Trophinin-mediated cell adhesion induces apoptosis of human endometrial epithelial cells through PKC-δ

References

• Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, et al. Embryo implantation. Developmental Biology 2000; 223:217 - 237
   PubMed Web of Science ®Google Scholar
• Fukuda MN, Sugihara K. Signal transduction in human embryo implantation. Cell Cycle 2007; 6:1153 - 1156
   PubMed Web of Science ®Google Scholar
• Fukuda MN, Sugihara K. An integrated view of L-selectin and trophinin function in human embryo implantation. J Obstet Gynaecol Res 2008; 34:129 - 136
   PubMed Web of Science ®Google Scholar
• Nakayama J, Aoki D, Suga T, Akama TO, Ishizone S, Yamaguchi H, et al. Implantation-Dependent Expression of Trophinin by Maternal Fallopian Tube Epithelia during Tubal Pregnancies: Possible Role of Human Chorionic Gonadotrophin on Ectopic Pregnancy. Am J Pathol 2003; 163:2211 - 2219
   PubMed Web of Science ®Google Scholar
• Sugihara K, Kabir-Salmani M, Byrne J, Wolf DP, Lessey B, Iwashita M, et al. Induction of trophinin in human endometrial surface epithelia by CGbeta and IL-1beta. FEBS Lett 2008; 582:197 - 202
   PubMed Web of Science ®Google Scholar
• Genbacev OD, Prakobphol A, Foulk RA, Krtolica AR, Ilic D, Singer MS, et al. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 2003; 299:405 - 408
   PubMed Web of Science ®Google Scholar
• Fukuda MN, Sato T, Nakayama J, Klier G, Mikami M, Aoki D, et al. Trophinin and tastin, a novel cell adhesion molecule complex with potential involvement in embryo implantation. Genes Dev 1995; 9:1199 - 1210
   PubMed Web of Science ®Google Scholar
• Suzuki N, Nakayama J, Shih IM, Aoki D, Nozawa S, Fukuda MN. Expression of trophinin, tastin and bystin by trophoblast and endometrial cells in human placenta. Biol Reprod 1999; 60:621 - 627
   PubMed Web of Science ®Google Scholar
• Sugihara K, Sugiyama D, Byrne J, Wolf DP, Lowitz KP, Kobayashi Y, et al. Trophoblast cell activation by trophinin ligation is implicated in human embryo implantation. Proc Natl Acad Sci USA 2007; 104:3799 - 3804
   PubMed Web of Science ®Google Scholar
• Suzuki N, Zara J, Sato T, Ong E, Bakhiet N, Oshima RG, et al. A novel cytoplasmic protein, bystin, interacts with trophinin, tastin and cytokeratin, and may be involved in trophinin mediated cell adhesion between trophoblast and endometrial epithelial cells. Proceedings of the National Academy of Sciences, USA 1998; 95:5027 - 5032
   PubMed Web of Science ®Google Scholar
• Welsh AO. Uterine cell death during implantation and early placentation. Microsc Res Tech 1993; 25:223 - 245
   PubMed Web of Science ®Google Scholar
• Galan A, O'Connor JE, Valbuena D, Herrer R, Remohi J, Pampfer S, et al. The human blastocyst regulates endometrial epithelial apoptosis in embryonic adhesion. Biol Reprod 2000; 63:430 - 439
   PubMed Web of Science ®Google Scholar
• Simon C, Dominguez F, Remohi J, Pellicer A. Embryo effects in human implantation: embryonic regulation of endometrial molecules in human implantation. Ann N Y Acad Sci 2001; 943:1 - 16
   PubMed Web of Science ®Google Scholar
• Li HY, Chang SP, Yuan CC, Chao HT, Ng HT, Sung YJ. Induction of p38 mitogen-activated protein kinase-mediated apoptosis is involved in outgrowth of trophoblast cells on endometrial epithelial cells in a model of human trophoblast-endometrial interactions. Biol Reprod 2003; 69:1515 - 1524
   PubMed Web of Science ®Google Scholar
• Fukuda MN, Nozawa S. Trophinin, tastin and bystin: a complex mediating unique attachment between trophoblastic and endometrial epithelial cells at their respective apical cell membranes. Semin Reprod Endocrinol 1999; 17:229 - 234
   PubMedGoogle Scholar
• Nagata S. Apoptosis by death factor. Cell 1997; 88:355 - 365
   PubMed Web of Science ®Google Scholar
• Hsu WL, Chen YH, Chao KC, Chang SP, Tsui KH, Li HY, et al. Anti-fas activating antibody enhances trophoblast outgrowth on endometrial epithelial cells by induction of P38 MAPK/JNK-mediated apoptosis. Placenta 2008; 29:338 - 346
   PubMed Web of Science ®Google Scholar
• Reyland ME. Protein kinase Cdelta and apoptosis. Biochem Soc Trans 2007; 35:1001 - 1004
   PubMed Web of Science ®Google Scholar
• Humphries MJ, Ohm AM, Schaack J, Adwan TS, Reyland ME. Tyrosine phosphorylation regulates nuclear translocation of PKCdelta. Oncogene 2008; 27:3045 - 3053
   PubMed Web of Science ®Google Scholar
• Hertig AT, Rock J. Searching for early fertilized human ova. Gynecol Invest 1973; 4:121 - 139
   PubMedGoogle Scholar
• Enders AC. Cytotrophoblast invasion of the endometrium in the human and macaque early villous stage of implantation. Trophoblast Res 1997; 10:83 - 95
   Google Scholar
• Moser G, Gauster M, Orendi K, Glasner A, Theuerkauf R, Huppertz B. Endoglandular trophoblast, an alternative route of trophoblast invasion? Analysis with novel confrontation co-culture models. Hum Reprod 25:1127 - 1136
   PubMed Web of Science ®Google Scholar
• Hatakeyama S, Ohyama C, Minagawa S, Inoue T, Kakinuma H, Kyan A, et al. Functional correlation of trophinin expression with the malignancy of testicular germ cell tumor. Cancer Res 2004; 64:4257 - 4262
   PubMed Web of Science ®Google Scholar
• Harada O, Suga T, Suzuki T, Nakamoto K, Kobayashi M, Nomiyama T, et al. The role of trophinin, an adhesion molecule unique to human trophoblasts, in progression of colorectal cancer. Int J Cancer 2007; 121:1072 - 1078
   PubMed Web of Science ®Google Scholar
• Fukuda MN, Sugihara K, Nakayama J. Trophinin: what embryo implantation teaches us about human cancer. Cancer Biol Ther 2008; 7:1165
   PubMed Web of Science ®Google Scholar
• Martelli AM, Faenza I, Billi AM, Fala F, Cocco L, Manzoli L. Nuclear protein kinase C isoforms: key players in multiple cell functions?. Histol Histopathol 2003; 18:1301 - 1312
   PubMed Web of Science ®Google Scholar
• Qi X, Mochly-Rosen D. The PKCdelta-Abl complex communicates ER stress to the mitochondria—an essential step in subsequent apoptosis. J Cell Sci 2008; 121:804 - 813
   PubMed Web of Science ®Google Scholar
• DeVries-Seimon TA, Ohm AM, Humphries MJ, Reyland ME. Induction of apoptosis is driven by nuclear retention of protein kinase Cdelta. J Biol Chem 2007; 282:22307 - 22314
   PubMed Web of Science ®Google Scholar
• Brodie C, Blumberg PM. Regulation of cell apoptosis by protein kinase cdelta. Apoptosis 2003; 8:19 - 27
   PubMed Web of Science ®Google Scholar
• Basu A, Adkins B, Basu C. Downregulation of caspase-2 by rottlerin via protein kinase C-delta-independent pathway. Cancer Res 2008; 68:2795 - 2802
   PubMed Web of Science ®Google Scholar
• Yuan ZM, Utsugisawa T, Ishiko T, Nakada S, Huang Y, Kharbanda S, et al. Activation of protein kinase Cdelta by the c-Abl tyrosine kinase in response to ionizing radiation. Oncogene 1998; 16:1643 - 1648
   PubMed Web of Science ®Google Scholar
• Scheel-Toellner D, Pilling D, Akbar AN, Hardie D, Lombardi G, Salmon M, et al. Inhibition of T cell apoptosis by IFNbeta rapidly reverses nuclear translocation of protein kinase C-delta. Eur J Immunol 1999; 29:2603 - 2612
   PubMed Web of Science ®Google Scholar
• Ghayur T, Hugunin M, Talanian RV, Ratnofsky S, Quinlan C, Emoto Y, et al. Proteolytic activation of protein kinase Cdelta by an ICE/CED 3-like protease induces characteristics of apoptosis. J Exp Med 1996; 184:2399 - 2404
   PubMed Web of Science ®Google Scholar
• Jackson DN, Foster DA. The enigmatic protein kinase Cdelta: complex roles in cell proliferation and survival. Faseb J 2004; 18:627 - 636
   PubMed Web of Science ®Google Scholar
• Lessey BA, Gui Y, Apparao KB, Young SL, Mulholland J. Regulated expression of heparin-binding EGF-like growth factor (HB-EGF) in the human endometrium: a potential paracrine role during implantation. Mol Reprod Dev 2002; 62:446 - 455
   PubMed Web of Science ®Google Scholar
• Yoo HJ, Barlow DH, Mardon HJ. Temporal and spatial regulation of expression of heparin-binding epidermal growth factor-like growth factor in the human endometrium: a possible role in blastocyst implantation. Dev Genet 1997; 21:102 - 108
   PubMedGoogle Scholar
• Stavreus-Evers A, Aghajanova L, Brismar H, Eriksson H, Landgren BM, Hovatta O. Co-existence of heparin-binding epidermal growth factor-like growth factor and pinopodes in human endometrium at the time of implantation. Mol Hum Reprod 2002; 8:765 - 769
   PubMed Web of Science ®Google Scholar
• Hatakeyama S, Sugihara K, Lee SH, Nadano D, Nakayama J, Ohyama C, et al. Enhancement of human sperm motility by trophinin binding peptide. J Urol 2008; 180:767 - 771
   PubMed Web of Science ®Google Scholar
• Izhar M, Siebert P, Oshima RG, DeWolf WC, Fukuda MN. Trophoblastic differentiation of human teratocarcinoma cell line HT-H. Developmental Biology 1986; 116:510 - 518
   PubMed Web of Science ®Google Scholar
• Ishiwata I, Nozawa S, Inoue T, Okumura H. Development and characterization of established cell lines from primary and metastatic regions of human endometrial adenocarcinoma. Cancer Res 1977; 37:1777 - 1785
   PubMed Web of Science ®Google Scholar
• Pederson T. Cells: a Laboratory Manual 1998; New York Cold Spring Harbor Laboratory Press
   Google Scholar
• Miyoshi M, Okajima T, Matsuda T, Fukuda MN, Nadano D. Bystin in human cancer cells: intracellular localization and function in ribosome biogenesis. Biochem J 2007; 404:373 - 381
   PubMed Web of Science ®Google Scholar