PAI-1, a target gene of miR-143, regulates invasion and metastasis by upregulating MMP-13 expression of human osteosarcoma

Cancer Medicine

Volumn 5, Issue 5, 2016, Pages 892-902

  Hirahata, Mio ^a   Osaki, Mitsuhiko ^a,b   Kanda, Yusuke ^a   Sugimoto, Yui ^a   Yoshioka, Yusuke ^c   Kosaka, Nobuyoshi ^c   Takeshita, Fumitaka ^c   Fujiwara, Tomohiro ^c   Kawai, Akira ^c   Ito, Hisao ^a   Ochiya, Takahiro ^c   Okada, Futoshi ^a,b  

^a TOTTORI UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c NATIONAL CANCER CENTER HOSPITAL   (Japan)

Author keywords

Metastasis; miR 143; MMP 13; Osteosarcoma; PAI 1

Indexed keywords

COLLAGENASE 3; MICRORNA 143; PLASMINOGEN ACTIVATOR INHIBITOR 1; SMALL INTERFERING RNA; MICRORNA; MIRN143 MICRORNA, HUMAN; MMP13 PROTEIN, HUMAN; SERPINE1 PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG METASTASIS; MALE; MOUSE; NONHUMAN; OSTEOLYSIS; OSTEOSARCOMA; OSTEOSARCOMA CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR INVASION; UPREGULATION; ANIMAL; BIOSYNTHESIS; BONE TUMOR; CANCER TRANSPLANTATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; LUNG NEOPLASMS; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SECONDARY; TUMOR CELL CULTURE; XENOGRAFT;

ANIMALS; BONE NEOPLASMS; CELL PROLIFERATION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MALE; MATRIX METALLOPROTEINASE 13; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; OSTEOSARCOMA; PLASMINOGEN ACTIVATOR INHIBITOR 1; RNA, SMALL INTERFERING; TRANSFECTION; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 85006216654     PISSN: None     EISSN: 20457634     Source Type: Journal    
DOI: 10.1002/cam4.651     Document Type: Article

References (39)

1. Wada, T., K. Isu, N. Takeda, M. Usui, S. Ishii, and S. Yamawaki . 1996. A preliminary report of neoadjuvant chemotherapy NSH-7 study in osteosarcoma: preoperative salvage chemotherapy based on clinical tumor response and the use of granulocyte colony-stimulating factor. Oncology 53:221-227.
2. Kempf-Bielack, B., S. S. Bielack, H. Jurgens, D. Branscheid, W. E. Berdel, G. U. Exner, et al. 2005. Osteosarcoma relapse after combined modality therapy: an analysis of unselected patients in the Cooperative Osteosarcoma Study Group (COSS). J. Clin. Oncol. 23:559-568.
3. Pasquinelli, A. E., B. J. Reinhart, F. Slack, M. Q. Martindale, M. I. Kuroda, B. Maller, et al. 2000. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408:86-89.
4. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
5. Lewis, B. P., C. B. Burge, and D. P. Bartel . 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
6. Lu, J., G. Getz, E. A. Miska, E. Alvarez-Saavedra, J. Lamb, D. Peck, et al. 2005. MicroRNA expression profiles classify human cancers. Nature 435:834-838.
7. Volinia, S., G. A. Calin, C. G. Liu, S. Ambs, A. Cimmino, F. Petrocca, et al. 2006. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 103:2257-2261.
8. Calin, G. A., M. Ferracin, A. Cimmino, G. Di Leva, M. Shimizu, S. E. Wojcik, et al. 2005. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353:1793-1801.
9. Jiang, J., Y. Gusev, I. Aderca, T. A. Mettler, D. M. Nagorney, D. J. Brackett, et al. 2008. Association of MicroRNA expression in hepatocellular carcinomas with hepatitis infection, cirrhosis, and patient survival. Clin. Cancer Res. 14:419-427.
10. Asangani, I. A., S. A. K. Rasheed, D. A. Nikolova, J. H. Leupold, N. H. Colburn, S. Post, et al. 2008. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128-2136.
11. Valastyan, S., F. Reinhardt, N. Benaich, D. Calogrias, A. M. Szász, Z. C. Wang, et al. 2009. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137:1032-1046.
12. Cimmino, A., G. A. Calin, M. Fabbri, M. V. Iorio, M. Ferracin, M. Shimizu, et al. 2005. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl. Acad. Sci. USA 102:13944-13949.
13. Osaki, M., F. Takeshita, Y. Sugimoto, N. Kosaka, Y. Yamamoto, Y. Yoshioka, et al. 2011. MicroRNA-143 regulates human osteosarcoma metastasis by regulating matrix metalloprotease-13 expression. Mol. Ther. 19:1123-1130.
14. Dawson, S., and A. Henney . 1992. The status of PAI-1 as a risk factor for arterial and thrombotic disease: a review. Atherosclerosis 95:105-117.
15. Ferroni, P., M. Roselli, I. Portarena, V. Formica, S. Riondino, and F. LA Farina . 2014. Plasma plasminogen activator inhibitor-1 (PAI-1) levels in breast cancer-relationship with clinical outcome. Anticancer Res. 34:1153-1162.
16. Ren, F., H. Shi, G. Zhang, and R. Zhang . 2013. Expression of deleted in liver cancer 1 and plasminogen activator inhibitor 1 protein in ovarian carcinoma and their clinical significance. J. Exp. Clin. Cancer Res. 32:60.
17. Santhekadur, P. K., M. Akiel, L. Emdad, R. Gredler, J. Srivastava, D. Rajasekaran, et al. 2014. Staphylococcal nuclease domain containing-1 (SND1) promotes migration and invasion via angiotensin 2 type 1 receptor (AT1R) and TGF-beta signaling. FEBS Open Bio 4:353-361.
18. Bajou, K., A. Noel, R. D. Gerard, V. Masson, N. Brunner, C. Holst-Hansen, et al. 1998. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat. Med. 4:923-928.
19. Isogai, C., W. E. Laug, H. Simada, P. J. Declerck, M. F. Stins, D. L. Durden, et al. 2001. Plasminogen activator inhibitor-1 promotes angiogenesis by stimulating endothelial cell migration toward fibronectin. Cancer Res. 61:5587-5594.
20. Bajou, K., C. Mallard, M. Jost, R. H. Lijnen, A. Gils, P. Declerck, et al. 2004. Host-derived plasminogen activator inhibitor-1 (PAI-1) concentration is critical for in vivo tumoral angiogenesis and growth. Oncogene 23:6986-6990.
21. Yan, L., and L. C. Demars . 2014. Effect of a high-fat diet on spontaneous metastasis of Lewis lung carcinoma in plasminogen activator inhibitor-1 deficient and wild-type mice. PLoS One 9:e110869.
22. Meryet-Figuières, M., S. Resina, C. Lavigne, G. Barlovatz-Meimon, B. Lebleu, and A. R. Thierry . 2007. Inhibition of PAI-1 expression in breast cancer carcinoma cells by siRNA at nanomolar range. Biochimie 89:1228-1233.
23. Suzuki, Y., H. Mogami, H. Ihara, and T. Urano . 2009. Unique secretory dynamics of tissue plasminogen activator and its modulation by plasminogen activator inhibitor-1 in vascular endothelial cells. Blood 113:470-478.
24. Peltier, H. J., and G. J. Latham . 2008. Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 14:844-852.
25. Leeman, M. F., S. Curran, and G. I. Murray . 2002. The structure, regulation, and function of human matrix metalloproteinase-13. Crit. Rev. Biochem. Mol. Biol. 37:149-166.
26. Chang, H. J., M. J. Yang, Y. H. Yang, M. F. Hou, E. J. Hsueh, and S. R. Lin . 2009. MMP13 is potentially a new tumor marker for breast cancer diagnosis. Oncol. Rep. 22:1119-1127.
27. Stokes, A., J. Joutsa, R. Ala-Aho, M. Pitchers, C. J. Pennington, C. Martin, et al. 2010. Expression profiles and clinical correlations of degradome components in the tumor microenvironment of head and neck squamous cell carcinoma. Clin. Cancer Res. 16:2022-2035.
28. Hsu, C. P., G. H. Shen, and J. L. Ko . 2006. Matrix metalloproteinase-13 expression is associated with bone marrow microenvironment and prognosis in non-small cell lung cancer. Lung Cancer 52:349-357.
29. Corte, M. D., L. O. Gonzalez, M. G. Corte, I. Quintela, I. Pidal, M. Bongera, et al. 2005. Collagenase-3 (MMP-13) expression in cutaneous malignant melanoma. Int. J. Biol. Markers 20:242-248.
30. Huang, M. Y., H. J. Chang, F. Y. Chung, M. J. Yang, Y. H. Yang, J. Y. Wang, et al. 2010. MMP13 is a potential prognostic marker for colorectal cancer. Oncol. Rep. 24:1241-1247.
31. Vincent-Chong, V. K., I. Salahshourifar, L. P. Karen-Ng, M. Y. Siow, T. G. Kallarakkal, A. Ramanathan, et al. 2014. Overexpression of MMP-13 is associated with clinical outcomes and poor prognosis in oral squamous cell carcinoma. Sci. World J. 2014:897523.
32. Foda, A. A., A. K. El-Hawary, and A. Abdel-Aziz . 2014. Matrix metalloproteinase-13 expression in the progression of colorectal adenoma to carcinoma: matrix metalloproteinase-13 expression in the colorectal adenoma and carcinoma. Tumour Biol. 35:5653-5658.
33. Wang, J., Y. Li, J. Wang, C. Li, K. Yu, and Q. Wang . 2012. Increased expression of matrix metalloproteinase-13 in glioma is associated with poor overall survival of patients. Med. Oncol. 29:2432-2437.
34. Nannuru, K. C., M. Futakuchi, M. L. Varney, T. M. Vincent, E. G. Marcusson, and R. K. Singh . 2010. Matrix metalloproteinase (MMP)-13 regulates mammary tumor-induced osteolysis by activating MMP9 and transforming growth factor-beta signaling at the tumor-bone interface. Cancer Res. 70:3494-3504.
35. Akech, J., J. J. Wixted, K. Bedard, M. van der Deen, S. Hussain, T. A. Guise, et al. 2010. Runx2 association with progression of prostate cancer in patients: mechanisms mediating bone osteolysis and osteoblastic metastatic lesions. Oncogene 29:811-821.
36. Zhou, Y., Z. Hu, N. Li, and R. Jiang . 2015. Interleukin-32 stimulates osteosarcoma cell invasion and motility via AKT pathway-mediated MMP-13 expression. Int. J. Mol. Med. 35:1729-1733.
37. Korpi, J. T., J. Hagström, N. Lehtonen, J. Parkkinen, T. Sorsa, T. Salo, et al. 2011. Expression of matrix metalloproteinases-2, -8, -13, -26, and tissue inhibitors of metalloproteinase-1 in human osteosarcoma. Surg. Oncol. 20:e18-e22.
38. Jimenez, M. J., M. Balbin, J. M. Lopez, J. Alvarez, T. Komori, and C. LoPez-Otin . 1999. Collagenase 3 is a target of Cbfa1 a transcription factor of the runt gene family involved in bone formation. Mol. Cell. Biol. 19:4431-4442.
39. Oda, T., Y. O. Jung, H. S. Kim, X. Cai, J. M. López-Guisa, Y. Ikeda, et al. 2001. PAI-1 deficiency attenuates the fibrogenic response to ureteral obstruction. Kidney Int. 30:587-596.