Regulation of the Ca2+ -independent phospholipase a 2 in liver mitochondria by changes in the energetic state

Journal of Lipid Research

Volumn 55, Issue 5, 2014, Pages 826-836

  Rauckhorst, Adam J ^a   Broekemeier, Kimberly M ^c,d   Pfeiffer, Douglas R ^a,b,c  

^a Departments of Molecular and Cellular Biochemistry   (United States)

^b Internal Medicine Institute for Mitochondrial Biology   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d OHIO NORTHERN UNIVERSITY   (United States)

Author keywords

Electron transport chain inhibitors; Membrane potential; Redox status

Indexed keywords

BROMOENOL LACTONE; CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CYTOCHROME A; CYTOCHROME C OXIDASE; MALONIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; UBIQUINOL CYTOCHROME C REDUCTASE; 6-(BROMOMETHYLENE)TETRAHYDRO-3-(1-NAPHTHALENEYL)-2H-PYRAN-2-ONE; NAPHTHALENE DERIVATIVE; PYRONE DERIVATIVE;

ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVATION; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; RAT; ANIMAL; DRUG EFFECTS; ENERGY METABOLISM; ENZYMOLOGY; METABOLISM;

ANIMALS; ELECTRON TRANSPORT; ENERGY METABOLISM; ENZYME ACTIVATION; MITOCHONDRIA, LIVER; NAPHTHALENES; PHOSPHOLIPASES A2, CALCIUM-INDEPENDENT; PYRONES; RATS;

EID: 84899539506     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M043307     Document Type: Article

References (58)

1. Hunter, F. E., Jr., and L. Ford. 1955. Inactivation of oxidative and phosphorylative systems in mitochondria by preincubation with phosphate and other ions. J. Biol. Chem. 216 : 357-369.
2. Wojtczak, L., and A. L. Lehninger. 1961. Formation and disappearance of an endogenous uncoupling factor during swelling and contraction of mitochondria. Biochim. Biophys. Acta. 51 : 442-456.
3. Chappell, J. B., and A. R. Crofts. 1965. Calcium ion accumulation and volume changes of isolated liver mitochondria. Calcium ioninduced swelling. Biochem. J. 95 : 378-386.
4. Waite, M., L. L. M. Van Deenen, T. J. C. Ruigrok, and P. F. Elbers. 1969. Relation of mitochondrial phospholipase A activity to mitochondrial swelling. J. Lipid Res. 10 : 599-608.
5. Pfeiffer, D. R., R. F. Kauffman, and H. A. Lardy. 1978. Effects of N-ethylmaleimide on the limited uptake of Ca 2+, Mn 2+, and Sr 2+ by rat liver mitochondria. J. Biol. Chem. 253 : 4165-4171.
6. Pfeiffer, D. R., P. C. Schmid, M. C. Beatrice, and H. H. O. Schmid. 1979. Intramitochondrial phospholipase activity and the effects of Ca 2+ plus N-ethylmaleimide on mitochondrial function. J. Biol. Chem. 254 : 11485-11494.
7. Haworth, R. A., and D. R. Hunter. 1979. The Ca 2+ -induced membrane transition in mitochondria. II. Nature of the Ca 2+ trigger site. Arch. Biochem. Biophys. 195 : 460-467.
8. Hunter, D. R., and R. A. Haworth. 1979. The Ca 2+ -induced membrane transition in mitochondria. I. The protective mechanisms. Arch. Biochem. Biophys. 195 : 453-459.
9. Hunter, D. R., and R. A. Haworth. 1979. The Ca 2+ -induced membrane transition in mitochondria. III. Transitional Ca 2+ release. Arch. Biochem. Biophys. 195 : 468-477.
10. Gunter, T. E., and D. R. Pfeiffer. 1990. The mechanisms by which mitochondria transport calcium. Am. J. Physiol. 258 : C755-C786.
11. Pfeiffer, D. R., T. E. Gunter, R. Eliseev, K. M. Broekemeier, and K. K. Gunter. 2001. Release of Ca 2+ from mitochondria via the saturable mechanisms and the permeability transition. IUBMB Life. 52 : 205-212.
12. Pfeiffer, D. R., T. H. Kuo, and T. T. Tchen. 1976. Some effects of Ca 2+, Mg 2+, and Mn 2+ on the ultrastructural, light-scattering properties, and malic enzyme activity of adrenal cortex mitochondria. Arch. Biochem. Biophys. 176 : 556-563.
13. Pfeiffer, D. R., and T. T. Tchen. 1975. The activation of adrenal cortex mitochondrial malic enzyme by Ca 2+ and Mg 2+. Biochemistry. 14 : 89-96.
14. Waite, M., and P. Sisson. 1971. Partial purification and characterization of the phospholipase A 2 from rat liver mitochondria. Biochemistry. 10 : 2377-2383.
15. De Winter, J. M., G. M. Vianen, and H. Van den Bosch. 1982. Purification of rat liver mitochondrial phospholipase A 2. Biochim. Biophys. Acta. 712 : 332-341.
16. Aarsman, A. J., J. G. N. de Jong, E. Arnoldussen, F. W. Neys, P. D. van Wassenaar, and H. Van den Bosch. 1989. Immunoaffinity purification, partial sequence, and subcellular localization of rat liver phospholipase A 2. J. Biol. Chem. 264 : 10008-10014.
17. Reers, M., and D. R. Pfeiffer. 1987. Inhibition of mitochondrial phospholipase A 2 by mono- and dilysocardiolipin. Biochemistry. 26 : 8038-8041.
18. Van Schaik, R. H. N., N. M. Verhoeven, F. W. Neijs, A. J. Aarsman, and H. Van den Bosch. 1993. Cloning of the cDNA for 14 kDa group II phospholipase A 2 from rat liver. Biochim. Biophys. Acta. 1169 : 1-11.
19. Inada, M., H. Tojo, S. Kawata, S. Tarui, and M. Okamoto. 1991. Preferential distribution of group-II-like phospholipase A 2 in mononuclear phagocytic cells in rat spleen and liver. Eur. J. Biochem. 197 : 323-329.
20. Hatch, G. M., D. E. Vance, and D. C. Wilton. 1993. Rat liver mitochondrial phospholipase A 2 is an endotoxin-stimulated membraneassociated enzyme of Kupffer cells which is released during liver perfusion. Biochem. J. 293 : 143-150.
21. Medvedev, B. I., E. P. Severina, V. G. Gogvadze, E. A. Chukhlova, and Y. V. Evtodienko. 1985. Participation of endogenous fatty acids in Ca 2+ release activation from mitochondria. Gen. Physiol. Biophys. 4 : 549-556.
22. Hunter, D. R., R. A. Haworth, and J. H. Southard. 1976. Relationship between configuration, function, and permeability in calciumtreated mitochondria. J. Biol. Chem. 251 : 5069-5077.
23. Roman, I., P. Gmaj, C. Nowicka, and S. Angielski. 1979. Regulation of Ca 2+ efflux from kidney and liver mitochondria by unsaturated fatty acids and Na+ ions. Eur. J. Biochem. 102 : 615-623.
24. Bernardi, P., K. M. Broekemeier, and D. R. Pfeiffer. 1994. Recent progress on regulation of the mitochondrial permeability transition: a cyclosporin sensitive pore in the inner mitochondrial membrane. J. Bioenerg. Biomembr. 26 : 509-517.
25. Broekemeier, K. M., and D. R. Pfeiffer. 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.
26. Broekemeier, K. M., J. R. Iben, E. G. LeVan, E. D. Crouser, and D. R. Pfeiffer. 2002. Pore formation and uncoupling initiate a Ca 2+ -independent degradation of mitochondrial phospholipids. Biochemistry. 41 : 7771-7780.
27. Gadd, M. E., K. M. Broekemeier, E. D. Crouser, J. Kumar, G. Graff, and D. R. Pfeiffer. 2006. Mitochondrial iPLA 2 activity modulates the release of cytochrome c from mitochondria and influences the permeability transition. J. Biol. Chem. 281 : 6931-6939.
28. Williams, S. D., and R. A. Gottlieb. 2002. Inhibition of mitochondrial calcium-independent phospholipase A 2 (iPLA 2 ) attenuates mitochondrial phospholipid loss and is cardioprotective. Biochem. J. 362 : 23-32.
29. Blum, J. L., G. R. Kinsey, P. Monian, B. Sun, B. S. Cummings, J. McHowat, and R. G. Schnellmann. 2011. Profiling of fatty acids released during calcium-induced mitochondrial permeability transition in isolated rabbit kidney mitochondria. Toxicol. In Vitro. 25 : 1001-1006.
30. Kinsey, G. R., J. McHowat, S. Beckett, and R. G. Schnellmann. 2007. Identification of calcium-independant phospholipase A2gamma in mitochondria and its role in mitochondrial oxidative stress. Am. J. Physiol. Renal Physiol. 292 : F853-F860.
31. Kinsey, G. R., J. McHowat, S. Beckett, and R. G. Schnellmann. 2007. Role of Ca 2+ -independent phospholipase A2gamma in Ca 2+ -induced mitochondrial permeability transition. J. Pharmacol. Exp. Ther. 321 : 707-715.
32. Brustovetsky, T., B. Antonsson, R. Jemmerson, J. M. Dubinsky, and N. N. Brustovetsky. 2005. Activation of calcium-independant phospholipase A (iPLA) in brain mitochondria and release of apoptogenic factors by BAX and truncated BID. J. Neurochem. 94 : 980-994.
33. Jaburek, M., J. Jezek, J. Zelenka, and P. Jezek. 2013. Antioxidant activity by a synergy of redox-sensitive mitochondrial phospholipase A 2 and uncoupling protein-2 in lung and spleen. Int. J. Biochem. Cell Biol. 45 : 816-825.
34. Broekemeier, K. M., P. C. Schmid, H. H. O. Schmid, and D. R. Pfeiffer. 1985. Effects of phospholipase A 2 inhibitors on ruthenium red-induced Ca 2+ release from mitochondria. J. Biol. Chem. 260 : 105-113.
35. Broekemeier, K. M., C. K. Klocek, and D. R. Pfeiffer. 1998. Proton selective substate of the mitochondrial permeability transition pore: regulation by the redox state of the electron transport chain.. Biochemistry. 37 : 13059-13065.
36. Igbavboa, U., and D. R. Pfeiffer. 1991. Transient induction of the mitochondrial permeability transition by uncoupler plus a Ca(2+)-specific chelator. Biochim. Biophys. Acta. 1059 : 339-347.
37. Marcinkeviciute, A., V. Mildaziene, S. Crumm, O. Demin, J. B. Hoek, and B. N. Kholodenko. 2000. Kinetics and control of oxidative phosphorylation in rat liver mitochondria after chronic ethanol feeding. Biochem. J. 349 : 519-526.
38. Chance, B., and G. R. Williams. 1955. Respiratory enzymes in oxidative phosphorylation. II. Difference spectra. J. Biol. Chem. 217 : 395-407.
39. Schlenk, H., and J. L. Gellerman. 1960. Esterification of fatty acids with diazomethane on a small scale. Anal. Chem. 32 : 1412-1414.
40. Ingledew, W. J., and T. Ohnishi. 1977. The probable site of action of thenoyltrifluoroacetone on the respiratory chain. Biochem. J. 164 : 617-620.
41. Nelson, B. D., B. Norling, B. Persson, and L. Ernster. 1971. Effect of thenoyltrifluoroacetone on the interaction of succinate dehydrogenase and cytochrome b in ubiquinone-depleted submitochondrial particles. Biochem. Biophys. Res. Commun. 44 : 1312-1320.
42. Pfeiffer, D. R., T. I. Gudz, S. A. Novgorodov, and W. L. Erdahl. 1995. The peptide mastoparan is a potent facilitator of the mitochondrial permeability transition. J. Biol. Chem. 270 : 4923-4932.
43. Giedt, R. J., D. R. Pfeiffer, A. Matzavinos, C. Y. Kao, and B. R. Alevriadou. 2012. Mitochondrial dynamics and motility inside living vascular endothelial cells: role of bioenergetics. Ann. Biomed. Eng. 40 : 1903-1916.
44. Mancuso, D. J., C. M. Jenkins, H. F. Sims, J. M. Cohen, J. Yang, and R. W. Gross. 2004. Complex transcriptional and translational regulation of iPLAgamma resulting in multiple gene products containing dual competing sites for mitochondrial or peroxisomal localization. Eur. J. Biochem. 271 : 4709-4724.
45. Mancuso, D. J., C. M. Jenkins, and R. W. Gross. 2000. The genomic organization, complete mRNA sequence, cloning, and expression of a novel human intracellular membrane-associated calciumindependent phospholipase A(2). J. Biol. Chem. 275 : 9937-9945.
46. Wolf, M. J., and R. W. Gross. 1996. Expression, purification, and kinetic characterization of a recombinant 80-kDa intracellular calcium-independent phospholipase A 2. J. Biol. Chem. 271 : 30879-30885.
47. Moon, S. H., C. M. Jenkins, X. Liu, S. Guan, D. J. Mancuso, and A. Gross. 2012. Activation of mitochondrial calcium-independent phospholipase A2γ (iPLA2γ) by divalent cations mediating arachidonate release and production of downstream eicosanoids. J. Biol. Chem. 287 : 14880-14895.
48. Moon, S. H., C. M. Jenkins, M. A. Kiebish, H. F. Sims, D. J. Mancuso, and R. W. Gross. 2012. Genetic ablation of calcium-independent phospholipase A(2)γ (iPLA(2)γ) attenuates calcium-induced opening of the mitochondrial permeability transition pore and resultant cytochrome c release. J. Biol. Chem. 287 : 29837-29850.
49. Lemasters, J. J., A-L. Nieminen, T. Qian, L. C. Trost, S. P. Elmore, Y. Nishimura, R. M. Crowl, W. E. Cascio, C. A. Bradham, D. A. Brenner, et al. 1998. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta. 1366 : 177-196.
50. Skulachev, V. P. 1998. Uncoupling: new approaches to an old problem of bioenergetics. Biochim. Biophys. Acta. 1363 : 100-124.
51. Song, H., S. Ramanadham, S. Bao, F. F. Hsu, and J. Turk. 2006. A bromoenol lactone suicide substrate inactivates group VIA phospholipase A 2 by generating a diffusible bromomethyl keto acid that alkylates cysteine thiols. Biochemistry. 45 : 1061-1073.
52. Hao, C. M., and M. D. Breyer. 2008. Physiological regulation of prostaglandins in the kidney. Annu. Rev. Physiol. 70 : 357-377.
53. Venuto, R. C., T. O'Dorisio, J. H. Stein, and T. F. Ferris. 1975. Uterine prostaglandin E secretion and uterine blood flow in the pregnant rabbit. J. Clin. Invest. 55 : 193-197.
54. Mancuso, D. J., H. F. Sims, X. Han, C. M. Jenkins, S. P. Gaun, K. Yang, S. H. Moon, T. Pietka, N. A. Abumrad, P. H. Schlesinger, et al. 2007. Genetic ablation of calcium-independent phospholipase A 2 gamma leads to alterations of mitochondrial lipid metabolism and function resulting in a deficient mitochondrial phenotype. J. Biol. Chem. 282 : 34611-34622.
55. Bao, S., H. Song, M. Wohltmann, S. Ramanadham, W. Jin, A. Bohrer, and J. Turk. 2006. Insulin secretory response and phospholipid composition of pancreatic islets from mice that do not express group VIA phospholipase A 2 and effects of metabolic stress on glucose homeostasis. J. Biol. Chem. 281 : 20958-20973.
56. Bao, S., D. J. Miller, Z. Ma, M. Wohltmann, G. Eng, S. Ramandham, K. Moley, and J. Turk. 2004. Male mice that do not express group VIA phospholipase A 2 produce spermatozoa with impaired motility and have greatly reduced fertility. J. Biol. Chem. 279 : 38194-38200.
57. Dennis, E. A., J. Cao, Y-H. Hsu, V. Margroti, and G. Kokotos. 2011. Phospholipase A 2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem. Rev. 111 : 6130-6185.
58. Crouser, E. D., M. E. Gadd, M. W. Julian, J. E. Huff, K. M. Broekemeier, K. A. Robbins, and D. R. Pfeiffer. 2003. Quantitation of cytochrome c release from rat liver mitochondria. Anal. Biochem. 317 : 67-75.