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Tazarotene-Induced Gene 1 Enhanced Cervical Cell Autophagy through Transmembrane Protein 192

  • Shyu, Rong-Yaun (Department of Internal Medicine, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation) ;
  • Wang, Chun-Hua (Department of Dermatology, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation) ;
  • Wu, Chang-Chieh (Department of Surgery, Tri-Service General Hospital, National Defense Medical Center) ;
  • Chen, Mao-Liang (Department of Research, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation) ;
  • Lee, Ming-Cheng (Department of Research, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation) ;
  • Wang, Lu-Kai (Radiation Biology Core Laboratory, Institute for Radiological Research, Chang Gung University/Chang Gung Memorial Hospital) ;
  • Jiang, Shun-Yuan (Department of Research, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation) ;
  • Tsai, Fu-Ming (Department of Research, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation)
  • 투고 : 2016.06.28
  • 심사 : 2016.11.18
  • 발행 : 2016.12.31

초록

Tazarotene-induced gene 1 (TIG1) is a retinoic acid-inducible protein that is considered a putative tumor suppressor. The expression of TIG1 is decreased in malignant prostate carcinoma or poorly differentiated colorectal adenocarcinoma, but TIG1 is present in benign or well-differentiated tumors. Ectopic TIG1 expression led to suppression of growth in cancer cells. However, the function of TIG1 in cell differentiation is still unknown. Using a yeast two-hybrid system, we found that transmembrane protein 192 (TMEM192) interacted with TIG1. We also found that both TIG1A and TIG1B isoforms interacted and co-localized with TMEM192 in HtTA cervical cancer cells. The expression of TIG1 induced the expression of autophagy-related proteins, including Beclin-1 and LC-3B. The silencing of TMEM192 reduced the TIG1-mediated upregulation of autophagic activity. Furthermore, silencing of either TIG1 or TMEM192 led to alleviation of the upregulation of autophagy induced by all-trans retinoic acid. Our results demonstrate that the expression of TIG1 leads to cell autophagy through TMEM192. Our study also suggests that TIG1 and TMEM192 play an important role in the all-trans retinoic acid-mediated upregulation of autophagic activity.

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참고문헌

  1. Aagaard, A., Listwan, P., Cowieson, N., Huber, T., Ravasi, T., Wells, C.A., Flanagan, J.U., Kellie, S., Hume, D.A., Kobe, B., et al. (2005). An inflammatory role for the mammalian carboxypeptidase inhibitor latexin: relationship to cystatins and the tumor suppressor TIG1. Structure 13, 309-317. https://doi.org/10.1016/j.str.2004.12.013
  2. Aita, V.M., Liang, X.H., Murty, V.V., Pincus, D.L., Yu, W., Cayanis, E., Kalachikov, S., Gilliam, T.C., and Levine, B. (1999). Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59, 59-65. https://doi.org/10.1006/geno.1999.5851
  3. Anguiano, J., Garner, T.P., Mahalingam, M., Das, B.C., Gavathiotis, E., and Cuervo, A.M. (2013). Chemical modulation of chaperonemediated autophagy by retinoic acid derivatives. Nat. Chem. Biol. 9, 374-382. https://doi.org/10.1038/nchembio.1230
  4. Bernard, M., Dieude, M., Yang, B., Hamelin, K., Underwood, K., and Hebert, M.J. (2014). Autophagy fosters myofibroblast differentiation through MTORC2 activation and downstream upregulation of CTGF. Autophagy 10, 2193-2207. https://doi.org/10.4161/15548627.2014.981786
  5. Chen, X.H., Wu, W.G., and Ding, J. (2014). Aberrant TIG1 methylation associated with its decreased expression and clinicopathological significance in hepatocellular carcinoma. Tumour Biol. 35, 967-971. https://doi.org/10.1007/s13277-013-1129-9
  6. Choi. A.M., Ryter, S.W., and Levine, B. (2013). Autophagy in human health and disease. N. Engl. J. Med. 368, 651-662. https://doi.org/10.1056/NEJMra1205406
  7. Dooley, H.C., Razi, M., Polson, H.E., Girardin, S.E., Wilson, M.I., and Tooze, S.A. (2014). WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol. Cell 55, 238-252. https://doi.org/10.1016/j.molcel.2014.05.021
  8. Guo, J.Y., Chen, H.Y., Mathew, R., Fan, J., Strohecker, A.M., Karsli-Uzunbas, G., Kamphorst. J.J., Chen, G., Lemons, J.M., Karantza, V., et al. (2011). Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev. 25, 460-470. https://doi.org/10.1101/gad.2016311
  9. Hanada. T., Noda, N.N., Satomi, Y., Ichimura, Y., Fujioka, Y., Takao, T., Inagaki, F., and Ohsumi, Y. (2007). The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282, 37298-37302. https://doi.org/10.1074/jbc.C700195200
  10. Hara, T., Takamura, A., Kishi, C., Iemura, S., Natsume, T., Guan, J.L., and Mizushima, N. (2008). FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J. Cell Biol. 181, 497-510. https://doi.org/10.1083/jcb.200712064
  11. Jing, C., El-Ghany, M.A., Beesley, C., Foster, C.S., Rudland, P.S., Smith, P., and Ke, Y. (2002). Tazarotene-induced gene 1 (TIG1) expression in prostate carcinomas and its relationship to tumorigenicity. J. Natl. Cancer Inst. 94, 482-490. https://doi.org/10.1093/jnci/94.7.482
  12. Kadowaki, M., and Karim, M.R. (2009). Cytosolic LC3 ratio as a quantitative index of macroautophagy. Methods Enzymol. 452, 199-213. https://doi.org/10.1016/S0076-6879(08)03613-6
  13. Kang, R., Zeh, H.J., Lotze, M.T., and Tang, D. (2011). The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18, 571-580. https://doi.org/10.1038/cdd.2010.191
  14. Kobayashi, S. (2015). Choose delicately and reuse adequately: the newly revealed process of autophagy. Biol. Pharm. Bull. 38, 1098-1103. https://doi.org/10.1248/bpb.b15-00096
  15. Kwok, W.K., Pang, J.C., Lo, K.W., and Ng, H.K. (2009). Role of the RARRES1 gene in nasopharyngeal carcinoma. Cancer Genet. Cytogenet. 194, 58-64. https://doi.org/10.1016/j.cancergencyto.2009.06.005
  16. Kwong. J., Lo, K.W., Chow, L.S., Chan, F.L., To, K.F., and Huang, D.P. (2005). Silencing of the retinoid response gene TIG1 by promoter hypermethylation in nasopharyngeal carcinoma. Int. J. Cancer 113, 386-392. https://doi.org/10.1002/ijc.20593
  17. Lamb, C.A., Yoshimori, T., and Tooze, S.A. (2013). The autophagosome: origins unknown, biogenesis complex. Nat. Rev. Mol. Cell Biol. 14, 759-774. https://doi.org/10.1038/nrm3696
  18. Lee, I.H., Cao, L., Mostoslavsky, R., Lombard, D.B., Liu, J., Bruns, N.E., Tsokos, M., Alt, F.W., and Finkel, T. (2008). A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl. Acad. Sci. USA 105, 3374-3379. https://doi.org/10.1073/pnas.0712145105
  19. Lee, J., Giordano, S., and Zhang, J. (2012). Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem. J. 441, 523-540. https://doi.org/10.1042/BJ20111451
  20. Liang, X.H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999). Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676. https://doi.org/10.1038/45257
  21. Liang, Y., Jansen, M., Aronow, B., Geiger, H., and Van Zant, G. (2007). The quantitative trait gene latexin influences the size of the hematopoietic stem cell population in mice. Nat. Genet. 39, 178-188. https://doi.org/10.1038/ng1938
  22. Liu, Z., Lv, Y.J., Song, Y.P., Li, X.H., Du, Y.N., Wang, C.H., and Hu, L.K. (2012). Lysosomal membrane protein TMEM192 deficiency triggers crosstalk between autophagy and apoptosis in HepG2 hepatoma cells. Oncol. Rep. 28, 985-991. https://doi.org/10.3892/or.2012.1881
  23. Lock, R., Roy, S., Kenific, C.M., Su, J.S., Salas, E., Ronen, S.M., and Debnath, J. (2011). Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation. Mol. Biol. Cell. 22, 165-178. https://doi.org/10.1091/mbc.E10-06-0500
  24. Lock, R., Kenific, C.M., Leidal, A.M., Salas, E., and Debnath, J. (2014). Autophagy-dependent production of secreted factors facilitates oncogenic RAS-driven invasion. Cancer Discov. 4, 466-479. https://doi.org/10.1158/2159-8290.CD-13-0841
  25. Mizuiri, H., Yoshida, K., Toge, T., Oue, N., Aung, P.P., Noguchi, T., and Yasui, W. (2005). DNA methylation of genes linked to retinoid signaling in squamous cell carcinoma of the esophagus: DNA methylation of CRBP1 and TIG1 is associated with tumor stage. Cancer Sci. 96, 571-577. https://doi.org/10.1111/j.1349-7006.2005.00082.x
  26. Mizushima, N., and Komatsu, M. (2011). Autophagy: renovation of cells and tissues. Cell 147, 728-741. https://doi.org/10.1016/j.cell.2011.10.026
  27. Mizushima, N., Yoshimori, T., and Ohsumi, Y. (2011). The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132. https://doi.org/10.1146/annurev-cellbio-092910-154005
  28. Nagpal, S., Patel, S., Asano, A.T., Johnson, A.T., Duvic, M., and Chandraratna, R.A. (1996). Tazarotene-induced gene 1 (TIG1), a novel retinoic acid receptor-responsive gene in skin. J. Invest. Dermatol. 106, 269-274. https://doi.org/10.1111/1523-1747.ep12340668
  29. Orfali, N., O'Donovan, T.R., Nyhan, M.J., Britschgi, A., Tschan, M.P., Cahill, M.R., Mongan, N.P., Gudas, L.J., and McKenna, S.L. (2015). Induction of autophagy is a key component of alltrans-retinoic acid-induced differentiation in leukemia cells and a potential target for pharmacologic modulation. Exp. Hematol. 43, 781-793 e782. https://doi.org/10.1016/j.exphem.2015.04.012
  30. Peng, Z., Shen, R., Li, Y.W., Teng, K.Y., Shapiro, C.L., and Lin, H.J. (2012). Epigenetic repression of RARRES1 is mediated by methylation of a proximal promoter and a loss of CTCF binding. PloS One 7, e36891. https://doi.org/10.1371/journal.pone.0036891
  31. Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.L., Mizushima, N., Ohsumi, Y., et al. (2003). Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809-1820. https://doi.org/10.1172/JCI20039
  32. Rajawat, Y., Hilioti, Z., and Bossis, I. (2010). Autophagy: a target for retinoic acids. Autophagy 6,1224-1226. https://doi.org/10.4161/auto.6.8.13793
  33. Russell, R.C., Tian, Y., Yuan, H., Park, H.W., Chang, Y.Y., Kim, J., Kim, H., Neufeld, T.P., Dillin, A., and Guan, K.L. (2013). ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat. Cell Biol. 15, 741-750. https://doi.org/10.1038/ncb2757
  34. Schroder, B., Wrocklage, C., Hasilik, A., and Saftig, P. (2010). Molecular characterisation of 'transmembrane protein 192' (TMEM192), a novel protein of the lysosomal membrane. Biol. Chem. 391, 695-704.
  35. Shutoh, M., Oue, N., Aung, P.P., Noguchi, T., Kuraoka, K., Nakayama, H., Kawahara, K., and Yasui, W. (2005). DNA methylation of genes linked with retinoid signaling in gastric carcinoma: expression of the retinoid acid receptor beta, cellular retinol-binding protein 1, and tazarotene-induced gene 1 genes is associated with DNA methylation. Cancer 104, 1609-1619. https://doi.org/10.1002/cncr.21392
  36. Simon, H.U. (2012). Autophagy in myocardial differentiation and cardiac development. Circ. Res. 110, 524-525. https://doi.org/10.1161/CIRCRESAHA.112.265157
  37. Takamura, A., Komatsu, M., Hara, T., Sakamoto, A., Kishi, C., Waguri, S., Eishi, Y., Hino, O., Tanaka, K., and Mizushima, N. (2011). Autophagy-deficient mice develop multiple liver tumors. Genes Dev. 25, 795-800. https://doi.org/10.1101/gad.2016211
  38. Tsai, F.M., Wu, C.C., Shyu, R.Y., Wang, C.H., and Jiang, S.Y. (2011). Tazarotene-induced gene 1 inhibits prostaglandin E2-stimulated HCT116 colon cancer cell growth. J. Biomed. Sci. 18, 88. https://doi.org/10.1186/1423-0127-18-88
  39. Vessoni, A.T., Muotri, A.R., and Okamoto, O.K. (2012). Autophagy in stem cell maintenance and differentiation. Stem Cells Dev. 21, 513-520. https://doi.org/10.1089/scd.2011.0526
  40. Wang, Z., Cao, L., Kang, R., Yang, M., Liu, L., Zhao, Y., Yu, Y., Xie, M., Yin, X., Livesey, K.M., et al. (2011). Autophagy regulates myeloid cell differentiation by p62/SQSTM1-mediated degradation of PML-RARalpha oncoprotein. Autophagy 7, 401-411. https://doi.org/10.4161/auto.7.4.14397
  41. White, E. (2015). The role for autophagy in cancer. J. Clin. Invest. 125, 42-46. https://doi.org/10.1172/JCI73941
  42. Wu, C.C., Shyu, R.Y., Chou, J.M., Jao, S.W., Chao, P.C., Kang, J.C., Wu, S.T., Huang, S.L., and Jiang, S.Y. (2006). RARRES1 expression is significantly related to tumour differentiation and staging in colorectal adenocarcinoma. Eur. J. Cancer 42, 557-565. https://doi.org/10.1016/j.ejca.2005.11.015
  43. Wu, C.C., Tsai, F.M., Shyu, R.Y., Tsai, Y.M., Wang, C.H., and Jiang, S.Y. (2011). G protein-coupled receptor kinase 5 mediates Tazarotene-induced gene 1-induced growth suppression of human colon cancer cells. BMC Cancer 11, 175. https://doi.org/10.1186/1471-2407-11-175
  44. Yanatatsaneejit, P., Chalermchai, T., Kerekhanjanarong, V., Shotelersuk, K., Supiyaphun, P., Mutirangura, A., and Sriuranpong, V. (2008). Promoter hypermethylation of CCNA1, RARRES1, and HRASLS3 in nasopharyngeal carcinoma. Oral Oncol. 44, 400-406. https://doi.org/10.1016/j.oraloncology.2007.05.008
  45. Yang, S., Wang, X., Contino, G., Liesa, M., Sahin, E., Ying, H., Bause, A., Li, Y., Stommel, J.M., Dell'antonio, G., et al. (2011). Pancreatic cancers require autophagy for tumor growth. Genes Dev. 25, 717-729. https://doi.org/10.1101/gad.2016111
  46. Yue, Z., Jin, S., Yang, C., Levine, A.J., and Heintz, N. (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. USA 100, 15077-15082. https://doi.org/10.1073/pnas.2436255100
  47. Zhang, J., Liu, L., and Pfeifer, G.P. (2004). Methylation of the retinoid response gene TIG1 in prostate cancer correlates with methylation of the retinoic acid receptor beta gene. Oncogene 23, 2241-2249. https://doi.org/10.1038/sj.onc.1207328
  48. Zhuang, W., Li, B., Long, L., Chen, L., Huang, Q., and Liang, Z. (2011). Induction of autophagy promotes differentiation of gliomainitiating cells and their radiosensitivity. Int. J. Cancer 129, 2720-2731. https://doi.org/10.1002/ijc.25975

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