Transient RNA silencing of tissue factor pathway inhibitor-2 modulates lung cancer cell invasion

Clinical and Experimental Metastasis

Volumn 26, Issue 5, 2009, Pages 457-467

  Iochmann, Sophie ^a,b   Bléchet, Claire ^a,c   Chabot, Valérie ^d   Saulnier, Annabelle ^a   Amini, Aniça ^a   Gaud, Guillaume ^a   Gruel, Yves ^a,b   Reverdiau, Pascale ^a,b  

^a UNIVERSITÉ DE TOURS   (France)

^b SERVICE DE DERMATOLOGIE   (France)

^c CHU BRETONNEAU   (France)

^d ETABLISSEMENT FRANÇAIS DU SANG   (France)

Author keywords

Cell invasion; Metalloproteinases; Non small cell lung cancer; SiRNA; TFPI 2

Indexed keywords

GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; MESSENGER RNA; PLACENTA PROTEIN 5; RNA; SMALL INTERFERING RNA; STROMELYSIN;

ARTICLE; CANCER CELL CULTURE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; LUNG NON SMALL CELL CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GLYCOPROTEINS; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NEOPLASM INVASIVENESS; RNA; RNA, SMALL INTERFERING;

EID: 67349145253     PISSN: 02620898     EISSN: 15737276     Source Type: Journal    
DOI: 10.1007/s10585-009-9245-z     Document Type: Article

References (66)

1. M Egeblad Z Werb 2002 New functions for the matrix metalloproteinases in cancer progression Nat Rev Cancer 2 3 161 174 10.1038/nrc745 (Pubitemid 37328786)
2. I Stamenkovic 2003 Extracellular matrix remodelling: the role of matrix metalloproteinases J Pathol 200 4 448 464 10.1002/path.1400
3. P Vihinen VM Kahari 2002 Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets Int J Cancer 99 2 157 166 10.1002/ijc.10329
4. J Westermarck VM Kahari 1999 Regulation of matrix metalloproteinase expression in tumor invasion FASEB J 13 8 781 792 (Pubitemid 29220691)
5. A Noel M Jost E Maquoi 2008 Matrix metalloproteinases at cancer tumor-host interface Semin Cell Dev Biol 19 1 52 60 10.1016/j.semcdb.2007.05.011
6. M Polette B Nawrocki-Raby C Gilles 2004 Tumour invasion and matrix metalloproteinases Crit Rev Oncol Hematol 49 3 179 186 10.1016/j.critrevonc. 2003.10.008
7. M Bjorklund E Koivunen 2005 Gelatinase-mediated migration and invasion of cancer cells Biochim Biophys Acta 1755 1 37 69 (Pubitemid 40720240)
8. HS Chand DC Foster W Kisiel 2005 Structure, function and biology of tissue factor pathway inhibitor-2 Thromb Haemost 94 6 1122 1130 (Pubitemid 41819605)
9. LC Petersen CA Sprecher DC Foster 1996 Inhibitory properties of a novel human Kunitz-type protease inhibitor homologous to tissue factor pathway inhibitor Biochemistry 35 1 266 272 10.1021/bi951501d
10. CN Rao S Mohanam A Puppala 1999 Regulation of ProMMP-1 and ProMMP-3 activation by tissue factor pathway inhibitor-2/matrix-associated serine protease inhibitor Biochem Biophys Res Commun 255 1 94 98 10.1006/bbrc.1999.0153
11. M Iino DC Foster W Kisiel 1998 Quantification and characterization of human endothelial cell-derived tissue factor pathway inhibitor-2 Arterioscler Thromb Vasc Biol 18 1 40 46 (Pubitemid 28047597)
12. S Iochmann P Reverdiau-Moalic F Hube 2002 Demonstration of inducible TFPI-2 mRNA synthesis in BeWo and JEG-3 trophoblast cells using a competitive RT-PCR Thromb Res 105 3 217 223 10.1016/S0049-3848(02)00018-X
13. CN Rao YY Liu CL Peavey 1995 Novel extracellular matrix-associated serine proteinase inhibitors from human skin fibroblasts Arch Biochem Biophys 317 1 311 314 10.1006/abbi.1995.1168
14. J Ortego J Escribano M Coca-Prados 1997 Gene expression of proteases and protease inhibitors in the human ciliary epithelium and ODM-2 cells Exp Eye Res 65 2 289 299 10.1006/exer.1997.0333
15. JT Crawley DA Goulding V Ferreira 2002 Expression and localization of tissue factor pathway inhibitor-2 in normal and atherosclerotic human vessels Arterioscler Thromb Vasc Biol 22 2 218 224 10.1161/hq0102.101842
16. F Hube P Reverdiau S Iochmann 2003 Demonstration of a tissue factor pathway inhibitor 2 messenger RNA synthesis by pure villous cytotrophoblast cells isolated from term human placentas Biol Reprod 68 5 1888 1894 10.1095/biolreprod.102.011858
17. N Lanir A Aharon B Brenner 2003 Procoagulant and anticoagulant mechanisms in human placenta Semin Thromb Hemost 29 2 175 184 10.1055/s-2003-38833
18. SD Konduri CN Rao N Chandrasekar 2001 A novel function of tissue factor pathway inhibitor-2 (TFPI-2) in human glioma invasion Oncogene 20 47 6938 6945 10.1038/sj.onc.1204847
19. CN Rao SS Lakka Y Kin 2001 Expression of tissue factor pathway inhibitor 2 inversely correlates during the progression of human gliomas Clin Cancer Res 7 3 570 576 (Pubitemid 32707980)
20. J Rollin S Iochmann C Blechet 2005 Expression and methylation status of tissue factor pathway inhibitor-2 gene in non-small-cell lung cancer Br J Cancer 92 4 775 783 10.1038/sj.bjc.6602298
21. MZ Wojtukiewicz E Sierko L Zimnoch 2003 Immunohistochemical localization of tissue factor pathway inhibitor-2 in human tumor tissue Thromb Haemost 90 1 140 146 (Pubitemid 36873870)
22. M Jin K Udagawa E Miyagi 2001 Expression of serine proteinase inhibitor PP5/TFPI-2/MSPI decreases the invasive potential of human choriocarcinoma cells in vitro and in vivo Gynecol Oncol 83 2 325 333 10.1006/gyno.2001.6394
23. CM Wong YL Ng JM Lee 2007 Tissue factor pathway inhibitor-2 as a frequently silenced tumor suppressor gene in hepatocellular carcinoma Hepatology (Baltimore, Md.) 45 5 1129 1138 10.1002/hep.21578
24. H Guo Y Lin H Zhang 2007 Tissue factor pathway inhibitor-2 was repressed by CpG hypermethylation through inhibition of KLF6 binding in highly invasive breast cancer cells BMC Mol Biol 8 110 10.1186/1471-2199-8-110
25. F Hube P Reverdiau S Iochmann 2003 Transcriptional silencing of the TFPI-2 gene by promoter hypermethylation in choriocarcinoma cells Biol Chem 384 7 1029 1034 10.1515/BC.2003.115
26. SD Konduri KS Srivenugopal N Yanamandra 2003 Promoter methylation and silencing of the tissue factor pathway inhibitor-2 (TFPI-2), a gene encoding an inhibitor of matrix metalloproteinases in human glioma cells Oncogene 22 29 4509 4516 10.1038/sj.onc.1206695
27. Y Nobeyama E Okochi-Takada J Furuta 2007 Silencing of tissue factor pathway inhibitor-2 gene in malignant melanomas Int J Cancer 121 2 301 307 10.1002/ijc.22637
28. SM Pulukuri S Patibandla J Patel 2007 Epigenetic inactivation of the tissue inhibitor of metalloproteinase-2 (TIMP-2) gene in human prostate tumors Oncogene 26 36 5229 5237 10.1038/sj.onc.1210329
29. CN Rao T Segawa JR Navari 2003 Methylation of TFPI-2 gene is not the sole cause of its silencing Int J Oncol 22 4 843 848
30. N Sato AR Parker N Fukushima 2005 Epigenetic inactivation of TFPI-2 as a common mechanism associated with growth and invasion of pancreatic ductal adenocarcinoma Oncogene 24 5 850 858 10.1038/sj.onc.1208050
31. DM Dykxhoorn CD Novina PA Sharp 2003 Killing the messenger: short RNAs that silence gene expression. Nature Reviews Mol Cell Biol 4 6 457 467 10.1038/nrm1129
32. R Blindt F Vogt D Lamby 2002 Characterization of differential gene expression in quiescent and invasive human arterial smooth muscle cells J Vasc Res 39 4 340 352 10.1159/000065546
33. V Chabot P Reverdiau S Iochmann 2006 CCL5-enhanced human immature dendritic cell migration through the basement membrane in vitro depends on matrix metalloproteinase-9 J Leukoc Biol 79 4 767 778 10.1189/jlb.0804464
34. SM Pulukuri B Gorantla JS Rao 2007 Inhibition of histone deacetylase activity promotes invasion of human cancer cells through activation of urokinase plasminogen activator J Biol Chem 282 49 35594 35603 10.1074/jbc.M705867200
35. P Kempaiah HS Chand W Kisiel 2007 Identification of a human TFPI-2 splice variant that is upregulated in human tumor tissues Mol Cancer 6 20 10.1186/1476-4598-6-20
36. L Aagaard JJ Rossi 2007 RNAi therapeutics: principles, prospects and challenges Adv Drug Deliv Rev 59 2-3 75 86 10.1016/j.addr.2007.03.005
37. MK Montgomery S Xu A Fire 1998 RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans Proc Natl Acad Sci USA 95 26 15502 15507 10.1073/pnas.95.26.15502
38. L Timmons A Fire 1998 Specific interference by ingested dsRNA Nature 395 6705 854 10.1038/27579
39. TV Achenbach B Brunner K Heermeier 2003 Oligonucleotide-based knockdown technologies: antisense versus RNA interference Chem Bio Chem 4 10 928 935 10.1002/cbic.200300708
40. JR Bertrand M Pottier A Vekris 2002 Comparison of antisense oligonucleotides and siRNAs in cell culture and in vivo Biochem Biophys Res Commun 296 4 1000 1004 10.1016/S0006-291X(02)02013-2
41. B Bilanges D Stokoe 2005 Direct comparison of the specificity of gene silencing using antisense oligonucleotides and RNAi Biochem J 388 Pt 2 573 583 10.1042/BJ20041956
42. SM Elbashir J Harborth W Lendeckel 2001 Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells Nature 411 6836 494 498 10.1038/35078107
43. TC Wun KK Kretzmer TJ Girard 1988 Cloning and characterization of a cDNA coding for the lipoprotein-associated coagulation inhibitor shows that it consists of three tandem Kunitz-type inhibitory domains J Biol Chem 263 13 6001 6004 (Pubitemid 18121620)
44. CA Sprecher W Kisiel S Mathewes 1994 Molecular cloning, expression, and partial characterization of a second human tissue-factor-pathway inhibitor Proc Natl Acad Sci USA 91 8 3353 3357 10.1073/pnas.91.8.3353 (Pubitemid 24130235)
45. SS Lakka SD Konduri S Mohanam 2000 In vitro modulation of human lung cancer cell line invasiveness by antisense cDNA of tissue factor pathway inhibitor-2 Clin Exp Metastasis 18 3 239 244 10.1023/A:1006755223357
46. SD Konduri A Tasiou N Chandrasekar 2000 Role of tissue factor pathway inhibitor-2 (TFPI-2) in amelanotic melanoma (C-32) invasion Clin Exp Metastasis 18 4 303 308 10.1023/A:1011085820250
47. SD Konduri A Tasiou N Chandrasekar 2001 Overexpression of tissue factor pathway inhibitor-2 (TFPI-2), decreases the invasiveness of prostate cancer cells in vitro Int J Oncol 18 1 127 131
48. N Yanamandra S Kondraganti CS Gondi 2005 Recombinant adeno-associated virus (rAAV) expressing TFPI-2 inhibits invasion, angiogenesis and tumor growth in a human glioblastoma cell line Int J Cancer 115 6 998 1005 10.1002/ijc.20965
49. S Kondraganti CS Gondi M Gujrati 2006 Restoration of tissue factor pathway inhibitor inhibits invasion and tumor growth in vitro and in vivo in a malignant meningioma cell line Int J Oncol 29 1 25 32
50. CN Rao B Cook Y Liu 1998 HT-1080 fibrosarcoma cell matrix degradation and invasion are inhibited by the matrix-associated serine protease inhibitor TFPI-2/33 kDa MSPI Int J Cancer 76 5 749 756 10.1002/(SICI)1097-0215(19980529) 76:5<749::AID-IJC21>3.0.CO;2-Y
51. H Izumi C Takahashi J Oh 2000 Tissue factor pathway inhibitor-2 suppresses the production of active matrix metalloproteinase-2 and is down-regulated in cells harboring activated ras oncogenes FEBS Lett 481 1 31 36 10.1016/S0014-5793(00)01902-5
52. D Kong D Ma H Bai 2004 Expression and characterization of the first kunitz domain of human tissue factor pathway inhibitor-2 Biochem Biophys Res Commun 324 4 1179 1185 10.1016/j.bbrc.2004.09.179
53. HS Chand X Du D Ma 2004 The effect of human tissue factor pathway inhibitor-2 on the growth and metastasis of fibrosarcoma tumors in athymic mice Blood 103 3 1069 1077 10.1182/blood-2003-06-1930
54. M Shibuya H Okamoto T Nozawa 2007 Proteomic and transcriptomic analyses of retinal pigment epithelial cells exposed to REF-1/TFPI-2 Invest Ophthalmol Vis Sci 48 2 516 521 10.1167/iovs.06-0434
55. M Seiki 2003 Membrane-type 1 matrix metalloproteinase: a key enzyme for tumor invasion Cancer Lett 194 1 1 11 10.1016/S0304-3835(02)00699-7
56. NE Sounni A Noel 2005 Membrane type-matrix metalloproteinases and tumor progression Biochimie 87 3-4 329 342 10.1016/j.biochi.2004.07.012
57. JT Huntington JM Shields CJ Der 2004 Overexpression of collagenase 1 (MMP-1) is mediated by the ERK pathway in invasive melanoma cells: role of BRAF mutation and fibroblast growth factor signaling J Biol Chem 279 33168 33176 10.1074/jbc.M405102200
58. SM Pulukuri JS Rao 2008 Matrix metalloproteinase-1 promotes prostate tumor growth and metastasis Int J Oncol 32 4 757 765
59. K Sossey-Alaoui TA Ranalli X Li 2005 WAVE3 promotes cell motility and invasion through the regulation of MMP-1, MMP-3, and MMP-9 expression Exp Cell Res 308 1 135 145 10.1016/j.yexcr.2005.04.011
60. CE Brinckerhoff JL Rutter U Benbow 2000 Interstitial collagenases as markers of tumor progression Clin Cancer Res 6 12 4823 4830 (Pubitemid 32110426)
61. S Cheng M Tada Y Hida 2008 High MMP-1 mRNA Expression is a Risk Factor for Disease-Free and Overall Survivals in Patients with Invasive Breast Carcinoma J Surg Res 146 1 104 109 10.1016/j.jss.2007.05.032
62. JS Blackburn CH Rhodes CI Coon 2007 RNA interference inhibition of matrix metalloproteinase-1 prevents melanoma metastasis by reducing tumor collagenase activity and angiogenesis Cancer Res 67 22 10849 10858 10.1158/0008-5472.CAN-07- 1791
63. X Jiang CM Dutton WN Qi 2005 siRNA mediated inhibition of MMP-1 reduces invasive potential of a human chondrosarcoma cell line J Cell Physiol 202 3 723 730 10.1002/jcp.20162
64. J George CS Gondi DH Dinh 2007 Restoration of tissue factor pathway inhibitor-2 in a human glioblastoma cell line triggers caspase-mediated pathway and apoptosis Clin Cancer Res 13 12 3507 3517 10.1158/1078-0432.CCR-06-3023
65. A Tasiou SD Konduri N Yanamandra 2001 A novel role of tissue factor pathway inhibitor-2 in apoptosis of malignant human gliomas Int J Oncol 19 3 591 597
66. L Ivanciu RD Gerard H Tang 2007 Adenovirus-mediated expression of tissue factor pathway inhibitor-2 inhibits endothelial cell migration and angiogenesis Arterioscler Thromb Vasc Biol 27 2 310 316 10.1161/01.ATV.0000254147.89321.cf