Activation of LTBP3 gene by a long noncoding RNA (IncRNA) MALAT1 transcript in mesenchymal stem cells from multiple myeloma

Journal of Biological Chemistry

Volumn 289, Issue 42, 2014, Pages 29365-29375

  Zhuang, Wenzhuo ^a   Li, Bingzong ^a   Chen, Ping ^a   Qu, Jing ^a   Shi, Lei ^a   Zhuang, Wenyue ^b   Fu, Jinxiang ^a   Li, Jun ^a   Zhang, Xiaohui ^a   Sun, Yu ^a  

^a SOOCHOW UNIVERSITY   (China)

^b BEIHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CELL CULTURE; CHEMICAL ACTIVATION; RNA; TRANSCRIPTION;

CELLULAR TRANSFORMATION; CHROMATIN IMMUNOPRECIPITATION; DIRECT INTERACTIONS; IMMUNOPRECIPITATIONS; MESENCHYMAL STEM CELL; ONCOGENIC PATHWAYS; TRANSCRIPTIONAL ACTIVATIONS; TUMOR SUPPRESSORS;

STEM CELLS;

LONG UNTRANSLATED RNA; TRANSCRIPTION FACTOR SP1; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; LTBP3 PROTEIN, HUMAN; MALAT1 LONG NON-CODING RNA, HUMAN; TUMOR MARKER;

ADULT; AGED; ARTICLE; BIOAVAILABILITY; CELL TRANSFORMATION; CHROMATIN IMMUNOPRECIPITATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LTBP3 GENE; LUCIFERASE ASSAY; MALAT1 GENE; MALE; MESENCHYMAL STEM CELL; MULTIPLE MYELOMA; RNA IMMUNOPRECIPITATION; RNA INTERFERENCE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; GENE EXPRESSION PROFILING; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; PROMOTER REGION; VERY ELDERLY;

AGED; AGED, 80 AND OVER; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LATENT TGF-BETA BINDING PROTEINS; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; MULTIPLE MYELOMA; PROMOTER REGIONS, GENETIC; RNA, LONG NONCODING; SP1 TRANSCRIPTION FACTOR; TUMOR MARKERS, BIOLOGICAL;

EID: 84908053091     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.572693     Document Type: Article

References (47)

1. Khaitan, D., Dinger, M. E., Mazar, J., Crawford, J., Smith, M. A., Mattick, J. S., and Perera, R. J. (2011) The melanoma-upregulated long noncoding RNA SPRY4-IT1 modulates apoptosis and invasion. Cancer Res. 71, 3852-3862
2. INK4B tumor suppressor gene. Oncogene 30, 1956-1962
3. Gupta, R. A., Shah, N., Wang, K. C., Kim, J., Horlings, H. M., Wong, D. J., Tsai, M. C., Hung, T., Argani, P., Rinn, J. L., Wang, Y., Brzoska, P., Kong, B., Li, R., West, R. B., van deVijver, M. J., Sukumar, S., and Chang, H. Y. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071-1076
4. Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M. C., Maeda, N., Oyama, R., Ravasi, T., Lenhard, B., Wells, C, Kodzius, R., Shimokawa, K., Bajic, V. B., Brenner, S. E., Batalov, S., Forrest, A. R., Zavolan, M., Davis, M. J., Wilming, L. G., Aidinis, V., Allen, J. E., Ambesi-Impiombato, A., Apweiler, R., Aturaliya, R. N., Bailey, T. L., Bansal, M., Baxter, L., Beisel, K. W., Bersano, T., Bono, H., Chalk, A. M., Chiu, K. P., Choudhary, V., Christoffels, A., Clutterbuck, D. R., Crowe, M. L., Dalla, E., Dalrymple, B. P., de Bono, B., Della Gatta, G., di Bernardo, D., Down, T., Engstrom, P., Fagiolini, M., Faulkner, G., Fletcher, C. F., Fukushima, T., Furuno, M., Futaki, S., Gariboldi, M., Georgii-Hemming, P., Gingeras, T. R., Gojobori, T., Green, R. E., Gustincich, S., Harbers, M., Hayashi, Y., Hensch, T. K., Hirokawa, N., Hill, D., Huminiecki, L., Iacono, M., Ikeo, K., Iwama, A., Ishikawa, T., Jakt, M., Kanapin, A., Katoh, M., Kawasawa, Y., Kelso, J., Kitamura, H., Kitano, H., Kollias, G., Krishnan, S. P., Kruger, A., Kummerfeld, S. K., Kurochkin, I. V., Lareau, L. F., Lazarevic, D., Lipovich, L., Liu, J., Liuni, S., McWilliam, S., Madan Babu, M., Madera, M., Marchionni, L., Matsuda, H., Matsuzawa, S., Miki, H., Mignone, F., Miyake, S., Morris, K., Mottagui-Tabar, S., Mulder, N., Nakano, N., Nakauchi, H., Ng, P., Nilsson, R., Nishiguchi, S., Nishikawa, S., Nori, F., Ohara, O., Okazaki, Y., Orlando, V., Pang, K. C, Pavan, W. J., Pavesi, G., Pesole, G., Petrovsky, N., Piazza, S., Reed, J., Reid, J. F., Ring, B. Z., Ringwald, M., Rost, B., Ruan, Y., Salzberg, S. L., Sandelin, A., Schneider, C, Schonbach, C, Sekiguchi, K., Semple, C. A., Seno, S., Sessa, L., Sheng, Y., Shibata, Y., Shimada, H., Shimada, K., Silva, D., Sinclair, B., Sperling, S., Stupka, E., Sugiura, K., Sultana, R., Takenaka, Y., Taki, K., Tammoja, K., Tan, S. L., Tang, S., Taylor, M. S., Tegner, J., Teichmann, S. A., Ueda, H. R., van Nimwegen, E., Verardo, R., Wei, C. L., Yagi, K., Yamanishi, H., Zabarovsky, E., Zhu, S., Zimmer, A., Hide, W., Bult, C, Grimmond, S. M., Teasdale, R. D., Liu, E. T., Brusic, V., Quackenbush, J., Wahlestedt, C, Mattick, J. S., Hume, D. A., Kai, C, Sasaki, D., Tomaru, Y., Fukuda, S., Kanamori-Katayama, M., Suzuki, M., Aoki, J., Arakawa, T., Iida, J., Imamura, K., Itoh, M., Kato, T., Kawaji, H., Kawagashira, N., Kawashima, T., Kojima, M., Kondo, S., Konno, H., Nakano, K., Ninomiya, N., Nishio, T., Okada, M., Plessy, C, Shibata, K., Shiraki, T., Suzuki, S., Tagami, M., Waki, K., Watahiki, A., Okamura-Oho, Y., Suzuki, H., Kawai, J., and Hayashizaki, Y. (2005) The transcriptional landscape of the mammalian genome. Science 309, 1559-1563
5. Huarte, M., Guttman, M., Feldser, D., Garber, M., Koziol, M. J., Kenzelmann-Broz, D., Khalil, A. M., Zuk, O., Amit, I., Rabani, M., Attardi, L. D., Regev, A., Lander, E. S., Jacks, T., and Rinn, J. L. (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409-419
6. Ji, P., Diederichs, S., Wang, W., Boing, S., Metzger, R., Schneider, P. M., Tidow, N., Brandt, B., Buerger, H., Bulk, E., Thomas, M., Berdel, W. E., Serve, H, and Müller-Tidow, C. (2003) MALAT-1, a novel noncoding RNA, and thymosin β4 predict metastasis and survival in early-stage nonsmall cell lung cancer. Oncogene 22, 8031-8041
7. Hutchinson, J. N, Ensminger, A. W., Clemson, C. M., Lynch, C. R., Lawrence, J. B., and Chess, A. (2007) A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics 8, 39
8. Bernard, D., Prasanth, K. V., Tripathi, V., Colasse, S., Nakamura, T., Xuan, Z., Zhang, M. Q., Sedel, F., Jourdren, L., Coulpier, F., Triller, A., Spector, D. L., and Bessis, A. (2010) A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J. 29, 3082-3093
9. Lin, R., Maeda, S., Liu, C, Karin, M., and Edgington, T. S. (2007) A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene 26, 851-858
10. Tano, K., Mizuno, R., Okada, T., Rakwal, R., Shibato, J., Masuo, Y., Ijiri, K., and Akimitsu, N. (2010) MALAT-1 enhances cell motility of lung adenocarcinoma cells by influencing the expression of motility-related genes. FEBSLett. 584, 4575-4580
11. Lin, R., Roychowdhury-Saha, M., Black, C, Watt, A. T., Marcusson, E. G., Freier, S. M., and Edgington, T. S. (2011) Control of RNA processing by a large non-coding RNA over-expressed in carcinomas. FEBS Lett. 585, 671-676
12. Schmidt, L. H, Spieker, T., Koschmieder, S., Schaffers, S., Humberg, J., Jungen, D., Bulk, E., Hascher, A., Wittmer, D., Marra, A., Hillejan, L., Wiebe, K., Berdel, W. E., Wiewrodt, R., and Muller-Tidow, C (2011) The long noncoding MALAT-1 RNA indicates a poor prognosis in non-small cell lung cancer and induces migration and tumor growth. J. Thorac. Oncol. 6, 1984-1992
13. Xu, C, Yang, M., Tian, J., Wang, X., and Li, Z. (2011) MALAT-1: a long non-coding RNA and its important 3' end functional motif in colorectal cancer metastasis. Int. J. Oncol 39, 169-175
14. Barille-Nion, S., and Bataille, R. (2003) New insights in myeloma-induced osteolysis. Leuk. Lymphoma 44, 1463-1467
15. Matsumoto, T., and Abe, M. (2011) TGF-β-related mechanisms of bone destruction in multiple myeloma. Bone 48, 129-134
16. Seyedin, S. M., Thomas, T. C, Thompson, A. Y., Rosen, D. M., and Piez, K. A. (1985) Purification and characterization of two cartilage-inducing factors from bovine demineralized bone. Proc. Natl. Acad. Sci. U. S. A. 82, 2267-2271
17. Miyazono, K., Olofsson, A., Colosetti, P., and Heldin, C. H. (1991) A role of the latent TGF-β1-binding protein in the assembly and secretion of TGF-β1. EMBOJ. 10, 1091-1101
18. Dabovic, B., Chen, Y., Colarossi, C, Obata, H, Zambuto, L., Perle, M. A., and Rifkin, D. B. (2002) Bone abnormalities in latent TGF-β binding protein (Ltbp)-3-null mice indicate a role for Ltbp-3 in modulating TGF-β bioavailability. J. Cell Biol. 156, 227-232
19. Dabovic, B., Chen, Y., Colarossi, C, Zambuto, L., Obata, H, and Rifkin, D. B. (2002) Bone defects in latent TGF-β binding protein (Ltbp)-3 null mice; a role for Ltbp in TGF-β presentation. J. Endocrinol. 175, 129-141
20. Lamond, A. I., and Spector, D. L. (2003) Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell. Biol. 4, 605-612
21. Calin, G. A., and Croce, C M. (2006) MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857-866
22. Yang, L., Lin, C, Liu, W., Zhang, J., Ohgi, K. A., Grinstein, J. D., Dorrestein, P. C, and Rosenfeld, M. G. (2011) ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 147, 773-788
23. Bumgarner, S. L., Neuert, G., Voight, B. F., Symbor-Nagrabska, A., Grisafi, P., van Oudenaarden, A., and Fink, G. R. (2012) Single-cell analysis reveals that noncoding RNAs contribute to clonal heterogeneity by modulating transcription factor recruitment. Mol. Cell 45, 470-482
24. Hongay, C. F., Grisafi, P. L., Galitski, T., and Fink, G. R. (2006) Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell 127, 735-745
25. Martens, J. A., Laprade, L., and Winston, F. (2004) Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature 429, 571-574
26. Petruk, S., Sedkov, Y., Riley, K. M., Hodgson, J., Schweisguth, F., Hirose, S., Jaynes, J. B., Brock, H. W., and Mazo, A. (2006) Transcription of noncoding bxd RNAs promoted by the Trithorax TAC1 complex represses Ubx by a transcriptional interference mechanism. Cell 127, 1209-1221
27. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R., and Young, R. A. (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88
28. Martianov, I., Ramadass, A., Serra Barros, A., Chow, N., and Akoulitchev, A. (2007) Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445, 666-670
29. Li, B., Fu, J., Chen, P., and Zhuang, W. (2010) Impairment in immunomodulatory function of mesenchymal stem cells from multiple myeloma patients. Arch. Med. Res. 41, 623-633
30. + mesenchymal stem cells in patients with multiple myeloma. Stem Cells Dev. 16, 921-930
31. Yuan, J. H., Yang, F., Wang, F., Ma, J. Z., Guo, Y. J., Tao, Q. F., Liu, F., Pan, W., Wang, T. T., Zhou, C. C, Wang, S. B., Wang, Y. Z., Yang, Y., Yang, N., Zhou, W. P., Yang, G. S., and Sun, S. H. (2014) A long noncoding RNA activated by TGF-β promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer Cell 25, 666-681
32. Kantola, A. K., Keski-Oja, J., and Koli, K. (2005) Induction of human LTBP-3 promoter activity by TGF-β1 is mediated by Smad3/4 and AP-1 binding elements. Gene 363, 142-150
33. Feng, J., Bi, C, Clark, B. S., Mady, R., Shah, P., and Kohtz, J. D. (2006) The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev. 20, 1470-1484
34. Cassiday, L. A., and Maher, L. J., 3rd. (2002) Having it both ways: transcription factors that bind DNA and RNA. Nucleic Acids Res. 30, 4118-4126
35. Eddy, S. R. (2001) Non-coding RNA genes and the modern RNA world. Nat. Rev. Genet 2, 919-929
36. Ponting, C. P., Oliver, P. L., and Reik, W. (2009) Evolution and functions of long noncoding RNAs. Cell 136, 629-641
37. Kapranov, P., Willingham, A. T., and Gingeras, T. R. (2007) Genome-wide transcription and the implications for genomic organization. Nat. Rev. Genet. 8, 413-423
38. Bernstein, E., and Allis, C. D. (2005) RNA meets chromatin. Genes Dev. 19, 1635-1655
39. Bertone, P., Stolc, V., Royce, T. E., Rozowsky, J. S., Urban, A. E., Zhu, X., Rinn, J. L., Tongprasit, W., Samanta, M., Weissman, S., Gerstein, M., and Snyder, M. (2004) Global identification of human transcribed sequences with genome tiling arrays. Science 306, 2242-2246
40. Rinn, J. L., Kertesz, M., Wang, J. K., Squazzo, S. L., Xu, X., Brugmann, S. A., Goodnough, L. H., Helms, J. A., Farnham, P. J., Segal, E., and Chang, H. Y. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323
41. 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
42. Lanz, R. B., McKenna, N. J., Onate, S. A., Albrecht, U., Wong, J., Tsai, S. Y., Tsai, M. J., and O'Malley, B. W. (1999) A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97, 17-27
43. O'Neill, M. J. (2005) The influence of non-coding RNAs on allele-specific gene expression in mammals. Hum. Mol. Genet. 14, Spec. No. 1, R113-R120
44. Zhang, B., Arun, G., Mao, Y. S., Lazar, Z., Hung, G., Bhattacharjee, G., Xiao, X., Booth, C. J., Wu, J., Zhang, C., and Spector, D. L. (2012) The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2, 111-123
45. Dubnau, J., and Struhl, G. (1996) RNA recognition and translational regulation by a homeodomain protein. Nature 379, 694-699
46. Rosenfeld, M. G., Lunyak, V. V., and Glass, C. K. (2006) Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signaldependent programs of transcriptional response. Genes Dev. 20, 1405-1428
47. McKenna, N. J., and O'Malley, B. W. (2002) Combinatorial controlof gene expression by nuclear receptors and coregulators. Cell 108, 465-474