Advertisement

Stem Cell Reviews and Reports

, Volume 15, Issue 2, pp 314–323 | Cite as

The Ambivalent Role of lncRNA Xist in Carcinogenesis

  • Yung-Kang Chen
  • Yun YenEmail author
Article

Abstract

Long non-coding RNA (lncRNA) Xist has emerged as a key modulator in dosage compensation by randomly inactivating one of the X chromosomes in mammals during embryonic development. Dysregulation of X chromosome inactivation (XCI) due to deletion of Xist has been proven to induce hematologic cancer in mice. However, this phenomenon is not consistent in humans as growing evidence suggests Xist can suppress or promote cancer growth in different organs of the human body. In this review, we discuss recent advances of XCI in human embryonic stem cells and provide an explanation for the seemingly contradictory roles of Xist in development of human cancer.

Keywords

Cancer stem cell Long non-coding RNA X Chromosome inactivation XIST non-coding RNA XACT non-coding RNA MicroRNAs Competing endogenous RNA Exosomes 

Notes

Acknowledgments

This study was supported by grants from the Ministry of Science and Technology (MOST 107-2321-B-038-002); “TMU Research Center of Cancer Translational Medicine” from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan; and the Center of Excellence for Cancer Research, Taipei Medical University, Taipei, Taiwan (MOHW107-TDU-B-212-114020; MOHW107-TDU-B-212-114014; MOHW107-TDU-B-212-114026B). We thank Dr. Frank Lu for his invaluable advice and English proofreading.

Compliance with Ethical Standards

Conflict of Interest

The authors report no conflict of interest.

References

  1. 1.
    Graves, J. A. (2006). Sex chromosome specialization and degeneration in mammals. Cell, 124(5), 901–914.CrossRefPubMedGoogle Scholar
  2. 2.
    Heard, E. (2006). Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes & Development, 20(14), 1848–1867.CrossRefGoogle Scholar
  3. 3.
    Crews, D. (2003). Sex determination: Where environment and genetics meet. Evolution & Development, 5, 50–55.CrossRefGoogle Scholar
  4. 4.
    Payer, B., & Lee, J. T. (2008). X chromosome dosage compensation: How mammals keep the balance. Annual Review of Genetics, 42, 733–772.CrossRefPubMedGoogle Scholar
  5. 5.
    Lyon, M. F. (1961). Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature, 190, 372–373.CrossRefPubMedGoogle Scholar
  6. 6.
    Wutz, A., Rasmussen, T. P., & Jaenisch, R. (2002). Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nature Genetics, 30, 167–174.CrossRefPubMedGoogle Scholar
  7. 7.
    Lee, J. T., & Bartolomei, M. S. (2013). X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell, 152, 1308–1323.CrossRefPubMedGoogle Scholar
  8. 8.
    Sakaguchi, T., Hasegawa, Y., Brockdorff, N., Tsutsui, K., Tsutsui, K. M., Sado, T., & Nakagawa, S. (2016). Control of chromosomal localization of Xist by hnRNP U family molecules. Developmental Cell, 39, 11–12.CrossRefPubMedGoogle Scholar
  9. 9.
    Chen, C. K., Blanco, M., Jackson, C., Aznauryan, E., Ollikainen, N., Surka, C., Chow, A., Cerase, A., McDonel, P., & Guttman, M. (2016). Xist recruits the X chromosome to the nuclear lamina to enable chromosome-wide silencing. Science, 354, 468–472.CrossRefPubMedGoogle Scholar
  10. 10.
    Chu, C., Zhang, Q. C., da Rocha, S. T., Flynn, R. A., Bharadwaj, M., Calabrese, J. M., Magnuson, T., Heard, E., & Chang, H. Y. (2015). Systematic discovery of Xist RNA binding proteins. Cell, 161, 404–416.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    McHugh, C. A., Chen, C. K., Chow, A., et al. (2015). The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature, 521, 232–236.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    da Rocha, S. T., & Heard, E. (2017). Novel players in X inactivation: Insights into Xist-mediated gene silencing and chromosome conformation. Nature Structural & Molecular Biology, 24, 197–204.CrossRefGoogle Scholar
  13. 13.
    Patil, D. P., Chen, C. K., Pickering, B. F., Chow, A., Jackson, C., Guttman, M., & Jaffrey, S. R. (2016). m(6)A RNA methylation promotes XIST-mediated transcriptional repression. Nature, 537, 369–373.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Mira-Bontenbal, H., & Gribnau, J. (2016). New Xist-interacting proteins in X-chromosome inactivation. Current Biology, 26, R338–R342.CrossRefPubMedGoogle Scholar
  15. 15.
    Keniry, A., & Blewitt, M. E. (2018). Studying X chromosome inactivation in the single-cell genomic era. Biochemical Society Transactions, 46, 577–586.CrossRefPubMedGoogle Scholar
  16. 16.
    Patrat, C., Okamoto, I., Diabangouaya, P., Vialon, V., le Baccon, P., Chow, J., & Heard, E. (2009). Dynamic changes in paternal X-chromosome activity during imprinted X-chromosome inactivation in mice. Proceedings of the National Academy of Sciences of the United States of America, 106, 5198–5203.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Takagi, N., & Sasaki, M. (1975). Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature, 256, 640–642.CrossRefPubMedGoogle Scholar
  18. 18.
    Sahakyan, A., Yang, Y., & Plath, K. (2018). The role of Xist in X-chromosome dosage compensation. Trends in Cell Biology, 28, 999–1013.CrossRefPubMedGoogle Scholar
  19. 19.
    Okamoto, I., Otte, A. P., Allis, C. D., Reinberg, D., & Heard, E. (2004). Epigenetic dynamics of imprinted X inactivation during early mouse development. Science, 303, 644–649.CrossRefPubMedGoogle Scholar
  20. 20.
    Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N. L., Meisig, J., Sedat, J., Gribnau, J., Barillot, E., Blüthgen, N., Dekker, J., & Heard, E. (2012). Spatial partitioning of the regulatory landscape of the X-inactivation Centre. Nature, 485, 381–385.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Robert Finestra, T., & Gribnau, J. (2017). X chromosome inactivation: Silencing, topology and reactivation. Current Opinion in Cell Biology, 46, 54–61.CrossRefPubMedGoogle Scholar
  22. 22.
    Navarro, P., Chambers, I., Karwacki-Neisius, V., Chureau, C., Morey, C., Rougeulle, C., & Avner, P. (2008). Molecular coupling of Xist regulation and pluripotency. Science, 321, 1693–1695.CrossRefPubMedGoogle Scholar
  23. 23.
    Donohoe, M. E., Silva, S. S., Pinter, S. F., Xu, N., & Lee, J. T. (2009). The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature, 460, 128–132.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Navarro, P., Oldfield, A., Legoupi, J., Festuccia, N., Dubois, A., Attia, M., Schoorlemmer, J., Rougeulle, C., Chambers, I., & Avner, P. (2010). Molecular coupling of Tsix regulation and pluripotency. Nature, 468, 457–460.CrossRefPubMedGoogle Scholar
  25. 25.
    Maduro, C., de Hoon, B., & Gribnau, J. (2016). Fitting the puzzle pieces: The bigger picture of XCI. Trends in Biochemical Sciences, 41, 138–147.CrossRefPubMedGoogle Scholar
  26. 26.
    Sahakyan A, Yang Y, Plath K. The Role of Xist in X-Chromosome Dosage Compensation. Trends Cell Biol 2018.Google Scholar
  27. 27.
    van den Berg, I. M., Laven, J. S., Stevens, M., et al. (2009). X chromosome inactivation is initiated in human preimplantation embryos. American Journal of Human Genetics, 84, 771–779.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Okamoto, I., Patrat, C., Thepot, D., et al. (2011). Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature, 472, 370–374.CrossRefPubMedGoogle Scholar
  29. 29.
    Saiba, R., Arava, M., & Gayen, S. (2018). Dosage compensation in human pre-implantation embryos: X-chromosome inactivation or dampening? EMBO Reports, 19, e46294.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Vallot, C., Patrat, C., Collier, A. J., Huret, C., Casanova, M., Liyakat Ali, T. M., Tosolini, M., Frydman, N., Heard, E., Rugg-Gunn, P. J., & Rougeulle, C. (2017). XACT noncoding RNA competes with XIST in the control of X chromosome activity during human early development. Cell Stem Cell, 20, 102–111.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Moreira de Mello, J. C., Fernandes, G. R., Vibranovski, M. D., & Pereira, L. V. (2017). Early X chromosome inactivation during human preimplantation development revealed by single-cell RNA-sequencing. Scientific Reports, 7, 10794.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Sahakyan, A., Kim, R., Chronis, C., Sabri, S., Bonora, G., Theunissen, T. W., Kuoy, E., Langerman, J., Clark, A. T., Jaenisch, R., & Plath, K. (2017). Human naive pluripotent stem cells model X chromosome dampening and X inactivation. Cell Stem Cell, 20, 87–101.CrossRefPubMedGoogle Scholar
  33. 33.
    Migeon, B. R., Lee, C. H., Chowdhury, A. K., & Carpenter, H. (2002). Species differences in TSIX/Tsix reveal the roles of these genes in X-chromosome inactivation. American Journal of Human Genetics, 71, 286–293.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Vallot, C., Huret, C., Lesecque, Y., Resch, A., Oudrhiri, N., Bennaceur-Griscelli, A., Duret, L., & Rougeulle, C. (2013). XACT, a long noncoding transcript coating the active X chromosome in human pluripotent cells. Nature Genetics, 45, 239–241.CrossRefPubMedGoogle Scholar
  35. 35.
    Deng, X., Berletch, J. B., Nguyen, D. K., & Disteche, C. M. (2014). X chromosome regulation: Diverse patterns in development, tissues and disease. Nature Reviews. Genetics, 15, 367–378.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Vallot, C., Ouimette, J. F., Makhlouf, M., Féraud, O., Pontis, J., Côme, J., Martinat, C., Bennaceur-Griscelli, A., Lalande, M., & Rougeulle, C. (2015). Erosion of X chromosome inactivation in human pluripotent cells initiates with XACT coating and depends on a specific heterochromatin landscape. Cell Stem Cell, 16, 533–546.CrossRefPubMedGoogle Scholar
  37. 37.
    Mekhoubad, S., Bock, C., de Boer, A. S., Kiskinis, E., Meissner, A., & Eggan, K. (2012). Erosion of dosage compensation impacts human iPSC disease modeling. Cell Stem Cell, 10, 595–609.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Patel, S., Bonora, G., Sahakyan, A., Kim, R., Chronis, C., Langerman, J., Fitz-Gibbon, S., Rubbi, L., Skelton, R. J. P., Ardehali, R., Pellegrini, M., Lowry, W. E., Clark, A. T., & Plath, K. (2017). Human embryonic stem cells do not change their X inactivation status during differentiation. Cell Reports, 18, 54–67.CrossRefPubMedGoogle Scholar
  39. 39.
    Bruck, T., Yanuka, O., & Benvenisty, N. (2013). Human pluripotent stem cells with distinct X inactivation status show molecular and cellular differences controlled by the X-linked ELK-1 gene. Cell Reports, 4, 262–270.CrossRefPubMedGoogle Scholar
  40. 40.
    Sahakyan, A., Plath, K., & Rougeulle, C. (2017). Regulation of X-chromosome dosage compensation in human: Mechanisms and model systems. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 372.Google Scholar
  41. 41.
    Pageau, G. J., Hall, L. L., Ganesan, S., Livingston, D. M., & Lawrence, J. B. (2007). The disappearing Barr body in breast and ovarian cancers. Nature Reviews. Cancer, 7, 628–633.CrossRefPubMedGoogle Scholar
  42. 42.
    Rosen, P. P., Savino, A., Menendez-Botet, C., Urban, J. A., Mike, V., Schwartz, M. K., & Melamed, M. R. (1977). Barr body distribution and estrogen receptor protein in mammary carcinoma. Annals of Clinical and Laboratory Science, 7, 491–499.PubMedGoogle Scholar
  43. 43.
    Jazaeri, A. A., Yee, C. J., Sotiriou, C., Brantley, K. R., Boyd, J., & Liu, E. T. (2002). Gene expression profiles of BRCA1-linked, BRCA2-linked, and sporadic ovarian cancers. Journal of the National Cancer Institute, 94, 990–1000.CrossRefPubMedGoogle Scholar
  44. 44.
    Jazaeri, A. A., Chandramouli, G. V., Aprelikova, O., et al. (2004). BRCA1-mediated repression of select X chromosome genes. Journal of Translational Medicine, 2, 32.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Ganesan, S., Silver, D. P., Greenberg, R. A., Avni, D., Drapkin, R., Miron, A., Mok, S. C., Randrianarison, V., Brodie, S., Salstrom, J., Rasmussen, T. P., Klimke, A., Marrese, C., Marahrens, Y., Deng, C. X., Feunteun, J., & Livingston, D. M. (2002). BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell, 111, 393–405.CrossRefPubMedGoogle Scholar
  46. 46.
    Xiao, C., Sharp, J. A., Kawahara, M., Davalos, A. R., Difilippantonio, M. J., Hu, Y., Li, W., Cao, L., Buetow, K., Ried, T., Chadwick, B. P., Deng, C. X., & Panning, B. (2007). The XIST noncoding RNA functions independently of BRCA1 in X inactivation. Cell, 128, 977–989.CrossRefPubMedGoogle Scholar
  47. 47.
    Chaligne, R., Popova, T., Mendoza-Parra, M. A., et al. (2015). The inactive X chromosome is epigenetically unstable and transcriptionally labile in breast cancer. Genome Research, 25, 488–503.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Jager, N., Schlesner, M., Jones, D. T., et al. (2013). Hypermutation of the inactive X chromosome is a frequent event in cancer. Cell, 155, 567–581.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Yildirim, E., Kirby, J. E., Brown, D. E., Mercier, F. E., Sadreyev, R. I., Scadden, D. T., & Lee, J. T. (2013). Xist RNA is a potent suppressor of hematologic cancer in mice. Cell, 152, 727–742.CrossRefPubMedGoogle Scholar
  50. 50.
    Zhang, R., & Xia, T. (2017). Long non-coding RNA XIST regulates PDCD4 expression by interacting with miR-21-5p and inhibits osteosarcoma cell growth and metastasis. International Journal of Oncology, 51, 1460–1470.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Du, Y., Weng, X. D., Wang, L., et al. (2017). LncRNA XIST acts as a tumor suppressor in prostate cancer through sponging miR-23a to modulate RKIP expression. Oncotarget, 8, 94358–94370.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Chang, S., Chen, B., Wang, X., Wu, K., & Sun, Y. (2017). Long non-coding RNA XIST regulates PTEN expression by sponging miR-181a and promotes hepatocellular carcinoma progression. BMC Cancer, 17, 248.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kobayashi, R., Miyagawa, R., Yamashita, H., Morikawa, T., Okuma, K., Fukayama, M., Ohtomo, K., & Nakagawa, K. (2016). Increased expression of long non-coding RNA XIST predicts favorable prognosis of cervical squamous cell carcinoma subsequent to definitive chemoradiation therapy. Oncology Letters, 12, 3066–3074.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Huang, Y. S., Chang, C. C., Lee, S. S., Jou, Y. S., & Shih, H. M. (2016). Xist reduction in breast cancer upregulates AKT phosphorylation via HDAC3-mediated repression of PHLPP1 expression. Oncotarget, 7, 43256–43266.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Zheng, R., Lin, S., Guan, L., Yuan, H., Liu, K., Liu, C., Ye, W., Liao, Y., Jia, J., & Zhang, R. (2018). Long non-coding RNA XIST inhibited breast cancer cell growth, migration, and invasion via miR-155/CDX1 axis. Biochemical and Biophysical Research Communications, 498, 1002–1008.CrossRefPubMedGoogle Scholar
  56. 56.
    Chen, D. L., Ju, H. Q., Lu, Y. X., Chen, L. Z., Zeng, Z. L., Zhang, D. S., Luo, H. Y., Wang, F., Qiu, M. Z., Wang, D. S., Xu, D. Z., Zhou, Z. W., Pelicano, H., Huang, P., Xie, D., Wang, F. H., Li, Y. H., & Xu, R. H. (2016). Long non-coding RNA XIST regulates gastric cancer progression by acting as a molecular sponge of miR-101 to modulate EZH2 expression. Journal of Experimental & Clinical Cancer Research, 35, 142.CrossRefGoogle Scholar
  57. 57.
    Ma, L., Zhou, Y., Luo, X., Gao, H., Deng, X., & Jiang, Y. (2017). Long non-coding RNA XIST promotes cell growth and invasion through regulating miR-497/MACC1 axis in gastric cancer. Oncotarget, 8, 4125–4135.PubMedGoogle Scholar
  58. 58.
    Xu, Y., Wang, J., & Wang, J. (2018). Long noncoding RNA XIST promotes proliferation and invasion by targeting miR-141 in papillary thyroid carcinoma. Onco Targets Ther, 11, 5035–5043.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Sun, N., Zhang, G., & Liu, Y. (2018). Long non-coding RNA XIST sponges miR-34a to promotes colon cancer progression via Wnt/beta-catenin signaling pathway. Gene, 665, 141–148.CrossRefPubMedGoogle Scholar
  60. 60.
    Zhu, J., Zhang, R., Yang, D., Li, J., Yan, X., Jin, K., Li, W., Liu, X., Zhao, J., Shang, W., & Yu, T. (2018). Knockdown of long non-coding RNA XIST inhibited doxorubicin resistance in colorectal Cancer by upregulation of miR-124 and downregulation of SGK1. Cellular Physiology and Biochemistry, 51, 113–128.CrossRefPubMedGoogle Scholar
  61. 61.
    Li, C., Wan, L., Liu, Z., Xu, G., Wang, S., Su, Z., Zhang, Y., Zhang, C., Liu, X., Lei, Z., & Zhang, H. T. (2018). Long non-coding RNA XIST promotes TGF-beta-induced epithelial-mesenchymal transition by regulating miR-367/141-ZEB2 axis in non-small-cell lung cancer. Cancer Letters, 418, 185–195.CrossRefPubMedGoogle Scholar
  62. 62.
    Xu, R., Zhu, X., Chen, F., Huang, C., Ai, K., Wu, H., Zhang, L., & Zhao, X. (2018). LncRNA XIST/miR-200c regulates the stemness properties and tumourigenicity of human bladder cancer stem cell-like cells. Cancer Cell International, 18, 41.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Sun, Z., Zhang, B., & Cui, T. (2018). Long non-coding RNA XIST exerts oncogenic functions in pancreatic cancer via miR-34a-5p. Oncology Reports, 39, 1591–1600.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Kong, Q., Zhang, S., Liang, C., Zhang, Y., Kong, Q., Chen, S., Qin, J., & Jin, Y. (2018). LncRNA XIST functions as a molecular sponge of miR-194-5p to regulate MAPK1 expression in hepatocellular carcinoma cell. Journal of Cellular Biochemistry, 119, 4458–4468.CrossRefPubMedGoogle Scholar
  65. 65.
    Cheng, Q., Xu, X., Jiang, H., Xu, L., & Li, Q. (2018). Knockdown of long non-coding RNA XIST suppresses nasopharyngeal carcinoma progression by activating miR-491-5p. Journal of Cellular Biochemistry, 119, 3936–3944.CrossRefPubMedGoogle Scholar
  66. 66.
    Cheng, Z., Li, Z., Ma, K., Li, X., Tian, N., Duan, J., Xiao, X., & Wang, Y. (2017). Long non-coding RNA XIST promotes glioma Tumorigenicity and angiogenesis by acting as a molecular sponge of miR-429. Journal of Cancer, 8, 4106–4116.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Tukiainen, T., Villani, A. C., Yen, A., Rivas, M. A., Marshall, J. L., Satija, R., Aguirre, M., Gauthier, L., Fleharty, M., Kirby, A., Cummings, B. B., Castel, S. E., Karczewski, K. J., Aguet, F., Byrnes, A., Aguet, F., Ardlie, K. G., Cummings, B. B., Gelfand, E. T., Getz, G., Hadley, K., Handsaker, R. E., Huang, K. H., Kashin, S., Karczewski, K. J., Lek, M., Li, X., MacArthur, D. G., Nedzel, J. L., Nguyen, D. T., Noble, M. S., Segrè, A. V., Trowbridge, C. A., Tukiainen, T., Abell, N. S., Balliu, B., Barshir, R., Basha, O., Battle, A., Bogu, G. K., Brown, A., Brown, C. D., Castel, S. E., Chen, L. S., Chiang, C., Conrad, D. F., Cox, N. J., Damani, F. N., Davis, J. R., Delaneau, O., Dermitzakis, E. T., Engelhardt, B. E., Eskin, E., Ferreira, P. G., Frésard, L., Gamazon, E. R., Garrido-Martín, D., Gewirtz, A. D. H., Gliner, G., Gloudemans, M. J., Guigo, R., Hall, I. M., Han, B., He, Y., Hormozdiari, F., Howald, C., Kyung Im, H., Jo, B., Yong Kang, E., Kim, Y., Kim-Hellmuth, S., Lappalainen, T., Li, G., Li, X., Liu, B., Mangul, S., McCarthy, M. I., McDowell, I. C., Mohammadi, P., Monlong, J., Montgomery, S. B., Muñoz-Aguirre, M., Ndungu, A. W., Nicolae, D. L., Nobel, A. B., Oliva, M., Ongen, H., Palowitch, J. J., Panousis, N., Papasaikas, P., Park, Y. S., Parsana, P., Payne, A. J., Peterson, C. B., Quan, J., Reverter, F., Sabatti, C., Saha, A., Sammeth, M., Scott, A. J., Shabalin, A. A., Sodaei, R., Stephens, M., Stranger, B. E., Strober, B. J., Sul, J. H., Tsang, E. K., Urbut, S., van de Bunt, M., Wang, G., Wen, X., Wright, F. A., Xi, H. S., Yeger-Lotem, E., Zappala, Z., Zaugg, J. B., Zhou, Y. H., Akey, J. M., Bates, D., Chan, J., Chen, L. S., Claussnitzer, M., Demanelis, K., Diegel, M., Doherty, J. A., Feinberg, A. P., Fernando, M. S., Halow, J., Hansen, K. D., Haugen, E., Hickey, P. F., Hou, L., Jasmine, F., Jian, R., Jiang, L., Johnson, A., Kaul, R., Kellis, M., Kibriya, M. G., Lee, K., Li, J. B., Li, Q., Li, X., Lin, J., Lin, S., Linder, S., Linke, C., Liu, Y., Maurano, M. T., Molinie, B., Montgomery, S. B., Nelson, J., Neri, F. J., Oliva, M., Park, Y., Pierce, B. L., Rinaldi, N. J., Rizzardi, L. F., Sandstrom, R., Skol, A., Smith, K. S., Snyder, M. P., Stamatoyannopoulos, J., Stranger, B. E., Tang, H., Tsang, E. K., Wang, L., Wang, M., van Wittenberghe, N., Wu, F., Zhang, R., Nierras, C. R., Branton, P. A., Carithers, L. J., Guan, P., Moore, H. M., Rao, A., Vaught, J. B., Gould, S. E., Lockart, N. C., Martin, C., Struewing, J. P., Volpi, S., Addington, A. M., Koester, S. E., Little, A. R., Brigham, L. E., Hasz, R., Hunter, M., Johns, C., Johnson, M., Kopen, G., Leinweber, W. F., Lonsdale, J. T., McDonald, A., Mestichelli, B., Myer, K., Roe, B., Salvatore, M., Shad, S., Thomas, J. A., Walters, G., Washington, M., Wheeler, J., Bridge, J., Foster, B. A., Gillard, B. M., Karasik, E., Kumar, R., Miklos, M., Moser, M. T., Jewell, S. D., Montroy, R. G., Rohrer, D. C., Valley, D. R., Davis, D. A., Mash, D. C., Undale, A. H., Smith, A. M., Tabor, D. E., Roche, N. V., McLean, J. A., Vatanian, N., Robinson, K. L., Sobin, L., Barcus, M. E., Valentino, K. M., Qi, L., Hunter, S., Hariharan, P., Singh, S., Um, K. S., Matose, T., Tomaszewski, M. M., Barker, L. K., Mosavel, M., Siminoff, L. A., Traino, H. M., Flicek, P., Juettemann, T., Ruffier, M., Sheppard, D., Taylor, K., Trevanion, S. J., Zerbino, D. R., Craft, B., Goldman, M., Haeussler, M., Kent, W. J., Lee, C. M., Paten, B., Rosenbloom, K. R., Vivian, J., Zhu, J., Lappalainen, T., Regev, A., Ardlie, K. G., Hacohen, N., & MacArthur, D. G. (2017). Landscape of X chromosome inactivation across human tissues. Nature, 550, 244–248.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Anguera, M. C., Sadreyev, R., Zhang, Z., Szanto, A., Payer, B., Sheridan, S. D., Kwok, S., Haggarty, S. J., Sur, M., Alvarez, J., Gimelbrant, A., Mitalipova, M., Kirby, J. E., & Lee, J. T. (2012). Molecular signatures of human induced pluripotent stem cells highlight sex differences and cancer genes. Cell Stem Cell, 11, 75–90.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Sousa, E. J., Stuart, H. T., Bates, L. E., Ghorbani, M., Nichols, J., Dietmann, S., & Silva, J. C. R. (2018). Exit from naive pluripotency induces a transient X chromosome inactivation-like state in males. Cell Stem Cell, 22, 919–928 e6.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Fidler, I. J. (2003). The pathogenesis of cancer metastasis: The 'seed and soil' hypothesis revisited. Nature Reviews. Cancer, 3, 453–458.CrossRefPubMedGoogle Scholar
  71. 71.
    Kaplan, R. N., Rafii, S., & Lyden, D. (2006). Preparing the "soil": The premetastatic niche. Cancer Research, 66, 11089–11093.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Mu, W., Rana, S., & Zoller, M. (2013). Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia, 15, 875–887.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Le, M. T., Hamar, P., Guo, C., et al. (2014). miR-200-containing extracellular vesicles promote breast cancer cell metastasis. The Journal of Clinical Investigation, 124, 5109–5128.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Hoshino, A., Costa-Silva, B., Shen, T. L., Rodrigues, G., Hashimoto, A., Tesic Mark, M., Molina, H., Kohsaka, S., di Giannatale, A., Ceder, S., Singh, S., Williams, C., Soplop, N., Uryu, K., Pharmer, L., King, T., Bojmar, L., Davies, A. E., Ararso, Y., Zhang, T., Zhang, H., Hernandez, J., Weiss, J. M., Dumont-Cole, V. D., Kramer, K., Wexler, L. H., Narendran, A., Schwartz, G. K., Healey, J. H., Sandstrom, P., Jørgen Labori, K., Kure, E. H., Grandgenett, P. M., Hollingsworth, M. A., de Sousa, M., Kaur, S., Jain, M., Mallya, K., Batra, S. K., Jarnagin, W. R., Brady, M. S., Fodstad, O., Muller, V., Pantel, K., Minn, A. J., Bissell, M. J., Garcia, B. A., Kang, Y., Rajasekhar, V. K., Ghajar, C. M., Matei, I., Peinado, H., Bromberg, J., & Lyden, D. (2015). Tumour exosome integrins determine organotropic metastasis. Nature, 527, 329–335.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Minks, J., Robinson, W. P., & Brown, C. J. (2008). A skewed view of X chromosome inactivation. The Journal of Clinical Investigation, 118, 20–23.CrossRefPubMedGoogle Scholar
  76. 76.
    Germain, D. P. (2010). Fabry disease. Orphanet Journal of Rare Diseases, 5, 30.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Plenge, R. M., Hendrich, B. D., Schwartz, C., Arena, J. F., Naumova, A., Sapienza, C., Winter, R. M., & Willard, H. F. (1997). A promoter mutation in the XIST gene in two unrelated families with skewed X-chromosome inactivation. Nature Genetics, 17, 353–356.CrossRefPubMedGoogle Scholar
  78. 78.
    Nesterova, T. B., Johnston, C. M., Appanah, R., Newall, A. E., Godwin, J., Alexiou, M., & Brockdorff, N. (2003). Skewing X chromosome choice by modulating sense transcription across the Xist locus. Genes & Development, 17, 2177–2190.CrossRefGoogle Scholar
  79. 79.
    Garzon, R., Liu, S., Fabbri, M., Liu, Z., Heaphy, C. E. A., Callegari, E., Schwind, S., Pang, J., Yu, J., Muthusamy, N., Havelange, V., Volinia, S., Blum, W., Rush, L. J., Perrotti, D., Andreeff, M., Bloomfield, C. D., Byrd, J. C., Chan, K., Wu, L. C., Croce, C. M., & Marcucci, G. (2009). MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood, 113, 6411–6418.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Alexander, R. P., Fang, G., Rozowsky, J., Snyder, M., & Gerstein, M. B. (2010). Annotating non-coding regions of the genome. Nature Reviews. Genetics, 11, 559–571.CrossRefPubMedGoogle Scholar
  81. 81.
    Anastasiadou, E., Jacob, L. S., & Slack, F. J. (2018). Non-coding RNA networks in cancer. Nature Reviews. Cancer, 18, 5–18.CrossRefPubMedGoogle Scholar
  82. 82.
    Tay, Y., Rinn, J., & Pandolfi, P. P. (2014). The multilayered complexity of ceRNA crosstalk and competition. Nature, 505, 344–352.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Hu, S., Chang, J., Li, Y., et al. (2018). Long non-coding RNA XIST as a potential prognostic biomarker in human cancers: A meta-analysis. Oncotarget, 9, 13911–13919.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of MedicineTaipei Medical UniversityTaipeiTaiwan
  2. 2.Department of General MedicineTaipei Veterans General HospitalTaipeiTaiwan
  3. 3.Graduate Institute of Medical InformaticsTaipei Medical UniversityTaipeiTaiwan
  4. 4.TMU Research Center of Cancer Translational MedicineTaipei Medical UniversityTaipei CityTaiwan
  5. 5.Taipei Municipal Wanfang HospitalTaipei Medical UniversityTaipeiTaiwan
  6. 6.Program for Cancer Molecular Biology and Drug Discovery, College of Medical Science and TechnologyTaipei Medical UniversityTaipeiTaiwan

Personalised recommendations