Exogenous C2 ceramide suppresses matrix metalloproteinase gene expression by inhibiting ROS production and MAPK signaling pathways in PMA-stimulated human astroglioma cells

International Journal of Molecular Sciences

Volumn 17, Issue 4, 2016, Pages

  Jung, Ji Sun ^a   Ahn, Young Ho ^a   Moon, Byung In ^a   Kim, Hee Sun ^a  

^a Ewha Womans University School of Medicine   (South Korea)

Author keywords

Astroglioma; C2 ceramide; Invasion; MMP; Signaling mechanism

Indexed keywords

C2 CERAMIDE; CERAMIDE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERSTITIAL COLLAGENASE; MATRIGEL; MATRIX METALLOPROTEINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PHORBOL 13 ACETATE 12 MYRISTATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; STROMELYSIN; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; MITOGEN ACTIVATED PROTEIN KINASE; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; ASTROCYTOMA; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; MATRIX METALLOPROTEINASE GENE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; CELL MOTION; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ASTROCYTOMA; CELL LINE, TUMOR; CELL MOVEMENT; CERAMIDES; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMANS; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NADPH OXIDASE; NF-KAPPA B; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTOR AP-1;

EID: 84962091485     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17040477     Document Type: Article

References (36)

1. Nagase, H.; Visse, R.; Murphy, G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006, 69, 562-573. [CrossRef] [PubMed]
2. Yong, V.W.; Krekoski, C.A.; Forsyth, P.A.; Bell, R.; Edwards, D.R. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci. 1998, 21, 75-80. [CrossRef]
3. Hua, H.; Li, M.; Luo, T.; Yin, Y.; Jiang, Y. Matrix metalloproteinases in tumorigenesis: An evolving paradigm. Cell. Mol. Life Sci. 2011, 68, 3853-3868. [CrossRef] [PubMed]
4. Onishi, M.; Ichikawa, T.; Kurozumi, K.; Date, I. Angiogenesis and invasion in glioma. Brain Tumor Pathol. 2011, 28, 13-24. [CrossRef] [PubMed]
5. Rao, J.S. Molecular mechanisms of glioma invasiveness: The role of proteases. Nat. Rev. Cancer 2003, 3, 489-501. [CrossRef] [PubMed]
6. Huang, H.C.; Tsai, L.L.; Tsai, J.P.; Hsieh, S.C.; Yang, S.F.; Hsueh, J.T.; Hsieh, Y.H. Licochalcone A inhibits the migration and invasion of human lung cancer cells via inactivation of the Akt signaling pathway with downregulation of MMP-1/-3 expression. Tumour Biol. 2014, 35, 12139-12149. [CrossRef] [PubMed]
7. Mercapide, J.; Lopez De Cicco, R.; Castresana, J.S.; Klein-Szanto, A.J. Stromelysin-1/matrix metalloproteinase-3 (MMP-3) expression accounts for invasive properties of human astrocytoma cell line. Int. J. Cancer 2003, 106, 676-682. [CrossRef] [PubMed]
8. Sawaya, R.; Go, Y.; Kyritisis, A.P.; Uhm, J.; Venkaiah, B.; Mohanam, S.; Gokaslan, Z.L.; Rao, J.S. Elevated levels of Mr 92,000 type IV collagenase during tumor growth in vivo. Biochem. Biophys. Res. Commun. 1998, 251, 632-636. [CrossRef] [PubMed]
9. Saddoughi, S.A.; Ogretmen, B. Diverse functions of ceramide in cancer cell death and proliferation. Adv. Cancer Res. 2013, 117, 37-58. [PubMed]
10. Galadari, S.; Rahman, A.; Pallichankandy, S.; Thayyullathil, F. Tumor suppressive functions of ceramide: Evidence and mechanisms. Apoptosis 2015, 20, 689-711. [CrossRef] [PubMed]
11. Dany, M.; Ogretmen, B. Ceramide induced mitophagy and tumor suppression. Biochim. Biophys. Acta 2015, 1853, 2834-2845. [CrossRef] [PubMed]
12. Hartmann, D.; Lucks, J.; Fuchs, S.; Schiffmann, S.; Schreiber, Y.; Ferreirós, N.; Merkens, J.; Marschalek, R.; Geisslinger, G.; Grösch, S. Long chain ceramides and very long chain ceramides have opposite effects on human breast and colon cancer cell growth. Int. J. Biochem. Cell Biol. 2012, 44, 620-628. [CrossRef] [PubMed]
13. Zhu,W.;Wang, X.; Zhou, Y.;Wang, H. C2-ceramide induces cell death and protective autophagy in head and neck squamous cell carcinoma cells. Int. J. Mol. Sci. 2014, 15, 3336-3355. [CrossRef] [PubMed]
14. Qin, L.S.; Yu, Z.Q.; Zhang, S.M.; Sun, G.; Zhu, J.; Xu, J.; Guo, J.; Fu, L.S. The short chain cell-permeable ceramide (C6) restores cell apoptosis and perifosine sensitivity in cultured glioblastoma cells. Mol. Biol. Rep. 2013, 40, 5645-5655. [CrossRef] [PubMed]
15. Debret, R.; Brassart-Pasco, S.; Lorin, J.; Martoriati, A.; Deshorgue, A.; Maquart, F.X.; Hornebeck, W.; Rahman, I.; Antonicelli, F. Ceramide inhibition of MMP-2 expression and human cancer bronchial cell invasiveness involve decreased histone acetylation. Biochim. Biophys. Acta 2008, 1783, 1718-1727. [CrossRef] [PubMed]
16. Lee, E.J.; Kim, S.Y.; Hyun, J.W.; Min, S.W.; Kim, D.H.; Kim, H.S. Glycitein inhibits glioma cell invasion through down-regulation of MMP-3 and MMP-9 gene expression. Chem. Biol. Interact. 2010, 15, 18-24. [CrossRef] [PubMed]
17. Kim, Y.S.; Joh, T.H. Matrix metalloproteinases, new insights into the understanding of neurodegenerative disorders. Biomol. Ther. (Seoul) 2012, 20, 133-143. [CrossRef] [PubMed]
18. Kim, S.Y.; Jung, S.H.; Kim, H.S. Curcumin is a potent broad spectrum inhibitor of matrix metalloproteinase gene expression in human astroglioma cells. Biochem. Biophys. Res. Commun. 2005, 337, 510-516. [CrossRef] [PubMed]
19. Nelson, K.K.; Melendez, J.A. Mitochondrial redox control of matrix metalloproteinases. Free Radic. Biol. Med. 2004, 37, 768-784. [CrossRef] [PubMed]
20. Szatrowski, T.P.; Nathan, C.F. Production of large amounts of hydrogen peroxide by human tumour cells. Cancer Res. 1991, 51, 794-798. [PubMed]
21. Lin, C.W.; Yang, L.Y.; Shen, S.C.; Chen, Y.C. IGF-I plus E2 induces proliferation via activation of ROS-dependent ERKs and JNKs in human breast carcinoma cells. J. Cell. Physiol. 2007, 212, 666-674. [CrossRef] [PubMed]
22. Wu,W.S. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 2006, 25, 695-705. [CrossRef] [PubMed]
23. Nishikawa, M. Reactive oxygen species in tumor metastasis. Cancer Lett. 2008, 266, 53-59. [CrossRef] [PubMed]
24. Belkhiri, A.; Richards, C.; Whaley, M.; McQueen, S.A.; Orr, F.W. Incresed expression of activated matrix metalloproteinase-2 by human endothelial cells after subethal H2O2 exposure. Lab. Investig. 1997, 77, 533-539. [PubMed]
25. Nelson, K.K.; Subbaram, S.; Connor, K.M.; Dasgupta, J.; Ha, X.F.; Meng, T.C.; Tonks, N.K.; Melendez, J.A. Redox-dependent matrix metalloproteinase-1 expression is regulated by JNK through Ets and AP-1 promoter motifs. J. Biol. Chem. 2006, 281, 14100-14110. [CrossRef] [PubMed]
26. Zhang, B.; Liu, Z.; Hu, X. Inhibiting cancer metastasis via targeting NADPH oxidase 4. Biochem. Pharmacol. 2013, 86, 253-266. [CrossRef] [PubMed]
27. Ushio-Fukai, M. Localizing NADPH oxidase-derived ROS. Sci. STKE 2006, 349, re8. [CrossRef] [PubMed]
28. Lambeth, J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 2004, 4, 181-189. [CrossRef] [PubMed]
29. Babior, B.M. NADPH oxidase: An update. Blood 1999, 93, 1464-1476. [PubMed]
30. Cheng, G.; Cao, Z.; Xu, Z.; van Meir, E.G.; Lambeth, J.D. Homologs of gp91phox: Cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 2001, 269, 131-140. [CrossRef]
31. Shono, T.; Yokoyama, N.; Uesaka, T.; Kuroda, J.; Takeya, R.; Yamasaki, T.; Amano, T.; Mizoguchi, M.; Suzuki, S.O.; Niiro, H.; et al. Enhanced expression of NADPH oxidase Nox4 in human gliomas and its roles in cell proliferation and survival. Int. J. Cancer 2008, 123, 787-792. [CrossRef] [PubMed]
32. Hsieh, C.H.; Shyu, W.C.; Chiang, C.Y.; Kuo, J.W.; Shen, W.C.; Liu, R.S. NADPH oxidase subunit 4-mediated reactive oxygen species contribute to cycling hypoxia-promoted tumor progression in glioblastoma multiforme. PLoS ONE 2011, 6, e23945. [CrossRef] [PubMed]
33. Hsieh, C.H.; Chang, H.T.; Shen, W.C.; Shyu, W.C.; Liu, R.S. Imaging the impact of Nox4 in cycling hypoxia-mediated U87 glioblastoma invasion and infiltration. Mol. Imaging Biol. 2012, 14, 489-499. [CrossRef] [PubMed]
34. Jung, S.H.;Woo, M.S.; Kim, S.Y.; Kim,W.K.; Hyun, J.W.; Kim, E.J.; Kim, D.H.; Kim, H.S. Ginseng saponin metabolite suppresses phorbol ester-induced matrix metalloproteinase-9 expression through inhibition of activator protein-1 and mitogen-activated protein kinase signaling pathways in human astroglioma cells. Int. J. Cancer 2006, 118, 490-497. [CrossRef] [PubMed]
35. Woo, M.S.; Jung, S.H.; Kim, S.Y.; Hyun, J.W.; Ko, K.H.; Kim, W.K.; Kim, H.S. Curcumin suppresses phorbol ester-induced matrix metalloproteinase-9expression by inhibiting the PKC to MAPK signaling pathways in human astroglioma cells. Biochem. Biophys. Res. Commun. 2005, 335, 1017-1025. [CrossRef] [PubMed]
36. Jung, J.S.; Ahn, J.H.; Le, T.K.; Kim, D.H.; Kim, H.S. Protopanaxatriol ginsenoside Rh1 inhibits the expression of matrix metalloproteinases and the in vitro invasion/migration of human astroglioma cells. Neurochem. Int. 2013, 63, 80-86. [CrossRef] [PubMed]