Tetraspanin CD9 Promotes the Invasive Phenotype of Human Fibrosarcoma Cells via Upregulation of Matrix Metalloproteinase-9

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Herr, Michael J ^a   Kotha, Jayaprakash ^b   Hagedorn, Nikolaus ^a   Smith, Blake ^a   Jennings, Lisa K ^a,b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b CirQuest Labs LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD9 ANTIGEN; GELATINASE B; MESSENGER RNA;

ARTICLE; CANCER GROWTH; CELL INVASION; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; ENZYME SYNTHESIS; FIBROSARCOMA; HUMAN; HUMAN CELL; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SYNTHESIS; SARCOMA CELL; UPREGULATION;

ANTIGENS, CD9; CELL LINE, TUMOR; FIBROSARCOMA; HUMANS; MATRIX METALLOPROTEINASE 9; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHENOTYPE; SIGNAL TRANSDUCTION; TETRASPANINS; UP-REGULATION;

EID: 84879516343     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067766     Document Type: Article

References (62)

1. Nagase H, Woessner JF Jr, (1999) Matrix metalloproteinases. J Biol Chem 274: 21491-21494.
2. Page-McCaw A, Ewald AJ, Werb Z, (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8: 221-233.
3. Zucker S, Cao J, Chen WT, (2000) Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene 19: 6642-6650.
4. Visse R, Nagase H, (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92: 827-839.
5. Skiles JW, Gonnella NC, Jeng AY, (2004) The design, structure, and clinical update of small molecular weight matrix metalloproteinase inhibitors. Curr Med Chem 11: 2911-2977.
6. Close DR, (2001) Matrix metalloproteinase inhibitors in rheumatic diseases. Ann Rheum Dis 60Suppl 3: iii62-67.
7. Kanetaka K, Sakamoto M, Yamamoto Y, Takamura M, Kanematsu T, et al. (2003) Possible involvement of tetraspanin CO-029 in hematogenous intrahepatic metastasis of liver cancer cells. J Gastroenterol Hepatol 18: 1309-1314.
8. Zijlstra A, Lewis J, Degryse B, Stuhlmann H, Quigley JP, (2008) The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell 13: 221-234.
9. Yanez-Mo M, Barreiro O, Gordon-Alonso M, Sala-Valdes M, Sanchez-Madrid F, (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 19: 434-446.
10. Berditchevski F, (2001) Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 114: 4143-4151.
11. Zoller M, (2009) Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer 9: 40-55.
12. Wang HX, Li Q, Sharma C, Knoblich K, Hemler ME, (2011) Tetraspanin protein contributions to cancer. Biochemical Society transactions 39: 547-552.
13. Hwang JR, Jo K, Lee Y, Sung BJ, Park YW, et al. (2012) Upregulation of CD9 in ovarian cancer is related to the induction of TNF-alpha gene expression and constitutive NF-kappaB activation. Carcinogenesis 33: 77-83.
14. Kischel P, Bellahcene A, Deux B, Lamour V, Dobson R, et al. (2012) Overexpression of CD9 in Human Breast Cancer Cells Promotes the Development of Bone Metastases. Anticancer Res 32: 5211-5220.
15. Iwasaki T, Takeda Y, Maruyama K, Yokosaki Y, Tsujino K, et al. (2012) Deletion of tetraspanin CD9 diminishes lymphangiogenesis in vivo and in vitro. J Biol Chem.
16. Hori H, Yano S, Koufuji K, Takeda J, Shirouzu K, (2004) CD9 expression in gastric cancer and its significance. The Journal of surgical research 117: 208-215.
17. Soyuer S, Soyuer I, Unal D, Ucar K, Yildiz OG, et al. (2010) Prognostic significance of CD9 expression in locally advanced gastric cancer treated with surgery and adjuvant chemoradiotherapy. Pathology, research and practice 206: 607-610.
18. Wang JC, Begin LR, Berube NG, Chevalier S, Aprikian AG, et al. (2007) Down-regulation of CD9 expression during prostate carcinoma progression is associated with CD9 mRNA modifications. Clinical cancer research: an official journal of the American Association for Cancer Research 13: 2354-2361.
19. Takino T, Miyamori H, Kawaguchi N, Uekita T, Seiki M, et al. (2003) Tetraspanin CD63 promotes targeting and lysosomal proteolysis of membrane-type 1 matrix metalloproteinase. Biochem Biophys Res Commun 304: 160-166.
20. Yanez-Mo M, Barreiro O, Gonzalo P, Batista A, Megias D, et al. (2008) MT1-MMP collagenolytic activity is regulated through association with tetraspanin CD151 in primary endothelial cells. Blood 112: 3217-3226.
21. Jung KK, Liu XW, Chirco R, Fridman R, Kim HR, (2006) Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein. EMBO J 25: 3934-3942.
22. Takeda Y, He P, Tachibana I, Zhou B, Miyado K, et al. (2008) Double deficiency of tetraspanins CD9 and CD81 alters cell motility and protease production of macrophages and causes chronic obstructive pulmonary disease-like phenotype in mice. J Biol Chem 283: 26089-26097.
23. Fujita Y, Shiomi T, Yanagimoto S, Matsumoto H, Toyama Y, et al. (2006) Tetraspanin CD151 is expressed in osteoarthritic cartilage and is involved in pericellular activation of pro-matrix metalloproteinase 7 in osteoarthritic chondrocytes. Arthritis Rheum 54: 3233-3243.
24. Chen S, Sun Y, Jin Z, Jing X, (2011) Functional and biochemical studies of CD9 in fibrosarcoma cell line. Molecular and cellular biochemistry 350: 89-99.
25. Funakoshi T, Tachibana I, Hoshida Y, Kimura H, Takeda Y, et al. (2003) Expression of tetraspanins in human lung cancer cells: frequent downregulation of CD9 and its contribution to cell motility in small cell lung cancer. Oncogene 22: 674-687.
26. Murayama Y, Shinomura Y, Oritani K, Miyagawa J, Yoshida H, et al. (2008) The tetraspanin CD9 modulates epidermal growth factor receptor signaling in cancer cells. J Cell Physiol 216: 135-143.
27. Hanyu A, Kojima K, Hatake K, Nomura K, Murayama H, et al. (2009) Functional in vivo optical imaging of tumor angiogenesis, growth, and metastasis prevented by administration of anti-human VEGF antibody in xenograft model of human fibrosarcoma HT1080 cells. Cancer Sci 100: 2085-2092.
28. Zhang C, Li Y, Shi X, Kim SK, (2010) Inhibition of the expression on MMP-2, 9 and morphological changes via human fibrosarcoma cell line by 6,6′-bieckol from marine alga Ecklonia cava. BMB Rep 43: 62-68.
29. Baldassarre M, Razinia Z, Brahme NN, Buccione R, Calderwood DA, (2012) Filamin A controls matrix metalloproteinase activity and regulates cell invasion in human fibrosarcoma cells. J Cell Sci 125: 3858-3869.
30. Peterfia B, Fule T, Baghy K, Szabadkai K, Fullar A, et al. (2012) Syndecan-1 enhances proliferation, migration and metastasis of HT-1080 cells in cooperation with syndecan-2. PLoS One 7: e39474.
31. Jennings LK, Fox CF, Kouns WC, McKay CP, Ballou LR, et al. (1990) The activation of human platelets mediated by anti-human platelet p24/CD9 monoclonal antibodies. J Biol Chem 265: 3815-3822.
32. Cook GA, Longhurst CM, Grgurevich S, Cholera S, Crossno JT Jr, et al. (2002) Identification of CD9 extracellular domains important in regulation of CHO cell adhesion to fibronectin and fibronectin pericellular matrix assembly. Blood 100: 4502-4511.
33. Tohami T, Drucker L, Shapiro H, Radnay J, Lishner M, (2007) Overexpression of tetraspanins affects multiple myeloma cell survival and invasive potential. FASEB J 21: 691-699.
34. Hong IK, Jin YJ, Byun HJ, Jeoung DI, Kim YM, et al. (2006) Homophilic interactions of Tetraspanin CD151 up-regulate motility and matrix metalloproteinase-9 expression of human melanoma cells through adhesion-dependent c-Jun activation signaling pathways. J Biol Chem 281: 24279-24292.
35. Hasuwa H, Shishido Y, Yamazaki A, Kobayashi T, Yu X, et al. (2001) CD9 amino acids critical for upregulation of diphtheria toxin binding. Biochem Biophys Res Commun 289: 782-790.
36. Longhurst CM, Jacobs JD, White MM, Crossno JT Jr, Fitzgerald DA, et al. (2002) Chinese hamster ovary cell motility to fibronectin is modulated by the second extracellular loop of CD9. Identification of a putative fibronectin binding site. J Biol Chem 277: 32445-32452.
37. Zhu GZ, Miller BJ, Boucheix C, Rubinstein E, Liu CC, et al. (2002) Residues SFQ (173-175) in the large extracellular loop of CD9 are required for gamete fusion. Development 129: 1995-2002.
38. Ovalle S, Gutierrez-Lopez MD, Olmo N, Turnay J, Lizarbe MA, et al. (2007) The tetraspanin CD9 inhibits the proliferation and tumorigenicity of human colon carcinoma cells. Int J Cancer 121: 2140-2152.
39. Furuya M, Kato H, Nishimura N, Ishiwata I, Ikeda H, et al. (2005) Down-regulation of CD9 in human ovarian carcinoma cell might contribute to peritoneal dissemination: morphologic alteration and reduced expression of beta1 integrin subsets. Cancer Res 65: 2617-2625.
40. Saito Y, Tachibana I, Takeda Y, Yamane H, He P, et al. (2006) Absence of CD9 enhances adhesion-dependent morphologic differentiation, survival, and matrix metalloproteinase-2 production in small cell lung cancer cells. Cancer Res 66: 9557-9565.
41. Sordat I, Decraene C, Silvestre T, Petermann O, Auffray C, et al. (2002) Complementary DNA arrays identify CD63 tetraspanin and alpha3 integrin chain as differentially expressed in low and high metastatic human colon carcinoma cells. Lab Invest 82: 1715-1724.
42. Lafleur MA, Xu D, Hemler ME, (2009) Tetraspanin proteins regulate membrane type-1 matrix metalloproteinase-dependent pericellular proteolysis. Mol Biol Cell 20: 2030-2040.
43. Testa JE, Brooks PC, Lin JM, Quigley JP, (1999) Eukaryotic expression cloning with an antimetastatic monoclonal antibody identifies a tetraspanin (PETA-3/CD151) as an effector of human tumor cell migration and metastasis. Cancer Res 59: 3812-3820.
44. Kohno M, Hasegawa H, Miyake M, Yamamoto T, Fujita S, (2002) CD151 enhances cell motility and metastasis of cancer cells in the presence of focal adhesion kinase. Int J Cancer 97: 336-343.
45. Zoller M, (2006) Gastrointestinal tumors: metastasis and tetraspanins. Z Gastroenterol 44: 573-586.
46. Riikonen T, Westermarck J, Koivisto L, Broberg A, Kahari VM, et al. (1995) Integrin alpha 2 beta 1 is a positive regulator of collagenase (MMP-1) and collagen alpha 1(I) gene expression. The Journal of biological chemistry 270: 13548-13552.
47. Pilcher BK, Dumin JA, Sudbeck BD, Krane SM, Welgus HG, et al. (1997) The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. The Journal of cell biology 137: 1445-1457.
48. Nakazawa Y, Sato S, Naito M, Kato Y, Mishima K, et al. (2008) Tetraspanin family member CD9 inhibits Aggrus/podoplanin-induced platelet aggregation and suppresses pulmonary metastasis. Blood 112: 1730-1739.
49. Zvieriev V, Wang JC, Chevrette M, (2005) Over-expression of CD9 does not affect in vivo tumorigenic or metastatic properties of human prostate cancer cells. Biochemical and Biophysical Research Communications 337: 498-504.
50. Zhu X, Tai W, Shi W, Song Y, Zhang H, et al. (2012) Matrix metalloproteinase-9 silencing by RNA interference promotes the adhesive-invasive switch in HT1080 human fibrosarcoma cells. Clin Lab 58: 313-322.
51. Jee BK, Park KM, Surendran S, Lee WK, Han CW, et al. (2006) KAI1/CD82 suppresses tumor invasion by MMP9 inactivation via TIMP1 up-regulation in the H1299 human lung carcinoma cell line. Biochemical and biophysical research communications 342: 655-661.
52. Okada Y, Gonoji Y, Naka K, Tomita K, Nakanishi I, et al. (1992) Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells. Purification and activation of the precursor and enzymic properties. J Biol Chem 267: 21712-21719.
53. Leco KJ, Apte SS, Taniguchi GT, Hawkes SP, Khokha R, et al. (1997) Murine tissue inhibitor of metalloproteinases-4 (Timp-4): cDNA isolation and expression in adult mouse tissues. FEBS Lett 401: 213-217.
54. Greene J, Wang M, Liu YE, Raymond LA, Rosen C, et al. (1996) Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J Biol Chem 271: 30375-30380.
55. Cheng JC, Chou CH, Kuo ML, Hsieh CY, (2006) Radiation-enhanced hepatocellular carcinoma cell invasion with MMP-9 expression through PI3K/Akt/NF-kappaB signal transduction pathway. Oncogene 25: 7009-7018.
56. Cho SJ, Chae MJ, Shin BK, Kim HK, Kim A, (2008) Akt- and MAPK-mediated activation and secretion of MMP-9 into stroma in breast cancer cells upon heregulin treatment. Mol Med Report 1: 83-88.
57. Chen JS, Wang Q, Fu XH, Huang XH, Chen XL, et al. (2009) Involvement of PI3K/PTEN/AKT/mTOR pathway in invasion and metastasis in hepatocellular carcinoma: Association with MMP-9. Hepatol Res 39: 177-186.
58. Zhu X, Wang L, Zhang B, Li J, Dou X, et al. (2011) TGF-beta1-induced PI3K/Akt/NF-kappaB/MMP9 signalling pathway is activated in Philadelphia chromosome-positive chronic myeloid leukaemia hemangioblasts. J Biochem 149: 405-414.
59. Thant AA, Nawa A, Kikkawa F, Ichigotani Y, Zhang Y, et al. (2000) Fibronectin activates matrix metalloproteinase-9 secretion via the MEK1-MAPK and the PI3K-Akt pathways in ovarian cancer cells. Clin Exp Metastasis 18: 423-428.
60. Kotha J, Longhurst C, Appling W, Jennings LK, (2008) Tetraspanin CD9 regulates beta 1 integrin activation and enhances cell motility to fibronectin via a PI-3 kinase-dependent pathway. Exp Cell Res 314: 1811-1822.
61. Kotha J, Zhang C, Longhurst CM, Lu Y, Jacobs J, et al. (2009) Functional relevance of tetraspanin CD9 in vascular smooth muscle cell injury phenotypes: a novel target for the prevention of neointimal hyperplasia. Atherosclerosis 203: 377-386.
62. Nakamoto T, Murayama Y, Oritani K, Boucheix C, Rubinstein E, et al. (2009) A novel therapeutic strategy with anti-CD9 antibody in gastric cancers. Journal of Gastroenterology 44: 889-896.