Trophinin: What embryo implantation teaches us about human cancer

Cancer Biology and Therapy

Volumn 7, Issue 8, 2008, Pages 1165-1170

  Fukuda, Michiko N ^a   Sugihara, Kazuhiro ^b   Nakayama, Jun ^c  

^a BURNHAM INSTITUTE   (United States)

^b HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

HB EGF; hCG; HMGB1; Placenta; Trophoblast

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; BYSTIN; CELL ADHESION MOLECULE; CHORIONIC GONADOTROPIN; EPIDERMAL GROWTH FACTOR RECEPTOR 4; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; L SELECTIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROGESTERONE; TASTIN; TROPHININ; UNCLASSIFIED DRUG;

CELL DIFFERENTIATION; CELL STRAIN COS1; CHORIOCARCINOMA; COLON CANCER; EMBRYONAL CARCINOMA; ENDOMETRIUM CARCINOMA; GERM CELL TUMOR; HUMAN; HYDATIDIFORM MOLE; IMMUNOHISTOCHEMISTRY; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; MOLECULAR CLONING; NIDATION; NONHUMAN; OVARY CANCER; PROGNOSIS; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SYNCYTIOTROPHOBLAST; TERATOCARCINOMA; TESTIS CANCER; TROPHOBLAST; X CHROMOSOME;

EID: 49749120207     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.7.8.6696     Document Type: Review

References (59)

1. Beard J. The cancer problem. Lancet 1905; 1:281-3.
2. Gurchot C. The trophoblast theory of cancer (John Beard, 1857-1924) revisited. Oncology 1975; 31:310-33.
3. Old LJ. Cancer/testis (CT) antigens - a new link between gametogenesis and cancer. Cancer Immun 2001; 1:1.
4. Iles RK. Ectopic hCGbeta expression by epithelial cancer: malignant behaviour, metastasis and inhibition of tumor cell apoptosis. Mol Cell Endocrinol 2007; 262:264-70.
5. Hotakainen K, Lintula S, Jarvinen R, Paju A, Stenman J, Rintala E, Stenman UH. Overexpression of human chorionic gonadotropin beta genes 3, 5 and 8 in tumor tissue and urinary cells of bladder cancer patients. Tumour Biol 2007; 28:52-6.
6. Madersbacher S, Gerth R, Mann K, Dirnhofer S, Berger P. Gonadotrophin secretion patterns in testicular cancer patients with greatly increased human chorionic gonadotrophin serum concentrations. J Endocrinol 1998; 159:451-8.
7. Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K. Embryo implantation. Developmental Biology 2000; 223:217-37.
8. Ramsey EM, Houston ML, Harris JW. Interactions of the trophoblast and maternal tissues in three closely related primate species. Am J Obstet Gynecol 1976; 124:647-52.
9. Enders AC. Cytotrophoblast invasion of the endometrium in the human and macaque early villous stage of implantation. Trophoblast Res 1997; 10:83-95.
10. Hertig AT, Rock J. Searching for early fertilized human ova. Gynecol Invest 1973; 4:121-39.
11. Enders AC. Cytology of human early implantation. Res Reprod 1976; 8:1-2.
12. Izhar M, Siebert P, Oshima RG, DeWolf WC, Fukuda MN. Trophoblastic differentiation of human teratocarcinoma cell line HT-H. Developmental Biology 1986; 116:510-8.
13. Fukuda MN, Sato T, Nakayama J, Klier G, Mikami M, Aoki D, Nozawa S. Trophinin and tastin, a novel cell adhesion molecule complex with potential involvement in embryo implantation. Genes Dev 1995; 9:1199-210.
14. Martin GR. Teratocarcinomas as a model system for the study of embryogenesis and neoplasia. Cell 1975; 5:229-43.
15. Andrews PW, Goodfellow PN, Damjanov I. Human teratocarcinoma cells in culture. Cancer Surveys 1983; 2:41-73.
16. Andrews PW, Bronson DL, Benham F, Strickland S, Knowles BB. A comparative study of eight cell lines derived from human testicular teratocarcinoma. Int J Cancer 1980; 26:269-80.
17. Knowles BB, Rappaport J, Solter D. Murine embryonic antigen (SSEA-1) is expressed on human cells and structurally related human blood group antigen I is expressed on mouse embryos. Dev Biol 1982; 93:54-8.
18. Andrew PW, Bronson DL, Benham F, Strickland S, Knowles BB. A comparative study of eight cell lines derived from human testicular teratocarcinoma. Int J Cancer 1980; 26:269-84.
19. 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; 37:1777-85.
20. 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; 17:229-34.
21. 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; 60:621-7.
22. Pack S, Tanigami A, Ledbetter DH, Sato T, Fukuda MN. Assignment of trophoblast/ endometrial epithelium cell adhesion molecule trophinin gene TRO to human chromosome bands Xp11.22Æp11.21 by in situ hybridization Cytogenet. Cell Genet 1997; 79:123-4.
23. Mandel JL, Monaco AP, Nelson DL, Schlessinger D, Willard H. Genome analysis and the human X chromosome. Science 1992; 258:103-9.
24. Nadano D, Sugihara K, Paria BC, Saburi S, Copeland NG, Gilbert DJ, Jenkins NA, Nakayama J, Fukuda MN. Significant differences between mouse and human trophinins are revealed by their expression patterns and targeted disruption of mouse trophinin gene. Biol Reprod 2002; 66:313-21.
25. Suzuki N, Nadano D, Paria BC, Kupriyanov S, Sugihara K, Fukuda MN. Trophinin expression in the mouse uterus coincides with implantation and is hormonally regulated but not induced by implanting blastocysts. Endocrinology 2000; 141:4247-54.
26. Nakayama J, Aoki D, Suga T, Akama TO, Ishizone S, Yamaguchi H, Imakawa K, Nadano D, Fazleabas AT, Katsuyama T, Nozawa S, Fukuda MN. 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; 163:2211-9.
27. Sugihara K, Kabir-Salmani M, Byrne J, Wolf DP, Lessey B, Iwashita M, Aoki D, Nakayama J, Fukuda MN. Induction of trophinin in human endometrial surface epithelia by CGbeta and IL-1beta. FEBS Lett 2008; 582:197-202.
28. Genbacev OD, Prakobphol A, Foulk RA, Krtolica AR, Ilic D, Singer MS, Yang ZQ, Kiessling LL, Rosen SD, Fisher SJ. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 2003; 299:405-8.
29. Fukuda MN, Sugihara K. An integrated view of L-selectin and trophinin function in human embryo implantation. J Obstet Gynaecol Res 2008; 34:129-36.
30. Suzuki N, Zara J, Sato T, Ong E, Bakhiet N, Oshima RG, Watson KL, Fukuda MN. 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; 95:5027-32.
31. Trachtulec Z, Forejt J. Synteny of orthologous genes conserved in mammals, snake, fly, nematode and fission yeast. Mamm Genome 2001; 12:227-31.
32. Roos J, Luz JM, Centoducati S, Sternglanz R, Lennarz WJ. ENP1, an essential gene encoding a nuclear protein that is highly conserved from yeast to humans. Gene 1997; 185:137-46.
33. Chen W, Bucaria J, Band DA, Sutton A, Sternglanz R. Enp1, a yeast protein associated with U3 and U14 snoRNAs, is required for pre-rRNA processing and 40S subunit synthesis. Nucleic Acids Res 2003; 31:690-9.
34. 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; 404:373-81.
35. Adachi K, Soeta-Saneyoshi C, Sagara H, Iwakura Y. Crucial role of Bysl in mammalian preimplantation development as an integral factor for 40S ribosome biogenesis. Mol Cell Biol 2007; 27:2202-14.
36. Sheng J, Yang S, Xu L, Wu C, Wu X, Li A, Yu Y, Ni H, Fukuda M, Zhou J. Bystin as a novel marker for reactive astrocytes in the adult rat brain following injury. Eur J Neurosci 2004; 20:873-84.
37. Basso K, Margolin AA, Stolovitzky G, Klein U, Dalla-Favera R, Califano A. Reverse engineering of regulatory networks in human B cells. Nat Genet 2005; 37:382-90.
38. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002; 298:597-600.
39. Ayala GE, Dai H, Li R, Ittmann M, Thompson TC, Rowley D, Wheeler TM. Bystin in perineural invasion of prostate cancer. Prostate 2006; 66:266-72.
40. Sugihara K, Sugiyama D, Byrne J, Wolf DP, Lowitz KP, Kobayashi Y, Kabir-Salmani M, Nadano D, Aoki D, Nozawa S, Nakayama J, Mustelin T, Ruoslahti E, Yamaguchi N, Fukuda MN. Trophoblast cell activation by trophinin ligation is implicated in human embryo implantation. Proc Natl Acad Sci USA 2007; 104:3799-804.
41. Fukuda MN, Sugihara K. Signal transduction in human embryo implantation. Cell Cycle 2007; 6:1153-6.
42. Lindenberg S. Ultrastructure in human implantation: transmission and scanning electron microscopy. Baillieres Clin Obstet Gynaecol 1991; 5:1-14.
43. Brewer JI, Torok EE, Kahan BD, Stanhope CR, Halpern B. Gestational trophoblastic disease: origin of choriocarcinoma, invasive mole and choriocarcinoma associated with hydatidiform mole, and some immunologic aspects. Adv Cancer Res 1978; 27:89-147.
44. Medeiros F, Callahan MJ, Elvin JA, Dorfman DM, Berkowitz RS, Quade BJ. Intraplacental choriocarcinoma arising in a second trimester placenta with partial hydatidiform mole. Int J Gynecol Pathol 2008; 27:247-51.
45. Hatakeyama S, Ohyama C, Minagawa S, Inoue T, Kakinuma H, Kyan A, Arai Y, Suga T, Nakayama J, Kato T, Habuchi T, Fukuda MN. Functional correlation of trophinin expression with the malignancy of testicular germ cell tumor. Cancer Res 2004; 64:4257-62.
46. Harada O, Suga T, Suzuki T, Nakamoto K, Kobayashi M, Nomiyama T, Nadano D, Ohyama C, Fukud MN, Nakayama J. The role of trophinin, an adhesion molecule unique to human trophoblasts, in progression of colorectal cancer. Int J Cancer 2007; 121:1072-8.
47. Baba T, Mori S, Matsumura N, Kariya M, Murphy SK, Kondoh E, Kusakari T, Kuroda H, Mandai M, Higuchi T, Takakura K, Fukuda MN, Fujii S. Trophinin is a potent prognostic marker of ovarian cancer involved in platinum sensitivity. Biochem Biophys Res Commun 2007.
48. Kato S, Espinoza N, Lange S, Villalon M, Cuello M, Owen GI. Characterization and phenotypic variation with passage number of cultured human endometrial adenocarcinoma cells. Tissue Cell 2008; 40:95-102.
49. Wilcox AJ, Baird DD, Weinberg CR. The time of implantation of the conceptus and loss of pregnancy. New Eng J Med 1999; 340:1796-9.
50. Mandai M, Konishi I, Kuroda H, Fujii S. LH/hCG action and development of ovarian cancer - a short review on biological and clinical/epidemiological aspects. Mol Cell Endocrinol 2007; 269:61-4.
51. Gudipudi DK, Hartzfeld K, Montemarano N, Del Priore G. Decreased breast cancer rates among women with choriocarcinoma. Gynecol Oncol 2008.
52. Mazumdar M, Bajorin DF, Bacik J, Higgins G, Motzer RJ, Bosl GJ. Predicting outcome to chemotherapy in patients with germ cell tumors: the value of the rate of decline of human chorionic gonadotrophin and alpha-fetoprotein during therapy. J Clin Oncol 2001; 19:2534-41.
53. Bellet D, Bidart JM, Jolivet M, Tartar A, Caillaud JM, Ozturk M, Strugo MC, Audibert F, Gras-Masse H, Assicot M, et al. A monoclonal antibody against a synthetic peptide is specific for the free native human chorionic gonadotropin beta-subunit. Endocrinology 1984; 115:330-6.
54. Lehtovirta P, Alfthan H, Vaetiainen J, Stenman U. Skin metastases of gynecological adenocarcinomas affecr serum levels of hCG beta but not those of SCC antigen. Tumor Biol 1999; 20:251-5.
55. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5:331-42.
56. Chen KY, Lee YC, Lai JM, Chang YL, Lee YC, Yu CJ, Huang CY, Yang PC. Identification of trophinin as an enhancer for cell invasion and a prognostic factor for early stage lung cancer. Eur J Cancer 2007; 43:782-90.
57. Patton SE, Martin ML, Nelsen LL, Fang X, Mills GB, Bast RC, Ostrowski MC Jr. Activation of the ras-mitogen-activated protein kinase pathway and phosphorylation of ets-2 at position threonine 72 in human ovarian cancer cell lines. Cancer Res 1998; 58:2253-9.
58. Liu J, Yang G, Thompson-Lanza JA, Glassman A, Hayes K, Patterson A, Marquez RT, Auersperg N, Yu Y, Hahn WC, Mills GB, Bast RC Jr. A genetically defined model for human ovarian cancer. Cancer Res 2004; 64:1655-63.
59. Janssens JP, Russo J, Russo I, Michiels L, Donders G, Verjans M, Riphagen I, Van den Bossche T, Deleu M, Sieprath P. Human chorionic gonadotropin (hCG) and prevention of breast cancer. Mol Cell Endocrinol 2007; 269:93-8.