Emerging role of long noncoding RNAs as regulators of innate immune cell development and inflammatory gene expression

European Journal of Immunology

Volumn 46, Issue 3, 2016, Pages 504-512

  Elling, Roland ^a   Chan, Jennie ^a   Fitzgerald, Katherine A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

(Long) noncoding RNA; Gene expression; Immune regulation; Inflammation; Innate immunity

Indexed keywords

LOCKED NUCLEIC ACID; LONG UNTRANSLATED RNA; MICRORNA; PATTERN RECOGNITION RECEPTOR; RIBONUCLEOPROTEIN; TRANSCRIPTION FACTOR; UNTRANSLATED RNA; MESSENGER RNA;

ARTICLE; CELL MATURATION; CHROMATIN; COMPLEX FORMATION; CYTOSOL; GENE DELETION; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; INTERACTIONS WITH DNA; INTERACTIONS WITH RNA; PRIORITY JOURNAL; RNA INTERFERENCE; CELL NUCLEUS; CRISPR CAS SYSTEM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM;

CELL NUCLEUS; CRISPR-CAS SYSTEMS; GENE DELETION; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INFLAMMATION; MICRORNAS; RECEPTORS, PATTERN RECOGNITION; RNA INTERFERENCE; RNA, LONG NONCODING; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 85000819273     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444558     Document Type: Article

References (58)

1. Janeway, C. A. Jr. and Medzhitov, R., Introduction: the role of innate immunity in the adaptive immune response. Semin. Immunol. 1998. 10: 349-350.
2. Medzhitov, R., Origin and physiological roles of inflammation. Nature 2008. 454: 428-435.
3. Smale, S. T., Tarakhovsky, A. and Natoli, G., Chromatin contributions to the regulation of innate immunity. Annu. Rev. Immunol. 2014. 32: 489-511.
4. Consortium, E. P., An integrated encyclopedia of DNA elements in the human genome. Nature 2012. 489: 57-74.
5. Dinger, M. E., Amaral, P. P., Mercer, T. R. and Mattick, J. S., Pervasive transcription of the eukaryotic genome: functional indices and conceptual implications. Brief Funct. Genomic. Proteomic. 2009. 8: 407-423.
6. Guttman, M., Amit, I., Garber, M., French, C., Lin, M. F., Feldser, D., Huarte, M. et al., Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009. 458: 223-227.
7. Li, K. and Ramchandran, R., Natural antisense transcript: a concomitant engagement with protein-coding transcript. Oncotarget 2010. 1: 447-452.
8. Mattick, J. S. and Rinn, J. L., Discovery and annotation of long noncoding RNAs. Nat. Struct. Mol. Biol. 2015. 22: 5-7.
9. Wu, X. and Sharp, P. A., Divergent transcription: a driving force for new gene origination? Cell 2013. 155: 990-996.
10. Berretta, J. and Morillon, A., Pervasive transcription constitutes a new level of eukaryotic genome regulation. EMBO Rep. 2009. 10: 973-982.
11. Khalil, A. M., Guttman, M., Huarte, M., Garber, M., Raj, A., Rivea Morales, D., Thomas, K. et al., Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA 2009. 106: 11667-11672.
12. Anderson, D. M., Anderson, K. M., Chang, C. L., Makarewich, C. A., Nelson, B. R., McAnally, J. R., Kasaragod, P. et al., A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 2015. 160: 595-606.
13. Ingolia, N. T., Brar, G. A., Stern-Ginossar, N., Harris, M. S., Talhouarne, G. J., Jackson, S. E., Wills, M. R. et al., Ribosome profiling reveals pervasive translation outside of annotated protein-coding genes. Cell Rep. 2014. 8: 1365-1379.
14. Rinn, J. L. and Chang, H. Y., Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 2012. 81: 145-166.
15. Ulitsky, I. and Bartel, D. P., lincRNAs: genomics, evolution, and mechanisms. Cell 2013. 154: 26-46.
16. Huarte, M., Guttman, M., Feldser, D., Garber, M., Koziol, M. J., Kenzelmann-Broz, D., Khalil, A. M. et al., A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010. 142: 409-419.
17. Dimitrova, N., Zamudio, J. R., Jong, R. M., Soukup, D., Resnick, R., Sarma, K., Ward, A. J. et al., LincRNA-p21 activates p21 in cis to promote Polycomb target gene expression and to enforce the G1/S checkpoint. Mol. Cell 2014. 54: 777-790.
18. Hasegawa, Y., Brockdorff, N., Kawano, S., Tsutui, K., Tsutui, K. and Nakagawa, S., The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell 2010. 19: 469-476.
19. Hacisuleyman, E., Goff, L. A., Trapnell, C., Williams, A., Henao-Mejia, J., Sun, L., McClanahan, P. et al., Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat. Struct. Mol. Biol. 2014. 21: 198-206.
20. Li, Z., Chao, T. C., Chang, K. Y., Lin, N., Patil, V. S., Shimizu, C., Head, S. R. et al., The long noncoding RNA THRIL regulates TNFalpha expression through its interaction with hnRNPL. Proc. Natl. Acad. Sci. USA 2014. 111: 1002-1007.
21. Carpenter, S., Aiello, D., Atianand, M. K., Ricci, E. P., Gandhi, P., Hall, L. L., Byron, M. et al., A long noncoding RNA mediates both activation and repression of immune response genes. Science 2013. 341: 789-792.
22. McHugh, C. A., Chen, C.-K., Chow, A., Surka, C. F., Tran, C., McDonel, P., Pandya-Jones, A. et al., The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 2015. 521: 232-236.
23. Wilusz, J. E., Sunwoo, H. and Spector, D. L., Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 2009. 23: 1494-1504.
24. Chaumeil, J., Le Baccon, P., Wutz, A. and Heard, E., A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev. 2006. 20: 2223-2237.
25. Matsui, K., Nishizawa, M., Ozaki, T., Kimura, T., Hashimoto, I., Yamada, M., Kaibori, M. et al., Natural antisense transcript stabilizes inducible nitric oxide synthase messenger RNA in rat hepatocytes. Hepatology 2008. 47: 686-697.
26. Tufarelli, C., Stanley, J. A., Garrick, D., Sharpe, J. A., Ayyub, H., Wood, W. G. and Higgs, D. R., Transcription of antisense RNA leading to gene silencing and methylation as a novel cause of human genetic disease. Nat. Genet. 2003. 34: 157-165.
27. Yu, W., Gius, D., Onyango, P., Muldoon-Jacobs, K., Karp, J., Feinberg, A. P. and Cui, H., Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 2008. 451: 202-206.
28. Hu, G., Tang, Q., Sharma, S., Yu, F., Escobar, T. M., Muljo, S. A., Zhu, J. et al., Expression and regulation of intergenic long noncoding RNAs during T cell development and differentiation. Nat. Immunol. 2013. 14: 1190-1198.
29. Ranzani, V., Rossetti, G., Panzeri, I., Arrigoni, A., Bonnal, R. J., Curti, S., Gruarin, P. et al., The long intergenic noncoding RNA landscape of human lymphocytes highlights the regulation of T cell differentiation by linc-MAF-4. Nat. Immunol. 2015. 16: 318-325.
30. Casero, D., Sandoval, S., Seet, C. S., Scholes, J., Zhu, Y., Ha, V. L., Luong, A. et al., Long non-coding RNA profiling of human lymphoid progenitor cells reveals transcriptional divergence of B cell and T cell lineages. Nat. Immunol. 2015. 16: 1282-1291.
31. Jiang, K., Sun, X., Chen, Y., Shen, Y. and Jarvis, J. N., RNA sequencing from human neutrophils reveals distinct transcriptional differences associated with chronic inflammatory states. BMC Med. Genomics 2015. 8: 55.
32. Zhang, X., Lian, Z., Padden, C., Gerstein, M. B., Rozowsky, J., Snyder, M., Gingeras, T. R. et al., A myelopoiesis-associated regulatory intergenic noncoding RNA transcript within the human HOXA cluster. Blood 2009. 113: 2526-2534.
33. Mayadas, T. N. and Cullere, X., Neutrophil beta2 integrins: moderators of life or death decisions. Trends Immunol. 2005. 26: 388-395.
34. Wang, P., Xue, Y., Han, Y., Lin, L., Wu, C., Xu, S., Jiang, Z. et al., The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science 2014. 344: 310-313.
35. Dijkstra, J. M. and Ballingall, K. T., Non-human lnc-DC orthologs encode Wdnm1-like protein. F1000Res. 2014. 3: 160.
36. Rapicavoli, N. A., Qu, K., Zhang, J., Mikhail, M., Laberge, R. M. and Chang, H. Y., A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. Elife 2013. 2: e00762.
37. Willingham, A. T., Orth, A. P., Batalov, S., Peters, E. C., Wen, B. G., Aza-Blanc, P., Hogenesch, J. B. et al., A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 2005. 309: 1570-1573.
38. Huang, W., Thomas, B., Flynn, R. A., Gavzy, S. J., Wu, L., Kim, S. V., Hall, J. A. et al., DDX5 and its associated lncRNA Rmrp modulate TH17 cell effector functions. Nature 2015. 528: 517-522.
39. Lu, J., Wu, X., Hong, M., Tobias, P. and Han, J., A potential suppressive effect of natural antisense IL-1beta RNA on lipopolysaccharide-induced IL-1beta expression. J. Immunol. 2013. 190: 6570-6578.
40. NE, I. I., Heward, J. A., Roux, B., Tsitsiou, E., Fenwick, P. S., Lenzi, L., Goodhead, I. et al., Long non-coding RNAs and enhancer RNAs regulate the lipopolysaccharide-induced inflammatory response in human monocytes. Nat. Commun. 2014. 5: 3979.
41. Chan, J., Atianand, M., Jiang, Z., Carpenter, S., Aiello, D., Elling, R., Fitzgerald, K. A. et al., Cutting edge: a natural antisense transcript, AS-IL1alpha, controls inducible transcription of the proinflammatory cytokine IL-1alpha. J. Immunol. 2015. 195: 1359-1363.
42. Tong, Q., Gong, A.-Y., Zhang, X., Lin, C., Ma, S., Chen, J., Hu, G. et al., LincRNA-Cox2 modulates TNF-α-induced transcription of Il12b gene in intestinal epithelial cells through regulation of Mi-2/NuRD-mediated epigenetic histone modifications. FASEB J. 2015: fj. 15-279166 [Epub ahead of print].
43. Krawczyk, M. and Emerson, B. M., p50-Associated COX-2 extragenic RNA (PACER) activates COX-2 gene expression by occluding repressive NF-kappaB complexes. Elife 2014. 3: e01776.
44. Tanne, A., Muniz, L. R., Puzio-Kuter, A., Leonova, K. I., Gudkov, A. V., Ting, D. T., Monasson, R. et al., Distinguishing the immunostimulatory properties of noncoding RNAs expressed in cancer cells. Proc. Natl. Acad. Sci. USA 2015. 112: 15154-15159.
45. Imamura, K., Imamachi, N., Akizuki, G., Kumakura, M., Kawaguchi, A., Nagata, K., Kato, A. et al., Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell 2014. 53: 393-406.
46. Zhang, Q., Chen, C. Y., Yedavalli, V. S. and Jeang, K. T., NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 2013. 4: e00596-e00512.
47. Ouyang, J., Zhu, X., Chen, Y., Wei, H., Chen, Q., Chi, X., Qi, B. et al. NRAV, a long noncoding RNA, modulates antiviral responses through suppression of interferon-stimulated gene transcription. Cell Host Microbe 2014. 16: 616-626.
48. Gomez, J. A., Wapinski, O. L., Yang, Y. W., Bureau, J. F., Gopinath, S., Monack, D. M., Chang, H. Y. et al., The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell 2013. 152: 743-754.
49. Sauvageau, M., Goff, L. A., Lodato, S., Bonev, B., Groff, A. F., Gerhardinger, C., Sanchez-Gomez, D. B. et al., Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife 2013. 2: e01749.
50. Grote, P., Wittler, L., Hendrix, D., Koch, F., Wahrisch, S., Beisaw, A., Macura, K. et al., The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev. Cell 2013. 24: 206-214.
51. Bassett, A. R., Akhtar, A., Barlow, D. P., Bird, A. P., Brockdorff, N., Duboule, D., Ephrussi, A. et al., Considerations when investigating lncRNA function in vivo. Elife 2014. 3: e03058.
52. Guttman, M., Donaghey, J., Carey, B. W., Garber, M., Grenier, J. K., Munson, G., Young, G. et al., lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011. 477: 295-300.
53. Sarma, K., Levasseur, P., Aristarkhov, A. and Lee, J. T., Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc. Natl. Acad. Sci. USA 2010. 107: 22196-22201.
54. Gilbert, L. A., Horlbeck, M. A., Adamson, B., Villalta, J. E., Chen, Y., Whitehead, E. H., Guimaraes, C. et al., Genome-scale CRISPR-mediated control of gene repression and activation. Cell 2014. 159: 647-661.
55. Konermann, S., Brigham, M. D., Trevino, A. E., Joung, J., Abudayyeh, O. O., Barcena, C., Hsu, P. D. et al., Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 2015. 517: 583-588.
56. Shalem, O., Sanjana, N. E. and Zhang, F., High-throughput functional genomics using CRISPR-Cas9. Nat. Rev. Genet. 2015. 16: 299-311.
57. Maurano, M. T., Humbert, R., Rynes, E., Thurman, R. E., Haugen, E., Wang, H., Reynolds, A. P. et al., Systematic localization of common disease-associated variation in regulatory DNA. Science 2012. 337: 1190-1195.
58. Kumar, V., Westra, H. J., Karjalainen, J., Zhernakova, D. V., Esko, T., Hrdlickova, B., Almeida, R. et al., Human disease-associated genetic variation impacts large intergenic non-coding RNA expression. PLoS Genet. 2013. 9: e1003201.