Phytoestrogen genistein protects against endothelial barrier dysfunction in vascular endothelial cells through PKA-mediated suppression of RhoA signaling

Endocrinology

Volumn 154, Issue 2, 2013, Pages 727-737

  Jia, Zhenquan ^a   Zhen, Wei ^b   Babu, Pon Velayutham Anandh ^b   Liu, Dongmin ^b  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE INHIBITOR; ESTROGEN RECEPTOR INHIBITOR; FULVESTRANT; GENISTEIN; GUANOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN; N(G) NITROARGININE METHYL ESTER; PHYTOESTROGEN; PROTEINASE INHIBITOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN INHIBITOR; SERINE; THREONINE; THROMBIN; UNCLASSIFIED DRUG;

ACTIN MYOSIN INTERACTION; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SOYBEAN; STRESS FIBER;

ANIMALS; CALCIUM; CATTLE; CELL MEMBRANE PERMEABILITY; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOTHELIAL CELLS; GENISTEIN; MYOSIN LIGHT CHAINS; PHYTOESTROGENS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; THROMBIN;

EID: 84872709435     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1774     Document Type: Article

References (70)

1. Rosamond W, Flegal K, Friday G, et al. Heart disease and stroke statistics - 2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2007;115:e69-e171. (Pubitemid 46226160)
2. Hennig B, Chung BH, Watkins BA, Alvarado A. Disruption of endothelial barrier function by lipolytic remnants of triglyceride-rich lipoproteins. Atherosclerosis. 1992;95:235-247.
3. Bogatcheva NV, Garcia JG, Verin AD. Molecular mechanisms of thrombin-induced endothelial cell permeability. Biochemistry (Moscow). 2002;67:75-84.
4. Sandoval R, Malik AB, Naqvi T, Mehta D, Tiruppathi C. Requirement for Ca2+ signaling in the mechanism of thrombin-induced increase in endothelial permeability. Am J Physiol. 2001;280:L239-L247.
5. Essler M, Amano M, Kruse HJ, Kaibuchi K, Weber PC, Aepfelbacher M. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem. 1998;273:21867-21874. (Pubitemid 28405364)
6. Kim H, Peterson TG, Barnes S. Mechanisms of action of the soy isoflavone genistein: emerging role for its effects via transforming growth factor beta signaling pathways. Am J Clin Nutr. 1998;68:1418S-1425S. (Pubitemid 28550923)
7. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology. 1997;138:863-870. (Pubitemid 27089735)
8. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem. 1987;262:5592-5595.
9. Anthony MS, Clarkson TB, Williams JK. Effects of soy isoflavones on atherosclerosis: potential mechanisms. Am J Clin Nutr. 1998;68:1390S-1393S. (Pubitemid 28550918)
10. van der Schouw YT, de Kleijn MJ, Peeters PH, Grobbee DE. Phyto-oestrogens and cardiovascular disease risk. Nutr Metab Cardiovasc Dis. 2000;10:154-167.
11. Wangen KE, Duncan AM, Xu X, Kurzer MS. Soy isoflavones improve plasma lipids in normocholesterolemic and mildly hypercholesterolemic postmenopausal women. Am J Clin Nutr. 2001;73:225-231. (Pubitemid 32109850)
12. Walker HA, Dean TS, Sanders TA, Jackson G, Ritter JM, Chowienczyk PJ. The phytoestrogen genistein produces acute nitric oxide-dependent dilation of human forearm vasculature with similar potency to 17ss-estradiol. Circulation. 2001;103:258-262. (Pubitemid 32095412)
13. Squadrito F, Altavilla D, Morabito N, et al. The effect of the phytoestrogen genistein on plasma nitric oxide concentrations, endothelin-1 levels and endothelium-dependent vasodilation in postmenopausal women. Atherosclerosis. 2002;163:339-347. (Pubitemid 34615825)
14. Squadrito F, Altavilla D, Crisafulli A, et al. Effect of genistein on endothelial function in postmenopausal women: a randomized, double-blind, controlled study. Am J Med. 2003;114:470-476. (Pubitemid 36515109)
15. Nestel PJ, Yamashita T, Sasahara T, et al. Soy isoflavones improve systemic arterial compliance but not plasma lipids in menopausal and perimenopausal women. Arterioscler Thromb Vasc Biol. 1997;17:3392-3398. (Pubitemid 28028547)
16. Hodgson JM, Puddey IB, Beilin LJ, Mori TA, Croft KD. Supplementation with isoflavonoid phytoestrogens does not alter serum lipid concentrations: a randomized controlled trial in humans. J Nutr. 1998;128:728-732. (Pubitemid 28158487)
17. Valsecchi AE, Franchi S, Panerai AE, Rossi A, Sacerdote P, Colleoni M. The soy isoflavone genistein reverses oxidative and inflammatory state, neuropathic pain, neurotrophic and vasculature deficits in diabetes mouse model. Eur J Pharmacol. 650:694-702.
18. Walker HA, Dean TS, Sanders TA, Jackson G, Ritter JM, Chowienczyk PJ. The phytoestrogen genistein produces acute nitric oxide-dependent dilation of human forearm vasculature with similar potency to 17beta-estradiol. Circulation. 2001;103:258-262. (Pubitemid 32095412)
19. Fotsis T, Pepper M, Adlercreutz H, Hase T, Montesano R, Schweigerer L. Genistein, a dietary ingested isoflavonoid, inhibits cell proliferation and in vitro angiogenesis. J Nutr. 1995;125:790S-797S.
20. Dubey RK, Gillespie DG, Imthurn B, Rosselli M, Jackson EK, Keller PJ. Phytoestrogens inhibit growth and MAP kinase activity in human aortic smooth muscle cells. Hypertension. 1999;33:177-182. (Pubitemid 29065656)
21. Xu X, Harris KS, Wang HJ, Murphy PA, Hendrich S. Bioavailability of soybean isoflavones depends upon gut microflora in women. Journal of Nutrition. 1995;125:2307-2315.
22. King RA, Bursill DB. Plasma and urinary kinetics of the isoflavones daidzein and genistein after a single soy meal in humans. Am J Clin Nutr. 1998;67:867-872. (Pubitemid 28196660)
23. Babu PV, Si H, Fu Z, Zhen W, Liu D. Genistein prevents hyperglycemia-induced monocyte adhesion to human aortic endothelial cells through preservation of the cAMP signaling pathway and ameliorates vascular inflammation in obese diabetic mice. J Nutr. 2012;142:724-730.
24. D'Angelo G, Lee H, Weiner RI. cAMP-dependent protein kinase inhibits the mitogenic action of vascular endothelial growth factor and fibroblast growth factor in capillary endothelial cells by blocking Raf activation. J Cell Biochem. 1997;67:353-366. (Pubitemid 27509471)
25. Morandini R, Ghanem G, Portier-Lemarie A, Robaye B, Renaud A, Boeynaems JM. Action of cAMP on expression and release of adhesion molecules in human endothelial cells. Am J Physiol. 1996;270:H807-H816.
26. Moy AB, Bodmer JE, Blackwell K, Shasby S, Shasby DM. cAMP protects endothelial barrier function independent of inhibiting MLC20-dependent tension development. Am J Physiol. 1998;274:L1024-L1029.
27. Lum H, Jaffe HA, Schulz IT, Masood A, RayChaudhury A, Green RD. Expression of PKA inhibitor (PKI) gene abolishes cAMP-mediated protection to endothelial barrier dysfunction. Am J Physiol. 1999;277:C580-C588. (Pubitemid 29458193)
28. Liu D, Jiang H, Grange RW. Genistein activates the 3′,5′- cyclic adenosine monophosphate signaling pathway in vascular endothelial cells and protects endothelial barrier function. Endocrinology. 2005;146:1312-1320. (Pubitemid 40289318)
29. Liu D, Homan LL, Dillon JS. Genistein acutely stimulates nitric oxide synthesis in vascular endothelial cells by a cyclic adenosine 5′-monophosphate-dependent mechanism. Endocrinology. 2004;145:5532-5539. (Pubitemid 39564593)
30. Langeler EG, van Hinsbergh VW. Norepinephrine and iloprost improve barrier function of human endothelial cell monolayers: role of cAMP. Am J Physiol. 1991;260:C1052-C1059.
31. van Nieuw Amerongen GP, Vermeer MA, Negre-Aminou P, Lankelma J, Emeis JJ, van Hinsbergh VW. Simvastatin improves disturbed endothelial barrier function. Circulation. 2000;102:2803-2809.
32. Nakano T, Watanabe H, Ozeki M, et al. Endoplasmic reticulum Ca2+ depletion induces endothelial cell apoptosis independently of caspase-12. Cardiovasc Res. 2006;69:908-915. (Pubitemid 43227989)
33. Fu Z, Liu D. Long-term exposure to genistein improves insulin secretory function of pancreatic beta-cells. Eur J Pharmacol. 2009;616:321-327.
34. Essler M, Amano M, Kruse HJ, Kaibuchi K, Weber PC, Aepfelbacher M. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem. 1998;273:21867-21874. (Pubitemid 28405364)
35. Draijer R, Atsma DE, van der Laarse A, van Hinsbergh VW. cGMP and nitric oxide modulate thrombin-induced endothelial permeability. Regulation via different pathways in human aortic and umbilical vein endothelial cells. Circ Res. 1995;76:199-208.
36. Nakashima S, Koike T, Nozawa Y. Genistein, a protein tyrosine kinase inhibitor, inhibits thromboxane A2-mediated human platelet responses. Mol Pharmacol. 1991;39:475-480.
37. Peterson G, Barnes S. Genistein inhibits both estrogen and growth factor-stimulated proliferation of human breast cancer cells. Cell Growth Differ. 1996;7:1345-1351. (Pubitemid 26360683)
38. Seasholtz TM, Zhang T, Morissette MR, Howes AL, Yang AH, Brown JH. Increased expression and activity of RhoA are associated with increased DNA synthesis and reduced p27(Kip1) expression in the vasculature of hypertensive rats. Circ Res. 2001;89:488-495. (Pubitemid 34132642)
39. Qiao J, Huang F, Lum H. PKA inhibits RhoA activation: a protection mechanism against endothelial barrier dysfunction. Am J Physiol. 2003;284:L972-L980. (Pubitemid 36687132)
40. Stevens T, Creighton J, Thompson WJ. Control of cAMP in lung endothelial cell phenotypes. Implications for control of barrier function. Am J Physiol. 1999;277:L119-L126. (Pubitemid 29356758)
41. Westendorp RG, Draijer R, Meinders AE, van Hinsbergh VW. Cyclic-GMP-mediated decrease in permeability of human umbilical and pulmonary artery endothelial cell monolayers. J Vasc Res. 1994;31:42-51. (Pubitemid 24026299)
42. Garcia JG, Davis HW, Patterson CE. Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J Cell Physiol. 1995;163:510-522.
43. Patterson CE, Lum H, Schaphorst KL, Verin AD, Garcia JG. Regulation of endothelial barrier function by the cAMP-dependent protein kinase. Endothelium. 2000;7:287-308.
44. Han X, Kobzik L, Balligand JL, Kelly RA, Smith TW. Nitric oxide synthase (NOS3)-mediated cholinergic modulation of Ca2+ current in adult rabbit atrioventricular nodal cells. Circ Res. 1996;78:998-1008.
45. Adlercreutz H, Markkanen H, Watanabe S. Plasma concentrations of phyto-oestrogens in Japanese men. Lancet. 1993;342:1209-1210. (Pubitemid 23331713)
46. Liu D, Si H, Reynolds KA, Zhen W, Jia Z, Dillon JS. Dehydroepiandrosterone protects vascular endothelial cells against apoptosis through a Galphai protein-dependent activation of phosphatidylinositol 3-kinase/Akt and regulation of antiapoptotic Bcl-2 expression. Endocrinology. 2007;148:3068-3076. (Pubitemid 46996987)
47. Groten T, Pierce AA, Huen AC, Schnaper HW. 17 beta-estradiol transiently disrupts adherens junctions in endothelial cells. Faseb J. 2005;19:1368-1370. (Pubitemid 41113752)
48. Simoncini T, Scorticati C, Mannella P, et al. Estrogen receptor alpha interacts with Galpha13 to drive actin remodeling and endothelial cell migration via the RhoA/Rho kinase/moesin pathway. Mol Endocrinol. 2006;20:1756-1771. (Pubitemid 44148082)
49. Aberdeen GW, Wiegand SJ, Bonagura TW Jr., Pepe GJ, Albrecht ED. Vascular endothelial growth factor mediates the estrogen-induced breakdown of tight junctions between and increase in proliferation of microvessel endothelial cells in the baboon endometrium. Endocrinology. 2008;149:6076-6083.
50. Oviedo PJ, Sobrino A, Laguna-Fernandez A, et al. Estradiol induces endothelial cell migration and proliferation through estrogen receptor-enhanced RhoA/ROCK pathway. Mol Cell Endocrinol. 2011;335:96-103.
51. Shi S, Verin AD, Schaphorst KL, et al. Role of tyrosine phosphorylation in thrombin-induced endothelial cell contraction and barrier function. Endothelium. 1998;6:153-171. (Pubitemid 128537717)
52. Yuan SY. Protein kinase signaling in the modulation of microvascular permeability. Vasc Pharmacol. 2002;39:213-223. (Pubitemid 37490747)
53. Yu J, Rudic RD, Sessa WC. Nitric oxide-releasing aspirin decreases vascular injury by reducing inflammation and promoting apoptosis. Lab Invest. 2002;82:825-832. (Pubitemid 34761657)
54. Kataoka C, Egashira K, Inoue S, et al. Important role of Rho-kinase in the pathogenesis of cardiovascular inflammation and remodeling induced by long-term blockade of nitric oxide synthesis in rats. Hypertension. 2002;39:245-250. (Pubitemid 34165223)
55. Thors B, Halldorsson H, Thorgeirsson G. eNOS activation mediated by AMPK after stimulation of endothelial cells with histamine or thrombin is dependent on LKB1. Biochim Biophys Acta. 2011;1813:322-331.
56. Stahmann N, Woods A, Carling D, Heller R. Thrombin activates AMP-activated protein kinase in endothelial cells via a pathway involving Ca2+/calmodulin-dependent protein kinase kinase beta. Mol Cell Biol. 2006;26:5933-5945. (Pubitemid 44204514)
57. van Nieuw Amerongen GP, Draijer R, Vermeer MA, van Hinsbergh VW. Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA. Circ Res. 1998;83:1115-1123. (Pubitemid 28533520)
58. Hirase T, Kawashima S, Wong EY, et al. Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms. J Biol Chem. 2001;276:10423-10431.
59. Wojciak-Stothard B, Ridley AJ. Rho GTPases and the regulation of endothelial permeability. Vasc Pharmacol. 2002;39:187-199. (Pubitemid 37492962)
60. Garcia JG, Verin AD, Schaphorst K, et al. Regulation of endothelial cell myosin light chain kinase by Rho, cortactin, and p60(src). Am J Physiol. 1999;276:L989-L998. (Pubitemid 29321177)
61. Velasco G, Armstrong C, Morrice N, Frame S, Cohen P. Phosphorylation of the regulatory subunit of smooth muscle protein phosphatase1M at Thr850 induces its dissociation from myosin. FEBS Lett. 2002;527:101-104. (Pubitemid 35253847)
62. Birukov KG, Jacobson JR, Flores AA, et al. Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch [comment]. Am J Physiol. 2003;285:L785-L797. (Pubitemid 37158824)
63. Ogawa S, Koga S, Kuwabara K, et al. Hypoxia-induced increased permeability of endothelial monolayers occurs through lowering of cellular cAMP levels. Am J Physiol. 1992;262:C546-C554.
64. Koga S, Morris S, Ogawa S, et al. TNF modulates endothelial properties by decreasing cAMP. Am J Physiol. 1995;268:C1104-C1113.
65. Cioffi DL, Moore TM, Schaack J, Creighton JR, Cooper DM, Stevens T. Dominant regulation of interendothelial cell gap formation by calcium-inhibited type 6 adenylyl cyclase. J Cell Biol. 2002;157:1267-1278. (Pubitemid 34847795)
66. Baumer Y, Spindler V, Werthmann RC, Bunemann M, Waschke J. Role of Rac 1 and cAMP in endothelial barrier stabilization and thrombin-induced barrier breakdown. J Cell Physiol. 2009;220:716-726.
67. Filardo EJ, Quinn JA, Frackelton AR Jr., Bland KI. Estrogen action via the Gprotein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol. 2002;16:70-84. (Pubitemid 34044499)
68. Ghahremani MH, Cheng P, Lembo PM, Albert PR. Distinct roles for Galphai2, Galphai3, and Gbeta gamma in modulation offorskolin- or Gs-mediated cAMP accumulation and calcium mobilization by dopamine D2S receptors. J Biol Chem. 1999;274:9238-9245.
69. Thomas P, Dong J. Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J Steroid Biochem Mol Biol. 2006;102:175-179. (Pubitemid 44750643)
70. Broughton BR, Miller AA, Sobey CG. Endothelium-dependent relaxation by G protein-coupled receptor 30 agonists in rat carotid arteries. Am J Physiol. 298:H1055-H1061.