Protective Role for Tissue Inhibitor of Metalloproteinase-4, a Novel Peroxisome Proliferator-Activated Receptor-γ Target Gene, in Smooth Muscle in Deoxycorticosterone Acetate-Salt Hypertension

Hypertension

Volumn 67, Issue 1, 2016, Pages 214-222

  Ketsawatsomkron, Pimonrat ^a   Keen, Henry L ^a   Davis, Deborah R ^a   Lu, Ko Ting ^a   Stump, Madeliene ^a   De Silva, T Michael ^a   Hilzendeger, Aline M ^a   Grobe, Justin L ^a   Faraci, Frank M ^a   Sigmund, Curt D ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

hypertension; PPAR ; smooth muscle; tissue inhibitor of metalloproteinase 4; vascular remodeling

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; DEOXYCORTICOSTERONE ACETATE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR RESPONSE ELEMENT; TISSUE INHIBITOR OF METALLOPROTEINASE 4; UNCLASSIFIED DRUG; DNA; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE-4;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTERY; ARTERY DISEASE; ARTICLE; CHROMATIN; CONTROLLED STUDY; DEOXYCORTICOSTERONE-SALT INDUCED HYPERTENSION; FEMALE; GENE EXPRESSION PROFILING; MALE; MESENTERIC ARTERY; MORPHOMETRICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER; VASCULAR REMODELING; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD PRESSURE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HYPERTENSION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALS; BLOOD PRESSURE; DESOXYCORTICOSTERONE ACETATE; DISEASE MODELS, ANIMAL; DNA; GENE EXPRESSION REGULATION; HYPERTENSION; MICE; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; PPAR GAMMA; TISSUE INHIBITOR OF METALLOPROTEINASES; VASOCONSTRICTION;

EID: 84950335650     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.06391     Document Type: Article

References (41)

1. Eldor R, DeFronzo RA, Abdul-Ghani M. In vivo actions of peroxisome proliferator-activated receptors: glycemic control, insulin sensitivity, and insulin secretion. Diabetes Care. 2013;36(Suppl 2):S162-S174. doi: 10.2337/dcS13-2003.
2. Ketsawatsomkron P, Sigmund CD. Molecular mechanisms regulating vascular tone by peroxisome proliferator activated receptor gamma. Curr Opin Nephrol Hypertens. 2015;24:123-130. doi: 10.1097/MNH.0000000000000103.
3. Guan Y, Hao C, Cha DR, Rao R, Lu W, Kohan DE, Magnuson MA, Redha R, Zhang Y, Breyer MD. Thiazolidinediones expand body fluid volume through PPARgamma stimulation of ENaC-mediated renal salt absorption. Nat Med. 2005;11:861-866. doi: 10.1038/nm1278.
4. Zhang L, Xie P, Wang J, Yang Q, Fang C, Zhou S, Li J. Impaired peroxisome proliferator-activated receptor-gamma contributes to phenotypic modulation of vascular smooth muscle cells during hypertension. J Biol Chem. 2010;285:13666-13677. doi: 10.1074/jbc.M109.087718.
5. Barroso I, Gurnell M, Crowley VE, Agostini M, Schwabe JW, Soos MA, Maslen GL, Williams TD, Lewis H, Schafer AJ, Chatterjee VK, O'Rahilly S. Dominant negative mutations in human PPARgamma associated with severe insulin resistance, diabetes mellitus and hypertension. Nature. 1999;402:880-883. doi: 10.1038/47254.
6. Caron-Debarle M, Auclair M, Vigouroux C, Boccara F, Capel E, Vigarel C, Guerci B, Lascols O, Capeau J. PPARG mutations responsible for lipodystrophy with severe hypertension activate the cellular renin-angiotensin system. Arterioscler Thromb Vasc Biol. 2013; 33:829-838.
7. Beyer AM, Baumbach GL, Halabi CM, Modrick ML, Lynch CM, Gerhold TD, Ghoneim SM, de Lange WJ, Keen HL, Tsai YS, Maeda N, Sigmund CD, Faraci FM. Interference with PPARgamma signaling causes cerebral vascular dysfunction, hypertrophy, and remodeling. Hypertension. 2008;51:867-871. doi: 10.1161/HYPERTENSIONAHA.107.103648.
8. Keen HL, Halabi CM, Beyer AM, de Lange WJ, Liu X, Maeda N, Faraci FM, Casavant TL, Sigmund CD. Bioinformatic analysis of gene sets regulated by ligand-activated and dominant-negative peroxisome proliferator-activated receptor gamma in mouse aorta. Arterioscler Thromb Vasc Biol. 2010;30:518-525. doi: 10.1161/ATVBAHA.109.200733.
9. Halabi CM, Beyer AM, de Lange WJ, Keen HL, Baumbach GL, Faraci FM, Sigmund CD. Interference with PPAR gamma function in smooth muscle causes vascular dysfunction and hypertension. Cell Metab. 2008;7:215-226. doi: 10.1016/j.cmet.2007.12.008.
10. Pelham CJ, Ketsawatsomkron P, Groh S, Grobe JL, de Lange WJ, Ibeawuchi SR, Keen HL, Weatherford ET, Faraci FM, Sigmund CD. Cullin-3 regulates vascular smooth muscle function and arterial blood pressure via PPARγ and RhoA/Rho-kinase. Cell Metab. 2012;16:462-472. doi: 10.1016/j.cmet.2012.08.011.
11. Ketsawatsomkron P, Lorca RA, Keen HL, Weatherford ET, Liu X, Pelham CJ, Grobe JL, Faraci FM, England SK, Sigmund CD. PPARγ regulates resistance vessel tone through a mechanism involving RGS5-mediated control of protein kinase C and BKCa channel activity. Circ Res. 2012;111:1446-1458. doi: 10.1161/CIRCRESAHA.112.271577.
12. De Silva TM, Ketsawatsomkron P, Pelham C, Sigmund CD, Faraci FM. Genetic interference with peroxisome proliferator-activated receptor γ in smooth muscle enhances myogenic tone in the cerebrovasculature via A Rho kinase-dependent mechanism. Hypertension. 2015;65:345-351. doi: 10.1161/HYPERTENSIONAHA.114.04541.
13. Ouchi Y, Share L, Crofton JT, Iitake K, Brooks DP. Sex difference in the development of deoxycorticosterone-salt hypertension in the rat. Hypertension. 1987;9:172-177.
14. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402-408. doi: 10.1006/meth.2001.1262.
15. Borges GR, Morgan DA, Ketsawatsomkron P, Mickle AD, Thompson AP, Cassell MD, Mohapatra DP, Rahmouni K, Sigmund CD. Interference with peroxisome proliferator-activated receptor-γ in vascular smooth muscle causes baroreflex impairment and autonomic dysfunction. Hypertension. 2014;64:590-596. doi: 10.1161/HYPERTENSIONAHA.114.03553.
16. Maisel A, Mueller C, Neath SX, et al. Copeptin helps in the early detection of patients with acute myocardial infarction: primary results of the CHOPIN trial (Copeptin Helps in the early detection Of Patients with acute myocardial INfarction). J Am Coll Cardiol. 2013;62:150-160. doi: 10.1016/j.jacc.2013.04.011.
17. Watts SW, Rondelli C, Thakali K, Li X, Uhal B, Pervaiz MH, Watson RE, Fink GD. Morphological and biochemical characterization of remodeling in aorta and vena cava of DOCA-salt hypertensive rats. Am J Physiol Heart Circ Physiol. 2007;292:H2438-H2448. doi: 10.1152/ajpheart.00900.2006.
18. Raffetto JD, Khalil RA. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol. 2008;75:346-359. doi: 10.1016/j.bcp.2007.07.004.
19. Li X, Ycaza J, Blumberg B. The environmental obesogen tributyltin chloride acts via peroxisome proliferator activated receptor gamma to induce adipogenesis in murine 3T3-L1 preadipocytes. J Steroid Biochem Mol Biol. 2011;127:9-15. doi: 10.1016/j.jsbmb.2011.03.012.
20. Rahkonen OP, Koskivirta IM, Oksjoki SM, Jokinen E, Vuorio EI. Characterization of the murine Timp4 gene, localization within intron 5 of the synapsin 2 gene and tissue distribution of the mRNA. Biochim Biophys Acta. 2002;1577:45-52.
21. Nielsen R, Pedersen TA, Hagenbeek D, Moulos P, Siersbaek R, Megens E, Denissov S, Børgesen M, Francoijs KJ, Mandrup S, Stunnenberg HG. Genome-wide profiling of PPARgamma: RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes Dev. 2008;22:2953-2967. doi: 10.1101/gad.501108.
22. Agostini M, Gurnell M, Savage DB, Wood EM, Smith AG, Rajanayagam O, Garnes KT, Levinson SH, Xu HE, Schwabe JW, Willson TM, O'Rahilly S, Chatterjee VK. Tyrosine agonists reverse the molecular defects associated with dominant-negative mutations in human peroxisome proliferator-activated receptor gamma. Endocrinology. 2004;145:1527-1538. doi: 10.1210/en.2003-1271.
23. Liang CC, Park AY, Guan JL. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc. 2007;2:329-333. doi: 10.1038/nprot.2007.30.
24. Dollery CM, McEwan JR, Wang M, Sang QA, Liu YE, Shi YE. TIMP-4 is regulated by vascular injury in rats. Ann N Y Acad Sci. 1999;878:740-741.
25. Guo YH, Gao W, Li Q, Li PF, Yao PY, Chen K. Tissue inhibitor of metalloproteinases-4 suppresses vascular smooth muscle cell migration and induces cell apoptosis. Life Sci. 2004;75:2483-2493. doi: 10.1016/j. lfs.2004.07.007.
26. Ryan MJ, Didion SP, Davis DR, Faraci FM, Sigmund CD. Endothelial dysfunction and blood pressure variability in selected inbred mouse strains. Arterioscler Thromb Vasc Biol. 2002;22:42-48.
27. Yang T, Huang YG, Ye W, Hansen P, Schnermann JB, Briggs JP. Influence of genetic background and gender on hypertension and renal failure in COX-2-deficient mice. Am J Physiol Renal Physiol. 2005;288:F1125-F1132. doi: 10.1152/ajprenal.00219.2004.
28. Laragh JH. Biochemical profiling and the natural history of hypertensive diseases: low-renin essential hypertension, a benign condition. Circulation. 1971;44:971-974.
29. Grobe JL, Buehrer BA, Hilzendeger AM, Liu X, Davis DR, Xu D, Sigmund CD. Angiotensinergic signaling in the brain mediates metabolic effects of deoxycorticosterone (DOCA)-salt in C57 mice. Hypertension. 2011;57:600-607. doi: 10.1161/HYPERTENSIONAHA.110.165829.
30. Kandlikar SS, Fink GD. Mild DOCA-salt hypertension: sympathetic system and role of renal nerves. Am J Physiol Heart Circ Physiol. 2011;300:H1781-H1787. doi: 10.1152/ajpheart.00972.2010.
31. Kandlikar SS, Fink GD. Splanchnic sympathetic nerves in the development of mild DOCA-salt hypertension. Am J Physiol Heart Circ Physiol. 2011;301:H1965-H1973. doi: 10.1152/ajpheart.00086.2011.
32. Hilzendeger AM, Cassell MD, Davis DR, Stauss HM, Mark AL, Grobe JL, Sigmund CD. Angiotensin type 1a receptors in the subfornical organ are required for deoxycorticosterone acetate-salt hypertension. Hypertension. 2013;61:716-722. doi: 10.1161/HYPERTENSIONAHA.111.00356.
33. Basu R, Lee J, Morton JS, Takawale A, Fan D, Kandalam V, Wang X, Davidge ST, Kassiri Z. TIMP3 is the primary TIMP to regulate agonist-induced vascular remodelling and hypertension. Cardiovasc Res. 2013;98:360-371. doi: 10.1093/cvr/cvt067.
34. Step SE, Lim HW, Marinis JM, Prokesch A, Steger DJ, You SH, Won KJ, Lazar MA. Anti-diabetic rosiglitazone remodels the adipocyte transcriptome by redistributing transcription to PPARγ-driven enhancers. Genes Dev. 2014;28:1018-1028. doi: 10.1101/gad.237628.114.
35. Li G, Leff T. Altered promoter recycling rates contribute to dominant-negative activity of human peroxisome proliferator-activated receptor-gamma mutations associated with diabetes. Mol Endocrinol. 2007;21:857-864. doi: 10.1210/me.2006-0401.
36. Holobotovskyy V, Chong YS, Burchell J, He B, Phillips M, Leader L, Murphy TV, Sandow SL, McKitrick DJ, Charles AK, Tare M, Arnolda LF, Ganss R. Regulator of G protein signaling 5 is a determinant of gestational hypertension and preeclampsia. Sci Transl Med. 2015;7:290ra88. doi: 10.1126/scitranslmed.aaa5038.
37. Koskivirta I, Kassiri Z, Rahkonen O, Kiviranta R, Oudit GY, McKee TD, Kytö V, Saraste A, Jokinen E, Liu PP, Vuorio E, Khokha R. Mice with tissue inhibitor of metalloproteinases 4 (Timp4) deletion succumb to induced myocardial infarction but not to cardiac pressure overload. J Biol Chem. 2010;285:24487-24493. doi: 10.1074/jbc. M110.136820.
38. Harris AK, Hutchinson JR, Sachidanandam K, Johnson MH, Dorrance AM, Stepp DW, Fagan SC, Ergul A. Type 2 diabetes causes remodeling of cerebrovasculature via differential regulation of matrix metalloproteinases and collagen synthesis: role of endothelin-1. Diabetes. 2005;54:2638-2644.
39. Schiffrin EL. Vascular remodeling in hypertension: mechanisms and treatment. Hypertension. 2012;59:367-374. doi: 10.1161/HYPERTENSIONAHA.111.187021.
40. Iglarz M, Touyz RM, Amiri F, Lavoie MF, Diep QN, Schiffrin EL. Effect of peroxisome proliferator-activated receptor-alpha and -gamma activators on vascular remodeling in endothelin-dependent hypertension. Arterioscler Thromb Vasc Biol. 2003;23:45-51.
41. Meredith D, Panchatcharam M, Miriyala S, Tsai YS, Morris AJ, Maeda N, Stouffer GA, Smyth SS. Dominant-negative loss of PPARgamma function enhances smooth muscle cell proliferation, migration, and vascular remodeling. Arterioscler Thromb Vasc Biol. 2009;29:465-471. doi: 10.1161/ATVBAHA.109.184234.