GSK-3β inhibitor attenuates urinary albumin excretion in type 2 diabetic db/db mice, and delays epithelial-to-mesenchymal transition in mouse kidneys and podocytes
- Authors:
- Jia Wan
- Peng Li
- Dong‑Wei Liu
- Ying Chen
- Hai‑Zhen Mo
- Ben‑Guo Liu
- Wen‑Jie Chen
- Xiao‑Qing Lu
- Jia Guo
- Qian Zhang
- Ying‑Jin Qiao
- Zhang‑Suo Liu
- Guang‑Rui Wan
-
Affiliations: Henan Food and Drug Administration, Zhengzhou, Henan 450012, P.R. China, Pharmaceutical College, Xinxiang Medical University, Xinxiang, Henan 453003, P.R. China, Department of Nephrology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450012, P.R. China, School of Life Science and Technology, Henan Institute of Science and Technology, Xinxiang, Henan 453003, P.R. China, Department of Food Science, Henan Institute of Science and Technology, Xinxiang, Henan 453003, P.R. China, Modern Education Technology Center, Xinxiang Medical University, Xinxiang, Henan 453003, P.R. China - Published online on: June 23, 2016 https://doi.org/10.3892/mmr.2016.5441
- Pages: 1771-1784
This article is mentioned in:
Abstract
US Renal Data System: 2009 USRDS Annual Data Report: Epidemiology of kidney disease in the United States. National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases; Bethesda, MD: 2009 | |
de Boer IH, Rue TC, Hall YN, Heagerty PJ, Weiss NS and Himmelfarb J: Temporal trends in the prevalence of diabetic kidney disease in the United States. JAMA. 305:2532–2539. 2011. View Article : Google Scholar : PubMed/NCBI | |
Panchapakesan U, Pegg K, Gross S, Komala MG, Mudaliar H, Forbes J, Pollock C and Mather A: Effects of SGLT2 inhibition in human kidney proximal tubular cells-renoprotection in diabetic nephropathy? PLoS One. 8:e544422013. View Article : Google Scholar | |
Dronavalli S, Duka I and Bakris GL: The pathogenesis of diabetic nephropathy. Nat Clin Pract Endocrinol Metab. 4:444–452. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kanwar YS, Wada J, Sun L, Xie P, Wallner EI, Chen S, Chugh S and Danesh FR: Diabetic nephropathy: Mechanisms of renal disease progression. Exp Biol Med (Maywood). 233:4–11. 2008. View Article : Google Scholar | |
Wolf G and Ziyadeh FN: Molecular mechanisms of diabetic renal hypertrophy. Kidney Int. 56:393–405. 1999. View Article : Google Scholar : PubMed/NCBI | |
Wolf G and Ziyadeh FN: Cellular and molecular mechanisms of proteinuria in diabetic nephropathy. Nephron Physiol. 106:p26–p31. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lomelí C, Rosas-Peralta M, Lorenzo A and Saucedo N; Grupo de investigadores participantes en México para el estudio I-Search: Microalbuminuria and associated cardiovascular risk factors in patients with arterial systemic hypertension. A subanalysis of the I-Search study. Arch Cardiol Mex. 82:93–104. 2012.In Spanish. | |
Monhart V: Microalbuminuria. From diabetes to cardiovascular risk. Vnitr Lek. 57:293–298. 2011.In Czech. PubMed/NCBI | |
Ozyol A, Yucel O, Ege MR, Zorlu A and Yilmaz MB: Microalbuminuria is associated with the severity of coronary artery disease independently of other cardiovascular risk factors. Angiology. 63:457–460. 2012. View Article : Google Scholar | |
Udenze IC, Azinge EC, Ebuehi OA, Awolola NA, Adekola OO, Menkiti I and Irurhe NK: The relationship between microalbuminuria, cardiovascular risk factors and disease management in type 2 diabetes. Nig Q J Hosp Med. 22:34–38. 2012.PubMed/NCBI | |
Harris RC: Podocyte ACE2 protects against diabetic nephropathy. Kidney Int. 82:255–256. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wiggins RC: The spectrum of podocytopathies: A unifying view of glomerular diseases. Kidney Int. 71:1205–1214. 2007. View Article : Google Scholar : PubMed/NCBI | |
Reidy K and Susztak K: Epithelial-mesenchymal transition and podocyte loss in diabetic kidney disease. Am J Kidney Dis. 54:590–593. 2009. View Article : Google Scholar : PubMed/NCBI | |
Steffes MW, Schmidt D, McCrery R and Basgen JM; International Diabetic Nephropathy Study Group: Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int. 59:2104–2113. 2001. View Article : Google Scholar : PubMed/NCBI | |
Susztak K, Raff AC, Schiffer M and Böttinger EP: Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes. 55:225–233. 2006. View Article : Google Scholar | |
Thibodeau JF, Holterman CE, Burger D, Read NC, Reudelhuber TL and Kennedy CR: A novel mouse model of advanced diabetic kidney disease. PLoS One. 9:e1134592014. View Article : Google Scholar : PubMed/NCBI | |
Hu P, Wang G, Shen M, Zhang P, Zhang J, Du J and Liu Q: Intratumoral polymorphonuclear granulocyte is associated with poor prognosis in squamous esophageal cancer by promoting epithelial-mesenchymal transition. Future Oncol. 11:771–783. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dai HY, Zheng M, Lv LL, Tang RN, Ma KL, Liu D, Wu M and Liu BC: The roles of connective tissue growth factor and integrin-linked kinase in high glucose-induced phenotypic alterations of podocytes. J Cell Biochem. 113:293–301. 2012. View Article : Google Scholar | |
Liang Y, Jing Z, Deng H, Li Z, Zhuang Z, Wang S and Wang Y: Soluble epoxide hydrolase inhibition ameliorates proteinuria-induced epithelial-mesenchymal transition by regulating the PI3K-Akt-GSK-3β signaling pathway. Biochem Biophys Res Commun. 463:70–75. 2015. View Article : Google Scholar : PubMed/NCBI | |
Obligado SH, Ibraghimov-Beskrovnaya O, Zuk A, Meijer L and Nelson PJ: CDK/GSK-3 inhibitors as therapeutic agents for parenchymal renal diseases. Kidney Int. 73:684–690. 2008. View Article : Google Scholar | |
Mundel P, Reiser J, Zúñiga Mejía Borja A, Pavenstädt H, Davidson GR, Kriz W and Zeller R: Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines. Exp Cell Res. 236:248–258. 1997. View Article : Google Scholar : PubMed/NCBI | |
Dai C, Stolz DB, Kiss LP, Monga SP, Holzman LB and Liu Y: Wnt/beta-catenin signaling promotes podocyte dysfunction and albuminuria. J Am Soc Nephrol. 20:1997–2008. 2009. View Article : Google Scholar : PubMed/NCBI | |
Jonathan Ryves W, Dalton EC, Harwood AJ and Williams RS: GSK-3 activity in neocortical cells is inhibited by lithium but not carbamazepine or valproic acid. Bipolar Disord. 7:260–265. 2005. View Article : Google Scholar : PubMed/NCBI | |
Hummel KP, Dickie MM and Coleman DL: Diabetes, a new mutation in the mouse. Science. 153:1127–1128. 1966. View Article : Google Scholar : PubMed/NCBI | |
Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, Lakey ND, Culpepper J, Moore KJ, Breitbart RE, et al: Evidence that the diabetes gene encodes the leptin receptor: Identification of a mutation in the leptin receptor gene in db/db mice. Cell. 84:491–495. 1996. View Article : Google Scholar : PubMed/NCBI | |
Lee GH, Proenca R, Montez JM, Carroll KM, Darvishzadeh JG, Lee JI and Friedman JM: Abnormal splicing of the leptin receptor in diabetic mice. Nature. 379:632–635. 1996. View Article : Google Scholar : PubMed/NCBI | |
Hummel KP, Coleman DL and Lane PW: The influence of genetic background on expression of mutations at the diabetes locus in the mouse. I. C57BL-KsJ and C57BL-6J strains. Biochem Genet. 7:1–13. 1972. View Article : Google Scholar : PubMed/NCBI | |
Chua S Jr, Liu SM, Li Q, Yang L, Thassanapaff VT and Fisher P: Differential beta cell responses to hyperglycaemia and insulin resistance in two novel congenic strains of diabetes (FVB-Lepr (db)) and obese (DBA-Lep (ob)) mice. Diabetologia. 45:976–990. 2002. View Article : Google Scholar : PubMed/NCBI | |
Cohen MP, Clements RS, Cohen JA and Shearman CW: Prevention of decline in renal function in the diabetic db/db mouse. Diabetologia. 39:270–274. 1996. View Article : Google Scholar : PubMed/NCBI | |
Lim AK, Ma FY, Nikolic-Paterson DJ, Thomas MC, Hurst LA and Tesch GH: Antibody blockade of c-fms suppresses the progression of inflammation and injury in early diabetic nephropathy in obese db/db mice. Diabetologia. 52:1669–1679. 2009. View Article : Google Scholar : PubMed/NCBI | |
Chow FY, Nikolic-Paterson DJ, Ozols E, Atkins RC and Tesch GH: Intercellular adhesion molecule-1 deficiency is protective against nephropathy in type 2 diabetic db/db mice. J Am Soc Nephrol. 16:1711–1722. 2005. View Article : Google Scholar : PubMed/NCBI | |
Chodavarapu H, Grobe N, Somineni HK, Salem ES, Madhu M and Elased KM: Rosiglitazone treatment of type 2 diabetic db/db mice attenuates urinary albumin and angiotensin converting enzyme 2 excretion. PLoS One. 8:e628332013. View Article : Google Scholar : PubMed/NCBI | |
Vivanco I and Sawyers CL: The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer. 2:489–501. 2002. View Article : Google Scholar : PubMed/NCBI | |
Ward SG and Finan P: Isoform-specific phosphoinositide 3-kinase inhibitors as therapeutic agents. Curr Opin Pharmacol. 3:426–434. 2003. View Article : Google Scholar : PubMed/NCBI | |
Franke TF, Hornik CP, Segev L, Shostak GA and Sugimoto C: PI3 K/Akt and apoptosis: Size matters. Oncogene. 22:8983–8998. 2003. View Article : Google Scholar : PubMed/NCBI | |
Chua S Jr, Li Y, Liu SM, Liu R, Chan KT, Martino J, Zheng Z, Susztak K, D'Agati VD and Gharavi AG: A susceptibility gene for kidney disease in an obese mouse model of type II diabetes maps to chromosome 8. Kidney Int. 78:453–462. 2010. View Article : Google Scholar : PubMed/NCBI | |
Taneda S, Honda K, Ohno M, Uchida K, Nitta K and Oda H: Podocyte and endothelial injury in focal segmental glomerulosclerosis: An ultrastructural analysis. Virchows Arch. 467:449–458. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lenoir O, Jasiek M, Hénique C, Guyonnet L, Hartleben B, Bork T, Chipont A, Flosseau K, Bensaada I, Schmitt A, et al: Endothelial cell and podocyte autophagy synergistically protect from diabetes-induced glomerulosclerosis. Autophagy. 11:1130–1145. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dai C, Stolz DB, Bastacky SI, St-Arnaud R, Wu C, Dedhar S and Liu Y: Essential role of integrin-linked kinase in podocyte biology: Bridging the integrin and slit diaphragm signaling. J Am Soc Nephrol. 17:2164–2175. 2006. View Article : Google Scholar : PubMed/NCBI | |
Xu W, Chen J, Lin J, Liu D, Mo L, Pan W, Feng J, Wu W and Zheng D: Exogenous H2S protects H9c2 cardiac cells against high glucose-induced injury and inflammation by inhibiting the activation of the NF-κB and IL-1β pathways. Int J Mol Med. 35:177–186. 2015. | |
El-Aouni C, Herbach N, Blattner SM, Henger A, Rastaldi MP, Jarad G, Miner JH, Moeller MJ, St-Arnaud R, Dedhar S, et al: Podocyte-specific deletion of integrin-linked kinase results in severe glomerular basement membrane alterations and progressive glomerulosclerosis. J Am Soc Nephrol. 17:1334–1344. 2006. View Article : Google Scholar : PubMed/NCBI | |
Langham RG, Kelly DJ, Cox AJ, Thomson NM, Holthöfer H, Zaoui P, Pinel N, Cordonnier DJ and Gilbert RE: Proteinuria and the expression of the podocyte slit diaphragm protein, nephrin, in diabetic nephropathy: Effects of angiotensin converting enzyme inhibition. Diabetologia. 45:1572–1576. 2002. View Article : Google Scholar : PubMed/NCBI | |
Nakatsue T, Koike H, Han GD, Suzuki K, Miyauchi N, Yuan H, Salant DJ, Gejyo F, Shimizu F and Kawachi H: Nephrin and podocin dissociate at the onset of proteinuria in experimental membranous nephropathy. Kidney Int. 67:2239–2253. 2005. View Article : Google Scholar : PubMed/NCBI | |
Mundel P, Heid HW, Mundel TM, Krüger M, Reiser J and Kriz W: Synaptopodin: An actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol. 139:193–204. 1997. View Article : Google Scholar : PubMed/NCBI | |
Liu W, Hu M, Wang Y, Sun B, Guo Y, Xu Z, Li J and Han B: Overexpression of interleukin-18 protein reduces viability and induces apoptosis of tongue squamous cell carcinoma cells by activation of glycogen synthase kinase-3β signaling. Oncol Rep. 33:1049–1056. 2015.PubMed/NCBI | |
Kang YS, Li Y, Dai C, Kiss LP, Wu C and Liu Y: Inhibition of integrin linked kinase blocks podocyte epithelial mesenchymal transition and ameliorates proteinuria. Kidney Int. 78:363–373. 2010. View Article : Google Scholar : PubMed/NCBI | |
Cai X, Han X, Luo Y and Ji L: Analysis of insulin doses of Chinese type 2 diabetic patients with intensive insulin treatment. PLoS One. 7:e389622012. View Article : Google Scholar : PubMed/NCBI | |
Tang L, Yi R, Yang B, Li H, Chen H and Liu Z: Valsartan inhibited HIF-1α pathway and attenuated renal interstitial fibrosis in streptozotocin-diabetic rats. Diabetes Res Clin Pract. 97:125–131. 2012. View Article : Google Scholar : PubMed/NCBI | |
Berwick DC, Hers I, Heesom KJ, Moule SK and Tavare JM: The identification of ATP-citrate lyase as a protein kinase B (Akt) substrate in primary adipocytes. J Biol Chem. 277:33895–33900. 2002. View Article : Google Scholar : PubMed/NCBI | |
Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J and Greenberg ME: Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 96:857–868. 1999. View Article : Google Scholar : PubMed/NCBI | |
Figueroa C, Tarras S, Taylor J and Vojtek AB: Akt2 negatively regulates assembly of the POSH-MLK-JNK signaling complex. J Biol Chem. 278:47922–47927. 2003. View Article : Google Scholar : PubMed/NCBI | |
Kim WY and Snider WD: Functions of GSK-3 Signaling in development of the nervous system. Front Mol Neurosci. 4:442011. View Article : Google Scholar : PubMed/NCBI | |
Lee J and Kim MS: The role of GSK3 in glucose homeostasis and the development of insulin resistance. Diabetes Res Clin Pract. 77(Suppl 1): S49–S57. 2007. View Article : Google Scholar : PubMed/NCBI | |
Yoshino J, Monkawa T, Tsuji M, Inukai M, Itoh H and Hayashi M: Snail1 is involved in the renal epithelial-mesenchymal transition. Biochem Biophys Res Commun. 362:63–68. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bachelder RE, Yoon SO, Franci C, de Herreros AG and Mercurio AM: Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: Implications for the epithelial-mesenchymal transition. J Cell Biol. 168:29–33. 2005. View Article : Google Scholar : PubMed/NCBI | |
Jiang J and Griffin JD: Wnt/β-catenin pathway modulates the sensitivity of the mutant flt3 receptor kinase inhibitors in a GSK-3β dependent manner. Genes Cancer. 1:164–176. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M and Hung MC: Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol. 6:931–940. 2004. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Feng W, Xue W, Tan Y, Hein DW, Li XK and Cai L: Inactivation of GSK-3beta by metallothionein prevents diabetes-related changes in cardiac energy metabolism, inflammation, nitrosative damage and remodeling. Diabetes. 58:1391–1402. 2009. View Article : Google Scholar : PubMed/NCBI | |
Shi WR, Liu Y, Xie JD, Zhuo S, Tu CX and Xie ZF: Changes in Wnt pathway inhibiting factors in nitrosamine-induced esophageal precancerosis lesions and effect of gexia zhuyu decoction. Zhongguo Zhong Yao Za Zhi. 39:3131–3135. 2014.In Chinese. PubMed/NCBI | |
Mariappan MM, Shetty M, Sataranatarajan K, Choudhury GG and Kasinath BS: Glycogen synthase kinase 3beta is a novel regulator of high glucose- and high insulin-induced extracellular matrix protein synthesis in renal proximal tubular epithelial cells. J Biol Chem. 283:30566–30575. 2008. View Article : Google Scholar : PubMed/NCBI | |
Yao CJ, Lai GM, Yeh CT, Lai MT, Shih PH, Chao WJ, Whang-Peng J, Chuang SE and Lai TY: Honokiol eliminates human oral cancer stem-like cells accompanied with suppression of Wnt/β-catenin signaling and apoptosis induction. Evid Based Complement Alternat Med. 2013:1461362013. View Article : Google Scholar | |
Li Y, Kang YS, Dai C, Kiss LP, Wen X and Liu Y: Epithelial-to-mesenchymal transition is a potential pathway leading to podocyte dysfunction and proteinuria. Am J Pathol. 172:299–308. 2008. View Article : Google Scholar : PubMed/NCBI | |
Solanas G, Porta-de-la-Riva M, Agustí C, Casagolda D, Sánchez-Aguilera F, Larriba MJ, Pons F, Peiró S, Escrivà M, Muñoz A, et al: E-cadherin controls beta-catenin and NF-kappaB transcriptional activity in mesenchymal gene expression. J Cell Sci. 121:2224–2234. 2008. View Article : Google Scholar : PubMed/NCBI | |
Cozzolino M, Brenna I, Volpi E, Ciceri P, Mehmeti F and Cusi D: Restoring the physiology of vitamin D receptor activation and the concept of selectivity. Contrib Nephrol. 171:151–156. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Deb DK, Kong J, Ning G, Wang Y, Li G, Chen Y, Zhang Z, Strugnell S, Sabbagh Y, et al: Long-term therapeutic effect of vitamin D analog doxercalciferol on diabetic nephropathy: Strong synergism with AT1 receptor antagonist. Am J Physiol Renal Physiol. 297:F791–F801. 2009. View Article : Google Scholar : PubMed/NCBI | |
Fretz JA, Zella LA, Kim S, Shevde NK and Pike JW: 1, 25-Dihydroxyvitamin D3 regulates the expression of low-density lipoprotein receptor-related protein 5 via deoxyribonucleic acid sequence elements located downstream of the start site of transcription. Mol Endocrinol. 20:2215–2230. 2006. View Article : Google Scholar : PubMed/NCBI | |
Rincon-Choles H, Vasylyeva TL, Pergola PE, Bhandari B, Bhandari K, Zhang JH, Wang W, Gorin Y, Barnes JL and Abboud HE: ZO-1 expression and phosphorylation in diabetic nephropathy. Diabetes. 55:894–900. 2006. View Article : Google Scholar : PubMed/NCBI | |
Xiong M, Gong J, Liu Y, Xiang R and Tan X: Loss of vitamin D receptor in chronic kidney disease: A potential mechanism linking inflammation to epithelial-to-mesenchymal transition. Am J Physiol Renal Physiol. 303:F1107–F1115. 2012. View Article : Google Scholar : PubMed/NCBI | |
Song H, Deng B, Zou C, Huai W, Zhao R and Zhao W: GSK3β negatively regulates LPS-induced osteopontin expression via inhibiting its transcription. Scand J Immunol. 81:186–191. 2015. View Article : Google Scholar : PubMed/NCBI | |
Liu Y: New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol. 21:212–222. 2010. View Article : Google Scholar | |
Jope RS, Yuskaitis CJ and Beurel E: Glycogen synthase kinase-3 (GSK3): Inflammation, diseases and therapeutics. Neurochem Res. 32:577–595. 2007. View Article : Google Scholar | |
Lin CL, Wang JY, Huang YT, Kuo YH, Surendran K and Wang FS: Wnt/beta-catenin signaling modulates survival of high glucose-stressed mesangial cells. J Am Soc Nephrol. 17:2812–2820. 2006. View Article : Google Scholar : PubMed/NCBI | |
Costabile V, Duraturo F, Delrio P, Rega D, Pace U, Liccardo R, Rossi GB, Genesio R, Nitsch L, Izzo P and de Rosa M: Lithium chloride induces mesenchymal-to-epithelial reverting transition in primary colon cancer cell cultures. Int J Oncol. 46:1913–1923. 2015.PubMed/NCBI |