The MicroRNA miR-181 Is a Critical Cellular Metabolic Rheostat Essential for NKT Cell Ontogenesis and Lymphocyte Development and Homeostasis

Immunity

Volumn 38, Issue 5, 2013, Pages 984-997

  Henao Mejia, Jorge ^a   Williams, Adam ^a   Goff, LoyalA ^b,c,d   Staron, Matthew ^a   Licona Limón, Paula ^a   Kaech, SusanM ^a,f   Nakayama, Maki ^e   Rinn, JohnL ^b,c   Flavell, RichardA ^a,f  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c Harvard University   (United States)

^d Department of Electrical Engineering and Computer Science   (United States)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 181; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOSYNTHESIS; CELL METABOLISM; CONTROLLED STUDY; ENZYME REGULATION; HOMEOSTASIS; LYMPHOCYTE DIFFERENTIATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CHEMOKINE CXCL12; DOWN-REGULATION; HOMEOSTASIS; LYMPHOCYTES; LYMPHOPOIESIS; MICE; MICRORNAS; NATURAL KILLER T-CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

EID: 84878203252     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.02.021     Document Type: Article

References (52)

1. Alimonti A., Carracedo A., Clohessy J.G., Trotman L.C., Nardella C., Egia A., Salmena L., Sampieri K., Haveman W.J., Brogi E., et al. Subtle variations in Pten dose determine cancer susceptibility. Nat. Genet. 2010, 42:454-458.
2. Amin R.H., Schlissel M.S. Foxo1 directly regulates the transcription of recombination-activating genes during B cell development. Nat. Immunol. 2008, 9:613-622.
3. Baracho G.V., Miletic A.V., Omori S.A., Cato M.H., Rickert R.C. Emergence of the PI3-kinase pathway as a central modulator of normal and aberrant B cell differentiation. Curr. Opin. Immunol. 2011, 23:178-183.
4. Barthel A., Okino S.T., Liao J., Nakatani K., Li J., Whitlock J.P., Roth R.A. Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1. J.Biol. Chem. 1999, 274:20281-20286.
5. Calin G.A., Ferracin M., Cimmino A., Di Leva G., Shimizu M., Wojcik S.E., Iorio M.V., Visone R., Sever N.I., Fabbri M., et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N.Engl. J. Med. 2005, 353:1793-1801.
6. Carracedo A., Alimonti A., Pandolfi P.P. PTEN level in tumor suppression: how much is too little?. Cancer Res. 2011, 71:629-633.
7. Christofk H.R., Vander Heiden M.G., Harris M.H., Ramanathan A., Gerszten R.E., Wei R., Fleming M.D., Schreiber S.L., Cantley L.C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230-233.
8. Cobb B.S., Nesterova T.B., Thompson E., Hertweck A., O'Connor E., Godwin J., Wilson C.B., Brockdorff N., Fisher A.G., Smale S.T., Merkenschlager M. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J.Exp. Med. 2005, 201:1367-1373.
9. D'Cruz L.M., Knell J., Fujimoto J.K., Goldrath A.W. An essential role for the transcription factor HEB in thymocyte survival, Tcra rearrangement and the development of natural killer Tcells. Nat. Immunol. 2010, 11:240-249.
10. Dengler H.S., Baracho G.V., Omori S.A., Bruckner S., Arden K.C., Castrillon D.H., DePinho R.A., Rickert R.C. Distinct functions for the transcription factor Foxo1 at various stages of B cell differentiation. Nat. Immunol. 2008, 9:1388-1398.
11. Dose M., Sleckman B.P., Han J., Bredemeyer A.L., Bendelac A., Gounari F. Intrathymic proliferation wave essential for Valpha14+ natural killer Tcell development depends on c-Myc. Proc. Natl. Acad. Sci. USA 2009, 106:8641-8646.
12. Ebert M.S., Sharp P.A. Roles for microRNAs in conferring robustness to biological processes. Cell 2012, 149:515-524.
13. Ebert P.J., Jiang S., Xie J., Li Q.J., Davis M.M. An endogenous positively selecting peptide enhances mature Tcell responses and becomes an autoantigen in the absence of microRNA miR-181a. Nat. Immunol. 2009, 10:1162-1169.
14. Fayard E., Gill J., Paolino M., Hynx D., Holländer G.A., Hemmings B.A. Deletion of PKBalpha/Akt1 affects thymic development. PLoS ONE 2007, 2:e992.
15. Fayard E., Moncayo G., Hemmings B.A., Holländer G.A. Phosphatidylinositol 3-kinase signaling in thymocytes: the need for stringent control. Sci. Signal. 2010, 3:re5.
16. Fedeli M., Napolitano A., Wong M.P., Marcais A., de Lalla C., Colucci F., Merkenschlager M., Dellabona P., Casorati G. Dicer-dependent microRNA pathway controls invariant NKT cell development. J.Immunol. 2009, 183:2506-2512.
17. Finlay D.K., Kelly A.P., Clarke R., Sinclair L.V., Deak M., Alessi D.R., Cantrell D.A. Temporal differences in the dependency on phosphoinositide-dependent kinase 1 distinguish the development of invariant Valpha14 NKT cells and conventional Tcells. J.Immunol. 2010, 185:5973-5982.
18. Fragoso R., Mao T., Wang S., Schaffert S., Gong X., Yue S., Luong R., Min H., Yashiro-Ohtani Y., Davis M., et al. Modulating the strength and threshold of NOTCH oncogenic signals by mir-181a-1/b-1. PLoS Genet. 2012, 8:e1002855.
19. Garcia-Cao I., Song M.S., Hobbs R.M., Laurent G., Giorgi C., de Boer V.C., Anastasiou D., Ito K., Sasaki A.T., Rameh L., et al. Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell 2012, 149:49-62.
20. Guo J., Hawwari A., Li H., Sun Z., Mahanta S.K., Littman D.R., Krangel M.S., He Y.W. Regulation of the TCRalpha repertoire by the survival window of CD4(+)CD8(+) thymocytes. Nat. Immunol. 2002, 3:469-476.
21. Hay N., Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004, 18:1926-1945.
22. Hinton H.J., Alessi D.R., Cantrell D.A. The serine kinase phosphoinositide-dependent kinase 1 (PDK1) regulates Tcell development. Nat. Immunol. 2004, 5:539-545.
23. Huse J.T., Brennan C., Hambardzumyan D., Wee B., Pena J., Rouhanifard S.H., Sohn-Lee C., le Sage C., Agami R., Tuschl T., Holland E.C. The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis invivo. Genes Dev. 2009, 23:1327-1337.
24. Inui M., Martello G., Piccolo S. MicroRNA control of signal transduction. Nat. Rev. Mol. Cell Biol. 2010, 11:252-263.
25. Janas M.L., Varano G., Gudmundsson K., Noda M., Nagasawa T., Turner M. Thymic development beyond beta-selection requires phosphatidylinositol 3-kinase activation by CXCR4. J.Exp. Med. 2010, 207:247-261.
26. Ji H., Rintelen F., Waltzinger C., Bertschy Meier D., Bilancio A., Pearce W., Hirsch E., Wymann M.P., Rückle T., Camps M., et al. Inactivation of PI3Kgamma and PI3Kdelta distorts T-cell development and causes multiple organ inflammation. Blood 2007, 110:2940-2947.
27. Ji J., Yamashita T., Budhu A., Forgues M., Jia H.L., Li C., Deng C., Wauthier E., Reid L.M., Ye Q.H., et al. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology 2009, 50:472-480.
28. Jones K.B., Salah Z., Del Mare S., Galasso M., Gaudio E., Nuovo G.J., Lovat F., LeBlanc K., Palatini J., Randall R.L., et al. miRNA signatures associate with pathogenesis and progression of osteosarcoma. Cancer Res. 2012, 72:1865-1877.
29. Juntilla M.M., Wofford J.A., Birnbaum M.J., Rathmell J.C., Koretzky G.A. Akt1 and Akt2 are required for alphabeta thymocyte survival and differentiation. Proc. Natl. Acad. Sci. USA 2007, 104:12105-12110.
30. Kelly A.P., Finlay D.K., Hinton H.J., Clarke R.G., Fiorini E., Radtke F., Cantrell D.A. Notch-induced Tcell development requires phosphoinositide-dependent kinase 1. EMBO J. 2007, 26:3441-3450.
31. Kuchen S., Resch W., Yamane A., Kuo N., Li Z., Chakraborty T., Wei L., Laurence A., Yasuda T., Peng S., et al. Regulation of microRNA expression and abundance during lymphopoiesis. Immunity 2010, 32:828-839.
32. Li Q.J., Chau J., Ebert P.J., Sylvester G., Min H., Liu G., Braich R., Manoharan M., Soutschek J., Skare P., et al. miR-181a is an intrinsic modulator of Tcell sensitivity and selection. Cell 2007, 129:147-161.
33. Ma X., Kumar M., Choudhury S.N., Becker Buscaglia L.E., Barker J.R., Kanakamedala K., Liu M.F., Li Y. Loss of the miR-21 allele elevates the expression of its target genes and reduces tumorigenesis. Proc. Natl. Acad. Sci. USA 2011, 108:10144-10149.
34. Mendell J.T., Olson E.N. MicroRNAs in stress signaling and human disease. Cell 2012, 148:1172-1187.
35. Mycko M.P., Ferrero I., Wilson A., Jiang W., Bianchi T., Trumpp A., MacDonald H.R. Selective requirement for c-Myc at an early stage of V(alpha)14i NKT cell development. J.Immunol. 2009, 182:4641-4648.
36. Olive V., Bennett M.J., Walker J.C., Ma C., Jiang I., Cordon-Cardo C., Li Q.J., Lowe S.W., Hannon G.J., He L. miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 2009, 23:2839-2849.
37. Ortega-Molina A., Efeyan A., Lopez-Guadamillas E., Muñoz-Martin M., Gómez-López G., Cañamero M., Mulero F., Pastor J., Martinez S., Romanos E., et al. Pten positively regulates brown adipose function, energy expenditure, and longevity. Cell Metab. 2012, 15:382-394.
38. Osthus R.C., Shim H., Kim S., Li Q., Reddy R., Mukherjee M., Xu Y., Wonsey D., Lee L.A., Dang C.V. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J.Biol. Chem. 2000, 275:21797-21800.
39. Pal A., Barber T.M., Van de Bunt M., Rudge S.A., Zhang Q., Lachlan K.L., Cooper N.S., Linden H., Levy J.C., Wakelam M.J., et al. PTEN mutations as a cause of constitutive insulin sensitivity and obesity. N.Engl. J. Med. 2012, 367:1002-1011.
40. Park C.Y., Choi Y.S., McManus M.T. Analysis of microRNA knockouts in mice. Hum. Mol. Genet. 2010, 19(R2):R169-R175.
41. Patrick D.M., Montgomery R.L., Qi X., Obad S., Kauppinen S., Hill J.A., van Rooij E., Olson E.N. Stress-dependent cardiac remodeling occurs in the absence of microRNA-21 in mice. J.Clin. Invest. 2010, 120:3912-3916.
42. Sasaki T., Irie-Sasaki J., Jones R.G., Oliveira-dos-Santos A.J., Stanford W.L., Bolon B., Wakeham A., Itie A., Bouchard D., Kozieradzki I., et al. Function of PI3Kgamma in thymocyte development, Tcell activation, and neutrophil migration. Science 2000, 287:1040-1046.
43. Small E.M., O'Rourke J.R., Moresi V., Sutherland L.B., McAnally J., Gerard R.D., Richardson J.A., Olson E.N. Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc. Natl. Acad. Sci. USA 2010, 107:4218-4223.
44. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
45. Swat W., Montgrain V., Doggett T.A., Douangpanya J., Puri K., Vermi W., Diacovo T.G. Essential role of PI3Kdelta and PI3Kgamma in thymocyte survival. Blood 2006, 107:2415-2422.
46. Trapnell C., Pachter L., Salzberg S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
47. Ventura A., Young A.G., Winslow M.M., Lintault L., Meissner A., Erkeland S.J., Newman J., Bronson R.T., Crowley D., Stone J.R., et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008, 132:875-886.
48. Wang W., Wykrzykowska J., Johnson T., Sen R., Sen J. A NF-kappa B/c-myc-dependent survival pathway is targeted by corticosteroids in immature thymocytes. J.Immunol. 1999, 162:314-322.
49. Webb L.M., Vigorito E., Wymann M.P., Hirsch E., Turner M. Cutting edge: Tcell development requires the combined activities of thep110gamma and p110delta catalytic isoforms of phosphatidylinositol 3-kinase. J.Immunol. 2005, 175:2783-2787.
50. Wieman H.L., Wofford J.A., Rathmell J.C. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol. Biol. Cell 2007, 18:1437-1446.
51. Zheng Q., Zhou L., Mi Q.S. MicroRNA miR-150 is involved in Vα14 invariant NKT cell development and function. J.Immunol. 2012, 188:2118-2126.
52. Zilberman Y., Zafrir E., Ovadia H., Yefenof E., Guy R., Sionov R.V. The glucocorticoid receptor mediates the thymic epithelial cell-induced apoptosis of CD4+8+ thymic lymphoma cells. Cell. Immunol. 2004, 227:12-23.