Placental ischemia in pregnant rats impairs cerebral blood flow autoregulation and increases blood-brain barrier permeability

Physiological Reports

Volumn 2, Issue 8, 2014, Pages

  Warrington, Junie P ^a   Fan, Fan ^a   Murphy, Sydney R ^a   Roman, Richard J ^a   Drummond, Heather A ^a   Granger, Joey P ^a   Ryan, Michael J ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

AQP4; Blood brain barrier; CBF autoregulation; Cerebrovascular abnormalities; Edema; Preeclampsia; Pregnancy; Tight junction proteins

Indexed keywords

ALBUMIN; AQUAPORIN 4; CLAUDIN 1; EVANS BLUE; OCCLUDIN; PROTEIN ZO1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOREGULATION; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD FLOW; BRAIN EDEMA; BRAIN ISCHEMIA; BRAIN WATER; CONTROLLED STUDY; FEMALE; LASER DOPPLER FLOWMETRY; MEAN ARTERIAL PRESSURE; NONHUMAN; PREECLAMPSIA; PREGNANCY; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

EID: 85002579742     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12134     Document Type: Article

References (34)

1. Amburgey, O. A., A. C. Chapman, V. May, I. M. Bernstein, and M. J. Cipolla. 2010. Plasma from preeclamptic women increases blood-brain barrier permeability: role of vascular endothelial growth factor signaling. Hypertension 56: 1003-1008.
2. Aygün, B. K., Y. Baykuş, S. Berilgen, B. Kavak, H. Celik, and B. Gürateş. 2010. Posterior reversible encephalopathy syndrome in severe preeclampsia: case report and literature review. J. Turk. Ger. Gynecol. Assoc. 11: 216-219.
3. Baumbach, G. L., and D. D. Heistad. 1985. Regional, segmental, and temporal heterogeneity of cerebral vascular autoregulation. Ann. Biomed. Eng. 13: 303-310.
4. Betz, A. L., F. Iannotti, and J. T. Hoff. 1989. Brain edema: a classification based on blood-brain barrier integrity. Cerebrovasc. Brain Metab. Rev. 1: 133-154.
5. Chakravarty, A., and S. D. Chakrabarti. 2002. The neurology of eclampsia: some observations. Neurol. India 50: 128-135.
6. Cipolla, M. J., and G. Osol. 1998. Vascular smooth muscle actin cytoskeleton in cerebral artery forced dilatation. Stroke 29: 1223-1228.
7. Cipolla, M. J., N. DeLance, and L. Vitullo. 2006. Pregnancy prevents hypertensive remodeling of cerebral arteries: a potential role in the development of eclampsia. Hypertension 47: 619-626.
8. Cipolla, M. J., J. Smith, N. Bishop, L. V. Bullinger, and J. A. Godfrey. 2008. Pregnancy reverses hypertensive remodeling of cerebral arteries. Hypertension 51: 1052-1057.
9. Cipolla, M. J., J. G. Sweet, and S. L. Chan. 2011. Cerebral vascular adaptation to pregnancy and its role in the neurological complications of eclampsia. J. Appl. Physiol. 110: 329-339.
10. Cipolla, M. J., N. Bishop, and S. L. Chan. 2012. Effect of pregnancy on autoregulation of cerebral blood flow in anterior versus posterior cerebrum. Hypertension 60: 705-711.
11. Demirtaş, O., F. Gelal, B. D. Vidinli, L. O. Demirtaş, E. Uluç, and A. Baloğlu. 2005. Cranial MR imaging with clinical correlation in preeclampsia and eclampsia. Diagn. Interv. Radiol. 11: 189-194.
12. Fukuda, A. M., and J. Badaut. 2012. Aquaporin 4: a player in cerebral edema and neuroinflammation. J. Neuroinfl. 9: 279.
13. Granger, J. P., B. B. LaMarca, K. Cockrell, M. Sedeek, C. Balzi, D. Chandler, et al. 2006. Reduced uterine perfusion pressure (RUPP) model for studying cardiovascular-renal dysfunction in response to placental ischemia. Methods Mol. Med. 122: 383-392.
14. Hirashima, C., A. Ohkuchi, S. Matsubara, M. Furukawa, T. Watanabe, and M. Suzuki. 2006. Hydrocephalus after intraventricular hemorrhage in eclamptic woman with HELLP syndrome. Hypertens. Preg. 25: 255-257.
15. Janzarik, W. G., E. Ehlers, R. Ehmann, T. A. Gerds, J. Schork, S. Mayer, et al. 2014. Dynamic cerebral autoregulation in pregnancy and the risk of preeclampsia. Hypertension 63: 161-166.
16. Koehler, R. C., R. J. Roman, and D. R. Harder. 2009. Astrocytes and the regulation of cerebral blood flow. Trends Neurosci. 32: 160-169.
17. Liu, W. Y., Z. B. Wang, L. C. Zhang, X. Wei, and L. Li. 2012. Tight junction in blood-brain barrier: an overview of structure, regulation, and regulator substances. CNS Neurosci. Ther. 18: 609-615.
18. MacKay, A. P., C. J. Berg, and H. K. Atrash. 2001. Pregnancy-related mortality from preeclampsia and eclampsia. Obstet. Gynecol. 97: 533-538.
19. Manfredi, M., A. Beltramello, L. G. Bongiovanni, A. Polo, L. Pistoia, and N. Rizzuto. 1997. Eclamptic encephalopathy: imaging and pathogenetic considerations. Acta Neurol. Scand. 96: 277-282.
20. Matsuda, H., K. Sakaguchi, T. Shibasaki, H. Takahashi, Y. Kawakami, K. Furuya, et al. 2005. Cerebral edema on MRI in severe preeclamptic women developing eclampsia. J. Perinat. Med. 33: 199-205.
21. Mitas, L., and L. Rogulski. 2012. Acute cortical blindness in preeclampsia-a case of reversible posterior encephalopathy syndrome. Ginekol. Pol. 83: 469-472.
22. Nicchia, G. P., B. Nico, L. M. Camassa, M. G. Mola, N. Loh, R. Dermietzel, et al. 2004. The role of aquaporin-4 in the blood-brain barrier development and integrity: studies in animal and cell culture models. Neuroscience 129: 935-945.
23. Osol, G., J. F. Brekke, K. McElroy-Yaggy, and N. I. Gokina. 2002. Myogenic tone, reactivity, and forced dilatation: a three-phase model of in vitro arterial myogenic behavior. Am. J. Physiol. Heart Circ. Physiol. 283: H2260-H2267.
24. Renic, M., J. A. Klaus, T. Omura, N. Kawashima, M. Onishi, N. Miyata, et al. 2009. Effect of 20-HETE inhibition on infarct volume and cerebral blood flow after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 29: 629-639.
25. Riskin-Mashiah, S., and M. A. Belfort. 2005. Preeclampsia is associated with global cerebral hemodynamic changes. J. Soc. Gynecol. Investig. 12: 253-256.
26. Ryan, M. J., E. L. Gilbert, P. H. Glover, E. M. George, C. W. Masterson, G. R. McLemore, et al. 2011. Placental ischemia impairs middle cerebral artery myogenic responses in the pregnant rat. Hypertension 58: 1126-1131.
27. Schreurs, M. P., and M. J. Cipolla. 2013. Cerebrovascular dysfunction and blood-brain barrier permeability induced by oxidized LDL are prevented by apocynin and magnesium sulfate in female rats. J. Cardiovasc. Pharmacol. 63: 33-39.
28. Schreurs, M. P., C. A. Hubel, I. M. Bernstein, A. Jeyabalan, and M. J. Cipolla. 2013. Increased oxidized low-density lipoprotein causes blood-brain barrier disruption in early-onset preeclampsia through LOX-1. FASEB J. 27: 1254-1263.
29. Topuz, S., I. Kalelioğlu, A. C. Iyibozkurt, S. Akhan, R. Has, M. Tunaci, et al. 2008. Cranial imaging spectrum in hypertensive disease of pregnancy. Clin. Exp. Obstet. Gynecol. 35: 194-197.
30. Verkman, A. S. 2011. Aquaporins at a glance. J. Cell Sci. 124: 2107-2112.
31. Vital, S. A., S. Terao, M. Nagai, and D. N. Granger. 2010. Mechanisms underlying the cerebral microvascular responses to angiotensin II-induced hypertension. Microcirculation 17: 641-649.
32. Wiegman, M. J., L. V. Bullinger, M. M. Kohlmeyer, T. C. Hunter, and M. J. Cipolla. 2008. Regional expression of aquaporin 1, 4, and 9 in the brain during pregnancy. Reprod. Sci. 15: 506-516.
33. Youssef, A. M., A. Hamidian Jahromi, C. G. Vijay, D. N. Granger, and J. S. Alexander. 2012. Intra-abdominal hypertension causes reversible blood-brain barrier disruption. J. Trauma Acute Care Surg. 72: 183-188.
34. Zunker, P., J. Ley-Pozo, F. Louwen, G. Schuierer, W. Holzgreve, and E. B. Ringelstein. 1995. Cerebral hemodynamics in pre-eclampsia/eclampsia syndrome. Ultrasound Obstet. Gynecol. 6: 411-415.