Protein kinase B/Akt activity is involved in renal TGF-β1-driven epithelial-mesenchymal transition in vitro and in vivo

American Journal of Physiology - Renal Physiology

Volumn 295, Issue 1, 2008, Pages

  Kattla, Jayesh J ^a   Carew, Rosemarie M ^a   Heljić, Mediha ^a   Godson, Catherine ^a   Brazil, Derek P ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Diabetic nephropathy; Transforming growth factor 1

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; PROTEIN ZO1; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN; 2 MORPHOLINO 8 PHENYLCHROMONE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; CHROMONE DERIVATIVE; DIMETHYL SULFOXIDE; MORPHOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPITHELIUM; EXPERIMENTAL MODEL; KIDNEY FIBROSIS; MALE; MESENCHYME; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; CELL TRANSDIFFERENTIATION; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; EXPERIMENTAL DIABETES MELLITUS; KIDNEY; MESENCHYMAL STEM CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL TRANSDIFFERENTIATION; CHROMONES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; DIMETHYL SULFOXIDE; EPITHELIAL CELLS; KIDNEY; MESENCHYMAL STEM CELLS; MORPHOLINES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 49949114895     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00548.2007     Document Type: Article

References (50)

1. Bachelder RE, Yoon SO, Franci C, de Herreros AG, 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.
2. Bakin AV, Rinehart C, Tomlinson AK, Arteaga CL. p38 mitogen-activated protein kinase is required for TGFβ-mediated fibroblastic transdifferentiation and cell migration. J Cell Sci 115: 3193-3206, 2002.
3. Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 275: 36803-36810, 2000.
4. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2: 84-89, 2000.
5. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, Arteaga CL, Moses HL. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 12: 27-36, 2001.
6. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
7. Burns WC, Twigg SM, Forbes JM, Pete J, Tikellis C, Thallas-Bonke V, Thomas MC, Cooper ME, Kantharidis P. 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 17: 2484-2494, 2006.
8. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2: 76-83, 2000.
9. Cho HJ, Baek KE, Saika S, Jeong MJ, Yoo J. Snail is required for transforming growth factor-beta-induced epithelial-mesenchymal transition by activating PI3 kinase/Akt signal pathway. Biochem Biophys Res Commun 353: 337-343, 2007.
10. WAF1 expression in LLC-PK1 cells. Kidney Int 71: 867-874, 2007.
11. Conery AR, Cao Y, Thompson EA, Townsend CM Jr, Ko TC, Luo K. Akt interacts directly with Smad3 to regulate the sensitivity to TGF-beta induced apoptosis. Nat Cell Biol 6: 366-372, 2004.
12. Dai C, Yang J, Liu Y. Transforming growth factor-beta 1 potentiates renal tubular epithelial cell death by a mechanism independent of Smad signaling. J Biol Chem 278: 12537-12545, 2003.
13. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 13: 2905-2927, 1999.
14. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105, 2000.
15. Feliers D, Duraisamy S, Faulkner JL, Duch J, Lee AV, Abboud HE, Choudhury GG, Kasinath BS. Activation of renal signaling pathways in db/db mice with type 2 diabetes. Kidney Int 60: 495-504, 2001.
16. Goto Y, Suzuki K, Ono T, Sasaki M, Toyota T. Development of diabetes in the non-obese NIDDM rat (GK rat). Adv Exp Med Biol 246: 29-31, 1988.
17. Higaki M, Shimokado K. Phosphatidylinositol 3-kinase is required for growth factor-induced amino acid uptake by vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 19: 2127-2132, 1999.
18. Horowitz JC, Lee DY, Waghray M, Keshamouni VG, Thomas PE, Zhang H, Cui Z, Thannickal VJ. Activation of the pro-survival phosphatidylinositol 3-kinase/AKT pathway by transforming growth factor-beta1 in mesenchymal cells is mediated by p38 MAPK-dependent induction of an autocrine growth factor. J Biol Chem 279: 1359-1367, 2004.
19. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J, Beug H, Grunert S. Ras and TGFβ cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 156: 299-313, 2002.
20. Janssen U, Phillips AO, Floege J. Rodent models of nephropathy associated with type II diabetes. J Nephrol 12: 159-172, 1999.
21. Julien S, Puig I, Caretti E, Bonaventure J, Nelles L, van Roy F, Dargemont C, de Herreros AG, Bellacosa A, Larue L. Activation of NF-κB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 26: 7445-7456, 2007.
22. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784, 2003.
23. Kattla JJ, Roxburgh S, Godson C, Brazil. DP. TGF β-mediated activation of protein kinase B (PKB/Akt) is important for tubulointerstitial fibrosis in diabetic nephropathy (Abstract). J Am Soc Nephrol 16: 610A, 2005.
24. Krymskaya VP, Hoffman R, Eszterhas A, Ciocca V, Panettieri RA Jr. TGF-β1 modulates EGF-stimulated phosphatidylinositol 3-kinase activity in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 273: L1220-L1227, 1997.
25. Li Y, Yang J, Dai C, Wu C, Liu Y. Role for integrin-linked kinase in mediating tubular epithelial to mesenchymal transition and renal interstitial fibrogenesis. J Clin Invest 112: 503-516, 2003.
26. Liu Y. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 15: 1-12, 2004.
27. Lloberas N, Cruzado JM, Franquesa M, Herrero-Fresneda I, Torras J, Alperovich G, Rama I, Vidal A, Grinyo JM. Mammalian target of rapamycin pathway blockade slows progression of diabetic kidney disease in rats. J Am Soc Nephrol 17: 1395-1404, 2006.
28. Massague J. How cells read TGF-β signals. Nat Rev Mol Cell Biol 1: 169-178, 2000.
29. Myers MP, Pass I, Batty IH, Van der Kaay J, Stolarov JP, Hemmings BA, Wigler MH, Downes CP, Tonks NK. The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc Natl Acad Sci USA 95: 13513-13518, 1998.
30. Nagai K, Matsubara T, Mima A, Sumi E, Kanamori H, Iehara N, Fukatsu A, Yanagita M, Nakano T, Ishimoto Y, Kita T, Doi T, Arai H. Gas6 induces Akt/mTOR-mediated mesangial hypertrophy in diabetic nephropathy. Kidney Int 68: 552-561, 2005.
31. Nath KA. Tubulointerstitial changes as a major determinant in the progression of renal damage. Am J Kidney Dis 20: 1-17, 1992.
32. Oldfield MD, Bach LA, Forbes JM, Nikolic-Paterson D, McRobert A, Thallas V, Atkins RC, Osicka T, Jerums G, Cooper ME. Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest 108: 1853-1863, 2001.
33. Piek E, Moustakas A, Kurisaki A, Heldin CH, ten Dijke P. TGF-β type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J Cell Sci 112: 4557-4568, 1999.
34. Rastaldi MP, Ferrario F, Giardino L, Dell'Antonio G, Grillo C, Grillo P, Strutz F, Muller GA, Colasanti G, D'Amico G. Epithelial-mesenchymal transition of tubular epithelial cells in human renal biopsies. Kidney Int 62: 137-146, 2002.
35. Remy I, Montmarquette A, Michnick SW. PKB/Akt modulates TGF-β signalling through a direct interaction with Smad3. Nat Cell Biol 6: 358-365, 2004.
36. Ritz E, Orth SR. Nephropathy in patients with type 2 diabetes mellitus. N Engl J Med 341: 1127-1133, 1999.
37. Runyan CE, Schnaper HW, Poncelet AC. The phosphatidylinositol 3-kinase/Akt pathway enhances Smad3-stimulated mesangial cell collagen I expression in response to transforming growth factor-beta1. J Biol Chem 279: 2632-2639, 2004.
38. Sheppard D. Transforming growth factor β: a central modulator of pulmonary and airway inflammation and fibrosis. Proc Am Thorac Soc 3: 413-417, 2006.
39. Sime PJ, Xing Z, Graham FL, Csaky KG, Gauldie J. Adenovector-mediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J Clin Invest 100: 768-776, 1997.
40. Slattery C, Campbell E, McMorrow T, Ryan MP. Cyclosporine A-induced renal fibrosis: a role for epithelial-mesenchymal transition. Am J Pathol 167: 395-407, 2005.
41. Strutz F, Okada H, Lo CW, Danoff T, Carone RL, Tomaszewski JE, Neilson EG. Identification and characterization of a fibroblast marker: FSP1. J Cell Biol 130: 393-405, 1995.
42. Strutz F, Zeisberg M, Ziyadeh FN, Yang CQ, Kalluri R, Muller GA, Neilson EG. Role of basic fibroblast growth factor-2 in epithelial- mesenchymal transformation. Kidney Int 61: 1714-1728, 2002.
43. Sugimoto H, Grahovac G, Zeisberg M, Kalluri R. Renal fibrosis and glomerulosclerosis in a new mouse model of diabetic nephropathy and its regression by bone morphogenic protein-7 and advanced glycation end product inhibitors. Diabetes 56: 1825-1833, 2007.
44. Tanaka T, Saika S, Ohnishi Y, Ooshima A, McAvoy JW, Liu CY, Azhar M, Doetschman T, Kao WW. Fibroblast growth factor 2: roles of regulation of lens cell proliferation and epithelial-mesenchymal transition in response to injury. Mol Vis 10: 462-467, 2004.
45. Ten Dijke P, Hill CS. New insights into TGF-beta-Smad signalling. Trends Biochem Sci 29: 265-273, 2004.
46. Vallance BA, Gunawan MI, Hewlett B, Bercik P, Van Kampen C, Galeazzi F, Sime PJ, Gauldie J, Collins SM. TGF-β1 gene transfer to the mouse colon leads to intestinal fibrosis. Am J Physiol Gastrointest Liver Physiol 289: G116-G128, 2005.
47. Vongwiwatana A, Tasanarong A, Rayner DC, Melk A, Halloran PF. Epithelial to mesenchymal transition during late deterioration of human kidney transplants: the role of tubular cells in fibrogenesis. Am J Transplant 5: 1367-1374, 2005.
48. Yang J, Liu Y. Blockage of tubular epithelial to myofibroblast transition by hepatocyte growth factor prevents renal interstitial fibrosis. J Am Soc Nephrol 13: 96-107, 2002.
49. Zeisberg M, Bonner G, Maeshima Y, Colorado P, Muller GA, Strutz F, Kalluri R. Renal fibrosis: collagen composition and assembly regulates epithelial-mesenchymal transdifferentiation. Am J Pathol 159: 1313-1321, 2001.
50. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC. Dual regulation of Snail by GSK-3β-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6: 931-940, 2004.