S-Adenosylhomocysteine promotes the invasion of C6 glioma cells via increased secretion of matrix metalloproteinase-2 in murine microglial BV2 cells

Toxicological Sciences

Volumn 112, Issue 2, 2009, Pages 322-330

  Lin, Hung Chi ^a   Song, Tuzz Ying ^b   Hu, Miao Lin ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b CHUNG CHOU INSTITUTE OF TECHNOLOGY   (Taiwan)

Author keywords

Invasion; MMP 2; S Adenosylhomocysteine

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; GELATINASE A; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; PROTEIN C JUN; PROTEIN KINASE B; S ADENOSYLHOMOCYSTEINE; SYNAPTOPHYSIN; PRIMER DNA; PROTEIN KINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CANCER INVASION; CONCENTRATION PROCESS; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; GLIOMA CELL; MICROGLIA; MOUSE; NEUROTOXICITY; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; ENZYMOLOGY; GLIOMA; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

MURINAE;

ANIMALS; BASE SEQUENCE; CELL LINE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; CULTURE MEDIA, CONDITIONED; DNA PRIMERS; GLIOMA; MATRIX METALLOPROTEINASE 2; MICE; MICROGLIA; NEOPLASM INVASIVENESS; NF-KAPPA B; PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; S-ADENOSYLHOMOCYSTEINE; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TRANSCRIPTION FACTORS;

EID: 74949089273     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp218     Document Type: Article

References (44)

1. Bergman, M. R., Cheng, S., Honbo, N., Piacentini, L., Karliner, J. S., and Lovett, D. H. (2003). A functional activating protein 1 (AP-1) site regulates matrix metalloproteinase 2 (MMP-2) transcription by cardiac cells through interactions with JunB-Fra1 and JunB-FosB heterodimers. Biochem. J 369, 485-496.
2. Bernstein, J. J., Goldberg, W. J., Laws, E. R., Jr, Conger, D., Morreale, V., and Wood, L. R. (1990). C6 glioma cell invasion and migration of rat brain after neural homografting: ultrastructure. Neurosurgery 26, 622-628.
3. Bonne, T. C., Johnson, M. J., De Clerck, Y. A., and Langley, K. E. (1990). cDNA cloning and expression of a metalloproteinase inhibitor related to tissue inhibitor of metalloproteinase. Proc. Natl. Acad. Sci. U.S.A 87, 2800-2804.
4. Brew, K., Dinakarpandian, D., and Nagase, H. (2000). Tissue inhibitors of metalloproteinase: Evolution, structure and function. Biochim. Biophys. Acta 1477, 267-283.
5. Chan-Hui, P., and Weaver, R. (1998). Human mitogen-activated protein kinase kinase kinase mediates the stress-induced activation of mitogen-activated protein kinase cascades. Biochem. J 336, 599-609.
6. Chen, Y. C., Kuo, T. C., Lin-Shiau, S. Y., and Lin, J. K. (1996). Induction of HSP70 gene expression by modulation of Ca(+2) ion and cellular p53 protein by curcumin in colorectal carcinoma cells. Mol. Carcinog 17, 224-234.
7. Collart, M. A., Baeuerle, P., and Vasalli, P. (1990). Regulation of tumor necrosis factor alpha transcription in macrophages: Involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B. Mol. Cell. Biol. 19, 1498-1505.
8. Crocker, S. J., Milner, R., Pham-Mitchell, N., and Campbell, I. L. (2006). Cell and agonist-specific regulation of genes for matrix metalloproteinases and their tissue inhibitors by primary glial cells. J. Neurochem. 98, 812-823.
9. Deryugina, E. I., Bourdon, M. A., Luo, G. X., Reisfeld, R. A., and Strongin, A. (1997). Matrix metalloproteinase-2 activation modulates glioma cell migration. J. Cell Sci. 110, 2473-2482.
10. Finkelstein, J. D. (2000). Pathways and regulation of homocysteine metabolism in mammals. Semin. Thromb. Hemost. 26, 219-225.
11. Fu, W., Dudman, N. P. B., Perry, M. A., Young, K., and Wang, X. I. (2000). Interrelation between plasma homocysteine and intracellular S-adenosylhomocysteine. Biochem. Biophys. Res. Commun 271, 47-53.
12. Goldberg, W. J., Law, E. R., Jr, and Bernstein, J. J. (1991). Individual C6 glioma cells migrate in adult rat brain after neural homografting. Int. J. Dev. Neurosci 9, 427-437.
13. Greene, J., Wang, M., Liu, Y. E., Raymond, L. A., Rosen, C., and Shi, Y. E. (1996). Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J. Biol. Chem. 271, 30375-30380.
14. Guo, P., Imanishi, Y., and Cackowski, F. C. (2005). Up-regulation of angiopoietin-2, matrix metalloproteinase-2, membrane type 1 metalloproteinase, and laminin 5 gamma 2 correlates with the invasiveness of human glioma. Am. J. Pathol. 196, 701-711.
15. Hoffman, D. R., Marion, D. W., Cornatzer, W. E., and Duerre, J. A. (1980). S-adenosylmethionine and S-adenosylhomocysteine metabolism in isolated liver. J. Biol. Chem. 22, 10822-10827.
16. Hwang, H. J., Park, H. J., Chung, H. J., Min, H. Y., Park, E. J., Hong, J. Y., and Lee, S. K. (2006). Inhibitory effects of caffeic acid phenethyl ester on cancer cell metastasis mediated by the down-regulation of matrix metalloproteinase expression in human HT1080 fibrosarcoma cells. J. Nutr. Biochem 17, 356-362.
17. James, S. J., Melnyk, S., Pogribny, M., Pogribny, I. P., and Caudill, M. A. (2002). Elevation in S-adenosylhomocysteine and DNA hypomethylation: Potential epigenetic mechanism for homocysteine-related pathology. J. Nutr 132, 2361S-2366S.
18. Kennedy, B. P., Bottiglieri, T., Hansen, A., and Masliah, E. (2004). Elevated S-adenosylhomocysteine in Alzheimer's brain: Influence on methyltransferase and cognitive function. J. Neural. Transm 111, 547-567.
19. Kerins, D. M., Koury, M. J., Capdevila, A., Rana, S., and Wagner, C. (2001). Plasma S-adenosylhomocysteine is a more sensitive indicator of cardiovascular disease than plasma homocysteine. Am. J. Clin. Nutr. 74, 723-729.
20. Kotelevets, L., Noë, V., Bruyneel, E., Myssiakine, E., Chastre, E., Mareel, M., and Gespach, C. (1998). Inhibition by platelet-activating factor of Src- and hepatocyte growth factor-dependent invasiveness of intestinal and kidney epithelial cells. Phosphatidylinositol 3'-kinase is a critical mediator of tumor invasion. J. Biol. Chem. 273, 14138-14145.
21. Liu, P., Cheng, H., Roberts, T. M., and Zhao, J. J. (2009). Targeting the phosphoinositide 3-kinase pathway in cancer. Nat. Rev. Drug Discov. 8, 627-644.
22. Lominadze, D., Roberts, A., Tyagi, N., and Tyagi, S. (2006). Homocysteine causes cerebrovascular leakage in mice. Am. J. Physiol. Heart Circ. Physiol. 290, H1206-H1213.
23. Markovic, D. S., Glass, R., Synowitz, M., Rooijen, N., and Kettenmann, H. (2005). Microglia stimulate the invasiveness of glioma cells by increasing the activity of metalloproteinase-2. J. Neuropathol. Exp. Neurol. 64, 754-762.
24. Moshal, K. S., Sen, U., Tyagi, N., Henderson, B., Steed, M., Ovechkin, A. V., and Tyagi, S. C. (2006). Regulation of homocysteine-induced MMP-9 by ERK1/2 pathways. Am. J. Physiol. Cell Physiol 290, 883-891.
25. Philip, S., and Kundu, G. C. (2003). Osteopontin induces nuclear factor kappa B-mediated promatrix metalloproteinase-2 activation through I kappa B alpha/IKK signaling pathways, and curcumin (diferulolylmethane) down-regulates these pathways. J. Biol. Chem. 278, 14487-14497.
26. Rao, J. S. (2003). Molecular mechanisms of glioma invasiveness: The role of proteases. Nat. Rev. Cancer 3, 489-501.
27. Repesh, L. A. (1989). A new in vitro assay for quantitating tumor cell invasion. Invasion Metastasis 9, 192-208.
28. Rosell, A., Ortega-Aznar, A., Alvarez-Sabin, J., Ribo, M., Molina, C. A., Lo, E. H., and Montaner, J. (2006). Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 37, 1399-1406.
29. Sampieri, C. L., Nuttall, R. K., Young, D. A., Goldspink, D., Clark, I. M., and Edward, D. R. (2008). Activation of p38 and JNK MAPK pathways abrogates requirement for new protein synthesis for phorbol ester mediated induction of select MMP and TIMP genes. Matrix Biol. 27, 128-138.
30. Sato, H., and Seiki, M. (1993). Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene 8, 395-405.
31. Schreck, R., and Baeuerle, P. A. (1990). NF-kappa B as inducible transcriptional activator of the granulocyte-macrophage colony-stimulating factor gene. Mol. Cell. Biol. 10, 1281-1286.
32. Shukla, S., Maclennan, G. T., Marengo, S. R., Resnick, M. I., and Gupta, S. (2005). Constitutive activation of P I3 K-Akt and NF-kappaB during prostate cancer progression in autochthonous transgenic mouse model. Prostate 64, 224-239.
33. Takahra, T., Smart, D. E., Oakley, F., and Mann, D. A. (2004). Induction of myofibroblast MMP-9 transcription in three-dimensional collagen I gel cultures: Regulation by NF-kappaB, AP-1 and Sp1. Int. J. Biochem. Cell Biol. 36, 353-363.
34. Tews, D. S. (2000). Adhesive and invasive features in gliomas. Pathol. Res. Pract 196, 701-711.
35. Theodorescu, D., Laderoute, K. R., and Gulding, K. M. (1998). Epidermal growth factor receptor-regulated human bladder cancer motility is in part a phosphatidylinositol 3-kinase-mediated process. Cell Growth Differ 9, 919-928.
36. Valli, A., Carrero, J. J., Qureshi, A. R., Garibotto, G., Barany, P., Axelsson, J., Lindholm, B., Stenvinkel, P., Anderstam, B., and Suliman, M. E. (2008). Elevated serum levels of S-adenosylhomocysteine, but not homocysteine, are associated with cardiovascular disease in stage 5 chronic kidney disease patients. Clin. Chim. Acta 395, 106-110.
37. Wagner, C., and Koury, M. J. (2007). S-adenosylhomocysteine: A better indicator of vascular disease than homocysteine? Am. J. Clin. Nutr. 86, 1581-1585.
38. Watters, J. J., Schartner, J. M., and Badie, B. (2005). Microglia function in brain tumors. J. Neurosci. Res. 81, 447-455.
39. Yamamoto, M., Mohanam, S., Sawaya, R., Fuller, G. N., Seiki, M., Sato, H., Gokaslan, Z. L., Liotta, L. A., Nicolson, G. L., and Rao, J. S. (1996). Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivo and in vitro. Cancer Res. 56, 384-392.
40. Yan, C., and Boyd, D. D. (2007). Regulation of matrix metalloproteinase gene expression. J. Cell Physiol. 211, 19-26.
41. Yang, T. H., and Hu, M. L. (2006). Intracellular levels of S-Adenosylhomocysteine but not homocysteine are highly correlated to the expression of nm23-H1 and the level of 5-methyldeoxycytidine in human hepatoma cells with different invasion activities. Nutr. Cancer 55, 224-231.
42. Yi, P., Melnyk, S., Pogribna, M., Pogribny, I. P., Hinet, R. J., and James, S. J. (2000). Increase in plasma homocysteine associated with parallel increases in plasma S-adenosylhomocysteine and lymphocyte DNA hypomethylation. J. Biol. Chem. 275, 29318-323.
43. Yong, V. W., Power, C., Forsyth, P., and Edwards, D. (2001). Metal-loproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2, 502-511.
44. Zhang, Z. H., Liu, X. G., Chen, G. P., Zhang, X. R., and Guo, M. Y. (2004). Significance of MMP-2 and TIMP-2 mRNA expressions on glomerular cells in the development of glomerulosclerosis. Chin. Med. Sci. J. 9, 84-88.