A mouse model of in vivo chemical inhibition of retinal calcium-independent phospholipase A2 (iPLA2)

Biochimie

Volumn 95, Issue 4, 2013, Pages 903-911

  Saab Aoudé, Sarah ^a   Bron, Alain M ^a,b   Creuzot Garcher, Catherine P ^a,b   Bretillon, Lionel ^a   Acar, Niyazi ^a  

^a CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

^b DIJON UNIVERSITY HOSPITAL   (France)

Author keywords

Activity; Brain; Bromoenol lactone; Mouse; Phospholipase A2; Retina

Indexed keywords

BROMOENOL LACTONE; CALCIUM INDEPENDENT PHOSPHOLIPASE A2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN FUNCTION; RETINA;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; GROUP VI PHOSPHOLIPASES A2; HOMEOSTASIS; MALE; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; RETINA; TIME FACTORS;

ANIMALIA; MUS;

EID: 84874649306     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.12.008     Document Type: Article

References (73)

1. Z. Ma, and J. Turk The molecular biology of the group VIA Ca2+-independent phospholipase A2 Prog. Nucleic Acid Res. Mol. Biol. 67 2001 1 33
2. A.A. Farooqui, H.C. Yang, T.A. Rosenberger, and L.A. Horrocks Phospholipase A2 and its role in brain tissue J. Neurochem. 69 1997 889 901
3. D.A. Six, and E.A. Dennis The expanding superfamily of phospholipase A(2) enzymes: classification and characterization Biochim. Biophys. Acta 1488 2000 1 19
4. E.A. Dennis, J. Cao, Y.H. Hsu, V. Magrioti, and G. Kokotos Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention Chem. Rev. 111 2011 6130 6185
5. R.J. Mayer, and L.A. Marshall New insights on mammalian phospholipase A2(s); comparison of arachidonoyl-selective and -nonselective enzymes Faseb J. 7 1993 339 348
6. Y. Hirashima, A.A. Farooqui, J.S. Mills, and L.A. Horrocks Identification and purification of calcium-independent phospholipase A2 from bovine brain cytosol J. Neurochem. 59 1992 708 714
7. D. Portilla, and G. Dai Purification of a novel calcium-independent phospholipase A2 from rabbit kidney J. Biol. Chem. 271 1996 15451 15457
8. S.L. Hazen, R.J. Stuppy, and R.W. Gross Purification and characterization of canine myocardial cytosolic phospholipase A2. A calcium-independent phospholipase with absolute f1-2 regiospecificity for diradyl glycerophospholipids J. Biol. Chem. 265 1990 10622 10630
9. H.C. Yang, M. Mosior, B. Ni, and E.A. Dennis Regional distribution, ontogeny, purification, and characterization of the Ca2+-independent phospholipase A2 from rat brain J. Neurochem. 73 1999 1278 1287
10. P.K. Larsson, H.E. Claesson, and B.P. Kennedy Multiple splice variants of the human calcium-independent phospholipase A2 and their effect on enzyme activity J. Biol. Chem. 273 1998 207 214
11. Y. Shirai, and M. Ito Specific differential expression of phospholipase A2 subtypes in rat cerebellum J. Neurocytol. 33 2004 297 307
12. M.A. Balboa, J. Balsinde, S.S. Jones, and E.A. Dennis Identity between the Ca2+-independent phospholipase A2 enzymes from P388D1 macrophages and Chinese hamster ovary cells J. Biol. Chem. 272 1997 8576 8580
13. Y.C. Lio, L.J. Reynolds, J. Balsinde, and E.A. Dennis Irreversible inhibition of Ca(2+)-independent phospholipase A2 by methyl arachidonyl fluorophosphonate Biochim. Biophys. Acta 1302 1996 55 60
14. E.J. Ackermann, K. Conde-Frieboes, and E.A. Dennis Inhibition of macrophage Ca(2+)-independent phospholipase A2 by bromoenol lactone and trifluoromethyl ketones J. Biol. Chem. 270 1995 445 450
15. K. Conde-Frieboes, L.J. Reynolds, Y.C. Lio, M.R. Hale, H.H. Wasserman, and E.A. Dennis Activated Ketones as Inhibitors of Intracellular Ca2+-Dependent and Ca2+-Independent Phospholipase A2 J. Am. Chem. Soc. 118 1996 5519 5525
16. A.A. Farooqui, W.Y. Ong, and L.A. Horrocks Inhibitors of brain phospholipase A2 activity: their neuropharmacological effects and therapeutic importance for the treatment of neurologic disorders Pharmacol. Rev. 58 2006 591 620
17. S.L. Hazen, L.A. Zupan, R.H. Weiss, D.P. Getman, and R.W. Gross Suicide inhibition of canine myocardial cytosolic calcium-independent phospholipase A2. Mechanism-based discrimination between calcium-dependent and -independent phospholipases A2 J. Biol. Chem. 266 1991 7227 7232
18. S.B. Daniels, E. Cooney, M.J. Sofia, P.K. Chakravarty, and J.A. Katzenellenbogen Haloenol lactones. Potent enzyme-activated irreversible inhibitors for alpha-chymotrypsin J. Biol. Chem. 258 1983 15046 15053
19. X.R. Lu, W.Y. Ong, B. Halliwell, L.A. Horrocks, and A.A. Farooqui Differential effects of calcium-dependent and calcium-independent phospholipase A(2) inhibitors on kainate-induced neuronal injury in rat hippocampal slices Free Radic. Biol. Med. 30 2001 1263 1273
20. P. Rahnema, Y. Shimoni, and A. Nygren Reduced conduction reserve in the diabetic rat heart: role of iPLA2 activation in the response to ischemia Am. J. Physiol. Heart Circ. Physiol. 300 2010 H326 H334
21. J. Balsinde, M.A. Balboa, and E.A. Dennis Antisense inhibition of group VI Ca2+-independent phospholipase A2 blocks phospholipid fatty acid remodeling in murine P388D1 macrophages J. Biol. Chem. 272 1997 29317 29321
22. G. Beck, Y. Sugiura, K. Shinzawa, S. Kato, M. Setou, Y. Tsujimoto, S. Sakoda, and H. Sumi-Akamaru Neuroaxonal dystrophy in calcium-independent phospholipase A2beta deficiency results from insufficient remodeling and degeneration of mitochondrial and presynaptic membranes J. Neurosci. 31 2011 11411 11420
23. C.D. Anfuso, G. Lupo, L. Romeo, G. Giurdanella, C. Motta, A. Pascale, C. Tirolo, B. Marchetti, and M. Alberghina Endothelial cell-pericyte cocultures induce PLA2 protein expression through activation of PKCalpha and the MAPK/ERK cascade J. Lipid Res. 48 2007 782 793
24. G. Giurdanella, C. Motta, S. Muriana, V. Arena, C.D. Anfuso, G. Lupo, and M. Alberghina Cytosolic and calcium-independent phospholipase A(2) mediate glioma-enhanced proangiogenic activity of brain endothelial cells Microvasc. Res. 81 2011 1 17
25. S.P. Herbert, and J.H. Walker Group VIA calcium-independent phospholipase A2 mediates endothelial cell S phase progression J. Biol. Chem. 281 2006 35709 35716
26. A. Maeda, Y. Ozaki, S. Sivakumaran, T. Akiyama, H. Urakubo, A. Usami, M. Sato, K. Kaibuchi, and S. Kuroda Ca2+-independent phospholipase A2-dependent sustained Rho-kinase activation exhibits all-or-none response Genes Cells 11 2006 1071 1083
27. A.A. Farooqui, H.C. Yang, and L. Horrocks Involvement of phospholipase A2 in neurodegeneration Neurochem. Int. 30 1997 517 522
28. W.Y. Ong, T. Farooqui, and A.A. Farooqui Involvement of cytosolic phospholipase A(2), calcium independent phospholipase A(2) and plasmalogen selective phospholipase A(2) in neurodegenerative and neuropsychiatric conditions Curr. Med. Chem. 17 2010 2746 2763
29. S. Khateeb, H. Flusser, R. Ofir, I. Shelef, G. Narkis, G. Vardi, Z. Shorer, R. Levy, A. Galil, K. Elbedour, and O.S. Birk PLA2G6 mutation underlies infantile neuroaxonal dystrophy Am. J. Hum. Genet. 79 2006 942 948
30. P. Zhang, Z. Gao, Y. Jiang, J. Wang, F. Zhang, S. Wang, Y. Yang, H. Xiong, Y. Zhang, X. Bao, J. Xiao, X. Wu, and Y. Wu Follow-up study of 25 Chinese children with PLA2G6-associated neurodegeneration Eur. J. Neurol. 2012
31. E.K. Tan, P. Ho, L. Tan, K.M. Prakash, and Y. Zhao PLA2G6 mutations and Parkinson's disease Ann. Neurol. 67 2010 148
32. J.Y. Tian, B.S. Tang, C.H. Shi, Z.Y. Lv, K. Li, R.L. Yu, L. Shen, X.X. Yan, and J.F. Guo Analysis of PLA2G6 gene mutation in sporadic early-onset parkinsonism patients from Chinese population Neurosci. Lett. 514 2012 156 158
33. K. Shinzawa, H. Sumi, M. Ikawa, Y. Matsuoka, M. Okabe, S. Sakoda, and Y. Tsujimoto Neuroaxonal dystrophy caused by group VIA phospholipase A2 deficiency in mice: a model of human neurodegenerative disease J. Neurosci. 28 2008 2212 2220
34. S. Bao, D.A. Jacobson, M. Wohltmann, A. Bohrer, W. Jin, L.H. Philipson, and J. Turk Glucose homeostasis, insulin secretion, and islet phospholipids in mice that overexpress iPLA2beta in pancreatic beta-cells and in iPLA2beta-null mice Am. J. Physiol. Endocrinol. Metab. 294 2008 E217 E229
35. S. Bao, H. Song, M. Wohltmann, S. Ramanadham, W. Jin, A. Bohrer, and J. Turk Insulin secretory responses and phospholipid composition of pancreatic islets from mice that do not express Group VIA phospholipase A2 and effects of metabolic stress on glucose homeostasis J. Biol. Chem. 281 2006 20958 20973
36. H. Song, M. Wohltmann, S. Bao, J.H. Ladenson, C.F. Semenkovich, and J. Turk Mice deficient in group VIB phospholipase A2 (iPLA2gamma) exhibit relative resistance to obesity and metabolic abnormalities induced by a Western diet Am. J. Physiol. Endocrinol. Metab. 298 2010 E1097 E1114
37. J. Wang, and M. Kolko Phospholipases A2 in ocular homeostasis and diseases Biochimie 92 2010 611 619
38. S. Ronkko, P. Rekonen, K. Kaarniranta, T. Puustjarvi, M. Terasvirta, and H. Uusitalo Phospholipase A2 in chamber angle of normal eyes and patients with primary open angle glaucoma and exfoliation glaucoma Mol. Vis. 13 2007 408 417
39. T. Pannicke, I. Iandiev, A. Wurm, O. Uckermann, F. vom Hagen, A. Reichenbach, P. Wiedemann, H.P. Hammes, and A. Bringmann Diabetes alters osmotic swelling characteristics and membrane conductance of glial cells in rat retina Diabetes 55 2006 633 639
40. J.M. Barnett, G.W. McCollum, and J.S. Penn Role of cytosolic phospholipase A(2) in retinal neovascularization Investig. Ophthalmol. Vis. Sci. 51 2009 1136 1142
41. M. Kolko, J. Wang, C. Zhan, K.A. Poulsen, J.U. Prause, M.H. Nissen, S. Heegaard, and N.G. Bazan Identification of intracellular phospholipases A2 in the human eye: involvement in phagocytosis of photoreceptor outer segments Investig. Ophthalmol. Vis. Sci. 48 2007 1401 1409
42. M. Kolko, J.F. Kiilgaard, J. Wang, K.A. Poulsen, J.R. Andreasen, M. la Cour, M.H. Nissen, S. Heegaard, N.G. Bazan, and J.U. Prause Calcium-independent phospholipase A2 regulates retinal pigment epithelium proliferation and may be important in the pathogenesis of retinal diseases Exp. Eye Res. 89 2009 383 391
43. C. Zhan, J. Wang, and M. Kolko Diverse Regulation of Retinal Pigment Epithelium Phagocytosis of Photoreceptor Outer Segments by Calcium-Independent Phospholipase A(2), Group VIA and Secretory Phospholipase A(2), Group IB Curr. Eye Res. 2012
44. K. Song, X. Zhang, C. Zhao, N.T. Ang, and Z.A. Ma Inhibition of Ca2+-independent phospholipase A2 results in insufficient insulin secretion and impaired glucose tolerance Mol. Endocrinol. 19 2005 504 515
45. C. Baskakis, V. Magrioti, N. Cotton, D. Stephens, V. Constantinou- Kokotou, E.A. Dennis, and G. Kokotos Synthesis of polyfluoro ketones for selective inhibition of human phospholipase A2 enzymes J. Med. Chem. 51 2008 8027 8037
46. R. Lopez-Vales, X. Navarro, T. Shimizu, C. Baskakis, G. Kokotos, V. Constantinou-Kokotou, D. Stephens, E.A. Dennis, and S. David Intracellular phospholipase A(2) group IVA and group VIA play important roles in Wallerian degeneration and axon regeneration after peripheral nerve injury Brain 131 2008 2620 2631
47. E. Boilard, S.G. Bourgoin, C. Bernatchez, P.E. Poubelle, and M.E. Surette Interaction of low molecular weight group IIA phospholipase A2 with apoptotic human T cells: role of heparan sulfate proteoglycans Faseb J. 17 2003 1068 1080
48. M. Fannon, K. Forsten-Williams, C.J. Dowd, D.A. Freedman, J. Folkman, and M.A. Nugent Binding inhibition of angiogenic factors by heparan sulfate proteoglycans in aqueous humor: potential mechanism for maintenance of an avascular environment Faseb J. 17 2003 902 904
49. H.C. Yang, A.A. Farooqui, and L.A. Horrocks Effects of glycosaminoglycans and glycosphingolipids on cytosolic phospholipases A2 from bovine brain Biochem. J. 299 Pt 1 1994 91 95
50. H.C. Yang, A.A. Farooqui, and L.A. Horrocks Characterization of plasmalogen-selective phospholipase A2 from bovine brain Adv. Exp. Med. Biol. 416 1996 309 313
51. H.C. Yang, A.A. Farooqui, and L.A. Horrocks Effects of sialic acid and sialoglycoconjugates on cytosolic phospholipases A2 from bovine brain Biochem. Biophys. Res. Commun. 199 1994 1158 1166
52. S.L. Hazen, L.A. Loeb, and R.W. Gross Purification and characterization of cytosolic phospholipase A2 activities from canine myocardium and sheep platelets Methods Enzymol. 197 1991 400 411
53. R.A. Wolf, and R.W. Gross Identification of neutral active phospholipase C which hydrolyzes choline glycerophospholipids and plasmalogen selective phospholipase A2 in canine myocardium J. Biol. Chem. 260 1985 7295 7303
54. A.A. Farooqui Studies on plasmalogen-selective phospholipase A2 in brain Mol. Neurobiol. 41 2010 267 273
55. C.M. Jenkins, D.J. Mancuso, W. Yan, H.F. Sims, B. Gibson, and R.W. Gross Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities J. Biol. Chem. 279 2004 48968 48975
56. J. Balsinde, M.A. Balboa, P.A. Insel, and E.A. Dennis Regulation and inhibition of phospholipase A2 Annu. Rev. Pharmacol. Toxicol. 39 1999 175 189
57. S. Fujita, Y. Ikegaya, N. Nishiyama, and N. Matsuki Ca2+-independent phospholipase A2 inhibitor impairs spatial memory of mice Jpn. J. Pharmacol. 83 2000 277 278
58. M.J. Wolf, Y. Izumi, C.F. Zorumski, and R.W. Gross Long-term potentiation requires activation of calcium-independent phospholipase A2 FEBS Lett. 377 1995 358 362
59. S. Fujita, Y. Ikegaya, M. Nishikawa, N. Nishiyama, and N. Matsuki Docosahexaenoic acid improves long-term potentiation attenuated by phospholipase A(2) inhibitor in rat hippocampal slices Br. J. Pharmacol. 132 2001 1417 1422
60. Z. Guo, W. Su, Z. Ma, G.M. Smith, and M.C. Gong Ca2+-independent phospholipase A2 is required for agonist-induced Ca2+ sensitization of contraction in vascular smooth muscle J. Biol. Chem. 278 2003 1856 1863
61. X. Ji, T. Nishihashi, C.C. Trandafir, A. Wang, Y. Shimizu, and K. Kurahashi Pharmacological nature of nicotine-induced contraction in the rat basilar artery: involvement of arachidonic acid metabolites Eur. J. Pharmacol. 577 2007 109 114
62. K.M. Park, M. Trucillo, N. Serban, R.A. Cohen, and V.M. Bolotina Role of iPLA2 and store-operated channels in agonist-induced Ca2+ influx and constriction in cerebral, mesenteric, and carotid arteries Am. J. Physiol. Heart Circ. Physiol. 294 2008 H1183 H1187
63. F. St-Gelais, C. Menard, P. Congar, L.E. Trudeau, and G. Massicotte Postsynaptic injection of calcium-independent phospholipase A2 inhibitors selectively increases AMPA receptor-mediated synaptic transmission Hippocampus 14 2004 319 325
64. W.J. Brown, K. Chambers, and A. Doody Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function Traffic 4 2003 214 221
65. N. Kuroiwa, M. Nakamura, M. Tagaya, and A. Takatsuki Arachidonyltrifluoromethy ketone, a phospholipase A(2) antagonist, induces dispersal of both Golgi stack- and trans Golgi network-resident proteins throughout the cytoplasm Biochem. Biophys. Res. Commun. 281 2001 582 588
66. P.A. Stewart, and U.I. Tuor Blood-eye barriers in the rat: correlation of ultrastructure with function J. Comp. Neurol. 340 1994 566 576
67. S.R. Ennis Permeability of the blood-ocular barrier to mannitol and PAH during experimental diabetes Curr. Eye Res. 9 1990 827 838
68. E.M. Cornford The blood-brain barrier, a dynamic regulatory interface Mol. Physiol. 7 1985 219 259
69. V.A. Levin Relationship of octanol/water partition coefficient and molecular weight to rat brain capillary permeability J. Med. Chem. 23 1980 682 684
70. K. Hosoya, A. Yamamoto, S. Akanuma, and M. Tachikawa Lipophilicity and transporter influence on blood-retinal barrier permeability: a comparison with blood-brain barrier permeability Pharm. Res. 27 2010 2715 2724
71. R. Toda, K. Kawazu, M. Oyabu, T. Miyazaki, and Y. Kiuchi Comparison of drug permeabilities across the blood-retinal barrier, blood-aqueous humor barrier, and blood-brain barrier J. Pharm. Sci. 100 2011 3904 3911
72. N. Acar, B. Bonhomme, C. Joffre, A.M. Bron, C. Creuzot-Garcher, L. Bretillon, M. Doly, and J.M. Chardigny The retina is more susceptible than the brain and the liver to the incorporation of trans isomers of DHA in rats consuming trans isomers of alpha-linolenic acid Reprod. Nutr. Dev. 46 2006 515 525
73. S.B. Daniels, and J.A. Katzenellenbogen Halo enol lactones: studies on the mechanism of inactivation of alpha-chymotrypsin Biochemistry 25 1986 1436 1444