p53 Mediates Epidermal Growth Factor (EGF) Induction of MMP-2 Transcription and Trophoblast Invasion

Placenta

Volumn 30, Issue 12, 2009, Pages 1029-1036

  Staun Ram, E ^a   Goldman, S ^a   Shalev, E ^a  

^a Department of Obstetrics and Gynecology   (Israel)

Author keywords

EGF; MMP 2; p53; Trophoblast invasion

Indexed keywords

EPIDERMAL GROWTH FACTOR; GELATINASE A; PROTEIN P53; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR AP 2 ALPHA; TRANSCRIPTION FACTOR AP 2 GAMMA; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP4; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER CELL CULTURE; CELL INVASION; CHORIOCARCINOMA; CONTROLLED STUDY; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION; TROPHOBLAST;

CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN; DNA, ANTISENSE; DRUG COMBINATIONS; EPIDERMAL GROWTH FACTOR; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LAMININ; MATRIX METALLOPROTEINASE 2; OLIGODEOXYRIBONUCLEOTIDES; PLACENTA; PREGNANCY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEOGLYCANS; SP TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR AP-2; TROPHOBLASTS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 70449624784     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2009.09.010     Document Type: Article

References (43)

1. Bischof P., and Campana A. Molecular mediators of implantation. Bailliere's Clin Obstet Gynaecol 14 5 (2000) 801-814
2. Staun-Ram E., and Shalev E. Human trophoblast function during the implantation process. Reprod Biol Endocrinol 3 (2005) 56
3. Bischof P., Martelli M., Campana A., Itoh Y., Ogata Y., and Nagase H. Importance of metalloproteinases (MMP) in human trophoblast invasion. Early Pregnancy Biol Med 1 (1995) 263-269
4. Staun-Ram E., Goldman S., Gabarin D., and Shalev E. Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and -9) in human trophoblast invasion. Reprod Biol Endocrinol 2 (2004) 59
5. Xu P., Wang Y., Zhu S., Luo S., Piao Y., and Zhuang L. Expression of matrix metalloproteinase-2, -9 and -14, tissue inhibitors of metalloproteinse-1, and matrix proteins in human placenta during the first trimester. Biol Reprod 62 (2000) 988-994
6. Di Simone N., Di Nicuolo F., Sanguinetti M., Ferrazzani S., D'Alessio M.C., Castellani R., et al. Low-molecular weight heparin induces in vitro trophoblast invasiveness: role of matrix metalloproteinases and tissue inhibitors. Placenta 28 4 (2007) 298-304
7. Anteby E.Y., Greenfield C., Natanson-Yaron S., Goldman-Wohl D., Hamani Y., Khudyak V., et al. Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod 10 4 (2004) 229-235
8. Qiu Q., Yang M., Tsang B.K., and Gruslin A. EGF-induced trophoblast secretion of MMP-9 and TIMP-1 involves activation of both PI3K and MAPK signaling pathways. Reproduction 128 3 (2004) 355-363
9. Bass K.E., Morrish D., Roth I., Bjardwaj D., Taylor R., Zhou Y., et al. Human cytotrophoblast invasion is up-regulated by epidermal growth factor: evidence that paracrine factors modify this process. Dev Biol 164 2 (1994) 550-561
10. Sternlicht M.D., and Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17 (2001) 463-516
11. Qin H., Sun Y., and Benveniste E.N. The transcription factors Sp1, Sp3, and AP-2 are required for constitutive matrix metalloproteinase-2 gene expression in astroglioma cells. J Biol Chem 274 41 (1999) 29130-29137
12. Blaschitz A., Weiss U., Dohr G., and Desoye G. Antibody reaction patterns in first trimester placenta: implications for trophoblast isolation and purity screening. Placenta 21 (2000) 733-741
13. Abdelrahim M., and Safe S. Cyclooxygenase-2 inhibitors decrease vascular endothelial growth factor expression in colon cancer cells by enhanced degradation of Sp1 and Sp4 proteins. Mol Pharmacol 68 2 (2005) 317-329
14. Saperschnig A., Koch F., Rischitor G., Mennenga T., and Suske G. Complexity of translationally controlled transcription factor Sp3 isoform expression. J Biol Chem 279 40 (2004) 42095-42105
15. Pan M.R., and Hung W.C. Nonsteroidal anti-flammatory drugs inhibit matrix metalloproteinase-2 via suppression of the ERK/SP1- mediated transcription. J Biol Chem 277 (2002) 32775-32780
16. Bergman M.R., Cheng S., Honbo N., Piacentini L., Karliner J.S., and Lovett D.H. A functional activating protein 1 (AP-1) site regulates matrix metalloproteinase 2 (MMP-2) transcription by cardiac cells through interactions with JunB-Fra1 and JunB-FosB heterodimers. Biochem J 369 Pt 3 (2003) 485-496
17. Bian J., and Sun Y. Transcriptional activation by p53 of the human type IV collagenase (gelatinase A or matrix metalloproteinase 2) promoter. Mol Cell Biol 17 11 (1997) 6330-6338
18. Frisch S.M., and Morisaki J.H. Positive and negative transcriptional elements of the human type IV collagenase gene. Mol Cell Biol 10 12 (1990) 6524-6532
19. Zhou W.H., Du M.R., Dong L., Zhu X.Y., Yang J.Y., He Y.Y., et al. Cyclosporin A increases expression of matrix metalloproteinase 9 and 2 and invasiveness in vitro of the first-trimester human trophoblast cells via the mitogen-activated protein kinase pathway. Hum Reprod 22 10 (2007) 2743-2750
20. Prast J., Saleh L., Husslein H., Sonseregger S., Helmer H., and Knöfler M. Human chorionic gonadotrophin stimulates trophoblast invasion through ERK and AKT signaling. Endocrinology 149 3 (2008) 979-987
21. Lin H.Y., Yang Q., Wang H.M., Qi J.G., Zhang H., Wang H.X., et al. Involvement of SMAD4, but not of SMAD2, in transforming growth factor-beta1-induced trophoblast expression of matrix metalloproteinase-2. Front Biosci 11 (2006) 637-646
22. Goldman S., and Shalev E. A proposed mechanism for progesterone regulation of trophoblast MMP2 transcription independent of classical progesterone response elements on its promoter. J Exp Clin Assist Reprod 6 3 (2006) 4
23. Goldman S., and Shalev E. Difference in progesterone-receptor isoforms ratio between early and late first-trimester human trophoblast is associated with differential cell invasion and matrix metalloproteinase 2 expression. Biol Reprod 74 1 (2006) 13-22
24. El-Deiry W.S., Kern S., Pietenpol J.A., Kinzler K.W., and Vogelstein B. Definition of a consensus binding site for p53. Nat Gene 1 1 (1992) 45-49
25. Ludes-Meyers J.H., Subler M.A., Shivakumar C.V., Munoz R.M., Jiang P., Bigger J.E., et al. Transcriptional activation of the human epidermal growth factor receptor promoter by human p53. Mol Cell Biol 16 11 (1996) 6009-6019
26. Miyashita T., and Reed J.C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80 2 (1995) 239-293
27. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell 88 3 (1997) 323-331
28. Somasundaram K., Jayaraman G., Williams T., Moran E., Frisch S., and Thimmapaya B. Repression of a matrix metalloprotease gene by E1A correlates with its ability to bind to cell type-specific transcription factor AP-2. Proc Natl Acad Sci U S A 93 7 (1996) 3088-3093
29. Hickson J.A., Fong B., Watson P.H., and Watson A.J. PP2Cdelta (Ppm1d, WIP1), an endogenous inhibitor of p38 MAPK, is regulated along with Trp53 and Cdkn2a following p38 MAPK inhibition during mouse preimplantation development. Mol Reprod Dev 74 7 (2007) 821-834
30. Jurisicova A., Latham K.E., Casper R.F., Casper R.F., and Varmuza S.L. Expression and regulation of genes associated with cell death during murine preimplantation embryo development. Mol Reprod Dev 51 3 (1998) 243-253
31. Komatsu D., Abe T., Sano Y., Shimazaki K., Tomita M., Kanayama N., et al. Increase of the trophoblast giant cells with prolactin-releasing peptide (PrRP) receptor expression in p53-null mice. Mol Reprod Dev 74 9 (2007) 1089-1094
32. Gudkov A.V., and Komarova E.A. Dangerous habits of a security guard: the two faces of p53 as a drug target. Hum Mol Genet 16 Spec No 1 (2007) R67-R72
33. Cohen M., Meisser A., Haenggeli L., Irminger-Finger I., and Bischof P. Status of p53 in first-trimester cytotrophoblastic cells. Mol Hum Reprod 13 2 (2007) 111-116
34. Marzusch K., Ruck P., Horny H.P., Dietl J., and Kaiserling E. Expression of the p53 tumour suppressor gene in human placenta: an immunohistochemical study. Placenta 16 1 (1995) 101-104
35. Cohen M., Wuillemin C., and Bischof P. Trophoblastic p53 is stabilised by a cis-trans isomerisation necessary for the formation of high molecular weight complexes involving the N-terminus of p53. Biochimie 90 6 (2008) 855-862
36. Levy R., Smith S.D., Yusuf K., Huettner P.C., Kraus F.T., Sadovsky Y., et al. Trophoblast apoptosis from pregnancies complicated by fetal growth restriction is associated with enhanced p53 expression. Am J Obstet Gynecol 186 5 (2002) 1056-1061
37. Haezell A.E., Lacey H.A., Jones C.J., Huppertz B., Baker P.N., and Crocker I.P. Effects of oxygen on cell turnover and expression of regulators of apoptosis in human placental trophoblast. Placenta 29 2 (2008) 175-186
38. Kale A., Sövlemez F., and Ensari A. Expressions of proliferation markers (Ki-67, proliferating cell nuclear antigen, and silver-staining nucleolar organizer regions) and of p53 tumor protein in gestational trophoblastic disease. Am J Obstet Gynecol 184 4 (2001) 567-574
39. Petignat P., Laurini R., Goffins F., Bruchim I., and Bischof P. Expression of matrix metalloproteinase-2 and mutant p53 is increased in hydatidiform mole as compared with normal placenta. Int J Gynecol Cancer 16 4 (2006) 1679-1684
40. Cheung A.N., Srivastava G., Chung L.P., Ngan H.Y., Man T.K., Liu Y.T., et al. Expression of the p53 gene in trophoblastic cells in hydatidiform moles and normal human placentas. J Reprod Med 39 3 (1994) 223-227
41. Fulop V., Mok S.C., Genest D.R., Gati I., Doszpod J., and Berkowitz R.S. p53, p21, Rb and mdm2 oncoproteins. Expression in normal placenta, partial and complete mole, and choriocarcinoma. J Reprod Med 43 2 (1998) 119-127
42. Halperin R., Peller S., Sandbank J., Bukovsky I., and Schneider D. Expression of the p53 gene and apoptosis in gestational trophoblastic disease. Placenta 21 1 (2000) 58-62
43. Cohen M., Wuillemin C., Irion O., and Bischof P. Regulation of MMP-9 by p53 in first trimester cytotrophoblastic cells. Hum Reprod 23 10 (2008) 2273-2281