Increased oxidized low-density lipoprotein causes blood-brain barrier disruption in early-onset preeclampsia through LOX-1

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1254-1263

  Schreurs, Malou P H ^a   Hubel, Carl A ^c,d   Bernstein, Ira M ^b   Jeyabalan, Arun ^c,d   Cipolla, Marilyn J ^a,b  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Neurological complications; Peroxynitrite; Pregnancy; Vascular permeability

Indexed keywords

OXIDIZED LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PEROXYNITRITE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIRTH WEIGHT; BLOOD BRAIN BARRIER; BRAIN VEIN; CLINICAL ARTICLE; CONTROLLED STUDY; DECOMPOSITION; DIASTOLIC BLOOD PRESSURE; FEMALE; FETUS GROWTH; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HYPERTENSION; LIPOPROTEIN BLOOD LEVEL; NEUROLOGIC DISEASE; NONHUMAN; PREECLAMPSIA; PREGNANCY; PREGNANCY OUTCOME; PRIORITY JOURNAL; RAT; SEIZURE; SYSTOLIC BLOOD PRESSURE;

ADULT; ANIMALS; BLOOD PRESSURE; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; FEMALE; FETAL GROWTH RETARDATION; HUMANS; LIPOPROTEINS, LDL; PEROXYNITROUS ACID; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY TRIMESTER, THIRD; RATS; RATS, SPRAGUE-DAWLEY; SCAVENGER RECEPTORS, CLASS E;

EID: 84874596863     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-222216     Document Type: Article

References (51)

1. Duley, L. (2009) The global impact of pre-eclampsia and eclampsia. Sem. Perinatol. 33, 130-137
2. Zeeman, G. G. (2009) Neurologic complications of pre-eclampsia. Sem. Perinatol. 33, 166-172
3. Okanloma, K. A., and Moodley, J. (2000) Neurological complications associated with the pre-eclampsia/eclampsia syndrome. Int. J. Gynecol. Obstet. 71, 223-225
4. Ogge, G., Chaiworapongsa, T., Romero, R., Hussein, Y., Kusanovic, J. P., Yeo, L., Kim, C. J., and Hassan, S. S. (2011) Placental lesions associated with maternal underperfusion are more frequent in early-onset than in late-onset preeclampsia. J. Perinat. Med. 39, 641-652
5. Douglas, K. A., and Redman, C. W. (1994) Eclampsia in the United Kingdom. Brit. Med. J. 309, 1395-1400 (Pubitemid 24351401)
6. von Dadelszen, P., Magee, L. A., and Roberts, J. M. (2003) Subclassification of preeclampsia. Hypertens. Pregnancy 22, 143-148 (Pubitemid 37521365)
7. Loureiro, R., Leite, C. C., Kahhale, S., Freire, S., Sousa, B., Cardoso, E. F., Alves, E. A., Borba, P., Cerri, G. G., and Zugaib, M. (2003) Diffusion imaging may predict reversible brain lesions in eclampsia and severe preeclampsia: initial experience. Am. J. Obstet. Gynecol. 189, 1350-1355 (Pubitemid 37542171)
8. Cipolla, M. J. (2007) Cerebrovascular function in pregnancy and eclampsia. Hypertension 50, 14-24 (Pubitemid 46986001)
9. Engelter, S. T., Provenzale, J. M., and Petrella, J. R. (2000) Assessment of vasogenic edema in eclampsia using diffusion imaging. Neuroradiology 42, 818-820
10. Friedman, A., Kaufer, D., and Heinemann, U. (2009) Bloodbrain barrier breakdown-inducing astrocytic transformation: novel targets for the prevention of epilepsy. Epilepsy Res. 85, 142-149
11. Foyouzi, N., Norwitz, E. R., Tsen, L. C., Buhimschi, C. S., and Buhimschi, I. A. (2006) Placental growth factor in the cerebrospinal fluid of women with preeclampsia. Int. J. Gynecol. Obstet. 92, 32-37 (Pubitemid 41773714)
12. Amburgey, O. A., Chapman, A. C., May, V., Bernstein, I. M., and Cipolla, M. J. (2010) Plasma from preeclamptic women increases blood-brain barrier permeability: role of vascular endothelial growth factor signaling. Hypertension 56, 1003-1008
13. Hubel, C. A., Lyall, F., Weissfeld, L., Gandley, R. E., and Roberts, J. M. (1998) Small low-density lipoproteins and vascular cell adhesion molecule-1 are increased in association with hyperlipidemia in preeclampsia. Metabolism 47, 1281-1288 (Pubitemid 28469258)
14. Belo, L., Santos-Silva, A., Caslake, M., Pereira-Leite, L., Quintanilha, A., and Rebelo, I. (2005) Oxidized-LDL levels in normal and pre-eclamptic pregnancies: contribution of LDL particle size. Atherosclerosis 183, 185-186 (Pubitemid 41416839)
15. Qiu, C., Phung, T. T., Vadachkoria, S., Muy-Rivera, M., Sanchez, S. E., and Williams, M. A. (2006) Oxidized low-density lipoprotein (oxidized LDL) and the risk of preeclampsia. Physiol. Res. 55, 491-500 (Pubitemid 44611194)
16. Redman, C. W., and Sargent, I. L. (2005) Latest advances in understanding preeclampsia. Science 308, 1592-1594 (Pubitemid 40807500)
17. Buhimschi, I. A., Saade, G. R., Chwalisz, K., and Garfield, R. E. (1998) The nitric oxide pathway in pre-eclampsia: pathophysiological implications. Hum. Reprod. Update 4, 25-42 (Pubitemid 28223053)
18. Ogura, S., Kakino, A., Sato, Y., Fujita, Y., Iwamoto, S., Otsui, K., Yoshimoto, R., and Sawamura, T. (2009) Lox-1: the multifunctional receptor underlying cardiovascular dysfunction. Circulation 73, 1993-1999
19. Mitra, S., Goyal, T., and Mehta, J. L. (2011) Oxidized LDL, LOX-1 and atherosclerosis. Cardiovasc. Drugs Ther. 25, 419-429
20. Morton, J. S., Abdalvand, A., Jiang, Y., Sawamura, T., Uwiera, R. R., and Davidge, S. T. (2012) Lectin-like oxidized low-density lipoprotein 1 receptor in a reduced uteroplacental perfusion pressure rat model of preeclampsia. Hypertension 59, 1014-1020
21. Sankaralingam, S., Xu, Y., Sawamura, T., and Davidge, S. T. (2009) Increased lectin-like oxidized low-density lipoprotein receptor-1 expression in the maternal vasculature of women with preeclampsia: role for peroxynitrite. Hypertension 53, 270-277
22. Sanchez, S. E., Williams, M. A., Muy-Rivera, M., Qiu, C., Vadachkoria, S., and Bazul, V. (2005) A case-control study of oxidized low density lipoproteins and preeclampsia risk. Gynecol. Endocrinol. 21, 193-199 (Pubitemid 41769994)
23. Cominacini, L., Rigoni, A., Pasini, A. F., Garbin, U., Davoli, A., Campagnola, M., Pastorino, A. M., Lo Cascio, V., and Sawamura, T. (2001) The binding of oxidized low density lipoprotein (ox-LDL) to ox-LDL receptor-1 reduces the intracellular concentration of nitric oxide in endothelial cells through an increased production of superoxide. J. Biol. Chem. 276, 13750-13755
24. Chen, X. P., Xun, K. L., Wu, Q., Zhang, T. T., Shi, J. S., and Du, G. H. (2007) Oxidized low density lipoprotein receptor-1 mediates oxidized low density lipoprotein-induced apoptosis in human umbilical vein endothelial cells: role of reactive oxygen species. Vasc. Pharmacol. 47, 1-9 (Pubitemid 46830770)
25. Beckman, J. S., and Koppenol, W. H. (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol. Cell Physiol. 271, C1424-C1437
26. Roberts, T. J., Chapman, A. C., and Cipolla, M. J. (2009) PPAR-gamma agonist rosiglitazone reverses increased cerebral venous hydraulic conductivity during hypertension. Am. J. Physiol. Heart Circ. Physiol. 297, H1347-H1353
27. Schreurs, M. P., Houston, E. M., May, V., and Cipolla, M. J. (2012) The adaptation of the blood-brain barrier to vascular endothelial growth factor and placental growth factor during pregnancy. FASEB J. 26, 355-362
28. Mayhan, W. G. (1995) Role of nitric oxide in disruption of the blood-brain barrier during acute hypertension. Brain Res. 686, 99-103
29. Xie, Z., Wei, M., Morgan, T. E., Fabrizio, P., Han, D., Finch, C. E., and Longo, V. D. (2002) Peroxynitrite mediates neurotoxicity of amyloid beta-peptide1-42- and lipopolysaccharide-activated microglia. J. Neurosci. 22, 3484-3492 (Pubitemid 37465754)
30. Palomares, S. M., Gardner-Morse, I., Sweet, J. G., and Cipolla, M. J. (2012) Peroxynitrite decomposition with FeTMPyP improves plasma-induced vascular dysfunction and infarction during mild but not severe hyperglycemic stroke. J. Cereb. Blood Flow Metab. 32, 1035-1045
31. Schreurs, M. P., and Cipolla M. J. (2012) Pregnancy enhances the effects of of hypercholesterolemia in posterior cerebral arteries. [E-pub ahead of print] Reprod. Sci. doi: 10.1177/1933719112459228
32. Marchi, N., Teng, Q., Ghosh, C., Fan, Q., Nguyen, M. T., Desai, N. K., Bawa, H., Rasmussen, P., Masaryk, T. K., and Janigro, D. (2010) Blood-brain barrier damage, but not parenchymal white blood cells, is a hallmark of seizure activity. Brain Res. 1353, 176-186
33. Chen, M., Masaki, T., and Sawamura, T. (2002) LOX-1, the receptor for oxidized low-density lipoprotein identified from endothelial cells: implications in endothelial dysfunction and atherosclerosis. Pharmacol. Ther. 95, 89-100
34. Enquobahrie, D. A., Williams, M. A., Butler, C. L., Frederick, I. O., Miller, R. S., and Luthy, D. A. (2004) Maternal plasma lipid concentrations in early pregnancy and risk of preeclampsia. Am. J. Hypertens. 17, 574-581 (Pubitemid 38844983)
35. Abbott, N. J., Ronnback, L., and Hansson, E. (2006) Astrocyteendothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53
36. Neal, C. R., Hunter, A. J., Harper, S. J., Soothill, P. W., and Bates, D. O. (2004) Plasma from women with severe preeclampsia increases microvascular permeability in an animal model in vivo. Clin. Sci. 107, 399-405 (Pubitemid 39389307)
37. Kim, Y. J., Park, H., Lee, H. Y., Ahn, Y. M., Ha, E. H., Suh, S. H., and Pang, M. G. (2007) Paraoxonase gene polymorphism, serum lipid, and oxidized low-density lipoprotein in preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 133, 47-52 (Pubitemid 46962877)
38. Uzun, H., Benian, A., Madazli, R., Topcuoglu, M. A., Aydin, S., and Albayrak, M. (2005) Circulating oxidized low-density lipoprotein and paraoxonase activity in preeclampsia. Gynecol. Obstet. Invest. 60, 195-200 (Pubitemid 41551970)
39. Branch, D. W., Mitchell, M. D., Miller, E., Palinski, W., and Witztum, J. L. (1994) Pre-eclampsia and serum antibodies to oxidised low-density lipoprotein. Lancet 343, 645-646 (Pubitemid 24087811)
40. Reyes, L. M., Garcia, R. G., Ruiz, S. L., Broadhurst, D., Aroca, G., Davidge, S. T., and Lopez-Jaramillo, P. (2012) Angiogenic imbalance and plasma lipid alterations in women with preeclampsia from a developing country. Growth Factors 30, 158-166
41. Pecks, U., Caspers, R., Schiessl, B., Bauerschlag, D., Piroth, D., Maass, N., and Rath, W. (2012) The evaluation of the oxidative state of low-density lipoproteins in intrauterine growth restriction and preeclampsia. Hypertens. Pregnancy 31, 156-165
42. Ross, R. (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801-809 (Pubitemid 23132154)
43. Staff, A. C., Dechend, R., and Pijnenborg, R. (2010) Learning from the placenta: acute atherosis and vascular remodeling in preeclampsia-novel aspects for atherosclerosis and future cardiovascular health. Hypertension 56, 1026-1034
44. Wikstrom, A.K., Nash, P., Eriksson, U. J., and Olovsson, M. H. (2009) Evidence of increased oxidative stress and a change in the plasminogen activator inhibitor (PAI)-1 to PAI-2 ratio in early-onset but not late-onset preeclampsia. Am. J. Obstet. Gynecol. 201, 597.e1-597.e8
45. Lee, H., Park, H., Kim, Y. J., Kim, H. J., Ahn, Y. M., Park, B., Park, J. H., and Lee, B. E. (2005) Expression of lectin-like oxidized low-density lipoprotein receptor-1 (LOX-1) in human preeclamptic placenta: possible implications in the process of trophoblast apoptosis. Placenta 26, 226-233 (Pubitemid 40247011)
46. Lin, Y. L., Chang, H. C., Chen, T. L., Chang, J. H., Chiu, W. T., Lin, J. W., and Chen, R. M. (2010) Resveratrol protects against oxidized LDL-induced breakage of the blood-brain barrier by lessening disruption of tight junctions and apoptotic insults to mouse cerebrovascular endothelial cells. J. Nutr. 140, 2187-2192
47. Nakano, A., Inoue, N., Sato, Y., Nishimichi, N., Takikawa, K., Fujita, Y., Kakino, A., Otsui, K., Yamaguchi, S., Matsuda, H., and Sawamura, T. (2010) LOX-1 mediates vascular lipid retention under hypertensive state. J. Hypertens. 28, 1273-1280
48. Roggensack, A. M., Zhang, Y., and Davidge, S. T. (1999) Evidence for peroxynitrite formation in the vasculature of women with preeclampsia. Hypertension 33, 83-89 (Pubitemid 29061846)
49. Heeba, G., Hassan, M. K., Khalifa, M., and Malinski, T. (2007) Adverse balance of nitric oxide/peroxynitrite in the dysfunctional endothelium can be reversed by statins. J. Cardiovasc. Pharmacol. 50, 391-398 (Pubitemid 350303816)
50. Miller, A. A., Drummond, G. R., De Silva, T. M., Mast, A. E., Hickey, H., Williams, J. P., Broughton, B. R., and Sobey, C. G. (2009) NADPH oxidase activity is higher in cerebral versus systemic arteries of four animal species: role of Nox2. Am. J. Physiol. Heart Circ. Physiol. 296, H220-H225
51. Kroll, J., and Waltenberger, J. (1999) A novel function of VEGF receptor-2 (KDR): rapid release of nitric oxide in response to VEGF-A stimulation in endothelial cells. Biochem. Biophys. Res. Commun. 265, 636-639