Proangiogenic effects of environmentally relevant levels of bisphenol a in human primary endothelial cells

Archives of Toxicology

Volumn 86, Issue 3, 2012, Pages 465-474

  Andersson, Helén ^a   Brittebo, Eva ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Angiogenesis; Bisphenol A; Endothelium; HUVEC; Nitric oxide; Tube formation

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CONNEXIN 43; CYCLOOXYGENASE 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; ESTROGEN RECEPTOR BETA; INTERLEUKIN 8; MESSENGER RNA; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

CELLS, CULTURED; CONNEXIN 43; ENDOTHELIAL CELLS; ENVIRONMENTAL POLLUTANTS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHENOLS; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84858071486     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-011-0766-2     Document Type: Article

References (52)

1. Andersson H, Piras E, Demma J, Hellman B, Brittebo E (2009) Low levels of the air pollutant 1-nitropyrene induce DNA damage, increased levels of reactive oxygen species and endoplasmic reticulum stress in human endothelial cells. Toxicology 262(1):57-64
2. Andersson H, Garscha U, Brittebo E (2011) Effects of PCB126 and 17beta-oestradiol on endothelium-derived vasoactive factors in human endothelial cells. Toxicology 285(1-2):46-56
3. Arnaoutova I, Kleinman HK (2010) In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc 5(4):628-635
4. Arnaoutova I, George J, Kleinman HK, Benton G (2009) The endothelial cell tube formation assay on basement membrane turns 20: state of the science and the art. Angiogenesis 12(3):267-274
5. Baumgartner-Parzer SM, Wagner L, Reining G, Sexl V, Nowotny P, Muller M, Brunner M, Waldhausl W (1997) Increase by triiodothyronine of endothelin-1, fibronectin and von Willebrand factor in cultured endothelial cells. J Endocrinol 154(2):231-239 (Pubitemid 27330635)
6. Bellafiore M, Sivverini G, Palumbo D, Macaluso F, Bianco A, Palma A, Farina F (2007) Increased cx43 and angiogenesis in exercised mouse hearts. Int J Sports Med 28(9):749-755 (Pubitemid 47414165)
7. Bonefeld-Jorgensen EC, Long M, Hofmeister MV, Vinggaard AM (2007) Endocrine-disrupting potential of bisphenol A, bisphenol A dimethacrylate, 4-n-nonylphenol, and 4-n-octylphenol in vitro: new data and a brief review. Environ Health Perspect 115 Suppl 1:69-76
8. Bosquiazzo VL, Varayoud J, Munoz-de-Toro M, Luque EH, Ramos JG (2011) Effects of neonatal exposure to bisphenol A on steroid regulation of vascular endothelial growth factor expression and endothelial cell proliferation in the adult rat uterus. Biol Reprod 82(1):86-95
9. Bouloumie A, Schini-Kerth VB, Busse R (1999) Vascular endothelial growth factor up-regulates nitric oxide synthase expression in endothelial cells. Cardiovasc Res 41(3):773-780 (Pubitemid 29130642)
10. Buteau-LozanoH,Velasco G, Cristofari M, Balaguer P, Perrot-Applanat M (2008) Xenoestrogens modulate vascular endothelial growth factor secretion in breast cancer cells through an estrogen receptor-dependent mechanism. J Endocrinol 196(2):399-412 (Pubitemid 351298525)
11. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9(6):653-660
12. Chevalier N, Bouskine A, Fenichel P (2011) Bisphenol A promotes testicular seminoma cell proliferation through GPER/GPR30. Int J Cancer [Epub ahead of print, 02/12/2011]. doi:10.1002/ijc.25972
13. Das H, George JC, Joseph M, Das M, Abdulhameed N, Blitz A, Khan M, Sakthivel R, Mao HQ, Hoit BD, Kuppusamy P, Pompili VJ (2009) Stem cell therapy with overexpressed VEGF and PDGF genes improves cardiac function in a rat infarct model. PLoS One 4(10):e7325. doi:10.1371/journal.pone.0007325
14. Dimmeler S, Dernbach E, Zeiher AM (2000) Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett 477(3): 258-262 (Pubitemid 30450177)
15. Durando M, Kass L, Perdomo V, Bosquiazzo VL, Luque EH, Munozde-Toro M (2011) Prenatal exposure to bisphenol A promotes angiogenesis and alters steroid-mediated responses in the mammary glands of cycling rats. J Steroid Biochem Mol Biol 127:35-43
16. Feng Y, Venema VJ, Venema RC, Tsai N, Caldwell RB (1999) VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun 256(1):192-197 (Pubitemid 29298939)
17. Figueroa XF, Duling BR (2009) Gap junctions in the control of vascular function. Antioxid Redox Signal 11(2):251-266
18. Florian M, Lu Y, Angle M, Magder S (2004) Estrogen induced changes in Akt-dependent activation of endothelial nitric oxide synthase and vasodilation. Steroids 69(10):637-645 (Pubitemid 39297702)
19. Fukumura D, Kashiwagi S, Jain RK (2006) The role of nitric oxide in tumour progression. Nat Rev Cancer 6(7):521-534 (Pubitemid 43980541)
20. Gossl M, Versari D, Hildebrandt HA, Bajanowski T, Sangiorgi G, Erbel R, Ritman EL, Lerman LO, Lerman A (2010) Segmental heterogeneity of vasa vasorum neovascularization in human coronary atherosclerosis. JACC Cardiovasc Imaging 3(1):32-40
21. Grasselli F, Baratta L, Baioni L, Bussolati S, Ramoni R, Grolli S, Basini G (2010) Bisphenol A disrupts granulosa cell function. Domest Anim Endocrinol 39(1):34-39
22. Jenkins S, Raghuraman N, Eltoum I, Carpenter M, Russo J, Lamartiniere CA (2009) Oral exposure to bisphenol a increases dimethylbenzanthracene-induced mammary cancer in rats. Environ Health Perspect 117(6):910-915
23. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139(10):4252-4263 (Pubitemid 28513713)
24. Kwak BR, Pepper MS, Gros DB, Meda P (2001) Inhibition of endothelial wound repair by dominant negative connexin inhibitors. Mol Biol Cell 12(4):831-845 (Pubitemid 33051982)
25. Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, Wallace RB, Melzer D (2008) Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300(11):1303-1310
26. Ledoux S, Queguiner I, Msika S, Calderari S, Rufat P, Gasc JM, Corvol P, Larger E (2008) Angiogenesis associated with visceral and subcutaneous adipose tissue in severe human obesity. Diabetes 57(12):3247-3257
27. Long X, Burke KA, Bigsby RM, Nephew KP (2001) Effects of the xenoestrogen bisphenol A on expression of vascular endothelial growth factor (VEGF) in the rat. Exp Biol Med (Maywood) 226(5):477-483 (Pubitemid 32506375)
28. Luksha L, Kublickiene K (2009) The role of estrogen receptor subtypes for vascular maintenance. Gynecol Endocrinol 25(2): 82-95
29. Luu NT, Rahman M, Stone PC, Rainger GE, Nash GB (2010) Responses of endothelial cells from different vessels to inflammatory cytokines and shear stress: evidence for the pliability of endothelial phenotype. J Vasc Res 47(5):451-461
30. Melzer D, Rice NE, Lewis C, Henley WE, Galloway TS (2010) Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLoS One 5(1): e8673
31. Miyawaki J, Sakayama K, Kato H, Yamamoto H, Masuno H (2007) Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb 14(5):245-252
32. Moreno PR, Purushothaman KR, Sirol M, Levy AP, Fuster V (2006) Neovascularization in human atherosclerosis. Circulation 113(18):2245-2252
33. Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M, Kanamoto N, Hataya Y, Shimatsu A, Kuzuya H, Nakao K (2002) Thyroid hormone action is disrupted by bisphenol A as an antagonist. J Clin Endocrinol Metab 87(11):5185-5190 (Pubitemid 35316363)
34. Noguchi S, Nakatsuka M, Asagiri K, Habara T, Takata M, Konishi H, Kudo T (2002) Bisphenol A stimulates NO synthesis through a non-genomic estrogen receptor-mediated mechanism in mouse endothelial cells. Toxicol Lett 135(1-2):95-101 (Pubitemid 35266721)
35. Oishi A, Takahashi K, Ohmichi M, Mochizuki Y, Inaba N, Kurachi H (2011) Role of glucocorticoid receptor in the inhibitory effect of medroxyprogesterone acetate on the estrogen-induced endothelial nitric oxide synthase phosphorylation in human umbilical vein endothelial cells. Fertil Steril 95(3):1168-1170
36. Piao M, Mori D, Satoh T, Sugita Y, Tokunaga O (2006) Inhibition of endothelial cell proliferation, in vitro angiogenesis, and the down-regulation of cell adhesion-related genes by genistein. Combined with a cDNA microarray analysis. Endothel J Endothel Cell Res 13(4):249-266 (Pubitemid 44463534)
37. Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, vom Saal FS (2007) In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 24(2):199-224 (Pubitemid 47385096)
38. Rutkowski JM, Davis KE, Scherer PE (2009) Mechanisms of obesity and related pathologies: the macro- and microcirculation of adipose tissue. FEBS J 276(20):5738-5746
39. Ryan KK, Haller AM, Sorrell JE, Woods SC, Jandacek RJ, Seeley RJ (2010) Perinatal exposure to bisphenol-a and the development of metabolic syndrome in CD-1 mice. Endocrinology 151(6): 2603-2612
40. Salian S, Doshi T, Vanage G (2009) Neonatal exposure of male rats to bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis. Toxicology 265(1-2):56-67
41. Sargis RM, Johnson DN, Choudhury RA, Brady MJ (2010) Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity (Silver Spring) 18(7):1283-1288
42. Sheng ZG, Zhu BZ (2011) Low Concentrations of bisphenol A induce mouse spermatogonial cell proliferation by G-protein-coupled receptor 30 and estrogen receptor-alpha. Environ Health Perspect [Epub ahead of print, 05/08/2011]. doi:10.1289/ehp.1103781
43. Somm E, Schwitzgebel VM, Toulotte A, Cederroth CR, Combescure C, Nef S, Aubert ML, Huppi PS (2009) Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect 117(10):1549-1555
44. Suzuma I, Mandai M, Takagi H, Suzuma K, Otani A, Oh H, Kobayashi K, Honda Y (1999) 17 Beta-estradiol increases VEGF receptor-2 and promotes DNA synthesis in retinal microvascular endothelial cells. Investig Ophthalmol Vis Sci 40(9):2122-2129 (Pubitemid 29365178)
45. Takayanagi S, Tokunaga T, Liu X, Okada H, Matsushima A, Shimohigashi Y (2006) Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERRgamma) with high constitutive activity. Toxicol Lett 167(2):95-105 (Pubitemid 44751375)
46. Talsness CE, Andrade AJ, Kuriyama SN, Taylor JA, vom Saal FS (2009) Components of plastic: experimental studies in animals and relevance for human health. Philos Trans R Soc Lond Ser B Biol Sci 364(1526):2079-2096
47. Thomas P, Dong J (2006) 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 102(1-5):175-179
48. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM (2009) Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 30(1):75-95
49. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G (2010) Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 118(8):1055-1070
50. Versari D, Daghini E, Virdis A, Ghiadoni L, Taddei S (2009) Endothelial dysfunction as a target for prevention of cardiovascular disease. Diabetes Care 32 Suppl 2:S314-S321
51. Wozniak AL, Bulayeva NN, Watson CS (2005) Xenoestrogens at picomolar to nanomolar concentrations trigger membrane estrogen receptor-alpha-mediated Ca2+ fluxes and prolactin release in GH3/B6 pituitary tumor cells. Environ Health Perspect 113(4):431-439 (Pubitemid 40601821)
52. Zhang X, Wang L, Dou Y, Zhao J, Jiang T, Qiao Z, Qiao J (2002) Testosterone and estradiol modulate TNF-alpha-induced expression of adhesion molecules in endothelial cells. Methods Find Exp Clin Pharmacol 24(3):125-130 (Pubitemid 34534587)