Characterisation of mice lacking all functional isoforms of the pro-survival BCL-2 family member A1 reveals minor defects in the haematopoietic compartment

Cell Death and Differentiation

Volumn 24, Issue 3, 2017, Pages 534-545

  Schenk, Robyn L ^a,b   Tuzlak, Selma ^b,c   Carrington, Emma M ^a,b   Zhan, Yifan ^a,b   Heinzel, Susanne ^a,b   Teh, Charis E ^a   Gray, Daniel H ^a,b   Tai, Lin ^a   Lew, Andrew M ^a,b   Villunger, Andreas ^c,d   Strasser, Andreas ^a,b   Herold, Marco J ^a,b  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^d TYROLEAN CANCER RESEARCH INSTITUTE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; HERMES ANTIGEN; L SELECTIN; PROTEIN BCL 2; PROTEIN BCL 2 A1A; PROTEIN BCL 2 A1B; PROTEIN BCL 2 A1D; PROTEIN BCL XL; PROTEIN MCL 1; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; BCL2-RELATED PROTEIN A1; ISOPROTEIN; MINOR HISTOCOMPATIBILITY ANTIGEN; PROTEIN BCL X; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MAST CELL; CD4+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; EMBRYO; FEMALE; GAMMA DELTA T LYMPHOCYTE; GENE LOCUS; HEMATOPOIESIS; IN VITRO STUDY; LOXP SITE; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; B LYMPHOCYTE; BONE MARROW; C57BL MOUSE; CYTOLOGY; DEFICIENCY; GENETICS; INTRAEPITHELIAL LYMPHOCYTE; KNOCKOUT MOUSE; METABOLISM; RNA INTERFERENCE; SPLEEN; THYMUS;

ANIMALS; B-LYMPHOCYTES; BCL-X PROTEIN; BONE MARROW; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; INTRAEPITHELIAL LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MINOR HISTOCOMPATIBILITY ANTIGENS; MOUSE EMBRYONIC STEM CELLS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPLEEN; THYMUS GLAND;

EID: 85010894760     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.156     Document Type: Article

References (56)

1. Strasser A, O'Connor L, Dixit VM. Apoptosis signaling. Annu Rev Biochem 2000; 69: 217-245
2. Kamada S, Shimono A, Shinto Y, Tsujimura T, Takahashi T, Noda T, et al. bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation and distorted small intestine. Cancer Res 1995; 55: 354-359
3. 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
4. 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
5. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K, et al. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 1995; 267: 1506-1510
6. Mason KD, Carpinelli MR, Fletcher JI, Collinge JE, Hilton AA, Ellis S, et al. Programmed anuclear cell death delimits platelet life span. Cell 2007; 128: 1173-1186
7. Wagner KU, Claudio E, Rucker EB 3rd, Riedlinger G, Broussard C, Schwartzberg PL, et al. Conditional deletion of the Bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development 2000; 127: 4949-4958
8. Rinkenberger JL, Horning S, Klocke B, Roth K, Korsmeyer SJ. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev 2000; 14: 23-27
9. Arbour N, Vanderluit JL, Le Grand JN, Jahani-Asl A, Ruzhynsky VA, Cheung EC, et al. Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J Neurosci 2008; 28: 6068-6078
10. Opferman JT, Letai A, Beard C, Sorcinelli MD, Ong CC, Korsmeyer SJ. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003; 426: 671-676
11. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K, et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 2005; 307: 1101-1104
12. Thomas RL, Roberts DJ, Kubli DA, Lee Y, Quinsay MN, Owens JB, et al. Loss of MCL-1 leads to impaired autophagy and rapid development of heart failure. Genes Dev 2013; 27: 1365-1377
13. Wang X, Bathina M, Lynch J, Koss B, Calabrese C, Frase S, et al. Deletion of MCL-1 causes lethal cardiac failure and mitochondrial dysfunction. Genes Dev 2013; 27: 1351-1364
14. Peperzak V, Vikstrom I, Walker J, Glaser SP, LePage M, Coquery CM, et al. Mcl-1 is essential for the survival of plasma cells. Nat Immunol 2013; 14: 290-297
15. Vikstrom I, Carotta S, Luthje K, Peperzak V, Jost PJ, Glaser S, et al. Mcl-1 is essential for germinal center formation and B cell memory. Science 2010; 330: 1095-1099
16. Print CG, Loveland KL, Gibson L, Meehan T, Stylianou A, Wreford N, et al. Apoptosis regulator bcl-w is essential for spermatogenesis but appears otherwise redundant. Proc Natl Acad Sci USA 1998; 95: 12424-12431
17. Ross AJ, Waymire KG, Moss JE, Parlow AF, Skinner MK, Russell LD, et al. Testicular degeneration in Bclw-deficient mice. Nat Genet 1998; 18: 251-256
18. 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
19. Choi SS, Park IC, Yun JW, Sung YC, Hong SI, Shin HS. A novel Bcl-2 related gene, Bfl-1, is overexpressed in stomach cancer and preferentially expressed in bone marrow. Oncogene 1995; 11: 1693-1698
20. Lin EY, Orlofsky A, Wang HG, Reed JC, Prystowsky MB. A1, a Bcl-2 family member, prolongs cell survival and permits myeloid differentiation. Blood 1996; 87: 983-992
21. Vogler M. BCL2A1: the underdog in the BCL2 family. Cell Death Differ 2012; 19: 67-74
22. Grumont RJ, Rourke IJ, Gerondakis S. Rel-dependent induction of A1 transcription is required to protect B cells from antigen receptor ligation-induced apoptosis. Genes Dev 1999; 13: 400-411
23. Wang CY, Guttridge DC, Mayo MW, Baldwin AS Jr. NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol Cell Biol 1999; 19: 5923-5929
24. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev 1999; 13: 382-387
25. Duriez PJ, Wong F, Dorovini-Zis K, Shahidi R, Karsan A. A1 functions at the mitochondria to delay endothelial apoptosis in response to tumor necrosis factor. J Biol Chem 2000; 275: 18099-18107
26. 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
27. Ottina E, Tischner D, Herold MJ, Villunger A. A1/Bfl-1 in leukocyte development and cell death. Exp Cell Res 2012; 318: 1291-1303
28. 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
29. 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
30. 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
31. 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
32. Sochalska M, Ottina E, Tuzlak S, Herzog S, Herold M, Villunger A. Conditional knockdown of BCL2A1 reveals rate-limiting roles in BCR-dependent B cell survival. Cell Death Differ 2016; 23: 628-639
33. Carrington EM, Zhang JG, Sutherland RM, Vikstrom IB, Brady JL, Soo P, et al. Prosurvival Bcl-2 family members reveal a distinct apoptotic identity between conventional and plasmacytoid dendritic cells. Proc Natl Acad Sci USA 2015; 112: 4044-4049
34. 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
35. Venigalla RK, McGuire VA, Clarke R, Patterson-Kane JC, Najafov A, Toth R, et al. PDK1 regulates VDJ recombination, cell-cycle exit and survival during B cell development. EMBO J 2013; 32: 1008-1022
36. 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
37. 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
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. Verschelde C, Michonneau D, Trescol-Biemont MC, Berberich I, Schimpl A, Bonnefoy-Berard N. Overexpression of the antiapoptotic protein A1 promotes the survival of double positive thymocytes awaiting positive selection. Cell Death Differ 2006; 13: 1213-1221
40. Gonzalez J, Orlofsky A, Prystowsky MB. A1 is a growth-permissive antiapoptotic factor mediating postactivation survival in T cells. Blood 2003; 101: 2679-2685
41. Verschelde C, Walzer T, Galia P, Biemont 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
42. Vier J, Groth M, Sochalska M, Kirschnek S. The anti-apoptotic Bcl-2 family protein A1/Bfl-1 regulates neutrophil survival and homeostasis and is controlled via PI3K and JAK/STAT signaling. Cell Death Dis 2016; 7: e2103
43. Koenen P, Heinzel S, Carrington EM, Happo L, Alexander WS, Zhang JG, et al. Mutually exclusive regulation of T cell survival by IL-7R and antigen receptor-induced signals. Nat Commun 2013 4: 1735
44. Tuzlak S, Schenk RL, Vasanthakumar A, Preston SP, Haschka MD, Zotos D, et al. The BCL-2 pro-survival protein A1 is dispensable for T cell homeostasis on viral infection Cell Death Diff 2016 (in press; doi: 10.1038/cdd.2016.155
45. Orlofsky A, Weiss LM, Kawachi N, Prystowsky MB. Deficiency in the anti-apoptotic protein A1-a results in a diminished acute inflammatory response. J Immunol 2002; 168: 1840-1846
46. Halder P, Kumar R, Jana K, Chakraborty S, Ghosh Z, Kundu M, et al. Gene expression profiling of Mycobacterium tuberculosis Lipoarabinomannan-treated macrophages: a role of the Bcl-2 family member A1 in inhibition of apoptosis in mycobacteria-infected macrophages. IUBMB Life 2015; 67: 726-736
47. Speir M, Lawlor KE, Glaser SP, Abraham G, Chow S, Vogrin A, et al. Eliminating Legionella by inhibiting BCL-XL to induce macrophage apoptosis. Nat Microbiol 2016; 1: 15034
48. Manzl C, Baumgartner F, Peintner L, Schuler F, Villunger A. Possible pitfalls investigating cell death responses in genetically engineered mouse models and derived cell lines. Methods 2013; 61: 130-137
49. Roberts AW, Davids MS, Pagel JM, Kahl BS, Puvvada SD, Gerecitano JF, et al. Targeting BCL2 with Venetoclax in Relapsed Chronic Lymphocytic Leukemia. N Engl J Med 2016; 374: 311-322
50. Kotschy A, Szlavik Z, Murray J, Davidson J, Maragno AL, Le Toumelin-Braizat G, et al. The MCL1 inhibitor S63845 is tolerable and effective in diverse cancer models. Nature 2016; 538: 477-482
51. Schwenk F, Baron U, Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 1995; 23: 5080-5081
52. Okamoto T, Coultas L, Metcalf D, van Delft MF, Glaser SP, Takiguchi M, et al. Enhanced stability of Mcl1, a prosurvival Bcl2 relative, blunts stress-induced apoptosis, causes male sterility and promotes tumorigenesis. Proc Natl Acad Sci USA 2014; 111: 261-266
53. Deenick EK, Gett AV, Hodgkin PD. Stochastic model of T cell proliferation: a calculus revealing IL-2 regulation of precursor frequencies, cell cycle time and survival. J Immunol 2003; 170: 4963-4972
54. Marchingo JM, Kan A, Sutherland RM, Duffy KR, Wellard CJ, Belz GT, et al. T cell signaling. Antigen affinity, costimulation and cytokine inputs sum linearly to amplify T cell expansion. Science 2014; 346: 1123-1127
55. Karasuyama H, Melchers F. Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur J Immunol 1988; 18: 97-104
56. Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol 2000; 164: 2978-2986