NF-κb plays an important role in indoxyl sulfate-induced cellular senescence, fibrotic gene expression, and inhibition of proliferation in proximal tubular cells

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 5, 2011, Pages

  Shimizu, Hidehisa ^a   Bolati, Dilinaer ^a   Adijiang, Ayinuer ^a   Muteliefu, Gulinuer ^a   Enomoto, Atsushi ^b   Nishijima, Fuyuhiko ^c   Dateki, Minori ^d   Niwa, Toshimitsu ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c KUREHA CORPORATION   (Japan)

^d TOHO UNIVERSITY   (Japan)

Author keywords

AST 120; Chronic renal failure; Renal fibrosis; Uremic toxin

Indexed keywords

ACETYLCYSTEINE; ALPHA SMOOTH MUSCLE ACTIN; INDICAN; MESSENGER RNA; PROTEIN P53; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ARTICLE; CELL AGING; CELL PROLIFERATION; CHRONIC KIDNEY FAILURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INHIBITION KINETICS; KIDNEY PROXIMAL TUBULE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; RAT; RNA ISOLATION; SENESCENCE; UPREGULATION;

ACTINS; ACUTE KIDNEY INJURY; ANIMALS; BENZOTHIAZOLES; BETA-GALACTOSIDASE; CELL AGING; CELL LINE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; HUMANS; INDICAN; KIDNEY TUBULES, PROXIMAL; MALE; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PYRROLIDINES; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SESQUITERPENES; THIOCARBAMATES; TOLUENE; TRANSFORMING GROWTH FACTOR BETA1; TUMOR SUPPRESSOR PROTEIN P53;

RATTUS;

EID: 80054884869     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00471.2010     Document Type: Article

References (47)

1. 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 23: 1892-1901, 2008.
2. Adijiang A, Niwa T. An oral sorbent, AST-120, increases Klotho expression and inhibits cell senescence in the kidney of uremic rats. Am J Nephrol 31: 160-164, 2010.
3. Adler AS, Kawahara TL, Segal E, Chang HY. Reversal of aging by NFkappaB blockade. Cell Cycle 7: 556-559, 2008.
4. Adler AS, Sinha S, Kawahara TL, Zhang JY, Segal E, Chang HY. Motif module map reveals enforcement of aging by continual NF-kappaB activity. Genes Dev 21: 3244-3257, 2007.
5. Aleyasin H, Cregan SP, Iyirhiaro G, O'Hare MJ, Callaghan SM, Slack RS, Park DS. Nuclear factor-(kappa)B modulates the p53 response in neurons exposed to DNA damage. J Neurosci 24: 2963-2973, 2004.
6. Benoit V, Hellin AC, Huygen S, Gielen J, Bours V, Merville MP. Additive effect between NF-kappaB subunits and p53 protein for transcriptional activation of human p53 promoter. Oncogene 19: 4787-4794, 2000.
7. Brink TC, Regenbrecht C, Demetrius L, Lehrach H, Adjaye J. Activation of the immune response is a key feature of aging in mice. Biogerontology 10: 721-734, 2009.
8. Comer KA, Dennis PA, Armstrong L, Catino JJ, Kastan MB, Kumar CC. Human smooth muscle alpha-actin gene is a transcriptional target of the p53 tumor suppressor protein. Oncogene 16: 1299-1308, 1998.
9. Doi S, Zou Y, Togao O, Pastor JV, John GB, Wang L, Shiizaki K, Gotschall R, Schiavi S, Yorioka N, Takahashi M, Boothman DA, Kuro-o M. Klotho inhibits transforming growth factor-beta1 (TGF-beta1) signaling and suppresses renal fibrosis and cancer metastasis in mice. J Biol Chem 286: 8655-8665, 2011.
10. Dou L, Bertrand E, Cerini C, Faure V, Sampol J, Vanholder R, Berland Y, Brunet P. The uremic solutes p-cresol and indoxyl sulfate inhibit endothelial proliferation and wound repair. Kidney Int 65: 442-451, 2004.
11. Dou L, Jourde-Chiche N, Faure V, Cerini C, Berland Y, Dignat-George F, Brunet P. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells. J Thromb Haemost 5: 1302-1308, 2007.
12. 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 13: 1711-1720, 2002.
13. Fan JM, Ng YY, Hill PA, Nikolic-Paterson DJ, Mu W, Atkins RC, Lan HY. Transforming growth factor-beta regulates tubular epithelial-myofibroblast transdifferentiation in vitro. Kidney Int 56: 1455-1467, 1999.
14. Fan YY, Kohno M, Hitomi H, Kitada K, Fujisawa Y, Yatabe J, Yatabe M, Felder RA, Ohsaki H, Rafiq K, Sherajee SJ, Noma T, Nishiyama A, Nakano D. Aldosterone/Mineralocorticoid receptor stimulation induces cellular senescence in the kidney. Endocrinology 152: 680-688, 2011.
15. Hemmati PG, Normand G, Verdoodt B, von Haefen C, Hasenjäger A, Güner D, Wendt J, Dörken B, Daniel PT. Loss of p21 disrupts p14 ARF-induced G1 cell cycle arrest but augments p14 ARF-induced apoptosis in human carcinoma cells. Oncogene 24: 4114-4128, 2005.
16. Helenius M, Hänninen M, Lehtinen SK, Salminen A. Changes associated with aging and replicative senescence in the regulation of transcription factor nuclear factor-kappa B. Biochem J 318: 603-608, 1996.
17. Hellin AC, Calmant P, Gielen J, Bours V, Merville MP. Nuculear factor-kappaB-dependent regulation of p53 gene expression induced by daunomycin genotoxic drug. Oncogene 16: 1187-1195, 1998.
18. Hwang I, Choi YS, Jeon MY, Jeong S. NF-κB p65 represses β-cateninactivated transcription of cyclin D1. Biochem Biophys Res Commun 403: 79-84, 2010.
19. Ito S, Osaka M, Higuchi Y, Nishijima F, Ishii H, Yoshida M. Indoxyl sulfate induces leukocyte-endothelial interactions through upregulation of E-selectin. J Biol Chem 285: 38869-38875, 2010.
20. Kirch HC, Flaswinkel S, Rumpf H, Brockmann D, Esche H. Expression of human p53 requires synergistic activation of transcription from the p53 promoter by AP-1, NF-kappaB and Myc/Max. Oncogene 18: 2728-2738, 1999.
21. 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 31: 1771-1779, 2010.
22. Lim CF, Bernard BF, de Jong M, Docter R, Krenning EP, Hennemann G. A furan fatty acid and indoxyl sulfate are the putative inhibitors of thyroxine hepatocyte transport in uremia. J Clin Endocrinol Metab 76: 318-324, 1993.
23. Liu SF, Ye X, Malik AB. Pyrrolidine dithiocarbamate prevents I.-kappaB degradation and reduces microvascular injury induced by lipopolysaccharide in multiple organs. Mol Pharmacol 55: 658-667, 1999.
24. Masai N, Tatebe J, Yoshino G, Morita T. Indoxyl sulfate stimulates monocyte chemoattractant protein-1 expression in human umbilical vein endothelial cells by inducing oxidative stress through activation of the N.A.D.P.H. oxidase-nuclear factor-k B. pathway. Circ J 74: 2216-2224, 2010.
25. Miyazaki T, Aoyama I, Ise M, Seo H, Niwa T. An oral sorbent reduces overload of indoxyl sulphate and gene expression of TGF-beta1 in uraemic rat kidneys. Nephrol Dial Transplant 15: 1773-1781, 2000.
26. Miyazaki T, Ise M, Hirata M, Endo K, Ito Y, Seo H, Niwa T. Indoxyl sulfate stimulates renal synthesis of transforming growth factor-β1 and progression of renal failure. Kidney Int Suppl 63: S211-S214, 1997.
27. Miyazaki T, Ise M, Seo H, Niwa T. Indoxyl sulfate increases the gene expressions of TGF-β1, TIMP-1 and pro-a1pha 1(I) collagen in uremic rat kidneys. Kidney Int Suppl 62: S15-S22, 1997.
28. Motojima M, Hosokawa A, Yamato H, Muraki T, Yoshioka T. Uremic toxins of organic anions up-regulate PAI-1 expression by induction of NF-κB and free radical in proximal tubular cells. Kidney Int 63: 1671-1680, 2003.
29. 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 24: 2051-2058, 2009.
30. Muteliefu G, Enomoto A, Niwa T. Indoxyl sulfate promotes proliferation of human aortic smooth muscle cells by inducing oxidative stress. J Ren Nutr 19: 29-32, 2009.
31. Nakagawa N, Hasebe N, Sumitomo K, Fujino T, Fukuzawa J, Hirayama T, Kikuchi K. An oral adsorbent, AST-120, suppresses oxidative stress in uremic rats. Am J Nephrol 26: 455-461, 2006.
32. Niwa T, Ise M. Indoxyl sulfate, a circulating uremic toxin, stimulates the progression of glomerular sclerosis. J Lab Clin Med 124: 96-104, 1994.
33. 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 14: 207-212, 1994.
34. Oh SM, Pyo CW, Kim Y, Choi SY. Neutrophil lactoferrin upregulates the human p53 gene through induction of NF-kappaB activation cascade. Oncogene 23: 8282-8291, 2004.
35. Ravi R, Mookerjee B, van Hensbergen Y, Bedi GC, Giordano A, El-Deiry WS, Fuchs EJ, Bedi A. p53-mediated repression of nuclear factor-kappaB RelA via the transcriptional integrator p300. Cancer Res 58: 4531-4536, 1998.
36. Ruan H, Pownall HJ, Lodish HF. Troglitazone antagonizes tumor necrosis factor-alpha-induced reprogramming of adipocyte gene expression by inhibiting the transcriptional regulatory functions of NF-kB. J Biol Chem 278: 28181-28192, 2003.
37. 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-_B. Am J Nephrol. 33: 319-324, 2011.
38. Shimizu H, Bolati D, Adijiang A, Enomoto A, Nishijima F, Dateki M, Niwa T. Senescence and dysfunction of proximal tubular cells are associated with activated p53 expression by indoxyl sulfate. Am J Physiol Cell Physiol 299: C1110-C1117, 2010.
39. Shimizu H, Hirose Y, Nishijima F, Tsubakihara Y, Miyazaki H. ROS and PDGF-β receptors are critically involved in indoxyl sulfate actions that promote vascular smooth muscle cell proliferation and migration. Am J Physiol Cell Physiol 297: C389-C396, 2009.
40. Taki K, Niwa T. Indoxyl sulfate-lowering capacity of oral sorbents affects the prognosis of kidney function and oxidative stress in chronic kidney disease. J Ren Nutr 17: 48-52, 2007.
41. Taki K, Tsuruta Y, Niwa T. Indoxyl sulfate and atherosclerotic risk factors in hemodialysis patients. Am J Nephrol 27: 30-35, 2007.
42. 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 31: 435-441, 2010.
43. Wang J, Jacob NK, Ladner KJ, Beg A, Perko JD, Tanner SM, Liyanarachchi S, Fishel R, Guttridge DC. RelA/p65 functions to maintain cellular senescence by regulating genomic stability and DNA repair. EMBO Rep 10: 1272-1278, 2009.
44. Wang S, El-Deiry WS. p73 or p53 directly regulates human p53 transcription to maintain cell cycle checkpoints. Cancer Res 66: 6982-6289, 2006.
45. Wiggins JE, Patel SR, Shedden KA, Goyal M, Wharram BL, Martini S, Kretzler M, Wiggins RC. NFkappaB promotes inflammation, coagulation, and fibrosis in the aging glomerulus. J Am Soc Nephro 21: 587-597, 2010.
46. Yamamoto H, Tsuruoka S, Ioka T, Ando H, Ito C, Akimoto T, Fujimura A, Asano Y, Kusano E. Indoxyl sulfate stimulates proliferation of rat vascular smooth muscle cells. Kidney Int 69: 1780-1785, 2006.
47. Yu M, Kim YJ, Kang DH. Indoxyl sulfate-induced endothelial dysfunction in patients with chronic kidney disease via an induction of oxidative stress. Clin J Am Soc Nephrol 6: 30-39, 2011.