Roles of Apolipoprotein E (ApoE) and Inducible Nitric Oxide Synthase (iNOS) in Inflammation and Apoptosis in Preeclampsia Pathogenesis and Progression

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Mao, Luyi ^a   Zhou, Qiongjie ^a   Zhou, Shufeng ^b   Wilbur, Rhonda R ^b   Li, Xiaotian ^a  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; BIOLOGICAL MARKER; CASPASE 3; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PROTEIN; PROTEIN BAX; PROTEIN BCL 2; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; LIPID; NITRIC OXIDE; NOS2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIRTH; BIRTH WEIGHT; BLOOD PRESSURE; CELL STRUCTURE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DISEASE COURSE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; FEMALE; GENOTYPE; INFLAMMATION; LIPID BLOOD LEVEL; LIPID METABOLISM; MOUSE; NONHUMAN; PATHOGENESIS; PLACENTA WEIGHT; POLYMERASE CHAIN REACTION; PREECLAMPSIA; PREGNANCY OUTCOME; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN URINE LEVEL; TRIACYLGLYCEROL BLOOD LEVEL; TROPHOBLAST; ULTRASTRUCTURE; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; ANIMAL; BLOOD; ENZYMOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PLACENTA; PREGNANCY;

ANIMALS; APOLIPOPROTEINS E; APOPTOSIS; BIOLOGICAL MARKERS; BLOOD PRESSURE; DISEASE PROGRESSION; FEMALE; GENOTYPE; INFLAMMATION; LIPID METABOLISM; LIPIDS; MICE; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PLACENTA; PRE-ECLAMPSIA; PREGNANCY;

EID: 84874615842     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058168     Document Type: Article

References (49)

1. Sibai B, Dekker G, Kupferminc M, (2005) Pre-eclampsia. The Lancet 365: 785-799.
2. Brown MA, Lindheimer MD, de Swiet M, Van Assche A, Moutquin JM (2001) The classification and diagnosis of the hypertensive disorders of pregnancy: statement from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Hypertension in pregnancy: official journal of the International Society for the Study of Hypertension in Pregnancy 20: IX.
3. Kashinakunti S, Sunitha H, Gurupadappa K, Shankarprasad D, Suryaprakash G, et al. (2010) Lipid Peroxidation and Antioxidant Status in Preeclampsia. Al Ameen J Med Sci 3: 38-41.
4. Henriksen T. The role of lipid oxidation and oxidative lipid derivatives in the development of preeclampsia; 2000. Elsevier. 29-32.
5. Borzychowski A, Sargent I, Redman C. Inflammation and pre-eclampsia; 2006. Elsevier. 309-316.
6. Hubel CA, Lyall F, Weissfeld L, Gandley RE, Roberts JM, (1998) Small low-density lipoproteins and vascular cell adhesion molecule-1 are increased in association with hyperlipidemia in preeclampsia. Metabolism 47: 1281-1288.
7. Belo LI, Caslake M, Gaffney D, Santos-Silva A, Pereira-Leite LI, et al. (2002) Changes in LDL size and HDL concentration in normal and preeclamptic pregnancies. Atherosclerosis 162: 425-432.
8. Stokes KY, Cooper D, Tailor A, Granger DN, (2002) Hypercholesterolemia promotes inflammation and microvascular dysfunction: role of nitric oxide and superoxide1. Free Radical Biology and Medicine 33: 1026-1036.
9. Scalia R, Appel III JZ, Lefer AM, (1998) Leukocyte-endothelium interaction during the early stages of hypercholesterolemia in the rabbit: role of P-selectin, ICAM-1, and VCAM-1. Arteriosclerosis, thrombosis, and vascular biology 18: 1093-1100.
10. Mahley RW, Huang Y, Weisgraber KH, (2006) Putting cholesterol in its place: apoE and reverse cholesterol transport. Journal of Clinical Investigation 116: 1226.
11. Belo L, Gaffney D, Caslake M, Santos-Silva A, Pereira-Leite L, et al. (2004) Apolipoprotein E and cholesteryl ester transfer protein polymorphisms in normal and preeclamptic pregnancies. European Journal of Obstetrics & Gynecology and Reproductive Biology 112: 9-15.
12. Curtiss LK, Boisvert WA, (2000) Apolipoprotein E and atherosclerosis. Current opinion in lipidology 11: 243.
13. De Wolf F, Robertson W, Brosens I, (1975) The ultrastructure of acute atherosis in hypertensive pregnancy. American Journal of Obstetrics and Gynecology 123: 164.
14. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R, (1994) ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arteriosclerosis, thrombosis, and vascular biology 14: 133-140.
15. Nagy B, Rigo J, Fintor L, Karadi I, Toth T, (1998) Apolipoprotein E alleles in women with severe pre-eclampsia. Journal of clinical pathology 51: 324.
16. Gratacós E, (2000) Lipid-mediated endothelial dysfunction: a common factor to preeclampsia and chronic vascular disease. European Journal of Obstetrics & Gynecology and Reproductive Biology 92: 63-66.
17. Kleinert H, Pautz A, Linker K, Schwarz PM, (2004) Regulation of the expression of inducible nitric oxide synthase. European journal of pharmacology 500: 255-266.
18. Eissa NT, Haggerty CM, Palmer CD, Patton W, Moss J, (2001) Identification of residues critical for enzymatic activity in the domain encoded by exons 8 and 9 of the human inducible nitric oxide synthase. American journal of respiratory cell and molecular biology 24: 616.
19. Galijasevic S, Saed GM, Diamond MP, Abu-Soud HM, (2003) Myeloperoxidase up-regulates the catalytic activity of inducible nitric oxide synthase by preventing nitric oxide feedback inhibition. Proceedings of the National Academy of Sciences of the United States of America 100: 14766.
20. Corrêa PBF, Pancoto JAT, de Oliveira-Pelegrin GR, Cárnio EC, Rocha MJA, (2007) Participation of iNOS-derived NO in hypothalamic activation and vasopressin release during polymicrobial sepsis. Journal of neuroimmunology 183: 17-25.
21. Thomson A, Telfer J, Kohnen G, Young A, Cameron I, et al. (1997) Nitric oxide synthase activity and localization do not change in uterus and placenta during human parturition. Human Reproduction 12: 2546-2552.
22. Schiessl B, Mylonas I, Hantschmann P, Kuhn C, Schulze S, et al. (2005) 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. Journal of Histochemistry & Cytochemistry 53: 1441.
23. Faxen M, Nisell H, Kublickiene KR, (2001) Altered mRNA expression of ecNOS and iNOS in myometrium and placenta from women with preeclampsia. Archives of Gynecology and Obstetrics 265: 45-50.
24. Schiessl B, Mylonas I, Kuhn C, Kunze S, Schulze S, et al. (2006) Expression of Estrogen Receptor-[alpha], Estrogen Receptor-[beta] and Placental Endothelial and Inducible NO Synthase in Intrauterine Growth-Restricted and Normal Placentas. Archives of medical research 37: 967-975.
25. Yoshida T, Limmroth V, Irikura K, Moskowitz MA, (1994) The NOS inhibitor, 7-nitroindazole, decreases focal infarct volume but not the response to topical acetylcholine in pial vessels. Journal of Cerebral Blood Flow & Metabolism 14: 924-929.
26. Moffett A, Hiby S, (2007) How does the maternal immune system contribute to the development of pre-eclampsia? Placenta 28: S51-S56.
27. Lee SC, Zhao ML, Hirano A, Dickson DW, (1999) Inducible nitric oxide synthase immunoreactivity in the Alzheimer disease hippocampus: association with Hirano bodies, neurofibrillary tangles, and senile plaques. Journal of neuropathology and experimental neurology 58: 1163.
28. Thorns V, Hansen L, Masliah E, (1998) nNOS expressing neurons in the entorhinal cortex and hippocampus are affected in patients with Alzheimer's disease. Experimental neurology 150: 14-20.
29. Rosselli M, Imthurn B, Keller PJ, Jackson EK, Dubey RK, (1995) Circulating Nitric Oxide (Nitrite/Nitrate) Levels in Postmenopausal Women Substituted With 17β-Estradiol and Norethisterone Acetate A Two-Year Follow-up Study. Hypertension 25: 848-853.
30. Conover W, Iman RL, (1981) Rank transformations as a bridge between parametric and nonparametric statistics. The American Statistician 35: 124-129.
31. Mi S, zhang L, Duan Y, Wang Y, (2009) Multiple comparsion of randomizen block design of non-parametric test by SPSS. China Academic Journal Electronic Publishing House 36: 217-219.
32. Leinonen E, Hurt-Camejo E, Wiklund O, Hultén LM, Hiukka A, et al. (2003) Insulin resistance and adiposity correlate with acute-phase reaction and soluble cell adhesion molecules in type 2 diabetes. Atherosclerosis 166: 387.
33. Svenungsson E, Fei G, Jensen-Urstad K, De Faire U, Hamsten A, et al. (2003) TNF-α: a link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease. Lupus 12: 454-461.
34. Mohrschladt M, Weverling-Rijnsburger A, De Man F, Stoeken DJ, Sturk A, et al. (2000) Hyperlipoproteinemia affects cytokine production in whole blood samples ex vivo. The influence of lipid-lowering therapy. Atherosclerosis 148: 413-419.
35. Ali K, Middleton M, Puré E, Rader DJ, (2005) Apolipoprotein E suppresses the type I inflammatory response in vivo. Circulation research 97: 922-927.
36. Redman CWG, Sacks GP, Sargent IL, (1999) Preeclampsia: an excessive maternal inflammatory response to pregnancy. American Journal of Obstetrics and Gynecology 180: 499-506.
37. Benyo DF, Smarason A, Redman CWG, Sims C, Conrad KP, (2001) Expression of inflammatory cytokines in placentas from women with preeclampsia. Journal of Clinical Endocrinology & Metabolism 86: 2505-2512.
38. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW, (1994) Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 83: 113-118.
39. Redman CW, Sargent IL, (2005) Latest advances in understanding preeclampsia. Science Signalling 308: 1592.
40. Maynard SE, Min JY, Merchan J, Lim KH, Li J, et al. (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. Journal of Clinical Investigation 111: 649-658.
41. Grainger DJ, Reckless J, McKilligin E, (2004) Apolipoprotein E modulates clearance of apoptotic bodies in vitro and in vivo, resulting in a systemic proinflammatory state in apolipoprotein E-deficient mice. The Journal of Immunology 173: 6366.
42. Chen YC, Pohl G, Wang TL, Morin PJ, Risberg B, et al. (2005) Apolipoprotein E is required for cell proliferation and survival in ovarian cancer. Cancer research 65: 331.
43. Shesely EG, Gilbert C, Granderson G, Carretero CD, Carretero OA, et al. (2001) Nitric oxide synthase gene knockout mice do not become hypertensive during pregnancy. American Journal of Obstetrics and Gynecology 185: 1198-1203.
44. Moncada S, Palmer R, Higgs E (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43.
45. Banning AP, Groves PH, Buttery LDK, Wharton J, Rutherford RAD, et al. (1999) Reciprocal changes in endothelial and inducible nitric oxide synthase expression following carotid angioplasty in the pig. Atherosclerosis 145: 17-32.
46. Kim YM, Kim TH, Seol DW, Talanian RV, Billiar TR, (1998) Nitric Oxide Suppression of Apoptosis Occurs in Association with an Inhibition of Bcl-2 Cleavage and Cytochrome cRelease. Journal of Biological Chemistry 273: 31437-31441.
47. Leist M, Single B, Naumann H, Fava E, Simon B, et al. (1999) Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Experimental cell research 249: 396-403.
48. Wong JM, Billiar TR, (1995) Regulation and function of inducible nitric oxide synthase during sepsis and acute inflammation. Advances in Pharmacology 34: 155-170.
49. Tranquilli AL, Giannubilo SR, Tedeschi E, Bezzeccheri V, Suzuki H, et al. (2005) Placental expression of nitric oxide synthase during HELLP syndrome: the correlation with maternal-fetal Doppler velocimetry. Acta obstetricia et gynecologica Scandinavica 84: 849-853.