Dyslipidemia, iron, and oxidative stress in preeclampsia: Assessment of maternal and feto-placental interactions

Seminars in Reproductive Endocrinology

Volumn 16, Issue 1, 1998, Pages 75-92

  Hubel, Carl A ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Iron kinetics; Maternal dyslipidemia; Oxidative stress; Preeclampsia

Indexed keywords

ANTIOXIDANT; ASCORBIC ACID; CERULOPLASMIN; FREE RADICAL; IRON; LIPID PEROXIDE; LOW DENSITY LIPOPROTEIN; PHOSPHOLIPID ANTIBODY; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TRANSFERRIN; TUMOR NECROSIS FACTOR ALPHA; XANTHINE OXIDASE;

DYSLIPIDEMIA; HUMAN; IRON KINETICS; LIPID PEROXIDATION; MOTHER FETUS RELATIONSHIP; OXIDATIVE STRESS; PLACENTA; POSITIVE FEEDBACK; PREECLAMPSIA; PRIORITY JOURNAL; REVIEW; VASCULAR ENDOTHELIUM;

EID: 0031750153     PISSN: 07348630     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2007-1016255     Document Type: Review

References (233)

1. Knock GA, Poston L. Bradykinin-mediated relaxation of isolated maternal resistance arteries in normal pregnancy and preeclampsia. Am J Obstet Gynecol 1996;175:1668-1674
2. Roberts JM, Taylor RN, Goldfien A. Endothelial cell activation as a pathogenetic factor in preeclampsia. Seminars Perinatol 1991;15:86-93
3. Roberts JM, Taylor RN, Goldfien A. Clinical and biochemical evidence of endothelial cell dysfunction in the pregnancy syndrome preeclampsia. Am J Hypertens 1991;4:700-708
4. deGroot CJM, Taylor RN. New insights into the etiology of pre-eclampsia. Ann Med 1993;25:243-249
5. Lorentzen B, Endresen MJ, Hovig T, Haug E, Henriksen T. Sera from preeclamptic women increase the content of triglycerides and reduce the release of prostacyclin in cultured endothelial cells. Thromb Res 1991;63:363-372
6. Davidge ST, Signorella AP, Hubel CA, Lykins DL, Roberts JM. Distinct factors in plasma of preeclamptic women increase endothelial nitric oxide or prostacyclin. Hypertension 1996;28:758-764
7. Taylor RN, Casal DC, Jones LA, Varma M, Martin JN, Roberts JM. Selective effects of preeclamptic sera on human endothelial cell procoagulant protein expression. Am J Obstet Gynecol 1991;165:1705-1710
8. Taylor RN, Musci TJ, Rodgers GM, Roberts JM. Preeclamptic sera stimulate increased platelet-derived growth factor mRNA and protein expression by cultured human endothelial cells. Am J Reprod Immunol 1991;25:105-108
9. Cross JC. Trophoblast function in normal and preeclamptic pregnancy. Fetal Maternal Med Rev 1996;8:57-66
10. Friedman SA, Taylor RN, Roberts JM. Pathophysiology of preeclampsia. Clin Perinatol 1991;18:661-682
11. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK. Preeclampsia: An endothelial cell disorder. Am J Obstet Gynecol 1990;163:1365-1366
12. Hubel C. Oxidative stress and preeclampsia. Fetal Maternal Med Rev 1997;9:73-101
13. Murai J, Muzykanskiy E, Taylor R. Maternal and fetal modulators of lipid metabolism correlate with the development of preeclampsia. Metabolism 1997;46:963-967
14. Ness RB, Roberts JM. Heterogeneous causes constituting the single syndrome of preeclampsia: A hypothesis and its implications. Am J Obstet Gynecol 1996;175:1365-1370
15. Sattar N, Gaw A, Packard CJ, Greer IA. Potential pathogenic roles of aberrant lipoprotein and fatty acid metabolism in pre-eclampsia. Br J Obstet Gynaecol 1996;103:614-620
16. Hubel CA, Roberts JM, Taylor RN, Musci TJ, Rogers GM, McLaughlin MK. Lipid peroxidation in pregnancy: New perspectives on preeclampsia. Am J Obstet Gynecol 1989;161:1025-1034
17. Walsh SC. Lipid peroxidation in pregnancy. Hypertens Pregnancy 1994;13:1-25
18. Zeeman GG, Dekker GA. Pathogenesis of preeclampsia: A hypothesis. Clin Obstet Gynecol 1992;35:317-337
19. Hubel CA, McLaughlin MK, Evans RW, Hauth BA, Sims CJ, Roberts JM. 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 1996;174:975-982
20. Lorentzen B, Drevon CA, Endressen MJ, Henriksen T. Fatty acid pattern of esterfied and free fatty acids in sera of women with normal and pre-eclamptic pregnancy. Br J Obstet Gynaecol 1995;102:530-537
21. Kaaja R, Tikkanen MJ, Viinikka L, Ylikorkala O. Serum lipoproteins, insulin, and urinary prostanoid metabolites in normal and hypertensive pregnant women. Obstet Gynecol 1995;85:353-356
22. Halliwell B, Gutteridge JMC, Cross CE. Free radicals, antioxidants, and human disease: Where are we now? J Lab Clin Med 1992;119:598-620
23. Halliwell B. The biochemistry of oxygen free radicals. In: Aruoma O (ed). Free radicals in tropical diseases. Chur, Switzerland: Harwood Academic Publishers, 1993:1-12
24. Buettner GR. The pecking order of free radicals and antioxidants: Lipid peroxidation, α-toxopherol, and ascorbate. Arch Biochem Biophys 1993;300:535-543
25. Sen CK, Packer L. Antioxidant and redox regulation of gene transcription. FASEB J 1996;10:709-720
26. Gutteridge JMC. Invited review free radicals in disease processes: A compilation of cause and consequence. Free Radic Res Comm 1993;19:141-58
27. Halliwell B. The role of oxygen radicals in human disease, with particular reference to the vascular system. Haemostasis 1993;23:118-126
28. Halliwell B. Free radicals, antioxidants, and human disease: Curiosity, cause, or consequence? Lancet 1994;344:721-724
29. Kirschner RE, Fantini GA. Role of iron and oxygen-derived free radicals in ischemia-reperfusion injury. J Am Coll Surg 1994;179:103-117
30. Omar B, McCord J, Downey J. Ischaemia-reperfusion. In: Sies H (ed). Oxidative stress: Oxidants and antioxidants. New York: Academic Press, 1991:493-527
31. Sussman MS, Bulkley GB. Oxygen-derived free radical in reperfusion injury. In: Packer L (ed). Methods in enzymology. San Diego: Academic Press, 1990:711-723
32. Bulkley GB. Reactive oxygen metabolites and reperfusion injury: Aberrant triggering of reticuloendothelial function. Lancet 1994;344:934-936
33. Halliwell B, Chirico S. Lipid peroxidation: Its mechanism, measurement, and significance. Am J Clin Nutr 1993;57:715S-725S
34. Wardman P, Candeias LP. Fenton chemistry: An introduction. Radiat Res 1996;145:523-531
35. Halliwell B. Reactive oxygen species in living systems: Source, biochemistry, and role in human disease. Am J Med 1991;91:14S-22S
36. Smith WL, Marnett LJ, DeWitt DL. Prostaglandin and thromboxane biosynthesis. Pharmac Ther 1991;49:153-179
37. Ursini F, Maiorino M, Gregolin C. The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim Biophys Acta 1985;839:62-70
38. Oury T, Day B, Crapo J. Extracellular Superoxide dismutase in vessels and airway of humans and baboons. Free Radic Biol Med 1996;20:957-965
39. Halliwell B, Gutteridge JMC. The antioxidants of human extracellular fluids. Arch Biochem Biophys 1990;280:1-8
40. Gutteridge JM, Smith A. Antioxidant protection by haemopexin of haem-stimulated lipid peroxidation. Biochem J 1988;256:861-865
41. Gutteridge JMC. The antioxidant activity of haptoglobin towards haemoglobin-stimulated lipid peroxidation. Biochim Biophys Acta 1987;917:219-223
42. Balla G, Jacob HS, Balla J, et al. Ferritin: A cytoprotective antioxidant strategem of endothelium. J Biol Chem 1992;267:18148-18153
43. Gutteridge JMC, Paterson SK, Segal AW, Halliwell B. Inhibition of lipid peroxidation by the iron-bindng protein lactoferrin. Biochem J 1981;199:259-261
44. Halliwell B, Gutteridge JMC. The antioxidants of human extracellular fluids. Arch Biochem Biophys 1990;280:1-8
45. Gutteridge JMC, Quintan GJ. Antioxidant protection against organic and inorganic oxygen radicals by normal human plasma: The important primary role for iron-binding and iron-oxidising proteins. Biochim Biophys Acta 1993;1156:144-150
46. Cranfield LM, Gollan JL, White AG, Dormandy TL. Serum antioxidant activity in normal and abnormal subjects. Ann Clin Biochem 1979;16:299-306
47. Aisen P. The binding and release of iron by transferrin. Birth Defects: Original Article Series 1976;12:81-95
48. Halliwell B, Gutteridge JM. Role of free radicals and catalytic metal ions in human disease: An overview. In: Packer L, Glazer AN (eds). Oxygen radicals in biological systems. San Diego: Academic Press, 1990:1-83
49. Halliwell B. Vitamin C : Antioxidant or pro-oxidant in vivo ? Free Radic Res 1996;25:439-454
50. Pepper JR, Mumby S, Gutteridge JMC. Sequential oxidative damage, and changes in iron-binding and iron-oxidising plasma antioxidants during cardiopulmonary bypass surgery. Free Radic Res 1994;21:377-385
51. Berger HM, Mumby S, Gutteridge JMC. Ferrous ions detected in iron-overloaded cord blood plasma from preterm and term babies: Implications for oxidative stress. Free Radic Res 1994;22:555-559
52. Hubel CA, Kozlov AV, Evans RW, Davidge ST, McLaughlin MK, Roberts JM. Decreased transferrin and increased transferrin saturation in sera of women with preeclampsia: Implications for oxidative stress. Am J Obstet Gynecol 1996;175:692-700
53. Harlan JM. Neutrophil-mediated vascular injury. Acta Med Scand 1987;715:123-129
54. Gorog P, Kovacs IB. Lipid peroxidation by activated platelets: A possible link between thrombosis and atherogenesis. Atherosclerosis 1995;115:121-128
55. Aviram M. LDL-platelet interaction under oxidative stress induces macrophage foam cell formation. Throb Haemostas 1995;74:560-564
56. Stewart DJ, Monge JC. Hyperlipidemia and endothelial dysfunction. Curr Opin Lipidol 1993;4:319-324
57. Endresen MJR. Preeclampsia and endothelial cell function. Acta Obstet Gynecol Scand 1995;74:667-669
58. Witztum JL. The oxidation hypothesis of atherosclerosis. Lancet 1994;344:793-795
59. Chisolm GM, Irwin KC, Penn MS. Lipoprotein oxidation and lipoprotein-induced cell injury in diabetes. Diabetes 1992;41:61-66
60. Berliner JA, Heinecke JA. The role of oxidized lipoproteins in atherogenesis. Free Radic Biol Med 1996;20:707-727
61. Steinberg D, Parthasarathy S, Carew T, Khoo J, Witztum JL. Beyond cholesterol: Modifications of low-density lipoprotein that increase its atheogenicity. N Engl J Med 1989;320:915-24
62. Yla-Herttuala S, Palinski W, Rosenfeld ME, et al. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest 1989;84:1086-1095
63. Dabbagh AJ, Frei B. Human suction blister interstitial fluid prevents metal ion-dependent oxidation of low density lipoprotein by macrophages and in cell-free systems. J Clin Invest 1995;96:1958-1966
64. Hubel CA, Griggs KC, McLaughlin MK. Lipid peroxidation and altered vascular function in vitamin E-deficient rats. Am J Physiol 1989;256:H1539-H1545
65. Cox DA, Cohen ML. Influence of gender on vasomotor effects of oxidized low-density lipoprotein in porcine coronary arteries. Am J Physiol 1997;272:H2577-H2583
66. Cox D, Cohen M. Effects of oxidized low-density lipoprotein on vascular contraction and relaxation: Clinical and pharmacological implications in atherosclerosis. Pharmacol Rev 1996;48:3-19
67. Janero DR. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 1990;9:515-540
68. Pryor WA, Godber SS. Noninvasive measures of oxidative stress status in humans. Free Radic Biol Med 1991;10:177-184
69. Puhl H, Waeg G, Esterbauer H. Methods to determine oxidation of low-density lipoproteins. In: Packer L (ed). Methods in enzymology. San Diego: Academic Press, 1994:425-441
70. Zhou Y, Damsky CH, Fisher SJ. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. J Clin Invest 1997;99:2152-2164
71. Lunell NO, Lewander R, Mamoun I, Nylund L, Sarby S, Thornstrom S. Uteroplacental blood flow in pregnancy induced hypertension. Scand J Clin Lab Invest 1984;44:28-35
72. Trudinger BJ, Giles WD, Cook CM, Bombarderi J, Collins L. Fetal umbilical artery flow velocity waveforms and placental resistance: Clinical significance. Br J Obstet Gynaecol 1985;92:23-30
73. Redman CWG. Current topic: Pre-eclampsia and the placenta. Placenta 1991;12:301-308
74. Wigglesworth JS. Morphologic variations in the insufficient placenta. J Obstet Gynecol Brit Commonw 1964;71:871-884
75. Tominaga T, Page EW. Accommodation of the human placenta to hypoxia. Am J Obstet Gynecol 1966;94:679-685
76. Zamudio S, Palmer SK, Regensteiner JG, Moore LG. High altitude and hypertension during pregnancy. Am J Human Biol 1995;7:183-193
77. Beckman JS, Koppenol WH. Nitric oxide, Superoxide, and peroxynitrite: The good, the bad, and the ugly. Am J Physiol 1996;271:C1424-C1437
78. Goda N, Suematsu M, Mukai M, et al. Modulation of mitochondrion-mediated oxidative stress by nitric oxide in human placental trophoblastic cells. Am J Physiol 1996;271:H1893-H1899
79. Rubbo H, Radi R, Trujillo M, et al. Nitric oxide regulation of Superoxide and peroxynitrite-dependent lipid peroxidation. J Biol Chem 1994;269:26066-26075
80. Beckmann JS, Ye YZ, Anderson PG, et al. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol Chem Hoppe-Seyler 1994;375:81-88
81. Kooy NW, Royall JA, Ye YZ, Kelly DR, Beckman JS. Evidence for in vivo peroxynitrite production in human acute lung injury. Am J Respir Crit Car Med 1995;151:1250-1254
82. Myatt L, Rosenfield RB, Eis ALW, Brockman DE, Greer I, Lyall F. Nitrotyrosine residues in placenta: Evidence of peroxynitrite formation and action. Hypertension 1996;28:488-493
83. Kimura E, Kosaka H, Shiga T, Yoshimine T, Hayakawa T. Elevation of plasma nitric oxide end products during focal cerebral ischemia and reperfusion in the rat. J Cereb Blood Flow Metab 1994;14:487-491
84. Kooy NW, Royall JA. Agonist-induced peroxynitrite production from endothelial cells. Arch Biochem Biophys 1994;310:352-359
85. Carreras MC, Pargament GA, Catz SD, Poderoso JJ, Boveris A. Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxynitrite during the respiratory burst of human neutrophils. FEBS Lett 1994;341:65-68
86. Halliwell B. What nitrates tyrosine? Is nitrotyrosine specific as a biomarker of peroxynitrite formation in vivo? FEBS Lett 1997;411:175-160
87. Many A, Hubel CA, Roberts JM. Hyperuricemia and xanthine oxidase in prceclampsia revisited. Am J Obstet Gynecol 1996;174:288-291
88. Bulkley GB. Endothelial xanthine oxidase: A radical transducer of inflammatory signals for reticuloendothelial activation. Br J Surg 1993;80:684-686
89. Hayashi T, Baldridge R, Olmsted P, Kimmel D. Purine nucleotide catabolism in placenta. Am J Obstet Gynecol 1964;88:470-478
90. Many A, Westerhausen-Larson A, Kanbour-Shakir A, Roberts JM. Xanthine oxidase/dehydrogenase is present in human placenta. Placenta 1996;17:361-365
91. Many A, Friedman SA, Hubel CA, Roberts JM. Xanthine oxidase activity in preeclamptic women is higher in invasive but not villous trophoblast. J Soc Gynecol Invest 1996;3:36A
92. Many A, Zhou Y, Hubel CA, Fisher SJ, Roberts JM. Invasive cytotrophoblast manifest evidence of oxidative stress in preeclampsia. 1997 (Submitted)
93. Takehara Y, Yoshioka T, Sasaki J. Changes in the levels of lipoperoxide and antioxidant factors in human placenta during gestation. Acta Med Okayama 1990;44:103-111
94. Sekiba K, Yoshioka T. Changes of lipid peroxidation and Superoxide dismutase activity in the human placenta. Am J Obstet Gynecol 1979;135:368-371
95. Poranen AK, Ekblad U, Uotila P, Ahotupa M. Lipid peroxidation and antioxidants in normal and pre-eclamptic pregnancies. Placenta 1996;17:401-105
96. Pandey S, Gujrati VR, Chandravati, Sanger KCS, Shanker K. Status of human placental lipid peroxidation, superoxide dismutase and catalase during pregnancy-induced hypertension (PIH). Asia Pacific J Pharmacol 1995;10:41-14
97. Wang Y, Walsh SW. Antioxidant activities and mRNA expression of Superoxide dismutase, catalase, and glutathione peroxidase in normal and preeclamptic placentas. J Soc Gynecol Invest 1996;3:179-184
98. Chen G, Wilson R, Boyd P, et al. Normal Superoxide dismutase (SOD) gene in pregnancy-induced hypertension: Is the decreased SOD activity a secondary phenomenon? Free Radic Res 1994;21:59-66
99. Wisdom SJ, Wilson R, McKillip JH, Walker JJ. Antioxidant systems in normal pregnancy and in pregnancy-induced hypertension. Am J Obstet Gynecol 1991;165:1701-1704
100. Myatt L, Eis A, Brockman D, Kossenjans W, Greer I, Lyall F. Differential localization of superoxide dismutase isoforms in placental villous tissue of normotensive, pre-eclamptic, ind intrauterine growth-restricted pregnancies. J Histochem Cytochem 1997;45:1433-1438
101. Lefer DJ, Scalia R, Campbell B, et al. Peroxynitrite inhibits leukocyte-endothelial cell interactions and protects against ischemia-reperfusion injury in rats. J Clin Invest 1997;99:684-691
102. DeWolf F, Robertson WB, Brosens I. The ultrastructure of acute atherosis in hypertensive pregnancy. Am J Obstet Gynecol 1975;123:164-174
103. Haust MD, Heras JL, Harding PG. Fat-containing uterine smooth muscle cells in "toxemia": Possible relevance to atherosclerosis? Science 1977;195:1353-1354
104. Sheppard BL, Bonnar J. An ultrastructural study of uteroplacental spiral arteries in hypertensive and normotensive pregancy and fetal growth retardation. Br J Obstet Gynaecol 1981;88:695-705
105. Fox H. Pathology of the placenta. London: W.B. Saunders, 1978:213-237
106. Garzetti GG, Tranquilli AL, Cugini AM, Mazzanti L, Cester N, Romanini C. Altered lipid composition, increased lipid peroxidation, and altered fluidity of the membrane as evidence of platelet damage in preeclampsia. Obstet Gynecol 1993;81:337-340
107. Sotnikova LG, Naumov AV, Kuznetsova VA. The value of some parameters of erythrocyte membrane lipid peroxidation in late gestosis. Akush Ginekol 1986;4:20-22
108. Wang Y, Walsh SW, Guo J, Zhang J. Maternal levels of prostacyclin, thromboxane, vitamin E, and lipid peroxides throughout normal pregnancy. Am J Obstet Gynecol 1991;165:1690-1694
109. Frei B. Ascorbic acid protects lipids in human plasma and low-density lipoprotein against oxidative damage. Am J Clin Nutr 1991;54:1113S-1118S
110. Minakami H, Kimura Z, Tamada T, Yasuda Y, Hirota N. Hepatocellular lipofuscin in pre-eclampsia. Asia-Oceania J Obstet Gynaecol 1989;15:277-280
111. Jansen H, Ghanem H, Kuypers JHSAM, Birkenhager JC. Autoantibodies against malondialdehyde-modified LDL are elevated in subjects with an LDL subclass pattern B. Atherosclerosis 1995;115:255-262
112. Armstrong VW, Wieland E, Diedrich F, et al. Serum antibodies to oxidised low-density lipoprotein in pre-eclampsia and coronary heart disease. Lancet 1994;343:1570
113. Branch DW, Mitchell MD, Miller E, Palinski W, Witztum JL. Pre-eclampsia and serum antibodies to oxidised low-density lipoprotein. Lancet 1994;343:645-646
114. Dekker GA, deVries JIP, Doelitzsch PM, et al. Underlying disorders associated with severe early-onset preeclampsia. Am J Obstet Gynecol 1995;173:1042-1048
115. Allen JY, Tapia-Santiago C, Kutteh WH. Antiphospholipid antibodies in patients with preeclampsia. Am J Reprod Immunol 1996;36:81-85
116. 2 glycoprotein 1 (and other proteins). Proc Natl Acad Sci (USA) 1997;94:10356-10361
117. Horkko S, Miller E, Dudl E, et al. Antiphospholipid antibodies are directed against epitopes of oxidized phospho-lipids. J Clin Invest 1996;98:815-825
118. Kurki T, Ailus K, Palosuo T, Ylikorkala O. Oxidized lowdensity lipoprotein, cardiolipin, and phosphatidyl serine fail to predict the risk of preeclampsia. Hypertens Preg 1996;15:251-256
119. Stocker R, Frei B. Endogenous antioxidant defences in human blood plasma. In: Sies H (ed). Oxidative stress: Oxidants and antioxidants. New York: Academic Press, 1991:213-243
120. Berger TM, Polidori MC, Dabbagh A, et al. Antioxidant activity of vitamin C in iron-overloaded human plasma. J Biol Chem 1997;272:15656-15660
121. Niki E. Vitamin C as an antioxidant. World Rev Nutr Diet 1991;64:1-30
122. Basu TK, Schorah CJ. Vitamin C in health and disease. Westport, CT: AVI Publishing Co., 1982:95-100
123. Clemetson CAB, Andersen L. Ascorbic acid metabolism in preeclampsia. Obstet Gynecol 1964;24:774-782
124. Mikhail MS, Anyaegbunam A, Garfinkel D, Palan PR, Basu J, Romney SL. Preeclampsia and antioxidant nutrients: Decreased plasma levels of reduced ascorbic acid, αtocopherol, and beta-carotene in women with preeclampsia. Am J Obstet Gynecol 1994;171:150-157
125. Hubel CA, Kagan VE, Kisin ER, McLaughlin MK, Roberts JM. Increased ascorbate radical formation and ascorbate depletion in plasma from women with preeclampsia: Implications for oxidative stress. Free Radic Biol Med 1997;23:597-609
126. Buettner GR, Jurkiewicz BA. Chemistry and biochemistry of ascorbic acid. In: Cadenas E, Packer L (eds). Handbook of antioxidants. New York: Marcel Dekker, 1996:91-115
127. Roginsky VA, Stegmann HB. Ascorbyl radical as natural indicator of oxidative stress: Quantitative regularities. Free Radic Biol Med 1994;17:93-103
128. Walker JJ. Hypertension in pregnancy. Br J Obstet Gynaecol 1994;101:639-644
129. Suhonen L, Teramo K. Hypertension and pre-eclampsia in women with gestational glucose intolerance. Acta Obstet Gynecol Scand 1993;72:269-272
130. Sibai BM, Gordon T, Thom E, et al. Risk factors for pre-eclampsia in healthy nulliparous women: A prospective multicenter study. Am J Obstet Gynecol 1995;172:642-648
131. Arbogast BW, Taylor RN. A unifying theory of preeclampsia. In: Molecular mechanisms of preeclampsia. Austin: R. G. Landes, 1996:175-187
132. Arbogast BW, Leeper SC, Merrick RD, Olive KE, Taylor RN. Which plasma factors bring about disturbance of endothelial function in preeclampsia? Lancet 1994;343:340-341
133. Herrera E, Lasuncion MA, Coronado DG, Aranda P, Luna PL, Maier I. Role of lipoprotein lipase activity on lipoprotein metabolism and the fate of circulating triglycerides in pregnancy. Am J Obstet Gynecol 1988;158:1575-1583
134. Knopp RH, Bonet B, Lasuncion MA, Montelongo A, Herrera E. Lipoprotein metabolism in pregnancy. In: Herrera E, Knopp R (eds). Perinatal biochemistry. Boca Raton, FL: CRC Press, 1992:20-51
135. Potter JM, Nestel PJ. The hyperlipidemia of pregnancy in normal and complicated pregnancies. Am J Obstet Gynecol 1979;133:165-170
136. Alvarez JJ, Montelongo A, Iglesias A, Lasuncion MA, Herrera E. Longitudinal study on lipoprotein profile, high density lipoprotein subclass, and postheparin lipases during gestation in women. J Lipid Res 1996;37:299-308
137. Coleman RA. The role of the placenta in lipid metabolism and transport. Semin Perinatol. 1989;13:180
138. Boyd EM, Kingston CM. Blood lipids in preeclampsia. Am J Obstet Gynecol 1936;32:937-944
139. Endresen MJ, Lorentzen B, Henriksen T. Increased lipolytic activity and high ratio of free fatty acids to albumin in sera from women with preeclampsia leads to triglyceride accumulation in cultured endothelial cells. Am J Obstet Gynecol 1992;167:440-447
140. Arbogast BW, Leeper SC, Merrick RD, Olive KE, Taylor RN. Plasma factors that determine endothelial cell lipid toxicity in vitro correctly identify women with preeclampsia in early and late pregnancy. Hypertens Pregnancy 1996;15:263-279
141. Lorentzen B, Endresen MJ, Clausen T, Henriksen T. Fasting serum free fatty acids and triglycerides are increased before 20 weeks of gestation in women who later develop preeclampsia. Hypertens Pregnancy 1994;13:103-109
142. Gratacos E, Casals E, Sanllehy C, Cararach V, Alonso PL, Fortuny A. Variation in lipid levels during pregnancy in women with different types of hypertension. Acta Obstet Gynecol Scand 1996;75:896-901
143. Reaven GM. Syndrome X: 6 years later. J Intern Med 1994;236:13-22
144. Haffner SM, Mykkanen L, Robbins D, et al. Preponderance of small dense LDL is associated with specific insulin, proinsulin and the components of the insulin resistance syndrome in non-diabetic subjects. Diabetologia 1995;38:1328-1336
145. Bonora E, Targher G, Zenere MB, et al. Relationship of uric acid concentration to cardiovascular risk factors in young men. Role of obesity and central fat distribution. The Verona Young Men Atherosclerosis Risk Factors Study. Int J Obesity 1996;20:975-980
146. Eskenazi B, Fenster L, Sidney S. A multivariate analysis of risk factors for preeclampsia. JAMA 1991;266:237-241
147. Hubel CA, Lyell F, Weissfeld L, Gandley RE, Roberts JM. Small low-density lipoproteins and vascular cell adhesion molecule (VCAM-1) are increased in association with hyperlipidemia in preeclampsia. Metabolism (in press)
148. Sattar N, Bedomir A, Berry C, Shepherd J, Greer IA, Packard CJ. Lipoprotein subfraction concentrations in preeclampsia: Pathogenic parallels to atherosclerosis. Obstet Gynecol 1997;89:403-408
149. Sowers JR. Insulin resistance, hyperinsulinemia, dyslipidemia, hypertension, and accelerated atherosclerosis. J Clin Pharmacol 1992;32:529-535
150. Knudsen P, Eriksson J, Lahdenpera S, Kahri J, Groop L, Taskinen M-R. Changes of lipolytic enzymes cluster with insulin resistance syndrome. Diabetologia 1995;38:344-350
151. Biezenski JJ. Maternal lipid metabolism. Obstet Gynecol Ann 1974;3:203-233
152. Paolisso G, Gambardella A, Tagliamonte MR, et al. Does free fatty acid infusion impair insulin action also through an increase in oxidative stress ? J Clin Endocrinol Metab 1996;81:4244-4248
153. Toborek M, Barger W, Mattson MP, Barve S, McClain CJ, Hening B. Linoleic acid and TNF-α cross-amplify oxidative inury and dysfunction of endothelial cells. J Lipid Res 1996;37:123-135
154. Krauss RM. Genetic, metabolic, and dietary influences on the atherogenic lipoprotein phenotype. In: Simopoulos AP (ed). World Rev Nutr Diet. Basel: Karger, 1997:2-243
155. Krauss RM. The tangled web of coronary risk factors. Am J Med 1991;90:2a-36s
156. Lewis GF, Steiner G. Hypertriglyceridemia and its metabolic consequences as a risk factor for atherosclerotic cardiovascular disease in non-insulin-dependent diabetes mellitus. Diabetes Metab Rev 1996;12:37-56
157. Pronai L, Hiramatsu K, Saigusa Y, Nakazawa H. Low superoxide scavenging acivity associated with enhanced superoxide generation by monocytes from male hypertriglyceridemia with and without diabetes. Atherosclerosis 1991;90:39-17
158. Hiramatsu K, Arimori S. Increased superoxide production by mononuclear cells of patients with hypertriglyceridemia and diabetes. Diabetes 1988;37:832-837
159. Hoogerbrugge N, Verkerk A, Jacobs ML, Postema PTE, Jongkind JF. Hypertriglyceridemia enhances monocyte binding to endothelial cells in NIDDM. Diabetes Care 1996;19:1122-1125
160. McNamara JR, Campos H, Ordovas JM, Peterson JH, Wilson PWF, Schaefer E. Effect of gender, age, and lipid status on low density lipoprotein subfraction distribution. Arteriosclerosis 1987;7:483-490
161. Griffin BA. Low-density lipoprotein heterogeneity. Clin Endocrinol Metab 1995;9:687-703
162. Gardner CD, Fortmann SP, Krauss RM. Association of small low-density lipoprotein particles with the incidence of coronary artery disease in men and women. JAMA 1996;276:875-881
163. Stampfer MJ, Krauss RM, Ma J, et al. A prospective study of triglyceride level, low-density lipoprotein particle diameter, and risk of myocardial infarction. JAMA 1996;276:882-888
164. Selby JV, Austin MA, Newman B, et al. LDL subcalss phenotypes and the insulin resistance syndrome in women. Circulation 1993;88:381-387
165. Raal FJ, Areias AJ, Joffe BI. Low density lipoproteins and atherosclerosis-quantity or quality? Redox Report 1995;1:171-174
166. Anber R, Griffin BA, McConnell M, Packard CJ, Shepherd J. Influence of plasma lipid and LDL-subfraction profile on the interaction between low density lipoprotein with human arterial wall proteoglycans. Atherosclerosis 1996;124:261-271
167. Nordestgaard BG, Nielsen LB. Atherosclerosis and arterial influx of lipoproteins. Curr Opin Lipidol 1994;5:252-257
168. Tribble DL, Theil PM, vandenBerg JJM, Krauss RM. Differing α-tocopherol oxidative lability and ascorbic acid sparing effects in buoyant and dense LDL. Arterioscler Thromb Vase Biol 1995;15:2025-2031
169. Chait A, Brazg RL, Tribble DL, Krauss RM. Susceptibility of small, dense, low-density lipoproteins to oxidative modification in subjects with the atherogenic lipoprotein phenotype, pattern B. Am J Med 1993;94:350-356
170. Austin MA. Genetic epidemiology of dyslipidaemia and atherosclerosis. Ann Med 1996;28:459-464
171. Dejager S, Bruckert E, Chapman MJ. Dense low density lipoprotein subspecies with diminshed oxidative resistance predominate in combined hyperlipidemia. J Lipid Res 1993;34:295-308
172. Witztum JL. Susceptibility of low-density lipoprotein to oxidative modification. Am J Med 1993;94:347-349
173. Dimitriadis E, Griffin M, Owens D, Johnson A, Collins P, Tomkin GH. Oxidation of low-density lipoprotien in NIDDM: Its relationship to fatty acid composition. Diabetologia 1995;38:1300-1306
174. Tribble DL, vandenBerg JJM, Motchnik PA, et al. Oxidative susceptibility of low density lipoprotein subfractions is related their ubiquinol-10 and α-tocopherol content. Proc Natl Acad Sci USA 1994;91:1183-1187
175. Weisser B, Locher R, deGraff J, Moser R, Sachinidis A. Low density lipoprotein subfractions increase thromboxane formation in endothelial cells. Biochem Biophys Res Commun 1993;192:1245-1250
176. i in vascular smooth muscle cells. Circ Res 1993;73:118-124
177. Silliman K, Shore V, Forte TM. Hypertriglyceridemia during late pregnancy is associated with the formation of small dense low-density lipoproteins and the presence of large buoyant high-density lipoproteins. Metabolism 1994;43:1035-1041
178. Hubel CA, Shakir Y, Gandley RE, McLaughlin MK, Roberts JM. The hypertriglyceridemia of normal pregnancy is associated with increased formation of small low-density lipoproteins. J Soc Gynecol Invest 1997;4(Suppl): 141A (Abstract)
179. Sattar N, Greer I, Louden J, et al. Lipoprotein subfraction changes in normal pregnancy: Threshold effect of plasma triglyceride on appearance of small, dense low density lipoprotein. J Clin Endocrinol Metab 1997;82:2483-2491
180. Pierucci F, Garnica JJP, Cosmi EV, Anceschi MM. Oxidability of low density lipoproteins in pregnancy-induced hypertension. Br J Obstet Gynaecol 1996;103:1159-1161
181. Hennig B, Toborek M, Joshi-Barve S, et al. Linoleic acid activates nuclear transcription factor-κB (NF-κB) and induces NF-κB-dependent transcription in cultured endothelial cells. Am J Clin Nutr 1996;63:322-328
182. Henriksen T, Mahoney EM, Steinberg D. Enhanced macrophage degredation of low density lipoprotein previously incubated with cltrued endothelial cells: Recognition by receptors for acetylated low density lipoproteins. Proc Natl Acad Sci USA 1981;78:6499-6503
183. Henriksen T, Mahoney EM, Steinberg D. Enhanced macrophage degradation of biologically modified low density lipoprotein. Arteriosclerosis 1983;3:149-159
184. Parthasarathy S, Printz D, Boyd D, Joy L, Steinberg D. Macrophage oxidation of low density lipoprotein generates a modified form recognized by the scacvenger receptor. Arteriosclerosis 1986;6:505-510
185. Leake D. Does an acidic pH explain why low density lipoprotein is oxidised in atherosclerostic lesions? Atherosclerosis 1997;129:149-157
186. Kuzuya M, Naito M, Yamada K, et al. Involvement of intracellular iron in the toxicity of oxidized low density lipoprotein to cultured endothelial cells. Biochem Int 1990;22:567-573
187. Smith C, Mitchinson MJ, Aruoma OI, Halliwell B. Stimulation of lipid peroxidation and hydroxyl-radical generation by the contents of human atherosclerotic lesions. Biochem J 1992;286:901-905
188. Davidge ST, Hubel CA, Brayden RD, Capeless EC, McLaughlin MK. Sera antioxidant activity in uncomplicated and preeclamptic pregnancies. Obstet Gynecol 1992;79:897-901
189. Pocklington T, Foster MA, Mallard JR. Plasma total iron-binding capacity measured by electron spin resonance. Phys Med Biol 1977;22:98-102
190. Milman N, Agger AO, Neilsen OJ. Iron supplementation during pregnancy. Dan Med Bull 1991;38:471-476
191. Entman SS, Moore RM, Richardson LD, Killam AP. Elevated serum iron in toxemia of pregnancy. Am J Obstet Gynecol 1982;143:398-404
192. Entman SS, Richardson LD. Clinical applications of the altered iron kinetics of toxemia of pregnancy. Am J Obstet Gynecol 1983;146:568-574
193. Entman SS, Kambam JR, Bradley CA, Cousar JB. Increased levels of carboxyhemoglobin and serum iron as an indicator of increasedred cell turnover in preeclampsia. Am J Obstet Gynecol 1987;156:1169-1173
194. Samuels P, Main EK, Mennuti MT, Gabbe SG. The origin of increased serum iron in pregnancy-induced hypertension. Am J Obstet Gynecol 1987;157:721-725
195. Morton AG, Tavill AS. The role of iron in the regulation of hepatic transferrin synthesis. Brit J Haematol 1977;36:383-394
196. Mendenhall HW. Serum protein concentrations in pregnancy. Am J Obstet Gynecol 1970;106:388-399
197. Entman SS, Kambam JR, Boehm FH. Effect of maternal heme degradation on fetal carboxyhemoglobin concentration in pregnancy-induced hypertension. Am J Obstet Gynecol 1989;160:1394-1399
198. Magnusson MK, Sigfusson N, Sigvaldason H, Johannesson GM, Magnusson S, Thorgeirsson G. Low iron-binding capacity as a risk factor for myocardial infarction. Circulation 1994;89:102-108
199. Morris CJ, Earl JR, Trenam CW, Blake DR. Reactive oxygen species and iron - a dangerous partnership in inflammation. Int J Biochem Cell Biol 1995;27:109-122
200. Miller RA, Rasmussen GT, Cox CD, Miller RA, Britigan BE. Protease cleavage of iron-transferrin augments pyocyanin-mediated endothelial cell injury via promotion of hydroxyl radical formation. Infect Immunol 1996;64:182-188
201. Lamb DJ, Leake DS. Iron released transferrin at acidic pH can catalyse the oxidation of low density lipoprotein. FEBS Lett 1994;352:15-18
202. Murata M, Kodama H, Goto K, Hirano H, Tanaka T. Decreased very-low-density lipoprotein and low-density lipoprotein receptor messenger ribonucleic acid expression in placentas from preeclamptic pregnancies. Am J Obstet Gynecol 1996;175:1551-1556
203. Bonet B, Chait A, Gown AM, Knopp RH. Metabolism of modified LDL by cultured human placental cells. Atherosclerosis 1995;112:125-136
204. Mondon F, Alsat E, Berthelier M, Rebourcet R, Goldstein S, Polonovski J. Presence of acetyl-like modified LDL in human placental blood. Med Sci Res 1987;15:385-386
205. Alaiz M, Beppu M, Ohishi K, Kikugawa K. Modification of delipidated apoprotein B of low density lipoprotein by lipid oxidation products in relation to macrophage scavenger receptor binding. Biol Pharm Bull 1994;17:51-57
206. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol: Modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 1989;320:915-924
207. Casasco A, Calligaro A, Casasco M, et al. Immunohisto-chemical localization of lipoperoxidation products in normal human placenta. Placenta 1997;18:249-253
208. Morris J, Endresen MJR, Watts A, Linton E, Redman CWG. Pre-eclamptic placental syncytiotrophoblast microvillous membranes have altered fluidity and inhibit endothelial cell proliferation. Hypertens Pregnancy 1996;16:78 (Abstract)
209. Smarason AK, Sargent IL, Starkey PM, Redman CWG. The effect of placental syncytiotrophoblast microvillous membranes from normal and pre-eclamptic women on the growth of endothelial cells in vitro. Br J Obstet Gynecol 1993;100:943-949
210. Cockell AP, Learmont JG, Smarason AK, Redman CWG, Sargent IL, Poston L. Human placental syncytiotrophoblast microvillous membranes impair maternal vascular endothelial function. Br J Obstet Gynaecol 1997;104:235-240
211. Zollner H, Schaur RJ, Esterbauer H. Biological activities of 4-hydroxyalkenals. In: Seis H (ed). Oxidative stress: Oxidants and antioxidants. San Diego: Academic Press, 1991:337-355
212. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991;11:81-128
213. Esterbauer H. Cytotoxicity and genotoxicity of lipid-oxidation products. Am J Clin Nutr 1993;57:779S-786S
214. Benyo DF, Miles TM, Conrad KP. Hypoxia stimulates cytokine production by villous explants from the human placenta. J Clin Endocrinol Metab 1997;82:1582-1588
215. Toborek M, Hennig B. Is endothelial cell autocrine production of tumor necrosis factor a mediator of lipid-induced endothelial dysfunction. Med Hypoth 1996;47:377-382
216. Stark JM. Pre-eclampsia and cytokine induced oxidative stress. Br J Obstet Gynaecol 1993;100:105-109
217. Hotamisligil GS, Arner P, Cro JF, Atkinson RL, Speigelman BM. Increased adipose tissue expression of tumor necrosis factor-a in human obesity and insulin resistance. J Clin Invest 1995;95:2409-2415
218. Kern PA, Saghizadeh M, Ong JM, Bosch RJ, Deem R, Simsolo RB. The expression of tumor necrosis factor in human adipose tissue: Regulation by obesity, weight loss, and relationship to lipoprotein lipase. J Clin Invest 1995;95:2111-2119
219. Butterworth BH, Green IA, Liston WA, Haddad NG, Johnston TA. Immunocytochemical localization of neutrophil elastase in term placenta decidua and myometrium in pregnancy-induced hypertension. Br J Obstet Gynaecol 1991;98:929-933
220. Lyall F, Greer IA. Pre-eclampsia: A multifaceted vascular disorder of pregnancy. J Hypertens 1994;12:1339-1345
221. Greer IA, Dawes J, Johnston TA, Calder AA. Neutrophil activation is confined to the maternal circulation in pregnancy-induced hypertension. Obstet Gynecol 1991;78:28-32
222. Johnston TA, Greer IA, Dawes J, Calder AA. Neutrophil activation in small for gestational age pregnancies. Brit J Obstet Gynaecol 1989;98:978-982
223. Greer IA, Leask R, Hodson BA, Dawes J, Kilpatrick DC, Liston WA. Endothelin, elastase, and endothelial dysfunction in preeclampsia. Lancet 1991;337:558
224. Packer L. Oxidative stress, antioxidants, aging and disease. In: Cutler RG, et al. (eds). Oxidative stress and aging. Basel: Birkhauser Verlag, 1995:1-14
225. Hazen SL, Hsu FF, Mueller DM, Crowley JR, Heinecke JW. Human neutrophils employ chlorine gas as an oxidant during phagocytosis. J Clin Invest 1996;98:1283-1289
226. Hansen PR, Stawski G. Neutrophil mediated damage to isolated myocytes after anoxia and reoxygenation. Cardiovasc Res 1994;28:565-569
227. Hardy SJ, Ferrante A, Poulos A, Robinson BS, Johnson DW, Murray AW. Effect of exogenous fatty acids with greater than 22 carbon atoms (very long chain fatty acids) on superoxide production by human neutrophils. J Immunol 1994;153:1754-1761
228. Gorog P. Activation of human blood monocytes by oxidized polyunsturated fatty acids: A possible mechanism for the generation of lipid peroxides in the circulation. Int J Exp Pathol 1991;72:227-237
229. Maeba R, Maruyama A, Tarutani O, Uea N, Shimasaki H. Oxidized low-density lipoprotein induces the production of superoxide by neutrophils. FEBS Lett 1995;377:309-312
230. Uhlinger DJ, Burnham DN, Mullins RE, et al. Functional differences in human neutrophils isolated pre- and post-prandially. FEBS Lett 1991;286:28-32
231. Bellinati-Pires R, Waitzberg DL, Salgado MM, Carneiro-Sampaio MM. Functional alterations of human neutrophils by medium-chain triglyceride emulsions: Evaluation of phagocytosis, bacterial killing, and oxidative activity. J Leukoc Biol 1993;53:404-410
232. Tsukimori K, Maeda H, Ishida K, Nagata H, Koyanagi T, Nakano H. The superoxide generation of neutrophils in normal and preeclamptic pregnancies. Obstet Gynecol 1993;81:536-540
233. Studena K, Sacks G, Sargent I, Redman C. Leukocyte phenotypic and functional changes in preeclampsia and normal pregnancy - combined detection by whole blood flow cytometry. J Soc Gynecol Invest 1997;4(Suppl):246A (Abstract)