Lysosome-mediated apoptosis is associated with cathepsin d-specific processing of bid at Phe24, Trp48, and Phe183

Annals of Clinical and Laboratory Science

Volumn 42, Issue 3, 2012, Pages 231-242

  Appelqvist, Hanna ^a   Johansson, Ann Charlotte ^a   Linderoth, Emma ^a,e   Johansson, Uno ^a   Antonsson, Bruno ^b   Steinfeld, Robert ^c   Kågedal, Katarina ^a   Öllinger, Karin ^a,d  

^a LINKÖPING UNIVERSITY   (Sweden)

^b MERCK SERONO S A   (Switzerland)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d Department of Clinical Immunology and Transfusion Medicine   (Sweden)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN D; CYTOCHROME C; PHENYLALANINE; PROTEIN BAX; PROTEIN BID; TRYPTOPHAN;

ACIDIFICATION; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; FIBROBLAST; LYSOSOME; LYSOSOME MEMBRANE; MEMBRANE PERMEABILITY; MICROINJECTION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; RAT; SIGNAL TRANSDUCTION;

14-3-3 PROTEINS; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CATHEPSIN D; HUMANS; INTRACELLULAR MEMBRANES; LYSOSOMES; MICE; MITOCHONDRIA; PERMEABILITY; PHENYLALANINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOLYSIS; RATS; RATS, SPRAGUE-DAWLEY; STAUROSPORINE; SUBSTRATE SPECIFICITY; TRYPTOPHAN;

EID: 84868657087     PISSN: 00917370     EISSN: 15508080     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Roberg K, Johansson U, Öllinger K. Lysosomal release of cathepsin D precedes relocation of cytochrome c and loss of mitochondrial transmembrane potential during apoptosis induced by oxidative stress. Free Radic Biol Med. 1999;27(11-12):1228-1237.
2. Guicciardi ME, Leist M, Gores GJ. Lysosomes in cell death. Oncogene. 2004;23(16):2881-2890.
3. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Mol Cell. 2010;37(3):299-310.
4. Sawada M, Sun W, Hayes P, Leskov K, Boothman DA, Matsuyama S. Ku70 suppresses the apoptotic translocation of Bax to mitochondria. Nat Cell Biol. 2003;5(4):320-329.
5. Nomura M, Shimizu S, Sugiyama T, Narita M, Ito T, Matsuda H, et al. 14-3-3 Interacts directly with and negatively regulates pro-apoptotic Bax. J Biol Chem. 2003;278(3):2058-2065.
6. Samuel T, Weber HO, Rauch P, Verdoodt B, Eppel JT, McShea A, et al. The G2/M regulator 14-3-3sigma prevents apoptosis through sequestration of Bax. J Biol Chem. 2001;276(48):45201-45206.
7. Won J, Kim DY, La M, Kim D, Meadows GG, Joe CO. Cleavage of 14-3-3 protein by caspase-3 facilitates bad interaction with Bcl-x(L) during apoptosis. J Biol Chem. 2003;278(21):19347-19351.
8. Kuzelova K, Grebenova D, Pluskalova M, Kavan D, Halada P, Hrkal Z. Isoform-specific cleavage of 14-3-3 proteins in apoptotic JURL-MK1 cells. J Cell Biochem. 2009;106(4):673-681.
9. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol. 1999;144(5):891-901.
10. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, et al. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 2000;14(16):2060-2071.
11. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 1998;94(4):491-501.
12. Barry M, Heibein JA, Pinkoski MJ, Lee SF, Moyer RW, Green DR, et al. Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid. Mol Cell Biol. 2000;20(11):3781-3794.
13. Chen M, He H, Zhan S, Krajewski S, Reed JC, Gottlieb RA. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J Biol Chem. 2001;276(33):30724-30728.
14. Cirman T, Oresic K, Mazovec GD, Turk V, Reed JC, Myers RM, et al. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papainlike lysosomal cathepsins. J Biol Chem. 2004;279(5):3578-3587.
15. Droga-Mazovec G, Bojic L, Petelin A, Ivanova S, Romih R, Repnik U, et al. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J Biol Chem. 2008;283(27):19140-19150.
16. Kågedal K, Johansson U, Öllinger K. The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J. 2001;15(9):1592-1594.
17. Johansson AC, Steen H, Öllinger K, Roberg K. Cathepsin D mediates cytochrome c release and caspase activation in human fibroblast apoptosis induced by staurosporine. Cell Death Differ. 2003;10(11):1253-1259.
18. Roberg K, Kågedal K, Öllinger K. Microinjection of cathepsin D induces caspase-dependent apoptosis in fibroblasts. Am J Pathol. 2002;161(1):89-96.
19. Heinrich M, Neumeyer J, Jakob M, Hallas C, Tchikov V, Winoto-Morbach S, et al. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ. 2004;11(5):550-563.
20. Caruso JA, Mathieu PA, Joiakim A, Zhang H, Reiners JJ, Jr. Aryl hydrocarbon receptor modulation of tumor necrosis factor-alpha-induced apoptosis and lysosomal disruption in a hepatoma model that is caspase-8-independent. J Biol Chem. 2006;281(16):10954-10967.
21. Gan Y, Zhao X, Hu J, Wang ZG, Zhao XT. HCCS1 overexpression induces apoptosis via cathepsin D and intracellular calcium, and HCCS1 disruption in mice causes placental abnormality. Cell Death Differ. 2008;15(9):1481-1490.
22. Yin XM, Wang K, Gross A, Zhao Y, Zinkel S, Klocke B, et al. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature. 1999;400(6747):886-891.
23. Steinfeld R, Reinhardt K, Schreiber K, Hillebrand M, Kraetzner R, Bruck W, et al. Cathepsin D deficiency is associated with a human neurodegenerative disorder. Am J Hum Genet. 2006;78(6):988-998.
24. Bivik C and Öllinger K. JNK mediates UVB-induced apoptosis upstream lysosomal membrane permeabilization and Bcl-2 family proteins. Apoptosis. 2008;13(9):1111-1120.
25. Appelqvist H, Nilsson C, Garner B, Brown AJ, Kågedal K, Öllinger K. Attenuation of the lysosomal death pathway by lysosomal cholesterol accumulation. Am J Pathol. 2011;178(2):629-639.
26. Nilsson C, Kågedal K, Johansson U, Öllinger K. Analysis of cytosolic and lysosomal pH in apoptotic cells by flow cytometry. Methods Cell Sci. 2003;25(3-4):185-194.
27. Kudla G, Montessuit S, Eskes R, Berrier C, Martinou JC, Ghazi A, et al. The destabilization of lipid membranes induced by the C-terminal fragment of caspase 8-cleaved bid is inhibited by the N-terminal fragment. J Biol Chem. 2000;275(30):22713-22718.
28. Roucou X, Montessuit S, Antonsson B, Martinou JC. Bax oligomerization in mitochondrial membranes requires tBid (caspase-8-cleaved Bid) and a mitochondrial protein. Biochem J. 2002;368(Pt 3):915-921.
29. Kågedal K, Johansson AC, Johansson U, Heimlich G, Roberg K, Wang NS, et al. Lysosomal membrane permeabilization during apoptosis - involvement of Bax? Int J Exp Pathol. 2005;86(5):309-321.
30. Johansson AC, Norberg-Spaak L, Roberg K. Role of lysosomal cathepsins in naphthazarin- and Fas-induced apoptosis in oral squamous cell carcinoma cells. Acta Otolaryngol. 2006;126(1):70-81.
31. Gottlieb RA, Nordberg J, Skowronski E, Babior BM. Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc Natl Acad Sci U S A. 1996;93(2):654-658.
32. Matsuyama S, Llopis J, Deveraux QL, Tsien RY, Reed JC. Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat Cell Biol. 2000;2(6):318-325.
33. Nilsson C, Johansson U, Johansson AC, Kågedal K, Öllinger K. Cytosolic acidification and lysosomal alkalinization during TNF-alpha induced apoptosis in U937 cells. Apoptosis. 2006;11(7):1149-1159.
34. Barrett AJ. Human cathepsin D. Adv Exp Med Biol. 1977;95:291-300.
35. Deiss LP, Galinka H, Berissi H, Cohen O, Kimchi A. Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J. 1996;15(15):3861-3870.
36. Öllinger K. Inhibition of cathepsin D prevents free-radical-induced apoptosis in rat cardiomyocytes. Arch Biochem Biophys. 2000;373(2):346-351.
37. Bidére N, Lorenzo HK, Carmona S, Laforge M, Harper F, Dumont C, et al. Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem. 2003;278(33):31401-31411.
38. Emert-Sedlak L, Shangary S, Rabinovitz A, Miranda MB, Delach SM, Johnson DE. Involvement of cathepsin D in chemotherapy-induced cytochrome c release, caspase activation, and cell death. Mol Cancer Ther. 2005;4(5):733-742.
39. Beaujouin M, Baghdiguian S, Glondu-Lassis M, Berchem G, Liaudet-Coopman E. Overexpression of both catalytically active and -inactive cathepsin D by cancer cells enhances apoptosis-dependent chemo-sensitivity. Oncogene. 2006;25(13):1967-1973.
40. Schestkowa O, Geisel D, Jacob R, Hasilik A. The catalytically inactive precursor of cathepsin D induces apoptosis in human fibroblasts and HeLa cells. J Cell Biochem. 2007;101(6):1558-1566.
41. Laforge M, Petit F, Estaquier J, Senik A. Commitment to apoptosis in CD4(+) T lymphocytes productively infected with human immunodeficiency virus type 1 is initiated by lysosomal membrane permeabilization, itself induced by the isolated expression of the viral protein Nef. J Virol. 2007;81(20):11426-11440.
42. Vogel S, Raulf N, Bregenhorn S, Biniossek ML, Maurer U, Czabotar P, et al. Cytosolic Bax: Does it require binding proteins to keep its pro-apoptotic activity in check? J Biol Chem. 2012.
43. Stoka V, Turk V, Turk B. Lysosomal cysteine cathepsins: signaling pathways in apoptosis. Biol Chem. 2007;388(6):555-560.
44. Deng Y, Ren X, Yang L, Lin Y, Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell. 2003;115(1):61-70.
45. Dietrich N, Thastrup J, Holmberg C, Gyrd-Hansen M, Fehrenbacher N, Lademann U, et al. JNK2 mediates TNFinduced cell death in mouse embryonic fibroblasts via regulation of both caspase and cathepsin protease pathways. Cell Death Differ. 2004;11(3):301-313.
46. Werneburg NW, Guicciardi ME, Bronk SF, Kaufmann SH, Gores GJ. Tumor necrosis factor-related apoptosis-inducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins. J Biol Chem. 2007;282(39):28960-28970.
47. Sanvicens N and Cotter TG. Ceramide is the key mediator of oxidative stress-induced apoptosis in retinal photoreceptor cells. J Neurochem. 2006;98(5):1432-1444.
48. Yin XM. Bid, a BH3-only multi-functional molecule, is at the cross road of life and death. Gene. 2006;369:7-19.