Regulation of miRNA biogenesis and turnover in the immune system

Immunological Reviews

Volumn 253, Issue 1, 2013, Pages 304-316

  Bronevetsky, Yelena ^a   Ansel, K Mark ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Argonaute; MiRNA processing; MiRNA turnover

Indexed keywords

ARGONAUTE PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIN28 PROTEIN; MICRORNA; MYC PROTEIN; NUCLEASE; PROTEIN; PROTEIN P53; SMAD PROTEIN; UNCLASSIFIED DRUG;

AUTOREGULATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; EXTRACELLULAR SPACE; FEEDBACK SYSTEM; GENE CONTROL; GENE EXPRESSION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW; RNA METABOLISM; RNA PROCESSING; RNA SYNTHESIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSCRIPTION REGULATION; TURNOVER TIME;

EID: 84875778506     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12059     Document Type: Review

References (129)

1. Ambros V. The evolution of our thinking about microRNAs. Nat Med 2008;14:1036-1040.
2. Castanotto D, Rossi JJ. The promises and pitfalls of RNA-interference-based therapeutics. Nature 2009;457:426-433.
3. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009;10:126-139.
4. Djuranovic S, Nahvi A, Green R. A parsimonious model for gene regulation by miRNAs. Science 2011;331:550-553.
5. Hoefig KP, Heissmeyer V. MicroRNAs grow up in the immune system. Curr Opin Immunol 2008;20:281-287.
6. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010;11:597-610.
7. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993;75:843-854.
8. Reinhart BJ, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000;403:901-906.
9. Ebert MS, Sharp PA. Roles for microRNAs in conferring robustness to biological processes. Cell 2012;149:515-524.
10. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012;148:1172-1187.
11. Xiao C, Rajewsky K. MicroRNA control in the immune system: basic principles. Cell 2009;136:26-36.
12. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010;10:111-122.
13. Schanen BC, Li X. Transcriptional regulation of mammalian miRNA genes. Genomics 2011;97:1-6.
14. Kirigin FF, et al. Dynamic microRNA gene transcription and processing during T cell development. J Immunol 2012;188:3257-3267.
15. Ozsolak F, et al. Chromatin structure analyses identify miRNA promoters. Genes Dev 2008;22:3172-3183.
16. Barski A, et al. Chromatin poises miRNA- and protein-coding genes for expression. Genome Res 2009;19:1742-1751.
17. Lee Y, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004;23:4051-4060.
18. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006;13:1097-1101.
19. Delgado MD, Leon J. Myc roles in hematopoiesis and leukemia. Genes Cancer 2010;1:605-616.
20. Wang R, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011;35:871-882.
21. Lin CY, et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 2012;151:56-67.
22. Nie Z, et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 2012;151:68-79.
23. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005;435:839-843.
24. Xiao C, et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 2008;9:405-414.
25. He L, et al. A microRNA polycistron as a potential human oncogene. Nature 2005;435:828-833.
26. Steiner DF, et al. MicroRNA-29 regulates T-box transcription factors and interferon-gamma production in helper T cells. Immunity 2011;35:169-181.
27. Jiang S, et al. Molecular dissection of the miR-17-92 cluster's critical dual roles in promoting Th1 responses and preventing inducible Treg differentiation. Blood 2011;118:5487-5497.
28. Bronevetsky Y, et al. T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J Exp Med 2013;210:417-432.
29. de Pontual L, et al. Germline deletion of the miR-17 approximately 92 cluster causes skeletal and growth defects in humans. Nat Genet 2011;43:1026-1030.
30. Chang TC, et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 2008;40:43-50.
31. Chang TC, et al. Lin-28B transactivation is necessary for Myc-mediated let-7 repression and proliferation. Proc Natl Acad Sci USA 2009;106:3384-3389.
32. Kim HH, Kuwano Y, Srikantan S, Lee EK, Martindale JL, Gorospe M. HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev 2009;23:1743-1748.
33. Boldin MP, Baltimore D. MicroRNAs, new effectors and regulators of NF-kappaB. Immunol Rev 2012;246:205-220.
34. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006;103:12481-12486.
35. Lu LF, et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 2010;142:914-929.
36. Yang L, et al. miR-146a controls the resolution of T cell responses in mice. J Exp Med 2012;209:1655-1670.
37. Zhao JL, Rao DS, Boldin MP, Taganov KD, O'Connell RM, Baltimore D. NF-kappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc Natl Acad Sci USA 2011;108:9184-9189.
38. Bazzoni F, et al. Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc Natl Acad Sci USA 2009;106:5282-5287.
39. Zhao H, Kalota A, Jin S, Gewirtz AM. The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood 2009;113:505-516.
40. Ben-Ami O, Pencovich N, Lotem J, Levanon D, Groner Y. A regulatory interplay between miR-27a and Runx1 during megakaryopoiesis. Proc Natl Acad Sci USA 2009;106:238-243.
41. Fazi F, et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 2005;123:819-831.
42. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev 2006;20:2202-2207.
43. Kuchen S, et al. Regulation of microRNA expression and abundance during lymphopoiesis. Immunity 2010;32:828-839.
44. Davis BN, Hata A. Regulation of MicroRNA Biogenesis: a miRiad of mechanisms. Cell Comm Signal 2009;7:18.
45. Blahna MT, Hata A. Smad-mediated regulation of microRNA biosynthesis. FEBS Lett 2012;586:1906-1912.
46. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008;454:56-61.
47. Fukuda T, et al. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat Cell Biol 2007;9:604-611.
48. Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A. Smad proteins bind a conserved RNA sequence to promote microRNA maturation by Drosha. Mol Cell 2010;39:373-384.
49. Yoshimura A, Wakabayashi Y, Mori T. Cellular and molecular basis for the regulation of inflammation by TGF-beta. J Biochem 2010;147:781-792.
50. Kang H, et al. Inhibition of microRNA-302 (miR-302) by bone morphogenetic protein 4 (BMP4) facilitates the BMP signaling pathway. J Biol Chem 2012;287:38656-38664.
51. Xu-Monette ZY, et al. Dysfunction of the TP53 tumor suppressor gene in lymphoid malignancies. Blood 2012;119:3668-3683.
52. Hermeking H. MicroRNAs in the p53 network: micromanagement of tumour suppression. Nat Rev Cancer 2012;12:613-626.
53. Klein U, et al. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 2010;17:28-40.
54. Park SY, Lee JH, Ha M, Nam JW, Kim VN. miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Cell Biol 2009;16:23-29.
55. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K. Modulation of microRNA processing by p53. Nature 2009;460:529-533.
56. Kumar MS, et al. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 2009;23:2700-2704.
57. Mudhasani R, et al. Loss of miRNA biogenesis induces p19Arf-p53 signaling and senescence in primary cells. J Cell Biol 2008;181:1055-1063.
58. Leveille N, et al. Selective inhibition of microRNA accessibility by RBM38 is required for p53 activity. Nat Commun 2011;2:513.
59. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science 2008;320:97-100.
60. Heo I, et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009;138:696-708.
61. Rybak A, et al. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 2008;10:987-993.
62. Mondol V, Pasquinelli AE. Let's make it happen: the role of let-7 microRNA in development. Curr Topics Cell Biol 2012;99:1-30.
63. Yuan J, Nguyen CK, Liu X, Kanellopoulou C, Muljo SA. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science 2012;335:1195-1200.
64. Yu J, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
65. Oertelt-Prigione S. The influence of sex and gender on the immune response. Autoimmun Rev 2012;11:A479-A485.
66. Yamagata K, et al. Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol Cell 2009;36:340-347.
67. Li X, et al. KSRP: a checkpoint for inflammatory cytokine production in astrocytes. Glia 2012;60:1773-1784.
68. Trabucchi M, et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009;459:1010-1014.
69. He Y, Smith R. Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B. Cell Mol Life Sci 2009;66:1239-1256.
70. Guil S, Caceres JF. The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat Struct Mol Biol 2007;14:591-596.
71. Michlewski G, Guil S, Semple CA, Caceres JF. Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell 2008;32:383-393.
72. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 2007;316:575-579.
73. Azuma-Mukai A, et al. Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc Natl Acad Sci U S A 2008;105:7964-7969.
74. Hafner M, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010;141:129-141.
75. Wang D, et al. Quantitative functions of Argonaute proteins in mammalian development. Genes Dev 2012;26:693-704.
76. O'Carroll D, et al. A Slicer-independent role for Argonaute 2 in hematopoiesis and the microRNA pathway. Genes Dev 2007;21:1999-2004.
77. Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007;131:1097-1108.
78. Lund E, Sheets MD, Imboden SB, Dahlberg JE. Limiting Ago protein restricts RNAi and microRNA biogenesis during early development in Xenopus laevis. Genes Dev 2011;25:1121-1131.
79. Zeng Y, Sankala H, Zhang X, Graves PR. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem J 2008;413:429-436.
80. Rudel S, et al. Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic Acids Res 2011;39:2330-2343.
81. Qi HH, et al. Prolyl 4-hydroxylation regulates Argonaute 2 stability. Nature 2008;455:421-424.
82. Adams BD, Claffey KP, White BA. Argonaute-2 expression is regulated by epidermal growth factor receptor and mitogen-activated protein kinase signaling and correlates with a transformed phenotype in breast cancer cells. Endocrinology 2009;150:14-23.
83. Rybak A, et al. The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat Cell Biol 2009;11:1411-1420.
84. Chen J, Lai F, Niswander L. The ubiquitin ligase mLin41 temporally promotes neural progenitor cell maintenance through FGF signaling. Genes Dev 2012;26:803-815.
85. Chang HM, Martinez NJ, Thornton JE, Hagan JP, Nguyen KD, Gregory RI. Trim71 cooperates with microRNAs to repress Cdkn1a expression and promote embryonic stem cell proliferation. Nat Commun 2012;3:923.
86. Loedige I, Gaidatzis D, Sack R, Meister G, Filipowicz W. The mammalian TRIM-NHL protein TRIM71/LIN-41 is a repressor of mRNA function. Nucleic Acids Res 2013;41:518-532.
87. Benoist C, Lanier L, Merad M, Mathis D. Consortium biology in immunology: the perspective from the Immunological Genome Project. Nat Rev Immunol 2012;12:734-740.
88. Muljo SA, Ansel KM, Kanellopoulou C, Livingston DM, Rao A, Rajewsky K. Aberrant T cell differentiation in the absence of Dicer. J Exp Med 2005;202:261-269.
89. Chong MM, Rasmussen JP, Rudensky AY, Littman DR. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J Exp Med 2008;205:2005-2017.
90. Rodriguez A, et al. Requirement of bic/microRNA-155 for normal immune function. Science 2007;316:608-611.
91. Thai TH, et al. Regulation of the germinal center response by microRNA-155. Science 2007;316:604-608.
92. Ma F, et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat Immunol 2011;12:861-869.
93. Smith KM, et al. miR-29ab1 deficiency identifies a negative feedback loop controlling Th1 bias that is dysregulated in multiple sclerosis. J Immunol 2012;189:1567-1576.
94. Lu J, et al. MicroRNA expression profiles classify human cancers. Nature 2005;435:834-838.
95. Gaur A, et al. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res 2007;67:2456-2468.
96. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 2007;39:673-677.
97. Lee YS, et al. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 2009;11:1150-1156.
98. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 2009;11:1143-1149.
99. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-659.
100. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002;2:569-579.
101. Zitvogel L, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 1998;4:594-600.
102. Zhang Y, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010;39:133-144.
103. Montecalvo A, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 2012;119:756-766.
104. Mittelbrunn M, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011;2:282.
105. Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA. MicroRNAs in body fluids-the mix of hormones and biomarkers. Nat Rev Clin Oncol 2011;8:467-477.
106. Lawrie CH, et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008;141:672-675.
107. Moussay E, et al. MicroRNA as biomarkers and regulators in B-cell chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2011;108:6573-6578.
108. Reid G, Kirschner MB, van Zandwijk N. Circulating microRNAs: association with disease and potential use as biomarkers. Crit Rev Oncol/hematol 2011;80:193-208.
109. Pritchard CC, et al. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res 2012;5:492-497.
110. Arroyo JD, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011;108:5003-5008.
111. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biology 2011;13:423-433.
112. Yu B, et al. Methylation as a crucial step in plant microRNA biogenesis. Science 2005;307:932-935.
113. Li J, Yang Z, Yu B, Liu J, Chen X. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol 2005;15:1501-1507.
114. Ramachandran V, Chen X. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 2008;321:1490-1492.
115. Upton JP, et al. IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 2012;338:818-822.
116. Hasnain SZ, Lourie R, Das I, Chen AC, McGuckin MA. The interplay between endoplasmic reticulum stress and inflammation. Immunol Cell Biol 2012;90:260-270.
117. Ansel KM, et al. Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Nat Struct Mol Biol 2008;15:523-530.
118. Gabel HW, Ruvkun G. The exonuclease ERI-1 has a conserved dual role in 5.8S rRNA processing and RNAi. Nat Struct Mol Biol 2008;15:531-533.
119. Dominski Z, Yang XC, Kaygun H, Dadlez M, Marzluff WF. A 3′ exonuclease that specifically interacts with the 3′ end of histone mRNA. Mol Cell 2003;12:295-305.
120. Hoefig KP, et al. Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-dependent decay. Nat Struct Mol Biol 2013;20:73-81.
121. Kennedy S, Wang D, Ruvkun G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 2004;427:645-649.
122. Thomas MF, et al. Eri1 regulates microRNA homeostasis and mouse lymphocyte development and antiviral function. Blood 2012;120:130-142.
123. Ameres SL, et al. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010;328:1534-1539.
124. Krutzfeldt J, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005;438:685-689.
125. Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 2007;4:721-726.
126. Cazalla D, Yario T, Steitz JA. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 2010;328:1563-1566.
127. Marcinowski L, et al. Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathogen 2012;8:e1002510.
128. Libri V, et al. Murine cytomegalovirus encodes a miR-27 inhibitor disguised as a target. Proc Natl Acad Sci USA 2012;109:279-284.
129. Backes S, et al. Degradation of host microRNAs by poxvirus poly(A) polymerase reveals terminal RNA methylation as a protective antiviral mechanism. Cell Host Microbe 2012;12:200-210.