Placental ischemia increases seizure susceptibility and cerebrospinal fluid cytokines

Physiological Reports

Volumn 3, Issue 11, 2015, Pages

  Warrington, Junie P ^a  

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

Author keywords

Cerebrospinal fluid; cytokine; eclampsia; neurokinin B; placental ischemia; seizure

Indexed keywords

EID: 84977605681     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12634     Document Type: Article

References (52)

1. Alexander, B. T., S. E. Kassab, M. T. Miller, S. R. Abram, J. F. Reckelhoff, W. A. Bennett, et al. 2001. Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertension 37:1191–1195.
2. Ali, N. A., S. K. Palat Chirakkara, J. J. Reddy, and S. Sinha. 2013. Unilateral brain oedema related to focal status epilepticus. BMJ Case Rep. 2013. doi: 10.1136/bcr-2013-200864.
3. 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.
4. American College of Obstetricians and Gynecologists. 2013. Hypertension in pregnancy. Report of the American college of obstetricians and gynecologists’ task force on hypertension in pregnancy. Obstet. Gynecol. 122:1122–1131.
5. Chakravarty, A., and S. D. Chakrabarti. 2002. The neurology of eclampsia: some observations. Neurol. India 50:128–135.
6. Cornelius, D. C., J. P. Hogg, J. Scott, K. Wallace, F. Herse, J. Moseley, et al. 2013. Administration of interleukin-17 soluble receptor C suppresses TH17 cells, oxidative stress, and hypertension in response to placental ischemia during pregnancy. Hypertension 62:1068–1073.
7. D'Anna, R., G. Baviera, F. Corrado, A. Crisafulli, R. Ientile, M. Buemi, et al. 2004. Neurokinin B and nitric oxide plasma levels in pre-eclampsia and isolated intrauterine growth restriction. BJOG 111:1046–1050.
8. Darmochwal-Kolarz, D., M. Kludka-Sternik, J. Tabarkiewicz, B. Kolarz, J. Rolinski, B. Leszczynska-Gorzelak, et al. 2012. The predominance of Th17 lymphocytes and decreased number and function of Treg cells in preeclampsia. J. Reprod. Immunol. 93:75–81.
9. Dhillion, P., K. Wallace, F. Herse, J. Scott, G. Wallukat, J. Heath, et al. 2012. IL-17-mediated oxidative stress is an important stimulator of AT1-AA and hypertension during pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303:R353–R358.
10. El-Kabarity, R. H., and A. H. Naguib. 2011. Serum levels of IL-18, IL-12 and TH-1/TH-2 ratio in patients with pre-eclampsia. Egypt J. Immunol. 18:1–8.
11. Gadonski, G., B. B. LaMarca, E. Sullivan, W. Bennett, D. Chandler, and J. P. Granger. 2006. Hypertension produced by reductions in uterine perfusion in the pregnant rat: role of interleukin 6. Hypertension 48:711–716.
12. Gilbert, J. S., S. A. Babcock, and J. P. Granger. 2007. Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 50:1142–1147.
13. Gilbert, J. S., S. A. Gilbert, M. Arany, and J. P. Granger. 2009. Hypertension produced by placental ischemia in pregnant rats is associated with increased soluble endoglin expression. Hypertension 53:399–403.
14. 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.
15. Grant, A. D., R. Akhtar, N. P. Gerard, and S. D. Brain. 2002a. Neurokinin B induces oedema formation in mouse lung via tachykinin receptor-independent mechanisms. J. Physiol. 543:1007–1014.
16. Grant, A. D., N. P. Gerard, and S. D. Brain. 2002b. Evidence of a role for NK1 and CGRP receptors in mediating neurogenic vasodilatation in the mouse ear. Br. J. Pharmacol. 135:356–362.
17. 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 Pregnancy 25:255–257.
18. Hovsepian, D. A., N. Sriram, H. Kamel, M. E. Fink, and B. B. Navi. 2014. Acute cerebrovascular disease occurring after hospital discharge for labor and delivery. Stroke 45:1947–1950.
19. Huang, X. D., H. F. Huang, M. Y. Dong, Q. W. Yao, and H. Z. Wang. 2005. Relationship between serum and placental interleukin-18 levels and preeclampsia. Zhejiang Da Xue Xue Bao Yi Xue Ban 34:495–498.
20. Huang, Q., L. Liu, B. Hu, X. Di, S. P. Brennecke, and H. Liu. 2014. Decreased seizure threshold in an eclampsia-like model induced in pregnant rats with lipopolysaccharide and pentylenetetrazol treatments. PLoS ONE 9:e89333.
21. Iliff, J. J., and M. Nedergaard. 2013. Is there a cerebral lymphatic system? Stroke 44:S93–S95.
22. Inoue, H., N. Nagata, and Y. Koshihara. 1996. Involvement of tachykinin receptors in oedema formation and plasma extravasation induced by substance P, neurokinin A, and neurokinin B in mouse ear. Inflamm. Res. 45:316–323.
23. Jansen, I., C. Alafaci, J. McCulloch, R. Uddman, and L. Edvinsson. 1991. Tachykinins (substance P, neurokinin A, neuropeptide K, and neurokinin B) in the cerebral circulation: vasomotor responses in vitro and in situ. J. Cereb. Blood Flow Metab. 11:567–575.
24. Johnson, A. C., S. M. Tremble, S. L. Chan, J. Moseley, B. LaMarca, K. J. Nagle, et al. 2014. Magnesium sulfate treatment reverses seizure susceptibility and decreases neuroinflammation in a rat model of severe preeclampsia. PLoS ONE 9:e113670.
25. LaMarca, B. B., W. A. Bennett, B. T. Alexander, K. Cockrell, and J. P. Granger. 2005. Hypertension produced by reductions in uterine perfusion in the pregnant rat: role of tumor necrosis factor-alpha. Hypertension 46:1022–1025.
26. Liu, Y., X. Chen, and H. Chen. 2009. Placental and umbilical cord levels of neurokinin B and neurokinin B receptor in pre-eclampsia. Int. J. Gynaecol. Obstet. 107:58–59.
27. MacKay, A. P., C. J. Berg, and H. K. Atrash. 2001. Pregnancy-related mortality from preeclampsia and eclampsia. Obstet. Gynecol. 97:533–538.
28. Marksteiner, J., R. Wahler, R. Bellmann, M. Ortler, J. E. Krause, and G. Sperk. 1992. Limbic seizures cause pronounced changes in the expression of neurokinin B in the hippocampus of the rat. Neuroscience 49:383–395.
29. Martínez-García, E. A., B. Chávez-Robles, P. E. Sánchez-Hernández, L. Núñez-Atahualpa, B. T. Martín-Máquez, A. Muñoz-Gómez, et al. 2011. IL-17 increased in the third trimester in healthy women with term labor. Am. J. Reprod. Immunol. 65:99–103.
30. 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.
31. Maubach, K. A., C. Cody, and R. S. Jones. 1998. Tachykinins may modify spontaneous epileptiform activity in the rat entorhinal cortex in vitro by activating GABAergic inhibition. Neuroscience 83:1047–1062.
32. Mendelsohn, A. R., and J. W. Larrick. 2013. Sleep facilitates clearance of metabolites from the brain: glymphatic function in aging and neurodegenerative diseases. Rejuvenation Res. 16:518–523.
33. Mitas, L., and L. Rogulski. 2012. Acute cortical blindness in preeclampsia–a case of reversible posterior encephalopathy syndrome. Ginekol. Pol. 83:469–472.
34. Molvarec, A., A. Szarka, S. Walentin, G. Beko, I. Karádi, Z. Prohászka, et al. 2011. Serum leptin levels in relation to circulating cytokines, chemokines, adhesion molecules and angiogenic factors in normal pregnancy and preeclampsia. Reprod. Biol. Endocrinol. 9:124.
35. Mostello, D., T. K. Catlin, L. Roman, W. L. Holcomb, and T. Leet. 2002. Preeclampsia in the parous woman: who is at risk? Am. J. Obstet. Gynecol. 187:425–429.
36. Nour, N. M. 2008. An introduction to maternal mortality. Rev. Obstet. Gynecol. 1:77–81.
37. Page, N. M., and P. J. Lowry. 2000. Is ‘pre-eclampsia’ simply a response to the side effects of a placental tachykinin? J. Endocrinol. 167:355–361.
38. Page, N. M., R. J. Woods, S. M. Gardiner, K. Lomthaisong, R. T. Gladwell, D. J. Butlin, et al. 2000. Excessive placental secretion of neurokinin B during the third trimester causes pre-eclampsia. Nature 405:797–800.
39. Parajuli, B., H. Horiuchi, T. Mizuno, H. Takeuchi, and A. Suzumura. 2015. CCL11 enhances excitotoxic neuronal death by producing reactive oxygen species in microglia. Glia 63:2274–2284.
40. Plog, B. A., M. L. Dashnaw, E. Hitomi, W. Peng, Y. Liao, N. Lou, et al. 2015. Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J. Neurosci. 35:518–526.
41. Röder, C., R. Bellmann, K. E. McCarson, J. E. Krause, and G. Sperk. 1994. Kainic acid induced seizures cause a marked increase in the expression of neurokinin-3 receptor mRNA in the rat cerebellum. Neurosci. Lett. 181:158–160.
42. 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.
43. Saftlas, A. F., D. R. Olson, A. L. Franks, H. K. Atrash, and R. Pokras. 1990. Epidemiology of preeclampsia and eclampsia in the United States, 1979-1986. Am. J. Obstet. Gynecol. 163:460–465.
44. Seol, H. J., E. S. Lee, S. E. Jung, N. H. Jeong, J. E. Lim, S. H. Park, et al. 2009. Serum levels of YKL-40 and interleukin-18 and their relationship to disease severity in patients with preeclampsia. J. Reprod. Immunol. 79:183–187.
45. Sibai, B. M. 2006. Preeclampsia as a cause of preterm and late preterm (near-term) births. Semin. Perinatol. 30:16–19.
46. Sibai, B., G. Dekker, and M. Kupferminc. 2005. Pre-eclampsia. Lancet 365:785–799.
47. Szarka, A., J. Rigó, L. Lázár, G. Beko, and A. Molvarec. 2010. Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol. 11:59.
48. Takeuchi, M., K. Matsuzaki, M. Harada, H. Nishitani, and T. Matsuda. 2005. Cerebral hyperperfusion in a patient with eclampsia with perfusion-weighted magnetic resonance imaging. Radiat. Med. 23:376–379.
49. Tang, C. H., C. S. Wu, T. H. Lee, S. T. Hung, C. Y. Yang, C. H. Lee, et al. 2009. Preeclampsia-eclampsia and the risk of stroke among peripartum in Taiwan. Stroke 40:1162–1168.
50. Toldi, G., J. Rigó, B. Stenczer, B. Vásárhelyi, and A. Molvarec. 2011. Increased prevalence of IL-17-producing peripheral blood lymphocytes in pre-eclampsia. Am. J. Reprod. Immunol. 66:223–229.
51. Warrington, J. P., F. Fan, S. R. Murphy, R. J. Roman, H. A. Drummond, J. P. Granger, et al. 2014. Placental ischemia in pregnant rats impairs cerebral blood flow autoregulation and increases blood-brain barrier permeability. Physiol. Rep. 2:e12134.
52. Warrington, J. P., H. A. Drummond, J. P. Granger, and M. J. Ryan. 2015. Placental ischemia-induced increases in brain water content and cerebrovascular permeability: role of TNFa. Am. J. Physiol. Regul. Integr. Comp. Physiol. ajpregu.00372.02015. [Epub ahead of print].