Differential regulation of Snail by hypoxia and hyperglycemia in human proximal tubule cells

International Journal of Biochemistry and Cell Biology

Volumn 42, Issue 10, 2010, Pages 1689-1697

  Sumual, Siska ^a   Saad, Sonia ^a   Tang, Owen ^a   Yong, Rachel ^a   McGinn, Stella ^a   Chen, Xin Ming ^a   Pollock, Carol A ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

EMT; Hyperglycemia; Hypoxia; Proximal tubule; Snail

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; LYSYL OXIDASE LIKE 2; NOTCH RECEPTOR; OXIDOREDUCTASE; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL HYPOXIA; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE SILENCING; HUMAN; HUMAN CELL; HYPERGLYCEMIA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; UPREGULATION;

AMINO ACID OXIDOREDUCTASES; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE; DIABETIC NEPHROPATHIES; EPITHELIAL-MESENCHYMAL TRANSITION; HOMEODOMAIN PROTEINS; HUMANS; HYPERGLYCEMIA; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY TUBULES, PROXIMAL; RECEPTOR, NOTCH1; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UP-REGULATION;

GASTROPODA;

EID: 77956183242     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2010.06.023     Document Type: Article

References (54)

1. Ayo S.H., Radnik R., Garoni J.A., Troyer D.A., Kreisberg J.I. High glucose increases diacylglycerol mass and activates protein kinase C in mesangial cell cultures. Am J Physiol 1991, 261:F571-F577.
2. Bandyopadhyay G., Sajan M.P., Kanoh Y., Standaert M.L., Burke T.R., Quon M.J., et al. Glucose activates mitogen-activated protein kinase (extracellular signal-regulated kinase) through proline-rich tyrosine kinase-2 and the Glut1 glucose transporter. J Biol Chem 2000, 275:40817-40826.
3. Bar Y., Russ H.A., Knoller S., Ouziel-Yahalom L., Efrat S. HES-1 is involved in adaptation of adult human beta-cells to proliferation in vitro. Diabetes 2008, 57:2413-2420.
4. Beavon I.R. Regulation of E-cadherin: does hypoxia initiate the metastatic cascade?. Mol Pathol 1999, 52:179-188.
5. Bechtel W., Zeisberg M. Twist: a new link from hypoxia to fibrosis. Kidney Int 2009, 75:1255-1256.
6. Bosman D.R., Winkler A.S., Marsden J.T., Macdougall I.C., Watkins P.J. Anemia with erythropoietin deficiency occurs early in diabetic nephropathy. Diabetes Care 2001, 24:495-499.
7. Boutet A., De Frutos C.A., Maxwell P.H., Mayol M.J., Romero J., Nieto M.A. Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. Embo J 2006, 25:5603-5613.
8. Burns W.C., Twigg S.M., Forbes J.M., Pete J., Tikellis C., Thallas-Bonke V., et al. Connective tissue growth factor plays an important role in advanced glycation end product-induced tubular epithelial-to-mesenchymal transition: implications for diabetic renal disease. J Am Soc Nephrol 2006, 17:2484-2494.
9. Catrina S.B., Okamoto K., Pereira T., Brismar K., Poellinger L. Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 2004, 53:3226-3232.
10. Chow E.K., Castrillo A., Shahangian A., Pei L., O'Connell R.M., Modlin R.L., et al. A role for IRF3-dependent RXRalpha repression in hepatotoxicity associated with viral infections. J Exp Med 2006, 203:2589-2602.
11. Craven P.A., DeRubertis F.R. Protein kinase C is activated in glomeruli from streptozotocin diabetic rats. Possible mediation by glucose. J Clin Invest 1989, 83:1667-1675.
12. Davis R.L., Turner D.L. Vertebrate hairy and Enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryonic patterning. Oncogene 2001, 20:8342-8357.
13. Erler J.T., Bennewith K.L., Nicolau M., Dornhofer N., Kong C., Le Q.T., et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006, 440:1222-1226.
14. Feliers D., Kasinath B.S. Mechanism of VEGF expression by high glucose in proximal tubule epithelial cells. Mol Cell Endocrinol 2009.
15. Gealekman O., Brodsky S.V., Zhang F., Chander P.N., Friedli C., Nasjletti A., et al. Endothelial dysfunction as a modifier of angiogenic response in Zucker diabetic fat rat: amelioration with Ebselen. Kidney Int 2004, 66:2337-2347.
16. Haase V.H. Oxygen regulates epithelial-to-mesenchymal transition: insights into molecular mechanisms and relevance to disease. Kidney Int 2009.
17. Higgins D.F., Kimura K., Bernhardt W.M., Shrimanker N., Akai Y., Hohenstein B., et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 2007, 117:3810-3820.
18. Higgins D.F., Kimura K., Iwano M., Haase V.H. Hypoxia-inducible factor signaling in the development of tissue fibrosis. Cell Cycle 2008, 7:1128-1132.
19. Holian J., Qi W., Kelly D.J., Zhang Y., Mreich E., Pollock C.A., et al. Role of Kruppel-like factor 6 in transforming growth factor-beta1-induced epithelial-mesenchymal transition of proximal tubule cells. Am J Physiol Renal Physiol 2008, 295:F1388-F1396.
20. Hotz B., Arndt M., Dullat S., Bhargava S., Buhr H.J., Hotz H.G. Epithelial to mesenchymal transition: expression of the regulators snail, slug, and twist in pancreatic cancer. Clin Cancer Res 2007, 13:4769-4776.
21. Imai T., Horiuchi A., Wang C., Oka K., Ohira S., Nikaido T., et al. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am J Pathol 2003, 163:1437-1447.
22. Kadesch T. Notch signaling: the demise of elegant simplicity. Curr Opin Genet Dev 2004, 14:506-512.
23. Kageyama R., Ohtsuka T., Kobayashi T. Roles of Hes genes in neural development. Dev Growth Differ 2008, 50(Suppl 1):S97-S103.
24. Katavetin P., Miyata T., Inagi R., Tanaka T., Sassa R., Ingelfinger J.R., et al. High glucose blunts vascular endothelial growth factor response to hypoxia via the oxidative stress-regulated hypoxia-inducible factor/hypoxia-responsible element pathway. J Am Soc Nephrol 2006, 17:1405-1413.
25. Katoh M. Transcriptional mechanisms of WNT5A based on NF-kappaB, Hedgehog, TGFbeta, and Notch signaling cascades. Int J Mol Med 2009, 23:763-769.
26. Kimura K., Iwano M., Higgins D.F., Yamaguchi Y., Nakatani K., Harada K., et al. Stable expression of HIF-1alpha in tubular epithelial cells promotes interstitial fibrosis. Am J Physiol Renal Physiol 2008, 295:F1023-F1029.
27. Krishnamachary B., Zagzag D., Nagasawa H., Rainey K., Okuyama H., Baek J.H., et al. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res 2006, 66:2725-2731.
28. Liu Y. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 2004, 15:1-12.
29. Lorber D., Reddan D. Clinical characteristics of chronic kidney disease patients with and without diabetes: a subanalysis of the PAERI study. Clin Nephrol 2006, 66:11-16.
30. Lu Z., Ghosh S., Wang Z., Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 2003, 4:499-515.
31. Manalo D.J., Rowan A., Lavoie T., Natarajan L., Kelly B.D., Ye S.Q., et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 2005, 105:659-669.
32. Manotham K., Tanaka T., Matsumoto M., Ohse T., Inagi R., Miyata T., et al. Transdifferentiation of cultured tubular cells induced by hypoxia. Kidney Int 2004, 65:871-880.
33. Moreno-Bueno G., Cubillo E., Sarrio D., Peinado H., Rodriguez-Pinilla S.M., Villa S., et al. Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epithelial-mesenchymal transition. Cancer Res 2006, 66:9543-9556.
34. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 2006, 17:17-25.
35. Nyengaard J.R., Rasch R. The impact of experimental diabetes mellitus in rats on glomerular capillary number and sizes. Diabetologia 1993, 36:189-194.
36. Peinado H., Ballestar E., Esteller M., Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol 2004, 24:306-319.
37. Peinado H., Del Carmen Iglesias-de la Cruz M., Olmeda D., Csiszar K., Fong K.S., Vega S., et al. A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. Embo J 2005, 24:3446-3458.
38. Sahlgren C., Gustafsson M.V., Jin S., Poellinger L., Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci U S A 2008, 105:6392-6397.
39. Sato M., Muragaki Y., Saika S., Roberts A.B., Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 2003, 112:1486-1494.
40. Schofield C.J., Ratcliffe P.J. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004, 5:343-354.
41. Singh D.K., Winocour P., Farrington K. Mechanisms of disease: the hypoxic tubular hypothesis of diabetic nephropathy. Nat Clin Pract Nephrol 2008, 4:216-226.
42. Stockhausen M.T., Sjolund J., Axelson H. Regulation of the Notch target gene Hes-1 by TGFalpha induced Ras/MAPK signaling in human neuroblastoma cells. Exp Cell Res 2005, 310:218-228.
43. Sun S., Ning X., Zhang Y., Lu Y., Nie Y., Han S., et al. Hypoxia-inducible factor-1alpha induces Twist expression in tubular epithelial cells subjected to hypoxia, leading to epithelial-to-mesenchymal transition. Kidney Int 2009, 75:1278-1287.
44. Takata H., Ikeda Y., Suehiro T., Ishibashi A., Inoue M., Kumon Y., et al. High glucose induces transactivation of the alpha2-HS glycoprotein gene through the ERK1/2 signaling pathway. J Atheroscler Thromb 2009, 16:448-456.
45. Takebayashi K., Sasai Y., Sakai Y., Watanabe T., Nakanishi S., Kageyama R. Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J Biol Chem 1994, 269:5150-5156.
46. Thomas M.C., Cooper M.E., Tsalamandris C., MacIsaac R., Jerums G. Anemia with impaired erythropoietin response in diabetic patients. Arch Intern Med 2005, 165:466-469.
47. Timmerman L.A., Grego-Bessa J., Raya A., Bertran E., Perez-Pomares J.M., Diez J., et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 2004, 18:99-115.
48. Warnecke C., Zaborowska Z., Kurreck J., Erdmann V.A., Frei U., Wiesener M., et al. Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. Faseb J 2004, 18:1462-1464.
49. Wenger R.H., Stiehl D.P., Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005, re12.
50. Willert K., Nusse R. Beta-catenin: a key mediator of Wnt signaling. Curr Opin Genet Dev 1998, 8:95-102.
51. Xu J., Lamouille S., Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res 2009, 19:156-172.
52. Yang M.H., Wu K.J. TWIST activation by hypoxia inducible factor-1 (HIF-1): implications in metastasis and development. Cell Cycle 2008, 7:2090-2096.
53. Yoshino J., Monkawa T., Tsuji M., Inukai M., Itoh H., Hayashi M. Snail1 is involved in the renal epithelial-mesenchymal transition. Biochem Biophys Res Commun 2007, 362:63-68.
54. Zavadil J., Bottinger E.P. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005, 24:5764-5774.