CD46 activation regulates miR-150-mediated control of GLUT1 expression and cytokine secretion in human CD4+ T cells

Journal of Immunology

Volumn 196, Issue 4, 2016, Pages 1636-1645

  King, Ben C ^a   Esguerra, Jonathan L S ^b   Golec, Ewelina ^a   Eliasson, Lena ^b   Kemper, Claudia ^c   Blom, Anna M ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c GUY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; GAMMA INTERFERON; GLUCOSE TRANSPORTER 1; INTERLEUKIN 10; MEMBRANE COFACTOR PROTEIN; MICRORNA; MICRORNA 150; UNCLASSIFIED DRUG; CD46 PROTEIN, HUMAN; CYTOKINE; MIRN150 MICRORNA, HUMAN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; GENE; GENE AMPLIFICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SILENCING; GENE TARGETING; GLUCOSE TRANSPORT; GLUT1 GENE; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; BIOSYNTHESIS; CELL SEPARATION; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; POLYMERASE CHAIN REACTION; SECRETION (PROCESS);

ANTIGENS, CD46; CD4-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CYTOKINES; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 1; HUMANS; IMMUNOBLOTTING; LYMPHOCYTE ACTIVATION; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; TH1 CELLS;

EID: 84958582282     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500516     Document Type: Article

References (59)

1. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
2. Gazzinelli, R. T., M. Wysocka, S. Hieny, T. Scharton-Kersten, A. Cheever, R. Kuhn, W. Muller, G. Trinchieri, and A. Sher. 1996. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-g and TNF-a. J. Immunol. 157: 798-805.
3. Hunter, C. A., L. A. Ellis-Neyes, T. Slifer, S. Kanaly, G. Grunig, M. Fort, D. Rennick, and F. G. Araujo. 1997. IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J. Immunol. 158: 3311-3316.
4. Trinchieri, G. 2007. Interleukin-10 production by effector T cells: Th1 cells show self control. J. Exp. Med. 204: 239-243.
5. Jankovic, D., M. C. Kullberg, C. G. Feng, R. S. Goldszmid, C. M. Collazo, M. Wilson, T. A. Wynn, M. Kamanaka, R. A. Flavell, and A. Sher. 2007. Conventional T-bet+Foxp32 Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204: 273-283.
6. Anderson, C. F., M. Oukka, V. J. Kuchroo, and D. Sacks. 2007. CD4+CD252 Foxp32 Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204: 285-297.
7. Gabrysová, L., K. S. Nicolson, H. B. Streeter, J. Verhagen, C. A. Sabatos-Peyton, D. J. Morgan, and D. C. Wraith. 2009. Negative feedback control of the autoimmune response through antigen-induced differentiation of IL-10-secreting Th1 cells. J. Exp. Med. 206: 1755-1767.
8. Meiler, F., J. Zumkehr, S. Klunker, B. Ruckert, C. A. Akdis, and M. Akdis. 2008. In vivo switch to IL-10-secreting T regulatory cells in high dose allergen exposure. J. Exp. Med. 205: 2887-2898.
9. Saraiva, M., J. R. Christensen, M. Veldhoen, T. L. Murphy, K. M. Murphy, and A. O'Garra. 2009. Interleukin-10 production by Th1 cells requires interleukin-12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 31: 209-219.
10. Cardone, J., G. Le Friec, P. Vantourout, A. Roberts, A. Fuchs, I. Jackson, T. Suddason, G. Lord, J. P. Atkinson, A. Cope, et al. 2010. Complement regulator CD46 temporally regulates cytokine production by conventional and unconventional T cells. Nat. Immunol. 11: 862-871.
11. Astier, A., M. C. Trescol-Biémont, O. Azocar, B. Lamouille, and C. Rabourdin-Combe. 2000. Cutting edge: CD46, a new costimulatory molecule for T cells, that induces p120CBL and LAT phosphorylation. J. Immunol. 164: 6091-6095.
12. Le Friec, G., D. Sheppard, P. Whiteman, C. M. Karsten, S. A. Shamoun, A. Laing, L. Bugeon, M. J. Dallman, T. Melchionna, C. Chillakuri, et al. 2012. The CD46-Jagged1 interaction is critical for human TH1 immunity. Nat. Immunol. 13: 1213-1221.
13. Kemper, C., A. C. Chan, J. M. Green, K. A. Brett, K. M. Murphy, and J. P. Atkinson. 2003. Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 421: 388-392.
14. Cattaneo, R. 2004. Four viruses, two bacteria, and one receptor: membrane cofactor protein (CD46) as pathogens' magnet. J. Virol. 78: 4385-4388.
15. Tsujimura, A., K. Shida, M. Kitamura, M. Nomura, J. Takeda, H. Tanaka, M. Matsumoto, K. Matsumiya, A. Okuyama, Y. Nishimune, et al. 1998. Molecular cloning of a murine homologue of membrane cofactor protein (CD46): preferential expression in testicular germ cells. Biochem. J. 330: 163-168.
16. Török, K., M. Kremlitzka, N. Sándor, E. A. Tóth, Z. Bajtay, and A. Erdei. 2012. Human T cell derived, cell-bound complement iC3b is integrally involved in T cell activation. Immunol. Lett. 143: 131-136.
17. Astier, A. L., G. Meiffren, S. Freeman, and D. A. Hafler. 2006. Alterations in CD46-mediated Tr1 regulatory T cells in patients with multiple sclerosis. J. Clin. Invest. 116: 3252-3257.
18. Baltimore, D., M. P. Boldin, R. M. O'Connell, D. S. Rao, and K. D. Taganov. 2008. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9: 839-845.
19. Zhou, X., L. T. Jeker, B. T. Fife, S. Zhu, M. S. Anderson, M. T. McManus, and J. A. Bluestone. 2008. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 205: 1983-1991.
20. Li, Q. J., J. Chau, P. J. Ebert, G. Sylvester, H. Min, G. Liu, R. Braich, M. Manoharan, J. Soutschek, P. Skare, et al. 2007. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 129: 147-161.
21. Henao-Mejia, J., A. Williams, L. A. Goff, M. Staron, P. Licona-Limón, S. M. Kaech, M. Nakayama, J. L. Rinn, and R. A. Flavell. 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.
22. Harris, C. L., O. B. Spiller, and B. P. Morgan. 2000. Human and rodent decayaccelerating factors (CD55) are not species restricted in their complementinhibiting activities. Immunology 100: 462-470.
23. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98: 5116-5121.
24. Saeed, A. I., V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, M. Thiagarajan, et al. 2003. TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
25. Vandesompele, J., K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman. 2002. Accurate normalization of real-time quantitative RTPCR data by geometric averaging of multiple internal control genes. Genome Biol. 3: research0034.
26. Kim, S. W., Z. Li, P. S. Moore, A. P. Monaghan, Y. Chang, M. Nichols, and B. John. 2010. A sensitive non-radioactive northern blot method to detect small RNAs. Nucleic Acids Res. 38: e98.
27. Zaffran, Y., O. Destaing, A. Roux, S. Ory, T. Nheu, P. Jurdic, C. Rabourdin-Combe, and A. L. Astier. 2001. CD46/CD3 costimulation induces morphological changes of human T cells and activation of Vav, Rac, and extracellular signalregulated kinase mitogen-activated protein kinase. J. Immunol. 167: 6780-6785.
28. Baumjohann, D., and K. M. Ansel. 2013. MicroRNA-mediated regulation of T helper cell differentiation and plasticity. Nat. Rev. Immunol. 13: 666-678.
29. Lee, K., N. Kunkeaw, S. H. Jeon, I. Lee, B. H. Johnson, G. Y. Kang, J. Y. Bang, H. S. Park, C. Leelayuwat, and Y. S. Lee. 2011. Precursor miR-886, a novel noncoding RNA repressed in cancer, associates with PKR and modulates its activity. RNA 17: 1076-1089.
30. Rodriguez, A., E. Vigorito, S. Clare, M. V. Warren, P. Couttet, D. R. Soond, S. van Dongen, R. J. Grocock, P. P. Das, E. A. Miska, et al. 2007. Requirement of bic/microRNA-155 for normal immune function. Science 316: 608-611.
31. Xiao, C., D. P. Calado, G. Galler, T. H. Thai, H. C. Patterson, J. Wang, N. Rajewsky, T. P. Bender, and K. Rajewsky. 2007. miR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131: 146-159.
32. Sonkoly, E., P. Janson, M. L. Majuri, T. Savinko, N. Fyhrquist, L. Eidsmo, N. Xu, F. Meisgen, T. Wei, M. Bradley, et al. 2010. miR-155 is overexpressed in patients with atopic dermatitis and modulates T-cell proliferative responses by targeting cytotoxic T lymphocyte-associated antigen 4. J. Allergy Clin. Immunol. 126: 581-589.e1-20.
33. Dudda, J. C., B. Salaun, Y. Ji, D. C. Palmer, G. C. Monnot, E. Merck, C. Boudousquie, D. T. Utzschneider, T. M. Escobar, R. Perret, et al. 2013. MicroRNA-155 is required for effector CD8+ T cell responses to virus infection and cancer. Immunity 38: 742-753.
34. Jacobs, S. R., C. E. Herman, N. J. Maciver, J. A. Wofford, H. L. Wieman, J. J. Hammen, and J. C. Rathmell. 2008. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 180: 4476-4486.
35. Frauwirth, K. A., J. L. Riley, M. H. Harris, R. V. Parry, J. C. Rathmell, D. R. Plas, R. L. Elstrom, C. H. June, and C. B. Thompson. 2002. The CD28 signaling pathway regulates glucose metabolism. Immunity 16: 769-777.
36. Kolev, M., S. Dimeloe, G. Le Friec, A. Navarini, G. Arbore, G. A. Povoleri, M. Fischer, R. Belle, J. Loeliger, L. Develioglu, et al. 2015. Complement regulates nutrient influx and metabolic reprogramming during Th1 cell responses. Immunity 42: 1033-1047.
37. Quintana, A. M., F. Liu, J. P. O'Rourke, and S. A. Ness. 2011. Identification and regulation of c-Myb target genes in MCF-7 cells. BMC Cancer 11: 30.
38. Nakata, Y., A. C. Brignier, S. Jin, Y. Shen, S. I. Rudnick, M. Sugita, and A. M. Gewirtz. 2010. c-Myb, Menin, GATA-3, and MLL form a dynamic transcription complex that plays a pivotal role in human T helper type 2 cell development. Blood 116: 1280-1290.
39. Bartel, D. P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
40. Tay, Y., L. Kats, L. Salmena, D. Weiss, S. M. Tan, U. Ala, F. Karreth, L. Poliseno, P. Provero, F. Di Cunto, et al. 2011. Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 147: 344-357.
41. Hansen, T. B., T. I. Jensen, B. H. Clausen, J. B. Bramsen, B. Finsen, C. K. Damgaard, and J. Kjems. 2013. Natural RNA circles function as efficient microRNA sponges. Nature 495: 384-388.
42. Thomas, M., J. Lieberman, and A. Lal. 2010. Desperately seeking microRNA targets. Nat. Struct. Mol. Biol. 17: 1169-1174.
43. Astier, A. L. 2008. T-cell regulation by CD46 and its relevance in multiple sclerosis. Immunology 124: 149-154.
44. Macintyre, A. N., V. A. Gerriets, A. G. Nichols, R. D. Michalek, M. C. Rudolph, D. Deoliveira, S. M. Anderson, E. D. Abel, B. J. Chen, L. P. Hale, and J. C. Rathmell. 2014. The glucose transporter Glut1 is selectively essential for CD4 T cell activation and effector function. Cell Metab. 20: 61-72.
45. Truscott, S. M., G. Abate, J. D. Price, C. Kemper, J. P. Atkinson, and D. F. Hoft. 2010. CD46 engagement on human CD4+ T cells produces T regulatory type 1-like regulation of antimycobacterial T cell responses. Infect. Immun. 78: 5295-5306.
46. Chang, C. H., J. D. Curtis, L. B. Maggi, Jr., B. Faubert, A. V. Villarino, D. O'Sullivan, S. C. Huang, G. J. van der Windt, J. Blagih, J. Qiu, et al. 2013. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153: 1239-1251.
47. Palmer, C. S., M. Ostrowski, B. Balderson, N. Christian, and S. M. Crowe. 2015. Glucose metabolism regulates T cell activation, differentiation, and functions. Front. Immunol. 6: 1.
48. Michalek, R. D., V. A. Gerriets, S. R. Jacobs, A. N. Macintyre, N. J. MacIver, E. F. Mason, S. A. Sullivan, A. G. Nichols, and J. C. Rathmell. 2011. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J. Immunol. 186: 3299-3303.
49. Selbach, M., B. Schwanhäusser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
50. Baek, D., J. Villén, C. Shin, F. D. Camargo, S. P. Gygi, and D. P. Bartel. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
51. Jiang, X., H. Huang, Z. Li, Y. Li, X. Wang, S. Gurbuxani, P. Chen, C. He, D. You, S. Zhang, et al. 2012. Blockade of miR-150 maturation by MLL-fusion/MYC/LIN-28 is required for MLL-associated leukemia. Cancer Cell 22: 524-535.
52. Cai, J., X. Liu, J. Cheng, Y. Li, X. Huang, Y. Li, X. Ma, H. Yu, H. Liu, and R. Wei. 2012. MicroRNA-200 is commonly repressed in conjunctival MALT lymphoma, and targets cyclin E2. Graefes Arch. Clin. Exp. Ophthalmol. 250: 523-531.
53. Gibcus, J. H., L. P. Tan, G. Harms, R. N. Schakel, D. de Jong, T. Blokzijl, P. Möller, S. Poppema, B. J. Kroesen, and A. van den Berg. 2009. Hodgkin lymphoma cell lines are characterized by a specific miRNA expression profile. Neoplasia 11: 167-176.
54. Chen, S., Z. Wang, X. Dai, J. Pan, J. Ge, X. Han, Z. Wu, X. Zhou, and T. Zhao. 2013. Re-expression of microRNA-150 induces EBV-positive Burkitt lymphoma differentiation by modulating c-Myb in vitro. Cancer Sci. 104: 826-834.
55. Watanabe, A., H. Tagawa, J. Yamashita, K. Teshima, M. Nara, K. Iwamoto, M. Kume, Y. Kameoka, N. Takahashi, T. Nakagawa, et al. 2011. The role of microRNA-150 as a tumor suppressor in malignant lymphoma. Leukemia 25: 1324-1334.
56. Ito, M., K. Teshima, S. Ikeda, A. Kitadate, A. Watanabe, M. Nara, J. Yamashita, K. Ohshima, K. Sawada, and H. Tagawa. 2014. MicroRNA-150 inhibits tumor invasion and metastasis by targeting the chemokine receptor CCR6, in advanced cutaneous T-cell lymphoma. Blood 123: 1499-1511.
57. Wei, G., L. Wei, J. Zhu, C. Zang, J. Hu-Li, Z. Yao, K. Cui, Y. Kanno, T. Y. Roh, W. T. Watford, et al. 2009. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30: 155-167.
58. Quintana, A. M., Y. E. Zhou, J. J. Pena, J. P. O'Rourke, and S. A. Ness. 2011. Dramatic repositioning of c-Myb to different promoters during the cell cycle observed by combining cell sorting with chromatin immunoprecipitation. PLoS One 6: e17362.
59. Yin, Y., S. C. Choi, Z. Xu, D. J. Perry, H. Seay, B. P. Croker, E. S. Sobel, T. M. Brusko, and L. Morel. 2015. Normalization of CD4+ T cell metabolism reverses lupus. Sci. Transl. Med. 7: 274ra18.