Lysosomal membrane permeabilization during apoptosis - Involvement of Bax?

International Journal of Experimental Pathology

Volumn 86, Issue 5, 2005, Pages 309-321

  Kågedal, Katarina ^a   Johansson, Ann Charlotte ^a   Johansson, Uno ^a   Heimlich, Gerd ^b   Roberg, Karin ^a   Wang, Nancy S ^c   Jürgensmeier, Juliane M ^b   Öllinger, Karin ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UNIVERSITY OF COLOGNE   (Germany)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bax; Cathepsins; Lysosomal membrane permeabilization; Lysosomes; Mitochondria

Indexed keywords

APOPTOSIS INDUCING FACTOR; CATHEPSIN D; LYSOSOME ENZYME; PROTEIN BAX; PROTEINASE; STAUROSPORINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; ENZYME RELEASE; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LYSOSOME MEMBRANE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CATHEPSIN D; CELL LINE; ENZYME INHIBITORS; FIBROBLASTS; HUMANS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR MEMBRANES; LIVER; LYSOSOMES; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; PERMEABILITY; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; STAUROSPORINE;

EID: 26244443655     PISSN: 09599673     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0959-9673.2005.00442.x     Document Type: Article

References (48)

1. Antonsson B., Conti F., Ciavatta A. et al. (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277, 370-372.
2. Antonsson B., Montessuit S., SancheZ. B., Martinou J.C. (2001) Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J. Biol. Chem. 276, 11615-11623.
3. 2 is a consequence of lysosomal rupture. Biochem. J. 356, 549-555.
4. Boya P., Andreau K., Poncet D. et al. (2003) Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J. Exp. Med. 197, 1323-1334.
5. Boya P., Gonzalez-Polo R.A., Poncet D. et al. (2003) Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine. Oncogene 22, 3927-3936.
6. Brunk U.T., Dalen H., Roberg K., Hellquist H.B. (1997) Photo-oxidative disruption of lysosomal membranes causes apoptosis of cultured human fibroblasts. Free Radic. Biol. Med. 23, 616-626.
7. Cartron P.F., Arokium H., Oliver L., Meflah K., Manon S., Vallette F.M. (2005) Distinct domains control the addressing and the insertion of Bax into mitochondria. J. Biol. Chem. 280, 10587-10598.
8. Desagher S., Osen-Sand A., Nichols A. et al. (1999) Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144, 891-901.
9. Donovan J.J., Simon M.I., Montal M. (1982) Insertion of diphtheria toxin into and across membranes: role of phosphoinositide asymmetry. Nature 298, 669-672.
10. Epand R.F., Martinou J.C., Fornallaz-Mulhauser M., Hughes D.W., Epand R.M. (2002) The apoptotic protein tBid promotes leakage by altering membrane curvature. J. Biol. Chem. 277, 32632-32639.
11. Eskes R., Antonsson B., Osen-Sand A. et al. (1998) Bax-induced cytochrome c release from mitochondria is independent of the permeability transition pore but highly dependent on Mg2 + ions. J. Cell Biol. 143, 217-224.
12. Foghsgaard L., Wissing D., Mauch D. et al. (2001) Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 153, 999-1010.
13. Coping I.S., Gross A., Lavoie J.N. et al. (1998) Regulated targeting of BAX to mitochondria. J. Cell Biol. 143, 207-215.
14. Gross A., Jockel J., Wei M.C., Korsmeyer S.J. (1998) Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17, 3878-3885.
15. Guicciardi M.E., Deussing J., Miyoshi H. et al. (2000) Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Invest. 106, 1127-1137.
16. Heimlich G., McKinnon A.D., Bernardo K. et al. (2004) Bax-induced cytochrome c release from mitochondria depends on alpha-helices-5. and -6. Biochem. J. 378, 247-255.
17. Hsu Y.T., Wolter K.G., Youle R.J. (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc. Natl. Acad. Sci. USA 94, 3668-3672.
18. Johansson A.C., Steen H., Öllinger K., Roberg K. (2003) Cathepsin D mediates cytochrome c release and caspase activation in human fibroblast apoptosis induced by staurosporine. Cell Death Differ. 10, 1253-1259.
19. Jürgensmeier J.M., Xie Z., Deveraux Q., Ellerby L., Bredesen D., Reed J.C. (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci USA 95, 4997-5002.
20. Kågedal K., Johansson U., Öllinger K. (2001) The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J. 15, 1592-1594.
21. Kågedal K., Zhao M., Svensson I., Brunk U. (2001) Sphingosine-induced apoptosis is dependent on lysosomal proteases Biochem. J. 359, 335-343.
22. Kroemer G., Zamzami N., Susin S.A. (1997) Mitochondrial control of apoptosis. Immunol. Today 18, 44-51.
23. Kuwana T., Mackey M.R., Perkins G. et al. (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342.
24. Li W., Yuan X., Nordgren G. et al. (2000) Induction of cell death by the lysosomotropic detergent MSDH. FEBS Lett. 470, 35-39.
25. Li H., Zhu H., Xu C.J., Yuan J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
26. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. (1998) Bid, a Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
27. Marzo I., Brenner C., Zamzami N. et al. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of Apoptosis. Science 281, 2027-2031.
28. Mathiasen I.S., Jäättelä M. (2002) Triggering caspase-independent cell death to combat cancer. Trends Mol. Med. 8, 212-220.
29. Montessuit S., Mazzei G., Magnenat E., Antonsson B. (1999) Expression and purification of full-length human Bax alpha. Protein Expr. Purif. 15, 202-206.
30. L, an inhibitor of programmed cell death. Nature 381, 335-341.
31. Narita M., Shimizu S., Ito T. et al. (1998) Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. USA 95, 14681-14686.
32. Persson H.L., Yu Z., Tirosh O., Eaton J.W., Brunk U.T. (2003) Prevention of oxidant-induced cell death by lysosomotropic iron chelators. Free Rad. Biol. Med. 34, 1295-1305.
33. Roberg K., Öllinger K. (1998) Oxidative stress causes relocation of the lysosomal enzyme cathepsin D with ensuing apoptosis in neonatal rat cardiomyocytes. Am. J. Pathol. 152, 1151-1156.
34. Roberg K., Öllinger K. (1998) A pre-embedding technique for immunocytochemical visualization of cathepsin D in cultured cells subjected to oxidative stress. J. Histochem. Cytochem. 46, 411-418.
35. Stoka V., Turk B., Schendel S.L. et al. (2001) Lysosomal protease pathways to apoptosis. Cleavage of Bid, not pro-caspases, is the most likely route. J. Biol. Chem. 276, 3149-3157.
36. Suzuki M., Youle R.J., Tjandra N. (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103, 645-654.
37. Turk B., Stoka V., Rozman-Pungercar J., Cirman T., Droga-Mazovec G., Oreic K. (2002) Apoptotic pathways: involvement of lysosomal proteases. Biol. Chem. 383, 1035-1044.
38. Vancompernolle K., Van Herreweghe F., Pynaert G. et al. (1998) Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett. 438, 150-158.
39. Vyssokikh M., Zorova L., Zorov D., Heimlich G., Jürgensmeier J.M., Brdiczka D. (2002) Localisation of cytochrome c in a complex of porin and adenine nucleotide translocator: Bax targeted cytochrome c release depends on the functional state of the complex. Mol. Biol. Rep. 29, 93-96.
40. Werneburg N., Guicciardi M.E., Yin X.M., Gores G.J. (2004) TNF-alpha-mediated lysosomal permeabilization is FAN and caspase 8/Bid dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G436-G443.
41. Wherrett J.R., Huterer S. (1972) Enrichment of bis-(monoacyl-glyceryl) phosphate in lysosomes from rat liver. J. Biol. Chem. 247, 4114-4120.
42. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., Youle R.J. (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139, 1281-1292.
43. Yang J., Liu X., Bhalla K. et al. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.
44. Yuan X.M., Li W., Dalen H. et al. (2002) Lysosomal destabilization in p53-induced apoptosis. Proc. Natl Acad. Sci. USA 99, 6286-6291.
45. Zang Y., Beard R.L., Chandraratna R.A., Kang J.X. (2001) Evidence of a lysosomal pathway for apoptosis induced by the synthetic retinoid CD437 in human leukemia HL-60 cells. Cell Death Differ. 8, 477-485.
46. Zha H., Fisk H.A., Yaffe M.P., Mahajan N., Herman B., Reed J.C. (1996) Structure-function comparisons of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell Biol. 16, 6494-6508.
47. Zhao M., Eaton J.W., Brunk U.T. (2000) Protection against oxidant-mediated lysosomal rupture: a new anti-apoptotic activity of bcl-2? FEBS Lett. 485, 104-108.
48. Zhao M., Eaton J.W., Brunk U.T. (2001) Bcl-2 phosphorylation is required for inhibition of oxidative stress-induced lysosomal leak and ensuing apoptosis. FEBS Lett. 509, 405-412.