4-Hydroxynonenal (HNE) modified proteins in metabolic diseases

Free Radical Biology and Medicine

Volumn 111, Issue , 2017, Pages 309-315

  Castro, José Pedro ^a,b,e,f   Jung, Tobias ^a,c   Grune, Tilman ^a,b,c,d   Siems, Werner ^g,h  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d NutriAct Competence Cluster for Nutritional Sciences Berlin Potsdam   (Germany)

^e University of Porto   (Portugal)

^f UNIVERSITY OF PORTO   (Portugal)

^g Institute of Physiotherapy and Gerontology   (Germany)

^h UNIVERSITY OF SALZBURG   (Austria)

Author keywords

4 hydroxynonenal; HNE metabolism; HNE modified Proteins; Proteasome; Proteolysis

Indexed keywords

4 HYDROXYNONENAL; BIOLOGICAL MARKER; PROTEIN; 4-HYDROXY-2-NONENAL; ALCOHOL DEHYDROGENASE; ALDEHYDE; ALDEHYDE DEHYDROGENASE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN; PROTEASOME;

CELL FATE; HUMAN; MAMMAL CELL; METABOLIC DISORDER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN TARGETING; REVIEW; ANIMAL; GENETICS; HYDROLYSIS; LIPID PEROXIDATION; METABOLISM; PATHOLOGY; PROTEIN DEGRADATION; PROTEIN PROCESSING;

ALCOHOL DEHYDROGENASE; ALDEHYDE DEHYDROGENASE; ALDEHYDES; ANIMALS; BIOMARKERS; GLUTATHIONE TRANSFERASE; HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; LIPID PEROXIDATION; METABOLIC DISEASES; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS;

EID: 85006789333     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.10.497     Document Type: Review

References (76)

1. Furukawa, S., Fujita, T., Shimabukuro, M., Iwaki, M., Yamada, Y., Nakajima, Y., Nakayama, O., Makishima, M., Matsuda, M., Shimomura, I., Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Investig. 114:12 (2004), 1752–1761.
2. Houstis, N., Rosen, E.D., Lander, E.S., Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:7086 (2006), 944–948.
3. Hou, N., Torii, S., Saito, N., Hosaka, M., Takeuchi, T., Reactive oxygen species-mediated pancreatic beta-cell death is regulated by interactions between stress-activated protein kinases, p38 and c-Jun N-terminal kinase, and mitogen-activated protein kinase phosphatases. Endocrinology 149:4 (2008), 1654–1665.
4. Møller, I.M., Rogowska-Wrzesinska, A., Rao, R.S.P., Protein carbonylation and metal-catalyzed Protein oxidation in a cellular perspective. J. Proteom. 74:11 (2011), 2228–2242.
5. Nyström, T., Role of oxidative carbonylation in protein quality control and senescence. EMBO J. 24:7 (2005), 1311–1317.
6. Höhn, A., Jung, T., Grune, T., Pathophysiological importance of aggregated damaged proteins. Free Radic. Biol. Med. 71:0 (2014), 70–89.
7. Curtis, J.M., Grimsrud, P.A., Wright, W.S., Xu, X., Foncea, R.E., Graham, D.W., Brestoff, J.R., Wiczer, B.M., Ilkayeva, O., Cianflone, K., Muoio, D.E., Arriaga, E.A., Bernlohr, D.A., Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction. Diabetes 59:5 (2010), 1132–1142.
8. Grimsrud, P.A., Picklo, M.J. Sr., Griffin, T.J., Bernlohr, D.A., Carbonylation of adipose proteins in obesity and insulin resistance: identification of adipocyte fatty acid-binding protein as a cellular target of 4-hydroxynonenal. Mol. Cell. Proteom. 6:4 (2007), 624–637.
9. Frohnert, B.I., Bernlohr, D.A., Protein carbonylation, mitochondrial dysfunction, and insulin resistance. Adv. Nutr.: Int. Rev. J. 4:2 (2013), 157–163.
10. Esterbauer, H., Schaur, R.J., Zollner, H., Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11:1 (1991), 81–128.
11. Spickett, C.M., The lipid peroxidation product 4-hydroxy-2-nonenal: advances in chemistry and analysis. Redox Biol. 1:1 (2013), 145–152.
12. Poli, G., Chiarpotto, E., Biasi, F., Pavia, R., Albano, E., Dianzani, M.U., Enzymatic impairment induced by biological aldehydes in intact rat liver cells. Res. Commun. Chem. Pathol. Pharmacol. 38:1 (1982), 71–76.
13. Grune, T., Siems, W.G., Petras, T., Identification of metabolic pathways of the lipid peroxidation product 4-hydroxynonenal in in situ perfused rat kidney. J. Lipid Res. 38:8 (1997), 1660–1665.
14. Lesgards, J.F., Frayne, I.R., Comte, B., Busseuil, D., Rheaume, E., Tardif, J.C., Rosiers, C.D., Differential distribution of 4-hydroxynonenal adducts to sulfur and nitrogen residues in blood proteins as revealed using Raney nickel and gas chromatography-mass spectrometry. Free Radic. Biol. Med. 47:10 (2009), 1375–1385.
15. Davies, K.J., Protein damage and degradation by oxygen radicals. I. general aspects. J. Biol. Chem. 262:20 (1987), 9895–9901.
16. Davies, K.J., Delsignore, M.E., Protein damage and degradation by oxygen radicals. III. Modification of secondary and tertiary structure. J. Biol. Chem. 262:20 (1987), 9908–9913.
17. Davies, K.J., Delsignore, M.E., Lin, S.W., Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J. Biol. Chem. 262:20 (1987), 9902–9907.
18. Siems, W.G., Capuozzo, E., Verginelli, D., Salerno, C., Crifo, C., Grune, T., Inhibition of NADPH oxidase-mediated superoxide radical formation in PMA-stimulated human neutrophils by 4-hydroxynonenal–binding to -SH and -NH2 groups. Free Radic. Res. 27:4 (1997), 353–358.
19. Hohn, A., Grune, T., Lipofuscin: formation, effects and role of macroautophagy. Redox Biol. 1 (2013), 140–144.
20. Yin, D., Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic. Biol. Med. 21:6 (1996), 871–888.
21. Siems, W., Grune, T., Intracellular metabolism of 4-hydroxynonenal. Mol. Asp. Med. 24:4–5 (2003), 167–175.
22. Codreanu, S.G., Zhang, B., Sobecki, S.M., Billheimer, D.D., Liebler, D.C., Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal. Mol. Cell. Proteom. 8:4 (2009), 670–680.
23. Chavez, J., Chung, W.G., Miranda, C.L., Singhal, M., Stevens, J.F., Maier, C.S., Site-specific protein adducts of 4-hydroxy-2(E)-nonenal in human THP-1 monocytic cells: protein carbonylation is diminished by ascorbic acid. Chem. Res. Toxicol. 23:1 (2010), 37–47.
24. Jung, T., Engels, M., Kaiser, B., Grune, T., Distribution of oxidized and HNE-modified proteins in U87 cells. BioFactors 24:1–4 (2005), 165–170.
25. Schaur, R.J., Siems, W., Bresgen, N., Eckl, P.M., 4-Hydroxy-nonenal-A bioactive lipid peroxidation product. Biomolecules 5:4 (2015), 2247–2337.
26. Just, J., Jung, T., Friis, N.A., Lykkemark, S., Drasbek, K., Siboska, G., Grune, T., Kristensen, P., Identification of an unstable 4-hydroxynoneal modification on the 20S proteasome subunit alpha7 by recombinant antibody technology. Free Radic. Biol. Med. 89 (2015), 786–792.
27. Carbone, D.L., Doorn, J.A., Kiebler, Z., Petersen, D.R., Cysteine modification by lipid peroxidation products inhibits protein disulfide isomerase. Chem. Res. Toxicol. 18:8 (2005), 1324–1331.
28. Haberzettl, P., Hill, B.G., Oxidized lipids activate autophagy in a JNK-dependent manner by stimulating the endoplasmic reticulum stress response. Redox Biol.(1), 2013, 56–64.
29. Okada, K., Wangpoengtrakul, C., Osawa, T., Toyokuni, S., Tanaka, K., Uchida, K., 4-Hydroxy-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. Identification of proteasomes as target molecules. J. Biol. Chem. 274:34 (1999), 23787–23793.
30. Vieira, O., Escargueil-Blanc, I., Jurgens, G., Borner, C., Almeida, L., Salvayre, R., Negre-Salvayre, A., Oxidized LDLs alter the activity of the ubiquitin-proteasome pathway: potential role in Oxidized LDL-induced apoptosis. FASEB J. 14:3 (2000), 532–542.
31. Ferrington, D.A., Kapphahn, R.J., Catalytic site-specific inhibition of the 20S proteasome by 4-hydroxynonenal. FEBS Lett. 578:3 (2004), 217–223.
32. Bardag-Gorce, F., Li, J., French, B.A., French, S.W., The effect of ethanol-induced CYP2E1 on proteasome activity: the role of 4-hydroxynonenal. Exp. Mol. Pathol. 78:2 (2005), 109–115.
33. Kessova, I.G., Cederbaum, A.I., The effect of CYP2E1-dependent oxidant stress on activity of proteasomes in HepG2 cells. J. Pharmacol. Exp. Ther. 315:1 (2005), 304–312.
34. Grune, T., Davies, K.J., The proteasomal system and HNE-modified proteins. Mol. Asp. Med. 24:4–5 (2003), 195–204.
35. Sitte, N., Huber, M., Grune, T., Ladhoff, A., Doecke, W.D., Von Zglinicki, T., Davies, K.J., Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J. 14:11 (2000), 1490–1498.
36. Sitte, N., Merker, K., Von Zglinicki, T., Davies, K.J., Grune, T., Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part II–aging of nondividing cells. FASEB J. 14:15 (2000), 2503–2510.
37. Sitte, N., Merker, K., Von Zglinicki, T., Grune, T., Davies, K.J., Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part I–effects of proliferative senescence. FASEB J. 14:15 (2000), 2495–2502.
38. Friguet, B., Stadtman, E.R., Szweda, L.I., Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Formation of cross-linked protein that inhibits the multicatalytic protease. J. Biol. Chem. 269:34 (1994), 21639–21643.
39. Friguet, B., Szweda, L.I., Stadtman, E.R., Susceptibility of glucose-6-phosphate dehydrogenase modified by 4-hydroxy-2-nonenal and metal-catalyzed oxidation to proteolysis by the multicatalytic protease. Arch. Biochem. Biophys. 311:1 (1994), 168–173.
40. Shringarpure, R., Grune, T., Sitte, N., Davies, K.J., 4-Hydroxynonenal-modified amyloid-beta peptide inhibits the proteasome: possible importance in Alzheimer's disease. Cell. Mol. Life Sci. 57:12 (2000), 1802–1809.
41. Grune, T., Michel, P., Sitte, N., Eggert, W., Albrecht-Nebe, H., Esterbauer, H., Siems, W.G., Increased levels of 4-hydroxynonenal modified proteins in plasma of children with autoimmune diseases. Free Radic. Biol. Med. 23:3 (1997), 357–360.
42. Petersen, D.R., Doorn, J.A., Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radic. Biol. Med. 37:7 (2004), 937–945.
43. Siems, W.G., Zollner, H., Grune, T., Esterbauer, H., Metabolic fate of 4-hydroxynonenal in hepatocytes: 1,4-dihydroxynonene is not the main product. J. Lipid Res. 38:3 (1997), 612–622.
44. Hohn, A., Konig, J., Grune, T., Protein oxidation in aging and the removal of oxidized proteins. J. Proteom. 92 (2013), 132–159.
45. Grune, T., Davies, K.J., Breakdown of oxidized proteins as a part of secondary antioxidant defenses in mammalian cells. BioFactors 6:2 (1997), 165–172.
46. Li, Q., Sadhukhan, S., Berthiaume, J.M., Ibarra, R.A., Tang, H., Deng, S., Hamilton, E., Nagy, L.E., Tochtrop, G.P., Zhang, G.F., 4-Hydroxy-2(E)-nonenal (HNE) catabolism and formation of HNE adducts are modulated by beta oxidation of fatty acids in the isolated rat heart. Free Radic. Biol. Med. 58 (2013), 35–44.
47. Alary, J., Gueraud, F., Cravedi, J.P., Fate of 4-hydroxynonenal in vivo: disposition and metabolic pathways. Mol. Asp. Med. 24:4–5 (2003), 177–187.
48. Alary, J., Bravais, F., Cravedi, J.P., Debrauwer, L., Rao, D., Bories, G., Mercapturic acid conjugates as urinary end metabolites of the lipid peroxidation product 4-hydroxy-2-nonenal in the rat. Chem. Res. Toxicol. 8:1 (1995), 34–39.
49. Siems, W.G., Hapner, S.J., van Kuijk, F.J., 4-hydroxynonenal inhibits Na(+)-K(+)-ATPase. Free Radic. Biol. Med. 20:2 (1996), 215–223.
50. Botzen, D., Grune, T., Degradation of HNE-modified proteins–possible role of ubiquitin. Redox Rep.: Commun. Free Radic. Res. 12:1 (2007), 63–67.
51. Grune, T., Merker, K., Sandig, G., Davies, K.J., Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem. Biophys. Res. Commun. 305:3 (2003), 709–718.
52. Shringarpure, R., Grune, T., Mehlhase, J., Davies, K.J., Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J. Biol. Chem. 278:1 (2003), 311–318.
53. Carbone, D.L., Doorn, J.A., Petersen, D.R., 4-Hydroxynonenal regulates 26S proteasomal degradation of alcohol dehydrogenase. Free Radic. Biol. Med. 37:9 (2004), 1430–1439.
54. Hyun, D.H., Lee, M.H., Halliwell, B., Jenner, P., Proteasomal dysfunction induced by 4-hydroxy-2,3-trans-nonenal, an end-product of lipid peroxidation: a mechanism contributing to neurodegeneration?. J. Neurochem. 83:2 (2002), 360–370.
55. Marques, C., Pereira, P., Taylor, A., Liang, J.N., Reddy, V.N., Szweda, L.I., Shang, F., Ubiquitin-dependent lysosomal degradation of the HNE-modified proteins in lens epithelial cells. FASEB J. 18:12 (2004), 1424–1426.
56. Yamaguchi, T., Yoneyama, M., Hinoi, E., Ogita, K., Involvement of calpain in 4-hydroxynonenal-induced disruption of gap junction-mediated intercellular communication among fibrocytes in primary cultures derived from the cochlear spiral ligament. J. Pharmacol. Sci. 129:2 (2015), 127–134.
57. Xu, G., Liu, Y., Sayre, L.M., Independent synthesis, solution behavior, and studies on the mechanism of formation of a primary amine-derived fluorophore representing cross-linking of proteins by (E)-4-hydroxy-2-nonenal. J. Org. Chem. 64:16 (1999), 5732–5745.
58. Castro, J.P., Ott, C., Jung, T., Grune, T., Almeida, H., Carbonylation of the cytoskeletal protein actin leads to aggregate formation. Free Radic. Biol. Med. 53:4 (2012), 916–925.
59. Grune, T., Jung, T., Merker, K., Davies, K.J., Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and ‘aggresomes’ during oxidative stress, aging, and disease. Int. J. Biochem. Cell Biol. 36:12 (2004), 2519–2530.
60. Hohn, A., Jung, T., Grimm, S., Catalgol, B., Weber, D., Grune, T., Lipofuscin inhibits the proteasome by binding to surface motifs. Free Radic. Biol. Med. 50:5 (2011), 585–591.
61. Sanchez, I., Xu, C.J., Juo, P., Kakizaka, A., Blenis, J., Yuan, J., Caspase-8 is required for cell death induced by expanded polyglutamine repeats. Neuron 22:3 (1999), 623–633.
62. Chondrogianni, N., Gonos, E.S., Proteasome function determines cellular homeostasis and the rate of aging. Adv. Exp. Med. Biol. 694 (2010), 38–46.
63. Csala, M., Kardon, T., Legeza, B., Lizak, B., Mandl, J., Margittai, E., Puskas, F., Szaraz, P., Szelenyi, P., Banhegyi, G., On the role of 4-hydroxynonenal in health and disease. Biochim. Biophys. Acta 1852:5 (2015), 826–838.
64. Barrera, G., Pizzimenti, S., Ciamporcero, E.S., Daga, M., Ullio, C., Arcaro, A., Cetrangolo, G.P., Ferretti, C., Dianzani, C., Lepore, A., Gentile, F., Role of 4-hydroxynonenal-protein adducts in human diseases. Antioxid. Redox Signal. 22:18 (2015), 1681–1702.
65. Naito, Y., Takagi, T., Handa, O., Yoshikawa, T., Lipid hydroperoxide-derived modification of proteins in gastrointestinal tract. Sub-Cell. Biochem. 77 (2014), 137–148.
66. Kumano-Kuramochi, M., Shimozu, Y., Wakita, C., Ohnishi-Kameyama, M., Shibata, T., Matsunaga, S., Takano-Ishikawa, Y., Watanabe, J., Goto, M., Xie, Q., Komba, S., Uchida, K., Machida, S., Identification of 4-hydroxy-2-nonenal-histidine adducts that serve as ligands for human lectin-like oxidized LDL receptor-1. Biochem. J. 442:1 (2012), 171–180.
67. Gargiulo, S., Gamba, P., Testa, G., Rossin, D., Biasi, F., Poli, G., Leonarduzzi, G., Relation between TLR4/NF-kappaB signaling pathway activation by 27-hydroxycholesterol and 4-hydroxynonenal, and atherosclerotic plaque instability. Aging Cell 14:4 (2015), 569–581.
68. Barnham, K.J., Masters, C.L., Bush, A.I., Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 3:3 (2004), 205–214.
69. Jomova, K., Vondrakova, D., Lawson, M., Valko, M., Metals, oxidative stress and neurodegenerative disorders. Mol. Cell. Biochem. 345:1–2 (2010), 91–104.
70. Hardas, S.S., Sultana, R., Clark, A.M., Beckett, T.L., Szweda, L.I., Murphy, M.P., Butterfield, D.A., Oxidative modification of lipoic acid by HNE in Alzheimer disease brain. Redox Biol. 1 (2013), 80–85.
71. Takeda, A., Smith, M.A., Avila, J., Nunomura, A., Siedlak, S.L., Zhu, X., Perry, G., Sayre, L.M., In Alzheimer's disease, heme oxygenase is coincident with Alz50, an epitope of tau induced by 4-hydroxy-2-nonenal modification. J. Neurochem. 75:3 (2000), 1234–1241.
72. Zhu, X., Castellani, R.J., Moreira, P.I., Aliev, G., Shenk, J.C., Siedlak, S.L., Harris, P.L., Fujioka, H., Sayre, L.M., Szweda, P.A., Szweda, L.I., Smith, M.A., Perry, G., Hydroxynonenal-generated crosslinking fluorophore accumulation in Alzheimer disease reveals a dichotomy of protein turnover. Free Radic. Biol. Med. 52:3 (2012), 699–704.
73. Yoritaka, A., Hattori, N., Uchida, K., Tanaka, M., Stadtman, E.R., Mizuno, Y., Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl. Acad. Sci. USA 93:7 (1996), 2696–2701.
74. Kurien, B.T., Hensley, K., Bachmann, M., Scofield, R.H., Oxidatively modified autoantigens in autoimmune diseases. Free Radic. Biol. Med. 41:4 (2006), 549–556.
75. Toyoda, K., Nagae, R., Akagawa, M., Ishino, K., Shibata, T., Ito, S., Shibata, N., Yamamoto, T., Kobayashi, M., Takasaki, Y., Matsuda, T., Uchida, K., Protein-bound 4-hydroxy-2-nonenal: an endogenous triggering antigen of antI-DNA response. J. Biol. Chem. 282:35 (2007), 25769–25778.
76. Uchida, K., Toyokuni, S., Nishikawa, K., Kawakishi, S., Oda, H., Hiai, H., Stadtman, E.R., Michael addition-type 4-hydroxy-2-nonenal adducts in modified low-density lipoproteins: markers for atherosclerosis. Biochemistry 33:41 (1994), 12487–12494.