Serine hydrolase inhibitors block necrotic cell death by preventing calcium overload of the mitochondria and permeability transition pore formation

Journal of Biological Chemistry

Volumn 289, Issue 3, 2014, Pages 1491-1504

  Yun, Bogeon ^a   Lee, Heejung ^a   Ghosh, Moumita ^a   Cravatt, Benjamin F ^b   Hsu, Ku Lung ^b   Bonventre, Joseph V ^c   Ewing, Heather ^d   Gelb, Michael H ^d   Leslie, Christina C ^a,e,f  

^a DEPARTMENT OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF COLORADO   (United States)

^f UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACIDS; CALCIUM SIGNALING; CALCIUM/CALMODULIN-DEPENDENT PROTEIN KINASE II; CYTOSOLIC PHOSPHOLIPASE; LACTATE DEHYDROGENASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NECROTIC CELL DEATHS; PERMEABILITY TRANSITION PORES;

AMINO ACIDS; CALCIUM; CELL CULTURE; CELL DEATH; ENZYMES; FIBROBLASTS; GLYCEROL; UNSATURATED FATTY ACIDS;

MITOCHONDRIA;

ARACHIDONIC ACID; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CYCLOSPORIN A; CYTOSOLIC PHOSPHOLIPASE A2; EGTAZIC ACID; GLYCEROL 2 ACETATE 1 OLEATE; HYDROLASE INHIBITOR; LACTATE DEHYDROGENASE; SERINE HYDROLASE INHIBITOR; THAPSIGARGIN; UNCLASSIFIED DRUG; 1-OLEOYL-2-ACETOYL-SN-GLYCEROL; CALCIUM; CARRIER PROTEIN; CHELATING AGENT; CYCLOSPORIN; DIACYLGLYCEROL; ISOENZYME; LACTATE DEHYDROGENASE 2; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PHOSPHOLIPASE A2 GROUP IV; PHOSPHOLIPASE A2 INHIBITOR; PYRROLIDINE DERIVATIVE; PYRROPHENONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM OVERLOAD; CALCIUM TRANSPORT; CELL DEATH; CHANNEL GATING; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME RELEASE; LUNG FIBROBLAST; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; FIBROBLAST; GENETICS; KNOCKOUT MOUSE; METABOLISM; NECROSIS; PATHOLOGY; TRANSFORMED CELL LINE;

ANIMALS; ARACHIDONIC ACID; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL LINE, TRANSFORMED; CHELATING AGENTS; CYCLOSPORINE; DIGLYCERIDES; EGTAZIC ACID; FIBROBLASTS; GROUP IV PHOSPHOLIPASES A2; ISOENZYMES; L-LACTATE DEHYDROGENASE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NECROSIS; PHOSPHOLIPASE A2 INHIBITORS; PYRROLIDINES; THAPSIGARGIN;

EID: 84892654514     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.497651     Document Type: Article

References (68)

1. Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., Gottlieb, E., Green, D. R., Hengartner, M. O., Kepp, O., Knight, R. A., Kumar, S., Lipton, S. A., Lu, X., Madeo, F., Malorni, W., Mehlen, P., Nuñez, G., Peter, M. E., Piacentini, M., Rubinsztein, D. C., Shi, Y., Simon, H. U., Vandenabeele, P., White, E., Yuan, J., Zhivotovsky, B., Melino, G., and Kroemer, G. (2012) Molecular definitions of cell death subroutines. Recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 19, 107-120
2. Yuan, J., and Kroemer, G. (2010) Alternative cell death mechanisms in development and beyond. Genes Dev. 24, 2592-2602
3. Baines, C. P. (2010) The cardiac mitochondrion. Nexus of stress. Annu. Rev. Physiol. 72, 61-80
4. Surmeier, D. J., Guzman, J. N., and Sanchez-Padilla, J. (2010) Calcium, cellular aging, and selective neuronal vulnerability in Parkinson's disease. Cell Calcium 47, 175-182
5. Noch, E., and Khalili, K. (2009) Molecular mechanisms of necrosis in glioblastoma. The role of glutamate excitotoxicity. Cancer Biol. Ther. 8, 1791-1797
6. Dong, Z., Saikumar, P., Weinberg, J. M., and Venkatachalam, M. A. (2006) Calcium in cell injury and death. Annu. Rev. Pathol. 1, 405-434
7. Zhivotovsky, B., and Orrenius, S. (2011) Calcium and cell death mechanisms. A perspective from the cell death community. Cell Calcium 50, 211-221
8. Lemasters, J. J., Theruvath, T. P., Zhong, Z., and Nieminen, A. L. (2009) Mitochondrial calcium and the permeability transition in cell death. Biochim. Biophys. Acta 1787, 1395-1401
9. Baines, C. P. (2011) The mitochondrial permeability transition pore and the cardiac necrotic program. Pediatr. Cardiol. 32, 258-262
10. Halestrap, A. P. (2010) A pore way to die. The role of mitochondria in reperfusion injury and cardioprotection. Biochem. Soc. Trans. 38, 841-860
11. Crompton, M., Ellinger, H., and Costi, A. (1988) Inhibition by cyclosporin Aof a Ca2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem. J 255, 357-360
12. Griffiths, E. J., and Halestrap, A. P. (1993) Protection by Cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J. Mol. Cell Cardiol. 25, 1461-1469 (Pubitemid 24049454)
13. Duchen, M. R., McGuinness, O., Brown, L. A., and Crompton, M. (1993) On the involvement of a cyclosporin A sensitive mitochondrial pore in myocardial reperfusion injury. Cardiovasc. Res. 27, 1790-1794 (Pubitemid 23337871)
14. Elrod, J. W., Wong, R., Mishra, S., Vagnozzi, R. J., Sakthievel, B., Goonasekera, S. A., Karch, J., Gabel, S., Farber, J., Force, T., Brown, J. H., Murphy, E., and Molkentin, J. D. (2010) Cyclophilin D controls mitochondrial poredependent Ca2+ exchange, metabolic flexibility, and propensity for heart failure in mice. J. Clin. Invest. 120, 3680-3687
15. Piot, C., Croisille, P., Staat, P., Thibault, H., Rioufol, G., Mewton, N., Elbelghiti, R., Cung, T. T., Bonnefoy, E., Angoulvant, D., Macia, C., Raczka, F., Sportouch, C., Gahide, G., Finet, G., André-Fouët, X., Revel, D., Kirkorian, G., Monassier, J. P., Derumeaux, G., and Ovize, M. (2008) Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N. Engl. J. Med. 359, 473-481
16. Hausenloy, D. J., Duchen, M. R., and Yellon, D. M. (2003) Inhibiting mitochondrial permeability transition pore opening at reperfusion protects against ischaemia-reperfusion injury. Cardiovasc. Res. 60, 617-625 (Pubitemid 37501119)
17. Lemasters, J. J. (1999) The mitochondrial permeability transition and the calcium, oxygen and pH paradoxes. One paradox after another. Cardiovasc. Res. 44, 470-473 (Pubitemid 30012048)
18. Rasola, A., Sciacovelli, M., Pantic, B., and Bernardi, P. (2010) Signal transduction to the permeability transition pore. FEBS Lett. 584, 1989-1996
19. Timmins, J. M., Ozcan, L., Seimon, T. A., Li, G., Malagelada, C., Backs, J., Backs, T., Bassel-Duby, R., Olson, E. N., Anderson, M. E., and Tabas, I. (2009) Calcium/calmodulin-dependent protein kinase II links ER stress with Fas and mitochondrial apoptosis pathways. J. Clin. Invest. 119, 2925-2941
20. Joiner, M. L., Koval, O. M., Li, J., He, B. J., Allamargot, C., Gao, Z., Luczak, E. D., Hall, D. D., Fink, B. D., Chen, B., Yang, J., Moore, S. A., Scholz, T. D., Strack, S., Mohler, P. J., Sivitz, W. I., Song, L. S., and Anderson, M. E. (2012) CaMKII determines mitochondrial stress responses in heart. Nature 491, 269-273
21. De Stefani, D., Raffaello, A., Teardo, E., Szabò, I., and Rizzuto, R. (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340
22. Baughman, J. M., Perocchi, F., Girgis, H. S., Plovanich, M., Belcher-Timme, C. A., Sancak, Y., Bao, X. R., Strittmatter, L., Goldberger, O., Bogorad, R. L., Koteliansky, V., and Mootha, V. K. (2011) Integrative genomics identifiesMCUas an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345
23. Raffaello, A., De Stefani, D., and Rizzuto, R. (2012) The mitochondrial Ca2+ uniporter. Cell Calcium 52, 16-21
24. Gouriou, Y., Demaurex, N., Bijlenga, P., and De Marchi, U. (2011) Mitochondrial calcium handling during ischemia-induced cell death in neurons. Biochimie 93, 2060-2067
25. Pfeiffer, D. R., Schmid, P. C., Beatrice, M. C., and Schmid, H. H. (1979) Intramitochondrial phospholipase activity and the effects of Ca2+ plus N-ethylmaleimide on mitochondrial function. J. Biol. Chem. 254, 11485-11494 (Pubitemid 10136164)
26. Broekemeier, K. M., and Pfeiffer, D. R. (1995) Inhibition of the mitochondrial permeability transition by cyclosporin A during long time frame experiments. Relationship between pore opening and the activity of mitochondrial phospholipases. Biochemistry 34, 16440-16449 (Pubitemid 26006490)
27. Blum, J. L., Kinsey, G. R., Monian, P., Sun, B., Cummings, B. S., McHowat, J., and Schnellmann, R. G. (2011) Profiling of fatty acids released during calcium-induced mitochondrial permeability transition in isolated rabbit kidney cortex mitochondria. Toxicol. in Vitro 25, 1001-1006
28. Kinsey, G. R., McHowat, J., Patrick, K. S., and Schnellmann, R. G. (2007) Role of Ca2+-independent phospholipase A2γ in Ca2+-induced mitochondrial permeability transition. J. Pharmacol. Exp. Ther. 321, 707-715 (Pubitemid 46624527)
29. Broekemeier, K. M., Iben, J. R., LeVan, E. G., Crouser, E. D., and Pfeiffer, D. R. (2002) Pore formation and uncoupling initiate a Ca2+-independent degradation of mitochondrial phospholipids. Biochemistry 41, 7771-7780 (Pubitemid 34627804)
30. Williams, S. D., and Gottlieb, R. A. (2002) Inhibition of mitochondrial calcium-independent phospholipaseA2 (iPLA2) attenuates mitochondrial phospholipid loss and is cardioprotective. Biochem. J. 362, 23-32 (Pubitemid 34174458)
31. Moon, S. H., Jenkins, C. M., Kiebish, M. A., Sims, H. F., Mancuso, D. J., and Gross, R. W. (2012) Genetic ablation of calcium-independent phospholipase A2γ (iPLA2γ) attenuates calcium-induced opening of the mitochondrial permeability transition pore and resultant cytochrome c release. J. Biol. Chem. 287, 29837-29850
32. Scorrano, L., Penzo, D., Petronilli, V., Pagano, F., and Bernardi, P. (2001) Arachidonic acid causes cell death through the mitochondrial permeability transition. Implications for tumor necrosis factor-α aopototic signaling. J. Biol. Chem. 276, 12035-12040
33. Penzo, D., Petronilli, V., Angelin, A., Cusan, C., Colonna, R., Scorrano, L., Pagano, F., Prato, M., Di Lisa, F., and Bernardi, P. (2004) Arachidonic acid released by phospholipase A2 activation triggers Ca2+-dependent apoptosis through the mitochondrial pathway. J. Biol. Chem. 279, 25219-25225 (Pubitemid 38756773)
34. Evans, J. H., Spencer, D. M., Zweifach, A., and Leslie, C. C. (2001) Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes. J. Biol. Chem. 276, 30150-30160
35. Leslie, C. C., Gangelhoff, T. A., and Gelb, M. H. (2010) Localization and function of cytosolic phospholipase A2γ at the Golgi. Biochimie 92, 620-626
36. Ni, Z., Okeley, N. M., Smart, B. P., and Gelb, M. H. (2006) Intracellular action of group IIA secreted phospholipase A2 and group IVA cytosolic phospholipase A2 contribute to arachidonic acid release and prostaglandin production in rat gastric mucosal cells and transfected human embryonic kidney cells. J. Biol. Chem. 281, 16245-16255
37. Hsu, K. L., Tsuboi, K., Adibekian, A., Pugh, H., Masuda, K., and Cravatt, B. F. (2012) DAGLβ inhibition perturbs a lipid network involved in macrophage inflammatory responses. Nat. Chem. Biol. 8, 999-1007
38. Ghosh, M., Stewart, A., Tucker, D. E., Bonventre, J. V., Murphy, R. C., and Leslie, C. C. (2004) Role of cytosolic phospholipase A2 in prostaglandin E2 production by lung fibroblasts. Am. J. Respir. Cell Mol. Biol. 30, 91-100 (Pubitemid 38085263)
39. Stewart, A., Ghosh, M., Spencer, D. M., and Leslie, C. C. (2002) Enzymatic properties of human cytosolic phospholipase A2γ. J. Biol. Chem. 277, 29526-29536 (Pubitemid 41079240)
40. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
41. Ghosh, M., Loper, R., Ghomashchi, F., Tucker, D. E., Bonventre, J. V., Gelb, M. H., and Leslie, C. C. (2007) Function, activity and membrane targeting of cytosolic phospholipase A2γ in mouse lung fibroblasts. J. Biol. Chem. 282, 11676-11686 (Pubitemid 47100705)
42. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408 (Pubitemid 34164012)
43. Mignen, O., Brink, C., Enfissi, A., Nadkarni, A., Shuttleworth, T. J., Giovannucci, D. R., and Capiod, T. (2005) Carboxyamidotriazole-induced inhibition of mitochondrial calcium import blocks capacitative calcium entry and cell proliferation in HEK-293 cells. J. Cell Sci. 118, 5615-5623 (Pubitemid 43079300)
44. Wieckowski, M. R., Giorgi, C., Lebiedzinska, M., Duszynski, J., and Pinton, P. (2009) Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat. Protoc. 4, 1582-1590
45. Wong, R., Steenbergen, C., and Murphy, E. (2012) Mitochondrial permeability transition pore and calcium handling. Methods Mol. Biol. 810, 235-242
46. Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., and Tsujimoto, Y. (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652-658 (Pubitemid 40488558)
47. Petronilli, V., Miotto, G., Canton, M., Brini, M., Colonna, R., Bernardi, P., and Di Lisa, F. (1999) Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 76, 725-734 (Pubitemid 29264555)
48. Nomura, D. K., Morrison, B. E., Blankman, J. L., Long, J. Z., Kinsey, S. G., Marcondes, M. C., Ward, A. M., Hahn, Y. K., Lichtman, A. H., Conti, B., and Cravatt, B. F. (2011) Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 334, 809-813
49. Bisogno, T., Howell, F., Williams, G., Minassi, A., Cascio, M. G., Ligresti, A., Matias, I., Schiano-Moriello, A., Paul, P., Williams, E. J., Gangadharan, U., Hobbs, C., Di Marzo, V., and Doherty, P. (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 163, 463-468 (Pubitemid 37429860)
50. Marrs, W. R., Blankman, J. L., Horne, E. A., Thomazeau, A., Lin, Y. H., Coy, J., Bodor, A. L., Muccioli, G. G., Hu, S. S., Woodruff, G., Fung, S., Lafourcade, M., Alexander, J. P., Long, J. Z., Li, W., Xu, C., Möller, T., Mackie, K., Manzoni, O. J., Cravatt, B. F., and Stella, N. (2010) The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors. Nat. Neurosci. 13, 951-957
51. Gelb, M. H., Svaren, J. P., and Abeles, R. H. (1985) Fluoro ketone inhibitors of hydrolytic enzymes. Biochemistry 24, 1813-1817 (Pubitemid 15019770)
52. Street, I. P., Lin, H. K., Laliberté, F., Ghomashchi, F., Wang, Z., Perrier, H., Tremblay, N. M., Huang, Z., Weech, P. K., and Gelb, M. H. (1993) Slowand tight-binding inhibitors of the 85-kDa human phospholipase A2. Biochemistry 32, 5935-5940 (Pubitemid 23198752)
53. Barbayianni, E., Stephens, D., Grkovich, A., Magrioti, V., Hsu, Y. H., Dolatzas, P., Kalogiannidis, D., Dennis, E. A., and Kokotos, G. (2009) 2-Oxoamide inhibitors of phospholipase A2 activity and cellular arachidonate release based on dipeptides and pseudodipeptides. Bioorg. Med. Chem. 17, 4833-4843
54. Matlib, M. A., Zhou, Z., Knight, S., Ahmed, S., Choi, K. M., Krause-Bauer, J., Phillips, R., Altschuld, R., Katsube, Y., Sperelakis, N., and Bers, D. M. (1998) Oxygen-bridged dinuclear ruthenium amine complex specifically inhibits Ca2+ uptake into mitochondria in vitro and in situ in single cardiac myocytes. J. Biol. Chem. 273, 10223-10231 (Pubitemid 28227624)
55. Contreras, L., Drago, I., Zampese, E., and Pozzan, T. (2010) Mitochondria. The calcium connection. Biochim. Biophys. Acta 1797, 607-618
56. Knox, C. D., Belous, A. E., Pierce, J. M., Wakata, A., Nicoud, I. B., Anderson, C. D., Pinson, C. W., and Chari, R. S. (2004) Novel role of phospholipase C-δ1. Regulation of liver mitochondrial Ca2+ uptake. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G533-540 (Pubitemid 39096618)
57. Chinopoulos, C., Starkov, A. A., Grigoriev, S., Dejean, L. M., Kinnally, K. W., Liu, X., Ambudkar, I. S., and Fiskum, G. (2005) Diacylglycerols activate mitochondrial cationic channel (s) and release sequestered Ca2+. J. Bioenerg. Biomembr. 37, 237-247 (Pubitemid 41420460)
58. Qiu, Z.-H., and Leslie, C. C. (1994) Protein kinase C-dependent and -independent pathways of mitogen-activated protein kinase activation in macrophages by stimuli that activate phospholipaseA2. J. Biol. Chem. 269, 19480-19487 (Pubitemid 24233475)
59. Leslie, C. C. (1997) Properties and regulation of cytosolic phospholipase A2. J. Biol. Chem. 272, 16709-16712
60. Nishizuka, Y. (1986) Studies and perspectives of protein kinase C. Science 233, 305-312
61. Korge, P., and Weiss, J. N. (1999) Thapsigargin directly induces the mitochondrial permeability transition. Eur. J. Biochem. 265, 273-280 (Pubitemid 29466036)
62. McGee, A. M., and Baines, C. P. (2011) Complement 1q-binding protein inhibits the mitochondrial permeability transition pore and protects against oxidative stress-induced death. Biochem. J. 433, 119-125
63. Vaseva, A. V., Marchenko, N. D., Ji, K., Tsirka, S. E., Holzmann, S., and Moll, U. M. (2012) p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 149, 1536-1548
64. Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S., Osinska, H., Hambleton, M. A., Brunskill, E. W., Sayen, M. R., Gottlieb, R. A., Dorn, G. W., Robbins, J., and Molkentin, J. D. (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662 (Pubitemid 40488559)
65. Adibekian, A., Martin, B. R., Wang, C., Hsu, K. L., Bachovchin, D. A., Niessen, S., Hoover, H., and Cravatt, B. F. (2011) Click-generated triazole ureas as ultrapotent in vivo-active serine hydrolase inhibitors. Nat. Chem. Biol. 7, 469-478
66. Hoover, H. S., Blankman, J. L., Niessen, S., and Cravatt, B. F. (2008) Selectivity of inhibitors of endocannabinoid biosynthesis evaluated by activitybased protein profiling. Bioorg. Med. Chem. Lett. 18, 5838-5841
67. Erickson, J. R., He, B. J., Grumbach, I. M., and Anderson, M. E. (2011) CaMKII in the cardiovascular system. Sensing redox states. Physiol. Rev. 91, 889-915
68. Salas, M. A., Valverde, C. A., Sánchez, G., Said, M., Rodriguez, J. S., Portiansky, E. L., Kaetzel, M. A., Dedman, J. R., Donoso, P., Kranias, E. G., and Mattiazzi, A. (2010) The signalling pathway of CaMKII-mediated apoptosis and necrosis in the ischemia/reperfusion injury. J. Mol. Cell Cardiol. 48, 1298-1306