Oxidative stress-induced S100B protein expression from placenta and amnion might affect soluble Endoglin release from endothelial cells.pdf
Author preprint (930.4 kB)
This is an electronic version (Author’s preprint) of an article published in Molecular Human Reproduction;2010 Mar;16(3):188-99;The original published version is available at:http://molehr.oxfordjournals.org/cgi/reprint/16/3/188
[en] Oxidative stress with elevated intracellular Ca(2+) concentration as well as endothelial dysfunction is a component of pre-eclampsia. Our aim was to investigate the oxidative stress-dependent expression of Endoglin and Ca(2+)-binding S100B protein from villous and amniotic tissue cultures, and to assess sEng expression from S100B protein-stimulated endothelial cells. We initially examined Endoglin and Hydroxy-nonenal-(HNE)-modified proteins in the placentas and amnion obtained from women with pre-eclampsia (n = 8), and healthy controls (n = 8) by immunohistochemistry. To examine oxidative stress and the S100B protein effect on sEng expression from endothelial cells, normal villous and amniotic tissue cultures were stimulated by 4-HNE, sodium fluoride and xanthine/xanthine oxidase, whereas human umbilical vein endothelial cell cultures were treated with S100B protein in a dose- and time-dependent manner at 37 degrees C in an environment of 95% air and 5% of CO(2). Culture supernatants were assessed using ELISA. Cell viability was determined using MTS assay. The concentrations of sEng and S100B protein were significantly increased in the villous and amniotic tissue culture supernatants under oxidative stress. S100B protein-stimulated endothelial cells released sEng into conditioned media with a significantly higher expression levels at a concentration of 200 pM-20 nM S100B by 2 h, whereas treated with 200 nM of S100B endothelial cells significantly expressed sEng by 12 h and stimulated the cell proliferation by the same period of time. Our findings show that oxidative stress affects sEng and S100B protein expression from villous and amniotic tissues, and picomolar and low nanomolar concentrations of S100B protein significantly up-regulate sEng release from endothelial cells leading to endothelial dysfunction.
Disciplines :
Reproductive medicine (gynecology, andrology, obstetrics)
Author, co-author :
Tskitishvili, Ekaterine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement > Osaka University Graduate School of Medicine, Department of Obstetrics and Gynecology
Sharentuya, Namuxila; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Temma-Asano, Kumiko; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Mimura, Kazuya; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Kinugasa-Taniguchi, Yukiko; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Kanagawa, Takeshi; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Fukuda, Hirotsugu; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Kimura, Tadashi; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Tomimatsu, Takuji; Osaka University Graduate School of Medicine > Department of Obstetrics and Gynecology
Shimoya, Koichiro; Kawasaki Medical School > Department of Obstetrics and Gynecology
Language :
English
Title :
Oxidative stress-induced S100B protein from placenta and amnion affects soluble Endoglin release from endothelial cells.
Bertolino P, Deckers M, Lebrin F, Ten-Dijke P. Transforming growth factor-b signal transduction in angiogenesis and vascular disorders. Chest 2005;128:585S-590S.
Bourdeau A, Dumont DJ, Letarte M. A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 1999;104:1343-1351.
Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 1992; 267:19027-19030.
Chlubek D, Zawierta J, Kazmierczyk A, Kramek J, Olszewska M, Stachowska E. Effect of different fluoride ion concentrations on malondialdehyde formation in the mitochondrial fraction of human placental cells. Bromat Chem Toksykol 1999;32:119-122.
Cindrova-Davies T. Gabor Than Award Lecture 2008: pre-eclampsia-from placental oxidative stress to maternal endothelial dysfunction. Placenta 2009;30(Suppl. A):S55-S65.
Cooke CL, Brockelsby JC, Baker PN, Davidge ST. The receptor for advanced glycation end products (RAGE) is elevated in women with preelcampsia. Hypertens Pregnancy 2003;22:173-184.
Cudmore M, Ahmad S, Al-Ani B, Fujusawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 2007;115:1789-1797.
Gajdusek CM, Luo Z, Mayberg MR. Basic fibroblast growth factor and transforming growth factor b-1: synergestic mediators of angiogenesis in vitro. Cell Physiol 1993;157:133-144.
Gougos A, St Jacques S, Greaves A, O'Connell PJ, A'Dapice AJ, Buhring HJ, Bernabeu C, Van Mourik JA, Letarte M. Identification of distinct epitopes of endoglin, an RGD-containing glycoprotein of endothelial cells, leukemic cells, and syncytiotrophoblasts. Int Immunol 1992;4:83-92.
Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, Ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-b1 receptors. EMBO J 2002;21:1743-1753.
Gu Y, Lewis DF, Wang Y. Placental productions and expressions of soluble endoglin, soluble fms-like tyrosine kinase receptor-1 and placental growth factor in normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2008;93:260-266.
Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P et al. RGAE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999;97:889-901.
Hirashima C, Ohkuchi A, Matsubara S, Suzuki H, Takahashi K, Usui R, Suzuki M. Alteration of serum soluble endoglin levels after the onset of preeclampsia is more pronounced in women with early-onset. Hypertens Res 2008;31:1541-1548.
Hung TH, Burton GJ. Hypoxia and reoxygenation: a possible mechanism for placental oxidative stress in preeclampsia. Taiwan J Obstet Gynecol 2006;45:189-200.
Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins: identification by morphologic and immunologic criteria. J Clin Invest 1973;52:2745-2756.
Jonker L, Arthur HM. Endoglin expression in early development is associated with vasculogenesis and angiogenesis. Mech Dev 2002; 110:193-196.
Kopcow HD, Karumanchi SA. Angiogenic factors and natural killer (NK) cells in the pathogenesis of preeclampsia. J Reprod Immunol 2007; 76:23-29.
Lastres P, Letamendia A, Zhang H, Rius C, Almendo N, Raab U, Lopez LA, Langa C, Fabra A, Letarte M et al. Endoglin modulates cellular responses to TGF-β1. J Cell Biol 1996;133:1109.
Lebrin F, Deckers M, Bertolino P, Ten-Dijke P. TGF-b receptor function in the endothelium. Cardiovasc Res 2005;65:599-608.
Leclerc E, Fritz G, Weibel M, Heizmann CW, Galichet A. S100B and S00A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation endproducts) immunoglobulin domains. J Biol Chem 2007;282:31317-31331.
Lee KY, Ito K, Hayashi R, Jazrawi EP, Barnes PJ, Adcock IM. NF-kappaB and activator protein 1 response elements and the role of histone modifications in IL-1 beta-induced TGF-beta1 gene transcription. J Immunol 2006;176:603-615.
Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thandani R et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006; 355:992-1005.
Li C, Issa R, Kumar P, Hampson IN, Lopez-Novoa JM, Bernabeu C, Kumar S. CD105 prevents apoptosis in hypoxic endothelial cells. J Cell Sci 2003;116:2677-2685.
Malek A, Sager R, Schneider H. Effect of hypoxia, oxidative stress and lipopolysaccharides on the release of prostaglandins and cytokines from human term placental explants. Placenta 2001;22(Suppl. A):S45-S50.
Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 2002;192:1-15.
McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J et al. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type1. Nat Genet 1994; 8:345-351.
Morikawa S, Kuraichi O, Tanaka M, Yoneda M, Uchida K, Itakura A, Furugori K, Mizutani S, Tomoda Y. Increased mitochondrial damage by lipid peroxidation in trophoblast cells of preeclamptic placentas. Biochem Mol Biol Int 1997;41:767-775.
Pepper MS, Vassalli JD, Orci L, Montesano R. Biphasic effect of transforming growth factor-β1 on in vitro angiogenesis. Exp Cell Res 1993;204:356-363.
Redman CW. The endoplasmic reticulum stress of placental impoverishment. Am J Pathol 2008;173:311-314.
Redman CWG, Sargent IL. Placental stress and pre-eclampsia: a revised view. Placenta 2009;30(Suppl. A):S38-S42.
Roberts JM, Gamill HS. Preeclampsia: recent insights. Hypertension 2005; 46:1243-1249.
Roberts JM, Hubel CA. The two-stage model of preeclampsia: variations on the theme. Placenta 2009;30(Suppl. A):S32-S37.
Robinson CJ, Johnson DD. Soluble endoglin as a second-trimester marker for peeclampsia. Am J Obstet Gynecol 2007;197:174.e1-174.e5.
Staff AC, Braekke K, Johnsen GJ, Karumanchi SA, Harsem NK. Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in preeclampsia. Am J Obstet Gynecol 2007; 197:176.e1-176.e6.
Shibata E, Ejima K, Nanri H, Toki N, Koyama C, Ikeda M, Kashimura M. Enhanced protein levels of protein thiol/disulphide oxidoreductases in placentae from pre-eclamptic subjects. Placenta 2001;22:566-572.
Takagi Y, Nikaido T, Toki T, Kita N, Kanai M, Ashida T. Levels of oxidative stress and redox-related molecules in the placenta in preeclampsia and fetal growth restriction. Virchows Arch 2004;444:49-55.
Temma K, Shimoya K, Zhang Q, Kimura T, Wasada K, Kanzaki T, Azuma C, Koyama M, Murata Y. Effects of 4-hydroxy-2-nonenal a marker of oxidative stress, on the cyclooxygenase-2 of human placenta in chorioamnionitis. Mol Hum Reprod 2004;10:167-171.
Tskitishvili E, Komoto Y, Temma-Asano K, Hayashi S, Kinugasa Y, Tsubouchi H, Song M, Kanagawa T, Shimoya K, Murata Y. S100B protein expression in the amnion and amniotic fluid in pregnancies complicated by pre-eclampsia. Mol Hum Reprod 2006;12:755-761.
Van Eldik LJ, Wainwright MS. The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci 2003;21:97-108.
Venkatesha S, Toporsian M, Lam C, Hanai JL, Mammoto T, Kim YM, Blodah Y, Lim KH, Yuan HT, Libermann TA et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006;12:642-649.
Walsh SW, Vaughan JE, Wang Y, Roberts LJ II. Placental isoprostane is significantly increased in preeclampsia. FASEB J 2000;14:1289-1296.
Yan SF, Ramasamy R, Naka Y, Schmidtt AM. Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ Res 2003;93:1169-1169.
Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ. Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human growth restriction. Am J Pathol 2008;173:451-462.
Yinon Y, Nevo O, Xu J, Many A, Rolfo A, Todros T, Post M, Caniggia I. Severe intrauterine growth restriction pregnancies have increased placental endoglin levels: hypoxic regulation via transforming growth factor-beta3. Am J Pathol 2008;172:77-85.
Zhang K, Kaufmann RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008;454:455-462.
Zhu Y, Sun Y, Xie L, Jin K, Sheibari N, Greenberg DA. Hypoxic induction of endoglin via mitogen-activated protein kinases in mouse brain microvascular endothelial cells. Stroke 2003;34:2483-2488.
