miR-181 and metabolic regulation in the immune system

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 78, Issue 1, 2013, Pages 223-230

  Williams, Adam ^a   Henao Mejia, Jorge ^a   Harman, Christian C D ^a   Flavell, Richard A ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b 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; 3' UNTRANSLATED REGION; MIRN181 MICRORNA, HUMAN; PTEN PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL METABOLISM; CELL MIGRATION; CELL PROLIFERATION; GENE TARGETING; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; METABOLIC REGULATION; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; 3' UNTRANSLATED REGION; ALLELE; ANIMAL; BODY SIZE; CELL ENLARGEMENT; CELL MOTION; CYTOLOGY; HOMEOSTASIS; METABOLISM; MOUSE; NATURAL KILLER CELL; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; ADAPTIVE IMMUNITY; ALLELES; ANIMALS; BODY SIZE; CELL DIFFERENTIATION; CELL ENLARGEMENT; CELL MOVEMENT; CELL PROLIFERATION; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; KILLER CELLS, NATURAL; MICE; MICRORNAS; PHOSPHATIDYLINOSITOL 3-KINASES; PTEN PHOSPHOHYDROLASE;

EID: 84904874431     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2013.78.020024     Document Type: Article

References (72)

1. Alimonti A, Carracedo A, Clohessy JG, Trotman LC, Nardella C, Egia A, Salmena L, Sampieri K, Haveman WJ, Brogi E, et al. 2010. Subtle variations in Pten dose determine cancer susceptibility. Nat Genet 42: 454-458.
2. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF, Larsen CP, Ahmed R. 2009. mTOR regulates memory CD8 T-cell differentiation. Nature 460: 108-112.
3. Barthel A, Okino ST, Liao J, Nakatani K, Li J, Whitlock JP Jr, Roth RA. 1999. Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1. J Biol Chem 274: 20281-20286.
4. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, et al. 2005. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353: 1793-1801.
5. Carracedo A, Alimonti A, Pandolfi PP. 2011. PTEN level in tumor suppression: How much is too little? Cancer Res 71:629-633.
6. Carrer M, Liu N, Grueter CE, Williams AH, Frisard MI, Hulver MW, Bassel-Duby R, Olson EN. 2012. Control of mitochondrial metabolism and systemic energy homeostasis by micro-RNAs 378 and 378~. Proc Natl Acad Sci 109: 15330-15335.
7. Chen B, Li H, Zeng X, Yang P, Liu X, Zhao X, Liang S. 2012. Roles of microRNA on cancer cell metabolism. J Transl Med 10: 228.
8. Chen YH, Heneidi S, Lee JM, Layman LC, Stepp DW, Gamboa GM, Chen BS, Chazenbalk G, Azziz R. 2013. miRNA-93 inhibits GLUT4 and is overexpressed in adipose tissue of polycystic ovary syndrome patients and women with insulin resistance. Diabetes 62: 2278-2286.
9. Chi H. 2012. Regulation and function of mTOR signalling in T cell fate decisions. Nat Rev Immunol 12: 325-338.
10. Cobbold SP, Adams E, Nolan KF, Regateiro FS, Waldmann H. 2010. Connecting the mechanisms of T-cell regulation: Dendritic cells as the missing link. Immunol Rev 236: 203-218.
11. Davalos A, Goedeke L, Smibert P, Ramirez CM, Warrier NP, Andreo U, Cirera-Salinas D, Rayner K, Suresh U, Pastor-Pareja JC, et al. 2011. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci 108: 9232-9237.
12. D'Cruz LM, Knell J, Fujimoto JK, Goldrath AW. 2010. An essential role for the transcription factor HEB in thymocyte survival, Tcra rearrangement and the development of natural killer T cells. Nat Immunol 11: 240-249.
13. {thorn} natural killer T cell development depends on c-Myc. Proc Natl Acad Sci 106: 8641-8646.
14. Ebert MS, Sharp PA. 2012. Roles for microRNAs in conferring robustness to biological processes. Cell 149: 515-524.
15. Ebert PJ, Jiang S, Xie J, Li QJ, Davis MM. 2009. An endogenous positively selecting peptide enhances mature T cell responses and becomes an autoantigen in the absence of microRNA miR-181a. Nat Immunol 10: 1162-1169.
16. El Ouaamari A, Baroukh N, Martens GA, Lebrun P, Pipeleers D, van Obberghen E. 2008. miR-375 targets 30-phosphoinositide-dependent protein kinase-1 and regulates glucose-induced biological responses in pancreatic b-cells. Diabetes 57: 2708-2717.
17. Fang R, Xiao T, Fang Z, Sun Y, Li F, Gao Y, Feng Y, Li L, Wang Y, Liu X, et al. 2012. MicroRNA-143 (miR-143) regulates cancer glycolysis via targeting hexokinase 2 gene. J Biol Chem 287: 23227-23235.
18. Fayard E, Gill J, Paolino M, Hynx D, Hollander GA, Hemmings BA. 2007. Deletion of PKBa/Akt1 affects thymic development. PLoS One 2: e992.
19. Fayard E, Moncayo G, Hemmings BA, Hollander GA. 2010. Phosphatidylinositol 3-kinase signaling in thymocytes: The need for stringent control. Sci Signal 3: re5.
20. Fedeli M, Napolitano A, Wong MP, Marcais A, de Lalla C, Colucci F, Merkenschlager M, Dellabona P, Casorati G. 2009. Dicer-dependent microRNA pathway controls invariant NKT cell development. J Immunol 183: 2506-2512.
21. Fei X, Qi M, Wu B, Song Y, Wang Y, Li T. 2012. MicroRNA-195-5p suppresses glucose uptake and proliferation of human bladder cancer T24 cells by regulating GLUT3 expression. FEBS Lett 586: 392-397.
22. Finlay DK, Kelly AP, Clarke R, Sinclair LV, Deak M, Alessi DR, Cantrell DA. 2010. Temporal differences in the dependency on phosphoinositide-dependent kinase 1 distinguish the development of invariant Va14 NKT cells and conventional T cells. J Immunol 185: 5973-5982.
23. Fox CJ, Hammerman PS, Thompson CB. 2005. Fuel feeds function:Energy metabolism and the T-cell response. Nat Rev Immunol 5: 844-852.
24. Frauwirth KA, Thompson CB. 2002. Activation and inhibition of lymphocytes by costimulation. J Clin Invest 109: 295-299.
25. Garcia-Cao I, Song MS, Hobbs RM, Laurent G, Giorgi C, de Boer VC, Anastasiou D, Ito K, Sasaki AT, Rameh L, et al. 2012. Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell 149: 49-62.
26. Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB, Hay N. 2001. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 15: 1406-1418.
27. Gregersen LH, Jacobsen A, Frankel LB, Wen J, Krogh A, Lund AH. 2012. MicroRNA-143 down-regulates Hexokinase 2 in colon cancer cells. BMC Cancer 12: 232.
28. {thorn} thymocytes. Nat Immunol 3: 469-476.
29. Hay N, Sonenberg N. 2004. Upstream and downstream of mTOR. Genes Dev 18: 1926-1945.
30. He XY, Chen JX, Zhang Z, Li CL, Peng QL, Peng HM. 2010. The let-7a microRNA protects from growth of lung carcinoma by suppression of k-Ras and c-Myc in nude mice. J Cancer Res Clin Oncol 136: 1023-1028.
31. Henao-Mejia J, Williams A, Goff LA, Staron M, Licona-Limon P, Kaech SM, Nakayama M, Rinn JL, Flavell RA. 2013. The microRNA miR-181 is a critical cellular metabolic rheostat essential for NKT cell ontogenesis and lymphocyte development and homeostasis. Immunity 38: 984-997.
32. Hinton HJ, Alessi DR, Cantrell DA. 2004. The serine kinase phosphoinositide-dependent kinase 1 (PDK1) regulates T cell development. Nat Immunol 5: 539-545.
33. Horie T, Ono K, Nishi H, Iwanaga Y, Nagao K, Kinoshita M, Kuwabara Y, Takanabe R, Hasegawa K, Kita T, et al. 2009. MicroRNA-133 regulates the expression of GLUT4 by targeting KLF15 and is involved in metabolic control in cardiac myocytes. Biochem Biophys Res Commun 389: 315-320.
34. Hu W, Chan CS, Wu R, Zhang C, Sun Y, Song JS, Tang LH, Levine AJ, Feng Z. 2010. Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol Cell 38: 689-699.
35. Jacobs SR, Herman CE, Maciver NJ, Wofford JA, Wieman HL, Hammen JJ, Rathmell JC. 2008. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J Immunol 180: 4476-4486.
36. Ji H, Rintelen F, Waltzinger C, Bertschy Meier D, Bilancio A, Pearce W, Hirsch E, Wymann MP, Ruckle T, Camps M, et al. 2007. Inactivation of PI3Kγ and PI3Kδ distorts T-cell development and causes multiple organ inflammation. Blood 110:2940-2947.
37. Ji J, Yamashita T, Budhu A, Forgues M, Jia HL, Li C, Deng C, Wauthier E, Reid LM, Ye QH, et al. 2009. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology 50:472-480.
38. Jiang S, Li C, Olive V, Lykken E, Feng F, Sevilla J, Wan Y, He L, Li QJ. 2011. Molecular dissection of the miR-17-92 cluster's critical dual roles in promoting Th1 responses and preventing inducible Treg differentiation. Blood 118: 5487-5497.
39. Jiang S, Zhang LF, Zhang HW, Hu S, Lu MH, Liang S, Li B, Li Y, Li D, Wang ED, et al. 2012. A novel miR-155/miR-143 cascade controls glycolysis by regulating hexokinase 2 in breast cancer cells. EMBO J 31: 1985-1998.
40. Jones KB, Salah Z, Del Mare S, Galasso M, Gaudio E, Nuovo GJ, Lovat F, LeBlanc K, Palatini J, Randall RL, et al. 2012. miRNA signatures associate with pathogenesis and progression of osteosarcoma. Cancer Res 72: 1865-1877.
41. Juntilla MM, Wofford JA, Birnbaum MJ, Rathmell JC, Koretzky GA. 2007. Akt1 and Akt2 are required for αβ thymocyte survival and differentiation. Proc Natl Acad Sci 104: 12105-12110.
42. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG, DeNicola G, Webster KA, Weiss D, Perez-Mancera PA, et al. 2011. In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 147: 382-395.
43. Kuchen S, Resch W, Yamane A, Kuo N, Li Z, Chakraborty T, Wei L, Laurence A, Yasuda T, Peng S, et al. 2010. Regulation of microRNA expression and abundance during lymphopoiesis. Immunity 32: 828-839.
44. Kumar M, Lu Z, Takwi AA, Chen W, Callander NS, Ramos KS, Young KH, Li Y. 2011. Negative regulation of the tumor suppressor p53 gene by microRNAs. Oncogene 30: 843-853.
45. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, Lim B. 2009. MicroRNA-125b is a novel negative regulator of p53. Genes Dev 23: 862-876.
46. Lee DY, Jeyapalan Z, Fang L, Yang J, Zhang Y, Yee AY, Li M, Du WW, Shatseva T, Yang BB. 2010. Expression of versican 30-untranslated region modulates endogenous microRNA functions. PLoS One 5: e13599.
47. Lopez-Rios F, Sanchez-Arago M, Garcia-Garcia E, Ortega AD, Berrendero JR, Pozo-Rodriguez F, Lopez-Encuentra A, Ballestin C, Cuezva JM. 2007. Loss of the mitochondrial bioenergetic capacity underlies the glucose avidity of carcinomas. Cancer Res 67: 9013-9017.
48. Ma X, Kumar M, Choudhury SN, Becker Buscaglia LE, Barker JR, Kanakamedala K, Liu MF, Li Y. 2011. Loss of the miR-21 allele elevates the expression of its target genes and reduces tumorigenesis. Proc Natl Acad Sci 108: 10144-10149.
49. Mycko MP, Ferrero I, Wilson A, Jiang W, Bianchi T, Trumpp A, MacDonald HR. 2009. Selective requirement for c-Myc at an early stage of Va14i NKT cell development. J Immunol 182:4641-4648.
50. Myers MP, Pass I, Batty IH, Van der Kaay J, Stolarov JP, Hemmings BA, Wigler MH, Downes CP, Tonks NK. 1998. The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc Natl Acad Sci 95: 13513-13518.
51. Olive V, Bennett MJ, Walker JC, Ma C, Jiang I, Cordon-Cardo C, Li QJ, Lowe SW, Hannon GJ, He L. 2009. miR-19 is a key oncogenic component of mir-17-92. Genes Dev 23: 2839-2849.
52. Ortega-Molina A, Efeyan A, Lopez-Guadamillas E, Munoz-Martin M, Gomez-Lopez G, Canamero M, Mulero F, Pastor J, Martinez S, Romanos E, et al. 2012. Pten positively regulates brown adipose function, energy expenditure, and longevity. Cell Metab 15: 382-394.
53. Parry R, Smith G, Reif K, Sansom DM, Ward S. 1997. Activation of the PI3 K effector protein kinase B following ligation of CD28 or Fas. Biochem Soc Trans 25: S589.
54. Patrick DM, Montgomery RL, Qi X, Obad S, Kauppinen S, Hill JA, van Rooij E, Olson EN. 2010. Stress-dependent cardiac remodeling occurs in the absence of microRNA-21 in mice. J Clin Invest 120: 3912-3916.
55. Pearce EL, Pearce EJ. 2013. Metabolic pathways in immune cell activation and quiescence. Immunity 38: 633-643.
56. Peschiaroli A, Giacobbe A, Formosa A, Markert EK, Bongiorno-Borbone L, Levine AJ, Candi E, D'Alessandro A, Zolla L, Finazzi Agro A, et al. 2013. miR-143 regulates hexokinase 2 expression in cancer cells. Oncogene 32:797-802.
57. Pezzolesi MG, Platzer P, Waite KA, Eng C. 2008. Differential expression of PTEN-targeting microRNAs miR-19a and miR-21 in Cowden syndrome. Am J Hum Genet 82: 1141-1149.
58. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, Sportoletti P, Varmeh S, Egia A, Fedele G, et al. 2010. Identification of the miR-106b~25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 3: ra29.
59. Sampson VB, Rong NH, Han J, Yang Q, Aris V, Soteropoulos P, Petrelli NJ, Dunn SP, Krueger LJ. 2007. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res 67: 9762-9770.
60. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos SAJ, Stanford WL, Bolon B, Wakeham A, Itie A, Bouchard D, Kozieradzki I, et al. 2000. Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science 287: 1040-1046.
61. Sinclair LV, Finlay D, Feijoo C, Cornish GH, Gray A, Ager A, Okkenhaug K, Hagenbeek TJ, Spits H, Cantrell DA. 2008. Phosphatidylinositol-3-OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nat Immunol 9: 513-521.
62. Song MS, Salmena L, Pandolfi PP. 2012. The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol 13: 283-296.
63. Summers SA, Yin VP, Whiteman EL, Garza LA, Cho H, Tuttle RL, Birnbaum MJ. 1999. Signaling pathways mediating insulin-stimulated glucose transport. Ann NY Acad Sci 892: 169-186.
64. Swat W, Montgrain V, Doggett TA, Douangpanya J, Puri K, Vermi W, Diacovo TG. 2006. Essential role of PI3Kδ and PI3Kγ in thymocyte survival. Blood 107: 2415-2422.
65. Ueki K, Yamamoto-Honda R, Kaburagi Y, Yamauchi T, Tobe K, Burgering BM, Coffer PJ, Komuro I, Akanuma Y, Yazaki Y, et al. 1998. Potential role of protein kinase B in insulininduced glucose transport, glycogen synthesis, and protein synthesis. J Biol Chem 273: 5315-5322.
66. Vacchio MS, Bosselut R. 2013. T cell metabolism: MicroRNAs cap PTEN to feed the expanding crowd. Immunity 38: 847-848.
67. Vander Heiden MG, Cantley LC, Thompson CB. 2009. Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 324: 1029-1033.
68. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, et al. 2008. Targeted deletion reveals essential and overlapping functions of the miR-17~92 family of miRNA clusters. Cell 132: 875-886.
69. Webb LM, Vigorito E, Wymann MP, Hirsch E, Turner M. 2005. Cutting edge: T cell development requires the combined activities of the p110g and p110d catalytic isoforms of phosphatidylinositol 3-kinase. J Immunol 175: 2783-2787.
70. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, Henderson JM, Kutok JL, Rajewsky K. 2008. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 9: 405-414.
71. Zhang L, Deng T, Li X, Liu H, Zhou H, Ma J, Wu M, Zhou M, Shen S, Niu Z, et al. 2010. microRNA-141 is involved in a nasopharyngeal carcinoma-related genes network. Carcinogenesis 31: 559-566.
72. Zhu G, Chai J, Ma L, Duan H, Zhang H. 2013. Downregulated microRNA-32 expression induced by high glucose inhibits cell cycle progression via PTEN upregulation and Akt inactivation in bone marrow-derived mesenchymal stem cells. Biochem Biophys Res Commun 433: 526-531.