Innate immunodeficiency following genetic ablation of Mcl1 in natural killer cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Sathe, Priyanka ^a,b   Delconte, Rebecca B ^a,b   Souza Fonseca Guimaraes, Fernando ^c,d   Seillet, Cyril ^a,b   Chopin, Michael ^a,b   Vandenberg, Cassandra J ^a,b   Rankin, Lucille C ^a,b   Mielke, Lisa A ^a,b   Vikstrom, Ingela ^a,b   Kolesnik, Tatiana B ^a,b   Nicholson, Sandra E ^a,b   Vivier, Eric ^e   Smyth, Mark J ^c,d   Nutt, Stephen L ^a,b   Glaser, Stefan P ^a,b   Strasser, Andreas ^a,b   Belz, Gabrielle T ^a,b   Carotta, Sebastian ^a,b   Huntington, Nicholas D ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 6; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; PROTEIN MCL 1; STAT5 PROTEIN; CYTOKINE; MCL1 PROTEIN, MOUSE;

CYTOLOGY; GENETIC ANALYSIS; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOASSAY;

3' UNTRANSLATED REGION; ALLOTRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; GENE DELETION; GENETIC ABLATION; IMMUNE DEFICIENCY; INNATE IMMUNITY; LYMPHOCYTOPENIA; MALE; MELANOMA METASTASIS; MITOCHONDRIAL MEMBRANE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN PHOSPHORYLATION; SEPSIS; ANIMAL; APOPTOSIS; C57BL MOUSE; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GENETICS; IMMUNOPATHOLOGY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE DELETION; IMMUNE SYSTEM DISEASES; IMMUNITY, INNATE; INTERLEUKIN-15; KILLER CELLS, NATURAL; LYMPHOPENIA; MALE; MICE; MICE, INBRED C57BL; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

EID: 84907377182     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5539     Document Type: Article

References (65)

1. Spits, H. &Cupedo, T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 30, 647-675 (2012).
2. Spits, H. et al. Innate lymphoid cells-A proposal for uniform nomenclature. Nat. Rev. Immunol. 13, 145-149 (2013).
3. Huntington, N. D., Vosshenrich, C. A. &Di Santo, J. P. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat. Rev. Immunol. 7, 703-714 (2007). (Pubitemid 47327395)
4. Lodolce, J. P. et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9, 669-676 (1998). (Pubitemid 28557595)
5. Kennedy, M. K. et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191, 771-780 (2000).
6. Suzuki, H., Duncan, G. S., Takimoto, H. &Mak, T. W. Abnormal development of intestinal intraepithelial lymphocytes and peripheral natural killer cells in mice lacking the IL-2 receptor beta chain. J. Exp. Med. 185, 499-505 (1997). (Pubitemid 27078368)
7. Carotta, S., Pang, S. H., Nutt, S. L. &Belz, G. T. Identification of the earliest NK-cell precursor in the mouse BM. Blood 117, 5449-5452 (2011).
8. Di Santo, J. P. Natural killer cell developmental pathways: a question of balance. Annu. Rev. Immunol. 24, 257-286 (2006).
9. Dubois, S., Mariner, J., Waldmann, T. A. &Tagaya, Y. IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 17, 537-547 (2002). (Pubitemid 35351500)
10. Cooper, M. A. et al. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 100, 3633-3638 (2002). (Pubitemid 35303933)
11. Koka, R. et al. Interleukin (IL)-15R[alpha]-deficient natural killer cells survive in normal but not IL-15R[alpha]-deficient mice. J. Exp. Med. 197, 977-984 (2003). (Pubitemid 36523195)
12. Sandau, M. M., Schluns, K. S., Lefrancois, L. &Jameson, S. C. Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15R alpha by the same cells. J. Immunol. 173, 6537-6541 (2004). (Pubitemid 39541036)
13. Burkett, P. R. et al. Coordinate expression and trans presentation of interleukin (IL)-15Ralpha and IL-15 supports natural killer cell and memory CD8 T cell homeostasis. J. Exp. Med. 200, 825-834 (2004). (Pubitemid 39362919)
14. Huntington, N. D. et al. Interleukin 15-mediated survival of natural killer cells is determined by interactions among Bim, Noxa and Mcl-1. Nat. Immunol. 8, 856-863 (2007). (Pubitemid 47103041)
15. Armant, M., Delespesse, G. &Sarfati, M. IL-2 and IL-7 but not IL-12 protect natural killer cells from death by apoptosis and up-regulate bcl-2 expression. Immunology 85, 331-337 (1995).
16. Jiang, S., Munker, R. &Andreeff, M. Bcl-2 is expressed in human natural killer cells and is regulated by interleukin-2. Nat. Immun. 15, 312-317 (1996).
17. Ranson, T. et al. IL-15 is an essential mediator of peripheral NK-cell homeostasis. Blood 101, 4887-4893 (2003). (Pubitemid 36857750)
18. Zheng, X. et al. Bcl-xL is associated with the anti-apoptotic effect of IL-15 on the survival of CD56(dim) natural killer cells. Mol. Immunol. 45, 2559-2569 (2008).
19. Hodge, D. L. et al. Interleukin-15 enhances proteasomal degradation of bid in normal lymphocytes: implications for large granular lymphocyte leukemias. Cancer Res. 69, 3986-3994 (2009).
20. Huntington, N. D. et al. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J. Exp. Med. 206, 25-34 (2009).
21. Dijkers, P. F., Medema, R. H., Lammers, J. W., Koenderman, L. &Coffer, P. J. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr. Biol. 10, 1201-1204 (2000).
22. Opferman, J. T. et al. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426, 671-676 (2003). (Pubitemid 38009376)
23. Pierson, W. et al. Antiapoptotic Mcl-1 is critical for the survival and nichefilling capacity of Foxp3() regulatory T cells. Nat. Immunol. 14, 959-965 (2013).
24. Perciavalle, R. M. et al. Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nat. Cell Biol. 14, 575-583 (2012).
25. Vikstrom, I. et al. Mcl-1 is essential for germinal center formation and B cell memory. Science 330, 1095-1099 (2010).
26. Glaser, S. P. et al. Anti-apoptotic Mcl-1 is essential for the development and sustained growth of acute myeloid leukemia. Genes Dev. 26, 120-125 (2012).
27. Huntington, N. D. et al. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J. Immunol. 178, 4764-4770 (2007). (Pubitemid 46595257)
28. Hayakawa, Y. &Smyth, M. J. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176, 1517-1524 (2006). (Pubitemid 43134295)
29. Kim, S. et al. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3, 523-528 (2002). (Pubitemid 34662303)
30. Opferman, J. T. et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307, 1101-1104 (2005). (Pubitemid 40262114)
31. Gordon, S. M. et al. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36, 55-67 (2012).
32. Narni-Mancinelli, E. et al. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl Acad. Sci. USA 108, 18324-18329 (2011).
33. Wagner, K. U. et al. Conditional deletion of the Bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development 127, 4949-4958 (2000).
34. Soldaini, E. et al. DNA binding site selection of dimeric and tetrameric Stat5 proteins reveals a large repertoire of divergent tetrameric Stat5a binding sites. Mol. Cell Biol. 20, 389-401 (2000). (Pubitemid 30002580)
35. Leonard, W. J. &O'Shea, J. J. Jaks and STATs: biological implications. Annu. Rev. Immunol. 16, 293-322 (1998). (Pubitemid 28183367)
36. Verdier, F. et al. Proteasomes regulate erythropoietin receptor and signal transducer and activator of transcription 5 (STAT5) activation. Possible involvement of the ubiquitinated Cis protein. J. Biol. Chem. 273, 28185-28190 (1998). (Pubitemid 28496116)
37. Campbell, K. J. et al. Elevated Mcl-1 perturbs lymphopoiesis, promotes transformation of hematopoietic stem/progenitor cells, and enhances drug resistance. Blood 116, 3197-3207 (2010).
38. Karre, K. NK cells, MHC class I molecules and the missing self. Scand. J. Immunol. 55, 221-228 (2002). (Pubitemid 34310025)
39. Cerwenka, A. &Lanier, L. L. Natural killer cells, viruses and cancer. Nat. Rev. Immunol. 1, 41-49 (2001). (Pubitemid 33741974)
40. Lotzova, E., Savary, C. A. &Pollack, S. B. Prevention of rejection of allogeneic bone marrow transplants by NK 1.1 antiserum. Transplantation 35, 490-494 (1983). (Pubitemid 13089923)
41. Murphy, W. J., Kumar, V. &Bennett, M. Acute rejection of murine bone marrow allografts by natural killer cells and T cells. Differences in kinetics and target antigens recognized. J. Exp. Med. 166, 1499-1509 (1987). (Pubitemid 18051439)
42. Nemzek, J. A., Hugunin, K. M. &Opp, M. R. Modeling sepsis in the laboratory: merging sound science with animal well-being. Comp. Med. 58, 120-128 (2008).
43. Dejager, L., Pinheiro, I., Dejonckheere, E. &Libert, C. Cecal ligation and puncture: the gold standard model for polymicrobial sepsis? Trends Microbiol. 19, 198-208 (2011).
44. Rinkevich, B. Primitive immune systems: are your ways my ways? Immunol. Rev. 198, 25-35 (2004). (Pubitemid 38406933)
45. Khalturin, K., Panzer, Z., Cooper, M. D. &Bosch, T. C. Recognition strategies in the innate immune system of ancestral chordates. Mol. Immunol. 41, 1077-1087 (2004). (Pubitemid 39345389)
46. Waldmann, T. A. &Tagaya, Y. The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu. Rev. Immunol. 17, 19-49 (1999). (Pubitemid 29241118)
47. Huntington, N. D. The unconventional expression of IL-15 and its role in NK cell homeostasis. Immunol. Cell Biol. 92, 210-213 (2014).
48. Opferman, J. T. Apoptosis in the development of the immune system. Cell Death Differ. 15, 234-242 (2008).
49. Strasser, A. The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5, 189-200 (2005). (Pubitemid 40364821)
50. Eckelhart, E. et al. A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development. Blood 117, 1565-1573 (2011).
51. Imada, K. et al. Stat5b is essential for natural killer cell-mediated proliferation and cytolytic activity. J. Exp. Med. 188, 2067-2074 (1998). (Pubitemid 28562523)
52. Wenzel, S. S. et al. MCL1 is deregulated in subgroups of diffuse large B-cell lymphoma. Leukemia 27, 1381-1390 (2013).
53. Abdulghani, J. et al. Sorafenib sensitizes solid tumors to Apo2L/TRAIL and Apo2L/TRAIL receptor agonist antibodies by the Jak2-Stat3-Mcl1 axis. PLoS ONE 8, e75414 (2013).
54. Zeng, R. et al. The molecular basis of IL-21-mediated proliferation. Blood 109, 4135-4142 (2007). (Pubitemid 46743374)
55. Kondo, M., Weissman, I. L. &Akashi, K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91, 661-672 (1997). (Pubitemid 27513657)
56. Malin, S. et al. Role of STAT5 in controlling cell survival and immunoglobulin gene recombination during pro-B cell development. Nat. Immunol. 11, 171-179 (2010).
57. Chiossone, L. et al. Maturation of mouse NK cells is a 4-stage developmental program. Blood 113, 5488-5496 (2009).
58. Smyth, M. J. &Kelly, J. M. Accessory function for NK1.1 natural killer cells producing interferon-gamma in xenospecific cytotoxic T lymphocyte differentiation. Transplantation 68, 840-843 (1999). (Pubitemid 29468203)
59. Colucci, F. et al. Dissecting NK cell development using a novel alymphoid mouse model: investigating the role of the c-abl proto-oncogene in murine NK cell differentiation. J. Immunol. 162, 2761-2765 (1999). (Pubitemid 29309300)
60. Srinivas, S. et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4 (2001).
61. Gilfillan, S. et al. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J. Exp. Med. 205, 2965-2973 (2008).
62. Sun, K., Li, M., Sayers, T. J., Welniak, L. A. &Murphy, W. J. Differential effects of donor T-cell cytokines on outcome with continuous bortezomib administration after allogeneic bone marrow transplantation. Blood 112, 1522-1529 (2008).
63. Huntington, N. D., Xu, Y., Nutt, S. L. &Tarlinton, D. M. A requirement for CD45 distinguishes Ly49D-mediated cytokine and chemokine production from killing in primary natural killer cells. J. Exp. Med. 201, 1421-1433 (2005). (Pubitemid 40664086)
64. Rittirsch, D., Huber-Lang, M. S., Flierl, M. A. &Ward, P. A. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 4, 31-36 (2009).
65. Peperzak, V. et al. Mcl-1 is essential for the survival of plasma cells. Nat. Immunol. 14, 290-297 (2013).