Compartmentalized megakaryocyte death generates functional platelets committed to caspase-independent death

Journal of Cell Biology

Volumn 160, Issue 4, 2003, Pages 577-587

  Clarke, Murray C H ^a   Savill, John ^a   Jones, David B ^c   Noble, Brendon S ^b   Brown, Simon B ^a,d  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b ROYAL INFIRMARY OF EDINBURGH   (United Kingdom)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Apoptosis; Caspases; Fas; Mitochondria; Thrombopoiesis

Indexed keywords

CASPASE; CASPASE 3; CASPASE 9; CYTOCHROME C;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; MEGAKARYOCYTE; MEMBRANE POTENTIAL; PHAGOCYTE; PRIORITY JOURNAL; STEM CELL; THROMBOCYTE;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; ANTIGENS, CD95; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; BLOOD PLATELETS; BONE AND BONES; CASPASES; CELL LINE; ENZYME ACTIVATION; ENZYME INHIBITORS; FLOW CYTOMETRY; FLUORESCENT DYES; HUMANS; LIGANDS; MACROPHAGES; MALE; MEGAKARYOCYTES; MEMBRANE POTENTIALS; MICE; MIDDLE AGED; MITOCHONDRIA; PROTEINS;

EID: 0037450786     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200210111     Document Type: Article

References (48)

1. Akahori, M., Y. Uedono, K. Yamagami, N. Takeyama, Y. Kitazawa, and T. Tanaka. 1995. Hypoxia alters the energy metabolism and aggregation of washed human platelets. Haematologia (Budap). 26:191-198.
2. Bantel, H., B. Sinha, W. Domschke, G. Peters, K. Schulze-Osthoff, and R.U. Janicke. 2001. alpha-Toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J. Cell Biol. 155:637-648.
3. Battinelli, E., S.R. Willoughby, T. Foxall, C.R. Valeri, and J. Loscalzo. 2001. Induction of platelet formation from megakaryocytoid cells by nitric oxide. Proc. Natl. Acad. Sci. USA. 98:14458-14463.
4. Bouillet, P., D. Metcalf, D.C. Huang, D.M. Tarlinton, T.W. Kay, F. Kontgen, J.M. Adams, and A. Strasser. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 286:1735-1738.
5. Brown, S.B., K. Bailey, and J. Savill. 1997. Actin is cleaved during constitutive apoptosis. Biochem. J. 323:233-237.
6. Brown, S.B., M.C. Clarke, L. Magowan, H. Sanderson, and J. Savill. 2000. Constitutive death of platelets leading to scavenger receptor-mediated phagocytosis. A caspase-independent cell clearance program. J. Biol. Chem. 275:5987-5996.
7. Chua, B.T., K. Guo, and P. Li. 2000. Direct cleavage by the calcium-activated protease calpain can lead to inactivation of caspases. J. Biol. Chem. 275:5131-5135.
8. Cramer, E.M., F. Norol, J. Guichard, J. Breton-Gorius, W. Vainchenker, J.M. Masse, and N. Debili. 1997. Ultrastructure of platelet formation by human megakaryocytes cultured with the Mpl ligand. Blood. 89:2336-2346.
9. De Botton, S., S. Sabri, E. Daugas, Y. Zermati, J.E. Guidotti, O. Hermine, G. Kroemer, W. Vainchenker, and N. Debili. 2002. Platelet formation is the consequence of caspase activation within megakaryocytes. Blood. 100:1310-1317.
10. Doery, J.C., J. Hirsh, and I. Cooper. 1970. Energy metabolism in human platelets: interrelationship between glycolysis and oxidative metabolism. Blood. 36:159-168.
11. Drachman, J.G., D.F. Sabath, N.E. Fox, and K. Kaushansky. 1997. Thrombopoietin signal transduction in purified murine megakaryocytes. Blood. 89:483-492.
12. Garcia-Calvo, M., E.P. Peterson, B. Leiting, R. Ruel, D.W. Nicholson, and N.A. Thornberry. 1998. Inhibition of human caspases by peptide-based and macromoleculat inhibitors. J. Biol. Chem. 273:32608-32613.
13. Gregory, C.J., and A.C. Eaves. 1978. Three stages of erythropoietic progenitor cell differentiation distinguished by a number of physical and biologic properties. Blood. 51:527-537.
14. Harper, L., P. Cockwell, D. Adu, and C.O. Savage. 2001. Neutrophil priming and apoptosis in anti-neutrophil cytoplasmic autoantibody-associated vasculitis. Kidney Int. 59:1729-1738.
15. Italiano, J.E., Jr., P. Lecine, R.A. Shivdasani, and J.H. Hartwig. 1999. Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes. J. Cell Biol. 147:1299-1312.
16. Kerr, J.F., A.H. Wyllie, and A.R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26:239-257.
17. Kluck, R.M., E. Bossy-Wetzel, D.R. Green, and D.D. Newmeyer. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1132-1136.
18. Knepper-Nicolai, B., J. Savill, and S.B. Brown. 1998. Constitutive apoptosis in human neutrophils requires synergy between calpains and the proteasome downstream of caspases. J. Biol. Chem. 273:30530-30536.
19. Lankiewicz, S., L.C. Marc, B.N. Truc, A.J. Krohn, M. Poppe, G.M. Cole, T.C. Saido, and J.H. Ptehn. 2000. Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death. J. Biol. Chem. 275:17064-17071.
20. Le Deist, F., J.F. Emile, F. Rieux-Laucat, M. Benkerrou, I. Roberts, N. Brousse, and A. Fischer. 1996. Clinical, immunological, and pathological consequences of Fas-deficient conditions. Lancet. 348:719-723.
21. Li, P., D. Nijhawan, I. Budihatdjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:479-489.
22. Liu, X., C.N. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptotic program in cell-free extracts: requitement for dATP and cytochrome c. Cell. 86:147-157.
23. Marchetti, P., M. Castedo, S.A. Susin, N. Zamzami, T. Hirsch, A. Macho, A. Haeffner, F. Hirsch, M. Geuskens, and G. Kroemer. 1996. Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 184:1155-1160.
24. Ogilvy, S., D. Metcalf, C.G. Print, M.L. Bath, A.W. Hatris, and J.M. Adams. 1999. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc. Natl. Acad. Sci. USA. 96:14943-14948.
25. Ogura, M., Y. Morishima, R. Ohno, Y. Kato, N. Hirabayashi, H. Nagura, and H., Saito. 1985. Establishment of a novel human megakaryoblastic leukemia cell line, MEG-01, with positive Philadelphia chromosome. Blood. 66:1384-1392.
26. Otterdal, K., T.M. Pedersen, and N.O. Solum. 2001. Platelet shape change induced by the peptide YFLLRNP. Thromb. Res. 103:411-420.
27. Parker, R.I., and H.R. Gralnick. 1997. Energy-dependent expression of platelet-von Willebrand factor on the surface of unstimulared and stimulated platelets. J. Lab. Clin. Med. 130:520-529.
28. Petit, P.X., H. Lecoeur, E. Zorn, C. Dauguet, B. Mignotte, and M.L. Gougeon. 1995. Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoprosis. J. Cell Biol. 130:157-167.
29. Radley, J.M., and C.J. Haller. 1983. Fate of senescent megakaryocytes in the bone marrow. Br. J. Haematol. 53:277-287.
30. Rieux-Laucat, F., F. Le Deist, C. Hivroz, I.A. Roberts, K.M. Debatin, A. Fischer, and J.P. de Villartay. 1995. Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science. 268:1347-1349.
31. Robertson, A.M., C.C. Bird, A.W. Waddell, and A.R. Currie. 1978. Morphological aspects of glucocorticoid-induced cell death in human lymphoblastoid cells. J. Pathol. 126:181-187.
32. Rojnuckarin, P., and K. Kaushansky. 2001. Actin reorganization and proplatelet formation in murine megakaryocytes: the role of protein kinase calpha. Blood. 97:154-161.
33. 6(3) or rhodamine 123, is a reliable fluorescent probe to assess delta psi changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett. 411:77-82.
34. + progenitors but is absent from senescent megakaryocytes. Exp. Hematol. 29:728-735.
35. Savill, J.S., A.H. Wyllie, J.E. Henson, M.J. Walport, P.M. Henson, and C. Haslett. 1989. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83:865-875.
36. Smith, E., and D.B. Jones, inventors and assignees. 1998 July 6. A combined perfusion and mechanical loading system for explanted bone. US patent 6,171,812.
37. Stenberg, P.E., and J. Levin. 1989. Mechanisms of platelet ptoduction. Blood Cells. 15:23-47.
38. Takeuchi, K., M. Satoh, H. Kuno, T. Yoshida, H. Kondo, and M. Takeuchi. 1998. Platelet-like particle formation in the human megakaryoblastic leukaemia cell lines, MEG-01 and MEG-01s. Br. J. Haematol. 100:436-444.
39. Tavassoli, M., and M. Aoki. 1989. Localization of megakaryocytes in the bone marrow. Blood Cells. 15:3-14.
40. Terui, Y., Y. Furukawa, J. Kikuchi, S. Iwase, K. Hatake, and Y. Miura. 1998. Bcl-x is a regulatory factor of apoptosis and differentiation in megakaryocytic lineage cells. Exp. Hematol. 26:236-244.
41. Uozumi, K., M. Otsuka, N. Ohno, T. Moriyama, S. Suzuki, S. Shimotakahara, I. Matsumuta, S. Hanada, and T. Arima. 2000. Establishment and characterization of a new human megakaryoblastic cell line (SET-2) that spontaneously matures to megakaryocytes and produces platelet-like particles. Leukemia. 14:142-152.
42. Watanabe, Y., M. Taniguchi, N. Fukamachi, M. Sakuma, and B. Kobayashi. 1990. Effects of gangliosides on cell maturation of murine megakaryocytes in a liquid culture system. Cell Srruct. Funct. 15:79-84.
43. Webb, P.R., K.Q. Wang, D. Scheel-Toellnet, J. Pongracz, M. Salmon, and J.M. Lord. 2000. Regulation of neutrophil apoptosis: a role for protein kinase C and phosphatidylinositol-3-kinase. Apoptosis. 5:451-458.
44. Wolf, B.B., J.C. Goldstein, H.R. Stennicke, H. Beere, G.P. Amarante-Mendes, G.S. Salvesen, and D.R. Green. 1999. Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. Blood. 94:1683-1692.
45. Wyllie, A.H. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 284:555-556.
46. Yang, J., X. Liu, K. Bhalla, C.N. Kim, A.M. Ibrado, J. Cai, T.I. Peng, D.P. Jones, and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mirochondria blocked. Science. 275:1129-1132.
47. Zauli, G., M. Vitale, E. Falcieri, D. Gibellini, A. Bassini, C. Celeghini, M. Columbaro, and S. Capitani. 1997. In vitro senescence and apoptotic cell death of human megakaryocytes. Blood. 90:2234-2243.
48. Zermati, Y., C. Garrido, S. Amsellem, S. Fishelson, D. Bouscary, F. Valensi, B. Varet, E. Solary, and O. Hermine. 2001. Caspase activation is required for terminal erythroid differentiation. J. Exp. Med. 193:247-254.