3,645
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

FGF21 and autophagy coordinately counteract kidney disease progression during aging and obesity

, , , , , , , , , , , & show all
Pages 489-504 | Received 01 Nov 2022, Accepted 11 Sep 2023, Published online: 24 Sep 2023

References

  • Jager KJ, Kovesdy C, Langham R, et al. A single number for advocacy and communication-worldwide more than 850 million individuals have kidney diseases. Kidney Int. 2019 Nov;96(5):1048–1050. doi: 10.1016/j.kint.2019.07.012
  • Global, regional, and znational age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: A systematic analysis for the global burden of disease study 2013. Lancet. 2015 Jan 10;385(9963):117–171. doi: 10.1016/S0140-6736(14)61682-2
  • Rhee CM, CP K. Epidemiology: spotlight on CKD deaths—increasing mortality worldwide. Nat Rev Nephrol. 2015 Apr;11(4):199–200. doi: 10.1038/nrneph.2015.25
  • Breyer MD, Susztak K. The next generation of therapeutics for chronic kidney disease. Nat Rev Drug Discov. 2016 Aug;15(8):568–588. doi: 10.1038/nrd.2016.67
  • Little MH, Humphreys BD. Regrow or repair: an update on potential regenerative therapies for the kidney. J Am Soc Nephrol. 2022 Jan;33(1):15–32. doi: 10.1681/ASN.2021081073
  • Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008 Feb 28;451(7182):1069–1075. doi: 10.1038/nature06639
  • Kimura T, Takabatake Y, Takahashi A, et al. Autophagy protects the proximal tubule from degeneration and acute ischemic injury. J Am Soc Nephrol. 2011 May;22(5):902–913. doi: 10.1681/ASN.2010070705
  • Yamamoto T, Takabatake Y, Kimura T, et al. Time-dependent dysregulation of autophagy: implications in aging and mitochondrial homeostasis in the kidney proximal tubule. Autophagy. 2016 May 3;12(5):801–813. doi: 10.1080/15548627.2016.1159376
  • Yamamoto T, Takabatake Y, Takahashi A, et al. High-fat diet-induced lysosomal dysfunction and impaired autophagic flux contribute to lipotoxicity in the kidney. J Am Soc Nephrol. 2017 May;28(5):1534–1551. doi: 10.1681/ASN.2016070731
  • Takahashi A, Takabatake Y, Kimura T, et al. Autophagy inhibits the accumulation of advanced glycation end products by promoting lysosomal biogenesis and function in the kidney proximal tubules. Diabetes. 2017 May;66(5):1359–1372. doi: 10.2337/db16-0397
  • Sakai S, Yamamoto T, Takabatake Y, et al. Proximal tubule autophagy differs in type 1 and 2 Diabetes. J Am Soc Nephrol. 2019 Jun;30(6):929–945. doi: 10.1681/ASN.2018100983
  • Bordi M, Berg MJ, Mohan PS, et al. Autophagy flux in CA1 neurons of alzheimer hippocampus: increased induction overburdens failing lysosomes to propel neuritic dystrophy. Autophagy. 2016 Dec;12(12):2467–2483. doi: 10.1080/15548627.2016.1239003
  • Takabatake Y, Yamamoto T, Isaka Y. Stagnation of autophagy: a novel mechanism of renal lipotoxicity. Autophagy. 2017 Apr 3;13(4):775–776. doi: 10.1080/15548627.2017.1283084
  • Yamamoto T, Takabatake Y, Minami S, et al. Eicosapentaenoic acid attenuates renal lipotoxicity by restoring autophagic flux. Autophagy. 2021 Jul;17(7):1700–1713. doi: 10.1080/15548627.2020.1782034
  • Yamamoto-Imoto H, Minami S, Shioda T, et al. Age-associated decline of MondoA drives cellular senescence through impaired autophagy and mitochondrial homeostasis. Cell Rep. 2022 Mar 1;38(9):110444. doi: 10.1016/j.celrep.2022.110444
  • Kharitonenkov A, DiMarchi R. Fibroblast growth factor 21 night watch: advances and uncertainties in the field. J Intern Med. 2017 Mar;281(3):233–246. doi: 10.1111/joim.12580
  • Xie T, Leung PS. Fibroblast growth factor 21: a regulator of metabolic disease and health span. Am J Physiol Endocrinol Metab. 2017 Sep 1;313(3):E292–E302. doi: 10.1152/ajpendo.00101.2017
  • Ye D, Wang Y, Li H, et al. Fibroblast growth factor 21 protects against acetaminophen-induced hepatotoxicity by potentiating peroxisome proliferator-activated receptor coactivator protein-1alpha-mediated antioxidant capacity in mice. Hepatology. 2014 Sep;60(3):977–989. doi: 10.1002/hep.27060
  • Kim SH, Kim KH, Kim HK, et al. Fibroblast growth factor 21 participates in adaptation to endoplasmic reticulum stress and attenuates obesity-induced hepatic metabolic stress. Diabetologia. 2015 Apr;58(4):809–818. doi: 10.1007/s00125-014-3475-6
  • Hojman P, Pedersen M, Nielsen AR, et al. Fibroblast growth factor-21 is induced in human skeletal muscles by hyperinsulinemia. Diabetes. 2009 Dec;58(12):2797–2801. doi: 10.2337/db09-0713
  • Kim KH, Jeong YT, Oh H, et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med. 2013 Jan;19(1):83–92. doi: 10.1038/nm.3014
  • Planavila A, Redondo I, Hondares E, et al. Fibroblast growth factor 21 protects against cardiac hypertrophy in mice. Nat Commun. 2013;4(1):2019. doi: 10.1038/ncomms3019
  • Salminen A, Kaarniranta K, Kauppinen A. Regulation of longevity by FGF21: interaction between energy metabolism and stress responses. Ageing Res Rev. 2017 May 25;37:79–93. doi: 10.1016/j.arr.2017.05.004
  • Youm YH, Horvath TL, Mangelsdorf DJ, et al. Prolongevity hormone FGF21 protects against immune senescence by delaying age-related thymic involution. Proc Natl Acad Sci U S A. 2016 Jan 26;113(4):1026–1031. doi: 10.1073/pnas.1514511113
  • Jimenez V, Jambrina C, Casana E, et al. FGF21 gene therapy as treatment for obesity and insulin resistance. EMBO Mol Med. 2018 Aug;10(8):e8791. doi: 10.15252/emmm.201708791
  • Zhang Y, Xie Y, Berglund ED, et al. The starvation hormone, fibroblast growth factor-21, extends lifespan in mice. Elife. 2012 Oct 15;1:e00065. doi: 10.7554/eLife.00065
  • Kim HW, Lee JE, Cha JJ, et al. Fibroblast growth factor 21 improves insulin resistance and ameliorates renal injury in db/db mice. Endocrinology. 2013 Sep;154(9):3366–3376. doi: 10.1210/en.2012-2276
  • Zhang C, Shao M, Yang H, et al. Attenuation of hyperlipidemia- and diabetes-induced early-stage apoptosis and late-stage renal dysfunction via administration of fibroblast growth factor-21 is associated with suppression of renal inflammation. PLoS One. 2013;8(12):e82275. doi: 10.1371/journal.pone.0082275
  • Minami S, Yamamoto T, Takabatake Y, et al. Lipophagy maintains energy homeostasis in the kidney proximal tubule during prolonged starvation. Autophagy. 2017 Oct 3;13(10):1629–1647. doi: 10.1080/15548627.2017.1341464
  • Loeffler I, Hopfer U, Koczan D, et al. Type VIII collagen modulates TGF-β1-induced proliferation of mesangial cells. J Am Soc Nephrol. 2011 Apr;22(4):649–663. doi: 10.1681/ASN.2010010098
  • Li F, Liu Z, Tang C, et al. FGF21 is induced in cisplatin nephrotoxicity to protect against kidney tubular cell injury. FASEB J. 2018 Jun;32(6):3423–3433. doi: 10.1096/fj.201701316R
  • Kawamoto S, Niwa H, Tashiro F, et al. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 2000 Mar 31;470(3):263–268. doi: 10.1016/S0014-5793(00)01338-7
  • Docherty MH, O’Sullivan ED, Bonventre JV, et al. Cellular senescence in the kidney. J Am Soc Nephrol. 2019 May;30(5):726–736. doi: 10.1681/ASN.2018121251
  • Tang C, Cai J, Yin XM, et al. Mitochondrial quality control in kidney injury and repair. Nat Rev Nephrol. 2021 May;17(5):299–318. doi: 10.1038/s41581-020-00369-0
  • Cybulsky AV. Endoplasmic reticulum stress, the unfolded protein response and autophagy in kidney diseases. Nat Rev Nephrol. 2017 Nov;13(11):681–696. doi: 10.1038/nrneph.2017.129
  • Yan J, Wang J, Huang H, et al. Fibroblast growth factor 21 delayed endothelial replicative senescence and protected cells from H(2)O(2)-induced premature senescence through SIRT1. Am J Transl Res. 2017;9(10):4492–4501.
  • Chen Q, Ma J, Yang X, et al. SIRT1 mediates effects of FGF21 to ameliorate cisplatin-induced acute kidney injury. Front Pharmacol. 2020;11:241. doi: 10.3389/fphar.2020.00241
  • Yuan X, Wei G, You Y, et al. Rutin ameliorates obesity through brown fat activation. FASEB J. 2017 Jan;31(1):333–345. doi: 10.1096/fj.201600459rr
  • Zhang C, He X, Sheng Y, et al. Allicin regulates energy homeostasis through brown adipose tissue. iScience. 2020 May 22;23(5):101113. doi: 10.1016/j.isci.2020.101113
  • Canto C, Gerhart-Hines Z, Feige JN, et al. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature. 2009 Apr 23;458(7241):1056–1060. doi: 10.1038/nature07813
  • Croon M, Szczepanowska K, Popovic M, et al. FGF21 modulates mitochondrial stress response in cardiomyocytes only under mild mitochondrial dysfunction. Sci Adv. 2022 Apr 8;8(14):eabn7105. doi: 10.1126/sciadv.abn7105
  • McWilliams TG, Prescott AR, Allen GF, et al. Mito-QC illuminates mitophagy and mitochondrial architecture in vivo. J Cell Bio. 2016 Aug 1;214(3):333–345. doi: 10.1083/jcb.201603039
  • Ishii K, Kobayashi H, Taguchi K, et al. Kidney epithelial targeted mitochondrial transcription factor a deficiency results in progressive mitochondrial depletion associated with severe cystic disease. Kidney Int. 2021 Mar;99(3):657–670. doi: 10.1016/j.kint.2020.10.013
  • Chung KW, Dhillon P, Huang S, et al. Mitochondrial damage and activation of the STING pathway lead to renal inflammation and fibrosis. Cell Metab. 2019 Oct 1;30(4):784–799 e5. doi: 10.1016/j.cmet.2019.08.003
  • Fisher FM, Chui PC, Antonellis PJ, et al. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes. 2010 Nov;59(11):2781–2789. doi: 10.2337/db10-0193
  • So WY, Cheng Q, Chen L, et al. High glucose represses β-klotho expression and impairs fibroblast growth factor 21 action in mouse pancreatic islets: involvement of peroxisome proliferator-activated receptor γ signaling. Diabetes. 2013 Nov;62(11):3751–3759. doi: 10.2337/db13-0645
  • Díaz-Delfín J, Hondares E, Iglesias R, et al. TNF-α represses β-Klotho expression and impairs FGF21 action in adipose cells: involvement of JNK1 in the FGF21 pathway. Endocrinology. 2012 Sep;153(9):4238–4245. doi: 10.1210/en.2012-1193
  • Hanks LJ, Gutiérrez OM, Bamman MM, et al. Circulating levels of fibroblast growth factor-21 increase with age independently of body composition indices among healthy individuals. J Clin Transl Endocrinol. 2015 Jun 1;2(2):77–82. doi: 10.1016/j.jcte.2015.02.001
  • Xia S, Zhang X, Zheng S, et al. An update on inflamm-aging: mechanisms, prevention, and treatment. J Immunol Res. 2016;2016:8426874. doi: 10.1155/2016/8426874
  • Stein S, Bachmann A, Lössner U, et al. Serum levels of the adipokine FGF21 depend on renal function. Diabetes Care. 2009 Jan;32(1):126–128. doi: 10.2337/dc08-1054
  • Lin Z, Zhou Z, Liu Y, et al. Circulating FGF21 levels are progressively increased from the early to end stages of chronic kidney diseases and are associated with renal function in Chinese. PLoS One. 2011;6(4):e18398. doi: 10.1371/journal.pone.0018398
  • Hindricks J, Ebert T, Bachmann A, et al. Serum levels of fibroblast growth factor-21 are increased in chronic and acute renal dysfunction. Clin Endocrinol (Oxf). 2014 Jun;80(6):918–924. doi: 10.1111/cen.12380
  • Lee CH, Hui EY, Woo YC, et al. Circulating fibroblast growth factor 21 levels predict progressive kidney disease in subjects with type 2 diabetes and normoalbuminuria. J Clin Endocrinol Metab. 2015 Apr;100(4):1368–1375. doi: 10.1210/jc.2014-3465
  • Ruperez C, Lerin C, Ferrer-Curriu G, et al. Autophagic control of cardiac steatosis through FGF21 in obesity-associated cardiomyopathy. Int J Cardiol. 2018 Jun 1;260:163–170. doi: 10.1016/j.ijcard.2018.02.109
  • Zhu S, Wu Y, Ye X, et al. FGF21 ameliorates nonalcoholic fatty liver disease by inducing autophagy. Mol Cell Biochem. 2016 Sep;420(1–2):107–119. doi: 10.1007/s11010-016-2774-2
  • Cheng STW, SYT L, Leung PS. Fibroblast growth factor 21 stimulates pancreatic islet autophagy via inhibition of AMPK-mTOR signaling. Int J Mol Sci. 2019 May 22;20(10):2517. doi: 10.3390/ijms20102517
  • Zhou K, Chen H, Lin J, et al. FGF21 augments autophagy in random-pattern skin flaps via AMPK signaling pathways and improves tissue survival. Cell Death Dis. 2019 Nov 18;10(12):872. doi: 10.1038/s41419-019-2105-0
  • Zhang J, Cheng Y, Gu J, et al. Fenofibrate increases cardiac autophagy via FGF21/SIRT1 and prevents fibrosis and inflammation in the hearts of type 1 diabetic mice. Clin Sci. 2016 Apr;130(8):625–641. doi: 10.1042/CS20150623
  • Pandey UB, Nie Z, Batlevi Y, et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature. 2007 Jun 14;447(7146):859–863. doi: 10.1038/nature05853
  • Massey AC, Kaushik S, Sovak G, et al. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5805–5810. doi: 10.1073/pnas.0507436103
  • Planavila A, Redondo-Angulo I, Ribas F, et al. Fibroblast growth factor 21 protects the heart from oxidative stress. Cardiovasc Res. 2015 Apr 1;106(1):19–31. doi: 10.1093/cvr/cvu263
  • Wang XM, Xiao H, Liu LL, et al. FGF21 represses cerebrovascular aging via improving mitochondrial biogenesis and inhibiting p53 signaling pathway in an AMPK-dependent manner. Exp Cell Res. 2016 Aug 15;346(2):147–156. doi: 10.1016/j.yexcr.2016.06.020
  • Li X, Hong Y, He H, et al. FGF21 mediates mesenchymal stem Cell senescence via Regulation of mitochondrial Dynamics. Oxid Med Cell Longev. 2019;2019:4915149. doi: 10.1155/2019/4915149
  • Li S, Zhu Z, Xue M, et al. Fibroblast growth factor 21 protects the heart from angiotensin II-induced cardiac hypertrophy and dysfunction via SIRT1. Biochim Biophys Acta Mol Basis Dis. 2019 Jun 1;1865(6):1241–1252. doi: 10.1016/j.bbadis.2019.01.019
  • Liu X, Wang Y, Hou L, et al. Fibroblast growth factor 21 (FGF21) promotes formation of aerobic myofibers via the FGF21-SIRT1-AMPK-PGC1alpha pathway. J Cell Physiol. 2017 Jul;232(7):1893–1906. doi: 10.1002/jcp.25735
  • Nakamura J, Yamamoto T, Takabatake Y, et al. TFEB-mediated lysosomal exocytosis alleviates high-fat diet-induced lipotoxicity in the kidney. JCI Insight. 2023 Feb 22;8(4). doi: 10.1172/jci.insight.162498
  • Matsui I, Ito T, Kurihara H, et al. Snail, a transcriptional regulator, represses nephrin expression in glomerular epithelial cells of nephrotic rats. Lab Invest. 2007 Mar;87(3):273–283. doi: 10.1038/labinvest.3700518