Skip to main content
Erschienen in: Archives of Gynecology and Obstetrics 2/2018

25.06.2018 | Gynecologic Endocrinology and Reproductive Medicine

High-density lipoproteins (HDL) composition and function in preeclampsia

verfasst von: Yael Einbinder, Tal Biron-Shental, Moran Agassi-Zaitler, Keren Tzadikevitch-Geffen, Jacob Vaya, Soliman Khatib, Meital Ohana, Sydney Benchetrit, Tali Zitman-Gal

Erschienen in: Archives of Gynecology and Obstetrics | Ausgabe 2/2018

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To evaluate (a) the properties of high-density lipoproteins (HDL)/cholesterol, which include apolipoprotein A-1 (ApoA1) and paraoxonase1 (PON1), both are negative predictors of cardiovascular risk and (b) HDL function, among women with preeclampsia (PE). PE is a multi-system disorder, characterized by onset of hypertension and proteinuria or other end-organ dysfunction in the second half of pregnancy. Preeclampsia is associated with increased risk for later cardiovascular disease. The inverse association between HDL, cholesterol levels and the risk of developing atherosclerotic cardiovascular disease is well-established.

Methods

Twenty-five pregnant women [19 with PE and 6 with normal pregnancy (NP)] were recruited during admission for delivery. HDL was isolated from blood samples. PON1 activity and HDL were analyzed. An in vitro model of endothelial cells was used to evaluate the effect of HDL on the transcription response of vascular cell adhesion molecule-1 (VCAM-1) and endothelial nitric oxide synthase (eNOS) mRNA expression.

Results

PON1 activity (units/ml serum) was lower in the PE group compared to normal pregnancy (NP) (6.51 ± 0.73 vs. 9.98 ± 0.54; P = 0.015). Increased ApoA1 was released from PE-HDL as compared to NP-HDL (3.54 ± 0.72 vs. 0.89 ± 0.35; P = 0.01). PE-HDL exhibited increased VCAM-1 mRNA expression and decreased eNOS mRNA expression on TNF-α stimulated endothelial cells as compared to NP-HDL.

Conclusions

HDL from women with PE reduced PON1 activity and increased ApoA1 release from HDL particles. This process was associated with increased HDL diameter, suggesting impaired HDL anti-oxidant activity. These changes might contribute to higher long-term cardiovascular risks among women with PE.
Literatur
1.
Zurück zum Zitat Noris M, Perico N, Remuzzi G (2005) Mechanisms of disease: pre-eclampsia. Nat Clin Pract Nephrol 1:98–114CrossRefPubMed Noris M, Perico N, Remuzzi G (2005) Mechanisms of disease: pre-eclampsia. Nat Clin Pract Nephrol 1:98–114CrossRefPubMed
3.
4.
Zurück zum Zitat Scantlebury DC, Hayes SN (2014) How does preeclampsia predispose to future cardiovascular disease? Curr Hypertens Rep 16:472CrossRefPubMed Scantlebury DC, Hayes SN (2014) How does preeclampsia predispose to future cardiovascular disease? Curr Hypertens Rep 16:472CrossRefPubMed
5.
Zurück zum Zitat Kopecky C, Genser B, Drechsler C et al (2015) Quantification of HDL proteins, cardiac events, and mortality in patients with type 2 diabetes on hemodialysis. Clin J Am Soc Nephrol 10:224–231CrossRefPubMed Kopecky C, Genser B, Drechsler C et al (2015) Quantification of HDL proteins, cardiac events, and mortality in patients with type 2 diabetes on hemodialysis. Clin J Am Soc Nephrol 10:224–231CrossRefPubMed
6.
7.
Zurück zum Zitat Flavahan NA (1992) Atherosclerosis or lipoprotein-induced endothelial dysfunction. Potential mechanisms underlying reduction in EDRF/nitric oxide activity. Circulation 85:1927–1938CrossRefPubMed Flavahan NA (1992) Atherosclerosis or lipoprotein-induced endothelial dysfunction. Potential mechanisms underlying reduction in EDRF/nitric oxide activity. Circulation 85:1927–1938CrossRefPubMed
8.
Zurück zum Zitat Ray K, Wainwright NW, Visser L et al (2012) Changes in HDL cholesterol and cardiovascular outcomes after lipid modification therapy. Heart 98:780–785CrossRefPubMedPubMedCentral Ray K, Wainwright NW, Visser L et al (2012) Changes in HDL cholesterol and cardiovascular outcomes after lipid modification therapy. Heart 98:780–785CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Toth PP, Barter PJ, Rosenson RS et al (2013) High-density lipoproteins: a consensus statement from the National Lipid Association. J Clin Lipidol 7:484–525CrossRefPubMed Toth PP, Barter PJ, Rosenson RS et al (2013) High-density lipoproteins: a consensus statement from the National Lipid Association. J Clin Lipidol 7:484–525CrossRefPubMed
10.
Zurück zum Zitat Gansevoort RT, Correa-Rotter R, Hemmelgarn BR et al (2013) Chronic kidney disease and cardiovascular risk: epidemiology, mechanisms, and prevention. Lancet 382:339–352CrossRefPubMed Gansevoort RT, Correa-Rotter R, Hemmelgarn BR et al (2013) Chronic kidney disease and cardiovascular risk: epidemiology, mechanisms, and prevention. Lancet 382:339–352CrossRefPubMed
11.
Zurück zum Zitat Maynard SE, Min JY, Merchan J et al (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111:649–658CrossRefPubMedPubMedCentral Maynard SE, Min JY, Merchan J et al (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111:649–658CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Rich-Edwards JW, Fraser A, Lawlor DA, Catov JM (2014) Pregnancy characteristics and women’s future cardiovascular health: an underused opportunity to improve women’s health? Epidemiol Rev 36:57–70CrossRefPubMed Rich-Edwards JW, Fraser A, Lawlor DA, Catov JM (2014) Pregnancy characteristics and women’s future cardiovascular health: an underused opportunity to improve women’s health? Epidemiol Rev 36:57–70CrossRefPubMed
14.
Zurück zum Zitat Belo L, Caslake M, Gaffney D et al (2002) Changes in LDL size and HDL concentration in normal and preeclamptic pregnancies. Atherosclerosis 162:425–432CrossRefPubMed Belo L, Caslake M, Gaffney D et al (2002) Changes in LDL size and HDL concentration in normal and preeclamptic pregnancies. Atherosclerosis 162:425–432CrossRefPubMed
15.
Zurück zum Zitat Gbandjaba NY, Ghalim N, Hassar M et al (2012) Paraoxonase activity in healthy, diabetic, and hemodialysis patients. Clin Biochem 45:470–474CrossRefPubMed Gbandjaba NY, Ghalim N, Hassar M et al (2012) Paraoxonase activity in healthy, diabetic, and hemodialysis patients. Clin Biochem 45:470–474CrossRefPubMed
16.
Zurück zum Zitat Barter PJ, Nicholls S, Rye KA, Anantharamaiah GM, Navab M, Fogelman AM (2004) Antiinflammatory properties of HDL. Circ Res 95:764–772CrossRefPubMed Barter PJ, Nicholls S, Rye KA, Anantharamaiah GM, Navab M, Fogelman AM (2004) Antiinflammatory properties of HDL. Circ Res 95:764–772CrossRefPubMed
17.
Zurück zum Zitat Phillips JC, Wriggers W, Li Z, Jonas A, Schulten K (1997) Predicting the structure of apolipoprotein A-I in reconstituted high-density lipoprotein disks. Biophys J 73:2337–2346CrossRefPubMedPubMedCentral Phillips JC, Wriggers W, Li Z, Jonas A, Schulten K (1997) Predicting the structure of apolipoprotein A-I in reconstituted high-density lipoprotein disks. Biophys J 73:2337–2346CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Demir B, Demir S, Atamer Y et al (2011) Serum levels of lipids, lipoproteins and paraoxonase activity in pre-eclampsia. J Int Med Res 39:1427–1431CrossRefPubMed Demir B, Demir S, Atamer Y et al (2011) Serum levels of lipids, lipoproteins and paraoxonase activity in pre-eclampsia. J Int Med Res 39:1427–1431CrossRefPubMed
19.
Zurück zum Zitat Riwanto M, Landmesser U (2013) High density lipoproteins and endothelial functions: mechanistic insights and alterations in cardiovascular disease. J Lipid Res 54:3227–3243CrossRefPubMedPubMedCentral Riwanto M, Landmesser U (2013) High density lipoproteins and endothelial functions: mechanistic insights and alterations in cardiovascular disease. J Lipid Res 54:3227–3243CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Shroff R, Speer T, Colin S et al (2014) HDL in children with CKD promotes endothelial dysfunction and an abnormal vascular phenotype. J Am Soc Nephrol 25:2658–2668CrossRefPubMedPubMedCentral Shroff R, Speer T, Colin S et al (2014) HDL in children with CKD promotes endothelial dysfunction and an abnormal vascular phenotype. J Am Soc Nephrol 25:2658–2668CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Mackness MI, Durrington PN (1995) HDL, its enzymes and its potential to influence lipid peroxidation. Atherosclerosis 115:243–253CrossRefPubMed Mackness MI, Durrington PN (1995) HDL, its enzymes and its potential to influence lipid peroxidation. Atherosclerosis 115:243–253CrossRefPubMed
22.
Zurück zum Zitat Demirci O, Tugrul AS, Dolgun N, Sozen H, Eren S (2011) Serum lipids level assessed in early pregnancy and risk of pre-eclampsia. J Obstet Gynaecol Res 37:1427–1432CrossRefPubMed Demirci O, Tugrul AS, Dolgun N, Sozen H, Eren S (2011) Serum lipids level assessed in early pregnancy and risk of pre-eclampsia. J Obstet Gynaecol Res 37:1427–1432CrossRefPubMed
23.
Zurück zum Zitat Aviram M (1983) Plasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med 30:111–118CrossRefPubMed Aviram M (1983) Plasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med 30:111–118CrossRefPubMed
24.
Zurück zum Zitat Khersonsky O, Tawfik DS (2006) Chromogenic and fluorogenic assays for the lactonase activity of serum paraoxonases. Chem BioChem 7:49–53 Khersonsky O, Tawfik DS (2006) Chromogenic and fluorogenic assays for the lactonase activity of serum paraoxonases. Chem BioChem 7:49–53
25.
Zurück zum Zitat Rashid G, Benchetrit S, Fishman D, Bernheim J (2004) Effect of advanced glycation end-products on gene expression and synthesis of TNF-alpha and endothelial nitric oxide synthase by endothelial cells. Kidney Int 66:1099–1106CrossRefPubMed Rashid G, Benchetrit S, Fishman D, Bernheim J (2004) Effect of advanced glycation end-products on gene expression and synthesis of TNF-alpha and endothelial nitric oxide synthase by endothelial cells. Kidney Int 66:1099–1106CrossRefPubMed
26.
Zurück zum Zitat Gugliucci A, Caccavello R, Kotani K, Sakane N, Kimura S (2013) Enzymatic assessment of paraoxonase 1 activity on HDL subclasses: a practical zymogram method to assess HDL function. Clin Chim Acta 415:162–168CrossRefPubMed Gugliucci A, Caccavello R, Kotani K, Sakane N, Kimura S (2013) Enzymatic assessment of paraoxonase 1 activity on HDL subclasses: a practical zymogram method to assess HDL function. Clin Chim Acta 415:162–168CrossRefPubMed
27.
Zurück zum Zitat Cohen E, Aviram M, Khatib S, Volkova N, Vaya J (2016) Human carotid atherosclerotic plaque protein(s) change HDL protein(s) composition and impair HDL anti-oxidant activity. BioFactors 42:115–128PubMed Cohen E, Aviram M, Khatib S, Volkova N, Vaya J (2016) Human carotid atherosclerotic plaque protein(s) change HDL protein(s) composition and impair HDL anti-oxidant activity. BioFactors 42:115–128PubMed
28.
Zurück zum Zitat Zitman-Gal T, Golan E, Green J, Bernheim J, Benchetrit S (2012) Vitamin D receptor activation in a diabetic-like environment: potential role in the activity of the endothelial pro-inflammatory and thioredoxin pathways. J Steroid Biochem Mol Biol 132:1–7CrossRefPubMed Zitman-Gal T, Golan E, Green J, Bernheim J, Benchetrit S (2012) Vitamin D receptor activation in a diabetic-like environment: potential role in the activity of the endothelial pro-inflammatory and thioredoxin pathways. J Steroid Biochem Mol Biol 132:1–7CrossRefPubMed
29.
Zurück zum Zitat Einbinder Y, Ohana M, Benchetrit S et al (2016) Glucagon-like peptide-1 and vitamin D: anti-inflammatory response in diabetic kidney disease in db/db mice and in cultured endothelial cells. Diabetes Metab Res Rev 32:805–815CrossRefPubMed Einbinder Y, Ohana M, Benchetrit S et al (2016) Glucagon-like peptide-1 and vitamin D: anti-inflammatory response in diabetic kidney disease in db/db mice and in cultured endothelial cells. Diabetes Metab Res Rev 32:805–815CrossRefPubMed
30.
Zurück zum Zitat Luscher TF, Landmesser U, von Eckardstein A, Fogelman AM (2014) High-density lipoprotein: vascular protective effects, dysfunction, and potential as therapeutic target. Circ Res 114:171–182CrossRefPubMed Luscher TF, Landmesser U, von Eckardstein A, Fogelman AM (2014) High-density lipoprotein: vascular protective effects, dysfunction, and potential as therapeutic target. Circ Res 114:171–182CrossRefPubMed
31.
Zurück zum Zitat Feig JE, Hewing B, Smith JD, Hazen SL, Fisher EA (2014) High-density lipoprotein and atherosclerosis regression: evidence from preclinical and clinical studies. Circ Res 114:205–213CrossRefPubMedPubMedCentral Feig JE, Hewing B, Smith JD, Hazen SL, Fisher EA (2014) High-density lipoprotein and atherosclerosis regression: evidence from preclinical and clinical studies. Circ Res 114:205–213CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Hedrick CC, Castellani LW, Wong H, Lusis AJ (2001) In vivo interactions of apoA-II, apoA-I, and hepatic lipase contributing to HDL structure and antiatherogenic functions. J Lipid Res 42:563–570PubMed Hedrick CC, Castellani LW, Wong H, Lusis AJ (2001) In vivo interactions of apoA-II, apoA-I, and hepatic lipase contributing to HDL structure and antiatherogenic functions. J Lipid Res 42:563–570PubMed
33.
Zurück zum Zitat van der Steeg WA, Holme I, Boekholdt SM et al (2008) High-density lipoprotein cholesterol, high-density lipoprotein particle size, and apolipoprotein A-I: significance for cardiovascular risk: the IDEAL and EPIC-Norfolk studies. J Am Coll Cardiol 51:634–642CrossRefPubMed van der Steeg WA, Holme I, Boekholdt SM et al (2008) High-density lipoprotein cholesterol, high-density lipoprotein particle size, and apolipoprotein A-I: significance for cardiovascular risk: the IDEAL and EPIC-Norfolk studies. J Am Coll Cardiol 51:634–642CrossRefPubMed
34.
Zurück zum Zitat Regieli JJ, Jukema JW, Doevendans PA et al (2009) Paraoxonase variants relate to 10-year risk in coronary artery disease: impact of a high-density lipoprotein-bound antioxidant in secondary prevention. J Am Coll Cardiol 54:1238–1245CrossRefPubMed Regieli JJ, Jukema JW, Doevendans PA et al (2009) Paraoxonase variants relate to 10-year risk in coronary artery disease: impact of a high-density lipoprotein-bound antioxidant in secondary prevention. J Am Coll Cardiol 54:1238–1245CrossRefPubMed
35.
Zurück zum Zitat Bhattacharyya T, Nicholls SJ, Topol EJ et al (2008) Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk. JAMA 299:1265–1276CrossRefPubMed Bhattacharyya T, Nicholls SJ, Topol EJ et al (2008) Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk. JAMA 299:1265–1276CrossRefPubMed
36.
Zurück zum Zitat Shih DM, Gu L, Xia YR et al (1998) Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 394:284–287CrossRefPubMed Shih DM, Gu L, Xia YR et al (1998) Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 394:284–287CrossRefPubMed
37.
Zurück zum Zitat Genc H, Uzun H, Benian A et al (2011) Evaluation of oxidative stress markers in first trimester for assessment of preeclampsia risk. Arch Gynecol Obstet 284:1367–1373CrossRefPubMed Genc H, Uzun H, Benian A et al (2011) Evaluation of oxidative stress markers in first trimester for assessment of preeclampsia risk. Arch Gynecol Obstet 284:1367–1373CrossRefPubMed
38.
Zurück zum Zitat Uzun H, Benian A, Madazli R, Topcuoglu MA, Aydin S, Albayrak M (2005) Circulating oxidized low-density lipoprotein and paraoxonase activity in preeclampsia. Gynecol Obstet Invest 60:195–200CrossRefPubMed Uzun H, Benian A, Madazli R, Topcuoglu MA, Aydin S, Albayrak M (2005) Circulating oxidized low-density lipoprotein and paraoxonase activity in preeclampsia. Gynecol Obstet Invest 60:195–200CrossRefPubMed
39.
Zurück zum Zitat Hubel CA, McLaughlin MK, Evans RW, Hauth BA, Sims CJ, Roberts JM (1996) Fasting serum triglycerides, free fatty acids, and malondialdehyde are increased in preeclampsia, are positively correlated, and decrease within 48 hours post partum. Am J Obstet Gynecol 174:975–982CrossRefPubMed Hubel CA, McLaughlin MK, Evans RW, Hauth BA, Sims CJ, Roberts JM (1996) Fasting serum triglycerides, free fatty acids, and malondialdehyde are increased in preeclampsia, are positively correlated, and decrease within 48 hours post partum. Am J Obstet Gynecol 174:975–982CrossRefPubMed
40.
Zurück zum Zitat Rosing U, Samsioe G, Olund A, Johansson B, Kallner A (1989) Serum levels of apolipoprotein A-I, A-II and HDL-cholesterol in second half of normal pregnancy and in pregnancy complicated by pre-eclampsia. Horm Metab Res 21:376–382CrossRefPubMed Rosing U, Samsioe G, Olund A, Johansson B, Kallner A (1989) Serum levels of apolipoprotein A-I, A-II and HDL-cholesterol in second half of normal pregnancy and in pregnancy complicated by pre-eclampsia. Horm Metab Res 21:376–382CrossRefPubMed
41.
Zurück zum Zitat Ramet ME, Ramet M, Lu Q et al (2003) High-density lipoprotein increases the abundance of eNOS protein in human vascular endothelial cells by increasing its half-life. J Am Coll Cardiol 41:2288–2297CrossRefPubMed Ramet ME, Ramet M, Lu Q et al (2003) High-density lipoprotein increases the abundance of eNOS protein in human vascular endothelial cells by increasing its half-life. J Am Coll Cardiol 41:2288–2297CrossRefPubMed
42.
Zurück zum Zitat Tai SC, Robb GB, Marsden PA (2004) Endothelial nitric oxide synthase: a new paradigm for gene regulation in the injured blood vessel. Arterioscler Thromb Vasc Biol 24:405–412CrossRefPubMed Tai SC, Robb GB, Marsden PA (2004) Endothelial nitric oxide synthase: a new paradigm for gene regulation in the injured blood vessel. Arterioscler Thromb Vasc Biol 24:405–412CrossRefPubMed
44.
Zurück zum Zitat Kaseda R, Jabs K, Hunley TE et al (2015) Dysfunctional high-density lipoproteins in children with chronic kidney disease. Metabolism 64:263–273CrossRefPubMed Kaseda R, Jabs K, Hunley TE et al (2015) Dysfunctional high-density lipoproteins in children with chronic kidney disease. Metabolism 64:263–273CrossRefPubMed
45.
Zurück zum Zitat Ortiz-Munoz G, Couret D, Lapergue B et al (2016) Dysfunctional HDL in acute stroke. Atherosclerosis 253:75–80CrossRefPubMed Ortiz-Munoz G, Couret D, Lapergue B et al (2016) Dysfunctional HDL in acute stroke. Atherosclerosis 253:75–80CrossRefPubMed
46.
Zurück zum Zitat Szarka A, Rigo J Jr, Lazar L, Beko G, Molvarec A (2010) Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol 11:59CrossRefPubMedPubMedCentral Szarka A, Rigo J Jr, Lazar L, Beko G, Molvarec A (2010) Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol 11:59CrossRefPubMedPubMedCentral
47.
Zurück zum Zitat Fainaru O, Lichtenberg D, Pinchuk I, Almog B, Gamzu R, Kupferminc M (2003) Preeclampsia is associated with increased susceptibility of serum lipids to copper-induced peroxidation in vitro. Acta Obstet Gynecol Scand 82:711–715CrossRefPubMed Fainaru O, Lichtenberg D, Pinchuk I, Almog B, Gamzu R, Kupferminc M (2003) Preeclampsia is associated with increased susceptibility of serum lipids to copper-induced peroxidation in vitro. Acta Obstet Gynecol Scand 82:711–715CrossRefPubMed
48.
Zurück zum Zitat Wakatsuki A, Ikenoue N, Okatani Y, Shinohara K, Fukaya T (2000) Lipoprotein particles in preeclampsia: susceptibility to oxidative modification. Obstet Gynecol 96:55–59PubMed Wakatsuki A, Ikenoue N, Okatani Y, Shinohara K, Fukaya T (2000) Lipoprotein particles in preeclampsia: susceptibility to oxidative modification. Obstet Gynecol 96:55–59PubMed
49.
Zurück zum Zitat Sarandol E, Safak O, Dirican M, Uncu G (2004) Oxidizability of apolipoprotein B-containing lipoproteins and serum paraoxonase/arylesterase activities in preeclampsia. Clin Biochem 37:990–996CrossRefPubMed Sarandol E, Safak O, Dirican M, Uncu G (2004) Oxidizability of apolipoprotein B-containing lipoproteins and serum paraoxonase/arylesterase activities in preeclampsia. Clin Biochem 37:990–996CrossRefPubMed
Metadaten
Titel
High-density lipoproteins (HDL) composition and function in preeclampsia
verfasst von
Yael Einbinder
Tal Biron-Shental
Moran Agassi-Zaitler
Keren Tzadikevitch-Geffen
Jacob Vaya
Soliman Khatib
Meital Ohana
Sydney Benchetrit
Tali Zitman-Gal
Publikationsdatum
25.06.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Archives of Gynecology and Obstetrics / Ausgabe 2/2018
Print ISSN: 0932-0067
Elektronische ISSN: 1432-0711
DOI
https://doi.org/10.1007/s00404-018-4824-3

Weitere Artikel der Ausgabe 2/2018

Archives of Gynecology and Obstetrics 2/2018 Zur Ausgabe

Update Gynäkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.