High glucose forces a positive feedback loop connecting Akt kinase and Foxo1 transcription factor to activate mTORC1 kinase for mesangial cell hypertrophy and matrix protein expression

Journal of Biological Chemistry

Volumn 289, Issue 47, 2014, Pages 32703-32716

  Das, Falguni ^b   Ghosh Choudhury, Nandini ^a,b   Dey, Nirmalya ^b   Bera, Amit ^b   Mariappan, Meenalakshmi M ^b   Kasinath, Balakuntalam S ^a,b   Choudhury, Goutam Ghosh ^a,b  

^a SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

^b University of Texas Health Science Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CELLS; CHEMICAL ACTIVATION; CYTOLOGY; DISEASES; ENZYMES; FEEDBACK; GLUCOSE; PATHOLOGY; PHOSPHORYLATION; PROTEINS; TRANSCRIPTION; TRANSCRIPTION FACTORS;

AKT PHOSPHORYLATION; ANTIOXIDANT ENZYME; CONSTITUTIVELY ACTIVES; DIABETIC NEPHROPATHY; DOMINANT NEGATIVE; POSITIVE FEEDBACK LOOP; REACTIVE OXYGEN SPECIES; SUSTAINED ACTIVATION;

CELL SIGNALING;

CATALASE; CELL PROTEIN; FIBRONECTIN; GLUCOSE; MAMMALIAN TARGET OF RAPAMYCIN; MATRIX PROTEIN; MTORC1 KINASE; PAI 1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; AKT1S1 PROTEIN, RAT; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, RAT; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; NERVE PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; REACTIVE OXYGEN METABOLITE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE;

ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FEEDBACK SYSTEM; KIDNEY HYPERTROPHY; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL SIZE; DOSE RESPONSE; DRUG EFFECTS; ENZYME ACTIVATION; GENE EXPRESSION; GENETICS; IMMUNOBLOTTING; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY CORTEX; MESANGIUM CELL; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CATALASE; CELL SIZE; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FEEDBACK, PHYSIOLOGICAL; FIBRONECTINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; GLUCOSE; IMMUNOBLOTTING; KIDNEY CORTEX; MESANGIAL CELLS; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTO-ONCOGENE PROTEINS C-AKT; RATS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOR SERINE-THREONINE KINASES;

EID: 84911375024     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.605196     Document Type: Article

References (50)

1. Kanwar, Y. S., Sun, L., Xie, P., Liu, F. Y., and Chen, S. (2011) A glimpse of various pathogenetic mechanisms of diabetic nephropathy. Annu. Rev. Pathol. 6, 395-423
2. Kanwar, Y. S., Wada, J., Sun, L., Xie, P., Wallner, E. I., Chen, S., Chugh, S., and Danesh, F. R. (2008) Diabetic nephropathy: mechanisms of renal disease progression. Exp. Biol. Med. 233, 4-11
3. Satriano, J. (2007) Kidney growth, hypertrophy and the unifying mechanism of diabetic complications. Amino Acids 33, 331-339
4. Lehmann, R., and Schleicher, E. D. (2000) Molecular mechanism of diabetic nephropathy. Clin. Chim. Acta 297, 135-144
5. Dey, N., Ghosh-Choudhury, N., Das, F., Li, X., Venkatesan, B., Barnes, J. L., Kasinath, B. S., and Ghosh Choudhury, G. (2010) PRAS40 acts as a nodal regulator of high glucose-induced TORC1 activation in glomerular mesangial cell hypertrophy. J. Cell Physiol. 225, 27-41
6. Feliers, D., Duraisamy, S., Faulkner, J. L., Duch, J., Lee, A. V., Abboud, H. E., Choudhury, G. G., and Kasinath, B. S. (2001) Activation of renal signaling pathways in db/db mice with type 2 diabetes. Kidney Int. 60, 495-504
7. Mahimainathan, L., Das, F., Venkatesan, B., and Choudhury, G. G. (2006) Mesangial cell hypertrophy by high glucose is mediated by downregulation of the tumor suppressor PTEN. Diabetes 55, 2115-2125
8. Mariappan, M. M., Feliers, D., Mummidi, S., Choudhury, G. G., and Kasinath, B. S. (2007) High glucose, high insulin, and their combination rapidly induce laminin-β1 synthesis by regulation of mRNA translation in renal epithelial cells. Diabetes 56, 476-485
9. Mariappan, M. M., Shetty, M., Sataranatarajan, K., Choudhury, G. G., and Kasinath, B. S. (2008) Glycogen synthase kinase 3β is a novel regulator of high glucose- and high insulin-induced extracellular matrix protein synthesis in renal proximal tubular epithelial cells. J. Biol. Chem. 283, 30566-30575
10. Nagai, K., Matsubara, T., Mima, A., Sumi, E., Kanamori, H., Iehara, N., Fukatsu, A., Yanagita, M., Nakano, T., Ishimoto, Y., Kita, T., Doi, T., and Arai, H. (2005) Gas6 induces Akt/mTOR-mediated mesangial hypertrophy in diabetic nephropathy. Kidney Int. 68, 552-561
11. Dey, N., Das, F., Mariappan, M. M., Mandal, C. C., Ghosh-Choudhury, N., Kasinath, B. S., and Choudhury, G. G. (2011) MicroRNA-21 orchestrates high glucose-induced signals to TOR complex 1, resulting in renal cell pathology in diabetes. J. Biol. Chem. 286, 25586-25603
12. Lam, E. W., Brosens, J. J., Gomes, A. R., and Koo, C. Y. (2013) Forkhead box proteins: tuning forks for transcriptional harmony. Nat. Rev. Cancer 13, 482-495
13. Tikhanovich, I., Cox, J., and Weinman, S. A. (2013) Forkhead box class O transcription factors in liver function and disease. J. Gastroenterol. Hepatol. 28, 125-131
14. Gorin, Y., and Block, K. (2013) Nox as a target for diabetic complications. Clin. Sci. 125, 361-382
15. Kato, M., Yuan, H., Xu, Z. G., Lanting, L., Li, S. L., Wang, M., Hu, M. C., Reddy, M. A., and Natarajan, R. (2006) Role of the Akt/FoxO3a pathway in TGF-β1-mediated mesangial cell dysfunction: a novel mechanism related to diabetic kidney disease. J. Am. Soc. Nephrol. 17, 3325-3335
16. Kops, G. J., Dansen, T. B., Polderman, P. E., Saarloos, I., Wirtz, K. W., Coffer, P. J., Huang, T. T., Bos, J. L., Medema, R. H., and Burgering, B. M. (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419, 316-321
17. Das, F., Ghosh-Choudhury, N., Mahimainathan, L., Venkatesan, B., Feliers, D., Riley, D. J., Kasinath, B. S., and Choudhury, G. G. (2008) Raptorrictor axis in TGFβ-induced protein synthesis. Cell. Signal. 20, 409-423
18. Ghosh Choudhury, G., Lenin, M., Calhaun, C., Zhang, J. H., and Abboud, H. E. (2003) PDGF inactivates forkhead family transcription factor by activation of Akt in glomerular mesangial cells. Cell. Signal. 15, 161-170
19. Epstein, P. N., Overbeek, P. A., and Means, A. R. (1989) Calmodulin-induced early-onset diabetes in transgenic mice. Cell 58, 1067-1073
20. Zheng, S., Noonan, W. T., Metreveli, N. S., Coventry, S., Kralik, P. M., Carlson, E. C., and Epstein, P. N. (2004) Development of late-stage diabetic nephropathy in OVE26 diabetic mice. Diabetes 53, 3248-3257
21. Eid, A. A., Ford, B. M., Bhandary, B., de Cassia Cavaglieri, R., Block, K., Barnes, J. L., Gorin, Y., Choudhury, G. G., and Abboud, H. E. (2013) Mammalian target of rapamycin regulates Nox4-mediated podocyte depletion in diabetic renal injury. Diabetes 62, 2935-2947
22. Das, F., Ghosh-Choudhury, N., Bera, A., Dey, N., Abboud, H. E., Kasinath, B. S., and Choudhury, G. G. (2013) Transforming growth factor β integrates Smad 3 to mechanistic target of rapamycin complexes to arrest deptor abundance for glomerular mesangial cell hypertrophy. J. Biol. Chem. 288, 7756-7768
23. Das, F., Ghosh-Choudhury, N., Venkatesan, B., Li, X., Mahimainathan, L., and Choudhury, G. G. (2008) Akt kinase targets association of CBP with SMAD 3 to regulate TGFβ-induced expression of plasminogen activator inhibitor-1. J. Cell Physiol. 214, 513-527
24. Mandal, C. C., Ganapathy, S., Gorin, Y., Mahadev, K., Block, K., Abboud, H. E., Harris, S. E., Ghosh-Choudhury, G., and Ghosh-Choudhury, N. (2011) Reactive oxygen species derived from Nox4 mediate BMP2 gene transcription and osteoblast differentiation. Biochem. J. 433, 393-402
25. Biggs, W. H., 3rd, Meisenhelder, J., Hunter, T., Cavenee, W. K., and Arden, K. C. (1999) Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. U.S.A. 96, 7421-7426
26. Accili, D., and Arden, K. C. (2004) FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117, 421-426
27. Sataranatarajan, K., Mariappan, M. M., Lee, M. J., Feliers, D., Choudhury, G. G., Barnes, J. L., and Kasinath, B. S. (2007) Regulation of elongation phase of mRNA translation in diabetic nephropathy: amelioration by rapamycin. Am. J. Pathol. 171, 1733-1742
28. Laplante, M., and Sabatini, D. M. (2012) mTOR signaling in growth control and disease. Cell 149, 274-293
29. Ma, L. J., and Fogo, A. B. (2009) PAI-1 and kidney fibrosis. Front Biosci. 14, 2028-2041
30. Ghosh Choudhury, G., and Abboud, H. E. (2004) Tyrosine phosphorylation-dependent PI 3 kinase/Akt signal transduction regulates TGFβ-induced fibronectin expression in mesangial cells. Cell. Signal. 16, 31-41
31. Nemoto, S., and Finkel, T. (2002) Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 295, 2450-2452
32. Ghosh-Choudhury, N., Abboud, S. L., Nishimura, R., Celeste, A., Mahimainathan, L., and Choudhury, G. G. (2002) Requirement of BMP-2-induced phosphatidylinositol 3-kinase and Akt serine/threonine kinase in osteoblast differentiation and Smad-dependent BMP-2 gene transcription. J. Biol. Chem. 277, 33361-33368
33. Cully, M., You, H., Levine, A. J., and Mak, T. W. (2006) Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat. Rev. Cancer 6, 184-192
34. Zhang, K., Li, L., Qi, Y., Zhu, X., Gan, B., DePinho, R. A., Averitt, T., and Guo, S. (2012) Hepatic suppression of Foxo1 and Foxo3 causes hypoglycemia and hyperlipidemia in mice. Endocrinology 153, 631-646
35. Zhang, W., Patil, S., Chauhan, B., Guo, S., Powell, D. R., Le, J., Klotsas, A., Matika, R., Xiao, X., Franks, R., Heidenreich, K. A., Sajan, M. P., Farese, R. V., Stolz, D. B., Tso, P., Koo, S. H., Montminy, M., and Unterman, T. G. (2006) FoxO1 regulates multiple metabolic pathways in the liver: effects on gluconeogenic, glycolytic, and lipogenic gene expression. J. Biol. Chem. 281, 10105-10117
36. Kamei, Y., Miura, S., Suzuki, M., Kai, Y., Mizukami, J., Taniguchi, T., Mochida, K., Hata, T., Matsuda, J., Aburatani, H., Nishino, I., and Ezaki, O. (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J. Biol. Chem. 279, 41114-41123
37. Ni, Y. G., Wang, N., Cao, D. J., Sachan, N., Morris, D. J., Gerard, R. D., Kuro, O. M., Rothermel, B. A., and Hill, J. A. (2007) FoxO transcription factors activate Akt and attenuate insulin signaling in heart by inhibiting protein phosphatases. Proc. Natl. Acad. Sci. U.S.A. 104, 20517-20522
38. Chen, C. C., Jeon, S. M., Bhaskar, P. T., Nogueira, V., Sundararajan, D., Tonic, I., Park, Y., and Hay, N. (2010) FoxOs inhibit mTORC1 and activate Akt by inducing the expression of Sestrin3 and Rictor. Dev. Cell 18, 592-604
39. Stokoe, D., Stephens, L. R., Copeland, T., Gaffney, P. R., Reese, C. B., Painter, G. F., Holmes, A. B., McCormick, F., and Hawkins, P. T. (1997) Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277, 567-570
40. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101
41. Beaulieu, J. M., Sotnikova, T. D., Marion, S., Lefkowitz, R. J., Gainetdinov, R. R., and Caron, M. G. (2005) An Akt/β-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122, 261-273
42. Kasinath, B. S., Feliers, D., Sataranatarajan, K., Ghosh Choudhury, G., Lee, M. J., and Mariappan, M. M. (2009) Regulation of mRNA translation in renal physiology and disease. Am. J. Physiol. Renal Physiol. 297, F1153-1165
43. Sena, L. A., and Chandel, N. S. (2012) Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48, 158-167
44. Tonks, N. K. (2005) Redox redux: revisiting PTPs and the control of cell signaling. Cell 121, 667-670
45. Antico Arciuch, V. G., Galli, S., Franco, M. C., Lam, P. Y., Cadenas, E., Carreras, M. C., and Poderoso, J. J. (2009) Akt1 intramitochondrial cycling is a crucial step in the redox modulation of cell cycle progression. PLoS ONE 4, e7523
46. Góth, L., and Nagy, T. (2012) Acatalasemia and diabetes mellitus. Arch. Biochem. Biophys. 525, 195-200
47. Hur, J., Sullivan, K. A., Schuyler, A. D., Hong, Y., Pande, M., States, D. J., Jagadish, H. V., and Feldman, E. L. (2010) Literature-based discovery of diabetes- and ROS-related targets. BMC Med. Genomics 3, 49
48. Ewens, K. G., George, R. A., Sharma, K., Ziyadeh, F. N., and Spielman, R. S. (2005) Assessment of 115 candidate genes for diabetic nephropathy by transmission/disequilibrium test. Diabetes 54, 3305-3318
49. Hodgkinson, A. D., Bartlett, T., Oates, P. J., Millward, B. A., and Demaine, A. G. (2003) The response of antioxidant genes to hyperglycemia is abnormal in patients with type 1 diabetes and diabetic nephropathy. Diabetes 52, 846-851
50. Glorieux, C., Auquier, J., Dejeans, N., Sid, B., Demoulin, J. B., Bertrand, L., Verrax, J., and Calderon, P. B. (2014) Catalase expression in MCF-7 breast cancer cells is mainly controlled by PI3K/Akt/mTor signaling pathway. Biochem. Pharmacol. 89, 217-223