Heme oxygenase-1 promotes migration and β-epithelial Na+ channel expression in cytotrophoblasts and ischemic placentas

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 306, Issue 9, 2014, Pages

  Warrington, Junie P ^a   Coleman, Kayla ^a   Skaggs, Courtney ^a   Hosick, Peter A ^a   George, Eric M ^a   Stec, David E ^a   Ryan, Michael J ^a   Granger, Joey P ^a   Drummond, Heather A ^a  

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

Author keywords

Cytotrophoblast; Heme oxygenase 1; Placenta; Preeclampsia; ENaC

Indexed keywords

AMILORIDE; BETA EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL; HEME OXYGENASE 1; PROTOPORPHYRIN COBALT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL MIGRATION; CONTROLLED STUDY; CYTOTROPHOBLAST; ENZYME INDUCTION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; IN VITRO STUDY; ISCHEMIA; NONHUMAN; PLACENTA; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UTERUS BLOOD FLOW;

CYTOTROPHOBLAST; HEME OXYGENASE-1; PLACENTA; PREECLAMPSIA; Β-ENAC;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE MODELS, ANIMAL; ENZYME INDUCTION; EPITHELIAL SODIUM CHANNELS; FEMALE; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; ISCHEMIA; PLACENTA; PLACENTAL CIRCULATION; PRE-ECLAMPSIA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFECTION; TROPHOBLASTS;

EID: 84900543672     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00566.2013     Document Type: Article

References (31)

1. Ahmed A, Rahman M, Zhang X, Acevedo CH, Nijjar S, Rushton I, Bussolati B, St. John J. Induction of placental heme oxygenase-1 is protective against TNFα-induced cytotoxicity and promotes vessel relaxation. Mol Med 6: 391-409, 2000.
2. Alexander BT, Kassab SE, Miller MT, Abram SR, Reckelhoff JF, Bennett WA, Granger JP. 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, 2001.
3. Althaus M, Fronius M, Buchäckert Y, Vadász I, Clauss WG, Seeger W, Motterlini R, Morty RE. Carbon monoxide rapidly impairs alveolar fluid clearance by inhibiting epithelial sodium channels. Am J Respir Cell Mol Biol 41: 639-650, 2009.
4. Barber A, Robson SC, Myatt L, Bulmer JN, Lyall F. Heme oxygenase expression in human placenta and placental bed: reduced expression of placenta endothelial HO-2 in preeclampsia and fetal growth restriction. FASEB J 15: 1158-1168, 2001.
5. del Mónaco S, Assef Y, Kotsias BA. Epithelial sodium channel in a human trophoblast cell line (BeWo). J Membr Biol 223: 127-139, 2008.
6. Del Mónaco SM, Marino GI, Assef YA, Damiano AE, Kotsias BA. Cell migration in BeWo cells and the role of epithelial sodium channels. J Membr Biol 232: 1-13, 2009.
7. Drummond HA, Furtado MM, Myers S, Grifoni S, Parker KA, Hoover A, Stec DE. ENaC proteins are required for NGF-induced neurite growth. Am J Physiol Cell Physiol 290: C404-C410, 2006.
8. + channel proteins: components of a vascular mechanosensor. Hypertension 44: 643-648, 2004.
9. George EM, Arany M, Cockrell K, Storm MV, Stec DE, Granger JP. Induction of heme oxygenase-1 attenuates sFlt-1-induced hypertension in pregnant rats. Am J Physiol Regul Integr Comp Physiol 301: R1495-R1500, 2011.
10. George EM, Cockrell K, Aranay M, Csongradi E, Stec DE, Granger JP. Induction of heme oxygenase 1 attenuates placental ischemia-induced hypertension. Hypertension 57: 941-948, 2011.
11. George EM, Colson D, Dixon J, Palei AC, Granger JP. Heme oxygenase-1 attenuates hypoxia-induced sFlt-1 and oxidative stress in placental villi through its metabolic products CO and bilirubin. Int J Hypertens 2012: 486053, 2012.
12. George EM, Hosick PA, Stec DE, Granger JP. Heme oxygenase inhibition increases blood pressure in pregnant rats. Am J Hypertens 26: 924-930, 2013.
13. Grifoni SC, Gannon KP, Stec DE, Drummond HA. ENaC proteins contribute to VSMC migration. Am J Physiol Heart Circ Physiol 291: H3076-H3086, 2006.
14. Jernigan NL, Drummond HA. Myogenic vasoconstriction in mouse renal interlobar arteries: role of endogenous β and γENaC. Am J Physiol Renal Physiol 291: F1184-F1191, 2006.
15. Jernigan NL, Drummond HA. Vascular ENaC proteins are required for renal myogenic constriction. Am J Physiol Renal Physiol 289: F891-F901, 2005.
16. Kaufmann P, Black S, Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69: 1-7, 2003.
17. Lyall F. Priming and remodelling of human placental bed spiral arteries during pregnancy-a review. Placenta 26 Suppl A: S31-S36, 2005.
18. Marino GI, Assef YA, Kotsias BA. The migratory capacity of human trophoblastic BeWo cells: effects of aldosterone and the epithelial sodium channel. J Membr Biol 246: 243-255, 2013.
19. Marino GI, Kotsias BA. Expression of the epithelial sodium channel sensitive to amiloride (ENaC) in normal and preeclamptic human placenta. Placenta 34: 197-200, 2013.
20. McCaig D, Lyall F. Inhibitors of heme oxygenase reduce invasion of human primary cytotrophoblast cells in vitro. Placenta 30: 536-538, 2009.
21. McDonald FJ, Price MP, Snyder PM, Welsh MJ. Cloning and expression of the beta-and gamma-subunits of the human epithelial sodium channel. Am J Physiol Cell Physiol 268: C1157-C1163, 1995.
22. Morgan T, Craven C, Ward K. Human spiral artery renin-angiotensin system. Hypertension 32: 683-687, 1998.
23. Odrcich MJ, Graham CH, Kimura KA, McLaughlin BE, Marks GS, Nakatsu K, Brien JF. Heme oxygenase and nitric oxide synthase in the placenta of the guinea-pig during gestation. Placenta 19: 509-516, 1998.
24. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA 94: 10925-10930, 1997.
25. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61: 748-755, 1968.
26. VanLandingham LG, Gannon KP, Drummond HA. Pressure-induced constriction is inhibited in a mouse model of reduced γ-ENaC. Am J Physiol Regul Integr Comp Physiol 297: R723-R728, 2009.
27. Wang S, He G, Yang Y, Liu Y, Diao R, Sheng K, Liu X, Xu W. Reduced expression of ENaC in placenta tissues of patients with severe preeclampsia is related to compromised trophoblastic cell migration and invasion during pregnancy. PLoS One 8: e72153, 2013.
28. Wang S, Publicover S, Gu Y. An oxygen-sensitive mechanism in regulation of epithelial sodium channel. Proc Natl Acad Sci USA 106: 2957-2962, 2009.
29. Zenclussen AC, Lim E, Knoeller S, Knackstedt M, Hertwig K, Hagen E, Klapp BF, Arck PC. Heme oxygenases in pregnancy II: HO-2 is downregulated in human pathologic pregnancies. Am J Reprod Immunol 50: 66-76, 2003.
30. Zhao H, Azuma J, Kalish F, Wong RJ, Stevenson DK. Maternal heme oxygenase 1 regulates placental vasculature development via angiogenic factors in mice. Biol Reprod 85: 1005-1012, 2011.
31. Zhao H, Wong RJ, Kalish FS, Nayak NR, Stevenson DK. Effect of heme oxygenase-1 deficiency on placental development. Placenta 30: 861-868, 2009.