MicroRNA-155 controls affinity-based selection by protecting c-MYC+ B cells from apoptosis

Journal of Clinical Investigation

Volumn 126, Issue 1, 2016, Pages 377-388

  Nakagawa, Rinako ^a   Leyland, Rebecca ^a   Meyer Hermann, Michael ^b,c   Lu, Dong ^a   Turner, Martin ^a   Arbore, Giuseppina ^a   Phan, Tri Giang ^d,e   Brink, Robert ^d,e   Vigorito, Elena ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^d GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA 155; JARID2 PROTEIN, MOUSE; MICRORNA; MIRN155 MICRORNA, MOUSE; MYC PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2;

ADOPTIVE TRANSFER; ANIMAL CELL; ANTIBODY AFFINITY; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CELL PROTECTION; CELL SELECTION; FLOW CYTOMETRY; GERMINAL CENTER; IMMUNOHISTOLOGY; MOUSE; NONHUMAN; ONCOGENE C MYC; PATHOGEN CLEARANCE; PRIORITY JOURNAL; SHEEP ERYTHROCYTE; SPLEEN CELL; ANIMAL; C57BL MOUSE; CELL SURVIVAL; PHYSIOLOGY;

ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CELL SURVIVAL; GERMINAL CENTER; MICE; MICE, INBRED C57BL; MICRORNAS; POLYCOMB REPRESSIVE COMPLEX 2; PROTO-ONCOGENE PROTEINS C-MYC;

EID: 84956678114     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI82914     Document Type: Article

References (50)

1. MacLennan IC. Germinal centers. Annu Rev Immunol. 1994;12:117-139.
2. Nieuwenhuis P, Opstelten D. Functional anatomy of germinal centers. Am J Anat. 1984;170(3):421-435.
3. Gitlin AD, Shulman Z, Nussenzweig MC. Clonal selection in the germinal centre by regulated proliferation and hypermutation. Nature. 2014;509(7502):637-640.
4. Victora GD, et al. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell. 2010;143(4):592-605.
5. Kepler TB, Perelson AS. Cyclic re-entry of germinal center B cells and the efficiency of affinity maturation. Immunol Today. 1993;14(8):412-415.
6. Meyer-Hermann M, Deutsch A, Or-Guil M. Recycling probability and dynamical properties of germinal center reactions. J Theor Biol. 2001;210(3):265-285.
7. Oprea M, Perelson AS. Somatic mutation leads to efficient affinity maturation when centrocytes recycle back to centroblasts. J Immunol. 1997;158(11):5155-5162.
8. Basso K, et al. BCL6 positively regulates AID and germinal center gene expression via repression of miR-155. J Exp Med. 2012;209(13):2455-2465.
9. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 2000;102(5):553-563.
10. Calado DP, et al. The cell-cycle regulator c-Myc is essential for the formation and maintenance of germinal centers. Nat Immunol. 2012;13(11):1092-1100.
11. Dominguez-Sola D, et al. The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat Immunol. 2012;13(11):1083-1091.
12. Rodriguez A, et al. Requirement of bic/ microRNA-155 for normal immune function. Science. 2007;316(5824):608-611.
13. Thai TH, et al. Regulation of the germinal center response by microRNA-155. Science. 2007;316(5824):604-608.
14. Vigorito E, et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity. 2007;27(6):847-859.
15. Lu D, et al. The miR-155-PU.1 axis acts on Pax5 to enable efficient terminal B cell differentiation. J Exp Med. 2014;211(11):2183-2198.
16. Phan TG, et al. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J Exp Med. 2003;197(7):845-860.
17. Chan TD, Gatto D, Wood K, Camidge T, Basten A, Brink R. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J Immunol. 2009;183(5):3139-3149.
18. Paus D, Phan TG, Chan TD, Gardam S, Basten A, Brink R. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J Exp Med. 2006;203(4):1081-1091.
19. Victora GD, Dominguez-Sola D, Holmes AB, Deroubaix S, Dalla-Favera R, Nussenzweig MC. Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas. Blood. 2012;120(11):2240-2248.
20. Meyer-Hermann M, Mohr E, Pelletier N, Zhang Y, Victora GD, Toellner KM. A theory of germinal center B cell selection, division, and exit. Cell Rep. 2012;2(1):162-174.
21. Huang CY, Bredemeyer AL, Walker LM, Bassing CH, Sleckman BP. Dynamic regulation of c-Myc proto-oncogene expression during lymphocyte development revealed by a GFP-c-Myc knock-in mouse. Eur J Immunol. 2008;38(2):342-349.
22. Phan TG, et al. High affinity germinal center B cells are actively selected into the plasma cell compartment. J Exp Med. 2006;203(11):2419-2424.
23. Meyer-Hermann M. Overcoming the dichotomy of quantity and quality in antibody responses. J Immunol. 2014;193(11):5414-5419.
24. Zhang Y, et al. Germinal center B cells govern their own fate via antibody feedback. J Exp Med. 2013;210(3):457-464.
25. Fabani MM, et al. Efficient inhibition of miR-155 function in vivo by peptide nucleic acids. Nucleic Acids Res. 2010;38(13):4466-4475.
26. O'Connell RM, et al. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med. 2008;205(3):585-594.
27. Takeuchi T, et al. Gene trap capture of a novel mouse gene, jumonji, required for neural tube formation. Genes Dev. 1995;9(10):1211-1222.
28. Bolisetty MT, Dy G, Tam W, Beemon KL. Reticuloendotheliosis virus strain T induces miR-155, which targets JARID2 and promotes cell survival. J Virol. 2009;83(23):12009-12017.
29. Dahlke C, et al. A microRNA encoded by Kaposi sarcoma-associated herpesvirus promotes B-cell expansion in vivo. PLoS One. 2012;7(11):e49435.
30. Vigorito E, Kohlhaas S, Lu D, Leyland R. miR-155: an ancient regulator of the immune system. Immunol Rev. 2013;253(1):146-157.
31. Tan LP, et al. miRNA profiling of B-cell subsets: specific miRNA profile for germinal center B cells with variation between centroblasts and centrocytes. Lab Invest. 2009;89(6):708-716.
32. Pasini D, et al. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature. 2010;464(7286):306-310.
33. Takeuchi T, Watanabe Y, Takano-Shimizu T, Kondo S. Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev Dyn. 2006;235(9):2449-2459.
34. Peng JC, et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell. 2009;139(7):1290-1302.
35. Shen X, et al. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell. 2009;139(7):1303-1314.
36. Caganova M, et al. Germinal center dysregulation by histone methyltransferase EZH2 promotes lymphomagenesis. J Clin Invest. 2013;123(12):5009-5022.
37. Askew DS, Ashmun RA, Simmons BC, Cleveland JL. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene. 1991;6(10):1915-1922.
38. Evan GI, et al. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 1992;69(1):119-128.
39. Shi Y, Glynn JM, Guilbert LJ, Cotter TG, Bissonnette RP, Green DR. Role for c-myc in activation-induced apoptotic cell death in T cell hybridomas. Science. 1992;257(5067):212-214.
40. Clurman BE, Hayward WS. Multiple proto-oncogene activations in avian leukosis virus-induced lymphomas: evidence for stage-specific events. Mol Cell Biol. 1989;9(6):2657-2664.
41. Tam W, Hughes SH, Hayward WS, Besmer P. Avian bic, a gene isolated from a common retroviral site in avian leukosis virus-induced lymphomas that encodes a noncoding RNA, cooperates with c-myc in lymphomagenesis and erythroleukemogenesis. J Virol. 2002;76(9):4275-4286.
42. Sabò A, et al. Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis. Nature. 2014;511(7510):488-492.
43. Alizadeh AA, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403(6769):503-511.
44. Hu S, et al. MYC/BCL2 protein coexpression contributes to the inferior survival of activated B-cell subtype of diffuse large B-cell lymphoma and demonstrates high-risk gene expression signatures: A report from The International DLBCL Rituximab-CHOP Consortium Program. Blood. 2013;121(20):4021-4031.
45. Johnson NA, et al. Concurrent expression of MYC and BCL2 in diffuse large B-cell lymphoma treated with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone. J Clin Oncol. 2012;30(28):3452-3459.
46. Eis PS, et al. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci U S A. 2005;102(10):3627-3632.
47. Kluiver J, et al. BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. J Pathol. 2005;207(2):243-249.
48. Shaffer AL. Pathogenesis of human B cell lymphomas. Annu Rev Immunol. 2012;30:565-610.
49. Goodnow CC, et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature. 1988;334(6184):676-682.
50. Kaji T, et al. Distinct cellular pathways select germline-encoded and somatically mutated antibodies into immunological memory. J Exp Med. 2012;209(11):2079-2097.