Negative regulation of NADPH oxidase 4 by Hydrogen peroxide-inducible clone 5 (Hic-5) protein

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18270-18278

  Desai, Leena P ^a   Zhou, Yong ^a   Estrada, Aida V ^a   Ding, Qiang ^a   Cheng, Guangjie ^a   Collawn, James F ^b   Thannickal, Victor J ^a  

^a UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CLONING; FIBROBLASTS; HYDROGEN PEROXIDE; OXYGEN; PEROXIDES;

ADAPTOR PROTEINS; FOCAL ADHESIONS; HEAT SHOCK PROTEIN; HUMAN DIPLOID FIBROBLASTS; NEGATIVE FEEDBACK MECHANISM; POSTTRANSLATIONAL REGULATION; PROTEIN EXPRESSIONS; UBIQUITIN LIGASES;

PROTEINS;

ADAPTOR PROTEIN; CBL PROTEIN; FOCAL ADHESION KINASE; HEAT SHOCK PROTEIN 27; HYDROGEN PEROXIDE INDUCIBLE CLONE 5; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; TRANSFORMING GROWTH FACTOR BETA1; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME INDUCTION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION AND TRANSLATION; HUMAN; HUMAN CELL; LUNG FIBROBLAST; MYOFIBROBLAST; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SENESCENCE; UBIQUITIN PROTEASOME SYSTEM; UBIQUITINATION;

ADAPTOR PROTEIN; FIBROSIS; HIC-5, CBL-C, HSP27, NOX4, P16, PRB, UPS; NADPH OXIDASE; SENESCENCE; UBIQUITINATION;

CELL DIFFERENTIATION; DOWN-REGULATION; FIBROBLASTS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIM DOMAIN PROTEINS; MYOFIBROBLASTS; NADPH OXIDASE; PROTEOLYSIS; TRANSFORMING GROWTH FACTOR BETA1; UBIQUITINATION;

EID: 84903530834     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.562249     Document Type: Article

References (44)

1. Bedard, K., and Krause, K. H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313
2. Serrander, L., Cartier, L., Bedard, K., Banfi, B., Lardy, B., Plastre, O., Sienkiewicz, A., Fórró, L., Schlegel, W., and Krause, K. H. (2007) NOX4activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem. J. 406, 105-114
3. 2-generating NADH oxidase in human lung fibroblasts by transforming growth factor β 1. J. Biol. Chem. 270, 30334-30338
4. von Löhneysen, K., Noack, D., Wood, M. R., Friedman, J. S., and Knaus, U. G. (2010) Structural insights into Nox4 and Nox2: motifs involved in function and cellular localization. Mol. Cell. Biol. 30, 961-975
5. Peshavariya, H., Jiang, F., Taylor, C. J., Selemidis, S., Chang, C. W., and Dusting, G. J. (2009) Translation-linked mRNA destabilization accompanying serum-induced Nox4 expression in human endothelial cells. Antioxid. Redox Signal. 11, 2399-2408
6. Shibanuma, M., Mashimo, J., Kuroki, T., and Nose, K. (1994) Characterization of the TGF β 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J. Biol. Chem. 269, 26767-26774
7. Shibanuma, M., Mochizuki, E., Maniwa, R., Mashimo, J., Nishiya, N., Imai, S., Takano, T., Oshimura, M., and Nose, K. (1997) Induction of senescencelike phenotypes by forced expression of hic-5, which encodes a novel LIM motif protein, in immortalized human fibroblasts. Mol. Cell. Biol. 17, 1224-1235
8. Zhang, J., Zhang, L. X., Meltzer, P. S., Barrett, J. C., and Trent, J. M. (2000) Molecular cloning of human Hic-5, a potential regulator involved in signal transduction and cellular senescence. Mol. Carcinog. 27, 177-183
9. Jia, Y., Ransom, R. F., Shibanuma, M., Liu, C., Welsh, M. J., and Smoyer, W. E. (2001) Identification and characterization of hic-5/ARA55 as an hsp27 binding protein. J. Biol. Chem. 276, 39911-39918
10. Parcellier, A., Schmitt, E., Gurbuxani, S., Seigneurin-Berny, D., Pance, A., Chantôme, A., Plenchette, S., Khochbin, S., Solary, E., and Garrido, C. (2003) HSP27 is a ubiquitin-binding protein involved in I-κBα proteasomal degradation. Mol. Cell. Biol. 23, 5790-5802
11. Ryan, P. E., Kales, S. C., Yadavalli, R., Nau, M. M., Zhang, H., and Lipkowitz, S. (2012) Cbl-c ubiquitin ligase activity is increased via the interaction of its RING finger domain with a LIM domain of the paxillin homolog, Hic 5. PLoS ONE 7, e49428
12. Sun, Y., Zhou, M., Fu, D., Xu, B., Fang, T., Ma, Y., Chen, J., and Zhang, J. (2011) Ubiquitination of heat shock protein 27 is mediated by its interaction with Smad ubiquitination regulatory factor 2 in A549 cells. Exp. Lung. Res. 37, 568-573
13. Kato, K., Tokuda, H., Adachi, S., Matsushima-Nishiwaki, R., Yamauchi, J., Natsume, H., Minamitani, C., Mizutani, J., Otsuka, T., and Kozawa, O. (2011) Role of heat shock protein 27 in transforming growth factor-β-stimulated vascular endothelial growth factor release in osteoblasts. Int. J. Mol. Med. 27, 423-428
14. Wettstein, G., Bellaye, P. S., Kolb, M., Hammann, A., Crestani, B., Soler, P., Marchal-Somme, J., Hazoume, A., Gauldie, J., Gunther, A., Micheau, O., Gleave, M., Camus, P., Garrido, C., and Bonniaud, P. (2013) Inhibition of HSP27 blocks fibrosis development and EMT features by promoting Snail degradation. FASEB J. 27, 1549-1560
15. Chen, J. H., Stoeber, K., Kingsbury, S., Ozanne, S. E., Williams, G. H., and Hales, C. N. (2004) Loss of proliferative capacity and induction of senescence in oxidatively stressed human fibroblasts. J. Biol. Chem. 279, 49439-49446
16. Komatsuda, A., Wakui, H., Oyama, Y., Imai, H., Miura, A. B., Itoh, H., and Tashima, Y. (1999) Overexpression of the human 72 kDa heat shock protein in renal tubular cells confers resistance against oxidative injury and cisplatin toxicity. Nephrol. Dial. Transplant. 14, 1385-1390
17. Vidyasagar, A., Reese, S. R., Hafez, O., Huang, L. J., Swain, W. F., Jacobson, L. M., Torrealba, J. R., Chammas, P. E., Wilson, N. A., and Djamali, A. (2013) Tubular expression of heat-shock protein 27 inhibits fibrogenesis in obstructive nephropathy. Kidney Int. 83, 84-92
18. Bahta, A. W., Farjo, N., Farjo, B., and Philpott, M. P. (2008) Premature senescence of balding dermal papilla cells in vitro is associated with p16 (INK4a) expression. J. Invest. Dermatol. 128, 1088-1094
19. Thannickal, V. J. (2012) Mechanisms of pulmonary fibrosis: role of activated myofibroblasts and NADPH oxidase. Fibrogenesis Tissue Repair 5, S23
20. Thannickal, V. J. (2010) Aging, antagonistic pleiotropy and fibrotic disease. Int. J. Biochem. Cell Biol. 42, 1398-1400
21. Thannickal, V. J., Lee, D. Y., White, E. S., Cui, Z., Larios, J. M., Chacon, R., Horowitz, J. C., Day, R. M., and Thomas, P. E. (2003) Myofibroblast differentiation by transforming growth factor-β1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J. Biol. Chem. 278, 12384-12389
22. Hecker, L., Vittal, R., Jones, T., Jagirdar, R., Luckhardt, T. R., Horowitz, J. C., Pennathur, S., Martinez, F. J., and Thannickal, V. J. (2009) NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat. Med. 15, 1077-1081
23. Bai, G., Hock, T. D., Logsdon, N., Zhou, Y., and Thannickal, V. J. (2014) A far-upstream AP-1/Smad binding box regulates human NOX4 promoter activation by transforming growth factor-β. Gene 540, 62-67
24. Walczak, H., Iwai, K., and Dikic, I. (2012) Generation and physiological roles of linear ubiquitin chains. BMC Biol. 10, 23
25. Martin-Garrido, A., Brown, D. I., Lyle, A. N., Dikalova, A., Seidel-Rogol, B., Lassègue, B., San Martín, A., and Griendling, K. K. (2011) NADPHoxidase 4 mediates TGF-β-induced smooth muscle α-actin via p38MAPK and serum response factor. Free Radic. Biol. Med. 50, 354-362
26. 2. Am. J. Physiol. Cell Physiol. 296, C711-723
27. Lambeth, J. D. (2004) NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189
28. Senturk, S., Mumcuoglu, M., Gursoy-Yuzugullu, O., Cingoz, B., Akcali, K. C., and Ozturk, M. (2010) Transforming growth factor-β induces senescence in hepatocellular carcinoma cells and inhibits tumor growth. Hepatology 52, 966-974
29. Weyemi, U., Lagente-Chevallier, O., Boufraqech, M., Prenois, F., Courtin, F., Caillou, B., Talbot, M., Dardalhon, M., Al Ghuzlan, A., Bidart, J. M., Schlumberger, M., and Dupuy, C. (2012) ROS-generating NADPH oxidase NOX4 is a critical mediator in oncogenic H-Ras-induced DNA damage and subsequent senescence. Oncogene 31, 1117-1129
30. Kodama, R., Kato, M., Furuta, S., Ueno, S., Zhang, Y., Matsuno, K., Yabe-Nishimura, C., Tanaka, E., and Kamata, T. (2013) ROS-generating oxidases Nox1 and Nox4 contribute to oncogenic Ras-induced premature senescence. Genes Cells 18, 32-41
31. Hecker, L., Logsdon, N. J., Kurundkar, D., Kurundkar, A., Bernard, K., Hock, T., Meldrum, E., Sanders, Y. Y., and Thannickal, V. J. (2014) Reversal of persistent fibrosis in aging by targeting Nox4-Nrf2 redox imbalance. Sci. Transl. Med. 6, 231-247
32. Wang, X., Hu, G., Betts, C., Harmon, E. Y., Keller, R. S., Van De Water, L., and Zhou, J. (2011) Transforming growth factor-β1-induced transcript 1 protein, a novel marker for smooth muscle contractile phenotype, is regulated by serum response factor/myocardin protein. J. Biol. Chem. 286, 41589-41599
33. Srinivasan, R., Forman, S., Quinlan, R. A., Ohanian, J., and Ohanian, V. (2008) Regulation of contractility by Hsp27 and Hic-5 in rat mesenteric small arteries. Am. J. Physiol. Heart Circ. Physiol. 294, H961-969
34. Dabiri, G., Tumbarello, D. A., Turner, C. E., and Van de Water, L. (2008) TGF-β1 slows the growth of pathogenic myofibroblasts through a mechanism requiring the focal adhesion protein, Hic-5. J. Invest. Dermatol. 128, 280-291
35. Dabiri, G., Tumbarello, D. A., Turner, C. E., and Van de Water, L. (2008) Hic-5 promotes the hypertrophic scar myofibroblast phenotype by regulating the TGF-β1 autocrine loop. J. Invest. Dermatol. 128, 2518-2525
36. Thannickal, V. J. (2013) Mechanistic links between aging and lung fibrosis. Biogerontology 14, 609-615
37. Ojha, J., Masilamoni, G., Dunlap, D., Udoff, R. A., and Cashikar, A. G. (2011) Sequestration of toxic oligomers by HspB1 as a cytoprotective mechanism. Mol. Cell. Biol. 31, 3146-3157
38. Yerbury, J. J., Gower, D., Vanags, L., Roberts, K., Lee, J. A., and Ecroyd, H. (2013) The small heat shock proteins αB-crystallin and Hsp27 suppress SOD1 aggregation in vitro. Cell Stress Chaperones 18, 251-257
39. Du, Y., Gu, H. J., Gong, Q. M., Yang, F., and Ling, J. Q. (2009) HSP25 affects the proliferation and differentiation of rat dental follicle cells. Int. J. Oral Sci. 1, 72-80
40. Takahashi-Horiuchi, Y., Sugiyama, K., Sakashita, H., and Amano, O. (2008) Expression of heat shock protein 27 with the transition from proliferation to differentiation of acinar precursor cell in regenerating submandibular gland of rats. Tohoku J. Exp. Med. 214, 221-230
41. Liu, T., Warburton, R. R., Guevara, O. E., Hill, N. S., Fanburg, B. L., Gaestel, M., and Kayyali, U. S. (2007) Lack of MK2 inhibits myofibroblast formation and exacerbates pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 37, 507-517
42. Acunzo, J., Katsogiannou, M., and Rocchi, P. (2012) Small heat shock proteins HSP27 (HspB1), αB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death. Int. J. Biochem. Cell Biol. 44, 1622-1631
43. Ito, H., Kamei, K., Iwamoto, I., Inaguma, Y., García-Mata, R., Sztul, E., and Kato, K. (2002) Inhibition of proteasomes induces accumulation, phosphorylation, and recruitment of HSP27 and αB-crystallin to aggresomes. J. Biochem. 131, 593-603
44. Hecker, L., Jagirdar, R., Jin, T., and Thannickal, V. J. (2011) Reversible differentiation of myofibroblasts by MyoD. Exp. Cell Res. 317, 1914-1921