A proteolytic cascade controls lysosome rupture and necrotic cell death mediated by lysosome-destabilizing adjuvants

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Brojatsch, Jürgen ^a   Lima Jr , Heriberto ^a   Kar, Alak K ^a   Jacobson, Lee S ^a,b   Muehlbauer, Stefan M ^a,b   Chandran, Kartik ^a   Diaz Griffero, Felipe ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM POTASSIUM SULFATE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CATHEPSIN B; CATHEPSIN B INHIBITOR; DIPEPTIDYL PEPTIDASE I; LEUCYLLEUCINE METHYL ESTER; MG 115; PROTEASOME; PROTEASOME INHIBITOR; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; ALDEHYDE; ANTHRAX TOXIN; BACTERIAL ANTIGEN; BACTERIAL TOXIN; CARBOBENZOXY-LEUCYL-LEUCYL-NORVALINAL; DIPEPTIDE; LEUCYL-LEUCINE-METHYL ESTER; LEUPEPTIN; N-(3-PROPYLCARBAMOYLOXIRANE-2-CARBONYL)-ISOLEUCYL-PROLINE; PEPTIDE; PHARMACEUTICAL VEHICLES AND ADDITIVES;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; IMMUNOREGULATION; LYSOSOME; MOUSE; NECROSIS; NONHUMAN; PROTEIN DEGRADATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; C57BL MOUSE; DRUG EFFECTS; INFLAMMATION; METABOLISM; PATHOLOGY; ULTRASTRUCTURE;

ADJUVANTS, PHARMACEUTIC; ALDEHYDES; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CATHEPSIN B; CATHEPSIN C; DIPEPTIDES; INFLAMMATION; LEUPEPTINS; LYSOSOMES; MICE, INBRED BALB C; MICE, INBRED C57BL; NECROSIS; PEPTIDES; PROTEASOME INHIBITORS; PROTEOLYSIS;

EID: 84902477963     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095032     Document Type: Article

References (44)

1. 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: 241-247.
2. Ting JPY, Willingham SB, Bergstralh DT (2008) NLRs at the intersection of cell death and immunity. Nat Rev Immunol 8: 372-379. (Pubitemid 351596409)
3. Li HF, Ambade A, Re F (2009) Cutting Edge: Necrosis Activates the NLRP3 Inflammasome. J Imm 183: 1528-1532.
4. Iyer SS, Pulskens WP, Sadler JJ, Butter LM, Teske GJ, et al. (2009) Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci U S A 106: 20388-20393.
5. Rovere-Querini P, Capobianco A, Scaffidi P, Valentinis B, Catalanotti F, et al. (2004) HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 5: 825-830. (Pubitemid 39199174)
6. Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8: 279-289. (Pubitemid 351432799)
7. Festjens N, Vanden Berghe T, Vandenabeele P (2006) Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757: 1371-1387. (Pubitemid 44472550)
8. 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 & Chaperones 5: 373-373.
9. Jacobson LS, Lima H Jr, Goldberg MF, Gocheva V, Tsiperson V, et al. (2013) Cathepsin-mediated necrosis controls the adaptive immune response by Th2 (T helper type 2)-associated adjuvants. J Biol Chem 288: 7481-7491.
10. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241. (Pubitemid 43372104)
11. Kool M, Soullie T, van Nimwegen M, Willart MA, Muskens F, et al. (2008) Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. Journal of Experimental Medicine 205: 869-882. (Pubitemid 351549884)
12. Marichal T, Ohata K, Bedoret D, Mesnil C, Sabatel C, et al. (2011) DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med 17: 996-1002.
13. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232. (Pubitemid 43372102)
14. Kroemer G, El-Deiry W, Golstein P, Peter ME, Vaux D, et al. (2005) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 12: 1463-1467. (Pubitemid 41553979)
15. Edinger AL, Thompson CB (2004) Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16: 663-669. (Pubitemid 39463117)
16. Fink SL, Cookson BT (2006) Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Micro 8: 1812-1825. (Pubitemid 44530672)
17. Brennan MA, Cookson BT (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Micro 38: 31-40.
18. Muehlbauer SM, Evering TH, Bonuccelli G, Squires RC, Ashton AW, et al. (2007) Anthrax lethal toxin kills macrophages in a strain-specific manner by apoptosis or caspase-1-mediated necrosis. Cell Cycle 6: 758-766. (Pubitemid 46535689)
19. Petrilli V, Dostert C, Muruve DA, Tschopp J (2007) The inflammasome: a danger sensing complex triggering innate immunity. Curr Opin Immunol 19: 615-622. (Pubitemid 350236810)
20. Nour AM, Yeung YG, Santambrogio L, Boyden ED, Stanley ER, et al. (2009) Anthrax lethal toxin triggers the formation of a membrane-associated inflammasome complex in murine macrophages. Infect Immun 77: 1262-1271.
21. Keller M, Ruegg A, Werner S, Beer HD (2008) Active caspase-1 is a regulator of unconventional protein secretion. Cell 132: 818-831. (Pubitemid 351312798)
22. Berghe TV, Vanlangenakker N, Parthoens E, Deckers W, Devos M, et al. (2010) Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ 17: 922-930.
23. Christofferson DE, Yuan JY (2010) Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol 22: 263-268.
24. Lima H Jr, Jacobson LS, Goldberg MF, Chandran K, Diaz-Griffero F, et al. (2013) Role of lysosome rupture in controlling Nlrp3 signaling and necrotic cell death. Cell Cycle 12: 1868-1878.
25. Guicciardi ME, Gores GJ (2013) Complete lysosomal disruption: a route to necrosis, not to the inflammasome. Cell Cycle 12: 1995.
26. Reinheckel T (2013) On the road to inflammation: linking lysosome disruption, lysosomal protease release and necrotic death of immune cells. Cell Cycle 12: 1994.
27. Guicciardi ME, Leist M, Gores GJ (2004) Lysosomes in cell death. Oncogene 23: 2881-2890. (Pubitemid 38638850)
28. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, et al. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9: 847-856.
29. Newman ZL, Leppla SH, Moayeri M (2009) CA-074Me protection against anthrax lethal toxin. Infect Immun 77: 4327-4336.
30. Orlowski RZ (1999) The role of the ubiquitin-proteasome pathway in apoptosis. Cell Death Differ 6: 303-313.
31. Squires RC, Muehlbauer SM, Brojatsch J (2007) Proteasomes control caspase-1 activation in anthrax lethal toxin-mediated cell killing. J Biol Chem 282: 34260-34267. (Pubitemid 350159474)
32. Muehlbauer SM, Lima H Jr, Goldman DL, Jacobson LS, Rivera J, et al. (2010) Proteasome inhibitors prevent caspase-1-mediated disease in rodents challenged with anthrax lethal toxin. Am J Path 177: 735-743.
33. Kisselev AF, Goldberg AL (2001) Proteasome inhibitors: from research tools to drug candidates. Chem & Biol 8: 739-758. (Pubitemid 32752454)
34. Turk BE (2007) Manipulation of host signalling pathways by anthrax toxins. The Biochem J 402: 405-417.
35. Brojatsch J, Casadevall A, Goldman DL (2014) Molecular determinants for a cardiovascular collapse in anthrax. Front Biosc 6: 139-147.
36. 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: 956-968. (Pubitemid 37069473)
37. Wang F, Krai P, Deu E, Bibb B, Lauritzen C, et al. (2011) Biochemical characterization of Plasmodium falciparum dipeptidyl aminopeptidase 1. Mol Bioch Parasitology 175: 10-20.
38. 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: 183-194.
39. Thiele DL, Lipsky PE (1990) Mechanism of L-leucyl-L-leucine 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: 83-87.
40. Alileche A, Squires RC, Muehlbauer SM, Lisanti MP, Brojatsch J (2006) Mitochondrial impairment is a critical event in anthrax lethal toxin-induced cytolysis of murine macrophages. Cell Cycle 5: 100-106.
41. Newman Z, Leppla S, Moayeri M (2009) CA-074Me protection against anthrax lethal toxin. Infect Immun: 1-43.
42. Halangk W, Lerch MM, Brandt-Nedelev B, Roth W, Ruthenbuerger M, et al. (2000) Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. The Journal of clinical investigation 106: 773-781.
43. Roth W, Deussing J, Botchkarev VA, Pauly-Evers M, Saftig P, et al. (2000) Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling. FASEB Journal 14: 2075-2086.
44. Diaz-Griffero F, Hoschander SA, Brojatsch J (2002) Endocytosis is a critical step in entry of subgroup B avian leukosis viruses. J Virol 76: 12866-12876. (Pubitemid 35386970)