Silibinin inhibits invasive properties of human glioblastoma U87MG cells through suppression of cathepsin B and nuclear factor kappa B-mediated induction of matrix metalloproteinase 9

Anti-Cancer Drugs

Volumn 21, Issue 3, 2010, Pages 252-260

  Momeny, Majid ^a   Malehmir, Mohsen ^a   Zakidizaji, Majid ^a   Ghasemi, Reza ^a   Ghadimi, Habibeh ^a   Shokrgozar, Mohammad A ^d   Emami, Amir H ^c   Nafissi, Shahriar ^b   Ghavamzadeh, Ardeshir ^a   Ghaffari, Seyed H ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

Cathepsin B; Gelatinolytic activity; Glioblastoma; Nuclear factor kappa B; Stefin A; Urokinase plasminogen activator; Urokinase plasminogen activator receptor

Indexed keywords

CATHEPSIN B; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; SILIBININ; STEFIN A; UROKINASE; UROKINASE RECEPTOR;

ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; DNA SYNTHESIS; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; GLIOBLASTOMA; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ZYMOGRAPHY;

ANTINEOPLASTIC AGENTS; CATHEPSIN B; CELL LINE, TUMOR; CELL PROLIFERATION; CYSTATIN A; GLIOBLASTOMA; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MATRIX METALLOPROTEINASE 9; NF-KAPPA B; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; SILYMARIN;

EID: 76649085810     PISSN: 09594973     EISSN: None     Source Type: Journal    
DOI: 10.1097/CAD.0b013e3283340cd7     Document Type: Article

References (51)

1. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, Berens ME. Molecular targets of glioma invasion. Cell Mol Life Sci 2007; 64:458-478.
2. Rao JS. Molecular mechanisms of glioma invasiveness: the role of proteases. Nat Rev Cancer 2003; 3:489-501.
3. Buck MR, Karutis DG, Day NA, Honn KV, Sloane KV. Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumor tissues. Biochem J 1992; 282:273-278.
4. Guo M, Mathieu PA, Linebaugh B, Sloane BF, Reiners JJ Jr. Phorbol ester activation of a proteolytic cascade capable of activating latent transforming growth factor XL a process initiated by the exocytosis of cathepsin B. J Biol Chem 2002; 277:14829-14837.
5. Kostoulas G, Lang A, Nagase H, Baici A. Stimulation of angiogenesis through cathepsin B inactivation of the tissue inhibitors of matrix metalloproteinases. FEBS Lett 1999; 455:286-290.
6. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002; 2:161-173.
7. Forsyth PA, Wong H, Laing TD, Rewcastle NB, Morris DG, Muzik H, et al. Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1-MMP) are involved in different aspects of the pathophysiology of malignant gliomas. Br J Cancer 1999; 79:1828-1835.
8. Baud V, Karin M. Is NFkB a good target for cancer therapy? Hopes and pitfalls. Nat Rev Drug Discov 2009; 8:33-40.
9. Nagai S, Washiyama K, Kurimoto M, Takaku A, Endo S, Kumanishi T. Aberrant nuclear factor-kappaB activity and its participation in the growth of human malignant astrocytoma. J Neurosurg 2002; 96:909-917.
10. Smith D, Shimamura T, Barbera S, Bejcek BE. NF-kB controls growth of glioblastomas/astrocytomas. Mol Cell Biochem 2008; 307:141-147.
11. Raychaudhuri B, Han Y, Lu T, Vogelbaum MA. Aberrant constitutive activation of nuclear factor kB in glioblastoma multiforme drives invasive phenotype. J Neurooncol 2007; 85:39-47.
12. Chintala SK, Sawaya R, Aggarwal BB, Majumder S, Giri DK, Kyritsis AP, et al. Induction of matrix metalloproteinase-9 requires a polymerized actin cytoskeleton in human malignant glioma cells. J Biol Chem 1998; 273:13545-13551.
13. Son YG, Kim EH, Kim JY, Kim SU, Kwon TK, Yoon A, et al. Silibinin sensitizes human glioma cells to TRAIL-mediated apoptosis via DR5 up-regulation and down-regulation of c-FLIP and Survivin. Cancer Res 2007; 67:8274-8284.
14. Cheung CW, Taylor PJ, Kirkpatrick CM, Vesey DA, Gobe GC,Winterford C, et al. Therapeutic value of orally administered silibinin in renal cell carcinoma: manipulation of insulin-like growth factor binding protein-3 levels. BJU Int 2007; 100:438-444.
15. Tyagi A, Agarwal C, Harrison G, Glode LM, Agarwal R. Silibinin causes cell cycle arrest and apoptosis in human bladder transitional cell carcinoma cells by regulating CDKI-CDK-cyclin cascade, and caspase 3 and PARP cleavages. Carcinogenesis 2004; 25:1711-1720.
16. Yang SH, Lin JK, Chen WS, Chiu JH. Anti-angiogenic effect of silymarin on colon cancer lovo cell line. J Surg Res 2003; 113:133-138.
17. Chu S, Chiou H, Chen P, Yang S, Hsieh Y. Silibinin inhibits the invasion of human lung cancer cells via decreased productions of urokinase-plasminogen activator and matrix metalloproteinase-2. Mol Carcinog 2004; 40:143-149.
18. Katiyar SK, Korman NJ, Mukhtar H, Agarwal R. Protective effects of silymarin against photocarcinogenesis in a mouse skin model. J Natl Cancer Inst 1997; 89:556-566.
19. Singh RP, Agarwal R. Prostate cancer prevention by silibinin. Curr Cancer Drug Targets 2004; 4:1-11.
20. Momeny M, Khorramizadeh MR, Ghaffari SH, Yousefi M, Yekaninejad MS, Esmaeili R, et al. Effects of silibinin on cell growth and invasive properties of a human hepatocellular carcinoma cell line, HepG-2, through inhibition of extracellular signal-regulated kinase 1/2 phosphorylation. Euro J Pharmacol 2008; 591:13-20.
21. Chen P, Hsieh Y, Chiang C, Chiou H, Yang S, Chu SC. Silibinin inhibits invasion of oral cancer cells by suppressing the MAPK pathway. J Dent Res 2006; 85:220-225.
22. Hsieh YS, Chu SC, Yang SF, Chen PN, Liu YC, Lu KH. Silibinin suppresses human osteosarcoma MG-63 cell invasion by inhibiting the ERK-dependent c-Jun/AP-1 induction of MMP-2. Carcinogenesis 2007; 28:977-987.
23. Lee S, Jeong Y, Im HG, Kim C, Chang Y, Lee IS. Silibinin suppresses PMA-induced MMP-9 expression by blocking the AP-1 activation via MAPK signaling pathways in MCF-7 human breast carcinoma cells. Biochem Biophys Res Commun 2007; 354:165-171.
24. Dhanalakshmi S, Singh RP, Agarwal C, Agarwal R. Silibinin inhibits constitutive and TNFalpha-induced activation of NF-kappaB and sensitizes human prostate carcinoma DU145 cells to TNFalpha-induced apoptosis. Oncogene 2002; 21:1759-1767. (Pubitemid 34259039)
25. Saliou C, Rihnc B, Cillardb J, Okamotod T, Packer L. Selective inhibition of NF-kB activation by the flavonoid hepatoprotector silymarin in HepG2: evidence for different activating pathways. FEBS Lett 1998; 440:8-12.
26. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 2008; 3:1101-1108.
27. Sawaya R, Ligon BL, Bindal AK, Bindal RK, Hess KR. Surgical treatment of metastatic brain tumors. J Neurooncol 1996; 27:269-277.
28. Sawaya RE, Yamamoto M, Gokaslan ZL,Wang SW, Mohanam S, Fuller GN, et al. Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin Exp Metastasis 1996; 14:35-42. (Pubitemid 26009753)
29. Kondraganti S, Mohanam S, Chintala SK, Kin Y, Jasti SL, Nirmala C, et al. Selective suppression of matrix metalloproteinase-9 in human glioblastoma cells by antisense gene transfer impairs glioblastoma cell invasion. Cancer Res 2000; 60:6851-6855.
30. Rao JS, Yamamoto M, Mohaman S, Gokaslan ZL, Fuller GN, Stetler-Stevenson WG, et al. Expression and localization of 92 kDa type IV collagenase/gelatinase B (MMP-9) in human gliomas. Clin Exp Metastasis 1996; 14:12-18. (Pubitemid 26009751)
31. Lakka SS, Rajan M, Gondi C, Yanamandra N, Chandrasekar N, Jasti SL, et al. Adenovirus-mediated expression of antisense MMP-9 in glioma cells inhibits tumor growth and invasion. Oncogene 2002; 21:8011-8019.
32. Mohanam S, Wang SW, Rayford A, Yamamoto M, Sawaya R, Nakajima M, et al. Expression of tissue inhibitors of metalloproteinases: negative regulators of human glioblastoma invasion in vivo. Clin Exp Metastasis 1995; 13:57-62.
33. Matsuzawa K, Fukuyama K, Hubbard SL, Dirks PB, Rutka JT. Transfection of an invasive human astrocytoma cell line with a TIMP-1 cDNA: modulation of astrocytoma invasive potential. J Neuropathol Exp Neurol 1996; 55:88-96.
34. Yamamoto M, Sawaya R, Mohanam S, Bindal AK, Bruner JM, Oka K, et al. Expression and localization of urokinase-type plasminogen activator in human astrocytomas in vivo. Cancer Res 1994; 54:3656-3661. (Pubitemid 24241173)
35. Gladson CL, Pijuan-Thompson V, Olman MA, Gillespie GY, Yacoub IZ. Up-regulation of urokinase and urokinase receptor genes in malignant astrocytoma. Am J Pathol 1995; 146:1150-1160.
36. Zhang X, Bu XY, Zhen HN, Fei Z, Zhang JN, Fu LA. Expression and localisation of urokinase-type plasminogen activator gene in gliomas. J Clin Neurosci 2000; 7:116-119. (Pubitemid 30482412)
37. Mohanam S, Sawaya R, McCutcheon I, Ali-Osman F, Boyd D, Rao JS. Modulation of in vitro invasion of human glioblastoma cells by urokinase-type plasminogen activator receptor antibody. Cancer Res 1993; 53:4143-4147.
38. Bhattacharya A, Lakka SS, Mohanam S, Boyd D, Rao JS. Regulation of the urokinase-type plasminogen activator receptor gene in different grades of human glioma cell lines. Clin Cancer Res 2001; 7:267-276.
39. Mohanam S, Jasti SL, Kondraganti SR, Chandrasekar N, Kin Y, Fuller GN, et al. Stable transfection of urokinase-type plasminogen activator antisense construct modulates invasion of human glioblastoma cells. Clin Cancer Res 2001; 7:2519-2526.
40. Mohanam S, Chintala SK, Go Y, Bhattacharya A, Venkaiah B, Boyd D, et al. In vitro inhibition of human glioblastoma cell line invasiveness by antisense uPA receptor. Oncogene 1997; 14:1351-1359.
41. Song H, Li Y, Lee J, Schwartz AL, Bu G. Low-density lipoprotein receptorrelated protein 1 promotes cancer cell migration and invasion by inducing the expression of matrix metalloproteinases 2 and 9. Cancer Res 2009; 69:879-886.
42. Demchik LL, Sameni M, Nelson K, Mikkelsen T, Sloane BF. Cathepsin B and glioma invasion. Int J Dev Neurosci 1999; 17:483-494.
43. Strojnik T, Zajc I, Bervar A, Zidanik B, Golouh R, Kos J, et al. Cathepsin B and its inhibitor stefin A in brain tumors. Pflugers Arch 2000; 439:R122-R123.
44. Konduri SD, Yanamandra N, Siddique K, Joseph A, Dinh DH, Olivero WC, et al. Modulation of cystatin C expression impairs the invasive and tumorigenic potential of human glioblastoma cells. Oncogene 2002; 21:8705-8712.
45. Konduri S, Lakka SS, Tasiou A, Yanamandra N, Gondi CS, Dinh DH, et al. Elevated levels of cathepsin B in human glioblastoma cell lines. Int J Oncol 2001; 19:519-524.
46. Mohanam S, Jasti SL, Kondraganti SR, Chandrasekar N, Lakka SS, Kin Y, et al. Down-regulation of cathepsin B expression impairs the invasive and tumorigenic potential of human glioblastoma cells. Oncogene 2001; 20:3665-3673.
47. Giusti I, D'Ascenzo S, Millimaggi D, Taraboletti G, Carta G, Franceschini N, et al. Cathepsin B mediates the pH-dependent proinvasive activity of tumorshed microvesicles. Neoplasia 2008; 10:481-488.
48. Bonizzi G, Karin M. The two NF-kappa activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25:280-288.
49. Demuth T, Berens ME. Molecular mechanisms of glioma cell migration and invasion. J Neurooncol 2004; 70:217-228.
50. Lakka SS, Gondi CS, Yanamandra N, Olivero WC, Dinh DH, Gujrati M, et al. Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduced tumor cell invasion, tumor growth and angiogenesis. Oncogene 2004; 23:4681-4689.
51. Gondi CS, Kandhukuri N, Kondraganti S, Gujrati M, Olivero WC, Dinh DH, et al. RNA interference-mediated simultaneous down-regulation of urokinase-type plasminogen activator receptor and cathepsin B induces caspase-8-mediated apoptosis in SNB19 human glioma cells. Mol Cancer Ther 2006; 5:3197-3208.