Intronic CArG box regulates cysteine-rich protein 2 expression in the adult but not in developing vasculature

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 30, Issue 4, 2010, Pages 835-842

  Chen, Chung Huang ^a,b   Wu, Meng Ling ^a   Lee, Yi Chung ^c   Layne, Matthew D ^d   Yet, Shaw Fang ^a  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adult; Cysteine rich protein 2; Element; Intron; Vascular smooth muscle cell

Indexed keywords

CYSTEINE RICH PROTEIN 2; MYOCARDIN; PROTEIN; SERUM RESPONSE FACTOR; UNCLASSIFIED DRUG; CSRP2 PROTEIN, MOUSE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HNRPAB PROTEIN, MOUSE; MUSCLE PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; INTRON; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; TRANSGENE; TRANSGENIC MOUSE; AGE; AGING; ANIMAL; ARTERY; BINDING SITE; C57BL MOUSE; CELL CULTURE; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LACTOSE OPERON; METABOLISM; MUTATION; RAT; REGULATORY SEQUENCE; REPORTER GENE; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; VASCULAR SMOOTH MUSCLE;

AGE FACTORS; AGING; ANIMALS; ARTERIES; BINDING SITES; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; INTRONS; LAC OPERON; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; MUTATION; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; RATS; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; SERUM RESPONSE FACTOR; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 77950877724     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.109.197251     Document Type: Article

References (37)

1. Weiskirchen R, Pino JD, Macalma T, Bister K, Beckerle MC. The cysteine-rich protein family of highly related LIM domain proteins. J Biol Chem. 1995;270:28946-28954.
2. Louis HA, Pino JD, Schmeichel KL, Pomies P, Beckerle MC. Comparison of three members of the cysteine-rich protein family reveals functional conservation and divergent patterns of gene expression. J Biol Chem. 1997;272:27484-27491.
3. Arber S, Hunter JJ, Ross J Jr, Hongo M, Sansig G, Borg J, Perriard JC, Chien KR, Caroni P. MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell. 1997;88:393-403.
4. Chang DF, Belaguli NS, Iyer D, Roberts WB, Wu SP, Dong XR, Marx JG, Moore MS, Beckerle MC, Majesky MW, Schwartz RJ. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev Cell. 2003;4:107-118.
5. Jain MK, Fujita KP, Hsieh C-M, Endege WO, Sibinga NE, Yet S-F, Kashiki S, Lee W-S, Perrella MA, Haber E, Lee M-E. Molecular cloning and characterization of SmLIM, a developmentally regulated LIM protein preferentially expressed in aortic smooth muscle cells. J Biol Chem. 1996;271:10194-10199. (Pubitemid 26131584)
6. Wei J, Gorman TE, Liu X, Ith B, Tseng A, Chen Z, Simon DI, Layne MD, Yet S-F. Increased neointima formation in cysteine-rich protein 2-deficient mice in response to vascular injury. Circ Res. 2005;97: 1323-1331.
7. Lin D-W, Chang I-C, Tseng A, Wu ML, Chen C-H, Patenaude CA, Layne MD, Yet S-F. Transforming growth factor/3 up-regulates cysteine-rich protein 2 in vascular smooth muscle cells via activating transcription factor 2. J Biol Chem. 2008;283:15003-15014.
8. Chang Y-F, Wei J, Liu X, Chen Y-H, Layne MD, Yet S-F. Identification of a CArG-independent region of the cysteine-rich protein 2 promoter that directs expression in the developing vasculature. Am J Physiol Heart Circ Physiol. 2003;285:H1675-H1683.
9. Madsen CS, Regan CP, Hungerford JE, White SL, Manabe I, Owens GK. Smooth muscle-specific expression of the smooth muscle myosin heavy chain gene in transgenic mice requires 5'-flanking and first intronic DNA sequence. Circ Res. 1998;82:908-917.
10. Mack CP, Owens GK. Regulation of smooth muscle a-actin expression in vivo is dependent on CArG elements within the 5' and first intron promoter regions. Circ Res. 1999;84:852-861.
11. Yet S-F, Folta SC, Jain MK, Hsieh C-M, Maemura K, Layne MD, Zhang D, Marria PB, Yoshizumi M, Chin MT, Perrella MA, Lee M-E. Molecular cloning, characterization, and promoter analysis of the mouse Crp2/SmLim gene: Preferential expression of its promoter in the vascular smooth muscle cells of transgenic mice. J Biol Chem. 1998;273: 10530-10537.
12. Okano I, Yamamoto T, Kaji A, Kimura T, Mizuno K, Nakamura T. Cloning of CRP2, a novel member of the cysteine-rich protein family with two repeats of an unusual LIM/double zinc-finger motif. FEBS Letters. 1993;333:51-55.
13. Henderson JR, Brown D, Richardson JA, Olson EN, Beckerle MC. Expression of the gene encoding the LIM protein CRP2: a developmental profile. J Histochem Cytochem. 2002;50:107-111.
14. Yoshida T, Owens GK. Molecular determinants of vascular smooth muscle cell diversity. Circ Res. 2005;96:280-291.
15. Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ Jr, Miano JM. Defining the mammalian CArGome. Genome Res. 2006;16:197-207.
16. Wang D, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA, Olson EN. Activation of cardiac gene expression by myo-cardin, a transcriptional cofactor for serum response factor. Cell. 2001; 105:851-862.
17. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A, Olson EN. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci USA. 2002;99:14855-14860.
18. Cen B, Selvaraj A, Burgess RC, Hitzler JK, Ma Z, Morris SW, Prywes R. Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol Cell Biol. 2003;23:6597-6608.
19. Li S, Wang DZ, Wang Z, Richardson JA, Olson EN. The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc Natl Acad Sci USA. 2003;100:9366-9370.
20. Du KL, Chen M, Li J, Lepore JJ, Mericko P, Parmacek MS. Megakaryoblastic leukemia factor-1 transduces cytoskeletal signals and induces smooth muscle cell differentiation from undifferentiated embryonic stem cells. J Biol Chem. 2004;279:17578-17586.
21. Hinson JS, Medlin MD, Lockman K, Taylor JM, Mack CP. Smooth muscle cell-specific transcription is regulated by nuclear localization of the myocardin-related transcription factors. Am J Physiol Heart Circ Physiol. 2007;292:H1170-H1180.
22. Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol. 2002;34:1345-1356.
23. Layne MD, Yet S-F, Maemura K, Hsieh C-M, Liu X, Ith B, Lee M-E, Perrella MA. Characterization of the mouse aortic carboxypeptidase-like protein promoter reveals activity in differentiated and dedifferentiated vascular smooth muscle cells. Circ Res. 2002;90:728-736.
24. Sayers RL, Sundberg-Smith LJ, Rojas M, Hayasaka H, Parsons JT, Mack CP, Taylor JM. FRNK expression promotes smooth muscle cell maturation during vascular development and after vascular injury. Arterioscler Thromb Vasc Biol. 2008;28:2115-2122.
25. Schlaeger TM, Bartunkova S, Lawitts JA, Teichmann G, Risau W, Deutsch U, Sato TN. Uniform vascular-endothelial-cell-specific gene expression in both embryonic and adult transgenic mice. Proc Natl Acad Sci USA. 1997;94:3058-3063.
26. Li L, Miano JM, Mercer B, Olson EN. Expression of the SM22a promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J Cell Biol. 1996;132:849-859.
27. Smith AF, Bigsby RM, Word RA, Herring BP. A 310-bp minimal promoter mediates smooth muscle cell-specific expression of telokin. Am J Physiol. 1998;274:C1188-C1195.
28. Lilly B, Olson EN, Beckerle MC. Identification of a CArG box-dependent enhancer within the cysteine-rich protein 1 gene that directs expression in arterial but not venous or visceral smooth muscle cells. Dev Biol. 2001; 240:531-547.
29. Manabe I, Owens GK. The smooth muscle myosin heavy chain gene exhibits smooth muscle subtype selective modular regulation in vivo. J Biol Chem. 2001;276:39076-39087.
30. Miano JM, Carlson MJ, Spencer JA, Misra RP. Serum response factor-dependent regulation of the smooth muscle calponin gene. J Biol Chem. 2000;275:9814-9822.
31. Manabe I, Owens GK. CArG elements control smooth muscle subtype-specific expression of smooth muscle myosin in vivo. J Clin Invest. 2001;107:823-834.
32. Balza RO Jr, Misra RP. Role of the serum response factor in regulating contractile apparatus gene expression and sarcomeric integrity in cardio-myocytes. J Biol Chem. 2006;281:6498-6510.
33. Sun Q, Taurin S, Sethakorn N, Long X, Imamura M, Wang DZ, Zimmer WE, Dulin NO, Miano JM. Myocardin-dependent activation of the CArG box-rich smooth muscle y-actin gene: preferential utilization of a single CArG element through functional association with the NKX3.1 home-odomain protein. J Biol Chem. 2009;284:32582-32590.
34. Hendrix JA, Wamhoff BR, McDonald OG, Sinha S, Yoshida T, Owens GK. 5' CArG degeneracy in smooth muscle a-actin is required for injury-induced gene suppression in vivo. J Clin Invest. 2005;115: 418-427.
35. 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.
36. Weiskirchen R, Erdel M, Utermann G, and Bister K. Cloning, structural analysis, and chromosomal localization of the human CSRP2 gene encoding the LIM domain protein CRP2. Genomics. 1997;44:83-93.
37. Selvaraj A, Prywes R. Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL dependent. BMC Mol Biol. 2004;5:13.