Hepatocyte nuclear factor-1β shapes the energetic homeostasis of kidney tubule cells.
Acute Kidney Injury
/ metabolism
Animals
CRISPR-Cas Systems
Cell Hypoxia
/ genetics
Cell Line
Cell Proliferation
/ genetics
Cell Survival
/ genetics
Epithelial Cells
/ metabolism
Gene Deletion
Gene Expression Regulation
Gene Knockout Techniques
/ methods
Glycolysis
/ genetics
Hepatocyte Nuclear Factor 1-beta
/ genetics
Homeostasis
/ genetics
Humans
Kidney Tubules, Proximal
/ cytology
Metabolome
Mice
Signal Transduction
/ genetics
Transcriptome
HNF-1β
hypoxia
kidney tubule
metabolism
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 2021
11 2021
Historique:
revised:
28
08
2021
received:
16
05
2021
accepted:
02
09
2021
entrez:
15
10
2021
pubmed:
16
10
2021
medline:
16
11
2021
Statut:
ppublish
Résumé
Energetic metabolism controls key steps of kidney development, homeostasis, and epithelial repair following acute kidney injury (AKI). Hepatocyte nuclear factor-1β (HNF-1β) is a master transcription factor that controls mitochondrial function in proximal tubule (PT) cells. Patients with HNF1B pathogenic variant display a wide range of kidney developmental abnormalities and progressive kidney fibrosis. Characterizing the metabolic changes in PT cells with HNF-1β deficiency may help to identify new targetable molecular hubs involved in HNF1B-related kidney phenotypes and AKI. Here, we combined
Identifiants
pubmed: 34653285
doi: 10.1096/fj.202100782RR
doi:
Substances chimiques
Hnf1b protein, mouse
0
Hepatocyte Nuclear Factor 1-beta
138674-15-4
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e21931Informations de copyright
© 2021 Federation of American Societies for Experimental Biology.
Références
Bhargava P, Schnellmann RG. Mitochondrial energetics in the kidney. Nat Rev Nephrol. 2017;13:629-646.
Liu J, Edgington-Giordano F, Dugas C, et al. Regulation of nephron progenitor cell self-renewal by intermediary metabolism. J Am Soc Nephrol. 2017;28:3323-3335.
Kang HM, Ahn SH, Choi P, et al. Defective fatty acid oxidation in renal tubular epithelial cells has a key role in kidney fibrosis development. Nat Med. 2015;21:37-46.
Li S-Y, Susztak K. The role of peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α) in kidney disease. Semin Nephrol. 2018;38:121-126.
Miguel V, Tituaña J, Herrero JI, et al. Renal tubule Cpt1a overexpression protects from kidney fibrosis by restoring mitochondrial homeostasis. J Clin Invest. 2021;131(5):e140695. https://doi.org/10.1172/JCI140695
Coffinier C, Barra J, Babinet C, Yaniv M. Expression of the vHNF1/HNF1beta homeoprotein gene during mouse organogenesis. Mech Dev. 1999;89:211-213.
Coffinier C, Thépot D, Babinet C, Yaniv M, Barra J. Essential role for the homeoprotein vHNF1/HNF1beta in visceral endoderm differentiation. Development. 1999;126:4785-4794.
Gresh L, Fischer E, Reimann A, et al. A transcriptional network in polycystic kidney disease. EMBO J. 2004;23:1657-1668.
Verdeguer F, Le Corre S, Fischer E, et al. A mitotic transcriptional switch in polycystic kidney disease. Nat Med. 2010;16:106-110.
Heliot C, Desgrange A, Buisson I, et al. HNF1B controls proximal-intermediate nephron segment identity in vertebrates by regulating Notch signalling components and Irx1/2. Development. 2013;140:873-885.
Massa F, Garbay S, Bouvier R, et al. Hepatocyte nuclear factor 1β controls nephron tubular development. Development. 2013;140:886-896.
Ma Z, Gong Y, Patel V, et al. Mutations of HNF-1beta inhibit epithelial morphogenesis through dysregulation of SOCS-3. Proc Natl Acad Sci USA. 2007;104:20386-20391.
Naylor RW, Przepiorski A, Ren Q, Yu J, Davidson AJ. HNF1β is essential for nephron segmentation during nephrogenesis. J Am Soc Nephrol. 2013;24:77-87.
Adalat S, Woolf AS, Johnstone KA, et al. HNF1B mutations associate with hypomagnesemia and renal magnesium wasting. J Am Soc Nephrol. 2009;20:1123-1131.
Kompatscher A, de Baaij JHF, Aboudehen K, et al. Loss of transcriptional activation of the potassium channel Kir5.1 by HNF1β drives autosomal dominant tubulointerstitial kidney disease. Kidney Int. 2017;92:1145-1156.
Ferrè S, Veenstra GJC, Bouwmeester R, Hoenderop JGJ, Bindels RJM. HNF-1B specifically regulates the transcription of the γa-subunit of the Na+/K+-ATPase. Biochem Biophys Res Commun. 2011;404:284-290.
Kompatscher A, de Baaij JHF, Aboudehen K, et al. Transcription factor HNF1β regulates expression of the calcium-sensing receptor in the thick ascending limb of the kidney. Am J Physiol Renal Physiol. 2018;315:F27-F35.
Aboudehen K, Noureddine L, Cobo-Stark P, et al. Hepatocyte nuclear factor-1β regulates urinary concentration and response to hypertonicity. J Am Soc Nephrol. 2017;28:2887-2900.
Clissold RL, Hamilton AJ, Hattersley AT, Ellard S, Bingham C. HNF1B-associated renal and extra-renal disease-an expanding clinical spectrum. Nat Rev Nephrol. 2015;11:102-112.
Dubois-Laforgue D, Cornu E, Saint-Martin C, Coste J, Bellanné-Chantelot C, Timsit J Diabetes, associated clinical spectrum, long-term prognosis, and genotype/phenotype correlations in 201 adult patients with hepatocyte nuclear factor 1B (HNF1B) molecular defects. Diabetes Care. 2017;40:1436-1443.
Faguer S, Decramer S, Chassaing N, et al. Diagnosis, management, and prognosis of HNF1B nephropathy in adulthood. Kidney Int. 2011;80:768-776.
Heidet L, Decramer S, Pawtowski A, et al. Spectrum of HNF1B mutations in a large cohort of patients who harbor renal diseases. Clin J Am Soc Nephrol. 2010;5:1079-1090.
Lokmane L, Heliot C, Garcia-Villalba P, Fabre M, Cereghini S. vHNF1 functions in distinct regulatory circuits to control ureteric bud branching and early nephrogenesis. Development. 2010;137:347-357.
Adalat S, Hayes WN, Bryant WA, et al. HNF1B mutations are associated with a gitelman-like tubulopathy that develops during childhood. Kidney Int Rep. 2019;4:1304-1311.
Chan SC, Zhang Y, Shao A, et al. Mechanism of fibrosis in HNF1B-related autosomal dominant tubulointerstitial kidney disease. J Am Soc Nephrol. 2018;29:2493-2509.
Casemayou A, Fournel A, Bagattin A, et al. Hepatocyte nuclear factor-1β controls mitochondrial respiration in renal tubular cells. J Am Soc Nephrol. 2017;28:3205-3217.
Simon N, Hertig A. Alteration of fatty acid oxidation in tubular epithelial cells: from acute kidney injury to renal fibrogenesis. Front Med (Lausanne). 2015;2:52.
Tran M, Tam D, Bardia A, et al. PGC-1α promotes recovery after acute kidney injury during systemic inflammation in mice. J Clin Invest. 2011;121:4003-4014.
Lan R, Geng H, Singha PK, et al. Mitochondrial pathology and glycolytic shift during proximal tubule atrophy after ischemic AKI. J Am Soc Nephrol. 2016;27:3356-3367.
Beckonert O, Keun HC, Ebbels TMD, et al. Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat Protoc. 2007;2:2692-2703.
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw. 2008;25:1-18.
Extract and Visualize the Results of Multivariate Data Analyses. https://rpkgs.datanovia.com/factoextra/index.html
Thévenot EA, Roux A, Xu Y, Ezan E, Junot C. Analysis of the human adult urinary metabolome variations with age, body mass index, and gender by implementing a comprehensive workflow for univariate and OPLS statistical analyses. J Proteome Res. 2015;14:3322-3335.
Haverty TP, Kelly CJ, Hines WH, et al. Characterization of a renal tubular epithelial cell line which secretes the autologous target antigen of autoimmune experimental interstitial nephritis. J Cell Biol. 1988;107:1359-1368.
Emma F, Montini G, Parikh SM, Salviati L. Mitochondrial dysfunction in inherited renal disease and acute kidney injury. Nat Rev Nephrol. 2016;12:267-280.
Wu G. Amino acids: metabolism, functions, and nutrition. Amino Acids. 2009;37:1-17.
Aboudehen K, Kim MS, Mitsche M, et al. Transcription factor hepatocyte nuclear factor-1β regulates renal cholesterol metabolism. J Am Soc Nephrol. 2016;27:2408-2421.
Ferrè S, Igarashi P. New insights into the role of HNF-1β in kidney (patho)physiology. Pediatr Nephrol. 2019;34:1325-1335.
Desgrange A, Heliot C, Skovorodkin I, et al. HNF1B controls epithelial organization and cell polarity during ureteric bud branching and collecting duct morphogenesis. Development. 2017;144:4704-4719.
Bockenhauer D, Jaureguiberry G. HNF1B-associated clinical phenotypes: the kidney and beyond. Pediatr Nephrol. 2016;31:707-714.
Yadav H, Quijano C, Kamaraju A, et al. Protection from obesity and diabetes by blockade of TGF-β/Smad3 signaling. Cell Metab. 2011;14:67-79.
Okamoto T, Mandai M, Matsumura N, et al. Hepatocyte nuclear factor-1β (HNF-1β) promotes glucose uptake and glycolytic activity in ovarian clear cell carcinoma. Mol Carcinog. 2015;54:35-49.
Yamaguchi K, Mandai M, Oura T, et al. Identification of an ovarian clear cell carcinoma gene signature that reflects inherent disease biology and the carcinogenic processes. Oncogene. 2010;29:1741-1752.
Mandai M, Amano Y, Yamaguchi K, et al. Ovarian clear cell carcinoma meets metabolism; HNF-1β confers survival benefits through the Warburg effect and ROS reduction. Oncotarget. 2015;6:30704-30714.
Amano Y, Mandai M, Yamaguchi K, et al. Metabolic alterations caused by HNF1β expression in ovarian clear cell carcinoma contribute to cell survival. Oncotarget. 2015;6:26002-26017.
Lu W, Sun J, Zhou H, et al. HNF1B inhibits cell proliferation via repression of SMAD6 expression in prostate cancer. J Cell Mol Med. 2020;24:14539-14548.
Chandra S, Srinivasan S, Batra J. Hepatocyte nuclear factor 1 beta: a perspective in cancer. Cancer Med. 2021;10:1791-1804.
Choi Y-H, McNally BT, Igarashi P. Zyxin regulates migration of renal epithelial cells through activation of hepatocyte nuclear factor-1β. Am J Physiol Renal Physiol. 2013;305:F100-F110.
Dudziak K, Mottalebi N, Senkel S, et al. Transcription factor HNF1β and novel partners affect nephrogenesis. Kidney Int. 2008;74:210-217.
Bonventre JV, Weinberg JM. Recent advances in the pathophysiology of ischemic acute renal failure. J Am Soc Nephrol. 2003;14:2199-2210.
Lankadeva YR, Okazaki N, Evans RG, Bellomo R, May CN. Renal medullary hypoxia: a new therapeutic target for septic acute kidney injury? Semin Nephrol. 2019;39:543-553.
Basile DP, Anderson MD, Sutton TA. Pathophysiology of acute kidney injury. Compr Physiol. 2012;2:1303-1353.
Shu S, Wang Y, Zheng M, et al. Hypoxia and hypoxia-inducible factors in kidney injury and repair. Cells. 2019;8(3):207.
Mimura I, Nangaku M. The suffocating kidney: tubulointerstitial hypoxia in end-stage renal disease. Nat Rev Nephrol. 2010;6:667-678.
He L, Wei Q, Liu J, et al. AKI on CKD: heightened injury, suppressed repair, and the underlying mechanisms. Kidney Int. 2017;92:1071-1083.
Bueno M, Calyeca J, Rojas M, Mora AL. Mitochondria dysfunction and metabolic reprogramming as drivers of idiopathic pulmonary fibrosis. Redox Biol. 2020;33:101509.
Li X, Zhang W, Cao Q, et al. Mitochondrial dysfunction in fibrotic diseases. Cell Death Discov. 2020;6:80.
Samuvel DJ, Sundararaj KP, Nareika A, Lopes-Virella MF, Huang Y. Lactate boosts TLR4 signaling and NF-kappaB pathway-mediated gene transcription in macrophages via monocarboxylate transporters and MD-2 up-regulation. J Immunol. 2009;182:2476-2484.
Ding H, Jiang L, Xu J, et al. Inhibiting aerobic glycolysis suppresses renal interstitial fibroblast activation and renal fibrosis. Am J Physiol Renal Physiol. 2017;313:F561-F575.
Yin X-N, Wang J, Cui L-F, Fan W-X. Enhanced glycolysis in the process of renal fibrosis aggravated the development of chronic kidney disease. Eur Rev Med Pharmacol Sci. 2018;22:4243-4251.
Wei Q, Su J, Dong G, et al. Glycolysis inhibitors suppress renal interstitial fibrosis via divergent effects on fibroblasts and tubular cells. Am J Physiol Renal Physiol. 2019;316:F1162-F1172.
Colegio OR, Chu N-Q, Szabo AL, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 2014;513:559-563.
Shen Y, Jiang L, Wen P, et al. Tubule-derived lactate is required for fibroblast activation in acute kidney injury. Am J Physiol Renal Physiol. 2020;318:F689-F701.
Leist M, Single B, Castoldi AF, Kühnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 1997;185:1481-1486.
Eguchi Y, Shimizu S, Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 1997;57:1835-1840.
Nicotera P, Leist M, Ferrando-May E. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett. 1998;102-103:139-142.
Mitra K, Wunder C, Roysam B, Lin G, Lippincott-Schwartz J. A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase. Proc Natl Acad Sci USA. 2009;106:11960-11965.
Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029-1033.
Zhu J, Thompson CB. Metabolic regulation of cell growth and proliferation. Nat Rev Mol Cell Biol. 2019;20:436-450.
He Z, Zhu X, Shi Z, Wu T, Wu L. Metabolic regulation of dendritic cell differentiation. Front Immunol. 2019;10:410.
Almeida L, Lochner M, Berod L, Sparwasser T. Metabolic pathways in T cell activation and lineage differentiation. Semin Immunol. 2016;28:514-524.
Zheng X, Boyer L, Jin M, et al. Metabolic reprogramming during neuronal differentiation from aerobic glycolysis to neuronal oxidative phosphorylation. Elife. 2016;5:e13374.
Zhang J, Nuebel E, Daley GQ, Koehler CM, Teitell MA. Metabolic regulation in pluripotent stem cells during reprogramming and self-renewal. Cell Stem Cell. 2012;11:589-595.
Faguer S, Mayeur N, Casemayou A, et al. Hnf-1β transcription factor is an early hif-1α-independent marker of epithelial hypoxia and controls renal repair. PLoS One. 2013;8:e63585.
Kent C. Regulation of phosphatidylcholine biosynthesis. Prog Lipid Res. 1990;29:87-105.
Toback FG, Havener LJ, Dodd RC, Spargo BH. Phospholipid metabolism during renal regeneration after acute tubular necrosis. Am J Physiol. 1977;232:216-222.
Solati Z, Edel AL, Shang Y, O K, Ravandi A. Oxidized phosphatidylcholines are produced in renal ischemia reperfusion injury. PLoS One. 2018;13(4):e0195172.
Rao S, Walters KB, Wilson L, et al. Early lipid changes in acute kidney injury using SWATH lipidomics coupled with MALDI tissue imaging. Am J Physiol Renal Physiol. 2016;310:F1136-F1147.
Scantlebery AML, Tammaro A, Mills JD, et al. The dysregulation of metabolic pathways and induction of the pentose phosphate pathway in renal ischaemia-reperfusion injury. J Pathol. 2021;253:404-414. https://doi.org/10.1002/path.5605
Kim S, Na J-Y, Song K, Kwon J. In vivo protective effect of phosphatidylcholine on carbon tetrachloride induced nephrotoxicity. Exp Toxicol Pathol. 2016;68:553-558.
Nagarajan SR, Paul-Heng M, Krycer JR, et al. Lipid and glucose metabolism in hepatocyte cell lines and primary mouse hepatocytes: a comprehensive resource for in vitro studies of hepatic metabolism. Am J Physiol Endocrinol Metab. 2019;316:E578-E589.
Khundmiri SJ, Chen L, Lederer ED, Yang C-R, Knepper MA. Transcriptomes of major proximal tubule cell culture models. J Am Soc Nephrol. 2021;32:86-97.