Apoptosis in megakaryocytes and platelets: the life and death of a lineage

Blood

Volumn 131, Issue 6, 2018, Pages 605-610

  McArthur, Kate ^a   Chappaz, Stephane ^a   Kile, Benjamin T ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BAK; PROTEIN BAX; PROTEIN BCL XL; PROTEIN MCL 1;

APOPTOSIS; CELL DEATH; HUMAN; MEGAKARYOCYTE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE LIFESPAN; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; PHAGOCYTOSIS; PHYSIOLOGY;

ANIMALS; APOPTOSIS; BLOOD PLATELETS; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; HUMANS; MEGAKARYOCYTES; PHAGOCYTOSIS;

EID: 85041891325     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2017-11-742684     Document Type: Review

References (83)

1. References myelodysplastic patients. Blood. 2005;105(9): 3472-3479.
2. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26(4):239-257.
3. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol. 2008;9(1):47-59.
4. Kovacs SB, Miao EA. Gasdermins: effectors of pyroptosis. Trends Cell Biol. 2017;27(9): 673-684.
5. Linkermann A, Green DR. Necroptosis. N Engl J Med. 2014;370(5):455-465.
6. Fearnhead HO, Vandenabeele P, Vanden Berghe T. How do we fit ferroptosis in the family of regulated cell death? Cell Death Differ. 2017;24(12):1991-1998.
7. Julien O, Wells JA. Caspases and their substrates. Cell Death Differ. 2017;24(8): 1380-1389.
8. Scaffidi C, Fulda S, Srinivasan A, et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 1998;17(6):1675-1687.
9. Yin XM, Wang K, Gross A, et al. Bid-deficient mice are resistant to Fas-induced hepatocel-lular apoptosis. Nature. 1999;400(6747): 886-891.
10. Jost PJ, Grabow S, Gray D, et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature. 2009;460(7258): 1035-1039.
11. Wei MC, Zong WX, Cheng EH, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 2001;292(5517):727-730.
12. Lindsten T, Ross AJ, King A, et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell. 2000;6(6):1389-1399.
13. Lindsten T, Thompson CB. Cell death in the absence of Bax and Bak. Cell Death Differ. 2006;13(8):1272-1276.
14. Ekert PG, Read SH, Silke J, et al. Apaf-1 and caspase-9 accelerate apoptosis, but do not determine whether factor-deprived or drug-treated cells die. J Cell Biol. 2004;165(6): 835-842.
15. Ekert PG, Jabbour AM, Manoharan A, et al. Cell death provoked by loss of interleukin-3 signaling is independent of Bad, Bim, and PI3 kinase, but depends in part on Puma. Blood. 2006;108(5):1461-1468.
16. White MJ, McArthur K, Metcalf D, et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production. Cell. 2014;159(7):1549-1562.
17. Rongvaux A, Jackson R, Harman CCD, et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell. 2014;159(7):1563-1577.
18. Kodama T, Hikita H, Kawaguchi T, et al. Mcl-1 and Bcl-xL regulate Bak/Bax-dependent apoptosis of the megakaryocytic lineage at multistages. Cell Death Differ. 2012;19(11): 1856-1869.
19. Debrincat MA, Josefsson EC, James C, et al. Mcl-1 and Bcl-x(L) coordinately regulate megakaryocyte survival. Blood. 2012;119(24): 5850-5858.
20. Zauli G, Vitale M, Falcieri E, et al. In vitro senescence and apoptotic cell death of human megakaryocytes. Blood. 1997;90(6): 2234-2243.
21. Morison IM, Cramer Bordé EM, Cheesman EJ, et al. A mutation of human cytochrome c enhances the intrinsic apoptotic pathway but causes only thrombocytopenia. Nat Genet. 2008;40(4):387-389.
22. Houwerzijl EJ, Blom NR, van der Want JJ, et al. Ultrastructural study shows morphologic features of apoptosis and para-apoptosis in megakaryocytes from patients with idiopathic thrombocytopenic purpura. Blood. 2004; 103(2):500-506.
23. Clarke MC, Savill J, Jones DB, Noble BS, Brown SB. Compartmentalized megakaryocyte death generates functional platelets committed to caspase-independent death. J Cell Biol. 2003;160(4):577-587.
24. Kaluzhny Y, Yu G, Sun S, et al. BclxL over-expression in megakaryocytes leads to impaired platelet fragmentation. Blood. 2002; 100(5):1670-1678.
25. De Botton S, Sabri S, Daugas E, et al. Platelet formation is the consequence of caspase activation within megakaryocytes. Blood. 2002; 100(4):1310-1317.
26. Brown SB, Clarke MC, Magowan L, Sanderson H, Savill J. Constitutive death of platelets leading to scavenger receptor-mediated phagocytosis. A caspase-independent cell clearance program. J Biol Chem. 2000;275(8): 5987-5996.
27. Ogilvy S, Metcalf D, Print CG, Bath ML, Harris AW, Adams JM. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc Natl Acad Sci USA. 1999;96(26):14943-14948.
28. Bouillet P, Metcalf D, Huang DC, et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 1999;286(5445):1735-1738.
29. Josefsson EC, Burnett DL, Lebois M, et al. Platelet production proceeds independently of the intrinsic and extrinsic apoptosis pathways. Nat Commun. 2014;5:3455.
30. Josefsson EC, James C, Henley KJ, et al. Megakaryocytes possess a functional intrinsic apoptosis pathway that must be restrained to survive and produce platelets. J Exp Med. 2011;208(10):2017-2031.
31. Kodama T, Takehara T, Hikita H, et al. BH3-only activator proteins Bid and Bim are dispensable for Bak/Bax-dependent thrombocyte apoptosis induced by Bcl-xL deficiency: molecular requisites for the mitochondrial pathway to apoptosis in platelets. J Biol Chem. 2011;286(16):13905-13913.
32. Kodama T, Takehara T, Hikita H, et al. Thrombocytopenia exacerbates cholestasis-induced liver fibrosis in mice. Gastroenterology. 2010;138(7):2487-98, 2498.e1-7.
33. White MJ, Schoenwaelder SM, Josefsson EC, et al. Caspase-9 mediates the apoptotic death of megakaryocytes and platelets, but is dispensable for their generation and function. Blood. 2012;119(18):4283-4290.
34. Radley JM, Haller CJ. Fate of senescent megakaryocytes in the bone marrow. Br J Haematol. 1983;53(2):277-287.
35. Houwerzijl EJ, Blom NR, van der Want JJL, et al. Increased peripheral platelet destruction and caspase-3-independent programmed cell death of bone marrow megakaryocytes in
36. Kaushansky K. The thrombocytopenia of cancer. Prospects for effective cytokine therapy. Hematol Oncol Clin North Am. 1996; 10(2):431-455.
37. Schattner M, Rivadeneyra L, Pozner RG, Gómez RM. Pathogenic mechanisms involved in the hematological alterations of arenavirus-induced hemorrhagic fevers. Viruses. 2013; 5(1):340-351.
38. Zauli G, Catani L, Gibellini D, et al. Impaired survival of bone marrow GPIIb/IIa1 megakaryocytic cells as an additional pathogenetic mechanism of HIV-1-related thrombocytopenia. Br J Haematol. 1996;92(3):711-717.
39. Noisakran S, Onlamoon N, Hsiao H-M, et al. Infection of bone marrow cells by dengue virus in vivo. Exp Hematol. 2012;40(3):250-259.e4.
40. Chen P-K, Chang H-H, Lin G-L, et al. Suppressive effects of anthrax lethal toxin on megakaryopoiesis. PLoS One. 2013;8(3): e59512.
41. Leeksma CHW, Cohen JA. Determination of the life of human blood platelets using la-belled diisopropylfluorophosphanate. Nature. 1955;175(4456):552-553.
42. Ault KA, Knowles C. In vivo biotinylation demonstrates that reticulated platelets are the youngest platelets in circulation. Exp Hematol. 1995;23(9):996-1001.
43. Shemin D, Rittenberg D. The life span of the human red blood cell. J Biol Chem. 1946; 166(2):627-636.
44. Wolf BB, Goldstein JC, Stennicke HR, et al. Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. Blood. 1999;94(5): 1683-1692.
45. Vanags DM, Orrenius S, Aguilar-Santelises M. Alterations in Bcl-2/Bax protein levels in platelets form part of an ionomycin-induced process that resembles apoptosis. Br J Haematol. 1997;99(4):824-831.
46. Shcherbina A, Remold-O’Donnell E. Role of caspase in a subset of human platelet activation responses. Blood. 1999;93(12): 4222-4231.
47. Li J, Xia Y, Bertino AM, Coburn JP, Kuter DJ. The mechanism of apoptosis in human platelets during storage. Transfusion. 2000; 40(11):1320-1329.
48. Oltersdorf T, Elmore SW, Shoemaker AR, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature. 2005; 435(7042):677-681.
49. Zhang H, Nimmer PM, Tahir SK, et al. Bcl-2 family proteins are essential for platelet survival. Cell Death Differ. 2007;14(5):943-951.
50. Mason KD, Carpinelli MR, Fletcher JI, et al. Programmed anuclear cell death delimits platelet life span. Cell. 2007;128(6): 1173-1186.
51. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. Cloning of the chromosome breakpoint of neoplastic B cells with the
52. t(14;18) chromosome translocation. Science. 1984;226(4678):1097-1099.
53. Tsujimoto Y, Cossman J, Jaffe E, Croce CM. Involvement of the bcl-2 gene in human follicular lymphoma. Science. 1985;228(4706): 1440-1443.
54. Wilson WH, O’Connor OA, Czuczman MS, et al. Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: a phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol. 2010; 11(12):1149-1159.
55. Rudin CM, Hann CL, Garon EB, et al. Phase II study of single-agent navitoclax (ABT-263) and biomarker correlates in patients with relapsed small cell lung cancer. Clin Cancer Res. 2012;18(11):3163-3169.
56. Roberts AW, Seymour JF, Brown JR, et al. Substantial susceptibility of chronic lymphocytic leukemia to BCL2 inhibition: results of a phase I study of navitoclax in patients with relapsed or refractory disease. J Clin Oncol. 2012;30(5):488-496.
57. Souers AJ, Leverson JD, Boghaert ER, et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med. 2013;19(2): 202-208.
58. Roberts AW, Davids MS, Pagel JM, et al. Targeting BCL2 with venetoclax in relapsed chronic lymphocytic leukemia. N Engl J Med. 2016;374(4):311-322.
59. Waibel M, Solomon VS, Knight DA, et al. Combined targeting of JAK2 and Bcl-2/Bcl-xL to cure mutant JAK2-driven malignancies and overcome acquired resistance to JAK2 inhibitors. Cell Rep. 2013;5(4):1047-1059.
60. Mustard JF, Rowsell HC, Murphy EA. Platelet economy (platelet survival and turnover). Br J Haematol. 1966;12(1):1-24.
61. Josefsson EC, Lebois M, Dowling MR, Kile BT. The regulation of platelet life span. In: Michelson AD, ed. Platelets. 3rd ed. Amsterdam, The Netherlands: Academic Press; 2013:51-65.
62. Ren D, Tu H-C, Kim H, et al. BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science. 2010;330(6009):1390-1393.
63. Kelly PN, White MJ, Goschnick MW, et al. Individual and overlapping roles of BH3-only proteins Bim and Bad in apoptosis of lymphocytes and platelets and in suppression of thymic lymphoma development. Cell Death Differ. 2010;17(10):1655-1664.
64. Zhang S, Ye J, Zhang Y, et al. P2Y12 protects platelets from apoptosis via PI3k-dependent Bak/Bax inactivation. J Thromb Haemost. 2013;11(1):149-160.
65. Chatterjee M, Borst O, Walker B, et al. Macrophage migration inhibitory factor limits activation-induced apoptosis of platelets via CXCR7-dependent Akt signaling. Circ Res. 2014;115(11):939-949.
66. Catani MV, Gasperi V, Evangelista D, Finazzi Agrò A, Avigliano L, Maccarrone M. Anandamide extends platelets survival
67. through CB(1)-dependent Akt signaling. Cell Mol Life Sci. 2010;67(4):601-610.
68. Zhao L, Liu J, He C, et al. Protein kinase A determines platelet life span and survival by regulating apoptosis [published online ahead of print 30 October 2017]. J Clin Invest. 2017; doi:10.1172/JCI95109.
69. Schoenwaelder SM, Yuan Y, Josefsson EC, et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood. 2009;114(3):663-666.
70. Zwaal RF, Comfurius P, van Deenen LL. Membrane asymmetry and blood coagulation. Nature. 1977;268(5618):358-360.
71. Bevers EM, Comfurius P, van Rijn JL, Hemker HC, Zwaal RF. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem. 1982;122(2): 429-436.
72. Jobe SM, Wilson KM, Leo L, et al. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood. 2008;111(3): 1257-1265.
73. Suzuki J, Umeda M, Sims PJ, Nagata S. Calcium-dependent phospholipid scrambling by TMEM16F. Nature. 2010;468(7325): 834-838.
74. Suzuki J, Denning DP, Imanishi E, Horvitz HR, Nagata S. Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science. 2013;341(6144): 403-406.
75. Leytin V. Apoptosis in the anucleate platelet. Blood Rev. 2012;26(2):51-63.
76. Niu X, Brahmbhatt H, Mergenthaler P, et al. A small-molecule inhibitor of Bax and Bak oligomerization prevents genotoxic cell death and promotes neuroprotection. Cell Chem Biol. 2017;24(4):493-506.e5.
77. Jiang X, Li L, Ying Z, et al. A small molecule that protects the integrity of the electron transfer chain blocks the mitochondrial apoptotic pathway. Mol Cell. 2016;63(2):229-239.
78. Yuan Y, Alwis I, Wu MCL, et al. Neutrophil macroaggregates promote widespread pulmonary thrombosis after gut ischemia. Sci Transl Med. 2017;9(409):eaam5861.
79. Hua VM, Abeynaike L, Glaros E, et al. Necrotic platelets provide a procoagulant surface during thrombosis. Blood. 2015;126(26): 2852-2862.
80. Jackson SP, Schoenwaelder SM. Procoagulant platelets: are they necrotic? Blood. 2010; 116(12):2011-2018.
81. Duke WW. The relation of blood platelets to hemorrhagic disease. By W.W. Duke. JAMA. 1983;250(9):1201-1209.
82. Grozovsky R, Begonja AJ, Liu K, et al. The Ashwell-Morell receptor regulates hepatic thrombopoietin production via JAK2-STAT3 signaling. Nat Med. 2015;21(1):47-54.
83. Schleicher RI, Reichenbach F, Kraft P, et al. Platelets induce apoptosis via membrane-bound FasL. Blood. 2015;126(12):1483-1493.