Maternal hypercholesterolemia in pregnancy associates with umbilical vein endothelial dysfunction: Role of endothelial nitric oxide synthase and arginase II

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 10, 2013, Pages 2444-2453

  Leiva, Andrea ^a   De Medina, Camila Diez ^a   Salsoso, Rocío ^a   Sáez, Tamara ^a   San Martín, Sebastián ^b   Abarzúa, Fernando ^a,c   Farías, Marcelo ^a   Guzmán Gutiérrez, Enrique ^a   Pardo, Fabián ^a   Sobrevia, Luis ^a,d  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD DE VALPARAÍSO   (Chile)

^c UNIVERSIDAD DEL DESARROLLO   (Chile)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

arginase; cholesterol; endothelium; nitric oxide; pregnancy

Indexed keywords

AMINO ACID TRANSPORTER; ARGINASE; ARGINASE 2; ARGININE; CALCITONIN; CHOLESTEROL; CITRULLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; UNCLASSIFIED DRUG; UREA;

ADULT; ARTICLE; BLOOD VESSEL REACTIVITY; CHOLESTEROL BLOOD LEVEL; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; FEMALE; HISTOCHEMISTRY; HUMAN; HYPERCHOLESTEROLEMIA; LIPID BLOOD LEVEL; LIPOPROTEIN BLOOD LEVEL; MAJOR CLINICAL STUDY; MATERNAL SUPRAPHYSIOLOGICAL HYPERCHOLESTEROLEMIA; PREGNANCY DISORDER; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UMBILICAL VEIN; UMBILICAL VEIN ENDOTHELIAL CELL;

ARGINASE; CHOLESTEROL; ENDOTHELIUM; NITRIC OXIDE; PREGNANCY;

ADULT; ARGINASE; CATIONIC AMINO ACID TRANSPORTER 1; CATIONIC AMINO ACID TRANSPORTER 2; CELLS, CULTURED; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPERCHOLESTEROLEMIA; KINETICS; LIPIDS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY TRIMESTERS; SIGNAL TRANSDUCTION; UMBILICAL VEINS; UREA; YOUNG ADULT;

EID: 84885085350     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301987     Document Type: Article

References (47)

1. Herrera E, Amusquivar E, López-Soldado I, Ortega H. Maternal lipid metabolism and placental lipid transfer. Horm Res. 2006;65(suppl 3):59-64
2. Basaran A. Pregnancy-induced hyperlipoproteinemia: Review of the literature. Reprod Sci. 2009;16:431-437
3. Montes A, Walden CE, Knopp RH, Cheung M, Chapman MB, Albers JJ. Physiologic and supraphysiologic increases in lipoprotein lipids and apoproteins in late pregnancy and postpartum. Possible markers for the diagnosis of ;prelipemia;. Arteriosclerosis. 1984;4:407-417
4. Leiva A, Pardo F, Ramírez MA, Farías M, Casanello P, Sobrevia L. Fetoplacental vascular endothelial dysfunction as an early phenomenon in the programming of human adult diseases in subjects born from gestational diabetes mellitus or obesity in pregnancy. Exp Diabetes Res. 2011;2011:349286
5. Napoli C, D'Armiento FP, Mancini FP, Postiglione A, Witztum JL, Palumbo G, Palinski W. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J Clin Invest. 1997; 100:2680-2690
6. Leiva A, Diez de Medina A, Guzmán-Gutiérrez E, Pardo F, Sobrevia L. Maternal hypercholesterolemia in gestational diabetes and the association with placental endothelial dysfunction. In: Sobrevia L, ed. Gestational Diabetes-Causes, Diagnosis and Treatment. Rijeka, Croatia: InTech; 2013:103-134
7. Stefulj J, Panzenboeck U, Becker T, Hirschmugl B, Schweinzer C, Lang I, Marsche G, Sadjak A, Lang U, Desoye G, Wadsack C. Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ Res. 2009;104:600-608
8. Napoli C, Ignarro LJ. Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch Pharm Res. 2009;32:1103-1108
9. Drexler H, Zeiher AM, Meinzer K, Just H. Correction of endothelial dysfunction in coronary microcirculation of hypercholesterolaemic patients by L-Arginine. Lancet. 1991;338:1546-1550
10. Speake PF, Glazier JD, Ayuk PT, Reade M, Sibley CP, D'Souza SW. L-Arginine transport across the basal plasma membrane of the syncytiotrophoblast of the human placenta from normal and preeclamptic pregnancies. J Clin Endocrinol Metab. 2003;88:4287-4292
11. da Costa BP, Steibel JP, Antonello IC, Guimarães JA, Poli de Figueiredo CE. L-Arginine erythrocyte transport in normal pregnant and preeclamptic women. Am J Obstet Gynecol. 2004;190:468-471
12. Topal G, Topal JL, Brunet A, Walch L, Boucher JL, David-Dufilho M. Mitochondrial arginase II modulates nitric-oxide synthesis through nonfreely exchangeable L-Arginine pools in human endothelial cells. J Pharmacol Exp Ther. 2006;318:1368-1374
13. Mann GE, Yudilevich DL, Sobrevia L. Regulation of amino acid and glucose transporters in endothelial and smooth muscle cells. Physiol Rev. 2003;83:183-252
14. Closs EI, Simon A, Vékony N, Rotmann A. Plasma membrane transporters for arginine. J Nutr. 2004;134(10 suppl):2752S-2759S; discussion 2765S.
15. Casanello P, Sobrevia L. Intrauterine growth retardation is associated with reduced activity and expression of the cationic amino acid transport systems y+/hCAT-1 and y+/hCAT-2B and lower activity of nitric oxide synthase in human umbilical vein endothelial cells. Circ Res. 2002;91:127-134
16. Guzmán-Gutiérrez E, Westermeier F, Salomón C, González M, Pardo F, Leiva A, Sobrevia L. Insulin-increased L-Arginine transport requires A(2A) adenosine receptors activation in human umbilical vein endothelium. PLoS One. 2012;7:e41705
17. Vásquez G, Sanhueza F, Vásquez R, González M, San Martín R, Casanello P, Sobrevia L. Role of adenosine transport in gestational diabetes-induced L-Arginine transport and nitric oxide synthesis in human umbilical vein endothelium. J Physiol. 2004;560(pt 1):111-122
18. Kiserud T, Acharya G. The fetal circulation. Prenat Diagn. 2004;24:1049-1059
19. Ryoo S, Lemmon CA, Soucy KG, Gupta G, White AR, Nyhan D, Shoukas A, Romer LH, Berkowitz DE. Oxidized low-density lipoprotein-dependent endothelial arginase II activation contributes to impaired nitric oxide signaling. Circ Res. 2006;99:951-960
20. Ryoo S, Gupta G, Benjo A, et al. Endothelial arginase II: A novel target for the treatment of atherosclerosis. Circ Res. 2008;102:923-932
21. Morris SM Jr. Arginases and arginine deficiency syndromes. Curr Opin Clin Nutr Metab Care. 2012;15:64-70
22. Holowatz LA, Santhanam L, Webb A, Berkowitz DE, Kenney WL. Oral atorvastatin therapy restores cutaneous microvascular function by decreasing arginase activity in hypercholesterolaemic humans. J Physiol. 2011;589(pt 8):2093-2103
23. Davignon J, Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation.2004;109:27-32
24. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499-502
25. National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III) final report. Circulation. 2002;106:3143-3421
26. Milcheva R, Janega P, Celec P, Russev R, Babál P. Alcohol based fixatives provide excellent tissue morphology, protein immunoreactivity and RNA integrity in paraffin embedded tissue specimens. Acta Histochem. 2013;115:279-289
27. Kiernan JA. Alkaline phosphatase method for use with resinous mounting media. Biotech Histochem. 2005;80:43-45
28. Dong YL, Vegiraju S, Chauhan M, Gangula PR, Hankins GD, Goodrum L, Yallampalli C. Involvement of calcitonin gene-related peptide in control of human fetoplacental vascular tone. Am J Physiol Heart Circ Physiol. 2004;286:H230-H239
29. Prieto CP, Krause BJ, Quezada C, San Martin R, Sobrevia L, Casanello P. Hypoxia-reduced nitric oxide synthase activity is partially explained by higher arginase-2 activity and cellular redistribution in human umbilical vein endothelium. Placenta. 2011;32:932-940
30. González M, Gallardo V, Rodríguez N, Salomón C, Westermeier F, Guzmán-Gutiérrez E, Abarzúa F, Leiva A, Casanello P, Sobrevia L. Insulin-stimulated L-Arginine transport requires SLC7A1 gene expression and is associated with human umbilical vein relaxation. J Cell Physiol. 2011;226:2916-2924
31. Liguori A, D'Armiento FP, Palagiano A, Balestrieri ML, Williams-Ignarro S, De Nigris F, Lerman LO, D'Amora M, Rienzo M, Fiorito C, Ignarro LJ, Palinski W, Napoli C. Effect of gestational hypercholesterolaemia on omental vasoreactivity, placental enzyme activity and transplacental passage of normal and oxidised fatty acids. BJOG. 2007;114:1547-1556
32. Napoli C, Glass CK, Witztum JL, Deutsch R, D'Armiento FP, Palinski W. Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet. 1999;354:1234-1241
33. Marseille-Tremblay C, Ethier-Chiasson M, Forest JC, Giguère Y, Masse A, Mounier C, Lafond J. Impact of maternal circulating cholesterol and gestational diabetes mellitus on lipid metabolism in human term placenta. Mol Reprod Dev. 2008;75:1054-1062
34. Ethier-Chiasson M, Duchesne A, Forest JC, Giguère Y, Masse A, Mounier C, Lafond J. Influence of maternal lipid profile on placental protein expression of LDLr and SR-BI. Biochem Biophys Res Commun. 2007;359:8-14
35. Pernow J. Actions of constrictor (NPY and endothelin) and dilator (substance P, CGRP and VIP) peptides on pig splenic and human skeletal muscle arteries: Involvement of the endothelium. Br J Pharmacol. 1989;97:983-989
36. Hovingh GK, Brownlie A, Bisoendial RJ, Dube MP, Levels JH, Petersen W, Dullaart RP, Stroes ES, Zwinderman AH, De Groot E, Hayden MR, Kuivenhoven JA, Kastelein JJ. A novel apoA-I mutation (L178p) leads to endothelial dysfunction, increased arterial wall thickness, and premature coronary artery disease. J Am Coll Cardiol. 2004;44:1429-1435
37. Krotova K, Patel JM, Block ER, Zharikov S. Endothelial arginase II responds to pharmacological inhibition by elevation in protein level. Mol Cell Biochem. 2010;343:211-216
38. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 1999;399:601-605
39. Fleming I, Fisslthaler B, Dimmeler S, Kemp BE, Busse R. Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res. 2001;88:E68-E75
40. Simon A, Plies L, Habermeier A, Martiné U, Reining M, Closs EI. Role of neutral amino acid transport and protein breakdown for substrate supply of nitric oxide synthase in human endothelial cells. Circ Res. 2003;93: 813-820
41. Wu G, Pond WG, Ott T, Bazer FW. Maternal dietary protein deficiency decreases amino acid concentrations in fetal plasma and allantoic fluid of pigs. J Nutr. 1998;128:894-902
42. Li H, Meininger CJ, Hawker JR Jr, Haynes TE, Kepka-Lenhart D, Mistry SK, Morris SM Jr, Wu G. Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells. Am J Physiol Endocrinol Metab. 2001;280:E75-E82
43. San Martín R, Sobrevia L. Gestational diabetes and the adenosine/L-Arginine/ nitric oxide (ALANO) pathway in human umbilical vein endothelium. Placenta. 2006;27:1-10
44. Hardy TA, May JM. Coordinate regulation of L-Arginine uptake and nitric oxide synthase activity in cultured endothelial cells. Free Radic Biol Med. 2002;32:122-131
45. Wu G, Morris SM Jr. Arginine metabolism: Nitric oxide and beyond. Biochem J. 1998;336(pt 1):1-17
46. Andersen MR, Simonsen U, Uldbjerg N, Aalkjaer C, Stender S. Smoking cessation early in pregnancy and birth weight, length, head circumference, and endothelial nitric oxide synthase activity in umbilical and chorionic vessels: An observational study of healthy singleton pregnancies. Circulation. 2009;119:857-864
47. Saarelainen H, Valtonen P, Punnonen K, Laitinen T, Raitakari OT, Juonala M, Heiskanen N, Lyyra-Laitinen T, Viikari JS, Vanninen E, Heinonen S. Subtle changes in ADMA and l-Arginine concentrations in normal pregnancies are unlikely to account for pregnancy-related increased flowmediated dilatation. Clin Physiol Funct Imaging. 2008;28:120-124