Insulin-Like Growth Factor Binding Protein 7 Modulates Estrogen-Induced Trophoblast Proliferation and Invasion in HTR-8 and JEG-3 Cells

Cell Biochemistry and Biophysics

Volumn 63, Issue 1, 2012, Pages 73-84

  Liu, Zhen Kun ^a,b   Liu, Hai Yan ^a,b   Fang, Wen Ning ^a   Yang, Ying ^a   Wang, Hong Mei ^a   Peng, Jing Pian ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Estrogen; IGFBP7; Invasion; Proliferation; Trophoblast

Indexed keywords

CYCLINE; DRUG DERIVATIVE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; GAMMA INTERFERON; GELATINASE A; GELATINASE B; INSULIN LIKE GROWTH FACTOR BINDING PROTEIN RELATED PROTEIN 1; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN-RELATED PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE; NEUTRALIZING ANTIBODY; RECOMBINANT PROTEIN; SOMATOMEDIN BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CELL LINE; CELL MOTION; CELL PROLIFERATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; TROPHOBLAST;

ANTIBODIES, NEUTRALIZING; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; ESTRADIOL; ESTROGENS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; INTERFERON-GAMMA; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; PHOSPHORYLATION; PROLIFERATING CELL NUCLEAR ANTIGEN; RECEPTORS, ESTROGEN; RECOMBINANT PROTEINS; TRANSFORMING GROWTH FACTOR BETA; TROPHOBLASTS;

EID: 84862806104     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-012-9342-5     Document Type: Article

References (58)

1. Hwa, V., Oh, Y., & Rosenfeld, R. G. (1999). The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocrine Reviews, 20(6), 761-787.
2. Yamashita, S., Tsujino, Y., Moriguchi, K., Tatematsu, M., & Ushijima, T. (2006). Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-2′-deoxycytidine treatment and oligonucleotide microarray. Cancer Science, 97(1), 64-71. doi: 10. 1111/j. 1349-7006. 2006. 00136. x.
3. Heesch, S., Bartram, I., Neumann, M., Reins, J., Mossner, M., Schlee, C., Stroux, A., Haferlach, T., Goekbuget, N., Hoelzer, D., Hofmann, W. -K., Thiel, E., & Baldus, C. D. (2010). Expression of IGFBP7 in acute leukemia is regulated by DNA methylation. Cancer Science, 102, 253-259. doi: 10. 1111/j. 1349-7006. 2010. 01760. x.
4. Ye, F., Chen, Y., Knosel, T., Schluns, K., Pacyna-Gengelbach, M., Deutschmann, N., et al. (2007). Decreased expression of insulin-like growth factor binding protein 7 in human colorectal carcinoma is related to DNA methylation. Journal of Cancer Research and Clinical Oncology, 133(5), 305-314. doi: 10. 1007/s00432-006-0171-z.
5. Wajapeyee, N., Serra, R. W., Zhu, X., Mahalingam, M., & Green, M. R. (2008). Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell, 132(3), 363-374. doi: 10. 1016/j. cell. 2007. 12. 032.
6. Dominguez, F., Avila, S., Cervero, A., Martin, J., Pellicer, A., Castrillo, J. L., et al. (2003). A combined approach for gene discovery identifies insulin-like growth factor-binding protein-related protein 1 as a new gene implicated in human endometrial receptivity. Journal of Clinical Endocrinology and Metabolism, 88(4), 1849-1857. doi: 10. 1210/jc. 2002-020724.
7. Tamura, K., Hara, T., Kutsukake, M., Iwatsuki, K., Yanagida, M., Yoshie, M., et al. (2004). Expression and the biological activities of insulin-like growth factor-binding protein related protein 1 in rat uterus during the preimplantation period. Endocrinology, 145(11), 5243-5251. doi: 10. 1210/en. 2004-0415.
8. Kutsukake, M., Ishihara, R., Yoshie, M., Kogo, H., & Tamura, K. (2007). Involvement of insulin-like growth factor-binding protein-related protein 1 in decidualization of human endometrial stromal cells. Molecular Human Reproduction, 13(10), 737-743. doi: 10. 1093/molehr/gam058.
9. Guibourdenche, J., Handschuh, K., Tsatsaris, V., Gerbaud, P., Leguy, M. C., Muller, F., et al. (2010). Hyperglycosylated hCG is a marker of early human trophoblast invasion. Journal of Clinical Endocrinology and Metabolism, 95(10), E240-E244. doi: 10. 1210/jc. 2010-0138.
10. Udayashankar, R., Baker, D., Tuckerman, E., Laird, S., Li, T. C., & Moore, H. D. (2011). Characterization of invasive trophoblasts generated from human embryonic stem cells. Human Reproduction, 26(2), 398-406. doi: 10. 1093/humrep/deq350.
11. Blomberg, L., Hashizume, K., & Viebahn, C. (2008). Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation. Reproduction, 135(2), 181-195. doi: 10. 1530/rep-07-0355.
12. Norwitz, E. R., Schust, D. J., & Fisher, S. J. (2001). Implantation and the survival of early pregnancy. New England Journal of Medicine, 345(19), 1400-1408. doi: 10. 1056/NEJMra000763.
13. Riquelme, G. (2009). Placental chloride channels: a review. Placenta, 30(8), 659-669. doi: 10. 1016/j. placenta. 2009. 06. 002.
14. Mendelson, C. R., Jiang, B., Shelton, J. M., Richardson, J. A., & Hinshelwood, M. M. (2005). Transcriptional regulation of aromatase in placenta and ovary. The Journal of Steroid Biochemistry and Molecular Biology, 95(1-5), 25-33. doi: 10. 1016/j. jsbmb. 2005. 04. 016.
15. Ringler, G. E., & Strauss, J. F. (1990). In vitro systems for the study of human placental endocrine function. Endocrine Reviews, 11(1), 105-123. doi: 10. 1210/edrv-11-1-105.
16. Pijnenborg, R., Bland, J. M., Robertson, W. B., & Brosens, I. (1983). Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta, 4(4), 397-413. doi: 10. 1016/s0143-4004(83)80043-5.
17. Pollheimer, J., & Knöfler, M. (2005). Signalling pathways regulating the invasive differentiation of human trophoblasts: A review. Placenta, 26(Supplement 1), S21-S30. doi: 10. 1016/j. placenta. 2004. 11. 013.
18. Koc, S., Ozdegirmenci, O., Tulunay, G., Ozgul, N., Kose, M. F., & Bulbul, D. (2006). Recurrent partial hydatidiform mole: A report of a patient with three consecutive molar pregnancies. International Journal of Gynecological Cancer, 16(2), 940-943. doi: 10. 1111/j. 1525-1438. 2006. 00232. x.
19. Yang, X., Zhang, Z., Jia, C., Li, J., Yin, L., & Jiang, S. (2002). The relationship between expression of c-ras, c-erbB-2, nm23, and p53 gene products and development of trophoblastic tumor and their predictive significance for the malignant transformation of complete hydatidiform mole. Gynecologic Oncology, 85(3), 438-444. doi: 10. 1006/gyno. 2002. 6652.
20. Tuncer, Z. S., Vegh, G. L., Fulop, V., Genest, D. R., Mok, S. C., & Berkowitz, R. S. (2000). Expression of epidermal growth factor receptor-related family products in gestational trophoblastic diseases and normal placenta and its relationship with development of postmolar tumor. Gynecologic Oncology, 77(3), 389-393. doi: 10. 1006/gyno. 2000. 5777.
21. Seckl, M. J., Fisher, R. A., Salerno, G., Rees, H., Paradinas, F. J., Foskett, M., et al. (2000). Choriocarcinoma and partial hydatidiform moles. The Lancet, 356(9223), 36-39. doi: 10. 1016/s0140-6736(00)02432-6.
22. Cui, J. Q., Shi, Y. F., Zhou, H. J., & Li, J. Q. (2004). The changes of gene expression profiles in hydatidiform mole and choriocarcinoma with hyperplasia of trophoblasts. International Journal of Gynecological Cancer, 14(5), 984-997. doi: 10. 1111/j. 1048-891X. 2004. 14539. x.
23. Yashwanth, R., Rama, S., Anbalagan, M., & Rao, A. J. (2006). Role of estrogen in regulation of cellular differentiation: A study using human placental and rat Leydig cells. Molecular and Cellular Endocrinology, 246(1-2), 114-120. doi: 10. 1016/j. mce. 2005. 11. 007.
24. Caniggia, I., Grisaru-Gravnosky, S., Kuliszewsky, M., Post, M., & Lye, S. J. (1999). Inhibition of TGF-β3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. The Journal of Clinical Investigation, 103(12), 1641-1650.
25. MacPhee, D. J., Mostachfi, H., Han, R., Lye, S. J., Post, M., & Caniggia, I. (2001). Focal adhesion kinase is a key mediator of human trophoblast development. Laboratory Investigation, 81(11), 1469-1483.
26. Ilic, D., Genbacev, O., Jin, F., Caceres, E., Almeida, E. A. C., Bellingard-Dubouchaud, V., et al. (2001). Plasma membrane-associated pY397FAK is a marker of cytotrophoblast invasion in vivo and in vitro. American Journal of Pathology, 159(1), 93-108.
27. Bifulco, G., Trencia, A., Caruso, M., Tommaselli, G. A., Miele, C., di Carlo, C., et al. (2003). Leptin induces mitogenic effect on human choriocarcinoma cell line (JAr) via MAP kinase activation in a glucose-dependent fashion. Placenta, 24(4), 385-391. doi: 10. 1053/plac. 2002. 0905.
28. Cartwright, J. E., Tse, W. K., & Whitley, G. S. (2002). Hepatocyte growth factor induced human trophoblast motility involves phosphatidylinositol-3-kinase, mitogen-activated protein kinase, and inducible nitric oxide synthase. Experimental Cell Research, 279(2), 219-226. doi: 10. 1006/excr. 2002. 5616.
29. Maymó, J. L., Pérez Pérez, A., Gambino, Y., Calvo, J. C., Sánchez-Margalet, V., & Varone, C. L. (2011). Review: Leptin gene expression in the placenta-Regulation of a key hormone in trophoblast proliferation and survival. Placenta 32, Supplement 2(0): S146-S153. doi: 10. 1016/j. placenta. 2011. 01. 004.
30. Gambino, Y. P., Maymó, J. L., Pérez Pérez, A., Calvo, J. C., Sánchez-Margalet, V., & Varone, C. L. (2012). Elsevier trophoblast research award lecture: Molecular mechanisms underlying estrogen functions in trophoblastic cells-Focus on leptin expression. Placenta. doi: 10. 1016/j. placenta. 2011. 12. 001.
31. Ramathal, C. Y., Bagchi, I. C., Taylor, R. N., & Bagchi, M. K. (2010). Endometrial decidualization: of mice and men. Seminars in Reproductive Medicine, 28 (01), 017-026. doi: 10. 1055/s-0029-1242989.
32. Leonard, S., Murrant, C., Tayade, C., van den Heuvel, M., Watering, R., & Croy, B. A. (2006). Mechanisms regulating immune cell contributions to spiral artery modification-Facts and hypotheses-A review. Placenta, 27, Supplement(0), 40-46. doi: 10. 1016/j. placenta. 2005. 11. 007.
33. Paulesu, L., Romagnoli, R., Cintorino, M., Grazia Ricci, M., & Garotta, G. (1994). First trimester human trophoblast expresses both interferon-γ and interferon-γ-receptor. Journal of Reproductive Immunology, 27(1), 37-48. doi: 10. 1016/0165-0378(94)90013-2.
34. Roberts, R. M., Chen, Y., Ezashi, T., & Walker, A. M. (2008). Interferons and the maternal-conceptus dialog in mammals. Seminars in Cell & Developmental Biology, 19(2), 170-177. doi: 10. 1016/j. semcdb. 2007. 10. 007.
35. Rajaraman, G., Murthi, P., Pathirage, N., Brennecke, S. P., & Kalionis, B. (2010). Downstream targets of homeobox gene HLX show altered expression in human idiopathic fetal growth restriction. The American Journal of Pathology, 176(1), 278-287. doi: 10. 2353/ajpath. 2010. 090187.
36. Wickert, L., Chatain, N., Kruschinsky, K., & Gressner, A. (2007). Glucocorticoids activate TGF-beta induced PAI-1 and CTGF expression in rat hepatocytes. Comparative Hepatology, 6(1), 5.
37. Jovanovic, M., & Vicovac, L. (2009). Interleukin-6 stimulates cell migration, invasion and integrin expression in HTR-8/SVneo cell line. Placenta, 30(4), 320-328. doi: 10. 1016/j. placenta. 2009. 01. 013.
38. Suman, P., Poehlmann, T. G., Prakash, G. J., Markert, U. R., & Gupta, S. K. (2009). Interleukin-11 increases invasiveness of JEG-3 choriocarcinoma cells by modulating STAT3 expression. Journal of Reproductive Immunology, 82(1), 1-11. doi: 10. 1016/j. jri. 2009. 07. 002.
39. Zhang, X., Green, K. E., Yallampalli, C., & Dong, Y. L. (2005). Adrenomedullin enhances invasion by trophoblast cell lines. Biology of Reproduction, 73(4), 619-626. doi: 10. 1095/biolreprod. 105. 040436.
40. King, A., Thomas, L., & Bischof, P. (2000). Cell culture models of trophoblast II: Trophoblast cell lines-A workshop report. Placenta, 21, S113-S119.
41. Bukovsky, A., Cekanova, M., Caudle, M., Wimalasena, J., Foster, J., Henley, D., et al. (2003). Expression and localization of estrogen receptor-alpha protein in normal and abnormal term placentae and stimulation of trophoblast differentiation by estradiol. Reproductive Biology and Endocrinology, 1(1), 1-18. doi: 10. 1186/1477-7827-1-13.
42. Ma, W. G., Song, H., Das, S. K., Paria, B. C., & Dey, S. K. (2003). Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proceedings of the National Academy of the United States of America, 100(5), 2963-2968. doi: 10. 1073/pnas. 0530162100.
43. Damon, S. E., Haugk, K. L., Swisshelm, K., & Quinn, L. S. (1997). Developmental regulation of Mac25/insulin-like growth factor-binding protein-7 expression in skeletal myogenesis. Experimental Cell Research, 237(1), 192-195. doi: 10. 1006/excr. 1997. 3787.
44. Pen, A., Moreno, M. J., Durocher, Y., Deb-Rinker, P., & Stanimirovic, D. B. (2008). Glioblastoma-secreted factors induce IGFBP7 and angiogenesis by modulating Smad-2-dependent TGF-beta signaling. Oncogene, 27(54), 6834-6844. doi: 10. 1038/onc. 2008. 287.
45. Hwa, V., Tomasini-Sprenger, C., Bermejo, A. L., Rosenfeld, R. G., & Plymate, S. R. (1998). Characterization of insulin-like growth factor-binding protein-related protein-1 in prostate cells. Journal of Clinical Endocrinology and Metabolism, 83(12), 4355-4362.
46. Graham, C. H., & Lala, P. K. (1991). Mechanism of control of trophoblast invasion in situ. Journal of Cellular Physiology, 148(2), 228-234. doi: 10. 1002/jcp. 1041480207.
47. Graham, C. H. (1997). Effect of transforming growth factor-[beta] on the plasminogen activator system in cultured first trimester human cytotrophoblasts. Placenta, 18(2-3), 137-143. doi: 10. 1016/s0143-4004(97)90085-0.
48. Ashkar, A. A., Di Santo, J. P., & Croy, B. A. (2000). Interferon γ contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. The Journal of Experimental Medicine, 192(2), 259-270. doi: 10. 1084/jem. 192. 2. 259.
49. Choi, J. C., Holtz, R., Petroff, M. G., Alfaidy, N., & Murphy, S. P. (2007). Dampening of IFN-γ-inducible gene expression in human choriocarcinoma cells is due to phosphatase-mediated inhibition of the JAK/STAT-1 pathway. The Journal of Immunology, 178(3), 1598-1607.
50. Irving, J. A., Lysiak, J. J., Graham, C. H., Hearn, S., Han, V. K. M., & Lala, P. K. (1995). Characteristic's of trophoblast cells migrating from first trimester chorionic villus explants and propagated in culture. Placenta, 16(5), 413-433. doi: 10. 1016/0143-4004(95)90100-0.
51. Tomimaru, Y., Eguchi, H., Wada, H., Noda, T., Murakami, M., Kobayashi, S., Marubashi, S., Takeda, Y., Tanemura, M., Umeshita, K., Doki, Y., Mori, M., & Nagano, H. (2010) Insulin-like growth factor-binding protein 7 alters the sensitivity to interferon-based anticancer therapy in hepatocellular carcinoma cells. British Journal of Cancer, 102 (10), 1483-1490. doi: http://www. nature. com/bjc/journal/v102/n10/suppinfo/6605669s1. html.
52. Librach, C. L., Werb, Z., Fitzgerald, M. L., Chiu, K., Corwin, N. M., Esteves, R. A., et al. (1991). 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. The Journal of Cell Biology, 113(2), 437-449. doi: 10. 1083/jcb. 113. 2. 437.
53. Cohen, M., Meisser, A., Haenggeli, L., & Bischof, P. (2006). Involvement of MAPK pathway in TNF-α-induced MMP-9 expression in human trophoblastic cells. Molecular Human Reproduction, 12(4), 225-232. doi: 10. 1093/molehr/gal023.
54. Bischoff, P., Meisser, A., & Campana, A. (2000). Paracrine and autocrine regulators of trophoblast invasion-A review. Placenta, 21(Supplement 1), S55-S60. doi: 10. 1053/plac. 2000. 0521.
55. Takahashi, T., & Caviness, V. S. (1993). PCNA-binding to DNA at the G1/S transition in proliferating cells of the developing cerebral wall. Journal of Neurocytology, 22(12), 1096-1102. doi: 10. 1007/bf01235751.
56. Kortylewski, M., Heinrich, P. C., Kauffmann, M. E., Böhm, M., MacKiewicz, A., & Behrmann, I. (2001). Mitogen-activated protein kinases control p27/Kip1 expression and growth of human melanoma cells. Biochemical Journal, 357(1), 297-303.
57. Dworakowska, D., Wlodek, E., Leontiou, C. A., Igreja, S., Cakir, M., Teng, M., et al. (2009). Activation of RAF/MEK/ERK and PI3K/AKT/mTOR pathways in pituitary adenomas and their effects on downstream effectors. Endocrine-Related Cancer, 16(4), 1329-1338. doi: 10. 1677/erc-09-0101.
58. Cho, A., Graves, J., & Reidy, M. A. (2000). Mitogen-activated protein kinases mediate matrix metalloproteinase-9 expression in vascular smooth muscle cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 20(12), 2527-2532. doi: 10. 1161/01. atv. 20. 12. 2527.