Decidual vascularization and the expression of angiogenic growth factors and proteases in first trimester spontaneous abortions

Human Reproduction

Volumn 24, Issue 1, 2009, Pages 185-197

  Plaisier, M ^a,b   Dennert, I ^b   Rost, E ^b   Koolwijk, P ^a,c   Van Hinsbergh, V W M ^c   Helmerhorst, F M ^b  

^a TNO   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Angiogenic factors; Decidua; Missed abortion; Uterine natural killer cells; Vascularization

Indexed keywords

ANGIOGENIC FACTOR; ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; CASPASE 3; CD56 ANTIGEN; CD68 ANTIGEN; COMPLEMENTARY DNA; KI 67 ANTIGEN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 15; MATRIX METALLOPROTEINASE 16; MEMBRANE TYPE MATRIX METALLOPROTEINASE 5; MESSENGER RNA; PLACENTAL GROWTH FACTOR; PROTEINASE; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ADULT; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BASAL DECIDUA; CELL PROLIFERATION; CONTROL GROUP; CONTROLLED STUDY; CORRELATION ANALYSIS; DECIDUA; DECIDUA SECRETORY ENDOMETRIUM; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMPLANTATION; MACROPHAGE; MISSED ABORTION; NATURAL KILLER CELL; PARIETAL DECIDUA; PREGNANCY TERMINATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SPONTANEOUS ABORTION; VACUUM ASPIRATION; VASCULARIZATION;

EID: 57749191895     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/den296     Document Type: Article

References (65)

1. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007;8:464-478.
2. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res 2005;97:512-523.
3. Asahara T, Chen D, Takahashi T, Fujikawa K, Kearney M, Magner M, Yancopoulos GD, Isner JM. Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circ Res 1998;83:233-240.
4. Bjorn SF, Hastrup N, Larsen JF, Lund LR, Pyke C. Messenger RNA for membrane-type 2 matrix metalloproteinase, MT2-MMP, is expressed in human placenta of first trimester. Placenta 2000;21:170-176.
5. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 1991;6:791-798.
6. Burton GJ, Jauniaux E, Watson AL. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: the Boyd collection revisited. Am J Obstet Gynecol 1999; 181:718-724.
7. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003; 9:653-660.
8. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 2001;7:575-583.
9. Charnock-Jones DS. Soluble flt-1 and the angiopoietins in the development and regulation of placental vasculature. J Anat 2002;200:607-615.
10. Craven CM, Morgan T, Ward K. Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta 1998; 19:241-252.
11. Curry TE Jr, Osteen KG. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 2003;24:428-465.
12. Dunk C, Shams M, Nijjar S, Rhaman M, Qiu Y, Bussolati B, Ahmed A. Angiopoietin-1 and angiopoietin-2 activate trophbalst Tie-2 to promote growth and migration during placental development. Am J Path 2000;156:2185-2199.
13. Fiedler U, Christian S, Koidl S, Kerjaschki D, Emmett MS, Bates DO, Christofori G, Augustin HG. The sialomucin CD34 is a marker of lymphatic endothelial cells in human tumors. Am J Pathol 2006; 168:1045- 1053.
14. Geva E, Jaffe RB. Role of angiopoietins in reproductive tract angiogenesis. Obstet Gynecol Surv 2000;55:511-519.
15. Gibbons GH, Dzau VJ. The emerging concept of vascular remodeling. N Engl J Med 1994;330:1431-1438.
16. Greenwold N, Jauniaux E, Gulbis B, Hempstock J, Gervy C, Burton GJ. Relationship among maternal serum endocrinology, placental karyotype, and intervillous circulation in early pregnancy failure. Fertil Steril 2003;79:1373-1379.
17. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006;12:1065-1074.
18. Harris LK, Keogh RJ, Wareing M, Baker PN, Cartwright JE, Aplin JD, Whitley GS. Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a fas ligand-dependent mechanism. Am J Pathol 2006; 169:1863-1874.
19. Hill JA, Melling Gc, Johnson PM. Immunohistochemical studies of human uteroplacental tissues from first trimester spontaneous abortion. Am J Obstet Gynecol 1995;173:90-96.
20. Hotary K, Allen E, Punturieri A, Yana I, Weiss SJ. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J Cell Biol 2000;149:1309-1323.
21. Hyder SM, Stancel GM. Regulation of angiogenic growth factors in the female reproductive tract by estrogens and progestins. Mol Endocrinol 1999;13:806-811.
22. Jackson MR, Carney EW, Lye SJ, Ritchie JW. Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation. Placenta 1994;15:341-353.
23. Jauniaux E, Burton GJ. Pathophysiology of histological changes in early pregnancy loss. Placenta 2005;26:114-123.
24. Jokimaa V, Oksjoki S, Kujari H, Vuorio E, Anttila L. Altered expression of genes involved in the production and degradation of endometrial extracellular matrix in patients with unexplained infertility and recurrent miscarriages. Mol Hum Reprod 2002;8:1111-1116.
25. Joswig A, Gabriel HD, Kibschull M, Winterhager E. Apoptosis in uterine epithelium and decidua in response to implantation: evidence for two different pathways. Reprod Biol Endocrinol 2003;1:44-52.
26. Kam EP, Gardner L, Loke YW, King A. The role of trophoblast in the physiological change in decidual spiral arteries. Hum Reprod 1999; 14:2131-2138.
27. Kapiteijn K, Koolwijk P, van der Weiden RM, van Nieuw Amerongen G, Plaisier M, van Hinsbergh VW, Helmerhorst FM. Human embryo-conditioned medium stimulates in vitro endometrial angiogenesis. Fertil Steril 2006;85(Suppl 1):1232-1239.
28. Kingdom JC, Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta 1997;18:613-621.
29. Kohnen G, Campbell S, Jeffers MD, Cameron IT. Spatially regulated differentiation of endometrial vascular smooth muscle cells. Hum Reprod 2000;15:284-292.
30. Korgun ET, Celik-Ozenci C, Acar N, Cayli S, Desoye G, Demir R. Location of cell cycle regulators cyclin B1, cyclin A, PCNA, Ki67 and cell cycle inhibitors p21, p27 and p57 in human first trimester placenta and deciduas. Histochem Cell Biol 2006;125:615-624.
31. Lisman BA, Boer K, Bleker OP, van Wely M, van Groningen K, Exalto N. Abnormal development of the vasculosyncytial membrane in early pregnancy failure. Fertil Steril 2004;82:654-660.
32. Llano E, Pendas AM, Freije JP, Nakano A, Knauper V, Murphy G, Lopez-Otin C. Identification and characterization of human MT5-MMP, a new membrane-bound activator of progelatinase a overexpressed in brain tumors. Cancer Res 1999;59:2570-2576.
33. Marx L, Arck P, Kapp M, Kieslich C, Dietl J. Leukocyte populations, hormone receptors and apoptosis in eutopic and ectopic first trimester human pregnancies. Hum Reprod 1999;14:1111-1117.
34. Maynard SE, Min J, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IS et al. Excess placental soluble fms-like tyrosine kinase 1 (sflt-1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003;111:649-658.
35. Meegdes BH, Ingenhoes R, Peeters LL, Exalto N. Early pregnancy wastage: relationship between chorionic vascularization and embryonic development. Fertil Steril 1988;49:216-220.
36. Nagy JA, Dvorak AM, Dvorak HF. VEGF-A(164/165) and PlGF: roles in angiogenesis and arteriogenesis. Trends Cardiovasc Med 2003;13:169-175.
37. Nawrocki B, Polette M, Marchand V, Maquoi E, Beorchia A, Tournier JM, Foidart JM, Birembaut P. Membrane-type Matrix metalloproteinase-1 expression at the site of human placentation. Placenta 1996;17:565-572.
38. Nelen WL, Bulten J, Steegers EA, Blom HJ, Hanselaar AG, Eskes TK. Maternal homocysteine and chorionic vascularization in recurrent early pregnancy loss. Hum Reprod 2000;15:954-960.
39. Pepper MS. Role of matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. ATVB 2001;21:1104-1117.
40. Pijnenborg R, Bland JM, Robertson WB, Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983;4:397-413.
41. Plaisier M, Kapiteijn K, Koolwijk P, Fijten C, Hanemaaijer R, Grimbergen JM, Mulder-Stapel A, Quax PH, Helmerhorst FM, van Hinsbergh VW. Involvement of membrane-type matrix metalloproteinases (MT-MMPs) in capillary tube formation by human endometrial microvascular endothelial cells: role of MT3-MMP. J Clin Endocrinol Metab 2004;89:5828-5836.
42. Plaisier M, Koolwijk P, Hanemaaijer R, Verwey A, Weiden RM, Risse KJ, Jungerius C, Helmerhorst M, Hinsbergh VW. Membrane-type matrix metalloproteinases and vascularisation in human endometrium during the menstrual cycle. Mol Hum Reprod 2006;12:11-18.
43. Plaisier M, Rodrigues S, Willems F, Koolwijk P, van Hinsbergh VW, Helmerhorst FM. Different degrees of vascularisation and their relation to the expression of VEGF, PlGF, angiopoietins and their receptors in first-trimester decidua. Fertil Steril 2007;88:176-187.
44. Plaisier M, Koowijk P, Willems F, van Hinsbergh VWM, Helmerhorst FM. The expression of pericellular acting proteases in human 1st trimester decidua. Mol Hum Reprod 2008;14:41-51.
45. Quack K, Vassiliadou N, Pudney J, Anderson DJ, Hill JA. Leucocyte activation in the decidua of chromosomally normal and abnormal foetuses from women with recurrent abortion. Human Reprod 2001; 16:949-955.
46. Quenby S, Bates M, Doig T, Brewster J, Lewis-Jones DI, Johnson PM, Vince G. Pre-implantation endometrial leukocytes in women with recurrent miscarriage. Hum Reprod 1999;14:2386-2391.
47. Rogers PA, Donoghue JF, Girling JE. Endometrial lymphangiogenesis. Placenta 2008 2008;29S:48-54.
48. Salamonsen LA, Dimitriadis E, Jones RL, Nie G. Complex regulation of decidualisation: a role for cytokines and proteases - a review. Placenta 2003;24:S76-S85.
49. Sharkey AM, Day K, McPherson A, Malik S, Licence D, Smith SK, Charnock Jones DS. Vascular endothelial growth factor expression in humane endometrium is regulated by hypoxia. J Clin Endocrinol Metab 2000;85:402-409.
50. Sherer DM, Abulafia O. Angiogenesis during implantation, and placental and early embryonic development. Placenta 2001;22:1-13.
51. Shimada S, Nishida R, Takeda M, Iwabuchi K, Kishi R, Onoe K, Minakami H, Yamada H. Natural killer, natural killer T, helper and cytotoxic T cells in the decidua from sporadic miscarriage. Am J Reprod Immunol 2006;56:193-200.
52. Simoncini T, Mannella P, Fornari L, Caruso A, Varone G, Genazzani AR. In vitro effects of progesterone and progestins on vascular cells. Steroids 2003;68:831-836.
53. Smith SK. Angiogenesis and implantation. Hum Reprod 2000;15(Suppl 6):59-66.
54. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996; 87:1171-1180.
55. Tuckerman E, Laird SM, Prakash A, Li TC. Prognostic value of the measurement of uterine natural killer cells in the endometrium of women with recurrent miscarriage. Hum Reprod 2007;22:2208-2213.
56. Vailhe B, Dietl J, Kapp M, Toth B, Arck P. Increased blood vessel density in decidua parietalis is associated with spontaneous human first trimester abortion. Hum Reprod 1999;14:1628-1634.
57. Van den Heuvel MJ, Chantakru S, Xuemei X, Evans SS, Tekpetey F, Mote PA, Clarke CL, Croy BA. Trafficking of circulating pro-NK cells to the decidualizing uterus: regulatory mechanisms in the mouse and human. Immunol Invest 2005;34:273-293.
58. Van Hinsbergh VWM, Engelse MA, Quax PHA. Pericellular proteases in angiogenesis and vasculogenesis. Arterioscl Thromb Vasc Biol 2006; 26:716-728.
59. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003;92:827-839.
60. Von Rango U, Krusche CA, Kertschanska S, Alfer J, Kaufmann P, Beier HM. Apoptosis of extravillous trophoblast cells limits the trophoblast invasion in uterine but not in tubal pregnancy during first trimester. Placenta 2003;24:929-940.
61. Vuorela P, Hatva E, Lymboussaki A, Kaipainen A, Joukov V, Persico MG, Alitalo K, Halmesmaki E. Expression of vascular endothelial growth factor and placental growth factor in human placenta. Biol Reprod 1997;56:489-494.
62. Vuorela P, Carpen O, Tulppala M, Halmesmaki E. VEGF, its receptors and the tie receptors in recurrent miscarriage. Mol Hum Reprod 2000; 6:276-282.
63. Zhang EG, Smith SK, Baker PN, Charnock-Jones DS. The regulation and localization of angiopoietin-1, -2, and their receptor Tie2 in normal and pathologic human placentae. Mol Med 2001;7:624-635.
64. Zygmunt M, Herr F, Keller-Schoenwetter S, Kunzi-Rapp K, Munstedt K, Rao CV, Lang U, Preissner KT. Characterization of human chorionic gonadotropin as a novel angiogenic factor. J Clin Endocrinol Metab 2002;87:5290- 5296.
65. Zygmunt M, Herr F, Munstedt K, Lang U, Liang OD. Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol 2003; 110:S10-S18.