Matrix metalloproteinase 9 is a distal-less 3 target-gene in placental trophoblast cells

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 2, 2013, Pages

  Clark, Patricia A ^a   Xie, Jianjun ^a   Li, Sha ^a   Zhang, Xuesen ^a   Coonrod, Scott ^a   Roberson, Mark S ^a  

^a Cornell University ^*  (United States)

Author keywords

Distal less 3; Human; Matrix metalloproteinase; Mouse; Placental trophoblast

Indexed keywords

DISTAL LESS 3 PROTEIN; GELATINASE B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; TROPHOBLAST;

DISTAL-LESS 3; HUMAN; MATRIX METALLOPROTEINASE; MOUSE; PLACENTAL TROPHOBLAST;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CHORIOCARCINOMA; FEMALE; GELATINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; PROTEIN BINDING; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84880180452     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00205.2012     Document Type: Article

References (49)

1. Backstrom JR, Tokes ZA. The 84-kDa form of human matrix metalloproteinase-9 degrades substance P and gelatin. J Neurochem 64: 1312-1318, 1995.
2. Belotti D, Paganoni P, Manenti L, Garofalo A, Marchini S, Taraboletti G, Giavazzi R. Matrix metalloproteinases (MMP9 and MMP2) induce the release of vascular endothelial growth factor (VEGF) by ovarian carcinoma cells: implications for ascites formation. Cancer Res 63: 5224-5229, 2003.
3. Berghorn KA, Clark PA, Encarnacion B, Deregis CJ, Folger JK, Morasso MI, Soares MJ, Wolfe MW, Roberson MS. Developmental expression of the homeobox protein Distal-less 3 and its relationship to progesterone production in mouse placenta. J Endocrinol 186: 315-323, 2005.
4. Berghorn KA, Clark-Campbell PA, Han L, McGrattan M, Weiss RS, Roberson MS. Smad6 represses Dlx3 transcriptional activity through inhibition of DNA binding. J Biol Chem 281: 20357-20367, 2006.
5. Campbell S, Rowe J, Jackson CJ, Gallery ED. Interaction of cocultured decidual endothelial cells and cytotrophoblasts in preeclampsia. Biol Reprod 71: 244-252, 2004.
6. Capobianco E, White V, Sosa M, Di M, I, Basualdo MN, Faingold MC, Jawerbaum A. Regulation of matrix metalloproteinases 2 and 9 activities by peroxynitrites in term placentas from type 2 diabetic patients. Reprod Sci 19: 814-822, 2012.
7. De SD, Nicolaus G, Maiuri MC, Cipolletta D, Galluzzi L, Cinelli MP, Tajana G, Iuvone T, Carnuccio R. NF-kappaB blockade upregulates Bax, TSP-1, and TSP-2 expression in rat granulation tissue. J Mol Med 87: 481-492, 2009.
8. Depew MJ, Simpson CA, Morasso M, Rubenstein JL. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J Anat 207: 501-561, 2005.
9. Gallery ED, Campbell S, Arkell J, Nguyen M, Jackson CJ. Preeclamptic decidual microvascular endothelial cells express lower levels of matrix metalloproteinase-1 than normals. Microvasc Res 57: 340-346, 1999.
10. Gargioli C, Coletta M, De GF, Cannata SM, Cossu G. PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat Med 14: 973-978, 2008.
11. Han L, Dias FM, Berghorn KA, Iwata TN, Clark-Campbell PA, Welsh IC, Wang W, O'Brien TP, Lin DM, Roberson MS. Analysis of the gene regulatory program induced by the homeobox transcription factor distal-less 3 in mouse placenta. Endocrinology 148: 1246-1254, 2007.
12. Harris LK, Keogh RJ, Wareing M, Baker PN, Cartwright JE, Whitley GS, Aplin JD. BeWo cells stimulate smooth muscle cell apoptosis and elastin breakdown in a model of spiral artery transformation. Hum Reprod 22: 2834-2841, 2007.
13. Herron GS, Banda MJ, Clark EJ, Gavrilovic J, Werb Z. Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J Biol Chem 261: 2814-2818, 1986.
14. Herron GS, Werb Z, Dwyer K, Banda MJ. Secretion of metalloproteinases by stimulated capillary endothelial cells. I. Production of procollagenase and prostromelysin exceeds expression of proteolytic activity. J Biol Chem 261: 2810-2813, 1986.
15. Hibbs MS, Hoidal JR, Kang AH. Expression of a metalloproteinase that degrades native type V collagen and denatured collagens by cultured human alveolar macrophages. J Clin Invest 80: 1644-1650, 1987.
16. Huisman MA, Timmer A, Zeinstra M, Serlier EK, Hanemaaijer R, Goor H, Erwich JJ. Matrix-metalloproteinase activity in first trimester placental bed biopsies in further complicated and uncomplicated pregnancies. Placenta 25: 253-258, 2004.
17. Ito A, Mukaiyama A, Itoh Y, Nagase H, Thogersen IB, Enghild JJ, Sasaguri Y, Mori Y. Degradation of interleukin 1beta by matrix metalloproteinases. J Biol Chem 271: 14657-14660, 1996.
18. Kamochi J, Tokunaga T, Tomii Y, Abe Y, Hatanaka H, Kijima H, Yamazaki H, Watanabe N, Matsuzaki S, Ueyama Y, Nakamura M. Overexpression of the thrombospondin 2 (TSP2) gene modulated by the matrix metalloproteinase family expression and production in human colon carcinoma cell line. Oncol Rep 10: 881-884, 2003.
19. Khong TY, Lane EB, Robertson WB. An immunocytochemical study of fetal cells at the maternal-placental interface using monoclonal antibodies to keratins, vimentin and desmin. Cell Tissue Res 246: 189-195, 1986.
20. Kobayashi T, Kishimoto J, Ge Y, Jin W, Hudson DL, Ouahes N, Ehama R, Shinkai H, Burgeson RE. A novel mechanism of matrix metalloproteinase-9 gene expression implies a role for keratinization. EMBO Rep 2: 604-608, 2001.
21. Krady MM, Zeng J, Yu J, MacLauchlan S, Skokos EA, Tian W, Bornstein P, Sessa WC, Kyriakides TR. Thrombospondin-2 modulates extracellular matrix remodeling during physiological angiogenesis. Am J Pathol 173: 879-891, 2008.
22. Kyriakides TR, Wulsin D, Skokos EA, Fleckman P, Pirrone A, Shipley JM, Senior RM, Bornstein P. Mice that lack matrix metalloproteinase-9 display delayed wound healing associated with delayed reepithelization and disordered collagen fibrillogenesis. Matrix Biol 28: 65-73, 2009.
23. Lelongt B, Bengatta S, Delauche M, Lund LR, Werb Z, Ronco PM. Matrix metalloproteinase 9 protects mice from anti-glomerular basement membrane nephritis through its fibrinolytic activity. J Exp Med 193: 793-802, 2001.
24. Li JK, Xiong Q, Zhou S, Yang PF. [Differences between the expression of matrix metalloproteinase-2, 9 in preeclampsia and normal placental tissues]. Zhonghua Fu Chan Ke Za Zhi 42: 73-75, 2007.
25. Liu Z, Zhou X, Shapiro SD, Shipley JM, Twining SS, Diaz LA, Senior RM, Werb Z. The serpin alpha1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell 102: 647-655, 2000.
26. Lockwood CJ, Oner C, Uz YH, Kayisli UA, Huang SJ, Buchwalder LF, Murk W, Funai EF, Schatz F. Matrix metalloproteinase 9 (MMP9) expression in preeclamptic decidua and MMP9 induction by tumor necrosis factor alpha and interleukin 1 beta in human first trimester decidual cells. Biol Reprod 78: 1064-1072, 2008.
27. MacLauchlan S, Skokos EA, Agah A, Zeng J, Tian W, Davidson JM, Bornstein P, Kyriakides TR. Enhanced angiogenesis and reduced contraction in thrombospondin-2-null wounds is associated with increased levels of matrix metalloproteinases-2 and-9, and soluble VEGF. J Histochem Cytochem 57: 301-313, 2009.
28. Martinez N, Sosa M, Higa R, Fornes D, Capobianco E, Jawerbaum A. Dietary treatments enriched in olive and safflower oils regulate seric and placental matrix metalloproteinases in maternal diabetes. Placenta 33: 8-16, 2012.
29. McFadyen IR, Price AB, Geirsson RT. The relation of birthweight to histological appearances in vessels of the placental bed. Br J Obstet Gynaecol 93: 476-481, 1986.
30. Morasso MI, Grinberg A, Robinson G, Sargent TD, Mahon KA. Placental failure in mice lacking the homeobox gene Dlx3. Proc Natl Acad Sci USA 96: 162-167, 1999.
31. Morasso MI, Markova NG, Sargent TD. Regulation of epidermal differentiation by a Distal-less homeodomain gene. J Cell Biol 135: 1879-1887, 1996.
32. Nakamura M, Oida Y, Abe Y, Yamazaki H, Mukai M, Matsuyama M, Chijiwa T, Matsumoto H, Ueyama Y. Thrombospondin-2 inhibits tumor cell invasion through the modulation of MMP-9 and uPA in pancreatic cancer cells. Mol Med Rep 1: 423-427, 2008.
33. Paiva P, Salamonsen LA, Manuelpillai U, Dimitriadis E. Interleukin 11 inhibits human trophoblast invasion indicating a likely role in the decidual restraint of trophoblast invasion during placentation. Biol Reprod 80: 302-310, 2009.
34. Palei AC, Sandrim VC, Cavalli RC, Tanus-Santos JE. Comparative assessment of matrix metalloproteinase (MMP)-2 and MMP-9, and their inhibitors, tissue inhibitors of metalloproteinase (TIMP)-1 and TIMP-2 in preeclampsia and gestational hypertension. Clin Biochem 41: 875-880, 2008.
35. Park GT, Morasso MI. Regulation of the Dlx3 homeobox gene upon differentiation of mouse keratinocytes. J Biol Chem 274: 26599-26608, 1999.
36. Pennington KA, Schlitt JM, Jackson DL, Schulz LC, Schust DJ. Preeclampsia: multiple approaches for a multifactorial disease. Dis Model Mech 5: 9-18, 2012.
37. Pijnenborg R, Anthony J, Davey DA, Rees A, Tiltman A, Vercruysse L, van AA. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 98: 648-655, 1991.
38. Pijnenborg R, Bland JM, Robertson WB, Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 4: 397-413, 1983.
39. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 27: 939-958, 2006.
40. Qiao C, Wang CH, Shang T, Lin QD. [Clinical significance of KiSS-1 and matrix metalloproteinase-9 expression in trophoblasts of women with preeclampsia and their relation to perinatal outcome of neonates]. Zhonghua Fu Chan Ke Za Zhi 40: 585-590, 2005.
41. Roberson MS, Meermann S, Morasso MI, Mulvaney-Musa JM, Zhang T. A role for the homeobox protein Distal-less 3 in the activation of the glycoprotein hormone alpha subunit gene in choriocarcinoma cells. J Biol Chem 276: 10016-10024, 2001.
42. Roberson MS, Misra-Press A, Laurance ME, Stork PJ, Maurer RA. A role for mitogen-activated protein kinase in mediating activation of the glycoprotein hormone alpha-subunit promoter by gonadotropin-releasing hormone. Mol Cell Biol 15: 3531-3539, 1995.
43. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet 2: 538-548, 2001.
44. Shokry M, Omran OM, Hassan HI, Elsedfy GO, Hussein MR. Expression of matrix metalloproteinases 2 and 9 in human trophoblasts of normal and preeclamptic placentas: preliminary findings. Exp Mol Pathol 87: 219-225, 2009.
45. Stetler-Stevenson WG. The tumor microenvironment: regulation by MMP-independent effects of tissue inhibitor of metalloproteinases-2. Cancer Metastasis Rev 27: 57-66, 2008.
46. Udayashankar R, Baker D, Tuckerman E, Laird S, Li TC, Moore HD. Characterization of invasive trophoblasts generated from human embryonic stem cells. Hum Reprod 26: 398-406, 2011.
47. Wang A, Rana S, Karumanchi SA. Preeclampsia: the role of angiogenic factors in its pathogenesis. Physiology (Bethesda) 24: 147-158, 2009.
48. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 14: 163-176, 2000.
49. Zhang H, Lin QD, Qiao C. [Expression of trophoblast invasion related genes mRNA and protein in human placenta in preeclampsia]. Zhonghua Fu Chan Ke Za Zhi 41: 509-513, 2006.