Regulation of apoptosis-associated lysosomal membrane permeabilization

Apoptosis

Volumn 15, Issue 5, 2010, Pages 527-540

  Johansson, Ann Charlotte ^a   Appelqvist, Hanna ^b   Nilsson, Cathrine ^a,b   Kågedal, Katarina ^b   Roberg, Karin ^a,b   Öllinger, Karin ^b  

^a LINKÖPING UNIVERSITY HOSPITAL   (Sweden)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Calpains; Caspases; Hsp; LAMP; Lysosomal release; Lysosome

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; AMYLOID BETA PROTEIN; ANTIOXIDANT; APOLIPOPROTEIN; AROMATIC HYDROCARBON RECEPTOR; BIM PROTEIN; CALPAIN; CASPASE; CATHEPSIN; CHOLESTEROL; GRANULYSIN; HEAT SHOCK PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; NEF PROTEIN; PHOSPHOLIPASE A2; PHOSPHOTRANSFERASE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; PROTEIN MCL 1; PROTEIN P53; PROTEINASE; REACTIVE OXYGEN METABOLITE; SPHINGOMYELIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; BACTERIAL INFECTION; CELL DEATH; CELL FATE; CELL PERMEABILIZATION; LIPID COMPOSITION; LIPID MEMBRANE; LIPID PEROXIDATION; LYSOSOME MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VIRUS INFECTION;

ANIMALS; APOPTOSIS; CATHEPSINS; CHOLESTEROL; HEAT-SHOCK PROTEINS; INTRACELLULAR MEMBRANES; LYSOSOMES; MYOCYTES, CARDIAC; PEPTIDE HYDROLASES; PERMEABILITY; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77951666702     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-009-0452-5     Document Type: Review

References (149)

1. C de Duve BC Pressman R Gianetto R Wattiaux F Applemans 1955 Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue Biochem J 60 604 617
2. C de Duve 1983 Lysosomes revisited Eur J Biochem 137 391 397 6319122 10.1111/j.1432-1033.1983.tb07841.x
3. B Turk V Stoka 2007 Protease signalling in cell death: caspases versus cysteine cathepsins FEBS Lett 581 2761 2767 17544407 10.1016/j.febslet.2007.05. 038 1:CAS:528:DC%2BD2sXmtlWit7k%3D (Pubitemid 46874395)
4. de Duve C (1959) Lysosomes, a new group of cytoplasmic particles. In: Hayashi T (ed) Subcellular particles. Ronald Press, New York, pp 128-159
5. K Roberg K Öllinger 1998 Oxidative stress causes relocation of the lysosomal enzyme cathepsin D with ensuing apoptosis in neonatal rat cardiomyocytes Am J Pathol 152 1151 1156 9588882 1:CAS:528:DyaK1cXjtlSnurk%3D
6. LP Deiss H Galinka H Berissi O Cohen A Kimchi 1996 Cathepsin D protease mediates programmed cell death induced by interferon-γ, Fas/APO-1 and TNF-α EMBO J 15 3861 3870 8670891 1:CAS:528:DyaK28XltFert78%3D
7. GS Wu P Saftig C Peters WS El-Deiry 1998 Potential role for cathepsin D in p53-dependent tumor suppression and chemosensitivity Oncogene 16 2177 2183 9619826 10.1038/sj.onc.1201755 1:CAS:528:DyaK1cXjtFegtL0%3D
8. UT Brunk H Dalen K Roberg HB Hellquist 1997 Photo-oxidative disruption of lysosomal membranes causes apoptosis of cultured human fibroblasts Free Radic Biol Med 23 616 626 9215807 10.1016/S0891-5849(97)00007-5 1:CAS:528: DyaK2sXksFajsLk%3D (Pubitemid 27287345)
9. UT Brunk I Svensson 1999 Oxidative stress, growth factor starvation and Fas activation may all cause apoptosis through lysosomal leak Redox Rep 4 3 11 10714269 10.1179/135100099101534675 1:STN:280:DC%2BD3c7nvVKntQ%3D%3D
10. K Kågedal M Zhao I Svensson UT Brunk 2001 Sphingosine-induced apoptosis is dependent on lysosomal proteases Biochem J 359 335 343 11583579 10.1042/0264-6021:3590335 (Pubitemid 32999777)
11. W Li XM Yuan G Nordgren, et al. 2000 Induction of cell death by the lysosomotropic detergent MSDH FEBS Lett 470 35 39 10722841 10.1016/S0014- 5793(00)01286-2 1:CAS:528:DC%2BD3cXhslaltrY%3D (Pubitemid 30155619)
12. 2 is a consequence of lysosomal rupture Biochem J 356 549 555 11368784 10.1042/0264-6021:3560549 1:CAS:528:DC%2BD3MXks1alurc%3D (Pubitemid 32532368)
13. P Boya G Kroemer 2008 Lysosomal membrane permeabilization in cell death Oncogene 27 6434 6451 18955971 10.1038/onc.2008.310 1:CAS:528:DC%2BD1cXht12ltLvF
14. CE Chwieralski T Welte F Bühling 2006 Cathepsin-regulated apoptosis Apoptosis 11 143 149 16502253 10.1007/s10495-006-3486-y 1:CAS:528: DC%2BD28XhvVSrtb0%3D (Pubitemid 43291015)
15. ME Guicciardi M Leist GJ Gores 2004 Lysosomes in cell death Oncogene 23 2881 2890 15077151 10.1038/sj.onc.1207512 1:CAS:528:DC%2BD2cXivFKms7w%3D (Pubitemid 38638850)
16. V Stoka V Turk B Turk 2007 Lysosomal cysteine cathepsins: signaling pathways in apoptosis Biol Chem 388 555 560 17552902 10.1515/BC.2007.064 1:CAS:528:DC%2BD2sXmsFeqtLg%3D (Pubitemid 46883446)
17. T Kirkegaard M Jäättelä 2009 Lysosomal involvement in cell death and cancer Biochim Biophys Acta 1793 746 754 18948147 10.1016/j.bbamcr.2008.09.008 1:CAS:528:DC%2BD1MXjslOltrw%3D
18. G Kroemer M Jaattela 2005 Lysosomes and autophagy in cell death control Nat Rev Cancer 5 886 897 16239905 10.1038/nrc1738 1:CAS:528:DC%2BD2MXht1Witb3L (Pubitemid 41746033)
19. H Zhang C Zhong L Shi Y Guo Z Fan 2009 Granulysin induces cathepsin B release from lysosomes of target tumor cells to attack mitochondria through processing of bid leading to Necroptosis J Immunol 182 6993 7000 19454696 10.4049/jimmunol.0802502 1:CAS:528:DC%2BD1MXmtVKqsLk%3D
20. K Roberg K Kågedal K Öllinger 2002 Microinjection of cathepsin D induces caspase-dependent apoptosis in fibroblasts Am J Pathol 161 89 96 12107093 1:CAS:528:DC%2BD38Xlsl2ksr8%3D
21. O Schestkowa D Geisel R Jacob A Hasilik 2007 The catalytically inactive precursor of cathepsin D induces apoptosis in human fibroblasts and HeLa cells J Cell Biochem 101 1558 1566 17340625 10.1002/jcb.21269 1:CAS:528: DC%2BD2sXpt1ansr4%3D (Pubitemid 47242783)
22. CA Bivik PK Larsson KM Kågedal IK Rosdahl KM Öllinger 2006 UVA/B-induced apoptosis in human melanocytes involves translocation of cathepsins and Bcl-2 family members J Invest Dermatol 126 1119 1127 16528366 10.1038/sj.jid.5700124 1:CAS:528:DC%2BD28XjsFSru7k%3D
23. E Nilsson R Ghassemifar UT Brunk 1997 Lysosomal heterogeneity between and within cells with respect to resistance against oxidative stress Histochem J 29 857 865 9466153 10.1023/A:1026441907803 1:CAS:528:DyaK1cXnslSnsw%3D%3D
24. K Ono SO Kim J Han 2003 Susceptibility of lysosomes to rupture is a determinant for plasma membrane disruption in tumor necrosis factor alpha-induced cell death Mol Cell Biol 23 665 676 12509464 10.1128/MCB.23.2.665- 676.2003 1:CAS:528:DC%2BD3sXjslajsQ%3D%3D (Pubitemid 36050559)
25. R Blomgran L Zheng O Stendahl 2007 Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization J Leukoc Biol 81 1213 1223 17264306 10.1189/jlb.0506359 1:CAS:528:DC%2BD2sXlsVWnurs%3D (Pubitemid 46702040)
26. K Kågedal AC Johansson U Johansson, et al. 2005 Lysosomal membrane permeabilization during apoptosis-involvement of Bax? Int J Exp Pathol 86 309 321 16191103 10.1111/j.0959-9673.2005.00442.x (Pubitemid 41413626)
27. J Nylandsted M Gyrd-Hansen A Danielewicz, et al. 2004 Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization J Exp Med 200 425 435 15314073 10.1084/jem.20040531 1:CAS:528:DC%2BD2cXmvFehtrw%3D (Pubitemid 39121900)
28. Q Miao Y Sun T Wei, et al. 2008 Chymotrypsin B cached in rat liver lysosomes and involved in apoptotic regulation through a mitochondrial pathway J Biol Chem 283 8218 8228 18211899 10.1074/jbc.M709789200 1:CAS:528: DC%2BD1cXjsFCgsr0%3D
29. C Nilsson U Johansson AC Johansson K Kågedal K Öllinger 2006 Cytosolic acidification and lysosomal alkalinization during TNF-alpha induced apoptosis in U937 cells Apoptosis 11 1149 1159 16699952 10.1007/s10495-006-7108- 5 1:CAS:528:DC%2BD28Xmslantr4%3D (Pubitemid 44035964)
30. B Mirnikjoo K Balasubramanian AJ Schroit 2009 Mobilization of lysosomal calcium regulates the externalization of phosphatidylserine during apoptosis J Biol Chem 284 6918 6923 19126538 10.1074/jbc.M805288200 1:CAS:528: DC%2BD1MXislWru7s%3D
31. NW Werneburg ME Guicciardi SF Bronk GJ Gores 2002 Tumor necrosis factor-alpha-associated lysosomal permeabilization is cathepsin B dependent Am J Physiol-Gastroint Liver Physiol 283 G947 G956 1:CAS:528:DC%2BD38XotV2qsLg%3D
32. N Bidère HK Lorenzo S Carmona, et al. 2003 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 278 31401 31411 12782632 10.1074/jbc.M301911200 1:CAS:528: DC%2BD3sXmtFCjsrY%3D (Pubitemid 36994661)
33. AV Birk EJ Dubovi L Cohen-Gould R Donis HH Szeto 2008 Cytoplasmic vacuolization responses to cytopathic bovine viral diarrhoea virus Virus Res 132 76 85 18054406 10.1016/j.virusres.2007.10.017 1:CAS:528:DC%2BD1cXitVOhurY%3D (Pubitemid 351232085)
34. M Di Piazza C Mader K Geletneky, et al. 2007 Cytosolic activation of cathepsins mediates parvovirus H-1-induced killing of cisplatin and TRAIL-resistant glioma cells J Virol 81 4186 4198 17287256 10.1128/JVI.02601-06 1:CAS:528:DC%2BD2sXksVKksLY%3D (Pubitemid 46586913)
35. DW Kaznelson S Bruun A Monrad, et al. 2004 Simultaneous human papilloma virus type 16 E7 and cdk inhibitor p21 expression induces apoptosis and cathepsin B activation Virology 320 301 312 15016552 10.1016/j.virol.2003.12.018 1:CAS:528:DC%2BD2cXhvVOqtr4%3D (Pubitemid 38315156)
36. + 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 81 11426 11440 17670831 10.1128/JVI.00597-07 1:CAS:528:DC%2BD2sXhtFeltL3M (Pubitemid 47536113)
37. MP O'Sullivan S O'Leary DM Kelly J Keane 2007 A caspase-independent pathway mediates macrophage cell death in response to Mycobacterium tuberculosis infection Infect Immun 75 1984 1993 17283090 10.1128/IAI.01107-06 1:CAS:528:DC%2BD2sXkt1Oht7o%3D (Pubitemid 46559468)
38. LR Prince SM Bianchi KM Vaughan, et al. 2008 Subversion of a lysosomal pathway regulating neutrophil apoptosis by a major bacterial toxin, pyocyanin J Immunol 180 3502 3511 18292577 1:CAS:528:DC%2BD1cXit1Okt7k%3D
39. Sandvig K (2003) Transport of toxins across intracellular membranes. In: Burns DL, Barbier JT, Iglewski BH (eds) Bacterial protein toxins. ASM, Washington, pp 157-172
40. K Sandvig S Olsnes 1980 Diphtheria toxin entry into cells is facilitated by low pH J Cell Biol 87 828 832 7462324 10.1083/jcb.87.3.828 1:CAS:528:DyaL3MXpslGmtA%3D%3D (Pubitemid 11161814)
41. JJ Donovan MI Simon RK Draper M Montal 1981 Diphtheria toxin forms transmembrane channels in planar lipid bilayers Proc Natl Acad Sci U S A 78 172 176 6264431 10.1073/pnas.78.1.172 1:CAS:528:DyaL3MXpslKjuw%3D%3D (Pubitemid 11131259)
42. BL Kagan A Finkelstein M Colombini 1981 Diphtheria toxin fragment forms large pores in phospholipid bilayer membranes Proc Natl Acad Sci U S A 78 4950 4954 6272284 10.1073/pnas.78.8.4950 1:CAS:528:DyaL3MXls1emsbg%3D
43. P Boquet E Duflot 1982 Tetanus toxin fragment forms channels in lipid vesicles at low pH Proc Natl Acad Sci U S A 79 7614 7618 6296842 10.1073/pnas.79.24.7614 1:CAS:528:DyaL3sXms1yhsg%3D%3D (Pubitemid 13173155)
44. JJ Donovan JL Middlebrook 1986 Ion-conducting channels produced by botulinum toxin in planar lipid membranes Biochemistry 25 2872 2876 2424493 10.1021/bi00358a020 1:CAS:528:DyaL28XitVWqsbs%3D
45. RO Blaustein TM Koehler RJ Collier A Finkelstein 1989 Anthrax toxin: channel-forming activity of protective antigen in planar phospholipid bilayers Proc Natl Acad Sci U S A 86 2209 2213 2467303 10.1073/pnas.86.7.2209 1:CAS:528:DyaL1MXitVOmtrg%3D (Pubitemid 19102481)
46. SW Muchmore M Sattler H Liang, et al. 1996 X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death Nature 381 335 341 8692274 10.1038/381335a0 1:CAS:528:DyaK28XjtFOmtro%3D (Pubitemid 26156091)
47. M Suzuki RJ Youle N Tjandra 2000 Structure of Bax: coregulation of dimer formation and intracellular localization Cell 103 645 654 11106734 10.1016/S0092-8674(00)00167-7 1:CAS:528:DC%2BD3cXot1Gnu7c%3D
48. AE Feldstein NW Werneburg A Canbay, et al. 2004 Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathway Hepatology 40 185 194 15239102 10.1002/hep.20283 1:CAS:528:DC%2BD2cXmtlSgur0%3D (Pubitemid 38868937)
49. AE Feldstein NW Werneburg Z Li SF Bronk GJ Gores 2006 Bax inhibition protects against free fatty acid-induced lysosomal permeabilization Am J Physiol-Gastroint Liver Physiol 290 G1339 G1346 10.1152/ajpgi.00509.2005 1:CAS:528:DC%2BD28XlvVeitr4%3D (Pubitemid 43788317)
50. NW Werneburg ME Guicciardi SF Bronk SH Kaufmann GJ Gores 2007 Tumor necrosis factor-related apoptosis-inducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins J Biol Chem 282 28960 28970 17686764 10.1074/jbc.M705671200 1:CAS:528:DC%2BD2sXhtVOmtbjJ (Pubitemid 47606073)
51. R Castino C Peracchio A Salini, et al. 2009 Chemotherapy drug response in ovarian cancer cells strictly depends on a cathepsin D-bax activation loop J Cell Mol Med 13 1096 1109 10.1111/j.1582-4934.2008.00435.x 1:CAS:528: DC%2BD1MXhtVSnurfN
52. NW Werneburg ME Guicciardi XM Yin GJ Gores 2004 TNF-alpha-mediated lysosomal permeabilization is FAN and caspase 8/Bid dependent Am J Physiol-Gastroint Liver Physiol 287 G436 G443 10.1152/ajpgi.00019.2004 1:CAS:528:DC%2BD2cXmvVKnu74%3D (Pubitemid 38955264)
53. RJ Youle A Strasser 2008 The BCL-2 protein family: opposing activities that mediate cell death Nat Rev Mol Cell Biol 9 47 59 18097445 10.1038/nrm2308 1:CAS:528:DC%2BD2sXhsVKrsrrP
54. P Boya K Andreau D Poncet, et al. 2003 Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion J Exp Med 197 1323 1334 12756268 10.1084/jem.20021952 1:CAS:528:DC%2BD3sXktVGgtbY%3D (Pubitemid 36617779)
55. XM Yuan W Li H Dalen, et al. 2002 Lysosomal destabilization in p53-induced apoptosis Proc Natl Acad Sci U S A 99 6286 6291 11959917 10.1073/pnas.092135599 1:CAS:528:DC%2BD38XjslWnsbk%3D (Pubitemid 34493304)
56. N Li Y Zheng W Chen, et al. 2007 Adaptor protein LAPF recruits phosphorylated p53 to lysosomes and triggers lysosomal destabilization in apoptosis Cancer Res 67 11176 11185 18056442 10.1158/0008-5472.CAN-07-2333 1:CAS:528:DC%2BD2sXhtlyiurnJ (Pubitemid 350248542)
57. W Chen N Li T Chen, et al. 2005 The lysosome-associated apoptosis-inducing protein containing the pleckstrin homology (PH) and FYVE domains (LAPF), representative of a novel family of PH and FYVE domain-containing proteins, induces caspase-independent apoptosis via the lysosomal-mitochondrial pathway J Biol Chem 280 40985 40995 16188880 10.1074/jbc.M502190200 1:CAS:528:DC%2BD2MXht1Oqt73N (Pubitemid 41780594)
58. A Gowran VA Campbell 2008 A role for p53 in the regulation of lysosomal permeability by delta 9-tetrahydrocannabinol in rat cortical neurones: implications for neurodegeneration J Neurochem 105 1513 1524 18248609 10.1111/j.1471-4159.2008.05278.x 1:CAS:528:DC%2BD1cXmsVOltrw%3D (Pubitemid 351590812)
59. MP Fogarty RM McCormack J Noonan D Murphy A Gowran VA Campbell 2008 A role for p53 in the beta-amyloid-mediated regulation of the lysosomal system Neurobiol Aging 10.1016/j.neurobiolaging.2008.09.018 19059678
60. JE Chipuk T Kuwana L Bouchier-Hayes, et al. 2004 Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis Science 303 1010 1014 14963330 10.1126/science.1092734 1:CAS:528:DC%2BD2cXhtlWnu7o%3D (Pubitemid 38209704)
61. M Mihara S Erster A Zaika, et al. 2003 p53 has a direct apoptogenic role at the mitochondria Mol Cell 11 577 590 12667443 10.1016/S1097-2765(03)00050-9 1:CAS:528:DC%2BD3sXjtVWktrk%3D (Pubitemid 36385115)
62. E Oda R Ohki H Murasawa, et al. 2000 Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis Science 288 1053 1058 10807576 10.1126/science.288.5468.1053 1:CAS:528:DC%2BD3cXjsVSnsbg%3D (Pubitemid 30324238)
63. J Yu L Zhang PM Hwang KW Kinzler B Vogelstein 2001 PUMA induces the rapid apoptosis of colorectal cancer cells Mol Cell 7 673 682 11463391 10.1016/S1097-2765(01)00213-1 1:CAS:528:DC%2BD3MXivVCmtLg%3D (Pubitemid 32706358)
64. K Nakano KH Vousden 2001 PUMA, a novel proapoptotic gene, is induced by p53 Mol Cell 7 683 694 11463392 10.1016/S1097-2765(01)00214-3 1:CAS:528:DC%2BD3MXivVCmtLk%3D (Pubitemid 32706359)
65. PK Wäster KM Öllinger 2009 Redox-dependent translocation of p53 to mitochondria or nucleus in human melanocytes after UVA- and UVB-induced apoptosis J Invest Dermatol 129 1769 1781 19158844 10.1038/jid.2008.421 1:CAS:528:DC%2BD1MXntFCisLo%3D
66. C Paris J Bertoglio J Bréard 2007 Lysosomal and mitochondrial pathways in miltefosine-induced apoptosis in U937 cells Apoptosis 12 1257 1267 17347868 10.1007/s10495-007-0052-1 1:CAS:528:DC%2BD2sXmtlShtLg%3D (Pubitemid 46890382)
67. ME Guicciardi J Deussing H Miyoshi, et al. 2000 Cathepsin B contributes to TNF-α-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c J Clin Invest 106 1127 1137 11067865 10.1172/JCI9914 1:CAS:528:DC%2BD3cXnvFyqur4%3D
68. M Gyrd-Hansen T Farkas N Fehrenbacher, et al. 2006 Apoptosome-independent activation of the lysosomal cell death pathway by caspase-9 Mol Cell Biol 26 7880 7891 16966373 10.1128/MCB.00716-06 1:CAS:528:DC%2BD28XhtFemur%2FO (Pubitemid 44630989)
69. K van Nierop FJ Muller J Stap CJ Van Noorden M van Eijk C de Groot 2006 Lysosomal destabilization contributes to apoptosis of germinal center B-lymphocytes J Histochem Cytochem 54 1425 1435 16957167 10.1369/jhc.6A6967.2006 1:CAS:528:DC%2BD28Xht1CnurvE (Pubitemid 44788827)
70. WC Huang YS Lin CL Chen CY Wang WH Chiu CF Lin 2009 Glycogen synthase kinase-3beta mediates endoplasmic reticulum stress-induced lysosomal apoptosis in leukemia J Pharmacol Exp Ther 329 524 531 19188482 10.1124/jpet.108.148122 1:CAS:528:DC%2BD1MXlt1Omu7k%3D
71. L prevents TRAIL-induced apoptosis of hepatocellular carcinoma cells by inhibiting the lysosomal pathway of apoptosis Am J Physiol-Gastroint Liver Physiol 292 G1337 G1346 10.1152/ajpgi.00497.2006 1:CAS:528:DC%2BD2sXls1yitbk%3D (Pubitemid 47084667)
72. N Liu SM Raja F Zazzeroni, et al. 2003 NF-kappaB protects from the lysosomal pathway of cell death EMBO J 22 5313 5322 14517268 10.1093/emboj/cdg510 1:CAS:528:DC%2BD3sXnvVequ78%3D (Pubitemid 37222050)
73. YW Yap M Whiteman BH Bay, et al. 2006 Hypochlorous acid induces apoptosis of cultured cortical neurons through activation of calpains and rupture of lysosomes J Neurochem 98 1597 1609 16923169 10.1111/j.1471-4159.2006.03996.x 1:CAS:528:DC%2BD28XhtVymtLnF (Pubitemid 44200449)
74. T Yamashima TC Saido M Takita, et al. 1996 Transient brain ischaemia provokes Ca2+, PIP2 and calpain responses prior to delayed neuronal death in monkeys Eur J Neurosci 8 1932 1944 8921284 10.1111/j.1460-9568.1996.tb01337.x 1:STN:280:DyaK2s%2FnvFGksQ%3D%3D
75. T Yamashima AB Tonchev T Tsukada, et al. 2003 Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates Hippocampus 13 791 800 14620874 10.1002/hipo.10127 1:CAS:528:DC%2BD3sXpvVygsbg%3D (Pubitemid 37407965)
76. JA Windelborn P Lipton 2008 Lysosomal release of cathepsins causes ischemic damage in the rat hippocampal slice and depends on NMDA-mediated calcium influx, arachidonic acid metabolism, and free radical production J Neurochem 106 56 69 18363826 10.1111/j.1471-4159.2008.05349.x 1:CAS:528:DC%2BD1cXot1Ohurk%3D (Pubitemid 351840201)
77. T Yamashima Y Kohda K Tsuchiya, et al. 1998 Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis' Eur J Neurosci 10 1723 1733 9751144 10.1046/j.1460-9568.1998.00184.x 1:STN:280:DyaK1cvitFOltg%3D%3D (Pubitemid 28327319)
78. JA Caruso PA Mathieu JJ Reiners Jr 2005 Sphingomyelins suppress the targeted disruption of lysosomes/endosomes by the photosensitizer NPe6 during photodynamic therapy Biochem J 392 325 334 15943580 10.1042/BJ20050313 1:CAS:528:DC%2BD2MXht1CrtLbN (Pubitemid 41796521)
79. D Kessel Y Luo P Mathieu JJ Reiners Jr 2000 Determinants of the apoptotic response to lysosomal photodamage Photochem Photobiol 71 196 200 10687394 10.1562/0031-8655(2000)071<0196:DOTART>2.0.CO;2 1:CAS:528: DC%2BD3cXhtF2mtrg%3D
80. JJ Reiners Jr JA Caruso P Mathieu B Chelladurai XM Yin D Kessel 2002 Release of cytochrome c and activation of pro-caspase-9 following lysosomal photodamage involves Bid cleavage Cell Death Differ 9 934 944 12181744 10.1038/sj.cdd.4401048 1:CAS:528:DC%2BD38XmtVOnu7w%3D (Pubitemid 35033432)
81. K Öllinger UT Brunk 1995 Cellular injury induced by oxidative stress is mediated through lysosomal damage Free Radic Biol Med 19 565 574 8529915 10.1016/0891-5849(95)00062-3
82. R Vene G Arena A Poggi, et al. 2007 Novel cell death pathways induced by N-(4-hydroxyphenyl)retinamide: therapeutic implications Mol Cancer Ther 6 286 298 17237288 10.1158/1535-7163.MCT-06-0346 1:CAS:528:DC%2BD2sXmsValug%3D%3D (Pubitemid 46206693)
83. A De Milito E Iessi M Logozzi, et al. 2007 Proton pump inhibitors induce apoptosis of human B-cell tumors through a caspase-independent mechanism involving reactive oxygen species Cancer Res 67 5408 5417 17545622 10.1158/0008-5472.CAN-06-4095 1:CAS:528:DC%2BD2sXmtVait7c%3D (Pubitemid 46997281)
84. B Garner W Li K Roberg UT Brunk 1997 On the cytoprotective role of ferritin in macrophages and its ability to enhance lysosomal stability Free Radic Res 27 487 500 9518065 10.3109/10715769709065788 1:CAS:528: DyaK1cXisVClsrk%3D
85. HL Persson KJ Nilsson UT Brunk 2001 Novel cellular defenses against iron and oxidation: ferritin and autophagocytosis preserve lysosomal stability in airway epithelium Redox Rep 6 57 63 11333118 10.1179/135100001101536049 1:CAS:528:DC%2BD3MXjsFSmurk%3D (Pubitemid 32331570)
86. HL Persson Z Yu O Tirosh JW Eaton UT Brunk 2003 Prevention of oxidant-induced cell death by lysosomotropic iron chelators Free Radic Biol Med 34 1295 1305 12726917 10.1016/S0891-5849(03)00106-0 1:CAS:528: DC%2BD3sXjt1KgsLg%3D (Pubitemid 36513971)
87. HL Persson T Kurz JW Eaton UT Brunk 2005 Radiation-induced cell death: importance of lysosomal destabilization Biochem J 389 877 884 15813701 10.1042/BJ20050271 1:CAS:528:DC%2BD2MXmsFCiur4%3D (Pubitemid 41117348)
88. Z Yu HL Persson JW Eaton UT Brunk 2003 Intralysosomal iron: a major determinant of oxidant-induced cell death Free Radic Biol Med 34 1243 1252 12726912 10.1016/S0891-5849(03)00109-6 1:CAS:528:DC%2BD3sXjt1KgsL8%3D (Pubitemid 36513967)
89. HL Persson 2005 Iron-dependent lysosomal destabilization initiates silica-induced apoptosis in murine macrophages Toxicol Lett 159 124 133 15949905 10.1016/j.toxlet.2005.05.002 1:CAS:528:DC%2BD2MXhtVartrfE (Pubitemid 41330931)
90. WJ Brown DB DeWald SD Emr H Plutner WE Balch 1995 Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells J Cell Biol 130 781 796 7642697 10.1083/jcb.130.4.781 1:CAS:528:DyaK2MXnsVymt7s%3D
91. SA Mousavi A Brech T Berg R Kjeken 2003 Phosphoinositide 3-kinase regulates maturation of lysosomes in rat hepatocytes Biochem J 372 861 869 12646047 10.1042/BJ20021136 1:CAS:528:DC%2BD3sXksVajsbc%3D (Pubitemid 36760399)
92. N Fehrenbacher M Philips 2009 Intracellular signaling: peripatetic Ras Curr Biol 19 R454 R457 19515353 10.1016/j.cub.2009.04.045 1:CAS:528: DC%2BD1MXntVGis7w%3D
93. N Fehrenbacher M Gyrd-Hansen B Poulsen, et al. 2004 Sensitization to the lysosomal cell death pathway upon immortalization and transformation Cancer Res 64 5301 5310 15289336 10.1158/0008-5472.CAN-04-1427 1:CAS:528: DC%2BD2cXmtF2murw%3D (Pubitemid 39006550)
94. LA Madge J-H Li J Choi JS Pober 2003 Inhibition of phosphatidylinositol 3-kinase sensitizes vascular endothelial cells to cytokine-initiated cathepsin-dependent apoptosis J Biol Chem 278 21295 21306 12663669 10.1074/jbc.M212837200 1:CAS:528:DC%2BD3sXkt1Witbk%3D (Pubitemid 36806445)
95. N Dietrich J Thastrup C Holmberg, et al. 2004 JNK2 mediates TNF-induced cell death in mouse embryonic fibroblasts via regulation of both caspase and cathepsin protease pathways Cell Death Differ 11 301 313 14685158 10.1038/sj.cdd.4401353 1:CAS:528:DC%2BD2cXht1CntLk%3D (Pubitemid 38313139)
96. C Bivik K Öllinger 2008 JNK mediates UVB-induced apoptosis upstream lysosomal membrane permeabilization and Bcl-2 family proteins Apoptosis 13 1111 1120 18651223 10.1007/s10495-008-0240-7 1:CAS:528:DC%2BD1cXps1ajsbo%3D
97. MP Fogarty EJ Downer V Campbell 2003 A role for c-Jun N-terminal kinase 1 (JNK1), but not JNK2, in the beta-amyloid-mediated stabilization of protein p53 and induction of the apoptotic cascade in cultured cortical neurons Biochem J 371 789 798 12534344 10.1042/BJ20021660 1:CAS:528:DC%2BD3sXjtFKmu7c%3D (Pubitemid 36578878)
98. N Fehrenbacher L Bastholm T Kirkegaard-Sorensen, et al. 2008 Sensitization to the lysosomal cell death pathway by oncogene-induced down-regulation of lysosome-associated membrane proteins 1 and 2 Cancer Res 68 6623 6633 18701486 10.1158/0008-5472.CAN-08-0463 1:CAS:528:DC%2BD1cXpslKmsr4%3D
99. HF Zhao X Wang GJ Zhang 2005 Lysosome destabilization by cytosolic extracts, putative involvement of Ca(2+)/phospholipase C FEBS Lett 579 1551 1556 15733872 10.1016/j.febslet.2005.01.061 1:CAS:528:DC%2BD2MXhslCisL4%3D (Pubitemid 40289211)
100. X Wang HF Zhao GJ Zhang 2006 Mechanism of cytosol phospholipase C and sphingomyelinase-induced lysosome destabilization Biochimie 88 913 922 16580116 10.1016/j.biochi.2006.02.005 1:CAS:528:DC%2BD28Xns12ks74%3D (Pubitemid 44142174)
101. JW Wang L Sun JS Hu YB Li GJ Zhang 2006 Effects of phospholipase A2 on the lysosomal ion permeability and osmotic sensitivity Chem Phys Lipids 144 117 126 16982042 10.1016/j.chemphyslip.2006.08.003 1:CAS:528:DC%2BD28Xht1elsrnM (Pubitemid 44737470)
102. X Wang LL Wang GJ Zhang 2006 Guanosine 5-[gamma-thio]triphosphate- mediated activation of cytosol phospholipase C caused lysosomal destabilization J Membr Biol 211 55 63 16988860 10.1007/s00232-006-0019-0 1:CAS:528: DC%2BD28XhtVWgtLbK (Pubitemid 44477360)
103. G Zhang YP Yi GJ Zhang 2006 Effects of arachidonic acid on the lysosomal ion permeability and osmotic stability J Bioenerg Biomembr 38 75 82 16732469 10.1007/s10863-006-9008-3 1:CAS:528:DC%2BD28XmvFeitr4%3D (Pubitemid 44078522)
104. JS Hu YB Li JW Wang L Sun GJ Zhang 2007 Mechanism of lysophosphatidylcholine-induced lysosome destabilization J Membr Biol 215 27 35 17510762 10.1007/s00232-007-9002-7 1:CAS:528:DC%2BD2sXot1yjtb8%3D (Pubitemid 47174614)
105. YP Yi X Wang G Zhang TS Fu GJ Zhang 2006 Phosphatidic acid osmotically destabilizes lysosomes through increased permeability to K+ and H+ Gen Physiol Biophys 25 149 160 16917129 1:CAS:528:DC%2BD28XhtVGitbjJ
106. M Zhao UT Brunk JW Eaton 2001 Delayed oxidant-induced cell death involves activation of phospholipase A2 FEBS Lett 509 399 404 11749963 10.1016/S0014-5793(01)03184-2 1:CAS:528:DC%2BD3MXptFymur8%3D (Pubitemid 34031968)
107. B Burlando B Marchi I Panfoli A Viarengo 2002 Essential role of Ca2+-dependent phospholipase A2 in estradiol-induced lysosome activation Am J Physiol Cell Physiol 283 C1461 C1468 12372807 1:CAS:528:DC%2BD38XovVOlsr4%3D
108. G Marone B Fimiani G Torella S Poto P Bianco M Condorelli 1983 Possible role of arachidonic acid and of phospholipase A2 in the control of lysosomal enzyme release from human polymorphonuclear leukocytes J Clin Lab Immunol 12 111 116 6644791 1:CAS:528:DyaL3sXmtFWjsL0%3D
109. B Marchi B Burlando MN Moore A Viarengo 2004 Mercury- and copper-induced lysosomal membrane destabilisation depends on [Ca2+]i dependent phospholipase A2 activation Aquat Toxicol 66 197 204 15036874 10.1016/j.aquatox.2003.09.003 1:CAS:528:DC%2BD2cXhsV2ksbg%3D (Pubitemid 38229254)
110. S Schutze T Machleidt D Adam, et al. 1999 Inhibition of receptor internalization by monodansylcadaverine selectively blocks p55 tumor necrosis factor receptor death domain signaling J Biol Chem 274 10203 10212 10187805 10.1074/jbc.274.15.10203 1:CAS:528:DyaK1MXis1GjtL0%3D (Pubitemid 29180892)
111. N Parent E Winstall M Beauchemin C Paquet GG Poirier R Bertrand 2009 Proteomic analysis of enriched lysosomes at early phase of camptothecin-induced apoptosis in human U-937 cells J Proteomics 72 960 973 19393779 10.1016/j.jprot.2009.04.003 1:CAS:528:DC%2BD1MXptlSrsrc%3D
112. YH Zeidan YA Hannun 2007 Activation of acid sphingomyelinase by protein kinase Cdelta-mediated phosphorylation J Biol Chem 282 11549 11561 17303575 10.1074/jbc.M609424200 1:CAS:528:DC%2BD2sXjvFagtbs%3D (Pubitemid 47100781)
113. K Ferlinz T Linke O Bartelsen M Weiler K Sandhoff 1999 Stimulation of lysosomal sphingomyelin degradation by sphingolipid activator proteins Chem Phys Lipids 102 35 43 11001559 10.1016/S0009-3084(99)00073-0 1:CAS:528: DyaK1MXmt1emt7s%3D (Pubitemid 29438657)
114. AJ Yang D Chandswangbhuvana T Shu A Henschen CG Glabe 1999 Intracellular accumulation of insoluble, newly synthesized abetan-42 in amyloid precursor protein-transfected cells that have been treated with Abeta1-42 J Biol Chem 274 20650 20656 10400697 10.1074/jbc.274.29.20650 1:CAS:528:DyaK1MXks1Ojtb4%3D (Pubitemid 29340429)
115. L Zheng K Kågedal N Dehvari, et al. 2009 Oxidative stress induces macroautophagy of amyloid beta-protein and ensuing apoptosis Free Radic Biol Med 46 422 429 19038331 10.1016/j.freeradbiomed.2008.10.043 1:CAS:528: DC%2BD1MXht1Wmuw%3D%3D
116. B Soreghan J Kosmoski C Glabe 1994 Surfactant properties of Alzheimer's A beta peptides and the mechanism of amyloid aggregation J Biol Chem 269 28551 28554 7961799 1:CAS:528:DyaK2cXmsFaqtrk%3D
117. A Lomakin DS Chung GB Benedek DA Kirschner DB Teplow 1996 On the nucleation and growth of amyloid beta-protein fibrils: detection of nuclei and quantitation of rate constants Proc Natl Acad Sci U S A 93 1125 1129 8577726 10.1073/pnas.93.3.1125 1:CAS:528:DyaK28Xptl2lsQ%3D%3D (Pubitemid 26054370)
118. S Forster L Scarlett JB Lloyd 1987 The effect of lysosomotropic detergents on the permeability properties of the lysosome membrane Biochim Biophys Acta 924 452 457 3297168 1:CAS:528:DyaL2sXlsVyks7s%3D
119. H Lin R Bhatia R Lal 2001 Amyloid beta protein forms ion channels: implications for Alzheimer's disease pathophysiology FASEB J 15 2433 2444 11689468 10.1096/fj.01-0377com 1:CAS:528:DC%2BD3MXoslSisrs%3D (Pubitemid 33063171)
120. A Quist I Doudevski H Lin, et al. 2005 Amyloid ion channels: a common structural link for protein-misfolding disease Proc Natl Acad Sci U S A 102 10427 10432 16020533 10.1073/pnas.0502066102 1:CAS:528:DC%2BD2MXntVSit7w%3D (Pubitemid 41061570)
121. ZS Ji RD Miranda YM Newhouse KH Weisgraber Y Huang RW Mahley 2002 Apolipoprotein E4 potentiates amyloid beta peptide-induced lysosomal leakage and apoptosis in neuronal cells J Biol Chem 277 21821 21828 11912196 10.1074/jbc.M112109200 1:CAS:528:DC%2BD38Xksl2js7c%3D (Pubitemid 34952334)
122. ZS Ji K Mullendorff IH Cheng RD Miranda Y Huang RW Mahley 2006 Reactivity of apolipoprotein E4 and amyloid beta peptide: lysosomal stability and neurodegeneration J Biol Chem 281 2683 2692 16298992 10.1074/jbc.M506646200 1:CAS:528:DC%2BD28XovVehsw%3D%3D (Pubitemid 43845731)
123. JA Caruso PA Mathieu A Joiakim H Zhang JJ Reiners Jr 2006 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 281 10954 10967 16446372 10.1074/jbc.M508383200 1:CAS:528: DC%2BD28XjsFWjsr0%3D (Pubitemid 43855518)
124. JA Caruso PA Mathieu A Joiakim, et al. 2004 Differential susceptibilities of murine hepatoma 1c1c7 and Tao cells to the lysosomal photosensitizer NPe6: influence of aryl hydrocarbon receptor on lysosomal fragility and protease contents Mol Pharmacol 65 1016 1028 15044632 10.1124/mol.65.4.1016 1:CAS:528:DC%2BD2cXivFaltbs%3D (Pubitemid 38420508)
125. K Vancompernolle F Van Herreweghe G Pynaert, et al. 1998 Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity FEBS Lett 438 150 158 9827536 10.1016/S0014-5793(98)01275-7 1:CAS:528:DyaK1cXnsFOmsbY%3D (Pubitemid 28529264)
126. M Jäättelä 1999 Escaping cell death: survival proteins in cancer Exp Cell Res 248 30 43 10094811 10.1006/excr.1999.4455 (Pubitemid 29393927)
127. C Bivik I Rosdahl K Öllinger 2007 Hsp70 protects against UVB induced apoptosis by preventing release of cathepsins and cytochrome c in human melanocytes Carcinogenesis 28 537 544 16950797 10.1093/carcin/bgl152 1:CAS:528:DC%2BD2sXjslOgu7Y%3D (Pubitemid 46523349)
128. PT Doulias P Kotoglou M Tenopoulou, et al. 2007 Involvement of heat shock protein-70 in the mechanism of hydrogen peroxide-induced DNA damage: the role of lysosomes and iron Free Radic Biol Med 42 567 577 17275689 10.1016/j.freeradbiomed.2006.11.022 (Pubitemid 46162124)
129. V Dudeja N Mujumdar P Phillips, et al. 2009 Heat shock protein 70 inhibits apoptosis in cancer cells through simultaneous and independent mechanisms Gastroenterology 136 1772 1782 19208367 10.1053/j.gastro.2009.01.070 1:CAS:528:DC%2BD1MXmtFajsrg%3D
130. T Kurz UT Brunk 2009 Autophagy of HSP70 and chelation of lysosomal iron in a non-redox-active form Autophagy 5 93 95 18989099 10.4161/auto.5.1.7248 1:CAS:528:DC%2BD1MXnvFCksLs%3D
131. T Gotoh K Terada S Oyadomari M Mori 2004 hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria Cell Death Differ 11 390 402 14752510 10.1038/sj.cdd. 4401369 1:CAS:528:DC%2BD2cXit12ntbk%3D (Pubitemid 38489417)
132. AR Stankiewicz G Lachapelle CP Foo SM Radicioni DD Mosser 2005 Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation J Biol Chem 280 38729 38739 16172114 10.1074/jbc.M509497200 1:CAS:528:DC%2BD2MXht1SktLjE (Pubitemid 43853776)
133. M Daugaard T Kirkegaard-Sørensen MS Ostenfeld, et al. 2007 Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer Cancer Res 67 2559 2567 17363574 10.1158/0008-5472. CAN-06-4121 1:CAS:528:DC%2BD2sXivV2nsrw%3D (Pubitemid 46548941)
134. M Zhao JW Eaton UT Brunk 2000 Protection against oxidant-mediated lysosomal rupture: a new anti-apoptotic activity of Bcl-2? FEBS Lett 485 104 108 11094149 10.1016/S0014-5793(00)02195-5 1:CAS:528:DC%2BD3cXotlGjsrw%3D
135. M Zhao JW Eaton UT Brunk 2001 Bcl-2 phosphorylation is required for inhibition of oxidative stress-induced lysosomal leak and ensuing apoptosis FEBS Lett 509 405 412 11749964 10.1016/S0014-5793(01)03185-4 1:CAS:528: DC%2BD3MXptFymurw%3D (Pubitemid 34031969)
136. B Halliwell 1999 Antioxidant defence mechanisms: from the beginning to the end (of the beginning) Free Radic Res 31 261 272 10517532 10.1080/10715769900300841 1:CAS:528:DyaK1MXmslGjsL4%3D (Pubitemid 29452853)
137. Y Yoshida Y Saito LS Jones Y Shigeri 2007 Chemical reactivities and physical effects in comparison between tocopherols and tocotrienols: physiological significance and prospects as antioxidants J Biosci Bioeng 104 439 445 18215628 10.1263/jbb.104.439 1:CAS:528:DC%2BD1cXisVejtL0%3D
138. AK Mukherjee SK Ghosal CR Maity 1997 Lysosomal membrane stabilization by alpha-tocopherol against the damaging action of Vipera russelli venom phospholipase A2 Cell Mol Life Sci 53 152 155 9118003 10.1007/PL00000586 1:CAS:528:DyaK2sXit1Kit78%3D (Pubitemid 27365886)
139. SK Baird T Kurz UT Brunk 2006 Metallothionein protects against oxidative stress-induced lysosomal destabilization Biochem J 394 275 283 16236025 10.1042/BJ20051143 1:CAS:528:DC%2BD28XpsValsA%3D%3D (Pubitemid 43259678)
140. F Fouchier JL Mego J Dang C Simon 1983 Thyroid lysosomes: the stability of the lysosomal membrane Eur J Cell Biol 30 272 278 11596502 1:CAS:528:DyaL3sXktlCrsL8%3D
141. D Deng N Jiang SJ Hao H Sun GJ Zhang 2009 Loss of membrane cholesterol influences lysosomal permeability to potassium ions and protons Biochim Biophys Acta 1788 470 476 19109925 10.1016/j.bbamem.2008.11.018 1:CAS:528: DC%2BD1MXhsFKls7k%3D
142. M Jadot F Andrianaivo F Dubois R Wattiaux 2001 Effects of methylcyclodextrin on lysosomes Eur J Biochem 268 1392 1399 11231291 10.1046/j.1432-1327.2001.02006.x 1:CAS:528:DC%2BD3MXhvFSktr4%3D (Pubitemid 32231892)
143. SJ Hao JF Hou N Jiang GJ Zhang 2008 Loss of membrane cholesterol affects lysosomal osmotic stability Gen Physiol Biophys 27 278 283 19202201 1:CAS:528:DC%2BD1MXjsVCitr0%3D
144. ND Ridgway 2000 Interactions between metabolism and intracellular distribution of cholesterol and sphingomyelin Biochim Biophys Acta 1484 129 141 10760463 1:CAS:528:DC%2BD3cXisVKgtLY%3D
145. K Simons E Ikonen 2000 How cells handle cholesterol Science 290 1721 1726 11099405 10.1126/science.290.5497.1721 1:CAS:528:DC%2BD3cXovVOitbc%3D (Pubitemid 32004797)
146. EL Eskelinen 2006 Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy Mol Aspects Med 27 495 502 16973206 10.1016/j.mam.2006.08.005 1:CAS:528:DC%2BD28XhtVagtbvE (Pubitemid 44466656)
147. M Fukuda 1991 Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking J Biol Chem 266 21327 21330 1939168 1:CAS:528:DyaK3MXmt1KhsLo%3D
148. K Furuta M Ikeda Y Nakayama, et al. 2001 Expression of lysosome-associated membrane proteins in human colorectal neoplasms and inflammatory diseases Am J Pathol 159 449 455 11485903 1:CAS:528: DC%2BD3MXms1Wisb0%3D
149. K Ozaki M Nagata M Suzuki, et al. 1998 Isolation and characterization of a novel human lung-specific gene homologous to lysosomal membrane glycoproteins 1 and 2: significantly increased expression in cancers of various tissues Cancer Res 58 3499 3503 9721848 1:CAS:528:DyaK1cXlsFajsbw%3D