Resveratrol reverses monocrotaline-induced pulmonary vascular and cardiac dysfunction: A potential role for atrogin-1 in smooth muscle

Vascular Pharmacology

Volumn 56, Issue 1-2, 2012, Pages 64-73

  Paffett, Michael L ^a   Lucas, Selita N ^a   Campen, Matthew J ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Atrogin 1; Atrophy; Phytoalexin; Resveratrol; Smooth muscle hypertrophy; Ubiquitin proteasome system

Indexed keywords

ATROGIN 1; DNA; MESSENGER RNA; MONOCROTALINE; PLATELET DERIVED GROWTH FACTOR; RESVERATROL; SILDENAFIL; SIRTUIN 1; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; CELL CULTURE; CELL DAMAGE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFICACY; GENE EXPRESSION; HEART DISEASE; HEART RIGHT VENTRICLE HYPERTROPHY; HEART RIGHT VENTRICLE PRESSURE; HUMAN; HUMAN CELL; INJECTION; MALE; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PULMONARY ARTERY; PULMONARY ARTERY SMOOTH MUSCLE CELL; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SYSTOLIC BLOOD PRESSURE;

AIRWAY REMODELING; ANIMALS; BLOOD PRESSURE; CELL PROLIFERATION; CELLS, CULTURED; DRUG INTERACTIONS; HUMANS; HYPERTENSION, PULMONARY; HYPERTROPHY; HYPERTROPHY, RIGHT VENTRICULAR; KV1.5 POTASSIUM CHANNEL; MALE; MONOCROTALINE; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NITRIC OXIDE SYNTHASE TYPE III; PROTEIN PRECURSORS; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIRTUIN 1; SKP CULLIN F-BOX PROTEIN LIGASES; STILBENES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS; VENTRICULAR REMODELING;

EID: 84856288270     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2011.11.002     Document Type: Article

References (43)

1. Bdolah Y., Segal A., Tanksale P., Karumanchi S.A., Lecker S.H. Atrophy-related ubiquitin ligases atrogin-1 and MuRF-1 are associated with uterine smooth muscle involution in the postpartum period. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292(2):R971-R976.
2. Bonnet S., Rochefort G., Sutendra G., Archer S.L., Haromy A., Webster L., Hashimoto K., Bonnet S.N., Michelakis E.D. The nuclear factor of activated T cells in pulmonary arterial hypertension can be therapeutically targeted. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(27):11418-11423.
3. Budhiraja R., Tuder R.M., Hassoun P.M. Endothelial dysfunction in pulmonary hypertension. Circulation 2004, 109(2):159-165.
4. Carvalho R.F., Castan E.P., Coelho C.A., Lopes F.S., Almeida F.L., Michelin A., de Souza R.W., Araujo J.P., Cicogna A.C., Pai-Silva M. Heart failure increases atrogin-1 and MuRF1 gene expression in skeletal muscle with fiber type-specific atrophy. J. Mol. Histol. 2010, 41(1):81-87.
5. Chicoine L.G., Stewart J.A., Lucchesi P.A. Is resveratrol the magic bullet for pulmonary hypertension?. Hypertension 2009, 54(3):473-474.
6. Csibi A., Leibovitch M.P., Cornille K., Tintignac L.A., Leibotvitch S.A. MAFbx/Atrogin-1 controls the activity of the initiation factor eIF3-f in skeletal muscle atrophy by targeting multiple C-terminal lysines. J. Biol. Chem. 2009, 284(7):4413-4421.
7. Csiszar A., Labinskyy N., Olson S., Pinto J.T., Gupte S., Wu J.M., Hu F., Ballabh P., Podlutsky A., Losonczy G., de Cabo R., Mathew R., Wolin M.S., Ungvari Z. Resveratrol Prevents Monocrotaline-Induced Pulmonary Hypertension in Rats. Hypertension 2009, 54(3):668-675.
8. Dai Z.K., Cheng Y.J., Chung H.H., Wu J.R., Chen I.J., Wu B.N. KMUP-1 ameliorates monocrotaline-induced pulmonary artery hypertension the modulation of Ca2+ sensitization and K+ channel. Life Sci. 2010, 86(19-20):747-755.
9. de Frutos S., Spangler R., Alo D., Gonzalez-Bosc L.V. NFATc3 mediates chronic hypoxia-induced pulmonary arterial remodeling with alpha-actin up-regulation. J. Biol. Chem. 2007, 282(20):15081-15089.
10. de Frutos S., Duling L., Alo D., Berry T., Jackson-Weaver O., Walker M., Kanagy N., Gonzalez-Bosc L. NFATc3 is required for intermittent hypoxia-induced hypertension. Am. J. Physiol. Heart Circ. Physiol. 2008, 294(5):H2382-H2390.
11. Essaghir A., Dif N., Marbehant C.Y., Coffer P.J., Demoulin J.B. The transcription of FOXO genes is stimulated by FOXO3 and repressed by growth factors. J. Biol. Chem. 2009, 284(16):10334-10342.
12. Fang D., Wang H.Y., Fang N., Altman Y., Elly C., Liu Y.C. Cbl-b, a RING-type E3 ubiquitin ligase, targets phosphatidylinositol 3-kinase for ubiquitination in T cells. J. Biol. Chem. 2001, 276(7):4872-4878.
13. Grammer J.B., Bleiziffer S., Monticelli F., Lange R., Bauernschmitt R. Calcineurin and matrix protein expression in cardiac hypertrophy: evidence for calcineurin B to control excessive hypertrophic signaling. Basic Res. Cardiol. 2006, 101(4):292-300.
14. Haider U.G., Sorescu D., Griendling K.K., Vollmar A.M., Dirsch V.M. Resveratrol suppresses angiotensin II-induced Akt/protein kinase B and p70 S6 kinase phosphorylation and subsequent hypertrophy in rat aortic smooth muscle cells. Mol. Pharmacol. 2002, 62(4):772-777.
15. Hepple R.T., Qin M., Nakamoto H., Goto S. Caloric restriction optimizes the proteasome pathway with aging in rat plantaris muscle: implications for sarcopenia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295(4):R1231-R1237.
16. Horinouchi H., Kumamoto T., Kimura N., Ueyama H., Tsuda T. Myosin loss in denervated rat soleus muscle after dexamethasone treatment. Pathobiology 2005, 72(3):108-116.
17. Humbert M., Morrell N.W., Archer S.L., Stenmark K.R., MacLean M.R., Lang I.M., Christman B.W., Weir E.K., Eickelberg O., Voelkel N.F., Rabinovitch M. Cellular and molecular pathobiology of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 2004, 43(12 Suppl. S):13S-24S.
18. Lagirand-Cantaloube J., Cornille K., Csibi A., Batonnet-Pichon S., Leibovitch M.P., Leibovitch S.A. Inhibition of atrogin-1/MAFbx mediated MyoD proteolysis prevents skeletal muscle atrophy in vivo. PLoS One 2009, 4(3):e4973.
19. Li H.H., Kedar V., Zhang C., McDonough H., Arya R., Wang D.Z., Patterson C. Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J. Clin. Invest. 2004, 114(8):1058-1071.
20. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(4):402-408.
21. Lund A.K., Knuckles T.L., Obot Akata C., Shohet R., McDonald J.D., Gigliotti A., Seagrave J.C., Campen M.J. Gasoline exhaust emissions induce vascular remodeling pathways involved in atherosclerosis. Toxicol. Sci. 2007, 95(2):485-494.
22. Marquis K., Debigare R., Lacasse Y., LeBlanc P., Jobin J., Carrier G., Maltais F. Midthigh muscle cross-sectional area is a better predictor of mortality than body mass index in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2002, 166(6):809-813.
23. McFarlane C., Plummer E., Thomas M., Hennebry A., Ashby M., Ling N., Smith H., Sharma M., Kambadur R. Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J. Cell. Physiol. 2006, 209(2):501-514.
24. McLoughlin T.J., Smith S.M., DeLong A.D., Wang H., Unterman T.G., Esser K.A. FoxO1 induces apoptosis in skeletal myotubes in a DNA-binding-dependent manner. Am. J. Physiol. Cell Physiol. 2009, 297(3):C548-C555.
25. Mouchaers K.T., Schalij I., de Boer M.A., Postmus P.E., van Hinsbergh V.W., Nieuw Amerongen G.P., Vonk N.A., van der Laarse W.J. Effective reduction of MCT-PAH by Fasudil. Comparison with Bosentan and Sildenafil. Eur. Respir. J. 2010, 36(4):800-807.
26. Newby A.C., Zaltsman A.B. Molecular mechanisms in intimal hyperplasia. J. Pathol. 2000, 190(3):300-309.
27. Ni Y.G., Berenji K., Wang N., Oh M., Sachan N., Dey A., Cheng J., Lu G., Morris D.J., Castrillon D.H., Gerard R.D., Rothermel B.A., Hill J.A. Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation 2006, 114(11):1159-1168.
28. Ni Y.G., Wang N., Cao D.J., Sachan N., Morris D.J., Gerard R.D., Kuro O., Rothermel B.A., Hill J.A. FoxO transcription factors activate Akt and attenuate insulin signaling in heart by inhibiting protein phosphatases. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(51):20517-20522.
29. Poussier B., Cordova A.C., Becquemin J.P., Sumpio B.E. Resveratrol inhibits vascular smooth muscle cell proliferation and induces apoptosis. J. Vasc. Surg. 2005, 42(6):1190-1197.
30. Razeghi P., Baskin K.K., Sharma S., Young M.E., Stepkowski S., Essop M.F., Taegtmeyer H. Atrophy, hypertrophy, and hypoxemia induce transcriptional regulators of the ubiquitin proteasome system in the rat heart. Biochem. Biophys. Res. Commun. 2006, 342(2):361-364.
31. Schermuly R.T., Kreisselmeier K.P., Ghofrani H.A., Yilmaz H., Butrous G., Ermert L., Ermert M., Weissmann N., Rose F., Guenther A., Walmrath D., Seeger W., Grimminger F. Chronic sildenafil treatment inhibits monocrotaline-induced pulmonary hypertension in rats. Am. J. Respir. Crit. Care Med. 2004, 169(1):39-45.
32. Siddiqui S., Martin J.G. Structural aspects of airway remodeling in asthma. Curr. Allergy Asthma Rep. 2008, 8(6):540-547.
33. Son Y.H., Jeong Y.T., Lee K.A., Choi K.H., Kim S.M., Rhim B.Y., Kim K. Roles of MAPK and NF-kappaB in interleukin-6 induction by lipopolysaccharide in vascular smooth muscle cells. J. Cardiovasc. Pharmacol. 2008, 51(1):71-77.
34. Stein T.P., Wade C.E. Protein turnover in atrophying muscle: from nutritional intervention to microarray expression analysis. Curr. Opin. Clin. Nutr. Metab. Care 2003, 6(1):95-102.
35. Stenmark K.R., Gerasimovskaya E., Nemenoff R.A., Das M. Hypoxic activation of adventitial fibroblasts: role in vascular remodeling. Chest 2002, 122(6 Suppl.):326S-334S.
36. Torres S.M., Divi R.L., Walker D.M., McCash C.L., Carter M.M., Campen M.J., Einem T.L., Chu Y., Seilkop S.K., Kang H., Poirier M.C., Walker V.E. In Utero Exposure of Female CD-1 Mice to AZT and/or 3TC: II. Persistence of Functional Alterations in Cardiac Tissue. Cardiovasc. Toxicol. 2010, 10(2):87-99.
37. Venkatesan B.A., Valente J., Reddy V.S., Siwik D.A., Chandrasekar B. Resveratrol blocks interleukin-18-EMMPRIN cross-regulation and smooth muscle cell migration. Am. J. Physiol. Heart Circ. Physiol. 2009, 297(2):H874-H886.
38. Wilson D.W., Segall H.J., Pan L.C., Dunston S.K. Progressive inflammatory and structural changes in the pulmonary vasculature of monocrotaline-treated rats. Microvasc. Res. 1989, 38(1):57-80.
39. Yang D.L., Zhang H.G., Xu Y.L., Gao Y.H., Yang X.J., Hao X.Q., Li X.H. Resveratrol inhibits right ventricular hypertrophy induced by monocrotaline in rats. Clin. Exp. Pharmacol. Physiol. 2010, 37(2):150-155.
40. Yen C.H., Leu S., Lin Y.C., Kao Y.H., Chang L.T., Chua S., Fu M., Wu C.J., Sun C.K., Yip H.K. Sildenafil limits monocrotaline-induced pulmonary hypertension in rats through suppression of pulmonary vascular remodeling. J. Cardiovasc. Pharmacol. 2010, 55(6):574-584.
41. Yu W., Fu Y.C., Zhou X.H., Chen C.J., Wang X., Lin R.B., Wang W. Effects of resveratrol on H(2)O(2)-induced apoptosis and expression of SIRTs in H9c2 cells. J. Cell. Biochem. 2009, 107(4):741-747.
42. Zeng Z., Li Y., Jiang Z., Wang C., Li B., Jiang W. The extracellular signal-regulated kinase is involved in the effects of sildenafil on pulmonary vascular remodeling. Cardiovasc. Ther. 2010, 28(1):23-29.
43. Zou J., Huang Y., Chen Q., Wang N., Cao K., Hsieh T.C., Wu J.M. Suppression of mitogenesis and regulation of cell cycle traverse by resveratrol in cultured smooth muscle cells. Int. J. Oncol. 1999, 15(4):647-651.