Distinct cathepsins control necrotic cell death mediated by pyroptosis inducers and lysosome-destabilizing agents

Cell Cycle

Volumn 14, Issue 7, 2015, Pages 964-972

  Brojatsch, Jürgen ^a   Lima, Heriberto ^a   Palliser, Deborah ^a   Jacobson, Lee S ^a   Muehlbauer, Stefan M ^b   Furtado, Raquel ^a   Goldman, David L ^a   Lisanti, Michael P ^c   Chandran, Kartik ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Caspase 1; IL; Inflammasome; Interleukin; L leucyl L leucine methyl ester; Lipopolysaccharide; LMN; LPS; Lysosome rupture; Lysosome mediated necrosis; Necrosis; NLR; Nucleotidebinding domain and leucine rich repeat; Pyroptosis abbreviations: LLOMe

Indexed keywords

CATHEPSIN; CATHEPSIN B; CATHEPSIN B INHIBITOR; CATHEPSIN D; DIPEPTIDYL PEPTIDASE I; LEUCYLLEUCINE METHYL ESTER; PROTEINASE; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; CA 074 METHYL ESTER; DIPEPTIDE; LEUCYL-LEUCINE-METHYL ESTER;

ADAPTIVE IMMUNITY; ANIMAL CELL; APOPTOSIS; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DOWN REGULATION; LYSOSOME; MOUSE; NEUTROPHIL; NONHUMAN; PROTEIN DEGRADATION; PYROPTOSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; C57BL MOUSE; DRUG EFFECTS; ENZYMOLOGY; NECROSIS; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CATHEPSIN B; CATHEPSIN C; CATHEPSIN D; DIPEPTIDES; LYSOSOMES; MICE, INBRED BALB C; MICE, INBRED C57BL; NECROSIS;

EID: 84928162724     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/15384101.2014.991194     Document Type: Article

References (55)

1. Averette KM, Pratt MR, Yang Y, Bassilian S, Whitelegge JP, Loo JA, Muir TW, Bradley KA. 2009. Anthrax lethal toxin induced lysosomal membrane permeabilization and cytosolic cathepsin release is Nlrp1b/Nalp1b-dependent. Plos One 4:e7913; PMID:19924255; http://dx.doi.org/10.1371/journal.pone.0007913
2. Aymeric L, Apetoh L, Ghiringhelli F, Tesniere A, Martins I, Kroemer G, Smyth MJ, Zitvogel L. 2010. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res 70:855-8; PMID:20086177; http://dx.doi.org/10.1158/0008-5472.CAN-09-3566
3. Basu S, Binder RJ, Suto R, Anderson K, Srivastava PK. 2000. Necrotic but not apoptiotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF kappa B pathway. Cell Stress Chaperon 5:373-373; PMID:11058573
4. Berghe TV, Vanlangenakker N, Parthoens E, Deckers W, Devos M, Festjens N, Guerin CJ, Brunk UT, Declercq W, Vandenabeele P. 2010. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ 17:922-30; PMID:20010783; http://dx.doi.org/10.1038/cdd.2009.184
5. Bergsbaken T, Fink SL, Cookson BT. 2009. Pyroptosis: host cell death and inflammation. Nat RevMicrobiol 7:99-109; PMID:19148178; http://dx.doi.org/10.1038/nrmicro2070
6. Bidere N, Lorenzo HK, Carmona S, Laforge M, Harper F, Dumont C, Senik A. 2003. Cathepsin D triggers bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. The Journal of biological chemistry 278:31401-11; PMID:12782632; http://dx.doi.org/10.1074/jbc.M301911200
7. Borner C, Monney L. 1999. Apoptosis without caspases: an inefficient molecular guillotine? Cell Death Differ 6:497-507; PMID:10381652; http://dx.doi.org/10.1038/sj.cdd.4400525
8. Brennan MA, Cookson BT. 2000. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38:31-40; PMID:11029688; http://dx.doi.org/10.1046/j.1365-2958.2000.02103.x
9. Brojatsch J, Casadevall A, Goldman DL. 2014. Molecular determinants for a cardiovascular collapse in anthrax. Front Biosci (Elite Ed) 6:139-47; PMID:24389148; http://dx.doi.org/10.2741/E697
10. Buttle DJ, Murata M, Knight CG, Barrett AJ. 1992. CA074 methyl ester: a proinhibitor for intracellular cathepsin B. Arch Biochem Biophys 299:377-80; PMID:1444478; http://dx.doi.org/10.1016/0003-9861(92)90290-D
11. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas Stubbs S, Obeid M, et al. 2005. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 202:1691-701; PMID:16365148; http://dx.doi.org/10.1084/jem.20050915
12. Christofferson DE, Yuan JY. 2010. Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol 22:263-8; PMID:20045303; http://dx.doi.org/10.1016/j.ceb.2009.12.003
13. Creagh EM, O’Neill LA. 2006. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol 27:352-7; PMID:16807108; http://dx.doi.org/10.1016/j.it.2006.06.003
14. Dahl SW, Halkier T, Lauritzen C, Dolenc I, Pedersen J, Turk V, Turk B. 2001. Human recombinant prodipeptidyl peptidase I (cathepsin C) can be activated by cathepsins L and S but not by autocatalytic processing. Biochemistry-Us 40:1671-8; PMID:11327826; http://dx.doi.org/10.1021/bi001693z
15. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. 2005. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury (1, 112, 2005).Nat ChemBiol; PMID:16408008
16. Diment S, Leech MS, Stahl PD. 1988. Cathepsin-D is membrane-associated in macrophage endosomes. J Biol Chem 263:6901-7; PMID:3360812
17. Edinger AL, Thompson CB. 2004. Death by design: apoptosis, necrosis and autophagy. Curr Opin Biol 16:663-9; PMID:15530778; http://dx.doi.org/10.1016/j.ceb.2004.09.011
18. Festjens N, Vanden Berghe T, Vandenabeele P. 2006. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Bio Biophysica Acta 1757:1371-87; PMID:16950166; http://dx.doi.org/10.1016/j.bbabio.2006.06.014
19. Fink SL, Cookson BT. 2006. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8:1812-25; PMID:16824040; http://dx.doi.org/10.1111/j.1462-5822.2006.00751.x
20. Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G. 2009. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 10:241-7; PMID:19221555; http://dx.doi.org/10.1038/ni.1703
21. Fujisawa A, Kambe N, Saito M, Nishikomori R, Tanizaki H, Kanazawa N, Adachi S, Heike T, Sagara J, Suda T. 2007. Disease-associated mutations in CIAS1 induce cathepsin B-dependent rapid cell death of human THP-1 monocytic cells. Blood 109:2903-11; PMID:17164343
22. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, Bazan NG, Blagosklonny MV, Blomgren K, Borner C, et al. 2009. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 16:1093-107; PMID:19373242; http://dx.doi.org/10.1038/cdd.2009.44
23. Guicciardi ME, Gores GJ. 2013. Complete lysosomal disruption: a route to necrosis, not to the inflammasome. Cell Cycle 12:1995; PMID:23759574; http://dx.doi.org/10.4161/cc.25317
24. Guicciardi ME, Miyoshi H, Bronk SF, Gores GJ. 2001. Cathepsin B knockout mice are resistant to tumor necrosis factor-alpha-mediated hepatocyte apoptosis and liver injury: implications for therapeutic applications. Am J Pathol 159:2045-54; PMID:11733355; http://dx.doi.org/10.1016/S0002-9440(10)63056-8
25. Hentze H, Lin XY, Choi MS, Porter AG. 2003. Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1-independent necrosis triggered by the microbial toxin nigericin. Cell Death Differ 10:956-68; PMID:12934070; http://dx.doi.org/10.1038/sj.cdd.4401264
26. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA, Latz E. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9:847-56; PMID:18604214; http://dx.doi.org/10.1038/ni.1631
27. Iyer SS, Pulskens WP, Sadler JJ, Butter LM, Teske GJ, Ulland TK, Eisenbarth SC, Florquin S, Flavell RA, Leemans JC, et al. 2009.Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA 106:20388-93; PMID:19918053; http://dx.doi.org/10.1073/pnas.0908698106
28. Jacobson LS, Lima H Jr, Goldberg MF, Gocheva V, Tsiperson V, Sutterwala FS, Joyce JA, Gapp BV, Blomen VA, Chandran K, et al. 2013. Cathepsin-mediated necrosis controls the adaptive immune response by Th2 (T helper type 2)-associated adjuvants. J Biol Chem 288:7481-91; PMID:23297415; http://dx.doi.org/10.1074/jbc.M112.400655
29. Keller M, Ruegg A, Werner S, Beer HD. 2008. Active caspase-1 is a regulator of unconventional protein secretion. Cell 132:818-31; PMID:18329368; http://dx.doi.org/10.1016/j.cell.2007.12.040
30. Kono H, Rock KL. 2008. How dying cells alert the immune system to danger. Nature reviews. Immunology 8:279-89; PMID:18340345; http://dx.doi.org/10.1038/nri2215
31. Kool M, Soullié T, van Nimwegen M, Willart MA, Muskens F, Jung S, Hoogsteden HC, Hammad H, Lambrecht BN. 2008. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 205:869-82; PMID:18362170; http://dx.doi.org/10.1084/jem.20071087
32. Kroemer G, et al. 2005. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 12:1463-7; PMID:16247491; http://dx.doi.org/10.1038/sj.cdd.4401724
33. Li HF, Ambade A, Re F. 2009. Cutting Edge: Necrosis Activates the NLRP3 Inflammasome. J Immunol 183:1528-32; PMID:19596994; http://dx.doi.org/10.4049/jimmunol.0901080
34. Liew FY, Xu D, Brint EK, O’Neill LA. 2005. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 5:446-58; PMID:15928677; http://dx.doi.org/10.1038/nri1630
35. Lima H, Jr., Jacobson LS, Goldberg MF, Chandran K, Diaz-Griffero F, Lisanti MP, Brojatsch J. 2013. Role of lysosome rupture in controlling nlrp3 signaling and necrotic cell death. Cell Cycle 12:1868-78; PMID:23708522; http://dx.doi.org/10.4161/cc.24903
36. Mariathasan S, Weiss DS, Newton K, McBride J, O’Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440:228-32; PMID:16407890; http://dx.doi.org/10.1038/nature04515
37. Marichal T, Ohata K, Bedoret D, Mesnil C, Sabatel C, Kobiyama K, Lekeux P, Coban C, Akira S, Ishii KJ, et al. 2011. DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med 17:996-1002; PMID:21765404; http://dx.doi.org/10.1038/nm.2403
38. Martinon F, Burns K, Tschopp J. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10:417-26; PMID:12191486; http://dx.doi.org/10.1016/S1097-2765(02)00599-3
39. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. 2006. Gout-associated uric acid crystals activate theNALP3 inflammasome. Nature 440:237-41; PMID:16407889; http://dx.doi.org/10.1038/nature04516
40. Muehlbauer SM, Evering TH, Bonuccelli G, Squires RC, Ashton AW, Porcelli SA, Lisanti MP, Brojatsch J. 2007. Anthrax lethal toxin kills macrophages in a strain-specific manner by apoptosis or caspase-1-mediated necrosis. Cell Cycle 6:758-66; PMID:17374996; http://dx.doi.org/10.4161/cc.6.6.3991
41. Muehlbauer SM, Lima H Jr, Goldman DL, Jacobson LS, Rivera J, Goldberg MF, Palladino MA, Casadevall A, Brojatsch J. 2010. Proteasome inhibitors prevent caspase-1-mediated disease in rodents challenged with anthrax lethal toxin.Am J Pathol 177:735-43; PMID:20595632; http://dx.doi.org/10.2353/ajpath.2010.090828
42. Newman ZL, Leppla SH, Moayeri M. 2009. CA-074Me protection against anthrax lethal toxin. Infect Immun 77:4327-36; PMID:19635822; http://dx.doi.org/10.1128/IAI.00730-09
43. Oberle C, Huai J, Reinheckel T, Tacke M, Rassner M, Ekert PG, Buellesbach J, Borner C. 2010. Lysosomal membrane permeabilization and cathepsin release is a Bax/Bak-dependent, amplifying event of apoptosis in fibroblasts and monocytes. Cell Death Differ 17:1167-78; PMID:20094062; http://dx.doi.org/10.1038/cdd.2009.214
44. Petrilli V, Dostert C, Muruve DA, Tschopp J. 2007. The inflammasome: a danger sensing complex triggering innate immunity. Curr Opin Immunol 19:615-22; PMID:17977705; http://dx.doi.org/10.1016/j.coi.2007.09.002
45. Reinheckel T. 2013. On the road to inflammation: linking lysosome disruption, lysosomal protease release and necrotic death of immune cells. Cell Cycle 12:1994; PMID:23759575; http://dx.doi.org/10.4161/cc.25316
46. Rovere-Querini P, Capobianco A, Scaffidi P, Valentinis B, Catalanotti F, Giazzon M, Dumitriu IE, Müller S, Iannacone M, Traversari C, et al. 2004. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 5:825-30; PMID:15272298; http://dx.doi.org/10.1038/sj.embor.7400205
47. Samarel AM, Ferguson AG, Decker RS, Lesch M. 1989. Effects of cysteine protease inhibitors on rabbit cathepsin-D maturation. Am J Physiol 257:C1069-79; PMID:2610247
48. Scaffidi P, Misteli T, Bianchi ME. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191-5; PMID:12110890; http://dx.doi.org/10.1038/nature00858
49. Squires RC, Muehlbauer SM, Brojatsch J. 2007. Proteasomes control caspase-1 activation in anthrax lethal toxin-mediated cell killing. J Biol Chem 282:34260-7; PMID:17878154; http://dx.doi.org/10.1074/jbc.M705687200
50. Thiele DL, Lipsky PE. 1990. The action of leucyl-leucine methyl ester on cytotoxic lymphocytes requires uptake by a novel dipeptide-specific facilitated transport system and dipeptidyl peptidase I-mediated conversion to membranolytic products. J Exp Med 172:183-94; PMID:1972727; http://dx.doi.org/10.1084/jem.172.1.183
51. Thiele DL, Lipsky PE. 1990. Mechanism of L-leucyl-Lleucine methyl ester-mediated killing of cytotoxic lymphocytes: dependence on a lysosomal thiol protease, dipeptidyl peptidase I, that is enriched in these cells. Proc Natl Acad Sci U S A 87:83-7; PMID:2296607; http://dx.doi.org/10.1073/pnas.87.1.83
52. Ting JPY, Willingham SB, Bergstralh DT. 2008. NLRs at the intersection of cell death and immunity. Nature Reviews Immunology 8:372-9; PMID:18362948; http://dx.doi.org/10.1038/nri2296
53. Turk B, Stoka V, Rozman-Pungercar J, Cirman T, Droga-Mazovec G, Oresi_c K, Turk V. 2002. Apoptotic pathways: involvement of lysosomal proteases. Biol Chem 383:1035-44; PMID:12437086; http://dx.doi.org/10.1515/BC.2002.112
54. Turk V, Turk B, Turk D. 2001. Lysosomal cysteine proteases: facts and opportunities. The EMBO journal 20:4629-33; PMID:11532926; http://dx.doi.org/10.1093/emboj/20.17.4629
55. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. 2010. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 11:700-14; PMID:20823910; http://dx.doi.org/10.1038/nrm2970