Trophoblast deportation part II: A review of the maternal consequences of trophoblast deportation

Placenta

Volumn 32, Issue 10, 2011, Pages 724-731

  Pantham, P ^a   Askelund, K J ^a   Chamley, L W ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Endothelial cell; Exosomes; Immune response; Microparticle; Preeclampsia; Syncytial knot; Trophoblast deportation

Indexed keywords

CELL ANTIGEN; FETAL ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; NANOPARTICLE;

CELL FUNCTION; CELL MEMBRANE; CELL PROLIFERATION; CYTOTROPHOBLAST; ENDOTHELIAL MICROPARTICLE; ENDOTHELIUM CELL; EXOSOME; FRAGMENTATION REACTION; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUNG BLOOD VESSEL; MEMBRANE MICROPARTICLE; NEUTROPHIL; NONHUMAN; PHAGOCYTE; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; REVIEW; SYNCYTIOTROPHOBLAST; TROPHOBLAST;

EID: 80052943869     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2011.06.019     Document Type: Article

References (85)

1. G. Schmorl Pathologisch-anatomische Untersuchungen über Puerperal-Eklampsie Vogel 1893
2. B. Sibai, G. Dekker, and M. Kupferminc Pre-eclampsia The Lancet 365 9461 2005 785 799 (Pubitemid 40311367)
3. G.P. Sacks, K. Studena, I.L. Sargent, and C.W.G. Redman Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis American Journal of Obstetrics and Gynecology 179 1 1998 80 86 (Pubitemid 28394477)
4. J.M. Roberts, R.N. Taylor, T.J. Musci, G.M. Rodgers, C.A. Hubel, and M.K. McLaughlin Preeclampsia: an endothelial cell disorder American Journal of Obstetrics and Gynecology 161 5 1989 1200 1204 (Pubitemid 20007682)
5. C.W. Redman, G.P. Sacks, and I.L. Sargent Preeclampsia: an excessive maternal inflammatory response to pregnancy American Journal of Obstetrics and Gynecology 180 2 Pt 1 1999 499 506 (Pubitemid 29093892)
6. I.L. Sargent, S.J. Germain, G.P. Sacks, S. Kumar, and C.W. Redman Trophoblast deportation and the maternal inflammatory response in pre-eclampsia Journal of Reproductive Immunology 59 2 2003 153 160 (Pubitemid 36945233)
7. B. Huppertz, J. Kingdom, I. Caniggia, G. Desoye, S. Black, and H. Korr Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotrophoblast into the maternal circulation Placenta 24 2003 181 190 (Pubitemid 37184714)
8. D.D. Taylor, S. Akyol, and C. Gercel-Taylor Pregnancy-associated exosomes and their modulation of T cell signaling Journal of Immunology 176 3 2006 1534 1542 (Pubitemid 43134297)
9. C.S. Hawes, H.A. Suskin, A. Petropoulos, S.E. Latham, and U.W. Mueller A morphologic study of trophoblast isolated from peripheral blood of pregnant women American Journal of Obstetrics and Gynecology 170 5 Pt 1 1994 1297 1300 (Pubitemid 24188692)
10. H.D. Attwood, and W.W. Park Embolism to the lungs by trophoblast The Journal of Obstetrics & Gynaecology of the British Commonwealth 68 1961 611 617
11. K. Benirschke, and P. Kaufmann Pathology of the human placenta 4th ed. 2006 Springer
12. F. Iklé Dissemination of syncytial trophoblastic cells in the maternal blood stream during pregnancy Bulletin der Scweizerischen Akademie der Medizinischen Wissenschaften 20 1964 62 72
13. B. Huppertz, H.G. Frank, J.C.P. Kingdom, F. Reister, and P. Kaufmann Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta Histochemistry and Cell Biology 110 5 1998 495 508 (Pubitemid 28480282)
14. Askelund K, Chamley L. Trophoblast deportation part I: review of the evidence demonstrating trophoblast death and shedding during human pregnancy. Placenta, in press.
15. B. Huppertz, M. Kadyrov, and J.C.P. Kingdom Apoptosis and its role in the trophoblast American Journal of Obstetrics and Gynecology 195 1 2006 29 39 (Pubitemid 43927489)
16. D.M. Nelson Apoptotic changes occur in syncytiotrophoblast of human placental villi where fibrin type fibrinoid is deposited at discontinuities in the villous trophoblast Placenta 17 7 1996 387 391 (Pubitemid 26381675)
17. V.S. Ratts, X.J. Tao, C.B. Webster, P.F. Swanson, P. Brownbill, and C. Sibley Regulation of apoptotic cell death within the trophoblast layer: role of Bcl-2, Bax and Bak in the term human placenta (Abstract) Journal of the Society for Gynecologic Investigation 5 Supplement 1998 126A
18. R. Austgulen, L. Chedwick, I.C. Vogt, L. Vatten, and C. Craven Trophoblast apoptosis in human placenta at term as detected by expression of a cytokeratin 18 degradation product of caspase Archives of Pathology and Laboratory Medicine 126 12 2002 1480 1486 (Pubitemid 36237254)
19. M. Kar, D. Ghosh, and J. Sengupta Histochemical and morphological examination of proliferation and apoptosis in human first trimester villous trophoblast Human Reproduction 22 11 2007 2814
20. S. Chua, T. Wilkins, I. Sargent, and C. Redman Trophoblast deportation in pre-eclamptic pregnancy British Journal of Obstetrics and Gynaecology 98 10 1991 973 979
21. M. Knight, C.W. Redman, E.A. Linton, and I.L. Sargent Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies British Journal of Obstetrics and Gynaecology 105 6 1998 632 640 (Pubitemid 28293481)
22. G.J. Burton, and C.J. Jones Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta Taiwanese Journal of Obstetrics and Gynecology 48 1 2009 28 37
23. N. Ishihara, H. Matsuo, H. Murakoshi, J.B. Laoag-Fernandez, T. Samoto, and T. Maruo Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation American Journal of Obstetrics and Gynecology 186 1 2002 158 166 (Pubitemid 34093758)
24. R. Kozma, M. Chapman, Y.W. Loke, P.M. Johnson, and M. Adinolfi Detection of trophoblast-like cells in maternal blood using specific monoclonal antibodies Journal of Reproductive Immunology 11 1 1987 55 61 (Pubitemid 17117562)
25. D.M. Nelson, E.C. Crouch, E.M. Curran, and D.R. Farmer Trophoblast interaction with fibrin matrix. Epithelialization of perivillous fibrin deposits as a mechanism for villous repair in the human placenta The American Journal of Pathology 136 4 1990 855 865 (Pubitemid 20142321)
26. M. Johansen, C.W. Redman, T. Wilkins, and I.L. Sargent Trophoblast deportation in human pregnancy-its relevance for pre-eclampsia Placenta 20 7 1999 531 539 (Pubitemid 29391296)
27. J.M. Foidart, J. Hustin, M. Dubois, and J.P. Schaaps The human placenta becomes haemochorial at the 13th week of pregnancy International Journal of Developmental Biology 36 3 1992 451 453
28. C.W.G. Redman, and I.L. Sargent Circulating microparticles in normal pregnancy and pre-eclampsia Placenta 29 2008 73 77
29. H. Schröcksnadel, G. Daxenbichler, E. Artner, G. Steckel-Berger, and O. Dapunt Tumor markers in hypertensive disorders of pregnancy Gynecologic and Obstetric Investigation 35 4 1993 204 208 (Pubitemid 23174507)
30. Y.M. Lo, T.N. Leung, M.S. Tein, I.L. Sargent, J. Zhang, and T.K. Lau Quantitative abnormalities of fetal DNA in maternal serum in preeclampsia Clinical Chemistry 45 2 1999 184 188 (Pubitemid 29079115)
31. L. Frängsmyr, V. Baranov, O. Nagaeva, U. Stendahl, L. Kjellberg, and L. Mincheva-Nilsson Cytoplasmic microvesicular form of Fas ligand in human early placenta: switching the tissue immune privilege hypothesis from cellular to vesicular level Molecular Human Reproduction 11 1 2005 35 41 (Pubitemid 40331001)
32. M. Hedlund, A.C. Stenqvist, O. Nagaeva, L. Kjellberg, M. Wulff, and V. Baranov Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function Journal of Immunology 183 1 2009 340 351
33. L. Mincheva-Nilsson, O. Nagaeva, T. Chen, U. Stendahl, J. Antsiferova, and I. Mogren Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival Journal of Immunology 176 6 2006 3585 3592 (Pubitemid 43364006)
34. L. Mincheva-Nilsson, and V. Baranov The role of placental exosomes in reproduction American Journal of Reproductive Immunology 63 6 2010 520 523
35. A.K. Stennett, and R.A. Khalil Neurovascular mechanisms of hypertension in pregnancy Current Neurovascular Research 3 2 2006 131 148 (Pubitemid 43764789)
36. W.A. Bardawil, and B.L. Toy The natural history of choriocarcinoma: problems of immunity and spontaneous regression Annals of the New York Academy of Sciences 80 1959 197 261
37. A.M. Baker, M.K. Morey, K.K. Berg, and J. Crosson Trophoblastic microemboli as a marker for preeclampsia-eclampsia in sudden unexpected maternal death: a case report and review of the literature The American Journal of Forensic Medicine and Pathology 21 4 2000 354 358
38. O.F. Coelho, and V. Valeri Pulmonary trophoblastic deportation. Cytologic aspects Acta Cytologica 21 2 1977 338 340 (Pubitemid 8090793)
39. A.E. Covone, D. Mutton, P.M. Johnson, and M. Adinolfi Trophoblast cells in peripheral blood from pregnant women The Lancet 2 8407 1984 841 843 (Pubitemid 14015469)
40. K. Benirschke, and L. Willes Deportation of trophoblastic emboli to maternal lung: a source of cell-free DNA in maternal blood? Chimerism 1 1 2010 15 18
41. G.W. Douglas, L. Thomas, M. Carr, N.M. Cullen, and R. Morris Trophoblast in the circulating blood during pregnancy American Journal of Obstetrics and Gynecology 78 1959 960 973
42. W. Lee, K.A. Ginsburg, D.B. Cotton, and R.H. Kaufman Squamous and trophoblastic cells in the maternal pulmonary circulation identified by invasive hemodynamic monitoring during the peripartum period American Journal of Obstetrics and Gynecology 155 5 1986 999 1001 (Pubitemid 17176665)
43. H.G. Burkitt, B. Young, and J.W. Heath Wheater's functional histology: a text and colour atlas 1993 Churchill Livingstone
44. L.M. Chen, B. Liu, H.B. Zhao, P. Stone, Q. Chen, and L. Chamley IL-6, TNFalpha and TGFbeta promote non-apoptotic trophoblast deportation and subsequently causes endothelial cell activation Placenta 31 1 2010 75 80
45. Q. Chen, P.R. Stone, L.M. McCowan, and L.W. Chamley Phagocytosis of necrotic but not apoptotic trophoblasts induces endothelial cell activation Hypertension 47 1 2006 116 121 (Pubitemid 43177824)
46. Q. Chen, P. Stone, L.M. Ching, and L. Chamley A role for interleukin-6 in spreading endothelial cell activation after phagocytosis of necrotic trophoblastic material: implications for the pathogenesis of pre-eclampsia The Journal of Pathology 217 1 2009 122 131
47. W.W. Park Experimental trophoblastic embolism of the lungs The Journal of Pathology and Bacteriology 75 2 1958 257 265
48. L.G. Tedeschi, and C.G. Tedeschi Experimental trophoblastic embolism and hyperplasminemia Archives of Pathology 76 1963 387 397
49. W.D. Billington, and B.J. Weir Deportation of trophoblast in the chinchilla Journal of Reproduction and Fertility 13 3 1967 593 595
50. S. Lau, S.J. Guild, C.J. Barrett, S.C. Malpas, and L. Chamley Injection of necrotic trophoblastic cells increased blood pressure in the final third of gestation in rats (Abstract) Placenta 31 9 2010 A137
51. U.W. Mueller, C.S. Hawes, A.E. Wright, A. Petropoulos, E. DeBoni, and F.A. Firgaira Isolation of fetal trophoblast cells from peripheral blood of pregnant women The Lancet 336 8709 1990 197 200 (Pubitemid 20229057)
52. M.H. Abumaree, P.R. Stone, and L.W. Chamley An in vitro model of human placental trophoblast deportation/shedding Molecular Human Reproduction 12 11 2006 687 694 (Pubitemid 44605601)
53. M.H. Abumaree, P.R. Stone, and L.W. Chamley The effects of apoptotic, deported human placental trophoblast on macrophages: possible consequences for pregnancy Journal of Reproductive Immunology 72 1-2 2006 33 45 (Pubitemid 44692309)
54. A.K. Smarason, I.L. Sargent, P.M. Starkey, and C.W. Redman The effect of placental syncytiotrophoblast microvillous membranes from normal and pre-eclamptic women on the growth of endothelial cells in vitro British Journal of Obstetrics and Gynaecology 100 10 1993 943 949 (Pubitemid 23308283)
55. A.K. Gupta, C. Rusterholz, B. Huppertz, A. Malek, H. Schneider, and W. Holzgreve A comparative study of the effect of three different syncytiotrophoblast micro-particles preparations on endothelial cells Placenta 26 1 2005 59 66 (Pubitemid 40123677)
56. C. Théry, S. Amigorena, G. Raposo, and A. Clayton Isolation and characterization of exosomes from cell culture supernatants and biological fluids Current Protocols in Cell Biology 2006 [Chapter 3(Unit 3.22)
57. R.A. Mathias, J.W. Lim, H. Ji, and R.J. Simpson Isolation of extracellular membranous vesicles for proteomic analysis Methods in Molecular Biology 528 2009 227 242
58. A. Clayton, H. Navabi, M. Adams, M.D. Mason, J.A. Hobot, and G.R. Newman Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry Journal of Immunological Methods 247 1 2001 163 174 (Pubitemid 32057053)
59. D.D. Taylor, C. Gercel-Taylor, and L.P. Parker Patient-derived tumor reactive antibodies as diagnostic markers for ovarian cancer Gynecologic Oncology 115 1 2009 112 120
60. S.P. Ardoin, J.C. Shanahan, and D.S. Pisetsky The role of microparticles in inflammation and thrombosis Scandinavian Journal of Immunology 66 2-3 2007 159 165 (Pubitemid 47063209)
61. E. Pap, E. Pállinger, A. Falus, A.A. Kiss, A. Kittel, and P. Kovács T lymphocytes are targets for platelet-and trophoblast-derived microvesicles during pregnancy Placenta 29 9 2008 826 832
62. S.J. Germain, G.P. Sacks, S.R. Sooranna, I.L. Sargent, and C.W. Redman Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles Journal of Immunology 178 9 2007 5949 5956 (Pubitemid 46674392)
63. S. Atay, C. Gercel-Taylor, M. Kesimer, and D.D. Taylor Morphologic and proteomic characterization of exosomes released by cultured extravillous trophoblast cells Experimental Cell Research 317 2011 1192 1202
64. R.A. Dragovic, C. Gardiner, A.S. Brooks, D.S. Tannetta, D.J.P. Ferguson, and P. Hole Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis Nanomedicine Nanotechnology, Biology and Medicine 2011 [Ahead of print
65. L.W. Chamley, Q. Chen, J. Ding, P.R. Stone, and M. Abumaree Trophoblast deportation: just a waste disposal system or antigen sharing? Journal of Reproductive Immunology 88 2 2011 99 105
66. W.D. Billington Trophoblast extensions from the placenta Proceedings of the Royal Society of Medicine 63 1 1970 57 59
67. R.E. Billingham, and E.M. Sparrow The effect of prior intravenous injections of dissociated epidermal cells and blood on the survival of skin homografts in rabbits Journal of Embryology and Experimental Morphology 3 3 1955 265 285
68. A. Sabapatha, C. Gercel-Taylor, and D.D. Taylor Specific isolation of placenta-derived exosomes from the circulation of pregnant women and their immunoregulatory consequences American Journal of Reproductive Immunology 56 5-6 2006 345 355 (Pubitemid 44669331)
69. S. Atay, C. Gercel-Taylor, J. Suttles, G. Mor, and D.D. Taylor Trophoblast-derived exosomes Mediate monocyte recruitment and differentiation American Journal of Reproductive Immunology 65 1 2011 65 77
70. S. Atay, C. Gercel-Taylor, and D.D. Taylor Human trophoblast-derived exosomal fibronectin induces pro-inflammatory Il-1 production by macrophages American Journal of Reproductive Immunology 2011 [Ahead of print
71. A.K. Gupta, P. Hasler, W. Holzgreve, S. Gebhardt, and S. Hahn Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia Human Immunology 66 11 2005 1146 1154
72. A. Gupta, P. Hasler, S. Gebhardt, W. Holzgreve, and S. Hahn Occurrence of neutrophil extracellular DNA traps (NETs) in pre-eclampsia: a link with elevated levels of cell-free DNA? Annals of the New York Academy of Sciences 1075 2006 118 122 (Pubitemid 44532773)
73. Z. Kertesz, G. Hurst, M. Ward, A.C. Willis, H. Caro, and E.A. Linton Purification and characterization of a complex from placental syncytiotrophoblast microvillous membranes which inhibits the proliferation of human umbilical vein endothelial cells Placenta 20 1 1999 71 79 (Pubitemid 29039253)
74. Q. Chen, B. Liu, H. Jin, and L. Chamley Phagocytosis of apoptotic syncytial knots prevents endothelial activation: an important adaptation for normal pregnancy (Abstract) Placenta 31 9 2010 A44
75. A.K. Gupta, M.B. Joshi, M. Philippova, P. Erne, P. Hasler, and S. Hahn Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death FEBS Letters 584 14 2010 3193 3197
76. Q. Chen, J.X. Ding, B. Liu, P. Stone, Y.J. Feng, and L. Chamley Spreading endothelial cell dysfunction in response to necrotic trophoblasts. Soluble factors released from endothelial cells that have phagocytosed necrotic shed trophoblasts reduce the proliferation of additional endothelial cells Placenta 31 11 2010 976 981
77. C.J. Jones, and H. Fox An ultrastructural and ultrahistochemical study of the human placenta in maternal pre-eclampsia Placenta 1 1 1980 61 76 (Pubitemid 11240950)
78. B. Huppertz, and J. Kingdom Apoptosis in the trophoblast - role of apoptosis in placental morphogenesis Journal of the Society for Gynecologic Investigation 11 2004 353 362 (Pubitemid 39179889)
79. A.E. Heazell, H.A. Lacey, C.J. Jones, B. Huppertz, P.N. Baker, and I.P. Crocker Effects of oxygen on cell turnover and expression of regulators of apoptosis in human placental trophoblast Placenta 29 2 2008 175 186
80. Q. Chen, X.L. Liversidge, B. Liu, P. Stone, and L.W. Chamley Does oxygen concentration affect shedding of trophoblastic debris or production of inflammatory mediators from first trimester human placenta? Placenta 32 5 2011 362 366
81. Q. Chen, C. Viall, Y. Kang, B. Liu, P. Stone, and L. Chamley Anti-phospholipid antibodies increase non-apoptotic trophoblast shedding: a contribution to the pathogenesis of pre-eclampsia in affected women? Placenta 30 9 2009 767 773
82. E.S. Hutchinson, P. Brownbill, N.W. Jones, V.M. Abrahams, P.N. Baker, and C.P. Sibley Utero-placental haemodynamics in the pathogenesis of pre-eclampsia Placenta 30 7 2009 634 641
83. K.E. Jäämeri, A.P. Koivuniemi, and E.O. Carpén Occurrence of trophoblasts in the blood of toxaemic patients Gynaecologia International Monthly Review of Obstetrics and Gynecology Revue Internationale Mensuelle d'obstétrique et de Gynécologie Monatsschrift für Geburtshilfe und Gynäkologie 160 5 1965 315 320
84. V.M. Abrahams, Y.M. Kim, S.L. Straszewski, R. Romero, and G. Mor Macrophages and apoptotic cell clearance during pregnancy American Journal of Reproductive Immunology 51 4 2004 275 282 (Pubitemid 38455729)
85. A.S. Aly, M. Khandelwal, J. Zhao, A.H. Mehmet, M.D. Sammel, and S. Parry Neutrophils are stimulated by syncytiotrophoblast microvillous membranes to generate superoxide radicals in women with preeclampsia American Journal of Obstetrics and Gynecology 190 1 2004 252 258 (Pubitemid 38156356)