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http://dx.doi.org/10.4062/biomolther.2012.20.3.286

Transglutaminase-2 Is Involved in All-Trans Retinoic Acid-Induced Invasion and Matrix Metalloproteinases Expression of SH-SY5Y Neuroblastoma Cells via NF-κB Pathway  

Lee, Hye-Ja (College of Pharmacy, Dongguk University)
Park, Mi-Kyung (College of Pharmacy, Dongguk University)
Bae, Hyun-Cheol (Division of Cancer Biology, Research Institute, National Cancer Center)
Yoon, Hee-Jung (Division of Cancer Biology, Research Institute, National Cancer Center)
Kim, Soo-Youl (Division of Cancer Biology, Research Institute, National Cancer Center)
Lee, Chang-Hoon (College of Pharmacy, Dongguk University)
Publication Information
Biomolecules & Therapeutics / v.20, no.3, 2012 , pp. 286-292 More about this Journal
Abstract
All-trans retinoic acid (ATRA) is currently used in adjuvant differentiation-based treatment of residual or relapsed neuroblastoma (NB). It has been reported that short-term ATRA treatment induces migration and invasion of SH-SY5Y via transglutaminase-2 (Tgase-2). However, the detailed mechanism of Tgase-2's involvement in NB cell invasion remains unclear. Therefore we investigated the role of Tgase-2 in invasion of NB cells using SH-SY5Y cells. ATRA dose-dependently induced the invasion of SH-SY5Y cells. Cystamine (CTM), a well known tgase inhibitor suppressed the ATRA-induced invasion of SH-SY5Y cells in a dose-dependent manner. Matrix metalloproteinase -9 (MMP-9) and MMP-2, well known genes involved in invasion of cancer cells were induced in the ATRA-induced invasion of the SH-SH5Y cells. Treatment of CTM suppressed the MMP-9 and MMP-2 enzyme activities in the ATRA-induced invasion of the SH-SY5Y cells. To confirm the involvement of Tgase-2, gene silencing of Tgase-2 was performed in the ATRA-induced invasion of the SH-SH5Y cells. The siRNA of Tgase-2 suppressed the MMP-9 and MMP-2 activity of the SH-SY5Y cells. MMP-2 and MMP-9 are well known target genes of NF-${\kappa}B$. Therefore the relationship of Tgase-2 and NF-${\kappa}B$ in the ATRA-induced invasion of the SH-SY5Y cells was examined using siRNA and CTM. ATRA induced the activation of NF-${\kappa}B$ in the SH-SY5Y cells and CTM suppressed the activation of NF-${\kappa}B$. Gene silencing of Tgase-2 suppressed the MMP expression by ATRA. These results suggested that Tgase-2 might be a new target for controlling the ATRA-induced invasion of NBs.
Keywords
All-trans retinoic acid; Transglutaminase-2; Invasion; Neuroblastoma; NF-${\kappa}B$; Matrix metalloproteinase;
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1 Kim, D. S., Park, S. S., Nam, B. H., Kim, I. H. and Kim, S. Y. (2006) Reversal of drug resistance in breast cancer cells by transglutaminase 2 inhibition and nuclear factor-kappaB inactivation. Cancer Res. 66, 10936-10943.   DOI   ScienceOn
2 Brodeur, G. M. (2002). Signifi cance of intratumoral genetic heterogeneity in neuroblastomas. Med. Pediatr. Oncol. 38, 112-113.   DOI
3 Cha, D. S., Shin, T. Y., Eun, J. S., Kim, D. K. and Jeon, H. (2011) Anti-metastatic properties of the leaves of Eriobotrya japonica. Arch. Pharm. Res. 34, 425-436.   DOI
4 Cho, S. Y., Jeong, E. M., Lee, J. H., Kim, H. J., Lim, J., Kim, C. W., Shin, D. M., Jeon, J. H., Choi, K. and Kim, I. G. (2012) Doxorubicin induces the persistent activation of intracellular transglutaminase 2 that protects from cell death. Mol. Cells 33, 235-241.   DOI
5 Cianfarani, S. and Rossi, P. (1997) Neuroblastoma and insulin-like growth factor system. New insights and clinical perspectives. Eur. J. Pediatr. 156, 256-261.   DOI
6 Condello, S., Caccamo, D., Currò, M., Ferlazzo, N., Parisi, G. and Ientile, R. (2008) Transglutaminase 2 and NF-kappaB interplay during NGF-induced differentiation of neuroblastoma cells. Brain Res. 1207, 1-8.   DOI
7 De Bosscher, K., Vanden Berghe, W. and Haegeman, G. (2006) Cross-talk between nuclear receptors and nuclear factor kappaB. Oncogene 25, 6868-6886.   DOI
8 DuBois, S. G., Kalika, Y., Lukens, J. N., Brodeur, G. M., Seeger, R. C., Atkinson, .J B., Haase, G. M., Black, C. T., Perez, C., Shimada, H., Gerbing, R., Stram, D. O. and Matthay, K. K. (1999) Metastatic sites in stage IV and IVS neuroblastoma correlate with age, tumor biology, and survival. J. Pediatr. Hematol. Oncol. 21, 181-189.   DOI
9 Farina, A. R., Masciulli, M. P., Tacconelli, A., Cappabianca, L., De Santis, G., Gulino, A. and Mackay, A. R. (2002) All-trans-retinoic acid induces nuclear factor kappaB activation and matrix metalloproteinase-9 expression and enhances basement membrane invasivity of differentiation-resistant human SK-N-BE 9N neuroblastoma Cells. Cell Growth Differ. 13, 343-354.
10 Akimov, S. S., Krylov, D., Fleischman, L. F. and Belkin, A. M. (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J. Cell Biol. 148, 825-838.   DOI   ScienceOn
11 Ara, T. and DeClerck, Y. A. (2006) Mechanisms of invasion and metastasis in human neuroblastoma. Cancer Metastasis Rev. 25, 645-657.
12 Arenzana-Seisdedos, F., Thompson, J., Rodriguez, M. S., Bachelerie, F., Thomas, D. and Hay, R. T. (1995) Inducible nuclear expression of newly synthesized I kappa B alpha negatively regulates DNAbinding and transcriptional activities of NF-kappa B. Mol. Cell Biol. 15, 2689-2696.
13 Sato, S., Seki, N., Hotta, Y. and Tabata, S. (1995) Expression profiles of a human gene identifi ed as a structural homologue of meiosisspecific recA-like genes. DNA Res. 2, 183-186.   DOI
14 Beck, K. E., De Girolamo, L. A., Griffi n, M. and Billett, E. E. (2006) The role of tissue transglutaminase in 1-methyl-4-phenylpyridinium (MPP+)-induced toxicity in differentiated human SH-SY5Y neuroblastoma cells. Neurosci. Lett. 405, 46-51.   DOI
15 Boccaccio, C. and Comoglio, P. M. (2006) Invasive growth: a METdriven genetic programme for cancer and stem cells. Nat. Rev. Cancer 6, 637-645.   DOI
16 Zemskov, E. A., Janiak, A., Hang, J., Waghray, A. and Belkin, A. M. (2006) The role of tissue transglutaminase in cell-matrix interactions. Front Biosci. 11, 1057-1076.   DOI
17 Park, M. K., Lee, H. J., Shin, J., Noh, M., Kim, S. Y. and Lee, C. H. (2011) Novel participation of transglutaminase-2 through c-Jun Nterminal kinase activation in sphingosylphosphorylcholine-induced keratin reorganization of PANC-1 cells. Biochim. Biophys. Acta 1811, 1021-1029.   DOI
18 Priglinger, S. G., Alge, C. S., Neubauer, A. S., Kristin, N., Hirneiss, C., Eibl, K., Kampik, A. and Welge-Lussen, U. (2004) TGF-beta2-induced cell surface tissue transglutaminase increases adhesion and migration of RPE cells on fi bronectin through the gelatin-binding domain. Invest. Ophthalmol. Vis. Sci. 45, 955-963.   DOI
19 Redfern, C. P., Lovat, P. E., Malcolm, A. J. and Pearson, A. D. (1995) Gene expression and neuroblastoma cell differentiation in response to retinoic acid: differential effects of 9-cis and all-trans retinoic acid. Eur. J. Cancer 31A, 486-494.
20 Roy Choudhury, S., Karmakar, S., Banik, N. L. and Ray, S. K. (2012) Targeting angiogenesis for controlling neuroblastoma. J. Oncol. 2012, 782020.
21 Schmidt, C., Bladt, F., Goedecke, S., Brinkmann, V., Zschiesche, W., Sharpe, M., Gherardi, E. and Birchmeier, C. (1995) Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373, 699-702.   DOI
22 Sugiura, Y., Shimada, H., Seeger, R. C., Laug, W. E. and DeClerck, Y. A. (1998) Matrix metalloproteinases-2 and -9 are expressed in human neuroblastoma: contribution of stromal cells to their production and correlation with metastasis. Cancer Res. 58, 2209-2216.
23 Woessner, J. F. Jr. (2002) MMPs and TIMPs--an historical perspective. Mol. Biotechnol. 22, 33-49.   DOI
24 Natoli, G. and Chiocca, S. (2008) Nuclear ubiquitin ligases, NF-kappaB degradation, and the control of inflammation. Sci. Signal. 1, pe1.   DOI
25 Lee, J. S., Kim, I. H. and Kim, S. Y. (2006) Changes in gene expression with increased transglutaminase 2 in a SH-SY5Y cell line. Front Biosci. 11, 2774-2781.   DOI
26 Kweon, S. M., Lee, Z. W., Yi, S. J., Kim, Y. M., Han, J. A., Paik, S. G. and Ha, S. S. (2004) Protective role of tissue transglutaminase in the cell death induced by TNF-alpha in SH-SY5Y neuroblastoma cells. J. Biochem. Mol. Biol. 37, 185-191.   DOI
27 Lee, A. C. (2012) Neuroblastoma: the challenge remains. Singapore Med. J. 53, 1-2.
28 Lee, C. H. and Kim, S. Y. (2009) NF-kappaB and therapeutic approach. Biomol. Ther. 17, 219-240.   DOI
29 Lee, J., Kim, Y. S., Choi, D. H., Bang, M. S., Han, T. R., Joh, T. H. and Kim, S. Y. (2004) Transglutaminase 2 induces nuclear factorkappaB activation via a novel pathway in BV-2 microglia. J. Biol. Chem. 279, 53725-53735.   DOI
30 Mackay, A. R., Ballin, M., Pelina, M. D., Farina, A. R., Nason, A. M., Hartzler, J. L. and Thorgeirsson, U. P. (1992) Effect of phorbol ester and cytokines on matrix metalloproteinase and tissue inhibitor of metalloproteinase expression in tumor and normal cell lines. Invasion Metastasis 12, 168-184.
31 Mehta, K., Fok, J., Miller, F. R., Koul, D. and Sahin, A. A. (2004) Prognostic significance of tissue transglutaminase in drug resistant and metastatic breast cancer. Clin. Cancer Res. 10, 8068-8076.   DOI
32 Modak, S. and Cheung, N. K. (2010) Neuroblastoma: Therapeutic strategies for a clinical enigma. Cancer Treat. Rev. 36, 307-317.   DOI   ScienceOn
33 Mueller, S. and Matthay, K. K. (2009) Neuroblastoma: biology and staging. Curr. Oncol. Rep. 11, 431-438.   DOI
34 Garattini, E., Gianni, M. and Terao, M. (2007) Retinoids as differentiating agents in oncology: a network of interactions with intracellular pathways as the basis for rational therapeutic combinations. Curr. Pharm. Des. 13, 1375-1400.   DOI
35 Murtaugh, M. P., Dennison, O., Stein, J. P. and Davies, P. J. (1986) Retinoic acid-induced gene expression in normal and leukemic myeloid cells. J. Exp. Med. 163, 1325-1330.   DOI
36 Festuccia, C., Bologna, M., Vicentini, C., Tacconelli, A., Miano, R., Violini, S. and Mackay, A. R. (1996) Increased matrix metalloproteinase- 9 secretion in short-term tissue cultures of prostatic tumor cells. Int. J. Cancer 69, 386-393.   DOI
37 Freemantle, S. J., Spinella, M. J. and Dmitrovsky, E. (2003) Retinoids in cancer therapy and chemoprevention: promise meets resistance. Oncogene 22, 7305-7315.   DOI   ScienceOn
38 Guidez, F., Li, A. C., Horvai, A., Welch, J. S. and Glass, C. K. (1998) Differential utilization of Ras signaling pathways by macrophage colony-stimulating factor (CSF) and granulocyte-macrophage CSF receptors during macrophage differentiation. Mol. Cell Biol. 18, 3851-3861.
39 Gurney, J. G., Ross, J. A., Wall, D. A., Bleyer, W. A., Severson, R. K. and Robison, L. L. (1997) Infant cancer in the U.S.: histologyspecifi c incidence and trends, 1973 to 1992. J. Pediatr. Hematol. Oncol. 19, 428-432.   DOI
40 Joshi, S., Guleria, R., Pan, J., DiPette, D. and Singh, U. S. (2006) Retinoic acid receptors and tissue-transglutaminase mediate short-term effect of retinoic acid on migration and invasion of neuroblastoma SH-SY5Y cells. Oncogene 25, 240-247.
41 Karin, M. and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18, 621-663.   DOI   ScienceOn