Apigenin inhibits indoxyl sulfate-induced endoplasmic reticulum stress and anti-proliferative pathways, CHOP and IL-6/p21, in human renal proximal tubular cells

European Review for Medical and Pharmacological Sciences

Volumn 19, Issue 12, 2015, Pages 2303-2310

  Jeon, B J ^a   Yang, H M ^a   Lyu, Y S ^a   Pae, H O ^a   Ju, S M ^a   Jeon, B H ^a  

^a Wonkwang University   (South Korea)

Author keywords

Apigenin; CHOP; ER stress; HK 2 cells; Indoxyl sulfate; P21

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; APIGENIN; CYCLIN D1; GLUCOSE REGULATED PROTEIN 78; GLYCOGEN SYNTHASE KINASE 3BETA; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INDICAN; INITIATION FACTOR 2ALPHA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P21; RETINOBLASTOMA PROTEIN; SALUBRINAL; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DDIT3 PROTEIN, HUMAN; IL6 PROTEIN, HUMAN;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL PROLIFERATION; CELL VIABILITY ASSAY; CONTROLLED STUDY; CULTURE MEDIUM; DRUG EFFECT; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMORTALIZED CELL LINE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; MTT ASSAY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CYCLE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; TRANSFORMED CELL LINE;

APIGENIN; CELL CYCLE; CELL LINE, TRANSFORMED; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ENDOPLASMIC RETICULUM STRESS; HUMANS; INDICAN; INTERLEUKIN-6; KIDNEY TUBULES, PROXIMAL; TRANSCRIPTION FACTOR CHOP;

EID: 84942292099     PISSN: 11283602     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (44)

1. RON D, WALTER P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529.
2. KOMOIKE Y, INAMURA H, MATSUOKA M. Effects of salubrinal on cadmium-induced apoptosis in HK-2 human renal proximal tubular cells. Arch Toxicol 2012;86:37-44.
3. INAGI R. Endoplasmic reticulum stress as a progression factor for kidney injury. Curr Opin Pharmacol 2010;10:156-165.
4. MIYAZAKI T, ISE M, SEO H, NIWA T. Indoxyl sulfate increases the gene expressions of TGF-beta 1, TIMP-1 and pro-alpha 1 (I) collagen in uremic rat kidneys. Kidney Int Suppl 1997;62:S15-22.
5. NIWA T, ISE M. Indoxyl sulfate, a circulating uremic toxin, stimulates the progression of glomerular sclerosis. J Lab Clin Med 1994;124:96-104.
6. NIWA T, ISE M, MIYAZAKI T. Progression of glomerular sclerosis in experimental uremic rats by administration of indole, a precursor of indoxyl sulfate. Am J Nephrol 1994;14:207-212.
7. SHIMIZU H, BOLATI D, ADIJIANG A, ADELIBIEKE Y, MUTELIEFU G, ENOMOTO A, HIGASHIYAMA Y, HIGUCHI Y, NISHIJIMA F, NIWA T. Indoxyl sulfate downregulates renal expression of Klotho through production of ROS and activation of nuclear factor-κGB. Am J Nephrol 2011;33:319-324.
8. ENOMOTO A, TAKEDA M, TOJO A, SEKINE T, CHA SH, KHAMDANG S, TAKAYAMA F, AOYAMA I, NAKAMURA S, ENDOU H, NIWA T. Role of organic anion transporters in the tubular transport of indoxyl sulfate and the induction of its nephrotoxicity. J Am Soc Nephrol 2002;13:1711-1720.
9. MOTOJIMA M, HOSOKAWA A, YAMATO H, MURAKI T, YOSHIOKA T. Uremic toxins of organic anions upregulate PAI-1 expression by induction of NF-kappaB and free radical in proximal tubular cells. Kidney Int 2003;63:1671-1680.
10. LEKAWANVIJIT S, ADRAHTAS A, KELLY DJ, KOMPA AR, WANG BH, KRUM H. Does indoxyl sulfate, a uraemic toxin, have direct effects on cardiac fibroblasts and myocytes? Eur Heart J 2010;31:1771-1779.
11. TUMUR Z, SHIMIZU H, ENOMOTO A, MIYAZAKI H, NIWA T. Indoxyl sulfate upregulates expression of ICAM-1 and MCP-1 by oxidative stress-induced NF-kappaB activation. Am J Nephrol 2010;31:435-441.
12. MUTELIEFU G, ENOMOTO A, NIWA T. Indoxyl sulfate promotes proliferation of human aortic smooth muscle cells by inducing oxidative stress. J Ren Nutr 2009;19:29-32.
13. SHIMIZU H, HIROSE Y, NISHIJIMA F, TSUBAKIHARA Y, MIYAZAKI H. ROS and PDGF-beta [corrected] receptors are critically involved in indoxyl sulfate actions that promote vascular smooth muscle cell proliferation and migration. Am J Physiol Cell Physiol 2009;297:C389-396.
14. ADIJIANG A, GOTO S, URAMOTO S, NISHIJIMA F, NIWA T. Indoxyl sulphate promotes aortic calcification with expression of osteoblast-specific proteins in hypertensive rats. Nephrol Dial Transplant 2008;23:1892-1901.
15. MUTELIEFU G, ENOMOTO A, JIANG P, TAKAHASHI M, NIWA T. Indoxyl sulphate induces oxidative stress and the expression of osteoblast-specific proteins in vascular smooth muscle cells. Nephrol Dial Transplant 2009;24:2051-2058.
16. TAKI K, TSURUTA Y, NIWA T. Indoxyl sulfate and atherosclerotic risk factors in hemodialysis patients. Am J Nephrol 2007;27:30-35.
17. KAWAKAMI T, INAGI R, WADA T, TANAKA T, FUJITA T, NANGAKU M. Indoxyl sulfate inhibits proliferation of human proximal tubular cells via endoplasmic reticulum stress. Am J Physiol Renal Physiol 2010;299:F568-576.
18. MANACH C, SCALBERT A, MORAND C, REMESY C, JIMENEZ L. Polyphenols: food sources and bioavailability. Am J Clin Nutr 2004;79:727-747.
19. SURH YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 2003;3:768-780.
20. SINGH JP, SELVENDIRAN K, BANU SM, PADMAVATHI R, SAKTHISEKARAN D. Protective role of Apigenin on the status of lipid peroxidation and antioxidant defense against hepatocarcinogenesis in Wistar albino rats. Phytomedicine 2004;11:309-314.
21. HA SK, LEE P, PARK JA, OH HR, LEE SY, PARK JH, LEE EH, RYU JH, LEE KR, KIM SY. Apigenin inhibits the production of NO and PGE2 in microglia and inhibits neuronal cell death in a middle cerebral artery occlusion-induced focal ischemia mice model. Neurochem Int 2008;52:878-886.
22. MYHRSTAD MC, CARLSEN H, NORDSTROM O, BLOMHOFF R, MOSKAUG JO. Flavonoids increase the intracellular glutathione level by transactivation of the gammaglutamylcysteine synthetase catalytical subunit promoter. Free Radic Biol Med 2002;32:386-393.
23. WEI H, TYE L, BRESNICK E, BIRT DF. Inhibitory effect of apigenin, a plant flavonoid, on epidermal ornithine decarboxylase and skin tumor promotion in mice. Cancer Res 1990;50:499-502.
24. CHOI AY, CHOI JH, LEE JY, YOON KS, CHOE W, HA J, YEO EJ, KANG I. Apigenin protects HT22 murine hippocampal neuronal cells against endoplasmic reticulum stress-induced apoptosis. Neurochem Int 2010;57:143-152.
25. SHERR CJ, ROBERTS JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999;13:1501-1512.
26. SARRO E, JACOBS-CACHA C, ITARTE E, MESEGUER A. A pharmacologically-based array to identify targets of cyclosporine A-induced toxicity in cultured renal proximal tubule cells. Toxicol Appl Pharmacol 2012;258:275-287.
27. LIANG J, SLINGERLAND JM. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003;2:339-345.
28. WANG CY, TSAI AC, PENG CY, CHANG YL, LEE KH, TENG CM, PAN SL. Dehydrocostuslactone suppresses angiogenesis in vitro and in vivo through inhibition of Akt/GSK-3β and mTOR signaling pathways. PLoS One 2012;7:e31195.
29. DIEHL JA, CHENG M, ROUSSEL MF, SHERR CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998;12:3499-3511.
30. DIEHL JA, ZINDY F, SHERR CJ. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev 1997;11:957-972.
31. GIACINTI C, GIORDANO A. RB and cell cycle progression. Oncogene 2006;25:5220-5227.
32. SHERR CJ, MCCORMICK F. The RB and p53 pathways in cancer. Cancer Cell 2002;2:103-112.
33. BREWER JW, DIEHL JA. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc Natl Acad Sci USA 2000;97:12625-12630.
34. BREWER JW, HENDERSHOT LM, SHERR CJ, DIEHL JA. Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression. Proc Natl Acad Sci USA 1999;96:8505-8510.
35. XU C, BAILLY-MAITRE B, REED JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005;115:2656-2664.
36. NICHOLAS C, BATRA S, VARGO MA, VOSS OH, GAVRILIN MA, WEWERS MD, GUTTRIDGE DC, GROTEWOLD E, DOSEFF AI. Apigenin blocks lipopolysaccharide-induced lethality in vivo and proinflammatory cytokines expression by inactivating NF-kappaB through the suppression of p65 phosphorylation. J Immunol 2007;179:7121-7127.
37. KANG OH, LEE JH, KWON DY. Apigenin inhibits release of inflammatory mediators by blocking the NF-κGB activation pathways in the HMC-1 cells. Immunopharmacol Immunotoxicol 2011;3:473-479.
38. WANG J, LIAO Y, FAN J, YE T, SUN X, DONG S. Apigenin inhibits the expression of IL-6, IL-8, and ICAM-1 in DEHP-stimulated human umbilical vein endothelial cells and in vivo. Inflammation 2012;35:1466-1476.
39. SHUKLA S, GUPTA S. Apigenin suppresses insulinlike growth factor I receptor signaling in human prostate cancer: an in vitro and in vivo study. Mol Carcinog 2009;48:243-252.
40. ORNELAS IM, SILVA TM, FRAGEL-MADEIRA L, VENTURA AL. Inhibition of PI3K/Akt pathway impairs G2/M transition of cell cycle in late developing progenitors of the avian embryo retina. PLoS One 2013;8:e53517.
41. ONG CS, ZHOU J, ONG CN, SHEN HM. Luteolin induces G1 arrest in human nasopharyngeal carcinoma cells via the Akt-GSK-3β-Cyclin D1 pathway. Cancer Lett 2010;298:167-175.
42. KNUDSEN ES, WANG JY. Dual mechanisms for the inhibition of E2F binding to RB by cyclin-dependent kinase-mediated RB phosphorylation. Mol Cell Biol 1997;17:5771-5783.
43. RAVEN JF, BALTZIS D, WANG S, MOUNIR Z, PAPADAKIS AI, GAO HQ, KOROMILAS AE. PKR and PKR-like endoplasmic reticulum kinase induce the proteasomedependent degradation of cyclin D1 via a mechanism requiring eukaryotic initiation factor 2alpha phosphorylation. J Biol Chem 2008;283:3097-3108.
44. BALTZIS D, PLUQUET O, PAPADAKIS AI, KAZEMI S, QU LK, KOROMILAS AE. The eIF2alpha kinases PERK and PKR activate glycogen synthase kinase 3 to promote the proteasomal degradation of p53. J Biol Chem 2007;282:31675-31687.