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Involvement of lncRNA-HOTTIP in the Repair of Ultraviolet Light-Induced DNA Damage in Spermatogenic Cells

  • Liang, Meng (Department of Biotechnology, School of Life Science, Bengbu Medical College) ;
  • Hu, Ke (Department of Biotechnology, School of Life Science, Bengbu Medical College)
  • 투고 : 2019.06.08
  • 심사 : 2019.09.17
  • 발행 : 2019.11.30

초록

Ultraviolet light (UV)-induced cellular response has been studied by numerous investigators for many years. Long noncoding RNAs (lncRNAs) are emerging as new regulators of diverse cellular process; however, little is known about the role of lncRNAs in the cellular response to UV treatment. Here, we demonstrate that levels of lncRNA-HOTTIP significantly increases after UV stimulation and regulates the UV-mediated cellular response to UV through the coordinate activation of its neighboring gene Hoxa13 in GC-1 cells (spermatogonia germ cell line). UV-induced, G2/M-phase arrest and early apoptosis can be regulated by lncRNA-HOTTIP and Hoxa13. Furthermore, lncRNA-HOTTIP can up-regulate ${\gamma}-H_2AX$ and p53 expression via Hoxa13 in UV-irradiated GC-1 cells. In addition, p53 has the ability to regulate the expression of both lncRNA-HOTTIP and Hoxa13 in vitro and in vivo. Our results provide new data regarding the role lncRNAs play in the UV response in spermatogenic cells.

키워드

참고문헌

  1. Armstrong, B.K. and Kricker, A. (2001). The epidemiology of UV induced skin cancer. J. Photochem. Photobiol. B 63, 8-18. https://doi.org/10.1016/S1011-1344(01)00198-1
  2. Ascer, L.G., Magalhaes, Y.T., Espinha, G., Osaki, J.H., Souza, R.C., and Forti, F.L. (2015). CDC42 Gtpase activation affects hela cell DNA repair and proliferation following UV radiation-induced genotoxic stress. J. Cell Biochem. 116, 2086-2097. https://doi.org/10.1002/jcb.25166
  3. Bohacek, J. and Mansuy, I.M. (2015). Molecular insights into transgenerational non-genetic inheritance of acquired behaviours. Nat. Rev. Genet. 16, 641-652. https://doi.org/10.1038/nrg3964
  4. Brosnan, C.A. and Voinnet, O. (2009). The long and the short of noncoding RNAs. Curr. Opin. Cell Biol. 21, 416-425. https://doi.org/10.1016/j.ceb.2009.04.001
  5. Burgess, D.J. (2011). Non-coding RNA: HOTTIP goes the distance. Nat. Rev. Genet. 12, 300. https://doi.org/10.1038/nrg2992
  6. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611-622. https://doi.org/10.1373/clinchem.2008.112797
  7. Carmona, S., Lin, B., Chou, T., Arroyo, K., and Sun, S. (2018). LncRNA Jpx induces Xist expression in mice using both trans and cis mechanisms. PLoS Genet. 14, e1007378. https://doi.org/10.1371/journal.pgen.1007378
  8. Chen, L.L. and Carmichael, G.G. (2010). Decoding the function of nuclear long non-coding RNAs. Curr. Opin. Cell Biol. 22, 357-364. https://doi.org/10.1016/j.ceb.2010.03.003
  9. de Gruijl, F.R. (1999). Skin cancer and solar UV radiation. Eur. J. Cancer 35, 2003-2009. https://doi.org/10.1016/S0959-8049(99)00283-X
  10. de Gruijl, F.R., van Kranen, H.J., and Mullenders, L.H. (2001). UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J. Photochem. Photobiol. B 63, 19-27. https://doi.org/10.1016/S1011-1344(01)00199-3
  11. Degueurce, G., D'Errico, I., Pich, C., Ibberson, M., Schutz, F., Montagner, A., Sgandurra, M., Mury, L., Jafari, P., Boda, A., et al. (2016). Identification of a novel PPARbeta/delta/miR-21-3p axis in UV-induced skin inflammation. EMBO Mol. Med. 8, 919-936. https://doi.org/10.15252/emmm.201505384
  12. Farrell, A.W., Halliday, G.M., and Lyons, J.G. (2018). Brahma deficiency in keratinocytes promotes UV carcinogenesis by accelerating the escape from cell cycle arrest and the formation of DNA photolesions. J. Dermatol. Sci. 92, 254-263. https://doi.org/10.1016/j.jdermsci.2018.11.006
  13. Gentile, M., Latonen, L., and Laiho, M. (2003). Cell cycle arrest and apoptosis provoked by UV radiation-induced DNA damage are transcriptionally highly divergent responses. Nucleic Acids Res. 31, 4779-4790. https://doi.org/10.1093/nar/gkg675
  14. Jiang, Y.J. and Bikle, D.D. (2014). LncRNA profiling reveals new mechanism for VDR protection against skin cancer formation. J. Steroid Biochem. 144 Pt A, 87-90. https://doi.org/10.1016/j.jsbmb.2013.11.018
  15. Joo, M.S., Shin, S.B., Kim, E.J., Koo, J.H., Yim, H., and Kim, S.G. (2019). Nrf2-lncRNA controls cell fate by modulating p53-dependent Nrf2 activation as an miRNA sponge for Plk2 and p21(cip1). FASEB J. 33, 7953-7969. https://doi.org/10.1096/fj.201802744R
  16. Kaneko, Y.S., Ota, A., Nakashima, A., Nagasaki, H., Kodani, Y., Mori, K., and Nagatsu, T. (2015). Lipopolysaccharide treatment arrests the cell cycle of BV-2 microglial cells in G(1) phase and protects them from UV lightinduced apoptosis. J. Neural Transm. 122, 187-199. https://doi.org/10.1007/s00702-014-1256-5
  17. Kapranov, P., Cheng, J., Dike, S., Nix, D.A., Duttagupta, R., Willingham, A.T., Stadler, P.F., Hertel, J., Hackermuller, J., Hofacker, I.L., et al. (2007). RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316, 1484-1488. https://doi.org/10.1126/science.1138341
  18. Kim, D., Song, J., Han, J., Kim, Y., Chun, C.H., and Jin, E.J. (2013). Two noncoding RNAs, MicroRNA-101 and HOTTIP contribute cartilage integrity by epigenetic and homeotic regulation of integrin-alpha1. Cell Signal 25, 2878-2887. https://doi.org/10.1016/j.cellsig.2013.08.034
  19. Koberle, B., Roginskaya, V., Zima, K.S., Masters, J.R., and Wood, R.D. (2008). Elevation of XPA protein level in testis tumor cells without increasing resistance to cisplatin or UV radiation. Mol. Carcinogen. 47, 580-586. https://doi.org/10.1002/mc.20418
  20. Lei, T., Lv, Z.Y., Fu, J.F., Wang, Z., Fan, Z., and Wang, Y. (2018). LncRNA NBAT-1 is down-regulated in lung cancer and influences cell proliferation, apoptosis and cell cycle. Eur. Rev. Med. Pharmaco. 22, 1958-1962.
  21. Li, A., Wei, G., Wang, Y., Zhou, Y., Zhang, X.E., Bi, L., and Chen, R. (2012). Identification of intermediate-size non-coding RNAs involved in the UVinduced DNA damage response in C. elegans. PLoS One 7, e48066. https://doi.org/10.1371/journal.pone.0048066
  22. Li, L., Zhang, X., Hong, S.L., Chen, Y., and Ren, G.H. (2018a). Long noncoding HOTTIP regulates preeclampsia by inhibiting RND3. Eur. Rev. Med. Pharmaco. 22, 3277-3285.
  23. Li, M.A., Amaral, P.P., Cheung, P., Bergmann, J.H., Kinoshita, M., Kalkan, T., Ralser, M., Robson, S., von Meyenn, F., Paramor, M., et al. (2017). A lncRNA fine tunes the dynamics of a cell state transition involving Lin28, let-7 and de novo DNA methylation. eLife 18, e23468.
  24. Li, X., Wang, X., Mao, L., Zhao, S., and Wei, H. (2018b). LncRNA TP73AS1 predicts poor prognosis and promotes cell proliferation in ovarian cancer via cell cycle and apoptosis regulation. Mol. Med. Rep. 18, 516-522.
  25. Li, Z., Zhao, X., Zhou, Y., Liu, Y., Zhou, Q., Ye, H., Wang, Y., Zeng, J., Song, Y., Gao, W., et al. (2015). The long non-coding RNA HOTTIP promotes progression and gemcitabine resistance by regulating HOXA13 in pancreatic cancer. J. Transl. Med. 13, 84. https://doi.org/10.1186/s12967-015-0442-z
  26. Liang, M., Yao, G., Yin, M., Lu, M., Tian, H., Liu, L., Lian, J., Huang, X., and Sun, F. (2013). Transcriptional cooperation between p53 and NF-kappaB p65 regulates microRNA-224 transcription in mouse ovarian granulosa cells. Mol. Cell. Endocrinol. 370, 119-129. https://doi.org/10.1016/j.mce.2013.02.014
  27. Liu, X., Li, D., Zhang, W., Guo, M., and Zhan, Q. (2012). Long non-coding RNA gadd7 interacts with TDP-43 and regulates Cdk6 mRNA decay. EMBO J. 31, 4415-4427. https://doi.org/10.1038/emboj.2012.292
  28. Ma, X., Hu, Y.W., Zhao, Z.L., Zheng, L., Qiu, Y.R., Huang, J.L., Wu, X.J., Mao, X.R., Yang, J., Zhao, J.Y., et al. (2013). Anti-inflammatory effects of propofol are mediated by apolipoprotein M in a hepatocyte nuclear factor-1alphadependent manner. Arch. Biochem. Biophys. 533, 1-10. https://doi.org/10.1016/j.abb.2013.03.002
  29. Matsunuma, R., Niida, H., Ohhata, T., Kitagawa, K., Sakai, S., Uchida, C., Shiotani, B., Matsumoto, M., Nakayama, K.I., Ogura, H., et al. (2016). UV damage-induced phosphorylation of HBO1 triggers CRL4DDB2-mediated degradation to regulate cell proliferation. Mol. Cell. Biol. 36, 394-406. https://doi.org/10.1128/MCB.00809-15
  30. Mercer, T.R., Dinger, M.E., and Mattick, J.S. (2009). Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10, 155-159. https://doi.org/10.1038/nrg2521
  31. Militti, C., Maenner, S., Becker, P.B., and Gebauer, F. (2014). UNR facilitates the interaction of MLE with the lncRNA roX2 during Drosophila dosage compensation. Nat. Commun. 5, 4762. https://doi.org/10.1038/ncomms5762
  32. Morgan, E.A., Nguyen, S.B., Scott, V., and Stadler, H.S. (2003). Loss of Bmp7 and Fgf8 signaling in Hoxa13-mutant mice causes hypospadia. Development 130, 3095-3109. https://doi.org/10.1242/dev.00530
  33. Navarro, A., Moises, J., Santasusagna, S., Marrades, R.M., Vinolas, N., Castellano, J.J., Canals, J., Munoz, C., Ramirez, J., Molins, L., et al. (2019). Clinical significance of long non-coding RNA HOTTIP in early-stage nonsmall-cell lung cancer. BMC Pulm. Med. 19, 55. https://doi.org/10.1186/s12890-019-0816-8
  34. Park, K.S., Mitra, A., Rahat, B., Kim, K., and Pfeifer, K. (2017). Loss of imprinting mutations define both distinct and overlapping roles for misexpression of IGF2 and of H19 lncRNA. Nucleic Acids Res. 45, 12766-12779. https://doi.org/10.1093/nar/gkx896
  35. Prasanth, K.V., and Spector, D.L. (2007). Eukaryotic regulatory RNAs: an answer to the 'genome complexity' conundrum. Gene. Dev. 21, 11-42. https://doi.org/10.1101/gad.1484207
  36. Qu, L.P., Zhong, Y.M., Zheng, Z., and Zhao, R.X. (2017). CDH17 is a downstream effector of HOXA13 in modulating the Wnt/beta-catenin signaling pathway in gastric cancer. Eur. Rev. Med. Pharmaco. 21, 1234-1241.
  37. Quagliata, L., Matter, M., Piscuoglio, S., Makowska, Z., Heim, M., Tornillo, L., Cillo, C., and Terracciano, L. (2013). Hoxa13 and hottip expression levels predict patients' survival and metastasis formation in hepatocellular carcinoma. J. Hepatol. 58, S39-S40.
  38. Rinn, J.L. and Chang, H.Y. (2012). Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81, 145-166. https://doi.org/10.1146/annurev-biochem-051410-092902
  39. Shi, Q., Shen, L., Dong, B., Fu, H., Kang, X., Dai, L., Yang, Y., Yan, W., and Chen, K.N. (2018). Downregulation of HOXA13 sensitizes human esophageal squamous cell carcinoma to chemotherapy. Thorac. Cancer 9, 836-846. https://doi.org/10.1111/1759-7714.12758
  40. Siegenthaler, B., Defila, C., Muzumdar, S., Beer, H.D., Meyer, M., Tanner, S., Bloch, W., Blank, V., Schafer, M., and Werner, S. (2018). Nrf3 promotes UVinduced keratinocyte apoptosis through suppression of cell adhesion. Cell Death Differ. 25, 1749-1765. https://doi.org/10.1038/s41418-018-0074-y
  41. Su, Y., Lu, J., Chen, X., Liang, C., Luo, P., Qin, C., and Zhang, J. (2019). Long non-coding RNA HOTTIP affects renal cell carcinoma progression by regulating autophagy via the PI3K/Akt/Atg13 signaling pathway. J. Cancer Res. Clin. 145, 573-588. https://doi.org/10.1007/s00432-018-2808-0
  42. Sun, Y. and Liu, Y.X. (2018). LncRNA HOTTIP improves diabetic retinopathy by regulating the p38-MAPK pathway. Eur. Rev. Med. Pharmaco. 22, 2941-2948.
  43. Tan, Y.F., Tang, L., OuYang, W.X., Jiang, T., Zhang, H., and Li, S.J. (2019). beta-catenin-coordinated lncRNA MALAT1 up-regulation of ZEB-1 could enhance the telomerase activity in HGF-mediated differentiation of bone marrow mesenchymal stem cells into hepatocytes. Pathol. Res. Pract. 215, 546-554. https://doi.org/10.1016/j.prp.2019.01.002
  44. Tripathi, V., Shen, Z., Chakraborty, A., Giri, S., Freier, S.M., Wu, X., Zhang, Y., Gorospe, M., Prasanth, S.G., Lal, A., et al. (2013). Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB. PLoS Genet. 9, e1003368. https://doi.org/10.1371/journal.pgen.1003368
  45. van der Wees, C.G., Vreeswijk, M.P., Persoon, M., van der Laarse, A., van Zeeland, A.A., and Mullenders, L.H. (2003). Deficient global genome repair of UV-induced cyclobutane pyrimidine dimers in terminally differentiated myocytes and proliferating fibroblasts from the rat heart. DNA Repair 2, 1297-1308. https://doi.org/10.1016/j.dnarep.2003.06.001
  46. Voce, D.J., Bernal, G.M., Wu, L., Crawley, C.D., Zhang, W., Mansour, N.M., Cahill, K.E., Szymura, S.J., Uppal, A., Raleigh, D.R., et al. (2019). Temozolomide treatment induces lncRNA MALAT1 in an NF-kappaB and p53 codependent manner in glioblastoma. Cancer Res. 79, 2536-2548. https://doi.org/10.1158/0008-5472.CAN-18-2170
  47. Wang, K.C., Yang, Y.W., Liu, B., Sanyal, A., Corces-Zimmerman, R., Chen, Y., Lajoie, B.R., Protacio, A., Flynn, R.A., Gupta, R.A., et al. (2011). A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120-124. https://doi.org/10.1038/nature09819
  48. Wang, R., Ma, Z., Feng, L., Yang, Y., Tan, C., Shi, Q., Lian, M., He, S., Ma, H., and Fang, J. (2018a). LncRNA MIR31HG targets HIF1A and P21 to facilitate head and neck cancer cell proliferation and tumorigenesis by promoting cell-cycle progression. Mol. Cancer 17, 162. https://doi.org/10.1186/s12943-018-0916-8
  49. Wang, Y., Li, G., Zhao, L., and Lv, J. (2018b). Long noncoding RNA HOTTIP alleviates oxygen-glucose deprivation-induced neuronal injury via modulating miR-143/hexokinase 2 pathway. J. Cell Biochem. 119, 10107-10117. https://doi.org/10.1002/jcb.27348
  50. Williamson, L., Saponaro, M., Boeing, S., East, P., Mitter, R., Kantidakis, T., Kelly, G.P., Lobley, A., Walker, J., Spencer-Dene, B., et al. (2017). UV irradiation induces a non-coding RNA that functionally opposes the protein encoded by the same gene. Cell 168, 843-855.e13. https://doi.org/10.1016/j.cell.2017.01.019
  51. Xu, X., Tian, J., and Li, Q.Y. (2018). Downregulation of HOTTIP regulates insulin secretion and cell cycle in islet beta cells via inhibiting MEK/ERK pathway. Eur. Rev. Med. Pharmaco. 22, 4962-4968.
  52. Zeng, T., Wang, D., Chen, J., Tian, Y., Cai, X., Peng, H., Zhu, L., Huang, A., and Tang, H. (2017). LncRNA-AF113014 promotes the expression of Egr2 by interaction with miR-20a to inhibit proliferation of hepatocellular carcinoma cells. PLoS One 12, e0177843. https://doi.org/10.1371/journal.pone.0177843
  53. Zhang, L., Kang, W., Lu, X., Ma, S., Dong, L., and Zou, B. (2018). LncRNA CASC11 promoted gastric cancer cell proliferation, migration and invasion in vitro by regulating cell cycle pathway. Cell Cycle 17, 1886-1900. https://doi.org/10.1080/15384101.2018.1502574
  54. Zhao, Y., Liu, Y., Lin, L., Huang, Q., He, W., Zhang, S., Dong, S., Wen, Z., Rao, J., Liao, W., et al. (2018). The lncRNA MACC1-AS1 promotes gastric cancer cell metabolic plasticity via AMPK/Lin28 mediated mRNA stability of MACC1. Mol. Cancer 17, 69. https://doi.org/10.1186/s12943-018-0820-2
  55. Zhou, Y., Zhong, Y., Wang, Y., Zhang, X., Batista, D.L., Gejman, R., Ansell, P.J., Zhao, J., Weng, C., and Klibanski, A. (2007). Activation of p53 by MEG3 non-coding RNA. J. Biol. Chem. 282, 24731-24742. https://doi.org/10.1074/jbc.M702029200
  56. Zhuang, M.F., Li, L.J., and Ma, J.B. (2019). LncRNA HOTTIP promotes proliferation and cell cycle progression of acute myeloid leukemia cells. Eur. Rev. Med. Pharmaco. 23, 2908-2915.

피인용 문헌

  1. Roles of Noncoding RNA in Reproduction vol.12, 2021, https://doi.org/10.3389/fgene.2021.777510