Dual inhibiting senescence and epithelial-to-mesenchymal transition by erythropoietin preserve tubular epithelial cell regeneration and ameliorate renal fibrosis in unilateral ureteral obstruction

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Tasanarong, Adis ^a   Kongkham, Supranee ^a   Khositseth, Sookkasem ^a  

^a THAMMASAT UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

CALVASCULIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; OSTEOGENIC PROTEIN 1; RECOMBINANT ERYTHROPOIETIN; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; ERYTHROPOIETIN; RECOMBINANT PROTEIN; SMAD PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATROPHY; CELL AGING; CELL REGENERATION; CELL STRESS; CONTROLLED STUDY; DISEASE MODEL; DOWN REGULATION; DRUG EFFECT; DUAL INHIBITING SENESCENCE; EPITHELIAL MESENCHYMAL TRANSITION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KIDNEY FIBROSIS; KIDNEY PARENCHYMA; KIDNEY TUBULE CELL; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RENAL PROTECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNILATERAL URETERAL OBSTRUCTION; UNILATERAL URETERIC OBSTRUCTION; UPREGULATION; URETER OBSTRUCTION; WESTERN BLOTTING; ANIMAL; EPITHELIUM CELL; FIBROSIS; GENETICS; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; KIDNEY TUBULE; METABOLISM; REGENERATION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 7; CELL AGING; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DOWN-REGULATION; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; ERYTHROPOIETIN; FIBROSIS; HUMANS; KIDNEY TUBULES; MALE; MICE; MICE, INBRED ICR; RECOMBINANT PROTEINS; REGENERATION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION; URETERAL OBSTRUCTION;

EID: 84890098158     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/308130     Document Type: Article

References (52)

1. Truong L. D., Petrusevska G., Yang G., Gurpinar T., Shappel S., Lechago J., Rouse D., Suki W. N., Cell apoptosis and proliferation in experimental chronic obstructive uropathy. Kidney International 1996 50 1 200 207 2-s2.0-0029841086 (Pubitemid 26323714)
2. Melk A., Halloran P. F., Cell senescence and its implications for nephrology. Journal of the American Society of Nephrology 2001 12 2 385 393 2-s2.0-0035141497 (Pubitemid 32116383)
3. Liu Y., New insights into epithelial-mesenchymal transition in kidney fibrosis. Journal of the American Society of Nephrology 2010 21 2 212 222 2-s2.0-77949351029 10.1681/ASN.2008121226
4. Kirkwood T. B. L., Austad S. N., Why do we age? Nature 2000 408 6809 233 238 2-s2.0-0034626774 10.1038/35041682
5. Campisi J., d'Adda Di Fagagna F., Cellular senescence: when bad things happen to good cells. Nature Reviews Molecular Cell Biology 2007 8 9 729 740 2-s2.0-34548186667 10.1038/nrm2233 (Pubitemid 47312822)
6. Matsuura I., Denissova N. G., Wang G., He D., Long J., Liu F., Cyclin-dependent kinases regulate the antiproliferative function of Smads. Nature 2004 430 6996 226 231 2-s2.0-3142546336 10.1038/nature02650 (Pubitemid 38902433)
7. Serrano M., Hannon G. J., Beach D., A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993 366 6456 704 707 2-s2.0-0027769876 10.1038/366704a0 (Pubitemid 24036021)
8. Vijayachandra K., Lee J., Glick A. B., Smad3 regulates senescence and malignant conversion in a mouse multistage skin carcinogenesis model. Cancer Research 2003 63 13 3447 3452 2-s2.0-0037742433 (Pubitemid 36793018)
9. Vijayachandra K., Higgins W., Lee J., Glick A., Induction of p16ink4a and p19ARF by TGF β 1 contributes to growth arrest and senescence response in mouse keratinocytes. Molecular Carcinogenesis 2009 48 3 181 186 2-s2.0-62349129614 10.1002/mc.20472
10. Halloran P. F., Melk A., Barth C., Rethinking chronic allograft nephropathy: the concept of accelerated senescence. Journal of the American Society of Nephrology 1999 10 1 167 181 2-s2.0-0032946290 (Pubitemid 29034957)
11. Liu Y., Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. Journal of the American Society of Nephrology 2004 15 1 1 12 2-s2.0-0347993932 10.1097/01.ASN.0000106015.29070.E7 (Pubitemid 38020692)
12. Sato M., Muragaki Y., Saika S., Roberts A. B., Ooshima A., Targeted disruption of TGF- β 1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. Journal of Clinical Investigation 2003 112 10 1486 1494 2-s2.0-0346727324 10.1172/JCI200319270 (Pubitemid 38056275)
13. Zhang D., Sun L., Xian W., Liu F., Ling G., Xiao L., Liu Y., Peng Y., Haruna Y., Kanwar Y. S., Low-dose paclitaxel ameliorates renal fibrosis in rat UUO model by inhibition of TGF- β /Smad activity. Laboratory Investigation 2010 90 3 436 447 2-s2.0-77649134470 10.1038/labinvest.2009.149
14. Inazaki K., Kanamaru Y., Kojima Y., Sueyoshi N., Okumura K., Kaneko K., Yamashiro Y., Ogawa H., Nakao A., Smad3 deficiency attenuates renal fibrosis, inflammation, and apoptosis after unilateral ureteral obstruction. Kidney International 2004 66 2 597 604 2-s2.0-3242797424 10.1111/j.1523-1755.2004. 00779.x (Pubitemid 38982001)
15. Zeisberg M., Hanai J., Sugimoto H., Mammoto T., Charytan D., Strutz F., Kalluri R., BMP-7 counteracts TGF- β 1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nature Medicine 2003 9 7 964 968 2-s2.0-0038717407 10.1038/nm888 (Pubitemid 36889942)
16. Tyler J. R., Robertson H., Booth T. A., Burt A. D., Kirby J. A., Chronic allograft nephropathy: intraepithelial signals generated by transforming growth factor- β and bone morphogenetic protein-7. The American Journal of Transplantation 2006 6 6 1367 1376 2-s2.0-33745819270 10.1111/j.1600-6143.2006. 01339.x (Pubitemid 44030319)
17. Strutz F., Okada H., Lo C. W., Danoff T., Carone R. L., Tomaszewski J. E., Neilson E. G., Identification and characterization of a fibroblast marker: FSP1. Journal of Cell Biology 1995 130 2 393 405 2-s2.0-0029091682 10.1083/jcb.130.2.393
18. Iwano M., Plieth D., Danoff T. M., Xue C., Okada H., Neilson E. G., Evidence that fibroblasts derive from epithelium during tissue fibrosis. Journal of Clinical Investigation 2002 110 3 341 350 2-s2.0-0036322007 10.1172/JCI200215518 (Pubitemid 34847966)
19. Sharples E. J., Patel N., Brown P., Stewart K., Mota-Philipe H., Sheaff M., Kieswich J., Allen D., Harwood S., Raftery M., Thiemermann C., Yaqoob M. M., Erythropoietin protects the kidney against the injury and dysfunction caused by ischemia-reperfusion. Journal of the American Society of Nephrology 2004 15 8 2115 2124 2-s2.0-3543097510 10.1097/01.ASN.0000135059.67385.5D (Pubitemid 39031350)
20. Lee S. H., Li C., Lim S. W., Ahn K. O., Choi B. S., Kim Y. S., Moon I. S., Kim J., Bang B. K., Yang C. W., Attenuation of interstitial inflammation and fibrosis by recombinant human erythropoietin in chronic cyclosporine nephropathy. The American Journal of Nephrology 2005 25 1 64 76 2-s2.0-20244390303 10.1159/000084275 (Pubitemid 40529278)
21. Park S. H., Choi M. J., Song I. K., Choi S. Y., Nam J. O., Kim C. D., Lee B. H., Park R. W., Park K. M., Kim Y. J., Kim I. S., Kwon T. H., Kim Y. L., Erythropoietin decreases renal fibrosis in mice with ureteral obstruction: role of inhibiting TGF- β -induced epithelial-to-mesenchymal transition. Journal of the American Society of Nephrology 2007 18 5 1497 1507 2-s2.0-34248191263 10.1681/ASN.2005080866 (Pubitemid 46717516)
22. Kumral A., Gonenc S., Acikgoz O., Sonmez A., Genc K., Yilmaz O., Gokmen N., Duman N., Ozkan H., Erythropoietin increases glutathione peroxidase enzyme activity and decreases lipid peroxidation levels in hypoxic-ischemic brain injury in neonatal rats. Biology of the Neonate 2005 87 1 15 18 2-s2.0-11844266604 10.1159/000080490 (Pubitemid 40091371)
23. Ribatti D., Vacca A., Roccaro A. M., Crivellato E., Presta M., Erythropoietin as an angiogenic factor. European Journal of Clinical Investigation 2003 33 10 891 896 2-s2.0-0141816771 10.1046/j.1365-2362.2003. 01245.x (Pubitemid 37215045)
24. Aydin Z., Duijs J., Bajema I. M., van Zonneveld A. J., Rabelink T. J., Erythropoietin, progenitors, and repair. Kidney International, Supplement 2007 72 107 S16 S20 2-s2.0-35348996575 10.1038/sj.ki.5002483 (Pubitemid 47609058)
25. Kuriyama S., Tomonari H., Yoshida H., Hashimoto T., Kawaguchi Y., Sakai O., Reversal of anemia by erythropoietin therapy retards the progression of chronic renal failure, especially in nondiabetic patients. Nephron 1997 77 2 176 185 2-s2.0-0030827804 (Pubitemid 27440408)
26. Gouva C., Nikolopoulos P., Ioannidis J. P. A., Siamopoulos K. C., Treating anemia early in renal failure patients slows the decline of renal function: a randomized controlled trial. Kidney International 2004 66 2 753 760 2-s2.0-3242780941 10.1111/j.1523-1755.2004.00797.x (Pubitemid 38982019)
27. Melk A., Schmidt B. M. W., Takeuchi O., Sawitzki B., Rayner D. C., Halloran P. F., Expression of p16INK4a and other cell cycle regulator and senescence associated genes in aging human kidney. Kidney International 2004 65 2 510 520 2-s2.0-1642561702 10.1111/j.1523-1755.2004.00438.x (Pubitemid 38130645)
28. Melk A., Schmidt B. M. W., Vongwiwatana A., Rayner D. C., Halloran P. F., Increased expression of senescence-associated cell cycle inhibitor p16/INK4a in deteriorating renal transplants and diseased native kidney. The American Journal of Transplantation 2005 5 6 1375 1382 2-s2.0-20544432681 10.1111/j.1600-6143.2005.00846.x (Pubitemid 40839428)
29. Sis B., Tasanarong A., Khoshjou F., Dadras F., Solez K., Halloran P. F., Accelerated expression of senescence associated cell cycle inhibitor p16INK4A in kidneys with glomerular disease. Kidney International 2007 71 3 218 226 2-s2.0-33846552655 10.1038/sj.ki.5002039 (Pubitemid 46160922)
30. Senturk S., Mumcuoglu M., Gursoy-Yuzugullu O., Cingoz B., Akcali K. C., Ozturk M., Transforming growth factor- β induces senescence in hepatocellular carcinoma cells and inhibits tumor growth. Hepatology 2010 52 3 966 974 2-s2.0-77956629716 10.1002/hep.23769
31. Kua H. Y., Liu H., Leong W. F., Li L., Jia D., Ma G., Hu Y., Wang X., Chau J. F., Chen Y. G., Mishina Y., Boast S., Yeh J., Xia L., Chen G. Q., He L., Goff S. P., Li B., c-Abl promotes osteoblast expansion by differentially regulating canonical and non-canonical BMP pathways and p16INK4a expression. Nature Cell Biology 2012 14 7 727 737 10.1038/ncb2528
32. Patel S. R., Dressler G. R., BMP7 signaling in renal development and disease. Trends in Molecular Medicine 2005 11 11 512 518 2-s2.0-27844595882 10.1016/j.molmed.2005.09.007 (Pubitemid 41653292)
33. Guarino M., Tosoni A., Nebuloni M., Direct contribution of epithelium to organ fibrosis: epithelial-mesenchymal transition. Human Pathology 2009 40 10 1365 1376 2-s2.0-69949124749 10.1016/j.humpath.2009.02.020
34. Lan H. Y., Chung A. C., TGF- β /Smad signaling in kidney disease. Seminars in Nephrology 2012 32 3 236 243 10.1016/j.semnephrol.2012.04.002
35. Sanchez-Nio M. D., Benito-Martin A., Gonalves S., Sanz A. B., Ucero A. C., Izquierdo M. C., Ramos A. M., Berzal S., Selgas R., Ruiz-Ortega M., Egido J., Ortiz A., TNF superfamily: a growing saga of kidney injury modulators. Mediators of Inflammation 2010 2010 11 2-s2.0-78349232814 10.1155/2010/182958 182958
36. Barreto D. V., Barreto F. C., Liabeuf S., Temmar M., Lemke H., Tribouilloy C., Choukroun G., Vanholder R., Massy Z. A., Plasma interleukin-6 is independently associated with mortality in both hemodialysis and pre-dialysis patients with chronic kidney disease. Kidney International 2010 77 6 550 556 2-s2.0-77949540909 10.1038/ki.2009.503
37. Liu J., Yang J. R., He Y. N., Cai G. Y., Zhang J. G., Lin L. R., Zhan J., Zhang J. H., Xiao H. S., Accelerated senescence of renal tubular epithelial cells is associated with disease progression of patients with immunoglobulin A, (IgA) nephropathy. Translational Research 2012 159 6 454 463 10.1016/j.trsl.2011.11.008
38. Braun H., Schmidt B. M., Raiss M., Baisantry A., Mircea-Constantin D., Wang S., Gross M. L., Serrano M., Schmitt R., Melk A., Cellular senescence limits regenerative capacity and allograft survival. Journal of the American Society of Nephrology 2012 23 9 1467 1473 10.1681/ASN.2011100967
39. Liu F., Matsuura I., Inhibition of Smad antiproliferative function by CDK phosphorylation. Cell Cycle 2005 4 1 63 66 2-s2.0-22844440952 (Pubitemid 41038929)
40. Kitada K., Nakano D., Hitomi H., Kobori H., Deguchi K., Mori H., Masaki T., Nishiyama A., Aldosterone induces p21-regulated apoptosis via increased synthesis and secretion of tumour necrosis factor- α in human proximal tubular cells. Clinical and Experimental Pharmacology and Physiology 2012 39 10 858 863 10.1111/j.1440-1681.2012.12001.x
41. Bihani T., Mason D. X., Jackson T. J., Chen S. C., Boeltner B., Lin A. W., Differential oncogenic ras signaling and senescence in tumor cells. Cell Cycle 2004 3 9 1201 1207 2-s2.0-13944250623 (Pubitemid 40268640)
42. Bahlmann F. H., Song R., Boehm S. M., Mengel M., von Wasielewski R., Lindschau C., Kirsch T., de Groot K., Laudeley R., Niemczyk E., Güler F., Menne J., Haller H., Fliser D., Low-dose therapy with the long-acting erythropoietin analogue darbepoetin α persistently activates endothelial Akt and attenuates progressive organ failure. Circulation 2004 110 8 1006 1012 2-s2.0-4344626952 10.1161/01.CIR.0000139335.04152.F3 (Pubitemid 39128626)
43. Cassis P., Gallon L., Benigni A., Mister M., Pezzotta A., Solini S., Gagliardini E., Cugini D., Abbate M., Aiello S., Rocchetta F., Scudeletti P., Perico N., Noris M., Remuzzi G., Erythropoietin, but not the correction of anemia alone, protects from chronic kidney allograft injury. Kidney International 2012 81 9 903 918 2-s2.0-84859754845 10.1038/ki.2011.473
44. Srisawat N., Manotham K., Eiam-Ong S., Katavetin P., Praditpornsilpa K., Eiam-Ong S., Erythropoietin and its non-erythropoietic derivative: do they ameliorate renal tubulointerstitial injury in ureteral obstruction? International Journal of Urology 2008 15 11 1011 1017 2-s2.0-54849412101 10.1111/j.1442-2042.2008.02149.x
45. Chang Y. K., Choi D. E., Na K. R., Lee S. J., Suh K. S., Kim S. Y., Shin Y. T., Lee K. W., Erythropoietin attenuates renal injury in an experimental model of rat unilateral ureteral obstruction via anti-inflammatory and anti-apoptotic effects. Journal of Urology 2009 181 3 1434 1443 2-s2.0-59349083513 10.1016/j.juro.2008.10.105
46. Lan H. Y., Diverse roles of TGF- β /Smads in renal fibrosis and inflammation. International Journal of Biological Sciences 2011 7 7 1056 1067
47. Krantz S. B., Erythropoietin. Blood 1991 77 3 419 434 2-s2.0-0026019106
48. Westenfelder C., Biddle D. L., Baranowski R. L., Human, rat, and mouse kidney cells express functional erythropoietin receptors. Kidney International 1999 55 3 808 820 2-s2.0-0033029430 10.1046/j.1523-1755.1999.055003808.x (Pubitemid 29100693)
49. Brines M., Grasso G., Fiordaliso F., Sfacteria A., Ghezzi P., Fratelli M., Latini R., Xie Q., Smart J., Su-Rick C., Pobre E., Diaz D., Gomez D., Hand C., Coleman T., Cerami A., Erythropoietin mediates tissue protection through an erythropoietin and common β -subunit heteroreceptor. Proceedings of the National Academy of Sciences of the United States of America 2004 101 41 14907 14912 2-s2.0-6944237300 10.1073/pnas.0406491101 (Pubitemid 39410773)
50. Brines M., Cerami A., Discovering erythropoietin's extra-hematopoietic functions: biology and clinical promise. Kidney International 2006 70 2 246 250 2-s2.0-33746137372 10.1038/sj.ki.5001546 (Pubitemid 44086573)
51. Su K. H., Shyue S. K., Kou Y. R., Ching L. C., Chiang A. N., Yu Y. B., Chen C. Y., Pan C. C., Lee T. S., β common receptor integrates the erythropoietin signaling in activation of endothelial nitric oxide synthase. Journal of Cellular Physiology 2011 226 12 3330 3339 2-s2.0-79956018414 10.1002/jcp.22678
52. Coldewey S. M., Khan A. I., Kapoor A., Collino M., Rogazzo M., Brines M., Cerami A., Hall P., Sheaff M., Kieswich J. E., Yaqoob M. M., Patel N. S., Thiemermann C., Erythropoietin attenuates acute kidney dysfunction in murine experimental sepsis by activation of the β -common receptor. Kidney International 2013 84 3 482 490 10.1038/ki.2013.118