Regulation of proliferation and apoptosis during development of the preimplantation embryo and the placenta

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 75, Issue 4, 2005, Pages 249-261

  Huppertz, Berthold ^a   Herrler, Andreas ^b  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

Apoptosis; Embryo; Fragmentation; Placenta; Preeclampsia; Proliferation; Trophoblast

Indexed keywords

APOPTOSIS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL METABOLISM; CELL PROLIFERATION; CELL TYPE; EMBRYO DEVELOPMENT; FETUS DEVELOPMENT; GENOME; HUMAN; INNER CELL MASS; MORPHOGENESIS; MORULA; NONHUMAN; PLACENTA DEVELOPMENT; PLACENTA VILLUS; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; REVIEW; TROPHOBLAST; ZYGOTE;

ANIMALS; APOPTOSIS; BLASTOCYST; CELL PROLIFERATION; EMBRYONIC DEVELOPMENT; FEMALE; HUMANS; MICE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; STEM CELLS; TROPHOBLASTS;

EID: 32644452163     PISSN: 1542975X     EISSN: None     Source Type: Journal    
DOI: 10.1002/bdrc.20056     Document Type: Review

References (110)

1. Allaire AD, Ballenger KA, Wells SR, et al. 2000. Placental apoptosis in preeclampsia. Obstet Gynecol 96:271-276.
2. Anson-Cartwright L, Dawson K, Holmyard D, et al. 2000. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 25:311-314.
3. Arnholdt H, Meisel F, Fandrey K, et al. 1991. Proliferation of villous trophoblast of the human placenta in normal and abnormal pregnancies. Virchows Arch B Cell Pathol Incl Mol Pathol 60:365-372.
4. Baczyk D, Satkunaratnam A, Nait-Oumesmar B, et al. 2004. Complex patterns of GCM1 mRNA and protein in villous and extravillous trophoblast cells of the human placenta. Placenta 25:553-559.
5. Baczyk D, Dunk C, Huppertz B, et al. Bi-potential behaviour of cytotrophoblasts in first trimester chorionic villi. Placenta [Epub ahead of print] PMID: 15950280.
6. Baserga R, Sell C, Porcu P, et al. 1994. The role of the IGF-I receptor in the growth and transformation of mammalian cells. Cell Prolif 27:63-71.
7. Behr B, Moortey S, Wen Y, et al. 2005. Preliminary experience with low concentration of granulocyte-macrophage colony-stimulating factor: a potential regulator in preimplantation mouse embryo development and apoptosis. J Assist Reprod Genet 22:25-32.
8. Benirschke K, Kaufmann P. 2000. Pathology of the human placenta. 4th ed. New York: Springer.
9. Black S, Kadyrov M, Kaufmann P, et al. 2004. Syncytial fusion of human trophoblast depends on caspase 8. Cell Death Differ 11:90-98.
10. Boyd JD, Hamilton WJ. 1970. The human placenta. Cambridge: Heffer and Sons.
11. Braude P, Bolton V, Moore S. 1988. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332:459-461.
12. Brison DR, Schultz RM. 1997. Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol Reprod 56:1088-1096.
13. Buster JE, Bustillo M, Rodi IA, et al. 1985. Biologic and morphologic development of donated human ova recovered by nonsurgical uterine lavage. Am J Obstet Gynecol 153:211-217.
14. Butt AJ, Firth SM, Baxter RC. 1999. The IGF axis and programmed cell death. Immunol Cell Biol 77:256-262.
15. Chia CM, Winston RM, Handyside AH. 1995. EGF, TGF-alpha and EGFR expression in human preimplantation embryos. Development 121:299-307.
16. Cohle SD, Petty CS. 1985. Sudden death caused by embolization of trophoblast from hydatidiform mole. J Forensic Sci 30:1279-1283.
17. Cronier L, Defamie N, Dupays L, et al. 2002. Connexin expression and gap junctional intercellular communication in human first trimester trophoblast. Mol Hum Reprod 8:1005-1013.
18. Cross JC, Baczyk D, Dobric N, et al. 2003. Genes, development and evolution of the placenta. Placenta 24:123-130.
19. Dawson KJ, Conaghan J, Ostera GR, et al. 1995. Delaying transfer to the third day post-insemination, to select non-arrested embryos, increases development to the fetal heart stage. Hum Reprod 10:177-182.
20. Delmis J, Pfeifer D, Ivanisevic M, et al. 2000. Sudden death from trophoblastic embolism in pregnancy. Eur J Obstet Gynecol Reprod Biol 92:225-227.
21. Devreker F, Englert Y. 2000. In vitro development and metabolism of the human embryo up to the blastocyst stage. Eur J Obstet Gynecol Reprod Biol 92:51-56.
22. Erel CT, Dane B, Calay Z, et al. 2001. Apoptosis in the placenta of pregnancies complicated with IUGR. Int J Gynaecol Obstet 73:229-235.
23. Exley GE, Tang C, McElhinny AS, et al. 1999. Expression of caspase and BCL-2 apoptotic family members in mouse preimplantation embryos. Biol Reprod 61:231-239.
24. Fabian D, Koppel J, Maddox-Hyttel P. 2005. Apoptotic processes during mammalian preimplantation development. Theriogenol 64:221-231.
25. Formigli L, Papucci L, Tani A, et al. 2000. Aponecrosis: morphological and biochemical exploration of a syncretic process of cell death sharing apoptosis and necrosis. J Cell Physiol 182:41-49.
26. Frisch SM, Francis H. 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124:619-626.
27. Gardner DK, Lane M. 1997. Culture and selection of viable blastocysts: a feasible proposition for human IVF? Hum Reprod Update 3:367-382.
28. Giorgetti C, Terriou P, Auquier P, et al. 1995. Embryo score to predict implantation after in-vitro fertilization: based on 957 single embryo transfers. Hum Reprod 10:2427-2431.
29. Gjorret JO, Knijn HM, Dieleman SJ, et al. 2003. Chronology of apoptosis in bovine embryos produced in vivo and in vitro. Biol Reprod 69:1193-1200.
30. Gobe G, Zhang XJ, Cuttle L, et al. 1999. Bcl-2 genes and growth factors in the pathology of ischaemic acute renal failure. Immunol Cell Biol 77:279-286.
31. Gorbe A, Becker DL, Dux L, et al. 2005. Transient upregulation of connexin43 gap junctions and synchronized cell cycle control precede myoblast fusion in regenerating skeletal muscle in vivo. Histochem Cell Biol 123:573-583.
32. Greenberg JT. 1996. Programmed cell death: a way of life for plants. Proc Natl Acad Sci USA 93:12094-12097.
33. Guilbert LJ, Winkler-Lowen B, Sherburne R, et al. 2002. Preparation and functional characterization of villous cytotrophoblasts free of syncytial fragments. Placenta 23:175-183.
34. Gutierrez-Adan A, Rizos D, Fair T, et al. 2004. Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. Mol Reprod Dev 68:441-448.
35. Hammerman MR. 1998. Growth factors and apoptosis in acute renal injury. Curr Opin Nephrol Hypertens 7:419-424.
36. Handyside AH, Hunter S. 1986. Cell division and death in the mouse blastocyst before implantation. Roux's Arch Dev Biol 195:519-526.
37. Hardy K, Handyside AH, Winston RM. 1989. The human blastocyst: cell number, death and allocation during late preimplantation development in vitro. Development 107:597-604.
38. Hardy K. 1993. Development of human blastocysts in vitro. In: Bavister BD, editor. Preimplantation embryo development. New York: Springer, pp. 184-199.
39. Hardy K. 1999. Apoptosis in the human embryo. Rev Reprod 4:125-134.
40. Hardy K, Spanos S. 2002. Growth factor expression and function in the human and mouse preimplantation embryo. J Endocrinol 172:221-236.
41. Hardy K, Stark J, Winston RM. 2003. Maintenance of the inner cell mass in human blastocysts from fragmented embryos. Biol Reprod 68:1165-1169.
42. Herrler A, Einspanier R, Beier HM. 1997. Binding of IGF-I to preimplantation rabbit embryos and their coats. Theriogenol 47:1595-1607.
43. Herrler A, Krusche CA, Beier HM. 1998. Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis. Biol Reprod 59:1302-1310.
44. Hertig AT, Rock J, Adams EC, et al. 1954. On the preimplantation stages of the human ovum: a description of four normal and four abnormal specimens ranging from the second to fifth day of development. Contrib Embryol 35:199-220.
45. Huang RP, Wu JX, Fan Y, et al. 1996. UV activates growth factor receptors via reactive oxygen intermediates. J Cell Biol 133:211-220.
46. Huang FJ, Shen CC, Chang SY, et al. 2003. Retinoic acid decreases the viability of mouse blastocysts in vitro. Hum Reprod 18:130-136.
47. Huang FJ, Hsu YC, Kang HY, et al. 2005. Effects of retinoic acid on the inner cell mass in mouse blastocysts. Fertil Steril 83:238-242.
48. Hughes M, Dobric N, Scott IC, et al. 2004. The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev Biol 271:26-37.
49. Human Fertilisation and Embryology Authority. 2000. Ninth annual report. London: Paxton House.
50. Huppertz B, Frank HG, Kingdom JC, et al. 1998. Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem Cell Biol 110:495-508.
51. Huppertz B, Frank HG, Reister F, et al. 1999. Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab Invest 79:1687-1702.
52. Huppertz B, Kaufmann P, Kingdom J. 2002. Trophoblast turnover in health and disease. Fetal Maternal Med Rev 13:103-118.
53. Huppertz B, Kingdom J, Caniggia I, et al. 2003. Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotrophoblast into the maternal circulation. Placenta 24:181-190.
54. Huppertz B, Kingdom JC. 2004. Apoptosis in the trophoblast-role of apoptosis in placental morphogenesis. J Soc Gynecol Invest 11:353-362.
55. Ikle FA. 1964. Trophoblastzellen im strömenden Blut. Schweiz Med Wochenschr 91:934-945.
56. Ishihara N, Matsuo H, Murakoshi H, et al. 2002. Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am J Obstet Gynecol 186:158-166.
57. Jacobson MD, Weil M, Raff MC. 1997. Programmed cell death in animal development. Cell 88:347-354.
58. Janatpour MJ, Utset MF, Cross JC, et al. 1999. A repertoire of differentially expressed transcription factors that offers insight into mechanisms of human cytotrophoblast differentiation. Dev Genet 25:146-157.
59. Jeong SY, Gaume B, Lee YJ, et al. 2004. Bcl-x(L) sequesters its C-terminal membrane anchor in soluble, cytosolic homodimers. EMBO J 23:2146-2155.
60. Johansen M, Redman CW, Wilkins T, et al. 1999. Trophoblast deportation in human pregnancy-its relevance for pre-eclampsia. Placenta 20:531-539.
61. Jurisicova A, Rogers I, Fasciani A, et al. 1998. Effect of maternal age and conditions of fertilization on programmed cell death during murine preimplantation embryo development. Mol Hum Reprod 4:139-145.
62. Jurisicova A, Antenos M, Varmuza S, et al. 2003. Expression of apoptosis-related genes during human preimplantation embryo development: potential roles for the Harakiri gene product and caspase-3 in blastomere fragmentation. Mol Hum Reprod 9:133-141.
63. Kadyrov M, Kaufmann P, Huppertz B. 2001. Expression of a cytokeratin 18 neo-epitope is a specific marker for trophoblast apoptosis in human placenta. Placenta 22:44-48.
64. Kamoi S, Ohaki Y, Mori O, et al. 2003. Placental villotrophoblastic pulmonary emboli after elective abortion: immunohistochemical diagnosis and comparison with ten control cases. Int J Gynecol Pathol 22:303-309.
65. Kane MT, Morgan PM, Coonan C. 1997. Peptide growth factors and preimplantation development. Hum Reprod Update 3:137-157.
66. Kanfer A, Bruch JF, Nguyen G, et al. 1996. Increased placental antifibrinolytic potential and fibrin deposits in pregnancy-induced hypertension and preeclampsia. Lab Invest 74:253-258.
67. Kawamura K, Fukuda J, Kodama H, et al. 2001. Expression of Fas and Fas ligand mRNA in rat and human preimplantation embryos. Mol Hum Reprod 7:431-436.
68. Kerr JF, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257.
69. Kitagawa Y, Suzuki K, Yoneda A, et al. 2004. Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62:1186-1197.
70. Kliman HJ, Nestler JE, Sermasi E, et al. 1986. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118:1567-1582.
71. Knight M, Redman CW, Linton EA, et al. 1998. Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br J Obstet Gynaecol 105:632-640.
72. Knijn HM, Gjorret JO, Vos PL, et al. 2003. Consequences of in vivo development and subsequent culture on apoptosis, cell number, and blastocyst formation in bovine embryos. Biol Reprod 69:1371-1378.
73. Kölle S, Stojkovic M, Boie G, et al. 2003. Growth hormone-related effects on apoptosis, mitosis, and expression of connexin 43 in bovine in vitro maturation cumulus-oocyte complexes. Biol Reprod 68:1584-1589.
74. Kunath T, Strumpf D, Rossant J. 2004. Early trophoblast determination and stem cell maintenance in the mouse: a review. Placenta 25:S32-S38.
75. Kurzawa R, Glabowski W, Baczkowski T, et al. 2002. Evaluation of mouse preimplantation embryos exposed to oxidative stress cultured with insulin-like growth factor I and II, epidermal growth factor, insulin, transferrin and selenium. Reprod Biol 2:143-162.
76. Kurzawa R, Glabowski W, Baczkowski T, et al. 2004. Growth factors protect in vitro cultured embryos from the consequences of oxidative stress. Zygote 12:231-240.
77. Lee W, Ginsburg KA, Cotton DB, et al. 1986. Squamous and trophoblastic cells in the maternal pulmonary circulation identified by invasive hemodynamic monitoring during the peripartum period. Am J Obstet Gynecol 155:999-1001.
78. Lighten AD, Moore GE, Winston RM, et al. 1998. Routine addition of human insulin-like growth factor-I ligand could benefit clinical in-vitro fertilization culture. Hum Reprod 13:3144-3150.
79. Liu L, Trimarchi JR, Keefe DL. 2002. Haploidy but not parthenogenetic activation leads to increased incidence of apoptosis in mouse embryos. Biol Reprod 66:204-210.
80. Lonergan P, Rizos D, Gutierrez-Adan A, et al. 2003. Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol Reprod 69:1424-1431.
81. Lunetta P, Penttila A. 1996. Immunohistochemical identification of syncytiotrophoblastic cells and megakaryocytes in pulmonary vessels in a fatal case of amniotic fluid embolism. Int J Legal Med 108:210-214.
82. Luz NP, Crottogini JJ, Negrete VS. 1966. A method for identification of chorionic villi in peripheral blood of pregnant women. Am J Obstet Gynecol 94:1079-1084.
83. Ma W, Zhang D, Hou Y, et al. 2005. Reduced expression of MAD2, BCL2, and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biol Reprod 72:373-383.
84. Majno G, Joris I. 1995. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146:3-15.
85. Martin SJ, Reutelingsperger CP, McGahon AJ, et al. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182:1545-1556.
86. Mayhew TM, Leach L, McGee R, et al. 1999. Proliferation, differentiation and apoptosis in villous trophoblast at 13-41 weeks of gestation (including observations on annulate lamellae and nuclear pore complexes). Placenta 20:407-422.
87. Metcalfe AD, Hunter HR, Bloor DJ, et al. 2004. Expression of 11 members of the BCL-2 family of apoptosis regulatory molecules during human preimplantation embryo development and fragmentation. Mol Reprod Dev 68:35-50.
88. Muggleton-Harris AL, Brown JJ. 1988. Cytoplasmic factors influence mitochondrial reorganization and resumption of cleavage during culture of early mouse embryos. Hum Reprod 3:1020-1028.
89. Mühlhauser J, Crescimanno C, Kaufmann P, et al. 1993. Differentiation and proliferation patterns in human trophoblast revealed by c-erbB-2 oncogene product and EGF-R. J Histochem Cytochem 41:165-173.
90. Munné S, Weier HU, Grifo J, et al. 1994. Chromosome mosaicism in human embryos. Biol Reprod 51:373-379.
91. Nelson DM. 1996. Apoptotic changes occur in syncytiotrophoblast of human placental villi where fibrin type fibrinoid is deposited at discontinuities in the villous trophoblast. Placenta 17:387-391.
92. Pollard JW. 1997. Role of colony-stimulating factor-1 in reproduction and development. Mol Reprod Dev 46:54-60.
93. Redman CW, Sargent IL. 2004. Preeclampsia and the systemic inflammatory response. Semin Nephrol 24:565-570.
94. Rock JA, Zacur HA. 1983. The clinical management of repeated early pregnancy wastage. Fertil Steril 39:123-140.
95. Roudabush FL, Pierce KL, Maudsley S, et al. 2000. Transactivation of the EGF receptor mediates IGF-1-stimulated Shc phosphorylation and ERK1/2 activation in COS-7 cells. J Biol Chem 275:22583-22589.
96. Sjoblom C, Wikland M, Robertson SA. 2002. Granulocyte-macrophage colony-stimulating factor (GM-CSF) acts independently of the beta common subunit of the GM-CSF receptor to prevent inner cell mass apoptosis in human embryos. Biol Reprod 67:1817-1823.
97. Smith SC, Baker PN, Symonds EM. 1997. Increased placental apoptosis in intrauterine growth restriction. Am J Obstet Gynecol 177:1395-1401.
98. Smotrich DB, Stillman RJ, Widra EA, et al. 1996. Immunocytochemical localization of growth factors and their receptors in human pre-embryos and Fallopian tubes. Hum Reprod 11:184-190.
99. Spanos S, Becker DL, Winston RM, et al. 2000. Anti-apoptotic action of insulin-like growth factor-I during human preimplantation embryo development. Biol Reprod 63:1413-1420.
100. Spanos S, Rice S, Karagiannis P, et al. 2002. Caspase activity and expression of cell death genes during development of human preimplantation embryos. Reproduction 124:353-363.
101. Stecca B, Nait-Oumesmar B, Kelley KA, et al. 2002. Gcm1 expression defines three stages of chorio-allantoic interaction during placental development. Mech Dev 115:27-34.
102. Tanaka S, Kunath T, Hadjantonakis AK, et al. 1998. Promotion of trophoblast stem cell proliferation by FGF4. Science 282:2072-2075.
103. Telford NA, Watson AJ, Schultz GA. 1990. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26:90-100.
104. van Blerkom J, Davis P, Alexander S. 2001. A microscopic and biochemical study of fragmentation phenotypes in stage-appropriate human embryos. Hum Reprod 16:719-729.
105. van den Eijnde SM, Boshart L, Baehrecke EH, et al. 1998. Cell surface exposure of phosphatidylserine during apoptosis is phylogenetically conserved. Apoptosis 3:9-16.
106. Wells D, Bermudez MG, Steuerwald N, et al. 2005. Expression of genes regulating chromosome segregation, the cell cycle and apoptosis during human preimplantation development. Hum Reprod 20:1339-1348.
107. Yang MY, Rajamahendran R. 2002. Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim Reprod Sci 70:159-169.
108. Zushi S, Shinomura Y, Kiyohara T, et al. 1998. STAT3 mediates the survival signal in oncogenic ras-transfected intestinal epithelial cells. Int J Cancer 78:326-330.
109. Zybina TG, Kaufmann P, Frank HG, et al. 2002. Genome multiplication of extravillous trophoblast cells in human placenta in the course of differentiation and invasion into endometrium and myometrium. I. Dynamics of polyploidization. Tsitologiia 44:1058-1067.
110. Zybina TG, Frank HG, Biesterfeld S, et al. 2004. Genome multiplication of extravillous trophoblast cells in human placenta in the course of differentiation and invasion into endometrium and myometrium. II. Mechanisms of polyploidization. Tsitologiia 46:640-648.