Res. 2010;25:178-189.
Yang H, Dong J, Xiong W, Fang Z, Guan H, Li F. N-cadherin restrains PTH repressive effects on sclerostin/SOST by regulating LRP6-PTH1R interaction. Ann N Y Acad Sci. 2016;1385:41-52.
Doyon A, Fischer D-C, Bayazit AK, et al. Markers of bone metabolism are affected by renal function and growth hormone therapy in children with chronic kidney disease. PLoS One. 2015;10:e0113482.
Tepel M, Armbruster FP, Gron HJ, et al. Nonoxidized, biologically active parathyroid hormone determines mortality in hemodialysis patients. J Clin Endocrinol Metab. 2013;98:4744-4751.
Cheloha RW, Gellman SH, Vilardaga JP, Gardella TJ. PTH receptor-1 signalling-mechanistic insights and therapeutic prospects. Nat Rev Endocrinol. 2015;11:712-724.
Zull JE, Smith SK, Wiltshire R. Effect of methionine oxidation and deletion of amino-terminal residues on the conformation of parathyroid hormone. Circular dichroism studies. J Biol Chem. 1990;265:5671-5676.
Frelinger AL 3rd, Zull JE. The role of the methionine residues in the structure and function of parathyroid hormone. Arch Biochem Biophys. 1986;244:641-649.
Lopez I, Rodriguez-Ortiz ME, Almaden Y, et al. Direct and indirect effects of parathyroid hormone on circulating levels of fibroblast growth factor 23 in vivo. Kidney Int. 2011;80:475-482.
Liu SG, Tang W, Zhou JP, et al. Fibroblast growth factor 23 is a counter-regulatory phosphaturic hormone for vitamin D. J Am Soc Nephrol. 2006;17:1305-1315.
Saji F, Shiizaki K, Shimada S, et al. Regulation of fibroblast growth factor 23 production in bone in uremic rats. Nephron Physiol. 2009;111:59-66.
Samadfam R, Richard C, Nguyen-Yamamoto L, Bolivar I, Goltzman D. Bone formation regulates circulating concentrations of fibroblast growth factor 23. Endocrinology. 2009;150:4835-4845.
Burnett-Bowie SAM, Henao MP, Dere ME, Lee H, Leder BZ. Effects of hPTH(1-34) infusion on circulating serum phosphate, 1,25-dihydroxyvitamin D, and FGF23 levels in healthy men. J Bone Miner Res. 2009;24:1681-1685.
Gutierrez OM, Smith KT, Barchi-Chung A, Patel NM, Isakova T, Wolf M. (1-34) parathyroid hormone infusion acutely lowers fibroblast growth factor 23 concentrations in adult volunteers. Clin J Am Soc Nephro. 2012;7:139-145.
Wolf M. Forging forward with 10 burning questions on FGF23 in kidney disease. J Am Soc Nephrol. 2010;21:1427-1435.
Xu G, Luo K, Liu H, Huang T, Fang X, Tu W. The progress of inflammation and oxidative stress in patients with chronic kidney disease. Ren Fail. 2015;37:45-49.
Lang F, Leibrock C, Pandyra AA, Stournaras C, Wagner CA, Foller M. Phosphate homeostasis, inflammation and the regulation of FGF-23. Kidney Blood Press Res. 2018;43:1742-1748.
Ursem SR, Francic V, Keppel M, et al. The effect of vitamin D supplementation on plasma non-oxidised PTH in a randomised clinical trial. Endocr Connect. 2019;8(5):518-527.
Hocher B, Zeng SF. Need for better PTH assays for clinical research and patient treatment. Clin Chem Lab Med. 2018;56:183-185.
Lu YP, Zeng S, Chu C, et al. Non-oxidized PTH (n-oxPTH) is associated with graft loss in kidney transplant recipients. Clin Chim Acta. 2020;508:92-97.
Cavalier E, Lukas P, Warling X, Moonen M, Smelten N, Delanaye P. The percentage of non-oxidized PTH concentration remains stable over a period of 1 year in hemodialyzed patients. Clin Chim Acta. 2020;506:107-109.
Ursem SR, Vervloet MG, de Jongh RT, Heijboer AC. Oxidation of parathyroid hormone. Clin Chim Acta. 2020;506:84-91.
Ursem S, Francic V, Keppel M, et al. The effect of vitamin D supplementation on plasma non-oxidised PTH in a randomised clinical trial. Endocr Connect. 2019;8:518-527.
van der Velde M, Matsushita K, Coresh J, et al. Lower estimated glomerular filtration rate and higher albuminuria are associated with all-cause and cardiovascular mortality. A collaborative meta-analysis of high-risk population cohorts. Kidney Int. 2011;79:1341-1352.
Hayek SS, Sever S, Ko YA, et al. Soluble urokinase receptor and chronic kidney disease. New Engl J Med. 2015;373:1916-1925.

Auteurs

Shufei Zeng (S)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
Department of Nephrology, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Uwe Querfeld (U)

Division of Gastroenterology, Nephrology and Metabolic Diseases, Department of Pediatrics, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Martina Feger (M)

Department of Physiology, University of Hohenheim, Stuttgart, Germany.

Dieter Haffner (D)

Department of Pediatric Kidney, Liver and Metabolic Diseases, Pediatric Research Center, Hannover Medical School, Hannover, Germany.

Ahmed A Hasan (AA)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
Institute of Nutritional Science, University of Potsdam, Potsdam, Germany.

Chang Chu (C)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
Department of Nephrology, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Torsten Slowinski (T)

Department of Nephrology, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Thomas Bernd Dschietzig (T)

Department of Cardiology, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Franz Schäfer (F)

Center for Pediatrics and Adolescent Medicine, University of Heidelberg, Heidelberg, Germany.

Yingquan Xiong (Y)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
Institute of Nutritional Science, University of Potsdam, Potsdam, Germany.

Bingbing Zhang (B)

Institute of Physiology, University of Tübingen, Tübingen, Germany.
College of Life Science and Technology, Heilongjiang Bayi Agricultural University, Daqing, China.

Steffen Rausch (S)

Department of Physiology, University of Hohenheim, Stuttgart, Germany.

Katarina Horvathova (K)

Biomedica Slovakia s.r.o., Bratislava, Slovakia.

Florian Lang (F)

Institute of Nutritional Science, University of Potsdam, Potsdam, Germany.

Bernhard Karl Krämer (B)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.

Michael Föller (M)

Department of Physiology, University of Hohenheim, Stuttgart, Germany.

Berthold Hocher (B)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
Key Laboratory of Study and Discovery of Small Targeted Molecules of Hunan Province, School of Medicine, Hunan Normal University, Changsha, China.
Reproductive and Genetic Hospital of CITIC-Xiangya, Changsha, China.
Institute of Medical Diagnostics, IMD, Berlin, , Berlin, Germany.

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