α-actinin 4 potentiates nuclear factor κ-light-chain-enhancer of activated B-cell (NF-κB) activity in podocytes independent of its cytoplasmic actin binding function

Journal of Biological Chemistry

Volumn 290, Issue 1, 2015, Pages 338-349

  Zhao, Xuan ^a   Hsu, Kuo Sheng ^a   Lim, Jun Hee ^a   Bruggeman, Leslie A ^a   Kao, Hung Ying ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CHEMICAL ACTIVATION; CYTOLOGY; TRANSCRIPTION;

ACTIN-BINDING ACTIVITY; ACTIN-BINDING PROTEINS; CHRONIC KIDNEY DISEASE; DIFFERENTIATED CELLS; GLOMERULOSCLEROSIS; NUCLEAR FUNCTION; NUCLEAR TRANSLOCATIONS; OVER-EXPRESSION;

PROTEINS;

ACTIN; ALPHA ACTININ 4; HISTONE DEACETYLASE 7; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 8; NEPHRIN; PROTEIN VARIANT; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; ACTININ; ACTN4 PROTEIN, HUMAN; PROTEIN BINDING; SMALL INTERFERING RNA;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FOCAL GLOMERULOSCLEROSIS; HUMAN; HUMAN CELL; PODOCYTE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; TRANSCRIPTION INITIATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; MALE; METABOLISM; MOUSE; SIGNAL TRANSDUCTION; TRANSFORMED CELL LINE;

ACTININ; ACTINS; ANIMALS; CELL LINE, TRANSFORMED; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; PODOCYTES; PROTEIN BINDING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84920693952     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.597260     Document Type: Article

References (43)

1. Mundel, P., and Shankland, S. J. (2002) Podocyte biology and response to injury. J. Am. Soc. Nephrol. 13, 3005-3015
2. Rood, I. M., Deegens, J. K., and Wetzels, J. F. (2012) Genetic causes of focal segmental glomerulosclerosis: implications for clinical practice. Nephrol. Dial. Transplant. 27, 882-890
3. Schell, C., and Huber, T. B. (2012) New players in the pathogenesis of focal segmental glomerulosclerosis. Nephrol. Dial. Transplant. 27, 3406-3412
4. Kaplan, J. M., Kim, S. H., North, K. N., Rennke, H., Correia, L. A., Tong, H. Q., Mathis, B. J., Rodríguez-Pérez, J. C., Allen, P. G., Beggs, A. H., and Pollak, M. R. (2000) Mutations in ACTN4, encoding α-actinin-4, cause familial focal segmental glomerulosclerosis. Nat. Genet. 24, 251-256
5. Choi, H. J., Lee, B. H., Cho, H. Y., Moon, K. C., Ha, I. S., Nagata, M., Choi, Y., and Cheong, H. I. (2008) Familial focal segmental glomerulosclerosis associated with an ACTN4 mutation and paternal germline mosaicism. Am. J. Kidney Dis. 51, 834-838
6. Honda, K., Yamada, T., Endo, R., Ino, Y., Gotoh, M., Tsuda, H., Yamada, Y., Chiba, H., and Hirohashi, S. (1998) Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion. J. Cell Biol. 140, 1383-1393
7. Chakraborty, S., Reineke, E. L., Lam, M., Li, X., Liu, Y., Gao, C., Khurana, S., and Kao, H. Y. (2006) Alpha-actinin 4 potentiates myocyte enhancer factor-2 transcription activity by antagonizing histone deacetylase 7. J. Biol. Chem. 281, 35070-35080
8. An, H. T., Kim, J., Yoo, S., and Ko, J. (2014) Small leucine zipper protein (sLZIP) negatively regulates skeletal muscle differentiation via interaction with α-actinin-4. J. Biol. Chem. 289, 4969-4979
9. Khurana, S., Chakraborty, S., Cheng, X., Su, Y. T., and Kao, H. Y. (2011) The actin-binding protein, actinin α 4 (ACTN4), is a nuclear receptor coactivator that promotes proliferation of MCF-7 breast cancer cells. J. Biol. Chem. 286, 1850-1859
10. Khurana, S., Chakraborty, S., Zhao, X., Liu, Y., Guan, D., Lam, M., Huang, W., Yang, S., and Kao, H. Y. (2012) Identification of a novel LXXLL motif in α-actinin 4-spliced isoform that is critical for its interaction with estrogen receptor α and co-activators. J. Biol. Chem. 287, 35418-35429
11. Khurana, S., Chakraborty, S., Lam, M., Liu, Y., Su, Y. T., Zhao, X., Saleem, M. A., Mathieson, P. W., Bruggeman, L. A., and Kao, H. Y. (2012) Familial focal segmental glomerulosclerosis (FSGS)-linked α-actinin 4 (ACTN4) protein mutants lose ability to activate transcription by nuclear hormone receptors. J. Biol. Chem. 287, 12027-12035
12. DiDonato, J. A., Mercurio, F., and Karin, M. (2012) NF-κB and the link between inflammation and cancer. Immunol. Rev. 246, 379-400
13. Tornatore, L., Thotakura, A. K., Bennett, J., Moretti, M., and Franzoso, G. (2012) The nuclear factor κB signaling pathway: integrating metabolism with inflammation. Trends Cell Biol. 22, 557-566
14. Martinka, S., and Bruggeman, L. A. (2006) Persistent NF-κB activation in renal epithelial cells in a mouse model of HIV-associated nephropathy. Am. J. Physiol. Renal Physiol. 290, F657-F665
15. Ross, M. J., Martinka, S., D'Agati, V. D., and Bruggeman, L. A. (2005) NF-κB regulates Fas-mediated apoptosis in HIV-associated nephropathy. J. Am. Soc. Nephrol. 16, 2403-2411
16. Brähler, S., Ising, C., Hagmann, H., Rasmus, M., Hoehne, M., Kurschat, C., Kisner, T., Goebel, H., Shankland, S., Addicks, K., Thaiss, F., Schermer, B., Pasparakis, M., Benzing, T., and Brinkkoetter, P. T. (2012) Intrinsic proinflammatory signaling in podocytes contributes to podocyte damage and prolonged proteinuria. Am. J. Physiol. Renal Physiol. 303, F1473-F1485
17. Bruggeman, L. A., Drawz, P. E., Kahoud, N., Lin, K., Barisoni, L., and Nelson, P. J. (2011) TNFR2 interposes the proliferative and NF-κB-mediated inflammatory response by podocytes to TNF-α. Lab. Invest. 91, 413-425
18. Hussain, S., Romio, L., Saleem, M., Mathieson, P., Serrano, M., Moscat, J., Diaz-Meco, M., Scambler, P., and Koziell, A. (2009) Nephrin deficiency activates NF-κB and promotes glomerular injury. J. Am. Soc. Nephrol. 20, 1733-1743
19. Yamashita, M., Millward, C. A., Inoshita, H., Saikia, P., Chattopadhyay, S., Sen, G. C., and Emancipator, S. N. (2013) Antiviral innate immunity disturbs podocyte cell function. J. Innate Immun. 5, 231-241
20. Liu, R., Zhong, Y., Li, X., Chen, H., Jim, B., Zhou, M. M., Chuang, P. Y., and He, J. C. (2014) Role of transcription factor acetylation in diabetic kidney disease. Diabetes 63, 2440-2453
21. Kao, H. Y., Lee, C. H., Komarov, A., Han, C. C., and Evans, R. M. (2002) Isolation and characterization of mammalian HDAC10, a novel histone deacetylase. J. Biol. Chem. 277, 187-193
22. Guan, D., Factor, D., Liu, Y., Wang, Z., and Kao, H. Y. (2013) The epigenetic regulator UHRF1 promotes ubiquitination-mediated degradation of the tumor-suppressor protein promyelocytic leukemia protein. Oncogene 32, 3819-3828
23. Schlondorff, D. (1990) Preparation and study of isolated glomeruli. Methods Enzymol. Methods Enzymol. 191, 130-140
24. Hsu, K. S., and Kao, H. Y. (2013) β-Transducin repeat-containing protein 1 (β-TrCP1)-mediated silencing mediator of retinoic acid and thyroid hormone receptor (SMRT) protein degradation promotes tumor necrosis factor α (TNFα)-induced inflammatory gene expression. J. Biol. Chem. 288, 25375-25386
25. Ristola, M., Arpiainen, S., Saleem, M. A., Holthöfer, H., and Lehtonen, S. (2012) Transcription of nephrin-Neph3 gene pair is synergistically activated by WT1 and NF-κB and silenced by DNA methylation. Nephrol. Dial. Transplant. 27, 1737-1745
26. Babakov, V. N., Petukhova, O. A., Turoverova, L. V., Kropacheva, I. V., Tentler, D. G., Bolshakova, A. V., Podolskaya, E. P., Magnusson, K. E., and Pinaev, G. P. (2008) RelA/NF-κB transcription factor associates with α-actinin-4. Exp. Cell Res. 314, 1030-1038
27. Chaturvedi, M. M., Sung, B., Yadav, V. R., Kannappan, R., and Aggarwal, B. B. (2011) NF-κB addiction and its role in cancer: 'one size does not fit all'. Oncogene 30, 1615-1630
28. Aksenova, V., Turoverova, L., Khotin, M., Magnusson, K. E., Tulchinsky, E., Melino, G., Pinaev, G. P., Barlev, N., and Tentler, D. (2013) Actin-binding protein α-actinin 4 (ACTN4) is a transcriptional co-activator of RelA/p65 sub-unit of NF-κB. Oncotarget 4, 362-372
29. Glass, C. K., and Saijo, K. (2010) Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells. Nat. Rev. Immunol. 10, 365-376
30. Xing, C. Y., Saleem, M. A., Coward, R. J., Ni, L., Witherden, I. R., and Mathieson, P. W. (2006) Direct effects of dexamethasone on human podocytes. Kidney Int. 70, 1038-1045
31. Ransom, R. F., Lam, N. G., Hallett, M. A., Atkinson, S. J., and Smoyer, W. E. (2005) Glucocorticoids protect and enhance recovery of cultured murine podocytes via actin filament stabilization. Kidney Int. 68, 2473-2483
32. Weins, A., Kenlan, P., Herbert, S., Le, T. C., Villegas, I., Kaplan, B. S., Appel, G. B., and Pollak, M. R. (2005) Mutational and biological analysis of α-actinin-4 in focal segmental glomerulosclerosis. J. Am. Soc. Nephrol. 16, 3694-3701
33. Yao, J., Le, T. C., Kos, C. H., Henderson, J. M., Allen, P. G., Denker, B. M., and Pollak, M. R. (2004) α-Actinin-4-mediated FSGS: an inherited kidney disease caused by an aggregated and rapidly degraded cytoskeletal protein. PLoS Biol. 2, e167
34. Kimura, M., Toyoda, M., Kato, M., Kobayashi, K., Abe, M., Kobayashi, T., Miyauchi, M., Yamamoto, N., Umezono, T., and Suzuki, D. (2008) Expression of α-actinin-4 in human diabetic nephropathy. Intern. Med. 47, 1099-1106
35. Dai, S., Wang, Z., Pan, X., Chen, X., Wang, W., Ren, H., Feng, Q., He, J. C., Han, B., and Chen, N. (2009) ACTN4 gene mutations and single nucleotide polymorphisms in idiopathic focal segmental glomerulosclerosis. Nephron Clin. Pract. 111, c87-94
36. Dai, S., Wang, Z., Pan, X., Wang, W., Chen, X., Ren, H., Hao, C., Han, B., and Chen, N. (2010) Functional analysis of promoter mutations in the ACTN4 and SYNPO genes in focal segmental glomerulosclerosis. Nephrol. Dial. Transplant. 25, 824-835
37. Liu, Z., Blattner, S. M., Tu, Y., Tisherman, R., Wang, J. H., Rastaldi, M. P., Kretzler, M., and Wu, C. (2011) α-Actinin-4 and CLP36 protein deficiencies contribute to podocyte defects in multiple human glomerulopathies. J. Biol. Chem. 286, 30795-30805
38. Kimura, J., Ichii, O., Otsuka, S., Sasaki, H., Hashimoto, Y., and Kon, Y. (2013) Close relations between podocyte injuries and membranous proliferative glomerulonephritis in autoimmune murine models. Am. J. Nephrol. 38, 27-38
39. Yasuno, K., Araki, S., Sakashita, H., Kobayashi, R., Baba, T., Kawakami, H., Kamiie, J., Ogihara, K., and Shirota, K. (2013) Development of podocyte injuries in Osborne-Mendel rats is accompanied by reduced expression of podocyte proteins. J Comp. Pathol. 149, 280-290
40. Kos, C. H., Le, T. C., Sinha, S., Henderson, J. M., Kim, S. H., Sugimoto, H., Kalluri, R., Gerszten, R. E., and Pollak, M. R. (2003) Mice deficient in α-actinin-4 have severe glomerular disease. J. Clin. Invest. 111, 1683-1690
41. Mudge, S. J., Paizis, K., Auwardt, R. B., Thomas, R. J., and Power, D. A. (2001) Activation of nuclear factor-κB by podocytes in the autologous phase of passive Heymann nephritis. Kidney Int. 59, 923-931
42. Schiffer, M., Bitzer, M., Roberts, I. S., Kopp, J. B., ten Dijke, P., Mundel, P., and Böttinger, E. P. (2001) Apoptosis in podocytes induced by TGF-β and Smad7. J. Clin. Invest. 108, 807-816
43. Ory, V., Fan, Q., Hamdaoui, N., Zhang, S. Y., Desvaux, D., Audard, V., Candelier, M., Noel, L. H., Lang, P., Guellaën, G., Pawlak, A., and Sahali, D. (2012) c-mip down-regulates NF-κB activity and promotes apoptosis in podocytes. Am. J. Pathol. 180, 2284-2292