A Long Noncoding RNA Perturbs the Circadian Rhythm of Hepatoma Cells to Facilitate Hepatocarcinogenesis

Neoplasia (United States)

Volumn 17, Issue 1, 2015, Pages 79-88

  Cui, Ming ^a   Zheng, Minying ^a   Sun, Baodi ^a   Wang, Yue ^a   Ye, Lihong ^a   Zhang, Xiaodong ^a  

^a NANKAI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; TRANSCRIPTION FACTOR CLOCK; 3' UNTRANSLATED REGION; MESSENGER RNA;

5' UNTRANSLATED REGION; ANCHORAGE INDEPENDENT GROWTH; ARTICLE; BASE PAIRING; CARCINOGENESIS; CELL PROLIFERATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HEPATOMA CELL; HEPG2 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MTT ASSAY; OSCILLATOR; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; TRANSIENT TRANSFECTION; UPREGULATION; WESTERN BLOTTING; 3' UNTRANSLATED REGION; ANIMAL; CELL TRANSFORMATION; CHEMISTRY; DISEASE MODEL; EXPERIMENTAL LIVER NEOPLASM; GENETICS; LIVER TUMOR; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RNA INTERFERENCE; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CIRCADIAN RHYTHM; CLOCK PROTEINS; DISEASE MODELS, ANIMAL; HUMANS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MOLECULAR SEQUENCE DATA; RNA INTERFERENCE; RNA, LONG NONCODING; RNA, MESSENGER;

EID: 84964694333     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2014.11.004     Document Type: Article

References (45)

1. [1] Schmieder, R, Puehler, F, Neuhaus, R, Kissel, M, Adjei, AA, Miner, JN, Mumberg, D, Ziegelbauer, K, Scholz, A, Allosteric MEK1/2 inhibitor refametinib (BAY 86-9766) in combination with sorafenib exhibits antitumor activity in preclinical murine and rat models of hepatocellular carcinoma. Neoplasia 15 (2013), 1161–1171.
2. [2] Su, JC, Tseng, PH, Wu, SH, Hsu, CY, Tai, WT, Li, YS, Chen, IT, Liu, CY, Chen, KF, Shiau, CW, SC-2001 overcomes STAT3-mediated sorafenib resistance through RFX-1/SHP-1 activation in hepatocellular carcinoma. Neoplasia, 2014, 10.1016/j.neo.2014.06.005 [pii: S1476-5586(14)00079-7, Epub ahead of print].
3. [3] Sakurai, T, Kudo, M, Umemura, A, He, G, Elsharkawy, AM, Seki, E, Karin, M, p38alpha inhibits liver fibrogenesis and consequent hepatocarcinogenesis by curtailing accumulation of reactive oxygen species. Cancer Res 73 (2013), 215–224.
4. [4] Zhang, T, Zhang, J, Cui, M, Liu, F, You, X, Du, Y, Gao, Y, Zhang, S, Lu, Z, Ye, L, et al. Hepatitis B virus X protein inhibits tumor suppressor miR-205 through inducing hypermethylation of miR-205 promoter to enhance carcinogenesis. Neoplasia 15 (2013), 1282–1291.
5. [5] Lin, YM, Chang, JH, Yeh, KT, Yang, MY, Liu, TC, Lin, SF, Su, WW, Chang, JG, Disturbance of circadian gene expression in hepatocellular carcinoma. Mol Carcinog 47 (2008), 925–933.
6. [6] Chang, HC, Guarente, L, SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 153 (2013), 1448–1460.
7. [7] Wang, TA, Yu, YV, Govindaiah, G, Ye, X, Artinian, L, Coleman, TP, Sweedler, JV, Cox, CL, Gillette, MU, Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science 337 (2012), 839–842.
8. [8] Eckel-Mahan, KL, Patel, VR, de Mateo, S, Orozco-Solis, R, Ceglia, NJ, Sahar, S, Dilag-Penilla, SA, Dyar, KA, Baldi, P, Sassone-Corsi, P, Reprogramming of the circadian clock by nutritional challenge. Cell 155 (2013), 1464–1478.
9. [9] Marcheva, B, Ramsey, KM, Buhr, ED, Kobayashi, Y, Su, H, Ko, CH, Ivanova, G, Omura, C, Mo, S, Vitaterna, MH, et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466 (2010), 627–631.
10. [10] Koike, N, Yoo, SH, Huang, HC, Kumar, V, Lee, C, Kim, TK, Takahashi, JS, Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338 (2012), 349–354.
11. [11] Spengler, ML, Kuropatwinski, KK, Comas, M, Gasparian, AV, Fedtsova, N, Gleiberman, AS, Gitlin, II, Artemicheva, NM, Deluca, KA, Gudkov, AV, et al. Core circadian protein CLOCK is a positive regulator of NF-kappaB–mediated transcription. Proc Natl Acad Sci U S A 109 (2012), E2457–E2465.
12. [12] Turek, FW, Allada, R, Liver has rhythm. Hepatology 35 (2002), 743–745.
13. [13] Fustin, JM, Doi, M, Yamaguchi, Y, Hida, H, Nishimura, S, Yoshida, M, Isagawa, T, Morioka, MS, Kakeya, H, Manabe, I, et al. RNA-methylation–dependent RNA processing controls the speed of the circadian clock. Cell 155 (2013), 793–806.
14. [14] Djebali, S, Davis, CA, Merkel, A, Dobin, A, Lassmann, T, Mortazavi, A, Tanzer, A, Lagarde, J, Lin, W, Schlesinger, F, et al. Landscape of transcription in human cells. Nature 489 (2012), 101–108.
15. [15] Yuan, SX, Yang, F, Yang, Y, Tao, QF, Zhang, J, Huang, G, Yang, Y, Wang, RY, Yang, S, Huo, XS, et al. Long noncoding RNA associated with microvascular invasion in hepatocellular carcinoma promotes angiogenesis and serves as a predictor for hepatocellular carcinoma patients’ poor recurrence-free survival after hepatectomy. Hepatology 56 (2012), 2231–2241.
16. [16] Wang, KC, Chang, HY, Molecular mechanisms of long noncoding RNAs. Mol Cell 43 (2011), 904–914.
17. [17] Aguilo, F, Zhou, MM, Walsh, MJ, Long noncoding RNA, polycomb, and the ghosts haunting INK4b-ARF-INK4a expression. Cancer Res 71 (2011), 5365–5369.
18. [18] Wapinski, O, Chang, HY, Long noncoding RNAs and human disease. Trends Cell Biol 21 (2011), 354–361.
19. [19] Gutschner, T, Hammerle, M, Eissmann, M, Hsu, J, Kim, Y, Hung, G, Revenko, A, Arun, G, Stentrup, M, Gross, M, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res 73 (2013), 1180–1189.
20. [20] Geisler, S, Lojek, L, Khalil, AM, Baker, KE, Coller, J, Decapping of long noncoding RNAs regulates inducible genes. Mol Cell 45 (2012), 279–291.
21. [21] Zhang, S, Shan, C, Kong, G, Du, Y, Ye, L, Zhang, X, MicroRNA-520e suppresses growth of hepatoma cells by targeting the NF-kappaB–inducing kinase (NIK). Oncogene 31 (2012), 3607–3620.
22. [22] You, X, Liu, F, Zhang, T, Lv, N, Liu, Q, Shan, C, Du, Y, Kong, G, Wang, T, Ye, L, et al. Hepatitis B virus X protein upregulates Lin28A/Lin28B through Sp-1/c-Myc to enhance the proliferation of hepatoma cells. Oncogene 33 (2014), 449–460.
23. [23] Shan, C, Xu, F, Zhang, S, You, J, You, X, Qiu, L, Zheng, J, Ye, L, Zhang, X, Hepatitis B virus X protein promotes liver cell proliferation via a positive cascade loop involving arachidonic acid metabolism and p-ERK1/2. Cell Res 20 (2010), 563–575.
24. [24] Du, Y, Kong, G, You, X, Zhang, S, Zhang, T, Gao, Y, Ye, L, Zhang, X, Elevation of highly up-regulated in liver cancer (HULC) by hepatitis B virus X protein promotes hepatoma cell proliferation via down-regulating p18. J Biol Chem 287 (2012), 26302–26311.
25. [25] St John, PC, Hirota, T, Kay, SA, Doyle, FJ III, Spatiotemporal separation of PER and CRY posttranslational regulation in the mammalian circadian clock. Proc Natl Acad Sci U S A 111 (2014), 2040–2045.
26. [26] Padmanabhan, K, Robles, MS, Westerling, T, Weitz, CJ, Feedback regulation of transcriptional termination by the mammalian circadian clock PERIOD complex. Science 337 (2012), 599–602.
27. [27] Hatori, M, Hirota, T, Iitsuka, M, Kurabayashi, N, Haraguchi, S, Kokame, K, Sato, R, Nakai, A, Miyata, T, Tsutsui, K, et al. Light-dependent and circadian clock–regulated activation of sterol regulatory element-binding protein, X-box–binding protein 1, and heat shock factor pathways. Proc Natl Acad Sci U S A 108 (2011), 4864–4869.
28. [28] Yuan, JH, Yang, F, Wang, F, Ma, JZ, Guo, YJ, Tao, QF, Liu, F, Pan, W, Wang, TT, Zhou, CC, et al. A long noncoding RNA activated by TGF-beta promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer Cell 25:5 (2014), 666–681, 10.1016/j.ccr.2014.03.010 [Epub 2014 Apr 24].
29. [29] Bugaut, A, Balasubramanian, S, 5’-UTR RNA G-quadruplexes: translation regulation and targeting. Nucleic Acids Res 40 (2012), 4727–4741.
30. [30] Li, MD, Ruan, HB, Hughes, ME, Lee, JS, Singh, JP, Jones, SP, Nitabach, MN, Yang, X, O-GlcNAc signaling entrains the circadian clock by inhibiting BMAL1/CLOCK ubiquitination. Cell Metab 17 (2013), 303–310.
31. [31] Winter, SL, Bosnoyan-Collins, L, Pinnaduwage, D, Andrulis, IL, Expression of the circadian clock genes Per1 and Per2 in sporadic and familial breast tumors. Neoplasia 9 (2007), 797–800.
32. [32] Gibb, EA, Brown, CJ, Lam, WL, The functional role of long non-coding RNA in human carcinomas. Mol Cancer, 10, 2011, 38.
33. [33] Panzitt, K, Tschernatsch, MM, Guelly, C, Moustafa, T, Stradner, M, Strohmaier, HM, Buck, CR, Denk, H, Schroeder, R, Trauner, M, et al. Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA. Gastroenterology 132 (2007), 330–342.
34. [34] Hammerle, M, Gutschner, T, Uckelmann, H, Ozgur, S, Fiskin, E, Gross, M, Skawran, B, Geffers, R, Longerich, T, Breuhahn, K, et al. Posttranscriptional destabilization of the liver-specific long noncoding RNA HULC by the IGF2 mRNA-binding protein 1 (IGF2BP1). Hepatology 58 (2013), 1703–1712.
35. [35] Orom, UA, Derrien, T, Beringer, M, Gumireddy, K, Gardini, A, Bussotti, G, Lai, F, Zytnicki, M, Notredame, C, Huang, Q, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 143 (2010), 46–58.
36. [36] Mercer, TR, Dinger, ME, Mattick, JS, Long non-coding RNAs: insights into functions. Nat Rev Genet 10 (2009), 155–159.
37. [37] Chen, G, Wang, Z, Wang, D, Qiu, C, Liu, M, Chen, X, Zhang, Q, Yan, G, Cui, Q, LncRNADisease: a database for long-non-coding RNA-associated diseases. Nucleic Acids Res 41 (2013), D983–D986.
38. [38] Guttman, M, Rinn, JL, Modular regulatory principles of large non-coding RNAs. Nature 482 (2012), 339–346.
39. [39] Wilusz, JE, Sunwoo, H, Spector, DL, Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23 (2009), 1494–1504.
40. [40] Wang, J, Liu, X, Wu, H, Ni, P, Gu, Z, Qiao, Y, Chen, N, Sun, F, Fan, Q, CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res 38 (2010), 5366–5383.
41. [41] Hoffman, AE, Yi, CH, Zheng, T, Stevens, RG, Leaderer, D, Zhang, Y, Holford, TR, Hansen, J, Paulson, J, Zhu, Y, CLOCK in breast tumorigenesis: genetic, epigenetic, and transcriptional profiling analyses. Cancer Res 70 (2010), 1459–1468.
42. [42] Rudic, RD, McNamara, P, Curtis, AM, Boston, RC, Panda, S, Hogenesch, JB, Fitzgerald, GA, BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol, 2, 2004, e377.
43. [43] Turek, FW, Joshu, C, Kohsaka, A, Lin, E, Ivanova, G, McDearmon, E, Laposky, A, Losee-Olson, S, Easton, A, Jensen, DR, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308 (2005), 1043–1045.
44. [44] Ma, D, Li, S, Molusky, MM, Lin, JD, Circadian autophagy rhythm: a link between clock and metabolism?. Trends Endocrinol Metab 23 (2012), 319–325.
45. [45] Feng, D, Lazar, MA, Clocks, metabolism, and the epigenome. Mol Cell 47 (2012), 158–167.