Battle of the midgets: Innate microRNA networking

RNA Biology

Volumn 9, Issue 6, 2012, Pages 792-798

  Elias, Shlomo ^a,b   Mandelboim, Ofer ^a  

^a HEBREW UNIVERSITY   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

ceRNA; MICA; MICB; miRNA; NK cells; NKG2D; ULBP

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1 CHAIN A; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1 CHAIN B; MICRORNA; NATURAL KILLER CELL RECEPTOR NKG2D; ULBP1 PROTEIN; ULBP2 PROTEIN; ULBP3 PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

3' UNTRANSLATED REGION; DISEASE COURSE; EPSTEIN BARR VIRUS; HUMAN; INNATE IMMUNITY; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW; VIRUS INFECTION;

EID: 84863471803     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.19717     Document Type: Review

References (67)

1. Kiessling R, Klein E, Pross H, Wigzell H. "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 1975; 5:117-21; PMID:1086218; http://dx.doi.org/10.1002/eji.1830050209.
2. Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol 2006; 7:517-23; PMID:16565719; http://dx.doi.org/10.1038/ ni1322.
3. Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med 1989; 320:1731-5; PMID:2543925; http://dx.doi.org/10.1056/NEJM198906293202605.
4. Pessino A, Sivori S, Bottino C, Malaspina A, Morelli L, Moretta L, et al. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med 1998; 188:953-60; PMID:9730896; http://dx.doi.org/10.1084/jem.188.5.953.
5. Pende D, Rivera P, Marcenaro S, Chang CC, Biassoni R, Conte R, et al. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res 2002; 62:6178-86; PMID:12414645.
6. Vitale M, Bottino C, Sivori S, Sanseverino L, Castriconi R, Marcenaro E, et al. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J Exp Med 1998; 187:2065-72; PMID:9625766; http://dx.doi.org/10.1084/jem.187.12.2065.
7. Bryceson YT, March ME, Ljunggren HG, Long EO. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol Rev 2006; 214:73-91; PMID:17100877; http://dx.doi.org/10.1111/j.1600-065X.2006.00457.x.
8. Halfteck GG, Elboim M, Gur C, Achdout H, Ghadially H, Mandelboim O. Enhanced in vivo growth of lymphoma tumors in the absence of the NK-activating receptor NKp46/NCR1. J Immunol 2009; 182:2221-30; PMID:19201876; http://dx.doi.org/10.4049/jimmunol.0801878.
9. Lanier LL. Turning on natural killer cells. J Exp Med 2000; 191:1259-62; PMID:10770793; http://dx.doi.org/10.1084/jem.191.8.1259.
10. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999; 285:727-9; PMID:10426993; http://dx.doi.org/10.1126/science. 285.5428.727.
11. Rölle A, Mousavi-Jazi M, Eriksson M, Odeberg J, Söderberg- Nauclér C, Cosman D, et al. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (ULBP)1 and ULBP2 is counteracted by the viral UL16 protein. J Immunol 2003; 171:902-8; PMID:12847260.
12. Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005; 436:1186-90; PMID:15995699; http://dx.doi.org/10.1038/nature03884.
13. Dunn C, Chalupny NJ, Sutherland CL, Dosch S, Sivakumar PV, Johnson DC, et al. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med 2003; 197:1427-39; PMID:12782710; http://dx.doi.org/10.1084/jem.20022059.
14. Cosman D, Müllberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001; 14:123-33; PMID:11239445; http://dx.doi.org/10.1016/S1074-7613(01)00095-4.
15. Salih HR, Antropius H, Gieseke F, Lutz SZ, Kanz L, Rammensee HG, et al. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 2003; 102:1389-96; PMID:12714493; http://dx.doi.org/10. 1182/blood-2003-01-0019.
16. Wu JD, Higgins LM, Steinle A, Cosman D, Haugk K, Plymate SR. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J Clin Invest 2004; 114:560-8; PMID:15314693.
17. Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002; 419:734-8; PMID:12384702; http://dx.doi.org/10.1038/nature01112.
18. Oppenheim DE, Roberts SJ, Clarke SL, Filler R, Lewis JM, Tigelaar RE, et al. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 2005; 6:928-37; PMID:16116470; http://dx.doi.org/10.1038/ni1239.
19. Andresen L, Jensen H, Pedersen MT, Hansen KA, Skov S. Molecular regulation of MHC class I chain-related protein A expression after HDAC-inhibitor treatment of Jurkat T cells. J Immunol 2007; 179:8235-42; PMID:18056367.
20. Butler JE, Moore MB, Presnell SR, Chan HW, Chalupny NJ, Lutz CT. Proteasome regulation of ULBP1 transcription. J Immunol 2009; 182:6600-9; PMID:19414815; http://dx.doi.org/10.4049/jimmunol.0801214.
21. Li H, Lakshmikanth T, Garofalo C, Enge M, Spinnler C, Anichini A, et al. Pharmacological activation of p53 triggers anticancer innate immune response through induction of ULBP2. Cell Cycle 2011; 10:3346-58; PMID:21941086; http://dx.doi.org/10.4161/cc.10.19.17630.
22. López-Soto A, Quiñones-Lombraña A, López-Arbesú R, López-Larrea C, González S. Transcriptional regulation of ULBP1, a human ligand of the NKG2D receptor. J Biol Chem 2006; 281:30419-30; PMID:16901903; http://dx.doi.org/10.1074/jbc. M604868200.
23. Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N, et al. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol 2008; 9:1065-73; PMID:18677316; http://dx.doi.org/ 10.1038/ni.1642.
24. Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, Biton M, et al. Host immune system gene targeting by a viral miRNA. Science 2007; 317:376-81; PMID:17641203; http://dx.doi.org/10.1126/science.1140956.
25. Bauman Y, Nachmani D, Vitenshtein A, Tsukerman P, Drayman N, Stern-Ginossar N, et al. An identical miRNA of the human JC and BK polyoma viruses targets the stress-induced ligand ULBP3 to escape immune elimination. Cell Host Microbe 2011; 9:93-102; PMID:21320692; http://dx.doi.org/10.1016/j. chom.2011.01.008.
26. Nachmani D, Lankry D, Wolf DG, Mandelboim O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol 2010; 11:806-13; PMID:20694010; http://dx.doi.org/10.1038/ni.1916.
27. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 2009; 5:376-85; PMID:19380116; http://dx.doi.org/10.1016/j.chom.2009.03.003.
28. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19:92-105; PMID:18955434; http://dx.doi.org/10.1101/gr.082701.108.
29. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9:102-14; PMID:18197166; http://dx.doi.org/10.1038/nrg2290.
30. Thomas M, Boname JM, Field S, Nejentsev S, Salio M, Cerundolo V, et al. Down-regulation of NKG2D and NKp80 ligands by Kaposi's sarcoma-associated herpesvirus K5 protects against NK cell cytotoxicity. Proc Natl Acad Sci U S A 2008; 105:1656-61; PMID:18230726; http://dx.doi.org/10.1073/pnas.0707883105.
31. Stephens HA. MICA and MICB genes: can the enigma of their polymorphism be resolved? Trends Immunol 2001; 22:378-85; PMID:11429322; http://dx.doi.org/10. 1016/S1471-4906(01)01960-3.
32. McSharry BP, Burgert HG, Owen DP, Stanton RJ, Prod'homme V, Sester M, et al. Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J Virol 2008; 82:4585-94; PMID:18287244; http://dx.doi.org/10.1128/JVI.02251-07.
33. Steinle A, Li P, Morris DL, Groh V, Lanier LL, Strong RK, et al. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics 2001; 53:279-87; PMID:11491531; http://dx.doi.org/10.1007/s002510100325.
34. Tagawa H, Seto M. A microRNA cluster as a target of genomic amplification in malignant lymphoma. Leukemia 2005; 19:2013-6; PMID:16167061; http://dx.doi.org/10.1038/sj.leu.2403942.
35. Dixon-McIver A, East P, Mein CA, Cazier JB, Molloy G, Chaplin T, et al. Distinctive patterns of microRNA expression associated with karyotype in acute myeloid leukaemia. PLoS One 2008; 3:e2141; PMID:18478077; http://dx.doi.org/10. 1371/journal.pone.0002141.
36. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Muckenthaler MU, et al. Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Blood 2007; 109:4399-405; PMID:17284533; http://dx.doi.org/10.1182/blood-2006-09-045104.
37. Li Z, Lu J, Sun M, Mi S, Zhang H, Luo RT, et al. Distinct microRNA expression profiles in acute myeloid leukemia with common translocations. Proc Natl Acad Sci U S A 2008; 105:15535-40; PMID:18832181; http://dx.doi.org/10. 1073/pnas.0808266105.
38. Li Y, Tan W, Neo TW, Aung MO, Wasser S, Lim SG, et al. Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci 2009; 100:1234-42; PMID:19486339; http://dx.doi.org/10.1111/j.1349-7006.2009.01164.x.
39. Blenkiron C, Goldstein LD, Thorne NP, Spiteri I, Chin SF, Dunning MJ, et al. MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol 2007; 8:R214; PMID:17922911; http://dx.doi.org/10. 1186/gb-2007-8-10-r214.
40. Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 2008; 10:202-10; PMID:18193036; http://dx.doi.org/10.1038/ncb1681.
41. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006; 9:189-98; PMID:16530703; http://dx.doi.org/10.1016/j.ccr.2006.01.025.
42. Voorhoeve PM, le Sage C, Schrier M, Gillis AJ, Stoop H, Nagel R, et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Adv Exp Med Biol 2007; 604:17-46; PMID:17695719; http://dx.doi.org/10.1007/978-0-387-69116-9-2.
43. Lee EJ, Gusev Y, Jiang J, Nuovo GJ, Lerner MR, Frankel WL, et al. Expression profiling identifies microRNA signature in pancreatic cancer. Int J Cancer 2007; 120:1046-54; PMID:17149698; http://dx.doi.org/10.1002/ijc.22394.
44. Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, van Oudenaarden A. MicroRNAs can generate thresholds in target gene expression. Nat Genet 2011; 43:854-9; PMID:21857679; http://dx.doi.org/10.1038/ng.905.
45. Heinemann A, Zhao F, Pechlivanis S, Eberle J, Steinle A, Diederichs S, et al. Tumor suppressive microRNAs miR-34a/c control cancer cell expression of ULBP2, a stress-induced ligand of the natural killer cell receptor NKG2D. Cancer Res 2012; 72:460-71; PMID:22102694; http://dx.doi.org/10.1158/0008-5472.CAN-11- 1977.
46. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17:193-9; PMID:19461653; http://dx.doi.org/10.1038/cdd.2009.56.
47. Corney DC, Hwang CI, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK, et al. Frequent downregulation of miR-34 family in human ovarian cancers. Clin Cancer Res 2010; 16:1119-28; PMID:20145172; http://dx.doi.org/10.1158/1078-0432. CCR-09-2642.
48. Lujambio A, Calin GA, Villanueva A, Ropero S, Sánchez- Céspedes M, Blanco D, et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci U S A 2008; 105:13556-61; PMID:18768788; http://dx.doi.org/10.1073/pnas.0803055105.
49. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y, et al. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 2008; 68:4123-32; PMID:18519671; http://dx.doi.org/10.1158/0008-5472.CAN-08-0325.
50. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Körner H, et al. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008; 7:2591-600; PMID:18719384; http://dx.doi.org/10. 4161/cc.7.16.6533.
51. Textor S, Fiegler N, Arnold A, Porgador A, Hofmann TG, Cerwenka A. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res 2011; 71:5998-6009; PMID:21764762; http://dx.doi.org/10.1158/0008-5472.CAN-10-3211.
52. Himmelreich H, Mathys A, Wodnar-Filipowicz A, Kalberer CP. Post-transcriptional regulation of ULBP1 ligand for the activating immunoreceptor NKG2D involves 3′ untranslated region. Hum Immunol 2011; 72:470-8; PMID:21406206; http://dx.doi.org/10.1016/j.humimm.2011.03.005.
53. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, Chi JT, et al. A viral microRNA functions as an orthologue of cellular miR-155. Nature 2007; 450:1096-9; PMID:18075594; http://dx.doi.org/10.1038/nature05992.
54. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M, Nusbaum JD, et al. Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 2011; 10:515-26; PMID:22100165; http://dx.doi.org/10. 1016/j.chom.2011.09.012.
55. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008; 455:58-63; PMID:18668040; http://dx.doi.org/10.1038/nature07228.
56. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37:495-500; PMID:15806104; http://dx.doi.org/10.1038/ng1536.
57. Stern-Ginossar N, Saleh N, Goldberg MD, Prichard M, Wolf DG, Mandelboim O. Analysis of human cytomegalovirus-encoded microRNA activity during infection. J Virol 2009; 83:10684-93; PMID:19656885; http://dx.doi.org/10.1128/JVI.01292- 09.
58. Grey F, Meyers H, White EA, Spector DH, Nelson J. A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog 2007; 3:e163; PMID:17983268; http://dx.doi.org/10.1371/journal.ppat.0030163.
59. Murphy E, Vanícek J, Robins H, Shenk T, Levine AJ. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc Natl Acad Sci U S A 2008; 105:5453-8; PMID:18378902; http://dx.doi.org/10.1073/pnas.0711910105.
60. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 2011; 146:353-8; PMID:21802130; http://dx.doi.org/10.1016/j.cell.2011.07.014.
61. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455:64-71; PMID:18668037; http://dx.doi.org/10.1038/nature07242.
62. Seitz H. Redefining microRNA targets. Curr Biol 2009; 19:870-3; PMID:19375315; http://dx.doi.org/10.1016/j.cub.2009.03.059.
63. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 2007; 39:1033-7; PMID:17643101; http://dx.doi.org/10.1038/ ng2079.
64. Sumazin P, Yang X, Chiu HS, Chung WJ, Iyer A, Llobet-Navas D, et al. An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 2011; 147:370-81; PMID:22000015; http://dx.doi.org/10.1016/j.cell.2011.09.041.
65. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG, et al. In vivo identification of tumor- suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 2011; 147:382-95; PMID:22000016; http://dx.doi.org/10.1016/j.cell.2011.09.032.
66. Tay Y, Kats L, Salmena L, Weiss D, Tan SM, Ala U, et al. Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 2011; 147:344-57; PMID:22000013; http://dx.doi.org/10. 1016/j.cell.2011.09.029.
67. Jalvy-Delvaille S, Maurel M, Majo V, Pierre N, Chabas S, Combe C, et al. Molecular basis of differential target regulation by miR-96 and miR-182: the Glypican-3 as a model. Nucleic Acids Res 2012; 40:1356-65; PMID:22009679; http://dx.doi.org/10.1093/nar/gkr843.