The transcriptional cofactor Nab2 is induced by TGF-β and suppresses fibroblast activation: Physiological roles and impaired expression in scleroderma

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Bhattacharyya, Swati ^a   Wei, Jun ^a   Melichian, Denisa S ^a   Milbrandt, Jeffrey ^b   Takehara, Kazuhiko ^c   Varga, John ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 1A2; EARLY GROWTH RESPONSE FACTOR 1; EARLY GROWTH RESPONSE FACTOR 1 BINDING PROTEIN 2; HISTONE H4; MESSENGER RNA; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ALPHA 2(I) COLLAGEN; COLLAGEN; NAB2 PROTEIN, HUMAN; REPRESSOR PROTEIN;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; COLLAGEN SYNTHESIS; CONTROLLED STUDY; FIBROBLAST; HUMAN; KERATINOCYTE; MOUSE; MYOFIBROBLAST; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; SCLERODERMA; SIGNAL TRANSDUCTION; SKIN BIOPSY; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CELL STRAIN 3T3; GENE DELETION; GENE EXPRESSION REGULATION; METABOLISM; SYSTEMIC SCLEROSIS;

MUS;

ACETYLATION; ANIMALS; CELL LINE; COLLAGEN; FIBROBLASTS; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; MICE; MODELS, GENETIC; NIH 3T3 CELLS; REPRESSOR PROTEINS; SCLERODERMA, SYSTEMIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 70449575813     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007620     Document Type: Article

References (45)

1. Jimenez SA, Derk CT (2004) Following the molecular pathways toward an understanding of the pathogenesis of systemic sclerosis. Ann Intern Med 140: 37-50.
2. Abraham DJ, Varga J (2005) Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol 26: 587-595.
3. Varga J, Rosenbloom J, Jimenez SA (1987) Transforming growth factor beta (TGF beta) causes a persistent increase in steady-state amounts of type I and type III collagen and fibronectin mRNAs in normal human dermal fibroblasts. Biochem J 247: 597-604.
4. Mauviel A (2005) Transforming growth factor-beta: a key mediator of fibrosis. Methods Mol Med 117: 69-80.
5. Derynck R, Akhurst RJ (2007) Differentiation plasticity regulated by TGF-beta family proteins in development and disease. Nat Cell Biol 9: 1000-1004.
6. Varga J, Abraham D (2007) Systemic sclerosis: a prototypic multisystem fibrotic disorder. J Clin Invest 117: 557-567.
7. Khachigian LM, Collins T (1998) Early growth response factor 1: a pleiotropic mediator of inducible gene expression. J Mol Med 76: 613-616.
8. Thiel G, Cibelli G (2002) Regulation of life and death by the zinc finger transcription factor Egr-1. J Cell Physiol 193: 287-292.
9. Gashler A, Sukhatme VP (1995) Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors. Prog Nucleic Acid Res Mol Biol 50: 191-224.
10. Chen SJ, Ning H, Ishida W, Sodin-Semrl S, Takagawa S, et al. (2006) The early-immediate gene EGR-1 is induced by transforming growth factor-beta and mediates stimulation of collagen gene expression. J Biol Chem 281: 21183-21197.
11. Bhattacharyya S, Chen SJ, Wu M, Warner-Blankenship M, Ning H, et al. (2008) Smad-independent transforming growth factor-beta regulation of early growth response-1 and sustained expression in fibrosis: implications for scleroderma. Am J Pathol 173: 1085-1099.
12. Bhattacharyya S, Ishida W, Wu M, Wilkes M, Mori Y, et al. (2009) A non-Smad mechanism of fibroblast activation by transforming growth factor-beta via c-Abl and Egr-1: selective modulation by imatinib mesylate. Oncogene 28: 1285-1297.
13. Russo MW, Sevetson BR, Milbrandt J (1995) Identification of NAB1, a repressor of NGFI-A- and Krox20-mediated transcription. Proc Natl Acad Sci U S A 92: 6873-6877.
14. Svaren J, Sevetson BR, Apel ED, Zimonjic DB, Popescu NC, et al. (1996) NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol Cell Biol 16: 3545-3553.
15. Svaren J, Sevetson BR, Golda T, Stanton JJ, Swirnoff AH, et al. (1998) Novel mutants of NAB corepressors enhance activation by Egr transactivators. EMBO J 17: 6010-6019.
16. Swirnoff AH, Apel ED, Svaren J, Sevetson BR, Zimonjic DB, et al. (1998) Nab1, a corepressor of NGFI-A (Egr-1), contains an active transcriptional repression domain. Mol Cell Biol 18: 512-524.
17. Le N, Nagarajan R, Wang JY, Svaren J, LaPash C, et al. (2005) Nab proteins are essential for peripheral nervous system myelination. Nat Neurosci 8: 932-940.
18. Mori Y, Ishida W, Bhattacharyya S, Li Y, Platanias LC, et al. (2004) Selective inhibition of activin receptor-like kinase 5 signaling blocks profibrotic transforming growth factor beta responses in skin fibroblasts. Arthritis Rheum 50: 4008-4021.
19. Wu M, Melichian DS, Chang E, Warner-Blankenship M, Ghosh AK, et al. (2009) Rosiglitazone abrogates bleomycin-induced scleroderma and blocks profibrotic responses through peroxisome proliferator-activated receptor-gamma. Am J Pathol 174: 519-533.
20. Ihn H, LeRoy EC, Trojanowska M (1997) Oncostatin M stimulates transcription of the human alpha2(I) collagen gene via the Sp1/ Sp3-binding site. J Biol Chem 272: 24666-24672.
21. Okano K, Schnaper HW, Bomsztyk K, Hayashida T (2006) RACK1 binds to Smad3 to modulate transforming growth factor-beta1-stimulated alpha2(I) collagen transcription in renal tubular epithelial cells. J Biol Chem 281: 26196-26204.
22. Thiel G, Kaufmann K, Magin A, Lietz M, Bach K, et al. (2000) The human transcriptional repressor protein NAB1: expression and biological activity. Biochim Biophys Acta 1493: 289-301.
23. Chen SJ, Yuan W, Lo S, Trojanowska M, Varga J (2000) Interaction of smad3 with a proximal smad-binding element of the human alpha2(I) procollagen gene promoter required for transcriptional activation by TGF-beta. J Cell Physiol 183: 381-392.
24. Ehrengruber MU, Muhlebach SG, Sohrman S, Leutenegger CM, Lester HA, et al. (2000) Modulation of early growth response (EGR) transcription factor-dependent gene expression by using recombinant adenovirus. Gene 258: 63-69.
25. Sevetson BR, Svaren J, Milbrandt J (2000) A novel activation function for NAB proteins in EGR-dependent transcription of the luteinizing hormone beta gene. J Biol Chem 275: 9749-9757.
26. Wu M, Melichian DS, de la Garza M, Gruner K, Bhattacharyya S, et al. (2009) Essential roles for early growth response transcription factor Egr-1 in tissue fibrosis and wound healing. Am J Pathol 175: 1041-1055.
27. Srinivasan R, Mager GM, Ward RM, Mayer J, Svaren J (2006) NAB2 represses transcription by interacting with the CHD4 subunit of the nucleosome remodeling and deacetylase (NuRD) complex. J Biol Chem 281: 15129-15137.
28. Xue Y, Wong J, Moreno GT, Young MK, Cote J, et al. (1998) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2: 851-861.
29. Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL (1998) Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395: 917-921.
30. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, et al. (1999) Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 13: 1924-1935.
31. Bowen NJ, Fujita N, Kajita M, Wade PA (2004) Mi-2/NuRD: multiple complexes for many purposes. Biochim Biophys Acta 1677: 52-57.
32. Becker PB, Horz W (2002) ATP-dependent nucleosome remodeling. Annu Rev Biochem 71: 247-273.
33. Milbrandt J (1987) A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238: 797-799.
34. Houston P, Campbell CJ, Svaren J, Milbrandt J, Braddock M (2001) The transcriptional corepressor NAB2 blocks Egr-1-mediated growth factor activation and angiogenesis. Biochem Biophys Res Commun 283: 480-486.
35. Gashler AL, Swaminathan S, Sukhatme VP (1993) A novel repression module, an extensive activation domain, and a bipartite nuclear localization signal defined in the immediate-early transcription factor Egr-1. Mol Cell Biol 13: 4556-4571.
36. Silverman ES, Khachigian LM, Santiago FS, Williams AJ, Lindner V, et al. (1999) Vascular smooth muscle cells express the transcriptional corepressor NAB2 in response to injury. Am J Pathol 155: 1311-1317.
37. Zhu X, Lin Y, Bacanamwo M, Chang L, Chai R, et al. (2007) Interleukin-1 beta-induced Id2 gene expression is mediated by Egr-1 in vascular smooth muscle cells. Cardiovasc Res 76: 141-148.
38. Kamimura M, Bea F, Akizawa T, Katus HA, Kreuzer J, et al. (2004) Platelet-derived growth factor induces tissue factor expression in vascular smooth muscle cells via activation of Egr-1. Hypertension 44: 944-951.
39. Fu M, Zhu X, Zhang J, Liang J, Lin Y, et al. (2003) Egr-1 target genes in human endothelial cells identified by microarray analysis. Gene 315: 33-41.
40. Lucerna M, Mechtcheriakova D, Kadl A, Schabbauer G, Schafer R, et al. (2003) NAB2, a corepressor of EGR-1, inhibits vascular endothelial growth factor-mediated gene induction and angiogenic responses of endothelial cells. J Biol Chem 278: 11433-11440.
41. Fukuda T, Kanomata K, Nojima J, Urakawa I, Suzawa T, et al. (2007) FGF23 induces expression of two isoforms of NAB2, which are corepressors of Egr-1. Biochem Biophys Res Commun 353: 147-151.
42. Schweighofer B, Schultes J, Pomyje J, Hofer E (2007) Signals and genes induced by angiogenic growth factors in comparison to inflammatory cytokines in endothelial cells. Clin Hemorheol Microcirc 37: 57-62.
43. Desmazieres A, Decker L, Vallat JM, Charnay P, Gilardi-Hebenstreit P (2008) Disruption of Krox20-Nab interaction in the mouse leads to peripheral neuropathy with biphasic evolution. J Neurosci 28: 5891-5900.
44. Baloh RH, Strickland A, Ryu E, Le N, Fahrner T, et al. (2009) Congenital hypomyelinating neuropathy with lethal conduction failure in mice carrying the Egr2 I268N mutation. J Neurosci 29: 2312-2321.
45. Ghosh AK, Bhattacharyya S, Wei J, Kim S, Barak Y, et al. (2009) Peroxisome proliferator-activated receptor-{gamma} abrogates Smad-dependent collagen stimulation by targeting the p300 transcriptional coactivator. FASEB J.