Inhibition of trophoblast-induced spiral artery remodeling reduces placental perfusion in rat pregnancy

Hypertension

Volumn 56, Issue 2, 2010, Pages 304-310

  Verlohren, Stefan ^a,b   Geusens, Nele ^c   Morton, Jude ^d   Verhaegen, Iris ^g   Hering, Lydia ^a   Herse, Florian ^a   Dudenhausen, Joachim W ^b   Muller, Dominik N ^a   Luft, Friedrich C ^a   Cartwright, Judith E ^e   Davidge, Sandra T ^d   Pijnenborg, Robert ^c   Dechend, Ralf ^a,f  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^d UNIVERSITY OF ALBERTA   (Canada)

^e ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^f HELIOS KLINIKUM BERLIN BUCH   (Germany)

^g NONE

Author keywords

animal models; doxycycline; matrix metalloproteinases; preeclampsia; pregnancy; rats; trophoblast

Indexed keywords

ALPHA ACTIN; CONTRAST MEDIUM; DOXYCYCLINE HYCLATE; FIBRIN; MATRIX METALLOPROTEINASE; ANGIOTENSINOGEN; RENIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMETRY; BODY WEIGHT; CONTROLLED STUDY; DRUG INHIBITION; FEMALE; FIBRIN DEPOSITION; GESTATIONAL AGE; HYPOTHESIS; INTRAUTERINE GROWTH RETARDATION; MALE; NONHUMAN; PLACENTA PERFUSION; PREECLAMPSIA; PREGNANCY; PREGNANT WOMAN; PRIORITY JOURNAL; RAT; TROPHOBLAST; VASCULARIZATION; ANIMAL; APOPTOSIS; ARTERY; BLOOD PRESSURE; GENETICS; HUMAN; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA; REFERENCE VALUE; SPRAGUE DAWLEY RAT; SYSTOLE;

ANGIOTENSINOGEN; ANIMALS; APOPTOSIS; ARTERIES; BLOOD PRESSURE; FEMALE; HUMANS; ORGAN SIZE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REFERENCE VALUES; RENIN; SYSTOLE; TROPHOBLASTS;

EID: 77955476641     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.110.153163     Document Type: Article

References (38)

1. Sibai BM, Dekker G and Kupferminc M. Pre-eclampsia. Lancet. 2005; 365: 785-799
2. 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 pro-teinuria in preeclampsia. J Clin Invest. 2003;111:649-658.
3. Verlohren S, Muller DN, Luft FC, Dechend R. Immunology in hypertension, preeclampsia, and target-organ damage. Hypertension. 2009;54: 439-443.
4. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta. 2006;27:939-958.
5. Hering L, Herse F, Verlohren S, Park JK, Wellner M, Qadri F, Pijnenborg R, Staff AC, Huppertz B, Muller DN, Luft FC, Dechend R. Trophoblasts reduce the vascular smooth muscle cell proatherogenic response. Hypertension. 2008;51:554-559.
6. Bohlender J, Ganten D, Luft FC. Rats transgenic for human renin and human angiotensinogen as a model for gestational hypertension. J Am Soc Nephrol. 2000;11:2056-2061.
7. Dechend R, Gratze P, Wallukat G, Shagdarsuren E, Plehm R, Brasen JH, Fiebeler A, Schneider W, Caluwaerts S, Vercruysse L, Pijnenborg R, Luft FC, Muller DN. Agonistic autoantibodies to the AT1 receptor in a transgenic rat model of preeclampsia. Hypertension. 2005;45:742-746.
8. Geusens N, Verlohren S, Luyten C, Taube M, Hering L, Vercruysse L, Hanssens M, Dudenhausen JW, Dechend R, Pijnenborg R. Endovascular trophoblast invasion, spiral artery remodelling and uteroplacental haemody-namics in a transgenic rat model of pre-eclampsia. Placenta. 2008;29: 614-623.
9. Verlohren S, Niehoff M, Hering L, Geusens N, Herse F, Tintu AN, Plagemann A, LeNoble F, Pijnenborg R, Muller DN, Luft FC, Duden-hausen JW, Gollasch M, Dechend R. Uterine vascular function in a transgenic preeclampsia rat model. Hypertension. 2008;51:547-553.
10. Caluwaerts S, Vercruysse L, Luyten C, Pijnenborg R. Endovascular trophoblast invasion and associated structural changes in uterine spiral arteries of the pregnant rat. Placenta. 2005;26:574-584.
11. Huppertz B, Kertschanska S, Demir AY, Frank HG, Kaufmann P. Immu-nohistochemistry of matrix metalloproteinases (MMP), their substrates, and their inhibitors (TIMP) during trophoblast invasion in the human placenta. Cell Tissue Res. 1998;291:133-148.
12. Tanaka SS, Togooka Y, Sato H, Seiki M, Tojo H, Tachi C. Expression and localization of membrane type matrix metalloproteinase-1 (MT1-MMP) in trophoblast cells of cultured mouse blastocysts and ecto-placental cones. Placenta. 1998;19:41-48.
13. Naruse K, Lash GE, Innes BA, Otun HA, Searle RF, Robson SC, Bulmer JN. Localization of matrix metalloproteinase (MMP)-2, MMP-9 and tissue inhibitors for MMPs (TIMPs) in uterine natural killer cells in early human pregnancy. Hum Reprod. 2009;24:553-561.
14. Palei AC, Zaneti RA, Fortuna GM, Gerlach RF, Tanus-Santos JE. He-modynamic benefits of matrix metalloproteinase-9 inhibition by doxy-cycline during experimental acute pulmonary embolism. Angiology. 2005;56:611-617.
15. Bouvet C, Gilbert LA, Girardot D, deBlois D, Moreau P. Different involvement of extracellular matrix components in small and large arteries during chronic NO synthase inhibition. Hypertension. 2005;45:432-437.
16. McCormick J, Whitley GS, Le Bouteiller P, Cartwright JE. Soluble HLA-G regulates motility and invasion of the trophoblast-derived cell line SGHPL-4. Hum Reprod. 2009;24:1339-1345.
17. Pijnenborg R, Aplin JD, Ain R, Bevilacqua E, Bulmer JN, Cartwright J, Huppertz B, Knofler M, Maxwell C, Vercruysse L. Trophoblast and the endometrium: a workshop report. Placenta. 2004;25(suppl A):S42-S44.
18. Pijnenborg R, Ball E, Bulmer JN, Hanssens M, Robson SC, Vercruysse L. In vivo analysis of trophoblast cell invasion in the human. Methods Mol Med. 2006;122:11-44.
19. Croy BA, Esadeg S, Chantakru S, van den Heuvel M, Paffaro VA, He H, Black GP, Ashkar AA, Kiso Y, Zhang J. Update on pathways regulating the activation of uterine Natural Killer cells, their interactions with decidual spiral arteries and homing of their precursors to the uterus. J Reprod Immunol. 2003;59:175-191.
20. Naruse K, Lash GE, Bulmer JN, Innes BA, Otun HA, Searle RF, Robson SC. The urokinase plasminogen activator (uPA) system in uterine natural killer cells in the placental bed during early pregnancy. Placenta. 2009; 30:398-404.
21. Zhou Y, Damsky CH, Fisher SJ. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype: one cause of defective endovascular invasion in this syndrome? J Clin Invest. 1997;99:2152-2164.
22. Myers JE, Merchant SJ, Macleod M, Mires GJ, Baker PN, Davidge ST. MMP-2 levels are elevated in the plasma of women who subsequently develop preeclampsia. Hypertens Pregnancy. 2005;24:103-115.
23. Arenas IA, Xu Y, Lopez-Jaramillo P, Davidge ST. Angiotensin II-induced MMP-2 release from endothelial cells is mediated by TNF-cn. Am J Physiol Cell Physiol. 2004;286:C779-C784.
24. Wang M, Zhang J, Spinetti G, Jiang LQ, Monticone R, Zhao D, Cheng L, Krawczyk M, Talan M, Pintus G, Lakatta EG. Angiotensin II activates matrix metalloproteinase type II and mimics age-associated carotid arterial remodeling in young rats. Am J Pathol. 2005;167:1429-1442.
25. Haddy FJ, Molnar JI, Borden CW, Texter EC Jr. Comparison of direct effects of angiotensin and other vasoactive agents on small and large blood vessels in several vascular beds. Circulation. 1962;25:239-246.
26. Ferris TF, Stein JH, Kauffman J. Uterine blood flow and uterine renin secretion. J Clin Invest. 1972;51:2827-2833.
27. Franklin GO, Dowd AJ, Caldwell BV, Speroff L. The effect of angiotensin-II intravenous infusion on plasma renin activity and prostaglandins A, E, and F levels in the uterine vein of the pregnant monkey. Prostaglandins. 1974;6:271-280.
28. Li C, Ansari R, Yu Z, Shah D. Definitive molecular evidence of renin-angiotensin system in human uterine decidual cells. Hypertension. 2000; 36:159-164.
29. Buttar HS. An overview of the influence of ACE inhibitors on fetal-placental circulation and perinatal development. Mol Cell Biochem. 1997; 176:61-71.
30. DeLano FA, Schmid-Schonbein GW. Proteinase activity and receptor cleavage: mechanism for insulin resistance in the spontaneously hypertensive rat. Hypertension. 2008;52:415-423.
31. Castro MM, Rizzi E, Prado CM, Rossi MA, Tanus-Santos JE, Gerlach RF. Imbalance between matrix metalloproteinases and tissue inhibitor of metalloproteinases in hypertensive vascular remodeling. Matrix Biol. 29:194-201.
32. Golub LM, Lee HM, Ryan ME, Giannobile WV, Payne J, Sorsa T. Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms. Adv Dent Res. 1998;12:12-26.
33. Kelly BA, Bond BC, Poston L. Gestational profile of matrix metalloproteinases in rat uterine artery. Mol Hum Reprod. 2003;9:351-358.
34. Ramamurthy NS, Schroeder KL, McNamara TF, Gwinnett AJ, Evans RT, Bosko C, Golub LM. Root-surface caries in rats and humans: inhibition by a non-antimicrobial property of tetracyclines. Adv Dent Res. 1998;12:43-50.
35. Petrinec D, Liao S, Holmes DR, Reilly JM, Parks WC, Thompson RW. Doxycycline inhibition of aneurysmal degeneration in an elastase-induced rat model of abdominal aortic aneurysm: preservation of aortic elastin associated with suppressed production of 92 kD gelatinase. J Vasc Surg. 1996;23:336-346.
36. Villarreal FJ, Griffin M, Omens J, Dillmann W, Nguyen J, Covell J. Early short-term treatment with doxycycline modulates postinfarction left ventricular remodeling. Circulation. 2003;108:1487-1492.
37. Siddiqui MA, Janjua MZ. Effect of prenatal doxycycline administration on skeletal differentiation in long bones of Albino rat. J Pak Med Assoc. 2002;52:211-214.
38. Lamparter S, Slight SH, Weber KT. Doxycycline and tissue repair in rats. J Lab Clin Med. 2002;139:295-302.