Upregulation of urotensin II receptor in preeclampsia causes in vitro placental release of soluble vascular endothelial growth factor receptor 1 in hypoxia

Hypertension

Volumn 56, Issue 1, 2010, Pages 172-178

  Gould, Phillip S ^a   Gu, Mei ^a   Liao, Jianqin ^a   Ahmad, Shakil ^c,d,e   Cudmore, Melissa J ^c,d   Ahmed, Asif ^c,d   Vatish, Manu ^a,b  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d BIRMINGHAM WOMEN S HOSPITAL   (United Kingdom)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

HIF 1 ; Placenta; Preeclampsia; SVEGFR 1; Urotensin II

Indexed keywords

BETA ACTIN; HORMONE RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; UROTENSIN II; UROTENSIN RECEPTOR; VASCULOTROPIN RECEPTOR 1;

ARTICLE; CONTROLLED STUDY; EXPLANT; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; PLACENTA; PREECLAMPSIA; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SYNCYTIOTROPHOBLAST; VASCULAR ENDOTHELIUM; VASCULARIZATION; WESTERN BLOTTING;

BLOTTING, WESTERN; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASODILATION;

EID: 77953811161     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.110.152074     Document Type: Article

References (49)

1. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005;308:1592-1594.
2. Gammill HS, Roberts JM. Emerging concepts in preeclampsia investigation. Front Biosci. 2007;12:2403-2411.
3. Karumanchi SA, Bdolah Y. Hypoxia and sflt-1 in preeclampsia: the "chicken-and-egg" question. Endocrinology. 2004;145:4835-4837.
4. Redman CW, Sargent IL. Placental stress and pre-eclampsia: a revised view. Placenta. 2009;30(suppl A):S38-S42.
5. Caniggia I, Winter JL. Adriana and luisa castellucci award lecture 2001. Hypoxia inducible factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies-a review. Placenta. 2002;23(suppl A):S47-S57.
6. Iwagaki S, Yokoyama Y, Tang L, Takahashi Y, Nakagawa Y, Tamaya T, Rajakumar A, Brandon HM, Daftary A, Ness R, Conrad KP. Augmentation of leptin and hypoxia-inducible factor 1a mrnas in the preeclamptic placenta evidence for the functional activity of hypoxia-inducible transcription factors overexpressed in preeclamptic placentae. Gynecol Endocrinol. 2004;18:263-268.
7. Rajakumar A, Brandon HM, Daftary A, Ness R, Conrad KP. Evidence for the functional activity of hypoxia-inducible transcription factors overexpressed in preeclamptic placentae. Placenta. 2004;25:763-769.
8. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee Kim Y, Goncalves LF, Gomez R, Edwin S. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia: young investigator award. Am J Obstet Gynecol. 2004;190:1541-1547.
9. Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA. Soluble fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res. 2005;57:1R-7R.
10. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA. Excess placental soluble fms-like tyrosine kinase 1 (sflt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003;111:649-658.
11. Walker JJ. Pre-eclampsia. Lancet. 2000;356:1260-1265.
12. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med. 2004;350:672-683.
13. Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res. 2004;95:884-891.
14. Zhou CC, Ahmad S, Mi T, Xia L, Abbasi S, Hewett PW, Sun C, Ahmed A, Kellems RE, Xia Y. Angiotensin II induces soluble fms-like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circ Res. 2007;100:88-95.
15. Gibson A. Complex effects of gillichthys urotensin II on rat aortic strips. Br J Pharmacol. 1987;91:205-212.
16. Spinazzi R, Albertin G, Nico B, Guidolin D, Di Liddo R, Rossi GP, Ribatti D, Nussdorfer GG. Urotensin-II and its receptor (ut-r) are expressed in rat brain endothelial cells, and urotensin-II via ut-r stimulates angiogenesis in vivo and in vitro. Int J Mol Med. 2006;18:1107-1112.
17. Albertin G, Guidolin D, Sorato E, Spinazzi R, Mascarin A, Oselladore B, Montopoli M, Antonello M, Ribatti D. Pro-angiogenic activity of urotensin-ii on different human vascular endothelial cell populations. Regul Pept. 2009;157:64-71.
18. Ames RS, Sarau HM, Chambers JK, Willette RN, Aiyar NV, Romanic AM, Louden CS, Foley JJ, Sauermelch CF, Coatney RW, Ao Z, Disa J, Holmes SD, Stadel JM, Martin JD, Liu WS, Glover GI, Wilson S, McNulty DE, Ellis CE, Elshourbagy NA, Shabon U, Trill JJ, Hay DW, Ohlstein EH, Bergsma DJ, Douglas SA. Human urotensin-II is a potent vasoconstrictor and agonist for the orphan receptor gpr14. Nature. 1999; 401:282-286.
19. Douglas SA, Sulpizio AC, Piercy V, Sarau HM, Ames RS, Aiyar NV, Ohlstein EH, Willette RN. Differential vasoconstrictor activity of human urotensin-II in vascular tissue isolated from the rat, mouse, dog, pig, marmoset and cynomolgus monkey. Br J Pharmacol. 2000;131: 1262-1274.
20. Proulx CD, Holleran BJ, Lavigne P, Escher E, Guillemette G, Leduc R. Biological properties and functional determinants of the urotensin II receptor. Peptides. 2008;29:691-699.
21. Totsune K, Takahashi K, Arihara Z, Sone M, Satoh F, Ito S, Kimura Y, Sasano H, Murakami O. Role of urotensin II in patients on dialysis. Lancet. 2001;358:810-811.
22. Maguire JJ, Kuc RE, Wiley KE, Kleinz MJ, Davenport AP. Cellular distribution of immunoreactive urotensin-II in human tissues with evidence of increased expression in atherosclerosis and a greater constrictor response of small compared to large coronary arteries. Peptides. 2004;25:1767-1774.
23. Zhu YC, Zhu YZ, Moore PK. The role of urotensin II in cardiovascular and renal physiology and diseases. Br J Pharmacol. 2006;148:884-901.
24. Zhang Y, Li J, Cao J, Chen J, Yang J, Zhang Z, Du J, Tang C. Effect of chronic hypoxia on contents of urotensin II and its functional receptors in rat myocardium. Heart Vessels. 2002;16:64-68.
25. Balat O, Aksoy F, Kutlar I, Ugur MG, Iyikosker H, Balat A, Anarat R. Increased plasma levels of urotensin-II in preeclampsia-eclampsia: a new mediator in pathogenesis? Eur J Obstet Gynecol Reprod Biol. 2005;120: 33-38.
26. Cowley E, Thompson JP, Sharpe P, Waugh J, Ali N, Lambert DG. Effects of pre-eclampsia on maternal plasma, cerebrospinal fluid, and umbilical cord urotensin II concentrations: a pilot study. Br J Anaesth. 2005;95: 495-499.
27. Qi JS, Minor LK, Smith C, Hu B, Yang J, Andrade-Gordon P, Damiano B. Characterization of functional urotensin II receptors in human skeletal muscle myoblasts: comparison with angiotensin II receptors. Peptides. 2005;26:683-690.
28. Douglas SA, Naselsky D, Ao Z, Disa J, Herold CL, Lynch F, Aiyar NV. Identification and pharmacological characterization of native, functional human urotensin-ii receptors in rhabdomyosarcoma cell lines. Br J Pharmacol. 2004;142:921-932.
29. Song W, McDonald J, Camarda V, Calo G, Guerrini R, Marzola E, Thompson JP, Rowbotham DJ, Lambert DG. Cell and tissue responses of a range of urotensin II analogs at cloned and native urotensin II receptors: evidence for coupling promiscuity. Naunyn Schmiedebergs Arch Pharmacol. 2006;373:148-157.
30. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins: identification by morphologic and immunologic criteria. J Clin Invest. 1973;52:2745-2756.
31. Kudo Y, Boyd CA, Sargent IL, Redman CW. Hypoxia alters expression and function of syncytin and its receptor during trophoblast cell fusion of human placental bewo cells: implications for impaired trophoblast syn-cytialisation in pre-eclampsia. Biochim Biophys Acta. 2003;1638:63-71.
32. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, Post M. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through tgf/3 (3). J Clin Invest. 2000;105:577-587.
33. Siman CM, Sibley CP, Jones CJ, Turner MA, Greenwood SL. The functional regeneration of syncytiotrophoblast in cultured explants of term placenta. Am J Physiol Regul Integr Comp Physiol. 2001;280: R1116-R1122.
34. Pritlove DC, Gu M, Boyd CA, Randeva HS, Vatish M. Novel placental expression of 2,3-bisphosphoglycerate mutase. Placenta. 2006;27: 924-927.
35. Vatish M, Randeva HS, Grammatopoulos DK. Hormonal regulation of placental nitric oxide and pathogenesis of pre-eclampsia. Trends Mol Med. 2006;12:223-233.
36. Kaluz S, Kaluzova M, Stanbridge EJ. Regulation of gene expression by hypoxia: integration of the HIF-transduced hypoxic signal at the hypox-ia-responsive element. Clin Chim Acta. 2008;395:6-13.
37. Segain JP, Rolli-Derkinderen M, Gervois N, Raingeard de la Bletiere D, Loirand G, Pacaud P. Urotensin II is a new chemotactic factor for ut receptor-expressing monocytes. J Immunol. 2007;179:901-909.
38. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, Many A, Zamudio S, Caniggia I. Increased expression of sflt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol. 2006;291:R1085-R1093.
39. Hornig C, Barleon B, Ahmad S, Vuorela P, Ahmed A, Weich HA. Release and complex formation of soluble VEGFR-1 from endothelial cells and biological fluids. Lab Invest. 2000;80:443-454.
40. Page NM, Woods RJ, Gardiner SM, Lomthaisong K, Gladwell RT, Butlin DJ, Manyonda IT, Lowry PJ. Excessive placental secretion of neurokinin b during the third trimester causes pre-eclampsia. Nature. 2000;405: 797-800.
41. Nielsen AH, Schauser KH, Poulsen K. Current topic: the uteroplacental renin-angiotensin system. Placenta. 2000;21:468-477.
42. Watanabe T, Kanome T, Miyazaki A, Katagiri T. Human urotensin II as a link between hypertension and coronary artery disease. Hypertens Res. 2006;29:375-387.
43. Mori M, Fujino M. Urotensin II-related peptide, the endogenous ligand for the urotensin II receptor in the rat brain. Peptides. 2004;25: 1815-1818.
44. Sugo T, Mori M. Another ligand fishing for g protein-coupled receptor 14 discovery of urotensin II-related peptide in the rat brain. Peptides. 2008; 29:809-1245.
45. Sugo T, Murakami Y, Shimomura Y, Harada M, Abe M, Ishibashi Y, Kitada C, Miyajima N, Suzuki N, Mori M, Fujino M. Identification of urotensin II-related peptide as the urotensin II-immunoreactive molecule in the rat brain. Biochem Biophys Res Commun. 2003;310:860-868.
46. Eubank TD, Roberts R, Galloway M, Wang Y, Cohn DE, Marsh CB. Gm-csf induces expression of soluble VEGF receptor-1 from human monocytes and inhibits angiogenesis in mice. Immunity. 2004;21: 831-842.
47. Bruegmann E, Gruemmer R, Neulen J, Motejlek K, Berghaus D, Weich HA, Eubank TD, Roberts R, Galloway M, Wang Y, Cohn DE, Marsh CB. Regulation of soluble vascular endothelial growth factor receptor 1 secretion from human endothelial cells by tissue inhibitor of metallopro-teinase 1. Mol Hum Reprod. 2009;15:749-756.
48. Gruemmer R, Motejlek K, Berghaus D, Weich HA, Neulen J. Regulation of soluble vascular endothelial growth factor receptor (sflt-1/svegfr-1) expression and release in endothelial cells by human follicular fluid and granulosa cells. Reprod Biol Endocrinol. 2005;3:57.
49. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW, Ahmed A. Negative regulation of soluble flt-1 and soluble endoglin release by heme oxygen-ase-1. Circulation. 2007;115:1789-1797.