Placental Vesicles Carry Active Endothelial Nitric Oxide Synthase and Their Activity is Reduced in Preeclampsia

Hypertension

Volumn 70, Issue 2, 2017, Pages 372-381

  Motta Mejia, Carolina ^a,b   Kandzija, Neva ^a   Zhang, Wei ^a   Mhlomi, Vuyane ^a   Cerdeira, Ana Sofia ^a   Burdujan, Alexandra ^a   Tannetta, Dionne ^b   Dragovic, Rebecca ^a   Sargent, Ian L ^a   Redman, Christopher W ^a   Kishore, Uday ^b   Vatish, Manu ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b BRUNEL UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

endothelial nitric oxide synthase; hypertension; nitric oxide; preeclampsia; syncytiotrophoblast extracellular vesicles

Indexed keywords

ALKALINE PHOSPHATASE PLACENTA ISOENZYME; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE;

ADULT; ARTICLE; BIRTH WEIGHT; BODY MASS; CATALYSIS; CENTRIFUGATION; CLINICAL ARTICLE; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DIMERIZATION; ENZYME ACTIVITY; EX VIVO STUDY; EXOSOME; FEMALE; FLOW CYTOMETRY; GESTATIONAL AGE; HUMAN; HUMAN CELL; MEMBRANE MICROPARTICLE; PARITY; PHENOTYPE; PLACENTAL TRANSFER; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; SMOKING; SYNCYTIOTROPHOBLAST; SYSTOLIC BLOOD PRESSURE; UTERINE BLOOD VESSEL; WESTERN BLOTTING; BLOOD PRESSURE MEASUREMENT; CELL CULTURE; HYPERTENSION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PROCEDURES; STATISTICS; TROPHOBLAST; VASCULAR RESISTANCE;

ADULT; BLOOD PRESSURE DETERMINATION; CELLS, CULTURED; EXTRACELLULAR VESICLES; FEMALE; HUMANS; HYPERTENSION; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PRE-ECLAMPSIA; PREGNANCY; STATISTICS AS TOPIC; TROPHOBLASTS; VASCULAR RESISTANCE;

EID: 85020705629     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.117.09321     Document Type: Article

References (43)

1. Sanghavi M, Rutherford JD. Cardiovascular physiology of pregnancy. Circulation. 2014;130:1003-1008. doi: 10.1161/ CIRCULATIONAHA.114.009029.
2. WHO. WHO recommendations for prevention and treatment of preeclampsia and eclampsia. World Health Organization; 2011.
3. Roberts JM, Redman CW. Pre-eclampsia: more than pregnancy-induced hypertension. Lancet. 1993;341:1447-1451.
4. Redman CW, Sargent IL, Staff AC. IFPA Senior Award Lecture: making sense of pre-eclampsia-two placental causes of preeclampsia? Placenta. 2014;35(suppl):S20-S25. doi: 10.1016/j.placenta.2013.12.008.
5. Redman CW, Sacks GP, Sargent IL. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol. 1999;180(2 Pt 1):499-506.
6. Sladek SM, Magness RR, Conrad KP. Nitric oxide and pregnancy. Am J Physiol. 1997;272(2 pt 2):R441-R463.
7. Ignarro LJ. Nitric oxide. A novel signal transduction mechanism for transcellular communication. Hypertension. 1990;16:477-483.
8. Shah DA, Khalil RA. Bioactive factors in uteroplacental and systemic circulation link placental ischemia to generalized vascular dysfunction in hypertensive pregnancy and preeclampsia. Biochem Pharmacol. 2015;95:211-226. doi: 10.1016/j.bcp.2015.04.012.
9. Ashworth JR, Warren AY, Johnson IR, Baker PN. Plasma from preeclamptic women and functional change in myometrial resistance arteries. Br J Obstet Gynaecol. 1998;105:459-461.
10. Hayman R, Warren A, Johnson I, Baker P. Inducible change in the behavior of resistance arteries from circulating factor in preeclampsia: an effect specific to myometrial vessels from pregnant women. Am J Obstet Gynecol. 2001;184:420-426. doi: 10.1067/mob.2001.109733.
11. English FA, McCarthy FP, McSweeney CL, Quon AL, Morton JS, Sawamura T, Davidge ST, Kenny LC. Inhibition of lectin-like oxidized low-density lipoprotein-1 receptor protects against plasma-mediated vascular dysfunction associated with pre-eclampsia. Am J Hypertens. 2013;26:279-286. doi: 10.1093/ajh/hps035.
12. Khalil A, Hardman L, O Brien P. The role of arginine, homoarginine and nitric oxide in pregnancy. Amino Acids. 2015;47:1715-1727. doi: 10.1007/s00726-015-2014-1.
13. Myatt L, Brockman DE, Eis AL, Pollock JS. Immunohistochemical localization of nitric oxide synthase in the human placenta. Placenta. 1993;14:487-495.
14. Conrad KP, Vill M, McGuire PG, Dail WG, Davis AK. Expression of nitric oxide synthase by syncytiotrophoblast in human placental villi. FASEB J. 1993;7:1269-1276.
15. Buttery LD, McCarthy A, Springall DR, Sullivan MH, Elder MG, Michel T, Polak JM. Endothelial nitric oxide synthase in the human placenta: regional distribution and proposed regulatory role at the feto-maternal interface. Placenta. 1994;15:257-265.
16. Redman CW. Current topic: pre-eclampsia and the placenta. Placenta. 1991;12:301-308.
17. Maltepe E, Fisher SJ. Placenta: The forgotten organ. Annu Rev Cell Dev Biol. 2015;31:523-552. doi: 10.1146/annurev-cellbio-100814-125620.
18. Sarker S, Scholz-Romero K, Perez A, Illanes SE, Mitchell MD, Rice GE, Salomon C. Placenta-derived exosomes continuously increase in maternal circulation over the first trimester of pregnancy. J Transl Med. 2014;12:204. doi: 10.1186/1479-5876-12-204.
19. Salomon C, Torres MJ, Kobayashi M, Scholz-Romero K, Sobrevia L, Dobierzewska A, Illanes SE, Mitchell MD, Rice GE. A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration. PLoS One. 2014;9:e98667. doi: 10.1371/journal. pone.0098667.
20. Tannetta DS, Dragovic RA, Gardiner C, Redman CW, Sargent IL. Characterisation of syncytiotrophoblast vesicles in normal pregnancy and pre-eclampsia: expression of Flt-1 and endoglin. PLoS One. 2013;8:e56754. doi: 10.1371/journal.pone.0056754.
21. Tong M, Chamley LW. Placental extracellular vesicles and feto-maternal communication. Cold Spring Harb Perspect Med. 2015;5:a023028. doi: 10.1101/cshperspect.a023028.
22. Dragovic RA, Collett GP, Hole P, Ferguson DJ, Redman CW, Sargent IL, Tannetta DS. Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence Nanoparticle Tracking Analysis. Methods. 2015;87:64-74. doi: 10.1016/j.ymeth.2015.03.028.
23. Dragovic RA, Southcombe JH, Tannetta DS, Redman CW, Sargent IL. Multicolor flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and pre-eclamptic women. Biol Reprod. 2013;89:151. doi: 10.1095/biolreprod.113.113266.
24. Inglis HC, Danesh A, Shah A, Lacroix J, Spinella PC, Norris PJ. Techniques to improve detection and analysis of extracellular vesicles using flow cytometry. Cytometry A. 2015;87:1052-1063. doi: 10.1002/ cyto.a.22649.
25. Cai S, Alp NJ, McDonald D, Smith I, Kay J, Canevari L, Heales S, Channon KM. GTP cyclohydrolase I gene transfer augments intracellular tetrahydrobiopterin in human endothelial cells: effects on nitric oxide synthase activity, protein levels and dimerisation. Cardiovasc Res. 2002;55:838-849.
26. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, Knowles RG. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem. 1997;272:4959-4963.
27. Cai S, Khoo J, Mussa S, Alp NJ, Channon KM. Endothelial nitric oxide synthase dysfunction in diabetic mice: importance of tetrahydrobiopterin in eNOS dimerisation. Diabetologia. 2005;48:1933-1940. doi: 10.1007/ s00125-005-1857-5.
28. Seligman SP, Buyon JP, Clancy RM, Young BK, Abramson SB. The role of nitric oxide in the pathogenesis of preeclampsia. Am J Obstet Gynecol. 1994;171:944-948.
29. Burke SD, Zsengellér ZK, Khankin EV, et al. Soluble fms-like tyrosine kinase 1 promotes angiotensin II sensitivity in preeclampsia. J Clin Invest. 2016;126:2561-2574. doi: 10.1172/JCI83918.
30. Conrad KP, Davis AK. Nitric oxide synthase activity in placentae from women with pre-eclampsia. Placenta. 1995;16:691-699.
31. Kakui K, Sagawa N, Itoh H, Yura S, Korita D, Takemura M, Nuamah MA, Fujii S. Expression of nitric oxide synthase isoforms in the human placenta is not altered by labor. Endocr J. 2003;50:535-544.
32. Schiessl B, Mylonas I, Hantschmann P, Kuhn C, Schulze S, Kunze S, Friese K, Jeschke U. Expression of endothelial NO synthase, inducible NO synthase, and estrogen receptors alpha and beta in placental tissue of normal, preeclamptic, and intrauterine growth-restricted pregnancies. J Histochem Cytochem. 2005;53:1441-1449. doi: 10.1369/ jhc.4A6480.2005.
33. Schiessl B, Mylonas I, Kuhn C, Kunze S, Schulze S, Friese K, Jeschke U. Expression of estrogen receptor-alpha, estrogen receptor-beta and placental endothelial and inducible NO synthase in intrauterine growthrestricted and normal placentals. Arch Med Res. 2006;37:967-975. doi: 10.1016/j.arcmed.2006.03.011.
34. Zarlingo TJ, Eis AL, Brockman DE, Kossenjans W, Myatt L. Comparative localization of endothelial and inducible nitric oxide synthase isoforms in haemochorial and epitheliochorial placentae. Placenta. 1997;18:511-520.
35. Lyall F. Development of the utero-placental circulation: The role of carbon monoxide and nitric oxide in trophoblast invasion and spiral artery transformation. Microsc Res Tech. 2003;60:402-411. doi: 10.1002/jemt.10278.
36. Yoshida T, Limmroth V, Irikura K, Moskowitz MA. The NOS inhibitor, 7-nitroindazole, decreases focal infarct volume but not the response to topical acetylcholine in pial vessels. J Cereb Blood Flow Metab. 1994;14:924-929. doi: 10.1038/jcbfm.1994.123.
37. Vanwijk MJ, Svedas E, Boer K, Nieuwland R, Vanbavel E, Kublickiene KR. Isolated microparticles, but not whole plasma, from women with preeclampsia impair endothelium-dependent relaxation in isolated myometrial arteries from healthy pregnant women. Am J Obstet Gynecol. 2002;187:1686-1693.
38. Shomer E, Katzenell S, Zipori Y, Sammour RN, Isermann B, Brenner B, Aharon A. Microvesicles of women with gestational hypertension and preeclampsia affect human trophoblast fate and endothelial function. Hypertension. 2013;62:893-898. doi: 10.1161/ HYPERTENSIONAHA.113.01494.
39. Horn P, Cortese-Krott MM, Amabile N, Hundsdörfer C, Kröncke KD, Kelm M, Heiss C. Circulating microparticles carry a functional endothelial nitric oxide synthase that is decreased in patients with endothelial dysfunction. J Am Heart Assoc. 2012;2:e003764. doi: 10.1161/ JAHA.112.003764.
40. Kao CK, Morton JS, Quon AL, Reyes LM, Lopez-Jaramillo P, Davidge ST. Mechanism of vascular dysfunction due to circulating factors in women with pre-eclampsia. Clin Sci (Lond). 2016;130:539-549. doi: 10.1042/CS20150678.
41. Myatt L, Webster RP. Vascular biology of preeclampsia. J Thromb Haemost. 2009;7:375-384. doi: 10.1111/j.1538-7836.2008.03259.x.
42. O' Kane PD, Jackson G, Ferro A. Whole body nitric oxide production is not decreased in patients with coronary atherosclerosis but is inversely related to plasma homocysteine. Atherosclerosis. 2008;196:574-579.
43. Heiss C, Schanz A, Amabile N, Jahn S, Chen Q, Wong ML, Rassaf T, Heinen Y, Cortese-Krott M, Grossman W, Yeghiazarians Y, Springer ML. Nitric oxide synthase expression and functional response to nitric oxide are both important modulators of circulating angiogenic cell response to angiogenic stimuli. Arterioscler Thromb Vasc Biol. 2010;30:2212-2218. doi: 10.1161/ATVBAHA.110.211581.