Caspase redundancy and release of mitochondrial apoptotic factors characterize interdigital apoptosis

Apoptosis

Volumn 11, Issue 5, 2006, Pages 701-715

  Zuzarte Luis, V ^a   Berciano, M T ^a   Lafarga, M ^a   Hurle J M ^a  

^a UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

AIF; Caspase 2; Cytochrome c; Limb development; Programmed cell death

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE; CASPASE 3; CASPASE 7; PAXILLIN; RNA; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; ASSAY; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING ORGAN SYSTEMS; CELL ADHESION; CELL DEATH; CHROMATIN; CYTOPLASM; CYTOSKELETON; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; ENZYME LOCALIZATION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASE 2; CASPASE 3; CASPASE 7; CASPASES; CELL DEATH; CELL NUCLEUS; CHICK EMBRYO; CYTOCHROMES C; CYTOPLASM; DOWN-REGULATION; ENZYME ACTIVATION; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MITOCHONDRIA; PAXILLIN; RNA, SMALL INTERFERING;

EID: 33745048075     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-006-5481-8     Document Type: Article

References (66)

1. Zuzarte-Luis V, Hurle JM. Programmed cell death in the developing limb. Int J Dev Biol 2002; 46: 871-876.
2. Fallon JF, Cameron J. Interdigital cell death during limb development of the turtle and lizard with an interpretation of evolutionary significance. J Embryol Exp Morphol 1977; 40: 285-289.
3. Milligan CE, Prevette D, Yaginuma H, et al. Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro. Neuron 1995; 15: 385-393.
4. Jacobson MD, Weil M, Rafff MC. Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J Cell Biol 1996; 133: 1041-1051.
5. Umpierre CC, Little SA, Mirkes PE. Co-localization of active caspase-3 and DNA fragmentation (TUNEL) in normal and hyperthermia-induced abnormal mouse development. Teratology 2001; 63: 134-143.
6. Huang C, Hales BF. Role of caspases in murine limb bud cell death induced by 4-hydroperoxycyclophosphamide, an activated analog of cyclophosphamide. Teratology 2002; 66: 288-299.
7. Kuida K, Zheng TS, Na S, et al. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 1996; 384: 368-372.
8. Chautan M, Chazal G, Cecconi F, Gruss P, Golstein P. Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr Biol 1999; 9: 967-970.
9. Wride MA, Lapchak PH, Sanders EJ. Distribution of TNF alpha-like proteins correlates with some regions of programmed cell death in the chick embryo. Int J Dev Biol 1994; 38: 673-682.
10. Wang J, Zheng L, Lobito A, et al. Inherited human Caspase 10 mutations underlie defective lymphocyte and dendritic cell apoptosis in autoimmune lymphoproliferative syndrome type II. Cell 1999; 98: 47-58.
11. Chun HJ, Zheng L, Ahmad M, et al. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 2002; 419: 395-399.
12. Dupe V, Ghyselinck NB, Thomazy V, et al. Essential roles of retinoic acid signalling in interdigital apoptosis and control of BMP-7 expression in mouse autopods. Dev Biol 1999; 208: 30-43.
13. Salas-Vidal E, Lomeli H, Castro-Obregon S, Cuervo R, Escalante-Alcalde D, Covarrubias L. Reactive oxygen species participate in the control of mouse embryonic cell death. Exp Cell Res 1998; 238: 136-147.
14. 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: 1389-1399.
15. Jurgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D, Reed JC. Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 1998; 95: 4997-5002.
16. Kuida K, Haydar TF, Kuan CY, et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 1998; 94: 325-337.
17. Drouin R, Lemieux N, Richer CL. Chromosome condensation from prophase to late metaphase: Relationship to chromosome bands and their replication time. Cytogenet Cell Genet 1991; 57: 91-99.
18. Rubio E, Valenciano AI, Segundo C, Sanchez N, de Pablo F, de la Rosa EJ. Programmed cell death m the neurulating embryo is prevented by the chaperone heat shock cognate 70. Eur J Neurosci 2002; 15: 1646-1654.
19. Jansen RP, Hurt EC, Kern H, Lehtonen H, Carmo-Fonseca M. Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast. J Cell Biol 1991; 113: 715-729.
20. Pena E, Berciano MT, Fernandez R, Ojeda JL, Lafarga M. Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J Comp Neurol 2001; 430: 250-263.
21. Macias D, Ganan Y, Ros MA, Hurle JM. In vivo inhibition of programmed cell death by local administration of FGF-2 and FGF-4 in the interdigital areas of the embryonic chick leg bud. Anat Embryol (Berl) 1996; 193: 533-541.
22. Berciano MT, Villagra NT, Ojeda JL, et al. Oculopharyngeal muscular dystrophy-like nuclear inclusions are present in normal magnocellular neurosecretory neurons of the hypothalamus. Hum Mol Genet 2004; 13: 829-838.
23. Mirkes PE, Little SA. cytochrome c release from the mitochondria of early postimplantation murine embryos exposed to 4-hydroperoxycyclophosphamide, heat shock and staurosponne. Tox App Pharma 2000; 162: 197-206.
24. Kihlmark M, Imreh G, Hallberg E. Sequential degradation of proteins from the nuclear envelope during apoptosis. J Cell Sci 2001; 114: 3643-3653.
25. Gregory PD, Wagner K, Horz W. Histone acetylation and chromatin remodeling. Exp Cell Res 2001; 265: 195-202.
26. Buendia B, Santa-Maria A, Courvalin JC. Caspase-dependent proteolysis of integral and peripheral proteins of nuclear membranes and nuclear pore complex proteins during apoptosis. J Cell Sci 1999; 112: 1743-1753.
27. Stott NS, Jiang TX, Chuong CM. Successive formative stages of precartilaginous mesenchymal condensations in vitro: Modulation of cell adhesion by Wnt-7A and BMP-2. J Cell Physiol 1999; 180: 314-324.
28. Merino R, Macias D, Ganan Y, et al. Control of digit formation by activin signalling. Development 1999; 126: 2161-2170.
29. Pedersen MV, Kohler LB, Ditlevsen DK, Li S, Berezin V, Bock E. Neuritogenic and survival-promoting effects of the P2 peptide derived from a homophilic binding site in the neural cell adhesion molecule. J Neurosci Res 2004; 75: 55-65.
30. Hanks SK, Ryzhova L, Shin NY, Brabek J. Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility. Front Biosci 2003; 8: 982-996.
31. Chay KO, Park SS, Mushinski JF. Linkage of caspase-mediated degradation of paxillin to apoptosis in Ba/F3 murine pro-B lymphocytes. J Biol Chem 2002; 277: 14521-14529.
32. Longuet M, Serduc R, Riva C. Implication of bax in apoptosis depends on microtubule network mobility. Int J Oncol 2004; 25: 309-317.
33. Byun Y, Chen F, Chang R, Trivedi M, Green KJ, Cryns VL. Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ 2001; 8: 443-450.
34. Martin DN, Baehrecke EH. Caspases function in autophagic programmed cell death in Drosophila. Development 2004; 131: 275-284.
35. Guicciardi ME, Leist M, Gores GJ. Lysosomes in cell death. Oncogene 2004; 23: 2881-2890.
36. Hurle J, Hinchcliffe JR. Cell death in the posterior necrotic zone (PNZ) of the chick wing-bud: A stereoscan and ultrastructural survey of autolysis and cell fragmentation. J Embryol Exp Morphol 1978; 43: 123-136.
37. Stewart S, Yi S, Kassabian G, Mayo M, Sank A, Shuler C. Changes in expression of the lysosomal membrane glycoprotein, LAMP-1 in interdigital regions during embryonic mouse limb development, in vivo and in vitro. Anat Embryol (Berl) 2000; 201: 483-490.
38. Salvesen GS, Abrams JM. Caspase activation - Stepping on the gas or releasing the brakes? Lessons from humans and flies. Oncogene 2004; 23: 2774-2784.
39. Zuzarte-Luis V, Hurle JM. Programmed cell death in the embryonic vertebrate limb. Sem Cell Dev Biol 2005; (in press).
40. Hong SJ, Dawson TM, Dawson VL. Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol Sci 2004; 25: 259-264.
41. Grossmann J, Walther K, Artinger M, Kiessling S, Scholmerich J. Apoptotic signaling during initiation of detachment-induced apoptosis ("anoikis") of primary human intestinal epithelial cells. Cell Growth Differ 2001; 12: 147-155.
42. De Arcangelis A, Mark M, Kreidberg J, Sorokin L, Georges-Labouesse E. Synergistic activities of alpha3 and alpha6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 1999; 126: 3957-3968.
43. Hurle JM, Corson G, Daniels K, Reiter RS, Sakai LY, Solursh M. Elastin exhibits a distinctive temporal and spatial pattern of distribution in the developing chick limb in association with the establishment of the cartilaginous skeleton. J Cell Sci 1994; 107: 2623-2634.
44. Miner JH, Cunningham J, Sanes JR. Roles for laminin in embryogenesis: Exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J Cell Biol 1998; 143: 1713-1723.
45. Arteaga-Solis E, Gayraud B, Lee SY, Shum L, Sakai L, Ramirez F. Regulation of limb patterning by extracellular microfibrils. J Cell Biol 2001; 154: 275-281.
46. Debeer P, Schoenmakers EF, Twal WO, et al. The fibulin-1 gene (FBLN1) is disrupted in a t(12; 22) associated with a complex type of synpolydactyly. J Med Genet 2002; 39: 98-104.
47. Smyth I, Du X, Taylor MS, Justice MJ, Beutler B, Jackson IJ. The extracellular matrix gene Frem1 is essential for the normal adhesion of the embryonic epidermis. Proc Natl Acad Sci USA 2004; 101: 13560-13565.
48. Takamiya K, Kostourou V, Adams S, et al. A direct functional link between the multi-PDZ domain protein GRIP1 and the Fraser syndrome protein Fras1. Nat Genet 2004; 36: 172-177.
49. Levine B, Klionsky DJ. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-477.
50. Hurle JM, Colvee E, Fernandez-Teran MA. Vascular regression during the formation of the free digits in the avian limb bud: A comparative study in chick and duck embryos. J Embryol Exp Morphol 1985; 85: 239-250.
51. Kihlmark M, Rustum C, Eriksson C, Beckman M, Iverfeldt K, Hallberg E. Correlation between nucleocytoplasmic transport and caspase-3-dependent dismantling of nuclear pores during apoptosis. Exp Cell Res 2004; 293: 346-356.
52. Ferrando-May E, Cordes V, Biller-Ckovric I, Mirkovic J, Gorlich D, Nicotera P. Caspases mediate nucleoporin cleavage, but not early redistribution of nuclear transport factors and modulation of nuclear permeability in apoptosis. Cell Death Differ 2001; 8: 495-505.
53. Yasuhara N, Eguchi Y, Tachibana T, Imamoto N, Yoneda Y, Tsujimoto Y. Essential role of active nuclear transport in apoptosis. Genes Cells 1997; 2: 55-64.
54. Zheng TS, Hunot S, Kuida K, Flavell RA. Caspase knockouts: Matters of life and death. Cell Death Differ 1999; 6: 1043-1053.
55. Fischer U, Janicke RU, Schulze-Osthoff K. Many cuts to ruin: A comprehensive update of caspase substrates. Cell Death Differ 2003; 10: 76-100.
56. Miyazaki K, Yoshida H, Sasaki M, et al. Caspase-independent cell death and mitochondrial disruptions observed in the Apaf1-deficient cells. J Biochem (Tokyo) 2001; 129: 963-969.
57. Joza N, Susin SA, Daugas E, et al. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 2001; 410: 549-554.
58. Sanders EJ, Parker E. Ablation of axial structures activates apoptotic pathways in somite cells of the chick embryo. Anat Embryol (Berl) 2001; 204: 389-398.
59. Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES. Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 2002; 277: 13430-13437.
60. Cregan SP, Fortin A, MacLaurin JG, et al. Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol 2002; 158: 507-517.
61. Broker LE, Kruyt FAE, Giaccone G. Cell Death Independent of Caspases: A review. Clin Cancer Res 2005; 11: 3155-3162.
62. Nakanishi K, Maruyama M, Shibata T, Morishima N. Identification of a caspase-9 substrate and detection of its cleavage in programmed cell death during mouse development. J Biol Chem 2001; 276: 41237-41244.
63. Bergeron L, Perez GI, Macdonald G, et al. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 1998; 12: 1304-1314.
64. Troy CM, Shelanski ML. Caspase-2 redux. Cell Death Differ 2003; 10: 101-107.
65. Wagner KW, Engels IH, Deveraux QL. Caspase-2 can function upstream of bid cleavage in the TRAIL apoptosis pathway. J Biol Chem 2004; 279: 35047-35052.
66. Zhivotovsky B, Orrenius S. Caspase-2 function in response to DNA damage. Biochem Biophys Res Commun 2005; 331: 859-867.