Breaking the chain at the membrane: Paraoxonase 2 counteracts lipid peroxidation at the plasma membrane

FASEB Journal

Volumn 28, Issue 4, 2014, Pages 1769-1779

  Hagmann, Henning ^a   Kuczkowski, Alexander ^a   Ruehl, Michael ^a   Lamkemeyer, Tobias ^b   Brodesser, Susanne ^a,b   Horke, Sven ^c   Dryer, Stuart ^d   Schermer, Bernhard ^a,b   Benzing, Thomas ^a,b   Brinkkoetter, Paul Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^d University of Houston   (United States)

Author keywords

Arylesterase; Atherosclerosis; Inflammation; Oxidative stress

Indexed keywords

ARYLDIALKYLPHOSPHATASE 2;

ARTICLE; BIOTINYLATION; CELL FRACTIONATION; CELL MEMBRANE; EMBRYO; FEMALE; GENETIC TRANSFECTION; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; LIPID PEROXIDATION; MEMBRANE STRUCTURE; MOLECULAR CLONING; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS;

ARYLESTERASE; ATHEROSCLEROSIS; INFLAMMATION; OXIDATIVE STRESS;

AMINO ACID SEQUENCE; ANIMALS; ARYLDIALKYLPHOSPHATASE; CALCIUM; CELL MEMBRANE; EPITHELIAL CELLS; GLUCOSYLCERAMIDES; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTESTINES; LIPID PEROXIDATION; MEMBRANE PROTEINS; MICE; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PROTEIN TRANSPORT; RNA INTERFERENCE;

EID: 84901020481     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-240309     Document Type: Article

References (52)

1. Wong-Eekkabut, J., Xu, Z., Triampo, W., Tielemann, P. and Monticelli, L. (2007) Effect of lipid peroxidation on the properties of lipid bilayers: a molecular dynamics study. Biophys. J. 93, 4225-4236
2. Jarerattanachat, V., Karttunen, M., and Wong-Ekkabut, J. (2013) Molecular dynamics study of oxidized lipid bilayers in NaCl solution. J. Phys. Chem. B 117, 8490-8501
3. Kunimoto, M., Inoue, K. and Nojima, S. (1981) Effect of ferrous ion and ascorbate-induced lipid peroxidation on liposomal membranes. BBA Biomembranes 646, 169 -178 (Pubitemid 11016444)
4. Minoguchi, K., Yokoe, T., Tanaka, A., Ohta, S., Hirano, T., Yoshino, G., O'Donnell, C. P., and Adachi, M. (2006) Association between lipid peroxidation and inflammation in obstructive sleep apnoea. Eur. Respir. J. 28, 378-385
5. Young, O., Crotty, T., O'Connell, R., O'Sullivan, J., and Curran, A. J. (2010) Levels of oxidative damage and lipid peroxidation in thyroid neoplasia. Head Neck 32, 750-756
6. Patel, B. P., Rawal, U. M., Dave, T. K., Rawal, R. M., Shukla, S. N., Shah, P. M., and Patel, P. S. (2007) Lipid peroxidation, total antioxidant status, and total thiol levels predict overall survival in patients with oral squamous cell carcinoma. Integr. Cancer Ther. 6, 365-372
7. Tsao, S.-M., Yin, M.-C., and Liu, W.-H. (2007) Oxidant stress and B vitamins status in patients with non-small cell lung cancer. Nutr. Cancer 59, 8-13
8. Völkel, W., Sicilia, T., Pähler, A., Gsell, W., Tatschner, T., Jellinger, K., Leblhuber, F., Riederer, P., Lutz, W. K., and Götz, M. E. (2006) Increased brain levels of 4-hydroxy-2-nonenal glutathione conjugates in severe Alzheimer's disease. Neurochem. Int. 48, 679-686
9. Patel, M., Liang, L. P., Hou, H., Williams, B. B., Kmiec, M., Swartz, H. M., Fessel, J. P., and Roberts, L. J., 2nd. (2008) Seizure-induced formation of isofurans: novel products of lipid peroxidation whose formation is positively modulated by oxygen tension. J. Neurochem. 104, 264-270
10. Musiek, E. S., Breeding, R. S., Milne, G. L., Zanoni, G., Morrow, J. D., and McLaughlin, B. (2006) Cyclopentenone isoprostanes are novel bioactive products of lipid oxidation which enhance neurodegeneration. J. Neurochem. 97, 1301-1313
11. Waddington, E. I., Croft, K. D., Sienuarine, K., Latham, B., and Puddey, I. B. (2003) Fatty acid oxidation products in human atherosclerotic plaque: an analysis of clinical and histopathological correlates. Atherosclerosis 167, 111-120
12. Ravandi, A., Babaei, S., Leung, R., Monge, J. C., Hoppe, G., Hoff, H., Kamido, H., and Kuksis, A. (2004) Phospholipids and oxophospholipids in atherosclerotic plaques at different stages of plaque development. Lipids 39, 97-109
13. Witztum, J. L., and Steinberg, D. (1991) Role of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 88, 1785-1792
14. Heinecke, J. W. (1998) Oxidants and antioxidants in the pathogenesis of atherosclerosis: implications for the oxidized low density lipoprotein hypothesis. Atherosclerosis 141, 1-15
15. Powers, S. K., and Jackson, M. J. (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 88, 1243-1276
16. Rhee, S. G., Chae, H. Z., and Kim, K. (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38, 1543-1552
17. Rosenblat, M., Coleman, R., Reddy, S. T., and Aviram, M. (2009) Paraoxonase 2 attenuates macrophage triglyceride accumulation via inhibition of diacylglycerol acyltransferase 1. J. Lipid Res. 50, 870-879
18. Ng, C. J., Bourquard, N., Grijalva, V., Hama, S., Shih, D. M., Navab, M., Fogelman, A. M., Lusis, A. J., Young, S., and Reddy, S. T. (2006) Paraoxonase-2 deficiency aggravates atherosclerosis in mice despite lower apolipoprotein-B-containing lipoproteins: anti-atherogenic role for paraoxonase-2. J. Biol. Chem. 281, 29491-29500
19. Ng, D. S., Chu, T., Esposito, B., Hui, P., Connelly, P. W., and Gross, P. L. (2008) Paraoxonase-1 deficiency in mice predisposes to vascular inflammation, oxidative stress, and thrombogenicity in the absence of hyperlipidemia. Cardiovasc. Path. 17, 226-232
20. Aviram, M., and Rosenblat, M. (2004) Paraoxonases 1, 2, and 3, oxidative stress, and macrophage foam cell formation during atherosclerosis development. Free Radic. Biol. Med. 37, 1304-1316
21. Mackness, B., Quarck, R., Verreth, W., Mackness, M. and Holvoet, P. (2006) Human paraoxonase-1 overexpression inhibits atherosclerosis in a mouse model of metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 26, 1545-1550
22. Aviram, M., and Rosenblat, M. (2008) Paraoxonases (PON1, PON2, PON3) analyses in vitro and in vivo in relation to cardiovascular diseases. In Advanced Protocols in Oxidative Stress I (Armstrong, D., ed) pp. 259-276, Humana Press, New York
23. Primo-Parmo, S. L., Sorenson, R. C., Teiber, J., and La Du, B. N. (1996) The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics 33, 498-507
24. Aviram, M., Rosenblat, M., Bisgaier, C. L., Newton, R. S., Primo-Parmo, S. L., and La Du, B. N. (1998) Paraoxonase inhibits high-density lipoprotein oxidation and preserves its functions. A possible peroxidative role for paraoxonase. J. Clin. Invest. 101, 1581-1590
25. Draganov, D. I., Stetson, P. L., Watson, C. E., Billecke, S. S., and La Du, B. N. (2000) Rabbit serum paraoxonase 3 (PON3) is a high density lipoprotein-associated lactonase and protects low density lipoprotein against oxidation. J. Biol. Chem. 275, 33435-33442
26. Mackness, M., Hallam, S., Peard, T., Warner, S., and Walker, C. (1985) The separation of sheep and human serum 'A'-esterase activity into the lipoprotein fraction by ultracentrifugation. Comp. Biochem. Physiol. B 82, 675-677
27. Horke, S., Witte, I., Wilgenbus, P., Krüger, M., Strand, D., and Förstermann, U. (2007) Paraoxonase-2 reduces oxidative stress in vascular cells and decreases endoplasmic reticulum stress-induced caspase activation. Circulation 115, 2055-2064
28. Ng, C. J., Wadleigh, D. J., Gangopadhyay, A., Hama, S., Grijalva, V. R., Navab, M., Fogelman, A. M., and Reddy, S. T. (2001) Paraoxonase-2 is a ubiquitously expressed protein with antioxidant properties and is capable of preventing cell-mediated oxidative modification of low density lipoprotein. J. Biol. Chem. 276, 44444-44449
29. Mackness, B., Beltran-Debon, R., Aragones, G., Joven, J., Camps, J., and Mackness, M. (2010) Human tissue distribution of paraoxonases 1 and 2 mRNA. IUBMB Life 62, 480-482
30. Goswami, B., Tayal, D., Gupta, N., and Mallika, V. (2009) Paraoxonase: a multifaceted biomolecule. Clin. Chim. Acta 410, 1-12.
31. Horke, S., Witte, I., Altenhöfer, S., Wilgenbus, P., Goldeck, M., Förstermann, U., Xiao, J., Kramer, G. L., Haines, D. C., Chowdhary, P. K., Haley, R. W., and Teiber, J. F. (2010) Paraoxonase 2 is down-regulated by the Pseudomonas aeruginosa quorum sensing signal N-(3-oxododecanoyl)-L-homoserine lactone and attenuates oxidative stress induced by pyocyanin. Biochem. J. 426, 73-83
32. Witte, I., Altenhöfer, S., Wilgenbus, P., Amort, J., Clement, A. M., Pautz, A., Li, H., Förstermann, U., and Horke, S. (2011) Beyond reduction of atherosclerosis: PON2 provides apoptosis resistance and stabilizes tumor cells. Cell Death Dis. 2, e112
33. Wang, W., and Malcolm, B. A. (2001) Two-stage polymerase chain reaction protocol allowing introduction of multiple mutations, deletions, and insertions, using QuikChange site-directed mutagenesis. In In Vitro Mutagenesis Protocols, Vol. 182 (Braman, J., ed) pp. 37-43, Springer, Secaucus, NJ, USA
34. Brown, D. A., and Rose, J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544
35. Schindler, J., Jung, S., Niedner-Schatteburg, G., Friauf, E., and Nothwang, H. G. (2006) Enrichment of integral membrane proteins from small amounts of brain tissue. J. Neural Transm. 113, 995-1013
36. Fujiki, Y., Hubbard, A. L., Fowler, S., and Lazarow, P. B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102
37. Rappsilber, J., Mann, M., and Ishihama, Y. (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906
38. Signorelli, P., and Hannun, Y. (2002) Analysis and quantitation of ceramide. Methods Enzymol. 345, 275-294
39. Schwamb, J., Feldhaus, V., Baumann, M., Patz, M., Brodesser, S., Brinker, R., Claasen, J., Pallasch, C. P., Hallek, M., Wendtner, C. M., and Frenzel, L. P. (2012) B-cell receptor triggers drug sensitivity of primary CLL cells by controlling glucosylation of ceramides. Blood 120, 3978-3985
40. Levy, E., Trudel, K., Bendayan, M., Seidman, E., Delvin, E., Elchebly, M., Lavoie, J. C., Precourt, L. P., Amre, D., and Sinnett, D. (2007) Biological role, protein expression, subcellular localization, and oxidative stress response of paraoxonase 2 in the intestine of humans and rats. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G1252-G1261
41. Yang, Y., Zhang, Y., Cuevas, S., Villar, V. A., Escano, C., D'Asico L., Yu, P., Grandy, D. K., Felder, R. A., Armando, I., and Jose, P. A. (2012) Paraoxonase 2 decreases renal reactive oxygen species production, lowers blood pressure, and mediates dopamine D2 receptor-induced inhibition of NADPH oxidase. Free Radic. Biol. Med. 53, 437-446
42. Barrera, G. (2012) Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol. 2012, 137289
43. Quintanar-Escorza, M. A., González-Martínez, M. T., Del Pilar, I.-O. M., and Calderón-Salinas, J. V. (2010) Oxidative damage increases intracellular free calcium [Ca2-]i concentration in human erythrocytes incubated with lead. Toxicol. In Vitro 24, 1338-1346
44. Nagy, L., Tontonoz, P., Alvarez, J. G., Chen, H., and Evans, R. M. (1998) Oxidized LDL regulates macrophage gene expression through ligand activation of PPAR-. Cell 93, 229-240
45. Musiek, E. S., Milne, G. L., McLaughlin, B. A., and Morrow, J. D. (2005) Cyclopentenone eicosanoids as mediators of neurodegeneration: a pathogenic mechanism of oxidative stress-mediated and cyclooxygenase-mediated neurotoxicity. Brain Pathol. 15, 149-158
46. Kumagai, T., Matsukawa, N., Kaneko, Y., Kusumi, Y., Mitsumata, M., and Uchida, K. (2004) A lipid peroxidation-derived inflammatory mediator: identification of 4-hydroxy-2-nonenal as a potential inducer of cyclooxygenase-2 in macrophages. J. Biol. Chem. 279, 48389-48396
47. Kawamoto, Y., Nakamura, Y., Naito, Y., Torii, Y., Kumagai, T., Osawa, T., Ohigashi, H., Satoh, K., Imagawa, M., and Uchida, K. (2000) Cyclopentenone prostaglandins as potential inducers of phase ii detoxification enzymes: 15-deoxy-12,14-prostaglandin j2-induced expression of glutathione s-transferases. J. Biol. Chem. 275, 11291-11299
48. Devarajan, A., Bourquard, N., Hama, S., Navab, M., Grijalva, V. R., Morvardi, S., Clarke, C. F., Vergnes, L., Reue, K., Teiber, J. F., and Reddy, S. T. (2011) Paraoxonase 2 deficiency alters mitochondrial function and exacerbates the development of atherosclerosis. Antioxid. Redox Signal. 14, 341-351
49. Altenhöfer, S., Witte, I., Teiber, J. F., Wilgenbus, P., Pautz, A., Li, H., Daiber, A., Witan, H., Clement, A. M., Förstermann, U., and Horke, S. (2010) One enzyme, two functions: PON2 prevents mitochondrial superoxide formation and apoptosis independent from its lactonase activity. J. Biol. Chem. 285, 24398-24403
50. Mochizuki, H., Scherer, S. W., Xi, T., Nickle, D. C., Majer, M., Huizenga, J. J., Tsui, L. C., and Prochazka, M. (1998) Human PON2 gene at 7q21.3: cloning, multiple mRNA forms, and missense polymorphisms in the coding sequence. Gene 213, 149-157
51. Sorenson, R. C., Bisgaier, C. L., Aviram, M., Hsu, C., Billecke, S., and La Du, B. N. (1999) Human serum paraoxonase/arylesterase's retained hydrophobic N-terminal leader sequence associates with HDLs by binding phospholipids apolipoprotein A-I stabilizes activity. Arterioscler. Thromb. Vasc. Biol. 19, 2214-2225
52. Teiber, J. F., Draganov, D. I., and La Du, B. N. (2004) Purified human serum PON1 does not protect LDL against oxidation in the in vitro assays initiated with copper or AAPH. J. Lipid Res. 45, 2260-2268