TFPI-2 silencing increases tumour progression and promotes metalloproteinase 1 and 3 induction through tumour-stromal cell interactions

Journal of Cellular and Molecular Medicine

Volumn 15, Issue 2, 2011, Pages 196-208

  Gaud, Guillaume ^a   Iochmann, Sophie ^a   Guillon Munos, Audrey ^a   Brillet, Benjamin ^a   Petiot, Stéphanie ^a   Seigneuret, Florian ^a   Touzé, Antoine ^a   Heuzé Vourc'h, Nathalie ^a   Courty, Yves ^a   Lerondel, Stéphanie ^b   Gruel, Yves ^a,c   Reverdiau, Pascale ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b hôpital d'Orléans   (France)

^c SERVICE DE DERMATOLOGIE   (France)

Author keywords

Cell adhesion; Cell invasion; Integrins; Matrix metalloproteinases; Micro interfering RNA (miRNA); Non small cell lung cancer; Tissue factor pathway inhibitor 2; Tumour growth

Indexed keywords

ALPHA1 INTEGRIN; COLLAGEN TYPE 4; GLYCOPROTEIN; LAMININ; MATRIX METALLOPROTEINASE; PLACENTA PROTEIN 5; TISSUE-FACTOR-PATHWAY INHIBITOR 2;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BIOSYNTHESIS; CANCER INVASION; CANCER TRANSPLANTATION; CELL ADHESION; CELL PROLIFERATION; DOWN REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LUNG NON SMALL CELL CANCER; LUNG TUMOR; MALE; METABOLISM; METASTASIS; MOUSE; NUDE MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; XENOGRAFT;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; COLLAGEN TYPE IV; DOWN-REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; INTEGRIN ALPHA1; LAMININ; LUNG NEOPLASMS; MALE; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSPLANTATION, HETEROLOGOUS; TUMOR MICROENVIRONMENT;

MUS MUSCULUS;

EID: 79951921383     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00989.x     Document Type: Article

References (52)

1. Axelrod R, Axelrod DE, Pienta KJ. Evolution of cooperation among tumor cells. Proc Natl Acad Sci USA. 2006; 103: 13474-9.
2. Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol. 2003; 200: 448-64.
3. Vihinen P, Kahari VM. Matrix metallopro-teinases in cancer: prognostic markers and therapeutic targets. Int J Cancer. 2002; 99: 157-66.
4. Noel A, Jost M, Maquoi E. Matrix metalloproteinases at cancer tumor-host interface. Semin Cell Dev Biol. 2008; 19: 52-60.
5. Bjorklund M, Koivunen E. Gelatinase-mediated migration and invasion of cancer cells. Biochim Biophys Acta. 2005; 1755: 37-69.
6. Rao CN, Mohanam S, Puppala, et al Regulation of ProMMP-1 and ProMMP-3 activation by tissue factor pathway inhibitor-2/matrix-associated serine pro-tease inhibitor. Biochem Biophys Res Commun. 1999; 255: 94-8.
7. Chand HS, Foster DC, Kisiel W. Structure, function and biology of tissue factor pathway inhibitor-2. Thromb Haemost. 2005; 94: 1122-30.
8. Rao CN, Liu YY, Peavey CL, et al Novel extracellular matrix-associated serine pro-teinase inhibitors from human skin fibroblasts. Arch Biochem Biophys. 1995; 317: 311-4.
9. Iochmann S, Reverdiau-Moalic P, Hube F, et al Demonstration of inducible TFPI-2 mRNA synthesis in BeWo and JEG-3 tro-phoblast cells using a competitive RT-PCR. Thromb Res. 2002; 105: 217-23.
10. Hube F, Reverdiau P, Iochmann S, et al Demonstration of a tissue factor pathway inhibitor 2 messenger RNA synthesis by pure villous cytotrophoblast cells isolated from term human placentas. Biol Reprod. 2003a; 68: 1888-94.
11. Sierko E, Wojtukiewicz MZ, Kisiel W. The role of tissue factor pathway inhibitor-2 in cancer biology. Semin Thromb Hemost. 2007; 33: 653-9.
12. Konduri SD, Tasiou A, Chandrasekar N, et al Role of tissue factor pathway inhibitor-2 (TFPI-2) in amelanotic melanoma (C-32) invasion. Clin Exp Metastasis. 2000; 18: 303-8.
13. Rao CN, Lakka SS, Kin Y, et al Expression of tissue factor pathway inhibitor 2 inversely correlates during the progression of human gliomas. Clin Cancer Res. 2001; 7: 570-6.
14. Wojtukiewicz MZ, Sierko E, Zimnoch L, et al Immunohistochemical localization of tissue factor pathway inhibitor-2 in human tumor tissue. Thromb Haemost. 2003; 90: 140-6.
15. Rollin J, Iochmann S, Blechet C, et al Expression and methylation status of tissue factor pathway inhibitor-2 gene in non-small-cell lung cancer. Br J Cancer. 2005; 92: 775-83.
16. Wong CM, Ng YL, Lee JM, et al Tissue factor pathway inhibitor-2 as a frequently silenced tumor suppressor gene in hepato-cellular carcinoma. Hepatology. 2007; 45: 1129-38.
17. Hube F, Reverdiau P, Iochmann S, et al Transcriptional silencing of the TFPI-2 gene by promoter hypermethylation in choriocarcinoma cells. Biol Chem. 2003b; 384: 1029-34.
18. Konduri SD, Srivenugopal KS, Yanamandra N, et al Promoter methyla-tion and silencing of the tissue factor pathway inhibitor-2 (TFPI-2), a gene encoding an inhibitor of matrix metalloproteinases in human glioma cells. Oncogene. 2003; 22: 4509-16.
19. Rao CN, Segawa T, Navari JR, et al Methylation of TFPI-2 gene is not the sole cause of its silencing. Int J Oncol. 2003; 22: 843-8.
20. Nobeyama Y, Okochi-Takada E, Furuta J, et al Silencing of tissue factor pathway inhibitor-2 gene in malignant melanomas. Int J Cancer. 2007; 121: 301-7.
21. Ohtsubo K, Watanabe H, Okada G, et al A case of pancreatic cancer with formation of a mass mimicking alcoholic or autoim-mune pancreatitis in a young man. Possibility of diagnosis by hypermethyla-tion of pure pancreatic juice. JOP. 2008; 9: 37-45.
22. Sprecher CA, Kisiel W, Mathewes S, et al Molecular cloning, expression, and partial characterization of a second human tissue-factor-pathway inhibitor. Proc Natl Acad Sci USA. 1994; 91: 3353-7.
23. Iochmann S, Blechet C, Chabot V, et al Transient RNA silencing of tissue factor pathway inhibitor-2 modulates lung cancer cell invasion. Clin Exp Metastasis. 2009; 26: 457-67.
24. Lagos-Quintana M, Rauhut R, Yalcin A, et al Identification of tissue-specific microRNAs from mouse. Curr Biol. 2002; 12: 735-9.
25. Gagnadoux F, Pape AL, Lemarie E, et al Aerosol delivery of chemotherapy in an orthotopic model of lung cancer. Eur Respir J. 2005; 26: 657-61.
26. Liang H, Li WH. MicroRNA regulation of human protein protein interaction network. RNA. 2007; 13: 1402-8.
27. Gabriely G, Wurdinger T, Kesari S, et al MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol. 2008; 28: 5369-80.
28. Lakka SS, Konduri SD, Mohanam S, et al in vitro modulation of human lung cancer cell line invasiveness by antisense cDNA of tissue factor pathway inhibitor-2. Clin Exp Metastasis. 2000; 18: 239-44.
29. Konduri SD, Tasiou A, Chandrasekar N, et al Overexpression of tissue factor pathway inhibitor-2 (TFPI-2), decreases the invasiveness of prostate cancer cells in vitro. Int J Oncol. 2001; 18: 127-31.
30. Kondraganti S, Gondi CS, Gujrati M, et al 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. 2006; 29: 25-32.
31. Mukhopadhyay NK, Gilchrist D, Gordon GJ, et al Integrin-dependent protein tyro-sine phosphorylation is a key regulatory event in collagen-IV-mediated adhesion and proliferation of human lung tumor cell line, Calu-1. Ann Thorac Surg. 2004; 78: 450-7.
32. Chen Q, Meng LH, Zhu CH, et al ADAM15 suppresses cell motility by driving integrin alpha5beta1 cell surface expression via Erk inactivation. Int J Biochem Cell Biol. 2008; 40: 2164-73.
33. Sossey-Alaoui K, Ranalli TA, Li X, et al WAVE3 promotes cell motility and invasion through the regulation of MMP-1, MMP-3, and MMP-9 expression. Exp Cell Res. 2005; 308: 135-45.
34. Pulukuri SM, Rao JS. Matrix metallopro-teinase-1 promotes prostate tumor growth and metastasis. Int J Oncol. 2008; 32: 757-65.
35. Cheng S, Tada M, Hida Y, et al High MMP-1 mRNA expression is a risk factor for disease-free and overall survivals in patients with invasive breast carcinoma. J Surg Res. 2008; 146: 104-9.
36. Jiang X, Dutton CM, Qi WN, et al siRNA mediated inhibition of MMP-1 reduces invasive potential of a human chondrosar-coma cell line. J Cell Physiol. 2005; 202: 723-30.
37. Blackburn JS, Rhodes CH, Coon CI, et al RNA interference inhibition of matrix met-alloproteinase-1 prevents melanoma metastasis by reducing tumor collagenase activity and angiogenesis. Cancer Res. 2007; 67: 10849-58.
38. Mercapide J, Lopez De Cicco R, Castresana JS, et al Stromelysin-1/matrix metalloproteinase-3 (MMP-3) expression accounts for invasive properties of human astrocytoma cell lines. Int J Cancer. 2003; 106: 676-82.
39. Nishimura T, Nakamura K, Kishioka Y, et al Inhibition of matrix metallopro-teinases suppresses the migration of skeletal muscle cells. J Muscle Res Cell Motil. 2008; 29: 37-44.
40. Kunapuli P, Kasyapa CS, Hawthorn L, et al LGI1, a putative tumor metastasis suppressor gene, controls in vitro invasiveness and expression of matrix metalloproteinases in glioma cells through the ERK1/2 pathway. J Biol Chem. 2004; 279: 23151-7.
41. Huntington JT, Shields JM, Der CJ, et al 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. 2004; 279: 33168-76.
42. Shin SY, Choi HY, Ahn BH, et al Phospholipase Cgamma1 stimulates transcriptional activation of the matrix metalloproteinase-3 gene via the protein kinase C/Raf/ERK cascade. Biochem Biophys Res Commun. 2007; 353: 611-6.
43. Shih YW, Shieh JM, Wu PF, et al Alpha-tomatine inactivates PI3K/Akt and ERK signaling pathways in human lung adenocarcinoma A549 cells: effect on metastasis. Food Chem Toxicol. 2009; 47: 1985-95.
44. Yue W, Sun Q, Landreneau R, et al Fibulin-5 suppresses lung cancer invasion by inhibiting matrix metalloproteinase-7 expression. Cancer Res. 2009; 69: 6339-46.
45. Zhang D, Bar-Eli M, Meloche S, et al Dual regulation of MMP-2 expression by the type 1 insulin-like growth factor receptor: the phosphatidylinositol 3-kinase/Akt and Raf/ERK pathways transmit opposing signals. J Biol Chem. 2004; 279: 19683-90.
46. Kanekura T, Chen X, Kanzaki T. Basigin (CD147) is expressed on melanoma cells and induces tumor cell invasion by stimulating production of matrix metallopro-teinases by fibroblasts. Int J Cancer. 2002; 99: 520-8.
47. Lo J, Hurta RA. Over-expression of K-FGF or bFGF results in altered expression of matrix metalloproteinases: correlations with malignant progression and cellular invasion. Cell Biol Int. 2002; 26: 319-25.
48. Domeij H, Yucel-Lindberg T, Modeer T. Signal pathways involved in the production of MMP-1 and MMP-3 in human gingival fibroblasts. Eur J Oral Sci. 2002; 110: 302-6.
49. Fang Q, Liu X, Al-Mugotir M, et al Thrombin and TNF-alpha/IL-1beta synergistically induce fibroblast-mediated collagen gel degradation. Am J Respir Cell Mol Biol. 2006; 35: 714-21.
50. Menashi S, Serova M, Ma L, et al Regulation of extracellular matrix metalloproteinase inducer and matrix metallopro-teinase expression by amphiregulin in transformed human breast epithelial cells. Cancer Res. 2003; 63: 7575-80.
51. Tang Y, Nakada MT, Kesavan P, et al Extracellular matrix metalloproteinase inducer stimulates tumor angiogenesis by elevating vascular endothelial cell growth factor and matrix metalloproteinases. Cancer Res. 2005; 65: 3193-9.
52. Nabeshima K, Iwasaki H, Koga K, et al Emmprin (basigin/CD147): matrix metalloproteinase modulator and multifunctional cell recognition molecule that plays a critical role in cancer progression. Pathol Int. 2006; 56: 359-67.