To be, or not to be, that is the question. Apoptosis in human trophoblast

Placenta

Volumn 21, Issue 1, 2000, Pages 1-13

  Levy, R ^a   Nelson, D M ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BARNES JEWISH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; PROTEIN BCL 2;

APOPTOSIS; FEMALE; FETUS; HUMAN; PLACENTA VILLUS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TROPHOBLAST;

EID: 0033954382     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1053/plac.1999.0450     Document Type: Editorial

References (115)

1. Adams J.M., Cory S. The Bcl-2 protein family: arbiters of cell survival. Science. 281:1998;1322-1326.
2. Ashkenazi A., Dixit V.M. Death receptors: signaling and modulation. Science. 281:1998;1305-1308.
3. Baker S.J., Reddy E.P. Modulation of life and death by the TNF receptor superfamily. Oncogene. 17:1998;3261-3270.
4. Baldwin A.S. Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol. 14:1996;649-683.
5. Bamberger A-M, Schulte H.M., Thuneke I., Erdmann I., Bamberger C.M., Asa S.L. Expression of the apoptosis-inducing Fas ligand (FasL) in human first and third trimester placenta and choriocarcinoma cells. J Clin Endocrinol Metab. 82:1997;3173-3175.
6. L , decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad Sci U S A. 96:1999;5492-5497.
7. Bellgrau D., Gold D., Selawry H., Moore J., Franzusoff A., Duke R.C. A role for CD95 ligand in preventing graft rejection. Nature. 377:1995;630-632.
8. Braun J.S., Kovak R., Herzog K-H, Bodner S.M., Cleveland J.L., Tuomanen E.I. Neuroprotection by a caspase inhibitor in acute bacterial meningitis. Nature Med. 5:1999;298-302.
9. Bulmer J.N., Morrison L., Johnson P.M., Meager A. Immunohistochemical localization of interferons in human placental tissues in normal, ectopic and molar pregnancies. Am J Reprod Immunol. 22:1990;109-116.
10. Cecconi F., Alvarez-Bolado G., Meyer B.I., Roth K.A., Gruss P. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell. 94:1998;727-737.
11. Chan C.C.W., Lao T.T., Cheung A.N.Y. Apoptotic and proliferative activities in first trimester placentae. Placenta. 20:1999;223-227.
12. Chen H-L, Yang Y., Hu X-L, Yelavarthi K.K., Fishback J.L., Hunt J.S. Tumor necrosis factor alpha mRNA and protein are present in human placental and uterine cells at early and late stages of gestation. Am J Pathol. 139:1991;327-335.
13. Cheng Y., Deshmukh M., D'Costa A., Demaro J.A., Gidday J.M., Shah A., Sun Y., Jacquin M.F., Johnson E.M. Jr, Holtzman D.M. Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury. J Clin Invest. 101:1998;1992-1999.
14. Cheung A.N.Y., Srivastava G., Chung L.P., Ngan H.Y.S., Man T.K., Liu Y.T., Chen W.Z., Collins R.J., Wong L.C., Ma H.K. Expression of the p-53 gene in trophoblastic cells in hydatiform moles and normal human placentas. J Reprod Med. 39:1994;223-227.
15. Cheville J.C., Robinson R.A., Benda J.A. P53 expression in placentas with hydropic change and hydatidiform moles. Mod Pathol. 9:1996;392-396.
16. Chou J.J., Li H., Salvesen G.S., Yuan J., Wagner G. Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell. 96:1999;615-624.
17. Cohen G.M. Caspases: the executioners of apoptosis. Biochem J. 326:1997;1-16.
18. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 91:1997;231-241.
19. Deveraux Q.L., Reed J.C. IAP family proteins - suppressors of apoptosis. Genes Dev. 13:1999;239-252.
20. DiFederico E., Genbacev O., Fisher S.J. Preeclampsia is associated with widespread apoptosis of placental cytotrophoblasts within the uterine wall. Am J Pathol. 155:1999;293-301.
21. Di Leonardo A., Linke S.P., Clarkin K., Wahl G.M. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev. 8:1994;2540-2551.
22. Eades D.K., Cornelius P., Pekala P.H. Characterization of the tumor necrosis factor receptor in human placenta. Placenta. 9:1988;247-251.
23. Fulop V., Mok S.C., Genest D.R., Gati I., Doszpod J., Berkowitz R.S. p53, p21, Rb and mdm2 oncoproteins: expression in normal placenta, partial and complete mole, and choriocarcinoma. J Reprod Med. 43:1998;119-127.
24. Gajewski T.F., Thompson C.B. Apoptosis meets signal transduction: elimination of a BAD influence. Cell. 87:1996;589-592.
25. Garcia-Lloret M.I., Yui J., Winkler-Lowen B., Guilbert L.J. Epidermal growth factor inhibits cytokine-induced apoptosis of primary human trophoblasts. J Cell Phys. 167:1996;324-332.
26. Gervais F.G., Thornberry N.A., Ruffolo S.C., Nicholson D.W., Roy S. Caspases cleave focal adhesion kinase during apoptosis to generate a FRNK-like polypeptide. J Biol Chem. 273:1998;17 102-17 108.
27. Gottlieb T.M., Oren M. P53 and apoptosis. Semin Cancer Biol. 8:1998;359-368.
28. Graeber T.G., Osmanian C., Jacks T., Housman D.E., Koch C.J., Lowe S.W., Giaccia A.J. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature. 379:1996;88-91.
29. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
30. Griffith T.S., Brunner T., Fletcher S.M., Green D.R., Ferguson T.A. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science. 270:1995;1189-1192.
31. Gross A., Jockel J., Wei M.C., Korsmeyer S.J. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17:1998;3878-3885.
32. Hale A.J., Smith C.A., Sutherland L.C., Stoneman V.E.A., Longthorne V.L., Culhane A.C., Williams G.T. Apoptosis: molecular regulation of cell death. Eur J Biochem. 236:1996;1-26.
33. Hammer A., Blaschitz A., Daxbock C., Walcher W., Dohr G. Fas and Fas-ligand are expressed in the uteroplacental unit of first-trimester pregnancy. Am J Reprod Immunol. 41:1999;41-51.
34. Harris A.L. Mutant p53: the commonest genetic abnormality in human cancer? J Pathol. 162:1990;5-6.
35. Hetts S.W. To die or not to die. An overview of apoptosis and its role in disease. JAMA. 279:1998;300-307.
36. Hockenbery D., Nuñez G., Milliman C., Schrieber R.D., Korsmeyer S.J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature. 348:1990;334-336.
37. Hockenbery D.M., Zutter M., Hickey W., Nahm M., Korsmeyer S.J. Bcl-2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl Acad Sci U S A. 88:1991;6961-6965.
38. Hofmann K., Bucher P., Tschopp J. The CARD domain: a new apoptotic signalling motif. Trends Biochem Sci. 22:1997;155-156.
39. Hu S., Snipas S.J., Vincenz C., Salvesen G., Dixit V.M. Caspase-14 is a novel developmentally regulated protease. J Biol Chem. 273:1998;29 648-29 653.
40. Hunt J.S., Vassmer D., Ferguson T.A., Miller L. Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J Immunol. 158:1997;4122-4128.
41. Huppertz B., Frank H-G, Kingdom J.C.P., Reister F., Kaufmann P. Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem Cell Biology. 110:1998;495-508.
42. Inohara N., Gourley T.S., Carrio R., Muñiz M., Merino J., Garcia I., Koseki T., Hu Y., Chen S., Nuñez G. Diva, a Bcl-2 homologue that binds directly to Apaf-1 and induces BH3-independent cell death. J Biol Chem. 273:1998;32 479-32 486.
43. Irmler M., Thome M., Hahne M., Schneider P., Hofmann K., Steiner V., Bodmer J.L., Schroter M., Burns K., Mattmann C., Rimoldi D., French L.E., Tschopp J. Inhibition of death receptor signals by cellular FLIP. Nature. 388:1997;190-195.
44. Kaplan H.J., Leibole M.A., Tezel T., Ferguson T.A. Fas ligand (CD95 ligand) controls angiogenesis beneath the retina. Nature Med. 5:1999;292-297.
45. Kaufmann S.H., Desnoyers S., Ottaviano Y., Davidson N.E., Poirier G. Specific proteolytic cleavage of poly (ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53:1993;3976-3985.
46. Kerr J.F.R., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide ranging implications in tissue kinetics. Br J Cancer. 26:1972;239-257.
47. Kingdom J.C.P., Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta. 18:1997;613-621.
48. Kitson J., Raven T., Jiang Y-P, Goeddel D.V., Giles K.M., Pun K-T, Grinham C.J., Brown R., Farrow S.N. A death-domain-containing receptor that mediates apoptosis. Nature. 384:1996;372-375.
49. Knudson C.M., Tung K., Tourtelloffe W.G., Brown G., Korsmeyer S.J. Bax deficient mice with lymphoid hyperplasia and male germ cell death. Science. 270:1995;96-99.
50. Ko L.J., Prives C. p53: puzzle and paradigm. Genes Dev. 10:1996;1054-1072.
51. Kokawa K., Shikone T., Nakano R. Apoptosis in human chorionic villi and decidua during normal embryonic development and spontaneous abortion in the first trimester. Placenta. 19:1998a;21-26.
52. Kokawa K., Shikone T., Nakano R. Apoptosis in human chorionic villi and decidua in normal and ectopic pregnancy. Molecular Hum Reprod. 4:1998b;87-91.
53. Kothakota S., Azuma T., Reinhard C., Klippel A., Tang J., Chu K., McGarry T.J., Kirschner M.W., Koths K., Kwiatkowski D.J., Williams L.T. Caspase 3-generated fragment of gelsolin: Effector of morphological change in apoptosis. Science. 278:1997;294-298.
54. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med. 3:1997;614-620.
55. Kuida K., Zheng T.S., Na S., Kuan C., Yang D., Arasuyama H., Rakic P., Flavell R.A. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature. 384:1996;368-372.
56. Kuida K., Haydar T.F., Kuan C-Y, Gu Y., Taya C., Karasuyama H., Su MS-S, Rakic P., Flavell R.A. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell. 94:1998;325-337.
57. Lee N., MacDonald H., Reinhard C., Halenbeck R., Roulston A., Shi T., Williams L.T. Activation of hPAK65 by caspase cleavage induces some of the morphological and biochemical changes of apoptosis. Proc Natl Acad Sci U S A. 94:1997;13 642-13 647.
58. Li H., Zhu H., Xu C-J, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
59. Li P., Allen H., Banerjee S., Franklin S., Herzog L., Johnston C., McDowell J., Paskind M., Rodman L., Salfeld J. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell. 80:1995;401-411.
60. Liu X., Zou H., Slaughter C., Wang X. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell. 89:1997;175-184.
61. Linnik M.D., Zobrist R.H., Hatfield M.D. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke. 24:1993;2002-2009.
62. Lyden T.W., NG A-K, Rote N.S. Modulation of phosphatidylserine epitope expression by BeWo cells during forskolin treatment. Placenta. 14:1993;177-186.
63. Martin S.J., Reutelingsperger C.P.M., McGahon A.J., Rader J.A., van Schie RCCA, LaFace D.M., Green D.R. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Ab1. J Exp Med. 182:1995;1545-1556.
64. Marzioni D., Mühlhauser J., Crescimanno C., Banita M., Pierleoni C., Castellucci M. Bcl-2 expression in the human placenta and its correlation with fibrin deposits. Human Reprod. 13:1998;1717-1722.
65. Mayhew T.M., Leach L., McGee R., Ismail W.W., Myklebust R., Lammiman M.J. Proliferation, differentiation and apoptosis in villous trophoblast at 13-41 weeks of gestation (including observations on annulate lamellae and nuclear pore complexes). Placenta. 20:1999;407-422.
66. McDonnell J.M., Fushman D., Milliman C.L., Korsmeyer S.J., Cowburn D. Solution structure of the proapoptotic molecule BID: A structural basis for apoptotic agonists and antagonists. Cell. 96:1999;625-634.
67. McPherson J.P., Goldenberg G.J. Induction of apoptosis by deregulated expression of DNA topoisomerase II alpha. Cancer Res. 58:1998;4519-4524.
68. XL acts downstream of Caspase-8 activation by the CD95 death-inducing signaling complex. J Biol Chem. 273:1998;3388-3398.
69. Messam C.A., Pittman R.N. Asynchrony and commitment to die during apoptosis. Exp Cell Res. 238:1998;389-398.
70. Miller M.J., Voelker C.A., Olister S., Thompson J.H., Zhang X.J., Rivera D., Eloby-Childress S., Liu X., Clark D.A., Pierce M.R. Fetal growth retardation in rats may result from apoptosis: role of peroxynitrite. Free Radic Biol Med. 21:1996;619-629.
71. Miyashita T., Reed J.C. Tumor suppressor p53 is a direct transcriptional activator of the human Bax gene. Cell. 80:1995;293-299.
72. Mor G., Gutierrez L.S., Eliza M., Kahyaoglu F., Arici A. Fas-Fas ligand system-induced apoptosis in human placenta and gestational trophoblastic disease. Am J Reprod Immunol. 402:1998;89-94.
73. Motoyama N., Wang F.P., Roth K.A., Sawa H., Nakayama K., Nakayama K., Negishi I., Senju S., Zhang Q., Fujii S., Loh D.Y. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science. 267:1995;1506-1510.
74. Muzio M., Stockwell B.R., Stennicke H.R., Salvesen G.S., Dixit V.M. An induced proximity model for caspase-8 activation. J Biol Chem. 273:1998;2926-2930.
75. Nagata S. Apoptosis by death factor. Cell. 88:1997;355-365.
76. Nagata S., Goldstein P. The Fas death factor. Science. 267:1995;1449-1456.
77. Nakajima T., Morita K., Ohi N., Arai T., Nozaki N., Kikuchi N., Osaka F., Yamao F., Oda K. Degradation of topoisomerase II alpha during adenovirus EIA-induced apoptosis is mediated by the activation of the ubiquitin proteolysis system. J Biol Chem. 271:1996;24 842-24 849.
78. Nelson D.M. Apoptotic changes occur in syncytiotrophoblast of human placental villi where fibrin type fibrinoid is deposited at discontinuities in the villous trophoblast. Placenta. 17:1996;387-391.
79. Nicholson D.W., Thornberry N.A. Caspases: killer proteases. Trends Biochem Sci. 8:1997;299-306.
80. Oltvai Z.N., Milliman C.L., Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell. 74:1993;609-619.
81. Oren M. Relationship of p53 to the control of apoptotic cell death. Semin Cancer Biol. 5:1994;221-227.
82. Pan G., Bauer J.H., Haridas V., Wang S., Liu D., Yu G., Vincenz C., Aggarwal B.B., Ni J., Dixit V.M. Identification and functional characterization of DR6, a novel death domain-containing TNF receptor. FEBS Lett. 431:1998;351-356.
83. Payne S.G., Smith S.C., Davidge S.T., Baker P.N., Guilbert L.J. Death receptor Fas/Apo-1/CD95 expressed by human placental cytotrophoblasts does not mediate apoptosis. Biol Reprod. 60:1999;1144-1150.
84. Polyak K., Xia Y., Zweier J.L., Kinzler K.W., Vogelstein B. A model for p53-induced apoptosis. Nature. 389:1997;300-305.
85. Qiao S., Nagasaka T., Harada T., Nakashima N. p53, Bax and Bcl-2 expression, and apoptosis in gestational trophoblast of complete hydatidiform mole. Placenta. 19:1998;361-369.
86. Rao L., Perez D., White E. Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol. 135:1996;1441-1455.
87. Reed J.C. Cytochrome c: Can't live with it - can't live without it (comment). Cell. 91:1997;559.
88. Rudin C.M., Thompson C.B. Apoptosis and disease: regulation and clinical relevance of programmed cell death. Annu Rev Med. 48:1997;267-281.
89. Runic R., Lockwood C.J., Ma Y., Dipasquale B., Guller S. Expression of Fas ligand by human cytotrophoblasts: implications in placentation and fetal survival. J Clin Endocrinol Metab. 81:1996;3119-3122.
90. Sakahira H., Enari M., Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degredation during apoptosis. Nature. 392:1998;96-99.
91. Sakuragi N., Matsuo H., Coukos G., Furth E.E., Bronner M.P., VanArsdale C.M., Krajewsky S., Reed J.C., Strauss III J.F. Differentiation-dependent expression of the BCL-2 proto-oncogene in the human trophoblast lineage. J Soc Gynecol Invest. 1:1994;164-172.
92. Salvesen G.S., Dixit V.M. Caspases: Intracellular signaling by proteolysis. Cell. 91:1997;443-446.
93. Sata M., Walsh K. Endothelial cell apoptosis induced by oxidized LDL is associated with the down-regulation of the cellular caspase inhibitor FLIP. J Biol Chem. 273:1998;33 103-33 106.
94. Satoh M.S., Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature. 26:1992;356-358.
95. Shi Y-F, Xie X., Zhao C-L, Ye D-F, Lu S-M, Hor J.J., Pao C.C. Lack of mutation in tumour-suppressor gene p53 in gestational trophoblastic tumors. Br J Cancer. 73:1996;1216-1219.
96. Savill J., Fadok V., Henson P., Haslett C. Phagocyte recognition of cells undergoing apoptosis. Immunol Today. 14:1993;131-136.
97. Smith S.C., Baker P.N., Symonds E.M. Placental apoptosis in normal human pregnancy. Am J Obstet Gynecol. 177:1997a;57-65.
98. Smith S.C., Baker P.N., Symonds E.M. Increased placental apoptosis in intrauterine growth restriction. Am J Obstet Gynecol. 177:1997b;1395-1401.
99. Smith S.C., Guilbert L.J., Yui J., Baker P.N., Davidge S.T. The role of reactive nitrogen/oxygen intermediates in cytokine-induced trophoblast apoptosis. Placenta. 20:1999;309-315.
100. Smyth M.J., Obeid L.M., Hannun Y.A. Ceramide: A novel lipid mediator of apoptosis. Adv Pharmacol. 41:1997;133-153.
101. Takayama S., Sato T., Krajewski S., Kochel K., Irie S., Millan J.A., Reed J.C. Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell. 80:1995;279-284.
102. Thornberry N.A., Lazebnik Y. Caspases: enemies within. Science. 281:1998;1312-1316.
103. Toki T., Horiuchi A., Ichikawa N., Mori A., Nikaido T., Fujii S. Inverse relationship between apoptosis and Bcl-2 expression in syncytiotrophoblast and fibrin-type fibrinoid in early gestation. Mol Human Reprod. 5:1999;246-251.
104. Uckan D., Steele A., Wang B-Y, Chamizo W., Koutsonikolis A., Gilbert-Barness E., Good R.A. Trophoblasts express Fas ligand: a proposed mechanism for immune privilege in placenta and maternal invasion. Mol Hum Reprod. 3:1997;655-662.
105. Vaux D.L., Korsmeyer S.J. Cell death in development. Cell. 96:1999;245-254.
106. Veis D.V., Sorenson C.M., Shutter J.R., Korsmeyer S.J. Bcl-2 deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell. 75:1993;229-240.
107. Wen L-P, Fahrni J.A., Troie S., Guan J-L, Orth K., Rosen G.D. Cleavage of focal adhesion kinase by caspases during apoptosis. J Biol Chem. 10:1997;26 056-26 061.
108. Wyllie A.H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 284:1980;555-556.
109. Yasuda M., Kawai K., Serizawa A., Tang X., Osamura R.Y. Immunohistochemical analysis of expression of p53 protein in normal placentas and trophoblastic diseases. Appl Immunohistochem. 3:1995a;132-136.
110. Yoshida H., Kong Y-Y, Yoshida R., Elia A.J., Hakem A., Hakem R., Penninger J.M., Mak T.W. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell. 94:1998;739-750.
111. Yuan J., Horvitz H.R. The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev Biol. 138:1990;33-41.
112. Yui J., Garcia-Lloret M.I., Wegmann T.G., Guilbert L.J. Cytotoxicity of tumor necrosis factor alpha and gamma-interferon against primary human placental trophoblasts. Placenta. 15:1994;819-825.
113. Yui J., Hemmings D., Garcia-Lloret M., Guilbert L.J. Expression of the human p55 and p75 tumor necrosis factor receptors in primary villous trophoblasts and their role in cytotoxic signal transduction. Biol Reprod. 55:1996;400-409.
114. L . Cell. 87:1996;619-628.
115. Zorzi W., Thellin O., Coumans B., Melot F., Hennen G., Lakaye B., Igout A., Heinen E. Demonstration of the expression of CD95 ligand transcript and protein in human placenta. Placenta. 19:1998;269-277.