Crucial role of Nrf3 in smooth muscle cell differentiation from stem cells

Circulation Research

Volumn 106, Issue 5, 2010, Pages 870-879

  Pepe, Anna Elena ^a   Xiao, Qingzhong ^a   Zampetaki, Anna ^a   Zhang, Zhongyi ^a   Kobayashi, Akira ^b   Hu, Yanhua ^a   Xu, Qingbo ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b DOSHISHA UNIVERSITY   (Japan)

Author keywords

Endoplasmic reticulum stress; Nrf3; Reactive oxygen species; Smooth muscle cells; Stem cells

Indexed keywords

MYOCARDIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; NOX4 PROTEIN, MOUSE; NRF3 PROTEIN, MOUSE; NUCLEAR PROTEIN; TRANSACTIVATOR PROTEIN;

ANTIOXIDANT ACTIVITY; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STEM CELL; UPREGULATION; ANIMAL; BINDING SITE; CELL LINE; CELL LINEAGE; CONFOCAL MICROSCOPY; EMBRYONIC STEM CELL; ENDOPLASMIC RETICULUM; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; OXIDATIVE STRESS; PROMOTER REGION; RNA INTERFERENCE; TIME; TRANSCRIPTION INITIATION;

ANIMALS; ANTIOXIDANTS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BINDING SITES; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CHROMATIN IMMUNOPRECIPITATION; EMBRYONIC STEM CELLS; ENDOPLASMIC RETICULUM; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; MICE; MICROSCOPY, CONFOCAL; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; NUCLEAR PROTEINS; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; UP-REGULATION;

EID: 77950892237     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.211417     Document Type: Article

References (41)

1. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K, Nishikawa S. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature. 2000;408:92-96.
2. Xiao Q, Zeng L, Zhang Z, Margariti A, Ali ZA, Channon KM, Xu Q, Hu Y. Sca-1+ progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler Thromb Vasc Biol. 2006;26:2244-2251.
3. Xiao Q, Zeng L, Zhang Z, Hu Y, Xu Q. Stem cell-derived Sca-1 + progenitors differentiate into smooth muscle cells, which is mediated by collagen IV-integrin alpha1/beta1/alphav and PDGF receptor pathways. Am J Physiol Cell Physiol. 2007;292: C342-C352.
4. Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S, Capogrossi MC, Hu Y, Xu Q. HDAC3 is crucial in shear-and VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol. 2006;174:1059-1069.
5. Zampetaki A, Zeng L, Xiao Q, Margariti A, Hu Y, Xu Q. Lacking cytokine production in ES cells and ES-cell-derived vascular cells stimulated by TNF-alpha is rescued by HDAC inhibitor trichostatin A. Am J Physiol Cell Physiol. 2007;293: C1226-C1238.
6. Margariti A, Xiao Q, Zampetaki A, Zhang Z, Li H, Martin D, Hu Y, Zeng L, Xu Q. Splicing of HDAC7 modulates the SRF-myocardin complex during stem-cell differentiation towards smooth muscle cells. J Cell Sci. 2009;122:460-470.
7. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev. 1995;75:487-517.
8. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340:115-126.
9. Rodriguez-Menocal L, St-Pierre M, Wei Y, Khan S, Mateu D, Calfa M, Rahnemai-Azar AA, Striker G, Pham SM, Vazquez-Padron RI. The origin of post-injury neointimal cells in the rat balloon injury model. Cardiovasc Res. 2009;81:46-53.
10. Campbell JH, Campbell GR. The role of smooth muscle cells in atherosclerosis. Curr Opin Lipidol. 1994;5:323-330.
11. Rafii S. Circulating endothelial precursors: mystery, reality, and promise. J Clin Invest. 2000;105:17-19.
12. Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM. Smooth muscle progenitor cells in human blood. Circulation. 2002;106:1199-1204.
13. Xu Q, Zhang Z, Davison F, Hu Y. Circulating progenitor cells regenerate endothelium of vein graft atherosclerosis, which is diminished in ApoE-deficient mice. Circ Res. 2003;93: e76-e86.
14. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest. 2004;113:1258-1265.
15. Kobayashi A, Ito E, Toki T, Kogame K, Takahashi S, Igarashi K, Hayashi N, Yamamoto M. Molecular cloning and functional characterization of a new Cap'n' collar family transcription factor Nrf3. J Biol Chem. 1999;274:6443-6452.
16. Andrews NC, Erdjument-Bromage H, Davidson MB, Tempst P, Orkin SH. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature. 1993;362:722-728.
17. Chenais B, Derjuga A, Massrieh W, Red-Horse K, Bellingard V, Fisher SJ, Blank V. Functional and placental expression analysis of the human NRF3 transcription factor. Mol Endocrinol. 2005;19:125-137.
18. Derjuga A, Gourley TS, Holm TM, Heng HH, Shivdasani RA, Ahmed R, Andrews NC, Blank V. Complexity of CNC transcription factors as revealed by gene targeting of the Nrf3 locus. Mol Cell Biol. 2004;24:3286-3294.
19. Sankaranarayanan K, Jaiswal AK. Nrf3 negatively regulates antioxidantresponse element-mediated expression and antioxidant induction of NAD (P) H:quinone oxidoreductase1 gene. J Biol Chem. 2004;279:50810-50817.
20. Chowdhury I, Mo Y, Gao L, Kazi A, Fisher AB, Feinstein SI. Oxidant stress stimulates expression of the human peroxiredoxin 6 gene by a transcriptional mechanism involving an antioxidant response element. Free Radic Biol Med. 2009;46:146-153.
21. Xiao Q, Luo Z, Pepe AE, Margariti A, Zeng L, Xu Q. Embryonic stem cell differentiation into smooth muscle cells is mediated by Nox4-produced H2O2. Am J Physiol Cell Physiol. 2009;296: C711-C723.
22. Yin X, Mayr M, Xiao Q, Wang W, Xu Q. Proteomic analysis reveals higher demand for antioxidant protection in embryonic stem cell-derived smooth muscle cells. Proteomics. 2006;6:6437-6446.
23. Etchevers HC. The cap 'n' collar family member NF-E2-related factor 3 (Nrf3) is expressed in mesodermal derivatives of the avian embryo. Int J Dev Biol. 2005;49:363-367.
24. Wang Z, Wang DZ, Hockemeyer D, McAnally J, Nordheim A, Olson EN. Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature. 2004;428:185-189.
25. Nouhi Z, Chevillard G, Derjuga A, Blank V. Endoplasmic reticulum association and N-linked glycosylation of the human Nrf3 transcription factor. FEBS Lett. 2007;581:5401-5406.
26. Zhang Y, Kobayashi A, Yamamoto M, Hayes JD. The Nrf3 transcription factor is a membrane-bound glycoprotein targeted to the endoplasmic reticulum through its N-terminal homology box 1 sequence. J Biol Chem. 2009;284:3195-3210.
27. Cui K, Coutts M, Stahl J, Sytkowski AJ. Novel interaction between the transcription factor CHOP (GADD153) and the ribosomal protein FTE/S3a modulates erythropoiesis. J Biol Chem. 2000;275:7591-7596.
28. Pereira RC, Delany AM, Canalis E. CCAAT/enhancer binding protein homologous protein (DDIT3) induces osteoblastic cell differentiation. Endocrinology. 2004;145:1952-1960.
29. Gass JN, Gifford NM, Brewer JW. Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J Biol Chem. 2002;277:49047-49054.
30. Yang L, Carlson SG, McBurney D, Horton WE Jr. Multiple signals induce endoplasmic reticulum stress in both primary and immortalized chondrocytes resulting in loss of differentiation, impaired cell growth, and apoptosis. J Biol Chem. 2005;280:31156-31165.
31. Cho YM, Jang YS, Jang YM, Chung SM, Kim HS, Lee JH, Jeong SW, Kim IK, Kim JJ, Kim KS, Kwon OJ. Induction of unfolded protein response during neuronal induction of rat bone marrow stromal cells and mouse embryonic stem cells. Exp Mol Med. 2009;41:440-452.
32. Nakanishi K, Dohmae N, Morishima N. Endoplasmic reticulum stress increases myofiber formation in vitro. FASEB J. 2007;21:2994-3003.
33. Yoshida H. ER stress and diseases. FEBS J. 2007;274:630-658.
34. Forman HJ, Fukuto JM, Torres M. Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol Cell Physiol. 2004;287: C246-C256.
35. Clempus RE, Griendling KK. Reactive oxygen species signaling in vascular smooth muscle cells. Cardiovasc Res. 2006;71:216-225.
36. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest. 2006;116:36-48.
37. Wang D, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA, Olson EN. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell. 2001;105:851-862.
38. Miano JM. Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol. 2003;35:577-593.
39. Perot G, Derre J, Coindre JM, Tirode F, Lucchesi C, Mariani O, Gibault L, Guillou L, Terrier P, Aurias A. Strong smooth muscle differentiation is dependent on myocardin gene amplification in most human retroperitoneal leiomyosarcomas. Cancer Res. 2009;69:2269-2278.
40. Long X, Creemers EE, Wang DZ, Olson EN, Miano JM. Myocardin is a bifunctional switch for smooth versus skeletal muscle differentiation. Proc Natl Acad Sci U S A. 2007;104:16570-16575.
41. Jeon ES, Moon HJ, Lee MJ, Song HY, Kim YM, Bae YC, Jung JS, Kim JH. Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a TGF-betadependent mechanism. J Cell Sci. 2006;119:4994-5005.