Browse > Article
http://dx.doi.org/10.14348/molcells.2018.2347

Tazarotene-Induced Gene 1 Interacts with DNAJC8 and Regulates Glycolysis in Cervical Cancer Cells  

Wang, Chun-Hua (Department of Dermatology, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation)
Shyu, Rong-Yaun (Department of Internal Medicine, Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation)
Wu, Chang-Chieh (Department of Surgery, Tri-Service General Hospital Keelung Branch, 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)
Lin, Yi-Yin (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)
Publication Information
Molecules and Cells / v.41, no.6, 2018 , pp. 562-574 More about this Journal
Abstract
The tazarotene-induced gene 1 (TIG1) protein is a retinoidinducible growth regulator and is considered a tumor suppressor. Here, we show that DnaJ heat shock protein family member C8 (DNAJC8) is a TIG1 target that regulates glycolysis. Ectopic DNAJC8 expression induced the translocation of pyruvate kinase M2 (PKM2) into the nucleus, subsequently inducing glucose transporter 1 (GLUT1) expression to promote glucose uptake. Silencing either DNAJC8 or PKM2 alleviated the upregulation of GLUT1 expression and glucose uptake induced by ectopic DNAJC8 expression. TIG1 interacted with DNAJC8 in the cytosol, and this interaction completely blocked DNAJC8-mediated PKM2 translocation and inhibited glucose uptake. Furthermore, increased glycose uptake was observed in cells in which TIG1 was silenced. In conclusion, TIG1 acts as a pivotal repressor of DNAJC8 to enhance glucose uptake by partially regulating PKM2 translocation.
Keywords
DNAJC8; glucose transporter; glycolysis; HSP40; pyruvate kinase M2; tazarotene-induced gene 1;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Edwards, K.M., and Munger, K. (2004). Depletion of physiological levels of the human TID1 protein renders cancer cell lines resistant to apoptosis mediated by multiple exogenous stimuli. Oncogene 23, 8419-8431.   DOI
2 Guo, F., Sigua, C., Bali, P., George, P., Fiskus, W., Scuto, A., Annavarapu, S., Mouttaki, A., Sondarva, G., Wei, S., et al. (2005). Mechanistic role of heat shock protein 70 in Bcr-Abl-mediated resistance to apoptosis in human acute leukemia cells. Blood 105, 1246-1255.
3 Hamelin, C., Cornut, E., Poirier, F., Pons, S., Beaulieu, C., Charrier, J.P., Haidous, H., Cotte, E., Lambert, C., Piard, F., et al. (2011). Identification and verification of heat shock protein 60 as a potential serum marker for colorectal cancer. FEBS J. 278, 4845-4859.   DOI
4 Hamrita, B., Chahed, K., Kabbage, M., Guillier, C.L., Trimeche, M., Chaieb, A., and Chouchane, L. (2008). Identification of tumor antigens that elicit a humoral immune response in breast cancer patients' sera by serological proteome analysis (SERPA). Clin. Chim. Acta 393, 95-102.   DOI
5 Huang, L., Yu, Z., Zhang, T., Zhao, X., and Huang, G. (2014). HSP40 interacts with pyruvate kinase M2 and regulates glycolysis and cell proliferation in tumor cells. PLoS One 9, e92949.   DOI
6 Hwang, Y.J., Lee, S.P., Kim, S.Y., Choi, Y.H., Kim, M.J., Lee, C.H., Lee, J.Y., and Kim, D.Y. (2009). Expression of heat shock protein 60 kDa is upregulated in cervical cancer. Yonsei Med. J. 50, 399-406.   DOI
7 Ito, N., Kamiguchi, K., Nakanishi, K., Sokolovskya, A., Hirohashi, Y., Tamura, Y., Murai, A., Yamamoto, E., Kanaseki, T., Tsukahara, T., et al. (2016). A novel nuclear DnaJ protein, DNAJC8, can suppress the formation of spinocerebellar ataxia 3 polyglutamine aggregation in a J-domain independent manner. Biochem. Biophys. Res. Commun. 474, 626-633.   DOI
8 Wang, X., Saso, H., Iwamoto, T., Xia, W., Gong, Y., Pusztai, L., Woodward, W.A., Reuben, J.M., Warner, S.L., Bearss, D.J., et al. (2013). TIG1 promotes the development and progression of inflammatory breast cancer through activation of Axl kinase. Cancer Res. 73, 6516-6525.   DOI
9 Warburg, O., Wind, F., and Negelein, E. (1927). The metabolism of tumors in the body. J Gen. Physiol. 8, 519-530.   DOI
10 Whitley, D., Goldberg, S.P., and Jordan, W.D. (1999). Heat shock proteins: a review of the molecular chaperones. J. Vasc. Surg. 29, 748-751.   DOI
11 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.   DOI
12 Yang, W., and Lu, Z. (2013). Regulation and function of pyruvate kinase M2 in cancer. Cancer Lett. 339, 153-158.   DOI
13 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.   DOI
14 Yan, Y., Li, Z., Xu, X., Chen, C., Wei, W., Fan, M., Chen, X., Li, J.J., Wang, Y., and Huang, J. (2016). All-trans retinoic acids induce differentiation and sensitize a radioresistant breast cancer cells to chemotherapy. BMC Complement Altern. Med. 16, 113.   DOI
15 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.   DOI
16 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.   DOI
17 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.   DOI
18 Kim, S.W., Chao, T.H., Xiang, R., Lo, J.F., Campbell, M.J., Fearns, C., and Lee, J.D. (2004). Tid1, the human homologue of a Drosophila tumor suppressor, reduces the malignant activity of ErbB-2 in carcinoma cells. Cancer Res. 64, 7732-7739.   DOI
19 Kim, S.W., Hayashi, M., Lo, J.F., Fearns, C., Xiang, R., Lazennec, G., Yang, Y., and Lee, J.D. (2005). Tid1 negatively regulates the migratory potential of cancer cells by inhibiting the production of interleukin-8. Cancer Res. 65, 8784-8791.   DOI
20 Lee, Y.M., Lee, J.O., Jung, J.H., Kim, J.H., Park, S.H., Park, J.M., Kim, E.K., Suh, P.G., and Kim, H.S. (2008). Retinoic acid leads to cytoskeletal rearrangement through AMPK-Rac1 and stimulates glucose uptake through AMPK-p38 MAPK in skeletal muscle cells. J. Biol. Chem. 283, 33969-33974.   DOI
21 Li, C., Zhang, G., Zhao, L., Ma, Z., and Chen, H. (2016). Metabolic reprogramming in cancer cells: glycolysis, glutaminolysis, and Bcl-2 proteins as novel therapeutic targets for cancer. World J. Surg. Oncol. 14, 15.
22 Miyake, H., Muramaki, M., Kurahashi, T., Yamanaka, K., Hara, I., and Fujisawa, M. (2006). Enhanced expression of heat shock protein 27 following neoadjuvant hormonal therapy is associated with poor clinical outcome in patients undergoing radical prostatectomy for prostate cancer. Anticancer Res. 26, 1583-1587.
23 Yang, W., Zheng, Y., Xia, Y., Ji, H., Chen, X., Guo, F., Lyssiotis, C.A., Aldape, K., Cantley, L.C., and Lu, Z. (2012). ERK1/2-dependent phosphorylation and nuclear translocation of PKM2 promotes the Warburg effect. Nat. Cell Biol. 14, 1295-1304.   DOI
24 Yoshidomi, K., Murakami, A., Yakabe, K., Sueoka, K., Nawata, S., and Sugino, N. (2014). Heat shock protein 70 is involved in malignant behaviors and chemosensitivities to cisplatin in cervical squamous cell carcinoma cells. J. Obstet. Gynaecol. Res. 40, 1188-1196.   DOI
25 Yu, M., Yongzhi, H., Chen, S., Luo, X., Lin, Y., Zhou, Y., Jin, H., Hou, B., Deng, Y., Tu, L., et al. (2017). The prognostic value of GLUT1 in cancers: a systematic review and meta-analysis. Oncotarget 8, 43356-43367.
26 Maehara, Y., Oki, E., Abe, T., Tokunaga, E., Shibahara, K., Kakeji, Y., and Sugimachi, K. (2000). Overexpression of the heat shock protein HSP70 family and p53 protein and prognosis for patients with gastric cancer. Oncology 58, 144-151.   DOI
27 Medina, R.A., and Owen, G.I. (2002). Glucose transporters: expression, regulation and cancer. Biol Res. 35, 9-26.
28 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.   DOI
29 Assimakopoulou, M. (2000). Human meningiomas: immunohistochemical localization of progesterone receptor and heat shock protein 27 and absence of estrogen receptor and PS2. Cancer Detect. Prev. 24, 163-168.
30 Banerjee, S., Lin, C.F., Skinner, K.A., Schiffhauer, L.M., Peacock, J., Hicks, D.G., Redmond, E.M., Morrow, D., Huston, A., Shayne, M., et al. (2011). Heat shock protein 27 differentiates tolerogenic macrophages that may support human breast cancer progression. Cancer Res. 71, 318-327.   DOI
31 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.   DOI
32 Mueckler, M., and Thorens, B. (2013). The SLC2 (GLUT) family of membrane transporters. Mol. Aspects Med. 34, 121-138.   DOI
33 Murphy, M.E. (2013). The HSP70 family and cancer. Carcinogenesis. 34, 1181-1188.   DOI
34 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.   DOI
35 Oka, M., Sato, S., Soda, H., Fukuda, M., Kawabata, S., Nakatomi, K., Shiozawa, K., Nakamura, Y., Ohtsuka, K., and Kohno, S. (2001). Autoantibody to heat shock protein Hsp40 in sera of lung cancer patients. Jpn. J. Cancer Res. 92, 316-320.   DOI
36 Carvalho, K.C., Cunha, I.W., Rocha, R.M., Ayala, F.R., Cajaiba, M.M., Begnami, M.D., Vilela, R.S., Paiva, G.R., Andrade, R.G., and Soares, F.A. (2011). GLUT1 expression in malignant tumors and its use as an immunodiagnostic marker. Clinics (Sao Paulo) 66, 965-972.   DOI
37 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.   DOI
38 Qiu, X.B., Shao, Y.M., Miao, S., and Wang, L. (2006). The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol. Life Sci. 63, 2560-2570.   DOI
39 Mitra, A., Shevde, L.A., and Samant, R.S. (2009). Multi-faceted role of HSP40 in cancer. Clin. Exp. Metastasis. 26, 559-567.   DOI
40 Bao, Y.P., Cook, L.J., O'Donovan, D., Uyama, E., and Rubinsztein, D.C. (2002). Mammalian, yeast, bacterial, and chemical chaperones reduce aggregate formation and death in a cell model of oculopharyngeal muscular dystrophy. J. Biol. Chem. 277, 12263-12269.   DOI
41 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.   DOI
42 Cheng, H., Cenciarelli, C., Nelkin, G., Tsan, R., Fan, D., Cheng-Mayer, C., and Fidler, I.J. (2005). Molecular mechanism of hTid-1, the human homolog of Drosophila tumor suppressor l(2)Tid, in the regulation of NF-kappaB activity and suppression of tumor growth. Mol. Cell Biol. 25, 44-59.   DOI
43 Ciocca, D.R., and Calderwood, S.K. (2005). Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones. 10, 86-103.   DOI
44 Clagett-Dame, M., and DeLuca, H.F. (2002). The role of vitamin A in mammalian reproduction and embryonic development. Annu. Rev. Nutr. 22, 347-381.   DOI
45 Degos, L., Dombret, H., Chomienne, C., Daniel, M.T., Miclea, J.M., Chastang, C., Castaigne, S., and Fenaux, P. (1995). All-trans-retinoic acid as a differentiating agent in the treatment of acute promyelocytic leukemia. Blood 85, 2643-2653.
46 Demand, J., Luders, J., and Hohfeld, J. (1998). The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Mol. Cell Biol. 18, 2023-2028.   DOI
47 Siddikuzzaman, Guruvayoorappan, C., and Berlin Grace, V.M. (2011). All trans retinoic acid and cancer. Immunopharmacol. Immunotoxicol. 33, 241-249.
48 Salani, B., Ravera, S., Amaro, A., Salis, A., Passalacqua, M., Millo, E., Damonte, G., Marini, C., Pfeffer, U., Sambuceti, G., et al. (2015). IGF1 regulates PKM2 function through Akt phosphorylation. Cell Cycle 14, 1559-1567.   DOI
49 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.   DOI
50 Shyu, R.Y., Wang, C.H., Wu, C.C., Chen, M.L., Lee, M.C., Wang, L.K., Jiang, S.Y., and Tsai, F.M. (2016). Tazarotene-induced gene 1 enhanced cervical cell autophagy through transmembrane protein 192. Mol. Cells 39, 877-887.   DOI
51 Sterrenberg, J.N., Blatch, G.L., and Edkins, A.L. (2011). Human DNAJ in cancer and stem cells. Cancer Lett. 312, 129-142.   DOI
52 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.   DOI
53 Syken, J., De-Medina, T., and Munger, K. (1999). TID1, a human homolog of the Drosophila tumor suppressor l(2)tid, encodes two mitochondrial modulators of apoptosis with opposing functions. Proc. Natl. Acad. Sci. USA 96, 8499-8504.   DOI
54 Takai, N., Kawamata, N., Walsh, C.S., Gery, S., Desmond, J.C., Whittaker, S., Said, J.W., Popoviciu, L.M., Jones, P.A., Miyakawa, I., et al. (2005). Discovery of epigenetically masked tumor suppressor genes in endometrial cancer. Mol. Cancer Res. 3, 261-269.   DOI