Conditional knockdown of BCL2A1 reveals rate-limiting roles in BCR-dependent B-cell survival

Cell Death and Differentiation

Volumn 23, Issue 4, 2016, Pages 628-639

  Sochalska, M ^a   Ottina, E ^a,c   Tuzlak, S ^a   Herzog, S ^a   Herold, M ^b   Villunger, A ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; BCL2 RELATED PROTEIN A1; BIM PROTEIN; BRUTON TYROSINE KINASE; DOXYCYCLINE; GRANULOCYTE COLONY STIMULATING FACTOR; PROTEIN KINASE SYK; SHORT HAIRPIN RNA; AGAMMAGLOBULINAEMIA TYROSINE KINASE; BCL2-RELATED PROTEIN A1; LYMPHOCYTE ANTIGEN RECEPTOR; MINOR HISTOCOMPATIBILITY ANTIGEN; PROTEIN BCL 2; PROTEIN TYROSINE KINASE; SYK PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL LOSS; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; GENE SILENCING; MOUSE; MYELOPOIESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SPLEEN CELL; ANIMAL; GENETICS; HUMAN; METABOLISM;

ANIMALS; B-LYMPHOCYTES; CELL SURVIVAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MINOR HISTOCOMPATIBILITY ANTIGENS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, ANTIGEN, B-CELL; SYK KINASE;

EID: 84960939928     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.130     Document Type: Article

References (52)

1. Czabotar PE, Lessene G, Strasser A, Adams JM. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 2014; 15: 49-63.
2. Tait SW, Green DR. Mitochondrial regulation of cell death. Cold Spring Harb Perspect Biol 2013; 5.
3. Sochalska M, Tuzlak S, Egle A, Villunger A. Lessons from gain-and loss-of-function models of pro-survival Bcl2 family proteins: implications for targeted therapy. FEBS J 2015; 282: 834-849.
4. Luciano F, Krajewska M, Ortiz-Rubio P, Krajewski S, Zhai D, Faustin B et al. Nur77 converts phenotype of Bcl-B, an antiapoptotic protein expressed in plasma cells and myeloma. Blood 2007; 109: 3849-3855.
5. Merino R, Ding L, Veis DJ, Korsmeyer SJ, Nunez G. Developmental regulation of the Bcl-2 protein and susceptibility to cell death in B lymphocytes. EMBO J 1994; 13: 683-691.
6. Nakayama K, Nakayama K, Negishi I, Kuida K, Shinkai Y, Louie MC et al. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science 1993; 261: 1584-1588.
7. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993; 75: 229-240.
8. Grillot DA, Merino R, Nunez G. Bcl-XL displays restricted distribution during T cell development and inhibits multiple forms of apoptosis but not clonal deletion in transgenic mice. J Exp Med 1995; 182: 1973-1983.
9. Dzhagalov I, Dunkle A, He YW. The anti-apoptotic Bcl-2 family member Mcl-1 promotes T lymphocyte survival at multiple stages. J Immunol 2008; 181: 521-528.
10. Opferman JT. Life and death during hematopoietic differentiation. Curr Opin Immunol 2007; 19: 497-502.
11. Lin EY, Orlofsky A, Berger MS, Prystowsky MB. Characterization of A1, a novel hemopoieticspecific early-response gene with sequence similarity to bcl-2. J Immunol 1993; 151: 1979-1988.
12. Herold MJ, Zeitz J, Pelzer C, Kraus C, Peters A, Wohlleben G et al. The stability and antiapoptotic function of A1 are controlled by its C terminus. J Biol Chem 2006; 281: 13663-13671.
13. Chuang PI, Yee E, Karsan A, Winn RK, Harlan JM. A1 is a constitutive and inducible Bcl-2 homologue in mature human neutrophils. Biochem Biophys Res Commun 1998; 249: 361-365.
14. Xiang Z, Ahmed AA, Moller C, Nakayama K, Hatakeyama S, Nilsson G. Essential role of the prosurvival bcl-2 homologue A1 in mast cell survival after allergic activation. J Exp Med 2001; 194: 1561-1569.
15. Ottina E, Lyberg K, Sochalska M, Villunger A, Nilsson GP. Knockdown of the antiapoptotic bcl-2 family member a1/bfl-1 protects mice from anaphylaxis. J Immunol 2015; 194: 1316-1322.
16. Ekoff M, Lyberg K, Krajewska M, Arvidsson M, Rak S, Reed JC et al. Anti-apoptotic BFL-1 is the major effector in activation-induced human mast cell survival. PLoS One 2012; 7: e39117.
17. Verschelde C, Walzer T, Galia P, Biémont MC, Quemeneur L, Revillard JP et al. A1/Bfl-1 expression is restricted to TCR engagement in T lymphocytes. Cell Death Differ 2003; 10: 1059-1067.
18. Trescol-Biemont MC, Verschelde C, Cottalorda A, Bonnefoy-Berard N. Regulation of A1/Bfl-1 expression in peripheral splenic B-cells. Biochimie 2004; 86: 287-294.
19. Wen R, Chen Y, Xue L, Schuman J, Yang S, Morris SW et al. Phospholipase Cgamma2 provides survival signals via Bcl2 and A1 in different subpopulations of B-cells. J Biol Chem 2003; 278: 43654-43662.
20. Gonzalez J, Orlofsky A, Prystowsky MB. A1 is a growth-permissive antiapoptotic factor mediating postactivation survival in T cells. Blood 2003; 101: 2679-2685.
21. Ottina E, Tischner D, Herold MJ, Villunger A. A1/Bfl-1 in leukocyte development and cell death. Exp Cell Res 2012; 318: 1291-1303.
22. Medina-Echeverz J, Haile LA, Zhao F, Gamrekelashvili J, Ma C, Métais JY et al. IFN-gamma regulates survival and function of tumor-induced CD11b+ Gr-1high myeloid derived suppressor cells by modulating the anti-apoptotic molecule Bcl2a1. Eur J Immunol 2014; 44: 2457-2467.
23. Vogler M. BCL2A1: the underdog in the BCL2 family. Cell Death Differ 2012; 19: 67-74.
24. Vogler M, Butterworth M, Majid A, Walewska RJ, Sun XM, Dyer MJ et al. Concurrent upregulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood 2009; 113: 4403-4413.
25. Hatakeyama S, Hamasaki A, Negishi I, Loh DY, Sendo F, Nakayama K et al. Multiple gene duplication and expression of mouse bcl-2-related genes, A1. Int Immunol 1998; 10: 631-637.
26. Hamasaki A, Sendo F, Nakayama K, Ishida N, Negishi I, Nakayama K et al. Accelerated neutrophil apoptosis in mice lacking A1-a, a subtype of the bcl-2-related A1 gene. J Exp Med 1998; 188: 1985-1992.
27. Oberdoerffer P, Kanellopoulou C, Heissmeyer V, Paeper C, Borowski C, Aifantis I et al. Efficiency of RNA interference in the mouse hematopoietic system varies between cell types and developmental stages. Mol Cell Biol 2005; 25: 3896-3905.
28. Ottina E, Grespi F, Tischner D, Soratroi C, Geley S, Ploner A et al. Targeting antiapoptotic A1/Bfl-1 by in vivo RNAi reveals multiple roles in leukocyte development in mice. Blood 2012; 119: 6032-6042.
29. Kim WI, Wiesner SM, Largaespada DA. Vav promoter-tTA conditional transgene expression system for hematopoietic cells drives high level expression in developing B and T cells. Exp Hematol 2007; 35: 1231-1239.
30. Takiguchi M, Dow LE, Prier JE, Carmichael CL, Kile BT, Turner SJ et al. Variability of inducible expression across the hematopoietic system of tetracycline transactivator transgenic mice. PLoS One 2013; 8: e54009.
31. Premsrirut PK, Dow LE, Kim SY, Camiolo M, Malone CD, Miething C et al. A rapid and scalable system for studying gene function in mice using conditional RNA interference. Cell 2011; 145: 145-158.
32. Kuss AW, Knodel M, Berberich-Siebelt F, Lindemann D, Schimpl A, Berberich I. A1 expression is stimulated by CD40 in B-cells and rescues WEHI 231 cells from anti-IgMinduced cell death. Eur J Immunol 1999; 29: 3077-3088.
33. Monroe JG, Bannish G, Fuentes-Panana EM, King LB, Sandel PC, Chung J et al. Positive and negative selection during B lymphocyte development. Immunol Res 2003; 27: 427-442.
34. Dow LE, Nasr Z, Saborowski M, Ebbesen SH, Manchado E, Tasdemir N et al. Conditional reverse tet-transactivator mouse strains for the efficient induction of TRE-regulated transgenes in mice. PLoS One 2014; 9: e95236.
35. Liu GJ, Cimmino L, Jude JG, Hu Y, Witkowski MT, McKenzie MD et al. Pax5 loss imposes a reversible differentiation block in B-progenitor acute lymphoblastic leukemia. Genes Dev 2014; 28: 1337-1350.
36. Chen C, Liu Y, Rappaport AR, Kitzing T, Schultz N, Zhao Z et al. MLL3 is a haploinsufficient 7q tumor suppressor in acute myeloid leukemia. Cancer Cell 2014; 25: 652-665.
37. Bouillet P, Robati M, Bath M, Strasser A. Polycystic kidney disease prevented by transgenic RNA interference. Cell Death Differ 2005; 12: 831-833.
38. Mandal M, Borowski C, Palomero T, Ferrando AA, Oberdoerffer P, Meng F et al. The BCL2A1 gene as a pre-T cell receptor-induced regulator of thymocyte survival. J Exp Med 2005; 201: 603-614.
39. Lee HW, Park SJ, Choi BK, Kim HH, Nam KO, Kwon BS. 4-1BB promotes the survival of CD8+ T lymphocytes by increasing expression of Bcl-xL and Bfl-1. J Immunol 2002; 169: 4882-4888.
40. Tomayko MM, Cancro MP. Long-lived B-cells are distinguished by elevated expression of A1. J Immunol 1998; 160: 107-111.
41. Schiemann B, Gommerman JL, Vora K, Cachero TG, Shulga-Morskaya S, Dobles M et al. An essential role for BAFF in the normal development of B-cells through a BCMAindependent pathway. Science 2001; 293: 2111-2114.
42. Lentz VM, Cancro MP, Nashold FE, Hayes CE. Bcmd governs recruitment of new B-cells into the stable peripheral B-cell pool in the A/WySnJ mouse. J Immunol 1996; 157: 598-606.
43. Kraus M, Pao LI, Reichlin A, Hu Y, Canono B, Cambier JC et al. Interference with immunoglobulin (Ig)alpha immunoreceptor tyrosine-based activation motif (ITAM) phosphorylation modulates or blocks B-cell development, depending on the availability of an Igbeta cytoplasmic tail. J Exp Med 2001; 194: 455-469.
44. Yamazaki T, Kurosaki T. Contribution of BCAP to maintenance of mature B-cells through c-Rel. Nat Immunol 2003; 4: 780-786.
45. Grumont RJ, Rourke IJ, O'Reilly LA, Strasser A, Miyake K, Sha W et al. B lymphocytes differentially use the Rel and nuclear factor kappaB1 (NF-kappaB1) transcription factors to regulate cell cycle progression and apoptosis in quiescent and mitogen-activated cells. J Exp Med 1998; 187: 663-674.
46. Herzog S, Reth M, Jumaa H. Regulation of B-cell proliferation and differentiation by pre-Bcell receptor signalling. Nat Rev Immunol 2009; 9: 195-205.
47. Goodnow CC, Crosbie J, Adelstein S, Lavoie TB, Smith-Gill SJ, Brink RA et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 1988; 334: 676-682.
48. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, Schneider P et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 1999; 190: 1697-1710.
49. Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Köntgen F et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 1999; 286: 1735-1738.
50. Villunger A, Michalak EM, Coultas L, Müllauer F, Böck G, Ausserlechner MJ et al. p53-and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003; 302: 1036-1038.
51. Ranger AM, Zha J, Harada H, Datta SR, Danial NN, Gilmore AP et al. Bad-deficient mice develop diffuse large B-cell lymphoma. Proc Natl Acad Sci USA 2003; 100: 9324-9329.
52. Lang MJ, Brennan MS, O'Reilly LA, Ottina E, Czabotar PE, Whitlock E et al. Characterisation of a novel A1-specific monoclonal antibody. Cell Death Dis 2014; 5: e1553.