Peroxiredoxin 6 in the repair of peroxidized cell membranes and cell signaling

Archives of Biochemistry and Biophysics

Volumn 617, Issue , 2017, Pages 68-83

  Fisher, Aron B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Anti oxidant defense; Lysophospholipid acyl transferase; NADPH oxidase; Phospholipase A2; Phospholipid hydroperoxide glutathione peroxidase; Phospholipid remodeling

Indexed keywords

ACYLTRANSFERASE; CYSTEINE; DIMER; GLUTATHIONE; HYDROPEROXIDE; LYSOPHOSPHATIDYLCHOLINE; MONOMER; PEROXIDASE; PEROXIREDOXIN 6; PHOSPHOLIPASE A2; 1 ACYLGLYCEROPHOSPHOCHOLINE ACYLTRANSFERASE; GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RECOMBINANT PROTEIN;

ANTIOXIDANT ACTIVITY; CATABOLISM; CELL COMMUNICATION; CELL MEMBRANE; CELL REGENERATION; CELLULAR DISTRIBUTION; DRUG TARGETING; ENDOTHELIUM CELL; ENZYME ACTIVITY; IN VITRO STUDY; LIPID PEROXIDATION; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PEROXIDIZED CELL MEMBRANE; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RECYCLING; REVIEW; STRUCTURE ACTIVITY RELATION; ANIMAL; CATALYSIS; CHEMISTRY; DIMERIZATION; HUMAN; HYDROLYSIS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

1-ACYLGLYCEROPHOSPHOCHOLINE O-ACYLTRANSFERASE; ANIMALS; CATALYSIS; CELL MEMBRANE; DIMERIZATION; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HUMANS; HYDROGEN PEROXIDE; HYDROLYSIS; MICE; MICE, TRANSGENIC; NADP; OXIDATIVE STRESS; PEROXIREDOXIN VI; PHOSPHOLIPASES A2; PHOSPHORYLATION; RATS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85009865173     PISSN: 00039861     EISSN: 10960384     Source Type: Journal    
DOI: 10.1016/j.abb.2016.12.003     Document Type: Review

References (163)

1. [1] Joly, J.S., Bourrat, F., Nguyen, V., Chourrout, D., Ol-Prx 3, a member of an additional class of homeobox genes, is unimodally expressed in several domains of the developing and adult central nervous system of the medaka (Oryzias latipes). Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 12987–12992.
2. [2] Shichi, H., Demar, J.C., Non-selenium glutathione peroxidase without glutathione S-transferase activity from bovine ciliary body. Experim Eye Res. 50 (1990), 513–520.
3. [3] Peshenko, I.V., Novoselov, V.I., Evdokimov, V.A., Nikolaev Yu, V., Shuvaeva, T.M., Lipkin, V.M., Fesenko, E.E., Novel 28-kDa secretory protein from rat olfactory epithelium. FEBS Lett. 381 (1996), 12–14.
4. [4] Akiba, S., Dodia, C., Chen, X., Fisher, A.B., Characterization of acidic Ca(2+)-independent phospholipase A2 of bovine lung. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 120 (1998), 393–404.
5. [5] Peshenko, I.V., Novoselov, V.I., Evdokimov, V.A., Nikolaev, Y.V., Kamzalov, S.S., Shuvaeva, T.M., Lipkin, V.M., Fesenko, E.E., Identification of a 28 kDa secretory protein from rat olfactory epithelium as a thiol-specific antioxidant. Free Radic. Biol. Med. 25 (1998), 654–659.
6. [6] Kim, T.S., Dodia, C., Chen, X., Hennigan, B.B., Jain, M., Feinstein, S.I., Fisher, A.B., Cloning and expression of rat lung acidic Ca(2+)-independent PLA2 and its organ distribution. Am. J. Physiol. Lung Cell Mol. Physiol. 274 (1998), L750–L761.
7. [7] Chae, H.Z., Robison, K., Poole, L.B., Church, G., Storz, G., Rhee, S.G., Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 7017–7021.
8. 2 and properties of the expressed protein. J. Biol. Chem. 272 (1997), 2542–2550.
9. [9] Nagase, T., Miyajima, N., Tanaka, A., Sazuka, T., Seki, N., Sato, S., Tabata, S., Ishikawa, K., Kawarabayasi, Y., Kotani, H., Nomura, N., Prediction of the coding sequences of unidentified human genes. III. The coding sequences of 40 new genes (KIAA0081-KIAA0120) deduced by analysis of cDNA clones from human cell line KG-1 (supplement). DNA Res. 2 (1995), 51–59.
10. [10] Phelan, S.A., Johnson, K.A., Beier, D.R., Paigen, B., Characterization of the murine gene encoding Aop2 (antioxidant protein 2) and identification of two highly related genes. Genomics 54 (1998), 132–139.
11. [11] Lee, T.H., Yu, S.L., Kim, S.U., Kim, Y.M., Choi, I., Kang, S.W., Rhee, S.G., Yu, D.Y., Characterization of the murine gene encoding 1-Cys peroxiredoxin and identification of highly homologous genes. Gene 234 (1999), 337–344.
12. [12] Rhee, S.G., Chae, H.Z., Kim, K., Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38 (2005), 1543–1552.
13. [13] Fisher, A.B., Dodia, C., Manevich, Y., Chen, J.W., Feinstein, S.I., Phospholipid hydroperoxides are substrates for non-selenium glutathione peroxidase. J. Biol. Chem. 274 (1999), 21326–21334.
14. [14] Frank, S., Munz, B., Werner, S., The human homologue of a bovine non-selenium glutathione peroxidase is a novel keratinocyte growth factor-regulated gene. Oncogene 14 (1997), 915–921.
15. [15] Phelan, S.A., AOP2 (antioxidant protein 2): structure and function of a unique thiol-specific antioxidant. Antioxid. Redox Signal 1 (1999), 571–584.
16. [16] Power, J.H., Nicholas, T.E., Immunohistochemical localization and characterization of a rat Clara cell 26-kDa protein (CC26) with similarities to glutathione peroxidase and phospholipase A2. Exp. Lung Res. 25 (1999), 379–392.
17. [17] Leavey, P.J., Gonzalez-Aller, C., Thurman, G., Kleinberg, M., Rinckel, L., Ambruso, D.W., Freeman, S., Kuypers, F.A., Ambruso, D.R., A 29-kDa protein associated with p67phox expresses both peroxiredoxin and phospholipase A2 activity and enhances superoxide anion production by a cell-free system of NADPH oxidase activity. J. Biol. Chem. 277 (2002), 45181–45187.
18. [18] Iakoubova, O.A., Pacella, L.A., Her, H., Beier, D.R., LTW4 protein on mouse chromosome 1 is a member of a family of antioxidant proteins. Genomics 42 (1997), 474–478.
19. 2 activities. Biochimie, 92, 2010, 638 634.
20. [20] Nelson, K.J., Knutson, S.T., Soito, L., Klomsiri, C., Poole, L.B., Fetrow, J.S., Analysis of the peroxiredoxin family: using active-site structure and sequence information for global classification and residue analysis. Proteins 79 (2011), 947–964.
21. [21] Tolomeo, A.M., Carraro, A., Bakiu, R., Toppo, S., Place, S.P., Ferro, D., Santovito, G., Peroxiredoxin 6 from the Antarctic emerald rockcod: molecular characterization of its response to warming. J. Comp. Physiol. B 186 (2015), 59–71.
22. [22] Rhee, S.G., Kang, S.W., Chang, T.S., Jeong, W., Kim, K., Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52 (2001), 35–41.
23. [23] Barranco-Medina, S., Lazaro, J.J., Dietz, K.J., The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett., 2009, 1809–1816.
24. [24] Mizohata, E., Sakai, H., Fusatomi, E., Terada, T., Murayama, K., Shirouzu, M., Yokoyama, S., Crystal structure of an archaeal peroxiredoxin from the aerobic hyperthermophilic crenarchaeon Aeropyrum pernix K1. J. Mol. Biol. 354 (2005), 317–329.
25. [25] Perkins, A., Nelson, K.J., Parsonage, D., Poole, L.B., Karplus, P.A., Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends biochem. Sci. 40 (2015), 435–445.
26. [26] Manevich, Y., Fisher, A.B., Peroxiredoxin 6, a 1-Cys peroxiredoxin, functions in antioxidant defense and lung phospholipid metabolism. Free Radic. Biol. Med. 38 (2005), 1422–1432.
27. [27] Schremmer, B., Manevich, Y., Feinstein, S.I., Fisher, A.B., Peroxiredoxins in the lung with emphasis on peroxiredoxin VI. Subcell. Biochem. 44 (2007), 317–344.
28. 2 activities. Antiox Redox Signal 15 (2011), 831–844.
29. [29] Peshenko, I.V., Shichi, H., Oxidation of active center cysteine of bovine 1-Cys peroxiredoxin to the cysteine sulfenic acid form by peroxide and peroxynitrite. Free Radic. Biol. Med. 31 (2001), 292–303.
30. [30] Chen, J.W., Dodia, C., Feinstein, S.I., Jain, M.K., Fisher, A.B., 1-Cys peroxiredoxin, a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. J. Biol. Chem. 275 (2000), 28421–28427.
31. [31] Hall, A., Nelson, K., Poole, L.B., Karplus, P.A., Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox Signal 15 (2011), 795–815.
32. [32] Kang, S.W., Baines, I.C., Rhee, S.G., Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. J. Biol. Chem. 273 (1998), 6303–6311.
33. [33] Manevich, Y., Shuvaeva, T., Dodia, C., Kazi, A., Feinstein, S.I., Fisher, A.B., Binding of peroxiredoxin 6 to substrate determines differential phospholipid hydroperoxide peroxidase and phospholipase A(2) activities. Arch. Biochem. Biophys. 485 (2009), 139–149.
34. [34] Toledo, J.C. Jr., Audi, R., Ogusucu, R., Monteiro, G., Netto, L.E., Augusto, O., Horseradish peroxidase compound I as a tool to investigate reactive protein-cysteine residues: from quantification to kinetics. Free Radic. Biol. Med. 50 (2011), 1032–1038.
35. 2 activity. Free Radic. Biol. Med. 94 (2016), 145–156.
36. [36] Manevich, Y., Feinstein, S.I., Fisher, A.B., Activation of the antioxidant enzyme 1-Cys peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 3780–3785.
37. [37] Ralat, L.A., Manevich, Y., Fisher, A.B., Colman, R.F., Direct evidence for the formation of a complex between 1-cysteine peroxiredoxin and glutathione S-transferase pi with activity changes in both enzymes. Biochemistry 45 (2006), 360–372.
38. [38] Chae, H.Z., Oubrahim, H., Park, J.W., Rhee, S.G., Chock, P.B., Protein glutathionylation in the regulation of peroxiredoxins: a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators. Antioxid. Redox Signal 16 (2012), 506–523.
39. [39] Peshenko, I.V., Singh, A.K., Shichi, H., Bovine eye 1-Cys peroxiredoxin: expression in E. coli and antioxidant properties. J. Ocul. Pharmacol. Ther. 17 (2001), 93–99.
40. [40] Ralat, L.A., Misquitta, S.A., Manevich, Y., Fisher, A.B., Colman, R.F., Characterization of the complex of glutathione S-transferase pi and 1-cysteine peroxiredoxin. Arch. Biochem. Biophys. 474 (2008), 109–118.
41. [41] Manevich, Y., Hutchens, S., Tew, K.D., Townsend, D.M., Allelic variants of glutathione S-transferase P1-1 differentially mediate the peroxidase function of peroxiredoxin VI and alter membrane lipid peroxidation. Free Radic. Biol. Med. 54 (2013), 62–70.
42. [42] Zhou, S., Lien, Y.C., Shuvaeva, T., DeBolt, K., Feinstein, S.I., Fisher, A.B., Functional interaction of glutathione S-transferase pi and peroxiredoxin 6 in intact cells. Intern. J. Biochem. Cell Biol. 45 (2013), 401–407.
43. [43] Choi, H.J., Kang, S.W., Yang, C.H., Rhee, S.G., Ryu, S.E., Crystal structure of a novel human peroxidase enzyme at 2.0 A resolution. Nat. Struct. Biol. 5 (1998), 400–406.
44. [44] Kim, K.H., Lee, W., Kim, E.E., Crystal structures of human peroxiredoxin 6 in different oxidation states. Biochem. Biophys. Res. Commun. 477 (2016), 717–722.
45. [45] Rivera-Santiago, R.F., Harper, S.L., Zhou, S., Sriswasdi, S., Feinstein, S.I., Fisher, A.B., Speicher, D.W., Solution structure of the reduced form of human peroxiredoxin-6 elucidated using zero-length chemical cross-linking and homology modelling. Biochem. J. 468 (2015), 87–98.
46. [46] Poole, L.B., Nelson, K.J., Distribution and features of the six classes of peroxiredoxins. Mol. Cells 39 (2016), 53–59.
47. [47] Board, P.G., Menon, D., Glutathione transferases, regulators of cellular metabolism and physiology. Biochim. Biophys. Acta 1830 (2013), 3267–3288.
48. [48] da Fonseca, R.R., Johnson, W.E., O'Brien, S.J., Vasconcelos, V., Antunes, A., Molecular evolution and the role of oxidative stress in the expansion and functional diversification of cytosolic glutathione transferases. BMC Evol. Biol., 10, 2010, 281.
49. [49] Terrier, P., Townsend, A.J., Coindre, J.M., Triche, T.J., Cowan, K.H., An immunohistochemical study of pi class glutathione S-transferase expression in normal human tissue. Am. J. Pathol. 137 (1990), 845–853.
50. [50] Gallagher, B.M., Phelan, S.A., Investigating transcriptional regulation of Prdx6 in mouse liver cells. Free Radic. Biol. Med. 42 (2007), 1270–1277.
51. [51] Monteiro, G., Horta, B.B., Pimenta, D.C., Augusto, O., Netto, L.E., Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 4886–4891.
52. [52] Greetham, D., Grant, C.M., Antioxidant activity of the yeast mitochondrial one-Cys peroxiredoxin is dependent on thioredoxin reductase and glutathione in vivo. Mol. Cell. Biol. 29 (2009), 3229–3240.
53. [53] Pedrajas, J.R., Padilla, C.A., McDonagh, B., Barcena, J.A., Glutaredoxin participates in the reduction of peroxides by the mitochondrial 1-CYS peroxiredoxin in Saccharomyces cerevisiae. Antioxid. Redox Signal 13 (2010), 249–258.
54. [54] Dietz, K.J., Peroxiredoxins in plants and cyanobacteria. Antioxid. Redox Signal 15 (2011), 1129–1159.
55. [55] Lee, S.P., Hwang, Y.S., Kim, Y.J., Kwon, K.S., Kim, H.J., Kim, K., Chae, H.Z., Cyclophilin A binds to peroxiredoxins and activates its peroxidase activity. J. Biol. Chem. 276 (2001), 29826–29832.
56. [56] Fukuhara, R., Kageyama, T., Structure, gene expression, and evolution of primate glutathione peroxidases. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 141 (2005), 428–436.
57. [57] Maiorino, M., Gregolin, C., Ursini, F., Phospholipid hydroperoxide glutathione peroxidase. Meth Enzymol. 186 (1990), 448–457.
58. [58] Han, X., Fan, Z., Yu, Y., Liu, S., Hao, Y., Huo, R., Wei, J., Expression and characterization of recombinant human phospholipid hydroperoxide glutathione peroxidase. IUBMB Life 65 (2013), 951–956.
59. [59] Kernstock, R.M., Girotti, A.W., New strategies for the isolation and activity determination of naturally occurring type-4 glutathione peroxidase. Prot. Expr. Purif. 62 (2008), 216–222.
60. [60] Weitzel, F., Ursini, F., Wendel, A., Phospholipid hydroperoxide glutathione peroxidase in various mouse organs during selenium deficiency and repletion. Biochim. Biophys. Acta 1036 (1990), 88–94.
61. [61] Brigelius-Flohe, R., Tissue-specific functions of individual glutathione peroxidases. Free Radic. Biol. Med. 27 (1999), 951–965.
62. [62] Baek, I.J., Seo, D.S., Yon, J.M., Lee, S.R., Jin, Y., Nahm, S.S., Jeong, J.H., Choo, Y.K., Kang, J.K., Lee, B.J., Yun, Y.W., Nam, S.Y., Tissue expression and cellular localization of phospholipid hydroperoxide glutathione peroxidase (PHGPx) mRNA in male mice. J. Mol. Histol. 38 (2007), 237–244.
63. [63] Brutsch, S.H., Wang, C.C., Li, L., Stender, H., Neziroglu, N., Richter, C., Kuhn, H., Borchert, A., Expression of inactive glutathione peroxidase 4 leads to embryonic lethality, and inactivation of the Alox15 gene does not rescue such knock-in mice. Antioxid. Redox Signal 22 (2015), 281–293.
64. [64] Liu, G., Feinstein, S.I., Wang, Y., Dodia, C., Fisher, D., Yu, K., Ho, Y.S., Fisher, A.B., Comparison of glutathione peroxidase 1 and peroxiredoxin 6 in protection against oxidative stress in the mouse lung. Free Radic. Biol. Med. 49 (2010), 1172–1181.
65. [65] Woo, H.A., Jeong, W., Chang, T.S., Park, K.J., Park, S.J., Yang, J.S., Rhee, S.G., Reduction of cysteine sulfinic acid by sulfiredoxin is specific to 2-cys peroxiredoxins. J. Biol. Chem. 280 (2005), 3125–3128.
66. [66] Claiborne, A., Mallett, T.C., Yeh, J.I., Luba, J., Parsonage, D., Structural, redox, and mechanistic parameters for cysteine-sulfenic acid function in catalysis and regulation. Adv. Prot. Chem. 58 (2001), 215–276.
67. [67] Lindgren, J., Eriksson Karlstrom, A., Intramolecular thioether crosslinking of therapeutic proteins to increase proteolytic stability. Chembiochem 15 (2014), 2132–2138.
68. [68] Sorokina, E.M., Dodia, C., Zhou, S., Tao, J.Q., Gao, L., Raabe, T., Feinstein, S.I., Fisher, A.B., Mutation of serine 32 to threonine in peroxiredoxin 6 preserves its structure and enzymatic function but abolishes its trafficking to lamellar bodies. J. Biol. Chem. 291 (2016), 9268–9280.
69. [69] Wu, Y., Feinstein, S.I., Manevich, Y., Chowdhury, I., Pak, J.H., Kazi, A., Dodia, C., Speicher, D.W., Fisher, A.B., Mitogen-activated protein kinase-mediated phosphorylation of peroxiredoxin 6 regulates its phospholipase A(2) activity. Biochem. J. 419 (2009), 669–679.
70. [70] Wu, Y.Z., Manevich, Y., Baldwin, J.L., Dodia, C., Yu, K., Feinstein, S.I., Fisher, A.B., Interaction of surfactant protein A with peroxiredoxin 6 regulates phospholipase A2 activity. J. Biol. Chem. 281 (2006), 7515–7525.
71. [71] Kramer, R.M., Johansen, B., Hession, C., Pepinsky, R.B., Structure and properties of a secretable phospholipase A2 from human platelets. Adv. Exp. Med. Biol. 275 (1990), 35–53.
72. [72] Ackermann, E.J., Kempner, E.S., Dennis, E.A., Ca(2+)-independent cytosolic phospholipase A2 from macrophage-like P388D1 cells. Isolation and characterization. J. Biol. Chem. 269 (1994), 9227–9233.
73. 2 enzymes in degradation of dipalmitoylphosphatidylcholine by granular pneumocytes. J. Lipid Res. 37 (1996), 1057–1064.
74. [74] Fisher, A.B., Dodia, C., Feinstein, S.I., Ho, Y.S., Altered lung phospholipid metabolism in mice with targeted deletion of lysosomal-type phospholipase A2. J. Lipid Res. 46 (2005), 1248–1256.
75. [75] Fisher, A.B., Dodia, C., Role of acidic Ca2+-independent phospholipase A2 in synthesis of lung dipalmitoyl phosphatidylcholine. Am. J. Physiol. Lung Cell Mol. Physiol. 272 (1997), L238–L243.
76. 2 and turnover of alveolar DPPC. Am. J. Physiol. Lung Cell Mol. Physiol. 280 (2001), L748–L754.
77. [77] Hiraoka, M., Abe, A., Shayman, J.A., Cloning and characterization of a lysosomal phospholipase A2, 1-O-acylceramide synthase. J. Biol. Chem. 277 (2002), 10090–10099.
78. [78] Manevich, Y., Reddy, K.S., Shuvaeva, T., Feinstein, S.I., Fisher, A.B., Structure and phospholipase function of peroxiredoxin 6: identification of the catalytic triad and its role in phospholipid substrate binding. J. Lipid Res. 48 (2007), 2306–2318.
79. [79] Fisher, A.B., Dodia, C., Chander, A., Jain, M., A competitive inhibitor of phospholipase A2 decreases surfactant phosphatidylcholine degradation by the rat lung. Biochem. J. 288:Pt 2 (1992), 407–411.
80. [80] Jain, M.K., Yu, B.Z., Rogers, J., Ranadive, G.N., Berg, O.G., Interfacial catalysis by phospholipase A2: dissociation constants for calcium, substrate, products, and competitive inhibitors. Biochemistry 30 (1991), 7306–7317.
81. [81] Fisher, A.B., Jain, M., Phospholipases: degradation of phospholipids in membranes and emulsions. Encyclopedia of Life Sciences, 2009, John Wiley & Sons, Chichester.
82. [82] Stryer, L., Berg, J. M., and Tymoczko, J. (2002). in Biochemistry, 5th Ed., W H Freeman, San Francisco, USA. Chapt. 9.1.
83. [83] Chatterjee, S., Feinstein, S.I., Dodia, C., Sorokina, E., Lien, Y.C., Nguyen, S., Debolt, K., Speicher, D., Fisher, A.B., Peroxiredoxin 6 phosphorylation and subsequent phospholipase A2 activity are required for agonist-mediated activation of NADPH oxidase in mouse pulmonary microvascular endothelium and alveolar macrophages. J. Biol. Chem. 286 (2011), 11696–11706.
84. [84] Fisher, A.B., Dodia, C., Sorokina, E.M., Li, H., Zhou, S., Raabe, T., Feinstein, S.I., A novel lysoPhosphatidylcholine acyl transferase activity is expressed by peroxiredoxin 6. J. Lipid Res. 57 (2016), 587–596.
85. [85] Shindou, H., Hishikawa, D., Harayama, T., Yuki, K., Shimizu, T., Recent progress on acyl CoA: lysophospholipid acyltransferase research. Suppl J. Lipid Res. 50 (2009), S46–S51.
86. [86] Chen, X., Hyatt, B.A., Mucenski, M.L., Mason, R.J., Shannon, J.M., Identification and characterization of a lysophosphatidylcholine acyltransferase in alveolar type II cells. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 11724–11729.
87. [87] Soupene, E., Fyrst, H., Kuypers, F.A., Mammalian acyl-CoA:lysophosphatidylcholine acyltransferase enzymes. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 88–93.
88. [88] Rahaman, H., Zhou, S., Dodia, C., Feinstein, S.I., Huang, S., Speicher, D., Fisher, A.B., Increased phospholipase A2 activity with phosphorylation of peroxiredoxin 6 requires a conformational change in the protein. Biochemistry 51 (2012), 5521–5530.
89. [89] Bemporad, F., Gsponer, J., Hopearuoho, H.I., Plakoutsi, G., Stati, G., Stefani, M., Taddei, N., Vendruscolo, M., Chiti, F., Biological function in a non-native partially folded state of a protein. EMBO J. 27 (2008), 1525–1535.
90. [90] Pervushin, K., Vamvaca, K., Vogeli, B., Hilvert, D., Structure and dynamics of a molten globular enzyme. Nat. Struct. Mol. Biol. 14 (2007), 1202–1206.
91. [91] Uversky, V.N., Kutyshenko, V.P., Protasova, N., Rogov, V.V., Vassilenko, K.S., Gudkov, A.T., Circularly permuted dihydrofolate reductase possesses all the properties of the molten globule state, but can resume functional tertiary structure by interaction with its ligands. Prot. Sci. 5 (1996), 1844–1851.
92. [92] Arpigny, J.L., Jaeger, K.E., Bacterial lipolytic enzymes: classification and properties. Biochem. J. 343:Pt 1 (1999), 177–183.
93. [93] Derewenda, Z.S., Sharp, A.M., News from the interface: the molecular structures of triacylglyceride lipases. Trends Biochem. Sci. 18 (1993), 20–25.
94. [94] Fujii, T., Fujii, J., Taniguchi, N., Augmented expression of peroxiredoxin VI in rat lung and kidney after birth implies an antioxidative role. Eur. J. Biochem. 268 (2001), 218–225.
95. [95] Sorokina, E.M., Feinstein, S.I., Zhou, S., Fisher, A.B., Intracellular targeting of peroxiredoxin 6 to lysosomal organelles requires MAPK activity and binding to 14-3-3epsilon. Am. J. Physiol. Lung Cell Mol. Physiol. 300 (2011), C1430–C1441.
96. [96] Sorokina, E.M., Feinstein, S.I., Milovanova, T.N., Fisher, A.B., Identification of the amino acid sequence that targets peroxiredoxin 6 to lysosome-like structures of lung epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 297 (2009), L871–L880.
97. [97] Fisher, A.B., Dodia, C., Chander, A., Inhibition of lung calcium-independent phospholipase A2 by surfactant protein A. Am. J. Physiol. Lung Cell Mol. Physiol. 267 (1994), L335–L341.
98. [98] Chander, A., Johnson, R.G., Reicherter, J., Fisher, A.B., Lung lamellar bodies maintain an acidic internal pH. J. Biol. Chem. 261 (1986), 6126–6131.
99. [99] Fisher, A.B., Chander, A., Intracellular processing of surfactant lipids in the lung. Ann. Rev. Physiol. 47 (1985), 789–802.
100. [100] Weaver, T.E., Na, C.L., Stahlman, M., Biogenesis of lamellar bodies, lysosome-related organelles involved in storage and secretion of pulmonary surfactant. Semin. Cell Dev. Biol. 13 (2002), 263–270.
101. [101] Fisher, A. B. (1998) Surfactant catabolism and recycling. in Lung Surfactant: Clearance and Cellular Processing, Chapter 8 (Rooney, S. A. ed.), Landes Bioscience, Austin, TX. 165-189.
102. [102] Kim, H.S., Pak, J.H., Gonzales, L.W., Feinstein, S.I., Fisher, A.B., Regulation of 1-cys peroxiredoxin expression in lung epithelial cells. Am. J. Respir. Cell Mol. Biol. 27 (2002), 227–233.
103. [103] Kim, H.S., Manevich, Y., Feinstein, S.I., Pak, J.H., Ho, Y.S., Fisher, A.B., Induction of 1-cys peroxiredoxin expression by oxidative stress in lung epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 285 (2003), L363–L369.
104. [104] Chowdhury, I., Mo, Y., Gao, L., Kazi, A., Fisher, A.B., Feinstein, S.I., Oxidant stress stimulates expression of the human peroxiredoxin 6 gene by a transcriptional mechanism involving an antioxidant response element. Free Radic. Biol. Med. 46 (2009), 146–153.
105. [105] Sparling, N.E., Phelan, S.A., Identification of multiple transcripts for antioxidant protein 2 (Aop2): differential regulation by oxidative stress and growth factors. Redox Rep. 8 (2003), 87–94.
106. [106] Chowdhury, I., Fisher, A.B., Christofidou-Solomidou, M., Gao, L., Tao, J.Q., Sorokina, E.M., Lien, Y.C., Bates, S.R., Feinstein, S.I., Keratinocyte growth factor and glucocorticoid induction of human peroxiredoxin 6 gene expression occur by independent mechanisms that are synergistic. Antioxid. Redox Signal 20 (2014), 391–402.
107. [107] Wu, X., Ji, P., Zhang, L., Bu, G., Gu, H., Wang, X., Xiong, Y., Zuo, B., The expression of porcine Prdx6 gene is up-regulated by C/EBPbeta and CREB. PLoS One, 10, 2015, e0144851.
108. [108] Krishnaiah, S.Y., Dodia, C., Sorokina, E.M., Li, H., Feinstein, S.I., Fisher, A.B., Binding sites for interaction of peroxiredoxin 6 with surfactant protein A. Biochim. Biophys. Acta 1864 (2016), 419–425.
109. [109] Jain, D., Dodia, C., Bates, S.R., Hawgood, S., Poulain, F.R., Fisher, A.B., SP-A is necessary for increased clearance of alveolar DPPC with hyperventilation or secretagogues. Am. J. Physiol. Lung Cell Mol. Physiol. 284 (2003), L759–L765.
110. [110] Krishnaiah, S.Y., Dodia, C., Feinstein, S.I., Fisher, A.B., p67phox terminates the phospholipase A2-derived signal for activation of NADPH oxidase (NOX2). FASEB J. 27 (2013), 2066–2073.
111. [111] Mo, Y., Feinstein, S.I., Manevich, Y., Zhang, Q., Lu, L., Ho, Y.S., Fisher, A.B., 1-Cys peroxiredoxin knock-out mice express mRNA but not protein for a highly related intronless gene. FEBS Lett. 555 (2003), 192–198.
112. [112] Wang, X., Phelan, S.A., Forsman-Semb, K., Taylor, E.F., Petros, C., Brown, A., Lerner, C.P., Paigen, B., Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J. Biol. Chem. 278 (2003), 25179–25190.
113. [113] Dierick, J.F., Wenders, F., Chainiaux, F., Remacle, J., Fisher, A.B., Toussaint, O., Retrovirally mediated overexpression of peroxiredoxin VI increases the survival of WI-38 human diploid fibroblasts exposed to cytotoxic doses of tert-butylhydroperoxide and UVB. Biogerontology 4 (2003), 125–131.
114. [114] Manevich, Y., Sweitzer, T., Pak, J.H., Feinstein, S.I., Muzykantov, V., Fisher, A.B., 1-Cys peroxiredoxin overexpression protects cells against phospholipid peroxidation-mediated membrane damage. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 11599–11604.
115. [115] Singh, S.P., Chhunchha, B., Fatma, N., Kubo, E., Singh, S.P., Singh, D.P., Delivery of a protein transduction domain-mediated Prdx6 protein ameliorates oxidative stress-induced injury in human and mouse neuronal cells. Am. J. Physiol. Cell Physiol. 310 (2016), C1–C16.
116. [116] Walsh, B., Pearl, A., Suchy, S., Tartaglio, J., Visco, K., Phelan, S.A., Overexpression of Prdx6 and resistance to peroxide-induced death in Hepa1-6 cells: Prdx suppression increases apoptosis. Redox Rep. 14 (2009), 275–284.
117. [117] Wang, Y., Manevich, Y., Feinstein, S.I., Fisher, A.B., Adenovirus-mediated transfer of the 1-cys peroxiredoxin gene to mouse lung protects against hyperoxic injury. Am. J. Physiol. Lung Cell Mol. Physiol. 286 (2004), L1188–L1193.
118. [118] Wang, Y., Phelan, S.A., Manevich, Y., Feinstein, S.I., Fisher, A.B., Transgenic mice overexpressing peroxiredoxin 6 show increased resistance to lung injury in hyperoxia. Am. J. Respir. Cell Mol. Biol. 34 (2006), 481–486.
119. [119] Wang, Y., Feinstein, S.I., Manevich, Y., Ho, Y.S., Fisher, A.B., Lung injury and mortality with hyperoxia are increased in peroxiredoxin 6 gene-targeted mice. Free Radic. Biol. Med. 37 (2004), 1736–1743.
120. [120] Wang, Y., Feinstein, S.I., Manevich, Y., Ho, Y.S., Fisher, A.B., Peroxiredoxin 6 gene-targeted mice show increased lung injury with paraquat-induced oxidative stress. Antioxid. Redox Signal 8 (2006), 229–237.
121. [121] Lien, Y.C., Feinstein, S.I., Dodia, C., Fisher, A.B., The roles of peroxidase and phospholipase A2 activities of peroxiredoxin 6 in protecting pulmonary microvascular endothelial cells against peroxidative stress. Antioxid. Redox Signal 16 (2012), 440–451.
122. 2-induced oxidative stress. J. Cell. Biochem. 104 (2008), 1274–1285.
123. [123] Ozkosem, B., Feinstein, S.I., Fisher, A.B., O'Flaherty, C., Absence of peroxiredoxin 6 amplifies the effect of oxidant stress on mobility and SCSA/CMA3 defined chromatin quality and impairs fertilizing ability of mouse spermatozoa. Biol. Reprod., 94, 2016, 68.
124. [124] Ozkosem, B., Feinstein, S.I., Fisher, A.B., O'Flaherty, C., Advancing age increases sperm chromatin damage and impairs fertility in peroxiredoxin 6 null mice. Redox Biol. 5 (2015), 15–23.
125. [125] Pak, J.H., Manevich, Y., Kim, H.S., Feinstein, S.I., Fisher, A.B., An antisense oligonucleotide to 1-cys peroxiredoxin causes lipid peroxidation and apoptosis in lung epithelial cells. J. Biol. Chem. 277 (2002), 49927–49934.
126. [126] Ayala, A., Munoz, M.F., Arguelles, S., Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell. Longev., 2014, 2014, 360438.
127. [127] Cao, J.Y., Dixon, S.J., Mechanisms of ferroptosis. Cell. Mol. Life Sci. 73 (2016), 2195–2209.
128. [128] Ursini, F., Maiorino, M., Gregolin, C., The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim. Biophys. Acta 839 (1985), 62–70.
129. [129] Sevanian, A., Muakkassah-Kelly, S.F., Montestruque, S., The influence of phospholipase A2 and glutathione peroxidase on the elimination of membrane lipid peroxides. Arch. Biochem. Biophys. 223 (1983), 441–452.
130. [130] Yang, W.S., Stockwell, B.R., Ferroptosis: death by lipid peroxidation. Trends Cell Biol. 26 (2016), 165–176.
131. [131] Moessinger, C., Klizaite, K., Steinhagen, A., Philippou-Massier, J., Shevchenko, A., Hoch, M., Ejsing, C.S., Thiele, C., Two different pathways of phosphatidylcholine synthesis, the Kennedy Pathway and the Lands Cycle, differentially regulate cellular triacylglycerol storage. BMC Cell Biol., 15, 2014, 43.
132. [132] Li, H., Benipal, B., Zhou, S., Dodia, C., Chatterjee, S., Tao, J.Q., Sorokina, E.M., Raabe, T., Feinstein, S.I., Fisher, A.B., Critical role of peroxiredoxin 6 in the repair of peroxidized cell membranes following oxidative stress. Free Radic. Biol. Med. 87 (2015), 356–365.
133. [133] Eismann, T., Huber, N., Shin, T., Kuboki, S., Galloway, E., Wyder, M., Edwards, M.J., Greis, K.D., Shertzer, H.G., Fisher, A.B., Lentsch, A.B., Peroxiredoxin-6 protects against mitochondrial dysfunction and liver injury during ischemia-reperfusion in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 296 (2009), G266–G274.
134. [134] Gong, S., San Gabriel, M.C., Zini, A., Chan, P., O'Flaherty, C., Low amounts and high thiol oxidation of peroxiredoxins in spermatozoa from infertile men. J. Androl. 33 (2012), 1342–1351.
135. [135] Goss, V., Hunt, A.N., Postle, A.D., Regulation of lung surfactant phospholipid synthesis and metabolism. Biochim. Biophys. Acta 1831 (2013), 448–458.
136. [136] Chander, A., Reicherter, J., Fisher, A.B., Degradation of dipalmitoyl phosphatidylcholine by isolated rat granular pneumocytes and reutilization for surfactant synthesis. J. Clin. Invest. 79 (1987), 1133–1138.
137. [137] Fisher, A.B., Dodia, C., Yu, K., Manevich, Y., Feinstein, S.I., Lung phospholipid metabolism in transgenic mice overexpressing peroxiredoxin 6. Biochim. Biophys. Acta 1761 (2006), 785–792.
138. [138] Kook, S., Wang, P., Young, L.R., Schwake, M., Saftig, P., Weng, X., Meng, Y., Neculai, D., Marks, M.S., Gonzales, L., Beers, M.F., Guttentag, S., Impaired lysosomal integral membrane protein 2-dependent peroxiredoxin 6 delivery to lamellar bodies accounts for altered alveolar phospholipid content in adaptor protein-3-deficient pearl mice. J. Biol. Chem. 291 (2016), 8414–8427.
139. [139] Bromberg, Y., Pick, E., Activation of NADPH-dependent superoxide production in a cell-free system by sodium dodecyl sulfate. J. Biol. Chem. 260 (1985), 13539–13545.
140. [140] Lowenthal, A., Levy, R., Essential requirement of cytosolic phospholipase A(2) for activation of the H(+) channel in phagocyte-like cells. J. Biol. Chem. 274 (1999), 21603–21608.
141. [141] Rubin, B.B., Downey, G.P., Koh, A., Degousee, N., Ghomashchi, F., Nallan, L., Stefanski, E., Harkin, D.W., Sun, C., Smart, B.P., Lindsay, T.F., Cherepanov, V., Vachon, E., Kelvin, D., Sadilek, M., Brown, G.E., Yaffe, M.B., Plumb, J., Grinstein, S., Glogauer, M., Gelb, M.H., Cytosolic phospholipase A2-alpha is necessary for platelet-activating factor biosynthesis, efficient neutrophil-mediated bacterial killing, and the innate immune response to pulmonary infection: cPLA2-alpha does not regulate neutrophil NADPH oxidase activity. J. Biol. Chem. 280 (2005), 7519–7529.
142. [142] Matonao, R., Miyano, K., Kiyohara, T., Sumimoto, H., Arachidonic acid induces direct interaction of the p67(phox)-Rac complex with the phagocyte oxidase Nox2, leading to superoxide production. J. Biol. Chem. 289 (2014), 24874–24884.
143. [143] Ellison, M.A., Thurman, G.W., Ambruso, D.R., Phox activity of differentiated PLB-985 cells is enhanced, in an agonist specific manner, by the PLA2 activity of Prdx6-PLA2. Eur. J. Immunol. 42 (2012), 1609–1617.
144. [144] Lee, I., Dodia, C., Chatterjee, S., Zagorski, J., Mesaros, C., Blair, I.A., Feinstein, S.I., Jain, M., Fisher, A.B., A novel nontoxic inhibitor of the activation of NADPH oxidase reduces reactive oxygen species production in mouse lung. J. Pharmacol. Exp. Ther. 345 (2013), 284–296.
145. [145] Lee, I., Dodia, C., Chatterjee, S., Feinstein, S.I., Fisher, A.B., Protection against LPS-induced acute lung injury by a mechanism based inhibitor of NADPH-oxidase (Type 2). Am. J. Physiol. Lung Cell Mol. Physiol. 306 (2014), 635–644.
146. 2 activity of peroxiredoxin 6 modulates NADPH oxidase 2 activation via lysophosphatidic acid receptor signaling in the pulmonary endothelium and alveolar macrophages. FASEB J. 30 (2016), 2885–2898.
147. [147] Bedard, K., Krause, K.H., The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87 (2007), 245–313.
148. [148] Kwon, J., Wang, A., Burke, D.J., Boudreau, H.E., Lekstrom, K.J., Korzeniowska, A., Sugamata, R., Kim, Y.S., Yi, L., Ersoy, I., Jaeger, S., Palaniappan, K., Ambruso, D.R., Jackson, S.H., Leto, T.L., Peroxiredoxin 6 (Prdx6) supports NADPH oxidase1 (Nox1)-based superoxide generation and cell migration. Free Radic. Biol. Med. 96 (2016), 99–115.
149. [149] Chatterjee, S., Fisher, A.B., Mechanotransduction in the endothelium: role of membrane proteins and reactive oxygen species in sensing, transduction, and transmission of the signal with altered blood flow. Antioxid. Redox Signal 20 (2014), 899–913.
150. [150] Browning, E.A., Chatterjee, S., Fisher, A.B., Stop the flow: a paradigm for cell signaling mediated by reactive oxygen species in the pulmonary endothelium. Annu. Rev. Physiol. 74 (2012), 403–424.
151. [151] Chatterjee, S., Fujiwara, K., Perez, N.G., Ushio-Fukai, M., Fisher, A.B., Mechanosignaling in the vasculature: emerging concepts in sensing, transduction and physiological responses. Am. J. Physiol. Heart Circ. Physiol. 308 (2015), H1451–H1462.
152. [152] Milovanova, T., Chatterjee, S., Hawkins, B.J., Hong, N., Sorokina, E.M., Debolt, K., Moore, J.S., Madesh, M., Fisher, A.B., Caveolae are an essential component of the pathway for endothelial cell signaling associated with abrupt reduction of shear stress. Biochim. Biophys. Acta 1783 (2008), 1866–1875.
153. [153] Zhang, Q., Chatterjee, S., Wei, Z., Liu, W.D., Fisher, A.B., Rac and PI3 kinase mediate endothelial cell-reactive oxygen species generation during normoxic lung ischemia. Antioxid. Redox Signal 10 (2008), 679–689.
154. [154] Chatterjee, C., Browning, E., Hong, N., Debolt, K.M., Sorokina, E.M., Liu, W., Birmbaum, M.J., Fisher, A.B., Membrane depolarization is the trigger for P13Kinase/Akt activation and leads to the generation of reactive oxygen species. Am. J. Physiol. Heart Circ. Physiol. 302 (2011), H105–H114.
155. [155] Browning, E., Wang, H., Hong, N., Yu, K., Buerk, D.G., DeBolt, K., Gonder, D., Sorokina, E.M., Patel, P., De Leon, D.D., Feinstein, S.I., Fisher, A.B., Chatterjee, S., Mechanotransduction drives post ischemic revascularization through K(ATP) channel closure and production of reactive oxygen species. Antioxid. Redox Signal 20 (2014), 872–886.
156. [156] Wei, Z., Manevich, Y., Al-Mehdi, A.B., Chatterjee, S., Fisher, A.B., Ca2+ flux through voltage-gated channels with flow cessation in pulmonary microvascular endothelial cells. Microcirculation 11 (2004), 517–526.
157. [157] Fukai, T., Ushio-Fukai, M., Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid. Redox Signal 15 (2011), 1583–1606.
158. [158] Fisher, A.B., Redox signaling across cell membranes. Antioxid. Redox Signal 11 (2009), 1349–1356.
159. [159] Frey, R.S., Ushio-Fukai, M., Malik, A.B., NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxid. Redox Signal 11 (2009), 791–810.
160. [160] Bernard, K., Hecker, L., Luckhardt, T.R., Cheng, G., Thannickal, V.J., NADPH oxidases in lung health and disease. Antioxid. Redox Signal 20 (2014), 2838–2853.
161. [161] Drummond, G.R., Selemidis, S., Griendling, K.K., Sobey, C.G., Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 10 (2011), 453–471.
162. [162] Benipal, B., Feinstein, S.I., Chatterjee, S., Dodia, C., Fisher, A.B., Inhibition of the phospholipase A2 activity of peroxiredoxin 6 prevents lung damage wih exposure to hyperoxia. Redox Biol. 4 (2015), 321–327.
163. [163] Matot, I., Manevich, Y., Al-Mehdi, A.B., Song, C., Fisher, A.B., Fluorescence imaging of lipid peroxidation in isolated rat lungs during nonhypoxic lung ischemia. Free Radic. Biol. Med. 34 (2003), 785–790.