Adhesion Molecules in Human Trophoblast - A Review. II. Extravillous Trophoblast

Placenta

Volumn 30, Issue 4, 2009, Pages 299-304

  Harris, L K ^a   Jones, C J P ^a   Aplin, J D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Adhesion molecule; Differentiation; Junction; Migration; Trophoblast; Ultrastructure

Indexed keywords

ACTIN; BETA1 INTEGRIN; CADHERIN; CELL ADHESION MOLECULE; EPHRIN; IMMUNOGLOBULIN; KISSPEPTIN; SELECTIN;

ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CYTOTROPHOBLAST; DESMOSOME; EXTRACELLULAR MATRIX; HUMAN; INTERMEDIATE FILAMENT; MYOMETRIUM; NONHUMAN; PLACENTA; PRIORITY JOURNAL; STROMA; TIGHT JUNCTION; TROPHOBLAST; UPREGULATION;

CADHERINS; CELL ADHESION MOLECULES; CELL PROLIFERATION; EPHRINS; FEMALE; HUMANS; INTEGRINS; INTERCELLULAR JUNCTIONS; PREGNANCY; SELECTINS; TROPHOBLASTS; TUMOR SUPPRESSOR PROTEINS;

EID: 62249176216     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2008.12.003     Document Type: Article

References (78)

1. Pijnenborg R., Vercruysse L., and Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 27 (2006) 939-958
2. Aplin J., and Jones C. Human placental development. In: Aplin J., Fazleabas A., Glasser S., and Giudice L. (Eds). The Endometrium (2008), Informa, London 422-431
3. Vicovac L., and Aplin J.D. Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel) 156 (1996) 202-216
4. Aplin J.D. Expression of integrin alpha 6 beta 4 in human trophoblast and its loss from extravillous cells. Placenta 14 (1993) 203-215
5. Damsky C.H., Librach C., Lim K.H., Fitzgerald M.L., McMaster M.T., Janatpour M., et al. Integrin switching regulates normal trophoblast invasion. Development 120 (1994) 3657-3666
6. Vicovac L., Jones C.J., and Aplin J.D. Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro. Placenta 16 (1995) 41-56
7. Zhou Y., Damsky C.H., Chiu K., Roberts J.M., and Fisher S.J. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 91 (1993) 950-960
8. Aplin J.D., Haigh T., Jones C.J., Church H.J., and Vicovac L. Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin alpha5beta1. Biol Reprod 60 (1999) 828-838
9. Damsky C.H., Fitzgerald M.L., and Fisher S.J. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 89 (1992) 210-222
10. Korhonen M., Ylanne J., Laitinen L., Cooper H.M., Quaranta V., and Virtanen I. Distribution of the alpha 1-alpha 6 integrin subunits in human developing and term placenta. Lab Invest 65 (1991) 347-356
11. Aplin J.D. Adhesion molecules in implantation. Rev Reprod 2 (1997) 84-93
12. Zhou Y., Fisher S.J., Janatpour M., Genbacev O., Dejana E., Wheelock M., et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?. J Clin Invest 99 (1997) 2139-2151
13. Bauer S., Pollheimer J., Hartmann J., Husslein P., Aplin J.D., and Knofler M. Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. J Clin Endocrinol Metab 89 (2004) 812-822
14. Genbacev O., Joslin R., Damsky C.H., Polliotti B.M., and Fisher S.J. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 97 (1996) 540-550
15. Irving J.A., and Lala P.K. Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-beta, IGF-II, and IGFBP-1. Exp Cell Res 217 (1995) 419-427
16. Thirkill T.L., Hendren S.R., Soghomonians A., Mariano N.F., Barakat A.I., and Douglas G.C. Regulation of trophoblast beta1-integrin expression by contact with endothelial cells. Cell Commun Signal 2 (2004) 4
17. Huppertz B., Kertschanska S., Frank H.G., Gaus G., Funayama H., and Kaufmann P. Extracellular matrix components of the placental extravillous trophoblast: immunocytochemistry and ultrastructural distribution. Histochem Cell Biol 106 (1996) 291-301
18. Kaufmann P., Huppertz B., and Frank H.G. The fibrinoids of the human placenta: origin, composition and functional relevance. Ann Anat 178 (1996) 485-501
19. Aplin J.D., Charlton A.K., and Ayad S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy. Cell Tissue Res 253 (1988) 231-240
20. Church H., Richards A., and Aplin J. Laminins in decidua, placenta and choriocarcinoma cells. Trophoblast Res 10 (1996) 143-162
21. Feinberg R.F., Kliman H.J., and Lockwood C.J. Is oncofetal fibronectin a trophoblast glue for human implantation?. Am J Pathol 138 (1991) 537-543
22. Spessotto P., Bulla R., Danussi C., Radillo O., Cervi M., Monami G., et al. EMILIN1 represents a major stromal element determining human trophoblast invasion of the uterine wall. J Cell Sci 119 (2006) 4574-4584
23. Araki-Taguchi M., Nomura S., Ino K., Sumigama S., Yamamoto E., Kotani-Ito T., et al. Angiotensin II mimics the hypoxic effect on regulating trophoblast proliferation and differentiation in human placental explant cultures. Life Sci 82 (2008) 59-67
24. Caniggia I., Mostachfi H., Winter J., Gassmann M., Lye S.J., Kuliszewski M., et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 105 (2000) 577-587
25. Genbacev O., Zhou Y., Ludlow J.W., and Fisher S.J. Regulation of human placental development by oxygen tension. Science 277 (1997) 1669-1672
26. Zhou Y., McMaster M., Woo K., Janatpour M., Perry J., Karpanen T., et al. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol 160 (2002) 1405-1423
27. Lacey H., Haigh T., Westwood M., and Aplin J.D. Mesenchymally-derived insulin-like growth factor 1 provides a paracrine stimulus for trophoblast migration. BMC Dev Biol 2 (2002) 5
28. Hirano T., Higuchi T., Ueda M., Inoue T., Kataoka N., Maeda M., et al. CD9 is expressed in extravillous trophoblasts in association with integrin alpha3 and integrin alpha5. Mol Hum Reprod 5 (1999) 162-167
29. Feinberg R.F., Kliman H.J., and Wang C.L. Transforming growth factor-beta stimulates trophoblast oncofetal fibronectin synthesis in vitro: implications for trophoblast implantation in vivo. J Clin Endocrinol Metab 78 (1994) 1241-1248
30. Bischof P., Haenggeli L., and Campana A. Gelatinase and oncofetal fibronectin secretion is dependent on integrin expression on human cytotrophoblasts. Hum Reprod 10 (1995) 734-742
31. Salamonsen L.A., Hannan N.J., and Dimitriadis E. Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Semin Reprod Med 25 (2007) 437-444
32. Thirkill T.L., and Douglas G.C. The vitronectin receptor plays a role in the adhesion of human cytotrophoblast cells to endothelial cells. Endothelium 6 (1999) 277-290
33. Soghomonians A., Barakat A.I., Thirkill T.L., Blankenship T.N., and Douglas G.C. Effect of shear stress on migration and integrin expression in macaque trophoblast cells. Biochim Biophys Acta 1589 (2002) 233-246
34. Douglas G.C., Thirkill T.L., and Blankenship T.N. Vitronectin receptors are expressed by macaque trophoblast cells and play a role in migration and adhesion to endothelium. Biochim Biophys Acta 1452 (1999) 36-45
35. Zhou Y., Damsky C.H., and Fisher S.J. 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 99 (1997) 2152-2164
36. Damsky C.H., and Fisher S.J. Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors. Curr Opin Cell Biol 10 (1998) 660-666
37. Divers M.J., Bulmer J.N., Miller D., and Lilford R.J. Beta 1 integrins in third trimester human placentae: no differential expression in pathological pregnancy. Placenta 16 (1995) 245-260
38. Dubernard G., Galtier-Fougairolles M., Cortez A., Uzan S., and Challier J.C. Immunohistochemistry of adhesion molecules, metalloproteinases and NO-synthases in extravillous trophoblast of tubal pregnancy. Cell Mol Biol (Noisy-le-grand) 51 Suppl. (2005) OL829-OL837
39. Burrows T.D., King A., and Loke Y.W. Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells: implications for vascular invasion during implantation. Placenta 15 (1994) 21-33
40. Blankenship T.N., and King B.F. Macaque intra-arterial trophoblast and extravillous trophoblast of the cell columns and cytotrophoblastic shell express neural cell adhesion molecule (NCAM). Anat Rec 245 (1996) 525-531
41. Woodfin A., Voisin M.B., and Nourshargh S. PECAM-1: a multi-functional molecule in inflammation and vascular biology. Arterioscler Thromb Vasc Biol 27 (2007) 2514-2523
42. Bulla R., Villa A., Bossi F., Cassetti A., Radillo O., Spessotto P., et al. VE-cadherin is a critical molecule for trophoblast-endothelial cell interaction in decidual spiral arteries. Exp Cell Res 303 (2005) 101-113
43. Coukos G., Makrigiannakis A., Amin K., Albelda S.M., and Coutifaris C. Platelet-endothelial cell adhesion molecule-1 is expressed by a subpopulation of human trophoblasts: a possible mechanism for trophoblast-endothelial interaction during haemochorial placentation. Mol Hum Reprod 4 (1998) 357-367
44. Lyall F., Bulmer J.N., Duffie E., Cousins F., Theriault A., and Robson S.C. Human trophoblast invasion and spiral artery transformation: the role of PECAM-1 in normal pregnancy, preeclampsia, and fetal growth restriction. Am J Pathol 158 (2001) 1713-1721
45. Pijnenborg R., Vercruysse L., Verbist L., and Van Assche F.A. Interaction of interstitial trophoblast with placental bed capillaries and venules of normotensive and pre-eclamptic pregnancies. Placenta 19 (1998) 569-575
46. Geusens N., Verlohren S., Luyten C., Taube M., Hering L., Vercruysse L., et al. Endovascular trophoblast invasion, spiral artery remodelling and uteroplacental haemodynamics in a transgenic rat model of pre-eclampsia. Placenta 29 (2008) 614-623
47. Blankenship T.N., and Enders A.C. Expression of platelet-endothelial cell adhesion molecule-1 (PECAM) by macaque trophoblast cells during invasion of the spiral arteries. Anat Rec 247 (1997) 413-419
48. Higuchi T., Fujiwara H., Egawa H., Sato Y., Yoshioka S., Tatsumi K., et al. Cyclic AMP enhances the expression of an extravillous trophoblast marker, melanoma cell adhesion molecule, in choriocarcinoma cell JEG3 and human chorionic villous explant cultures. Mol Hum Reprod 9 (2003) 359-366
49. Shih I.M., and Kurman R.J. Expression of melanoma cell adhesion molecule in intermediate trophoblast. Lab Invest 75 (1996) 377-388
50. Liu Q., Zhang B., Zhao X., Zhang Y., Liu Y., and Yan X. Blockade of adhesion molecule CD146 causes pregnancy failure in mice. J Cell Physiol 215 (2008) 621-626
51. Shih I., Wang T., Wu T., Kurman R.J., and Gearhart J.D. Expression of Mel-CAM in implantation site intermediate trophoblastic cell line, IST-1, limits its migration on uterine smooth muscle cells. J Cell Sci 111 Pt 17 (1998) 2655-2664
52. Thirkill T.L., Cao T., Stout M., Blankenship T.N., Barakat A., and Douglas G.C. MUC1 is involved in trophoblast transendothelial migration. Biochim Biophys Acta 1773 (2007) 1007-1014
53. Shyu M.K., Lin M.C., Liu C.H., Fu Y.R., Shih J.C., Lee C.N., et al. MUC1 expression is increased during human placental development and suppresses trophoblast-like cell invasion in vitro. Biol Reprod 79 (2008) 233-239
54. Genbacev O.D., Prakobphol A., Foulk R.A., Krtolica A.R., Ilic D., Singer M.S., et al. Trophoblast l-selectin-mediated adhesion at the maternal-fetal interface. Science 299 (2003) 405-408
55. Prakobphol A., Genbacev O., Gormley M., Kapidzic M., and Fisher S.J. A role for the l-selectin adhesion system in mediating cytotrophoblast emigration from the placenta. Dev Biol 298 (2006) 107-117
56. Zhou Y., Genbacev O., and Fisher S.J. The human placenta remodels the uterus by using a combination of molecules that govern vasculogenesis or leukocyte extravasation. Ann N Y Acad Sci 995 (2003) 73-83
57. Floridon C., Nielsen O., Holund B., Sunde L., Westergaard J.G., Thomsen S.G., et al. Localization of E-cadherin in villous, extravillous and vascular trophoblasts during intrauterine, ectopic and molar pregnancy. Mol Hum Reprod 6 (2000) 943-950
58. Fisher S.J., Cui T.Y., Zhang L., Hartman L., Grahl K., Zhang G.Y., et al. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 109 (1989) 891-902
59. MacCalman C.D., Getsios S., and Chen G.T. Type 2 cadherins in the human endometrium and placenta: their putative roles in human implantation and placentation. Am J Reprod Immunol 39 (1998) 96-107
60. Chen G.T., Getsios S., and MacCalman C.D. Cadherin-11 is a hormonally regulated cellular marker of decidualization in human endometrial stromal cells. Mol Reprod Dev 52 (1999) 158-165
61. Ino Y., Gotoh M., Sakamoto M., Tsukagoshi K., and Hirohashi S. Dysadherin, a cancer-associated cell membrane glycoprotein, down-regulates E-cadherin and promotes metastasis. Proc Natl Acad Sci U S A 99 (2002) 365-370
62. Batistatou A., Makrydimas G., Zagorianakou N., Zagorianakou P., Nakanishi Y., Agnantis N.J., et al. Expression of dysadherin and E-cadherin in trophoblastic tissue in normal and abnormal pregnancies. Placenta 28 (2007) 590-592
63. Bilban M., Ghaffari-Tabrizi N., Hintermann E., Bauer S., Molzer S., Zoratti C., et al. Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci 117 (2004) 1319-1328
64. Hiden U., Bilban M., Knofler M., and Desoye G. Kisspeptins and the placenta: regulation of trophoblast invasion. Rev Endocr Metab Disord 8 (2007) 31-39
65. Chennakesava C.S., Di Santo S., Ziemiecki A., Schneider H., and Andres A.C. Differential expression of the receptor tyrosine kinase EphB4 and its ligand Ephrin-B2 during human placental development. Placenta 27 (2006) 959-967
66. Red-Horse K., Kapidzic M., Zhou Y., Feng K.T., Singh H., and Fisher S.J. EPHB4 regulates chemokine-evoked trophoblast responses: a mechanism for incorporating the human placenta into the maternal circulation. Development 132 (2005) 4097-4106
67. Enders A.C., Blankenship T.N., Fazleabas A.T., and Jones C.J. Structure of anchoring villi and the trophoblastic shell in the human, baboon and macaque placenta. Placenta 22 (2001) 284-303
68. Enders A.C. Fine structure of anchoring villi of the human placenta. Am J Anat 122 (1968) 419-451
69. Marzioni D., Banita M., Felici A., Paradinas F.J., Newlands E., De Nictolis M., et al. Expression of ZO-1 and occludin in normal human placenta and in hydatidiform moles. Mol Hum Reprod 7 (2001) 279-285
70. Nishimura T., Dunk C., Lu Y., Feng X., Gellhaus A., Winterhager E., et al. Gap junctions are required for trophoblast proliferation in early human placental development. Placenta 25 (2004) 595-607
71. Wright J.K., Dunk C.E., Perkins J.E., Winterhager E., Kingdom J.C., and Lye S.J. EGF modulates trophoblast migration through regulation of connexin 40. Placenta 27 Suppl. A (2006) S114-S121
72. Meekins J.W., Pijnenborg R., Hanssens M., McFadyen I.R., and van Asshe A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 101 (1994) 669-674
73. Aardema M.W., Oosterhof H., Timmer A., van Rooy I., and Aarnoudse J.G. Uterine artery Doppler flow and uteroplacental vascular pathology in normal pregnancies and pregnancies complicated by pre-eclampsia and small for gestational age fetuses. Placenta 22 (2001) 405-411
74. Gerretsen G., Huisjes H.J., and Elema J.D. Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol 88 (1981) 876-881
75. Kim Y.M., Bujold E., Chaiworapongsa T., Gomez R., Yoon B.H., Thaler H.T., et al. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol 189 (2003) 1063-1069
76. Ball E., Bulmer J.N., Ayis S., Lyall F., and Robson S.C. Late sporadic miscarriage is associated with abnormalities in spiral artery transformation and trophoblast invasion. J Pathol 208 (2006) 535-542
77. Pijnenborg R., Anthony J., Davey D.A., Rees A., Tiltman A., Vercruysse L., et al. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 98 (1991) 648-655
78. Madazli R., Somunkiran A., Calay Z., Ilvan S., and Aksu M.F. Histomorphology of the placenta and the placental bed of growth restricted foetuses and correlation with the Doppler velocimetries of the uterine and umbilical arteries. Placenta 24 (2003) 510-516