The proteases HtrA2/Omi and UCH-L1 regulate TNF-induced necroptosis

Cell Communication and Signaling

Volumn 11, Issue 1, 2013, Pages

  Sosna, Justyna ^a   Voigt, Susann ^a   Mathieu, Sabine ^a   Kabelitz, Dieter ^a   Trad, Ahmad ^a   Janssen, Ottmar ^a   Meyer Schwesinger, Catherine ^b   Schütze, Stefan ^a   Adam, Dieter ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Apoptosis; HtrA2 Omi; Kidney failure; Necroptosis; Programmed necrosis; Proteases; Tumor necrosis factor; UCH L1

Indexed keywords

CALPAIN; CASPASE; CATHEPSIN; CYSTEINE PROTEINASE; METALLOPROTEINASE; METALLOPROTEINASE INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SERINE PROTEINASE INHIBITOR; SERINE PROTEINASE OMI; TUMOR NECROSIS FACTOR; UBIQUITIN THIOLESTERASE; UCH L1 PROTEIN; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN; SERINE PROTEINASE; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN CARBOXYL TERMINAL HYDROLASE L 1, MOUSE; UBIQUITIN CARBOXYL-TERMINAL HYDROLASE L-1, MOUSE; UCH L1 PROTEIN, RAT; UCH-L1 PROTEIN, RAT; UCHL1 PROTEIN, HUMAN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROTECTION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DELETION; HUMAN; HUMAN CELL; MOUSE; NECROPTOSIS; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; RNA INTERFERENCE; UBIQUITINATION; VALIDATION STUDY; ANIMAL; CELL CULTURE; CELL STRAIN 3T3; CELL STRAIN HT29; LEUKEMIA CELL LINE; METABOLISM; PHYSIOLOGY; WISTAR RAT; 3T3 CELL LINE; HT 29 CELL LINE; JURKAT CELL LINE;

MURINAE;

ANIMALS; APOPTOSIS; CELLS, CULTURED; HT29 CELLS; HUMANS; JURKAT CELLS; MICE; MITOCHONDRIAL PROTEINS; NIH 3T3 CELLS; PODOCYTES; RATS; RATS, WISTAR; SERINE ENDOPEPTIDASES; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN THIOLESTERASE;

EID: 84884824441     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-11-76     Document Type: Article

References (53)

1. Expansion and evolution of cell death programmes. Degterev A, Yuan J, Nat Rev Mol Cell Biol 2008 9 378 390 10.1038/nrm2393 18414491 (Pubitemid 351574200)
2. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Festjens N, Vanden Berghe T, Vandenabeele P, Biochim Biophys Acta 2006 1757 1371 1387 10.1016/j.bbabio. 2006.06.014 16950166 (Pubitemid 44472550)
3. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Mocarski ES, Upton JW, Kaiser WJ, Nat Rev Immunol 2012 12 79 88
4. Programmed necrosis: backup to and competitor with apoptosis in the immune system. Han J, Zhong CQ, Zhang DW, Nat Immunol 2011 12 1143 1149 10.1038/ni.2159 22089220
5. Mechanisms of necroptosis in T cells. Ch'en IL, Tsau JS, Molkentin JD, Komatsu M, Hedrick SM, J Exp Med 2011 208 633 641 10.1084/jem.20110251 21402742
6. Programmed necrosis: a prominent mechanism of cell death following neonatal brain injury. Chavez-Valdez R, Martin LJ, Northington FJ, Neurol Res Int 2012 2012 257563 22666585
7. Molecular mechanisms that differentiate apoptosis from programmed necrosis. Dorn GW 2nd, Toxicol Pathol 2013 41 227 234 10.1177/0192623312466961 23222994
8. Dual face apoptotic machinery: from initiator of apoptosis to guardian of necroptosis. Declercq W, Takahashi N, Vandenabeele P, Immunity 2011 35 493 495 10.1016/j.immuni.2011.10.007 22035842
9. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Kaczmarek A, Vandenabeele P, Krysko DV, Immunity 2013 38 209 223 10.1016/j.immuni.2013.02.003 23438821
10. Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Kang TB, Yang SH, Toth B, Kovalenko A, Wallach D, Immunity 2013 38 27 40 10.1016/j.immuni.2012.09.015 23260196
11. RIP3 finds partners in crime. Chan FK, Baehrecke EH, Cell 2012 148 17 18 10.1016/j.cell.2011.12.020 22265396
12. Molecular mechanisms of necroptosis: an ordered cellular explosion. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G, Nat Rev Mol Cell Biol 2010 11 700 714 10.1038/nrm2970 20823910
13. Overexpression of acid ceramidase protects from tumor necrosis factor-induced cell death. Strelow A, Bernardo K, Adam-Klages S, Linke T, Sandhoff K, Krönke M, Adam D, J Exp Med 2000 192 601 611 10.1084/jem.192.5.601 10974027
14. Ceramide mediates caspase-independent programmed cell death. Thon L, Möhlig H, Mathieu S, Lange A, Bulanova E, Winoto-Morbach S, Schütze S, Bulfone-Paus S, Adam D, FASEB J 2005 19 1945 1956 10.1096/fj.05-3726com 16319138 (Pubitemid 41759740)
15. TNF-induced necroptosis and PARP-1-mediated necrosis represent distinct routes to programmed necrotic cell death. Sosna J, Voigt S, Mathieu S, Lange A, Thon L, Davarnia P, Herdegen T, Linkermann A, Rittger A, Chan FK, et al. Cell Mol Life Sci 2013 epub ahead of print, doi: 10.1007/s00018-013-1381-6
16. Four deaths and a funeral: from caspases to alternative mechanisms. Leist M, Jäättelä M, Nat Rev Mol Cell Biol 2001 2 589 598 10.1038/35085008 11483992 (Pubitemid 33674010)
17. Cell death independent of caspases: a review. Bröker LE, Kruyt FA, Giaccone G, Clin Cancer Res 2005 11 3155 3162 10.1158/1078-0432.CCR-04-2223 15867207 (Pubitemid 40627860)
18. Serine protease inhibitors block neutral sphingomyelinase activation, ceramide generation, and apoptosis triggered by daunorubicin. Mansat V, Bettaieb A, Levade T, Laurent G, Jaffrezou JP, FASEB J 1997 11 695 702 9240970 (Pubitemid 27318286)
19. Activation of an alternative death receptor-induced signaling pathway in human hepatocytes under caspase arrest. Dünstl G, Weiland T, Schlaeger C, Nüssler A, Künstle G, Wendel A, Arch Biochem Biophys 2007 462 140 149 10.1016/j.abb.2007.03.030 17466932 (Pubitemid 46856325)
20. Serine proteases mediate apoptosis-like cell death and phagocytosis under caspase-inhibiting conditions. Egger L, Schneider J, Rhême C, Tapernoux M, Häcki J, Borner C, Cell Death Differ 2003 10 1188 1203 10.1038/sj.cdd.4401288 14502242 (Pubitemid 37258584)
21. Tumour necrosis factor-induced necrosis versus anti-Fas-induced apoptosis in L929 cells. Vercammen D, Vandenabeele P, Beyaert R, Declercq W, Fiers W, Cytokine 1997 9 801 808 10.1006/cyto.1997.0252 9367540 (Pubitemid 27494144)
22. New methodology is a key to progress. Robertson JD, Zhivotovsky B, Cell Cycle 2002 1 119 121 12429919
23. The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. van Loo G, van Gurp M, Depuydt B, Srinivasula SM, Rodriguez I, Alnemri ES, Gevaert K, Vandekerckhove J, Declercq W, Vandenabeele P, Cell Death Differ 2002 9 20 26 10.1038/sj.cdd.4400970 11803371 (Pubitemid 34071990)
24. Neuroprotective role of the Reaper-related serine protease HtrA2/Omi revealed by targeted deletion in mice. Martins LM, Morrison A, Klupsch K, Fedele V, Moisoi N, Teismann P, Abuin A, Grau E, Geppert M, Livi GP, et al. Mol Cell Biol 2004 24 9848 9862 10.1128/MCB.24.22.9848-9862.2004 15509788 (Pubitemid 39458812)
25. The mitochondrial serine protease HtrA2/Omi cleaves RIP1 during apoptosis of Ba/F3 cells induced by growth factor withdrawal. Vande Walle L, Wirawan E, Lamkanfi M, Festjens N, Verspurten J, Saelens X, Vanden Berghe T, Vandenabeele P, Cell Res 2010 20 421 433 10.1038/cr.2010.18 20125124
26. A novel mechanism for imatinib mesylate-induced cell death of BCR-ABL-positive human leukemic cells: caspase-independent, necrosis-like programmed cell death mediated by serine protease activity. Okada M, Adachi S, Imai T, Watanabe K, Toyokuni SY, Ueno M, Zervos AS, Kroemer G, Nakahata T, Blood 2004 103 2299 2307 10.1182/blood-2003-05-1605 14645012 (Pubitemid 38326250)
27. HtrA2/Omi terminates cytomegalovirus infection and is controlled by the viral mitochondrial inhibitor of apoptosis (vMIA). McCormick AL, Roback L, Mocarski ES, PLoS Pathog 2008 4 1000063 10.1371/journal.ppat.1000063 18769594 (Pubitemid 351811533)
28. A new role for the neuronal ubiquitin C-terminal hydrolase-L1 (UCH-L1) in podocyte process formation and podocyte injury in human glomerulopathies. Meyer-Schwesinger C, Meyer TN, Münster S, Klug P, Saleem M, Helmchen U, Stahl RAK, J Pathol 2009 217 452 464 10.1002/path.2446 18985619
29. Ubiquitin vinyl methyl ester binding orients the misaligned active site of the ubiquitin hydrolase UCHL1 into productive conformation. Boudreaux DA, Maiti TK, Davies CW, Das C, Proc Natl Acad Sci USA 2010 107 9117 9122 10.1073/pnas.0910870107 20439756
30. Ubiquitin C-terminal hydrolase-l1 activity induces polyubiquitin accumulation in podocytes and increases proteinuria in rat membranous nephropathy. Meyer-Schwesinger C, Meyer TN, Sievert H, Hoxha E, Sachs M, Klupp EM, Münster S, Balabanov S, Carrier L, Helmchen U, et al. Am J Pathol 2011 178 2044 2057 10.1016/j.ajpath.2011.01.017 21514420
31. The regulation of the UCH-L1 gene by transcription factor NF-kappaB in podocytes. Zhang H, Sun Y, Hu R, Luo W, Mao X, Zhao Z, Chen Q, Zhang Z, Cell Signal 2013 25 1574 1585 10.1016/j.cellsig.2013.03.018 23567262
32. Regulation of synaptic structure by ubiquitin C-terminal hydrolase L1. Cartier AE, Djakovic SN, Salehi A, Wilson SM, Masliah E, Patrick GN, J Neurosci 2009 29 7857 7868 10.1523/JNEUROSCI.1817-09.2009 19535597
33. The murine TRAIL receptor signals caspase-independent cell death through ceramide. Thon L, Mathieu S, Kabelitz D, Adam D, Exp Cell Res 2006 312 3808 3821 10.1016/j.yexcr.2006.08.017 17026999 (Pubitemid 44633882)
34. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X, Cell 2009 137 1100 1111 10.1016/j.cell.2009.05.021 19524512
35. Endoplasmic reticulum stress-induced cell death mediated by the proteasome. Egger L, Madden DT, Rhême C, Rao RV, Bredesen DE, Cell Death Differ 2007 14 1172 1180 10.1038/sj.cdd.4402125 17396132 (Pubitemid 46785108)
36. Characterization of a novel and specific inhibitor for the pro-apoptotic protease Omi/HtrA2. Cilenti L, Lee Y, Hess S, Srinivasula S, Park KM, Junqueira D, Davis H, Bonventre JV, Alnemri ES, Zervos AS, J Biol Chem 2003 278 11489 11494 10.1074/jbc.M212819200 12529364 (Pubitemid 36792709)
37. A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. Chan FKM, Shisler J, Bixby JG, Felices M, Zheng L, Appel M, Orenstein J, Moss B, Lenardo MJ, J Biol Chem 2003 278 51613 51621 10.1074/jbc.M305633200 14532286 (Pubitemid 38020406)
38. The serine protease HtrA2 cleaves UCH-L1 and inhibits its hydrolase activity: implication in the UCH-L1-mediated cell death. Park DW, Nam MK, Rhim H, Biochem Biophys Res Commun 2011 415 24 29 10.1016/j.bbrc.2011.09.148 22001920
39. Reversible monoubiquitination regulates the Parkinson disease-associated ubiquitin hydrolase UCH-L1. Meray RK, Lansbury PT Jr, J Biol Chem 2007 282 10567 10575 10.1074/jbc.M611153200 17259170 (Pubitemid 47093406)
40. Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. Liu Y, Lashuel HA, Choi S, Xing X, Case A, Ni J, Yeh LA, Cuny GD, Stein RL, Lansbury PT Jr, Chem Biol 2003 10 837 846 10.1016/j.chembiol.2003.08.010 14522054 (Pubitemid 37171901)
41. How many ways can a podocyte die? Tharaux PL, Huber TB, Semin Nephrol 2012 32 394 404 10.1016/j.semnephrol.2012.06.011 22958494
42. Rip1 (receptor-interacting protein kinase 1) mediates necroptosis and contributes to renal ischemia/reperfusion injury. Linkermann A, Bräsen JH, Himmerkus N, Liu S, Huber TB, Kunzendorf U, Krautwald S, Kidney Int 2012 81 751 761 10.1038/ki.2011.450 22237751
43. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. Vercammen D, Beyaert R, Denecker G, Goossens V, van Loo G, Declercq W, Grooten J, Fiers W, Vandenabeele P, J Exp Med 1998 187 1477 1485 10.1084/jem.187.9.1477 9565639 (Pubitemid 28215406)
44. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC, Nature 1994 371 346 347 10.1038/371346a0 8090205 (Pubitemid 24300618)
45. Caspase inhibition causes hyperacute tumor necrosis factor-induced shock via oxidative stress and phospholipase A2. Cauwels A, Janssen B, Waeytens A, Cuvelier C, Brouckaert P, Nat Immunol 2003 4 387 393 10.1038/ni914 12652297 (Pubitemid 36432323)
46. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G, Sweeney HL, Robbins J, Molkentin JD, Nat Med 2008 14 442 447 10.1038/nm1736 18345011 (Pubitemid 351499389)
47. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK, Cell 2009 137 1112 1123 10.1016/j.cell.2009.05.037 19524513
48. Intramitochondrial serine protease activity of Omi/HtrA2 is required for caspase-independent cell death of human neutrophils. Blink E, Maianski NA, Alnemri ES, Zervos AS, Roos D, Kuijpers TW, Cell Death Differ 2004 11 937 939 10.1038/sj.cdd.4401409 15044964 (Pubitemid 39139752)
49. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Linkermann A, Bräsen JH, Darding M, Jin MK, Sanz AB, Heller JO, De Zen F, Weinlich R, Ortiz A, Walczak H, et al. Proc Natl Acad Sci USA 2013 110 12024 12029 10.1073/pnas.1305538110 23818611
50. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J, Science 2009 325 332 336 10.1126/science.1172308 19498109
51. Sensitization to death receptor cytotoxicity by inhibition of Fas-associated death domain protein (FADD)/caspase signaling-Requirement of cell cycle progression. Lüschen S, Ussat S, Scherer G, Kabelitz D, Adam-Klages S, J Biol Chem 2000 275 24670 24678 10.1074/jbc.M003280200 10827087 (Pubitemid 30626567)
52. Stable expression of nephrin and localization to cell-cell contacts in novel murine podocyte cell lines. Schiwek D, Endlich N, Holzman L, Holthöfer H, Kriz W, Endlich K, Kidney Int 2004 66 91 101 10.1111/j.1523-1755.2004.00711.x 15200416 (Pubitemid 38870085)
53. Enrichment and analysis of secretory lysosomes from lymphocyte populations. Schmidt H, Gelhaus C, Lucius R, Nebendahl M, Leippe M, Janssen O, BMC Immunol 2009 10 41 10.1186/1471-2172-10-41 19640298