Overview on major lipid peroxidation bioactive factor 4-hydroxynonenal as pluripotent growth-regulating factor

Free Radical Research

Volumn 49, Issue 7, 2015, Pages 850-860

  Milkovic, L ^a   Gasparovic, A Cipak ^a   Zarkovic, N ^a,b  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b University for Applied Sciences   (Croatia)

Author keywords

Cell; Growth regulation; Hormesis; Lipid peroxidation; Oxidative stress; Proliferation

Indexed keywords

4 HYDROXYNONENAL; BIOMATERIAL; GROWTH FACTOR; PLURIPOTENT GROWTH REGULATING FACTOR; UNCLASSIFIED DRUG; 4-HYDROXY-2-NONENAL; ALDEHYDE; ANTIOXIDANT; BIOLOGICAL MARKER; CYTOKINE;

APOPTOSIS; BIOLOGICAL ACTIVITY; BONE CELL; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL SPECIFICITY; GROWTH REGULATION; HUMAN; LIPID PEROXIDATION; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; TISSUE SPECIFICITY; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ALDEHYDES; ANTIOXIDANTS; APOPTOSIS; BIOMARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; HUMANS; LIPID PEROXIDATION; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION;

EID: 84936746182     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2014.999056     Document Type: Review

References (122)

1. Zarkovic N, Cipak A, Cindric M, Waeg G, Borovic Sunjic S, Mrakovcic L, et al. 4-Hydroxynonenal-protein adducts as biomarkers of oxidative stress, lipid peroxidation and oxidative homeostasis. In Free Radicals, Health and Lifestyle: Proceedings from the Europe Meeting of the Society for Free Radical Research. Medimond Srl 2009; 37-45.
2. Sies H. Oxidative stress: Introductory remarks. In: Sies H (ed.). Oxidative stress. London: Academic Press; 1985. pp. 1-7.
3. Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol 2010; 38: 96-109.
4. Pham-Huy LA, He H, Pham-Huy C. Free radicals, antioxidants in disease and health. Int J Biomed Sci 2008; 4: 89-96.
5. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 2008; 88: 1243-1276.
6. Poppek D, Grune T. Proteasomal defense of oxidative protein modifications. Antioxid Redox Signal 2006; 8: 173-184.
7. Trachootham D, Lu W, Ogasawara Ma, Nilsa R-DV, Huang P. Redox regulation of cell survival. Antioxid Redox Signal 2008; 10: 1343-1374.
8. Wall SB, Oh J-Y, Diers AR, Landar A. Oxidative modification of proteins: an emerging mechanism of cell signaling. Front Physiol 2012; 3: 369.
9. Ray PD, Huang B-W, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012; 24: 981-990.
10. D'Autreaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007; 8: 813-824.
11. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 2011; 194: 7-15.
12. Ayala A, Munoz MF, Arguelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014; 2014: 360438.
13. Yin H, Xu L, Porter NA. Free radical lipid peroxidation: mechanisms and analysis. Chem Rev 2011; 111: 5944-5972.
14. Niki E. Lipid peroxidation: physiological levels and dual biological effects. Free Radic Biol Med 2009; 47: 469-484.
15. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991; 11: 81-128.
16. Pizzimenti S, Toaldo C, Pettazzoni P, Dianzani MU, Barrera G. The " two-faced" effects of reactive oxygen species and the lipid peroxidation product 4-hydroxynonenal in the hallmarks of cancer. Cancers (Basel) 2010; 2: 338-363.
17. Leonarduzzi G, Chiarpotto E, Biasi F, Poli G. 4-Hydroxynonenal and cholesterol oxidation products in atherosclerosis. Mol Nutr Food Res 2005; 49: 1044-1049.
18. Mattson MP. Roles of the lipid peroxidation product 4-hydroxynonenal in obesity, the metabolic syndrome, and associated vascular and neurodegenerative disorders. Exp Gerontol 2009; 44: 625-633.
19. Zarkovic K. 4-hydroxynonenal and neurodegenerative diseases. Mol Aspects Med 2003; 24: 293-303.
20. Negre-Salvayre A, Auge N, Ayala V, Basaga H, Boada J, Brenke R, et al. Pathological aspects of lipid peroxidation. Free Radic Res 2010; 44: 1125-1171.
21. Wildburger R, Mrakovcic L, Stroser M, Andrisic L, Borovic Sunjic S, Zarkovic K, Zarkovic N. Lipid Peroxidation and Age-Associated Diseases-Cause or Consequence ?: Review. Turkiye Klin J Med Sci 2009; 29: 189-193.
22. Gueraud F, Atalay M, Bresgen N, Cipak A, Eckl PM, Huc L, et al. Chemistry and biochemistry of lipid peroxidation products. Free Radic Res 2010; 44: 1098-1124.
23. Liu W, Porter NA, Schneider C, Brash AR, Yin H. Formation of 4-hydroxynonenal from cardiolipin oxidation: Intramolecular peroxyl radical addition and decomposition. Free Radic Biol Med 2011; 50: 166-178.
24. Schneider C, Porter NA, Brash AR. Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. J Biol Chem 2008; 283: 15539-15543.
25. Zhong H, Lu J, Xia L, Zhu M, Yin H. Formation of electrophilic oxidation products from mitochondrial cardiolipin in vitro and in vivo in the context of apoptosis and atherosclerosis. Redox Biol 2014; 2: 878-883.
26. Schaur R. Basic aspects of the biochemical reactivity of 4-hydroxynonenal. Mol Aspects Med 2003; 24: 149-159.
27. Forman HJ, Fukuto JM, Miller T, Zhang H, Rinna A, Levy S. The chemistry of cell signaling by reactive oxygen and nitrogen species and 4-hydroxynonenal. Arch Biochem Biophys 2008; 477: 183-195.
28. Lushchak VI. Glutathione homeostasis and functions: potential targets for medical interventions. J Amino Acids 2012; 2012: 736837.
29. Awasthi S, Singhal SS, Awasthi YC, Martin B, Woo J-H, Cunningham CC, Frankel AE. RLIP76 and Cancer. Clin Cancer Res 2008; 14: 4372-4377.
30. Siems W, Grune T. Intracellular metabolism of 4-hydroxynonenal. Mol Aspects Med 2003; 24: 167-175.
31. Srivastava S, Liu SQ, Conklin DJ, Zacarias A, Srivastava SK, Bhatnagar A. Involvement of aldose reductase in the metabolism of atherogenic aldehydes. Chem Biol Interact 2001; 130-132: 563-571.
32. Baradat M, Jouanin I, Dalleau S, Tach S, Gieules M, Debrauwer L, Huc L, Dupuy J, Pierre FHF. 4-Hydroxy-2 (E) -nonenal metabolism differs in Apc +/+ cells and in Apc Min/+ cells: it may explain colon cancer promotion by Heme iron. Chem Res Toxicol. 2011; 24: 1984-1993.
33. Choudhary S, Srivastava S, Xiao T, Andley UP, Srivastava SK, Ansari NH. Metabolism of lipid derived aldehyde, 4-hydroxynonenal in human lens epithelial cells and rat lens. Invest Ophthalmol Vis Sci 2003; 44: 2675-2682.
34. Canuto RA, Muzio G, Maggiora M, Poli G, Biasi F, Dianzani MU, et al. Ability of different hepatoma cells to metabolize 4-hydroxynonenal. Cell Biochem Funct 1993; 11: 79-86.
35. Poli G, Schaur RJ, Siems WG, Leonarduzzi G. 4-hydroxynonenal: a membrane lipid oxidation product of medicinal interest. Med Res Rev 2008; 28: 569-631.
36. Smathers RL, Fritz KS, Galligan JJ, Shearn CT, Reigan P, Marks MJ, Petersen DR. Characterization of 4-HNE modified L-FABP reveals alterations in structural and functional dynamics. PLoS One 2012; 7: e38459.
37. Lee W-C, Wong H-Y, Chai Y-Y, Shi C-W, Amino N, Kikuchi S, Huang S-H. Lipid peroxidation dysregulation in ischemic stroke: plasma 4-HNE as a potential biomarker? Biochem Biophys Res Commun 2012; 425: 842-847.
38. Dalleau S, Baradat M, Gueraud F, Huc L. Cell death and diseases related to oxidative stress: 4-hydroxynonenal (HNE) in the balance. Cell Death Differ 2013; 20: 1615-1630.
39. Zarkovic N. 4-hydroxynonenal as a bioactive marker of pathophysiological processes. Mol Aspects Med 2003; 24: 281-291.
40. Dianzani MU. 4-Hydroxynonenal from pathology to physiology. Mol Aspects Med 2003; 24: 263-272.
41. Chen Z-H, Niki E. 4-hydroxynonenal (4-HNE) has been widely accepted as an inducer of oxidative stress. Is this the whole truth about it or can 4-HNE also exert protective effects? IUBMB Life 2006; 58: 372-373.
42. Sunjic SB, Cipak A, Rabuzin F, Wildburger R, Zarkovic N. The influence of 4-hydroxy-2-nonenal on proliferation, differentiation and apoptosis of human osteosarcoma cells. Biofactors 2005; 24: 141-148.
43. Kreuzer T, Grube R, Wutte A, Zarkovic N, Schaur RJ. 4-Hydroxynonenal modifies the effects of serum growth factors on the expression of the c-fos proto-oncogene and the proliferation of HeLa carcinoma cells. Free Radic Biol Med 1998; 25: 42-49.
44. Biasi F, Vizio B, Mascia C, Gaia E, Zarkovic N, Chiarpotto E, et al. c-Jun N-terminal kinase upregulation as a key event in the proapoptotic interaction between transforming growth factor-beta1 and 4-hydroxynonenal in colon mucosa. Free Radic Biol Med 2006; 41: 443-454.
45. Uchida K. 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 2003; 42: 318-343.
46. Jorgensen P, Milkovic L, Zarkovic N, Waeg G, Rattan SIS. Lipid peroxidation-derived 4-hydroxynonenal-modified proteins accumulate in human facial skin fibroblasts during ageing in vitro. Biogerontology 2014; 15: 105-110.
47. Zarkovic N, Cipak A, Jaganjac M, Borovic S, Zarkovic K. Pathophysiological relevance of aldehydic protein modifications. J Proteomics 2013; 92: 239-247.
48. Curzio M. Interaction between neutrophils and 4-hydroxyalkenals and consequences on neutrophil motility. Free Radic Res Commun 1988; 5: 55-66.
49. Curzio M, Torrielli MV, Giroud JP, Esterbauer H, Dianzani MU. Neutrophil chemotactic responses to aldehydes. Res Commun Chem Pathol Pharmacol 1982; 36: 463-476.
50. Rossi MA, Curzio M, Mauro C Di, Fidale F, Garramone A, Esterbauer H, et al. Experimental studies on the mechanism of action of 4-hydroxy-2,3-trans-nonenal, a lipid peroxidation product displaying chemotactic activity toward rat neutrophils. Cell Biochem Funct 1991; 9: 163-170.
51. Curzio M, Esterbauer H, Mauro C Di, Dianzani MU. Influence of the lipid peroxidation product 4-hydroxynonenal on human neutrophil migration. Int J Immunother 1990; 6: 13-18.
52. Paradisi L, Panagini C, Parola M, Barrera G, Dianzani MU. Effects of 4-hydroxynonenal on adenylate cyclase and 5′-nucleotidase activities in rat liver plasma membranes. Chem Biol Interact 1985; 53: 209-217.
53. Rossi MA, Dianzani MU. Action of 2-nonenal and 4-hydroxynonenal on phosphoinositide-specific phosopholipase C in undifferentiated and DMSO-differentiated HL-60 cells. Cell Biochem Funct 2000; 18: 209-214.
54. Maggiora M, Rossi MA. Experimental researches on the role of phosphoinositide-specific phospholipase C in 4-hydroxynonenal induced exocytosis. Cell Biochem Funct 2003; 21: 155-160.
55. Rossi MA, Garramone A, Dianzani MU. Stimulation of phospholipase C activity by 4-hydroxynonenal; influence of GTP and calcium concentration. Int J Tissue React 1988; 10: 321-325.
56. Ramana KV, Bhatnagar A, Srivastava S, Yadav UC, Awasthi S, Awasthi YC, Srivastava SK. Mitogenic responses of vascular smooth muscle cells to lipid peroxidation-derived aldehyde 4-hydroxy-trans-2-nonenal (HNE): role of aldose reductase-catalyzed reduction of the HNE-glutathione conjugates in regulating cell growth. J Biol Chem 2006; 281: 17652-17660.
57. Chiarpotto E, Domenicotti C, Paola D, Vitali A, Nitti M, Pronzato MA, et al. Regulation of rat hepatocyte protein kinase C beta isoenzymes by the lipid peroxidation product 4-hydroxy-2,3-nonenal: A signaling pathway to modulate vesicular transport of glycoproteins. Hepatology 1999; 29: 1565-1572.
58. Leonarduzzi G, Robbesyn F, Poli G. Signaling kinases modulated by 4-hydroxynonenal. Free Radic Biol Med 2004; 37: 1694-1702.
59. Liu W, Kato M, Anwaral A, Hayakawa A, Suzuki H, Miyata T. 4-hydroxynonenal induces a cellular redox statusrelated activation of the caspase cascade for apoptotic cell death. 2000; 641: 635-641.
60. Abarikwu SO, Pant AB, Farombi EO. 4-Hydroxynonenal induces mitochondrial-mediated apoptosis and oxidative stress in SH-SY5Y human neuronal cells. Basic Clin Pharmacol Toxicol 2012; 110: 441-448.
61. Ruef J, Rao GN, Li F, Bode C, Patterson C, Bhatnagar A, Runge MS. Induction of rat aortic smooth muscle cell growth by the lipid peroxidation product 4-hydroxy-2-nonenal. Circulation 1998; 97: 1071-1078.
62. Barrera G, Muraca R, Pizzimenti S, Serra A, Rosso C, Saglio G, et al. Inhibition of c-myc expression induced by 4-hydroxynonenal, a product of lipid peroxidation, in the HL-60 human leukemic cell line. Biochem Biophys Res Commun 1994; 203: 553-561.
63. Cerbone A, Toaldo C, Laurora S, Briatore F, Pizzimenti S, Dianzani MU, et al. 4-Hydroxynonenal and PPARgamma ligands affect proliferation, differentiation, and apoptosis in colon cancer cells. Free Radic Biol Med 2007; 42: 1661-1670.
64. Zanetti D, Poli G, Vizio B, Zingaro B, Chiarpotto E, Biasi F. 4-hydroxynonenal and transforming growth factorbeta1 expression in colon cancer. Mol Aspects Med 2003; 24: 273-280.
65. Uchida K, Shiraishi M, Naito Y, Torii Y, Nakamura Y, Osawa T. Activation of stress signaling pathways by the end product of lipid peroxidation. 4-hydroxy-2-nonenal is a potential inducer of intracellular peroxide production. J Biol Chem 1999; 274: 2234-2242.
66. Kutuk O, Basaga H. Apoptosis signalling by 4-hydroxynonenal: a role for JNK-c-Jun/AP-1 pathway. Redox Rep 2007; 12: 30-34.
67. Camandola S, Poli G, Mattson MP. The lipid peroxidation product 4-hydroxy-2,3-nonenal increases AP-1-binding activity through caspase activation in neurons. J Neurochem 2000; 74: 159-168.
68. Usatyuk PV, Natarajan V. Role of mitogen-activated protein kinases in 4-hydroxy-2-nonenal-induced actin remodeling and barrier function in endothelial cells. J Biol Chem. 2004; 279: 11789-11797.
69. Lin M-H, Yen J-H, Weng C-Y, Wang L, Ha C-L, Wu M-J. Lipid peroxidation end product 4-hydroxy-trans-2-nonenal triggers unfolded protein response and heme oxygenase-1 expression in PC12 cells: Roles of ROS and MAPK pathways. Toxicology 2014; 315: 24-37.
70. McElhanon KE, Bose C, Sharma R, Wu L, Awasthi YC, Singh SP. Gsta4 Null Mouse Embryonic Fibroblasts Exhibit Enhanced Sensitivity to Oxidants: Role of 4-Hydroxynonenal in Oxidant Toxicity. Open J Apoptosis 2013; 2: 1-11.
71. Liu W, Akhand AA, Kato M, Yokoyama I, Miyata T, Kurokawa K, et al. 4-hydroxynonenal triggers an epidermal growth factor receptor-linked signal pathway for growth inhibition. J Cell Sci 1999; 112 (Pt 14): 2409-2417.
72. Suc I, Meilhac O, Lajoie-Mazenc I, Vandaele J, Jurgens G, Salvayre R, Negre-Salvayre A. Activation of EGF receptor by oxidized LDL. FASEB J 1998; 12: 665-671.
73. Barrera G, Pizzimenti S, Dianzani MU. 4-hydroxynonenal and regulation of cell cycle: effects on the pRb/E2F pathway. Free Radic Biol Med 2004; 37: 597-606.
74. Akiba S, Kumazawa S, Yamaguchi H, Hontani N, Matsumoto T, Ikeda T, et al. Acceleration of matrix metalloproteinase- 1 production and activation of platelet-derived growth factor receptor beta in human coronary smooth muscle cells by oxidized LDL and 4-hydroxynonenal. Biochim Biophys Acta 2006; 1763: 797-804.
75. Lee SJ, Seo KW, Yun MR, Bae SS, Lee WS, Hong KW, Kim CD. 4-Hydroxynonenal enhances MMP-2 production in vascular smooth muscle cells via mitochondrial ROS-mediated activation of the Akt/NF-kappaB signaling pathways. Free Radic Biol Med 2008; 45: 1487-1492.
76. Ishikado A, Nishio Y, Morino K, Ugi S, Kondo H, Makino T, et al. Low concentration of 4-hydroxy hexenal increases heme oxygenase-1 expression through activation of Nrf2 and antioxidative activity in vascular endothelial cells. Biochem Biophys Res Commun 2010; 402: 99-104.
77. Huang Y, Li W, Kong A-N. Anti-oxidative stress regulator NF-E2-related factor 2 mediates the adaptive induction of antioxidant and detoxifying enzymes by lipid peroxidation metabolite 4-hydroxynonenal. Cell Biosci 2012; 2: 40.
78. Zheng R, Heck DE, Mishin V, Black AT, Shakarjian MP, Kong A-N, et al. Modulation of keratinocyte expression of antioxidants by 4-hydroxynonenal, a lipid peroxidation end product. Toxicol Appl Pharmacol 2014; 275: 113-121.
79. Usatyuk PV, Parinandi NL, Natarajan V. Redox regulation of 4-hydroxy-2-nonenal-mediated endothelial barrier dysfunction by focal adhesion, adherens, and tight junction proteins. J Biol Chem 2006; 281: 35554-35566.
80. Pizzimenti S, Barrera G, Calzavara E, Mirandola L, Toaldo C, Dianzani MU, et al. Down-regulation of Notch1 expression is involved in HL-60 cell growth inhibition induced by 4-hydroxynonenal, a product of lipid peroxidation. Med Chem 2008; 4: 551-557.
81. Borovic S, Sunjic I, Wildburger R, Mittelbach M, Waeg G, Zarkovic N. Lipid peroxidation end product as a modulator of cell growth. In: Hayashi T, (ed.). Progress in Cell Growth Process Research. New York: Nova Science Publishers, Inc. F. Columbus, New York, Inc.; 2008. p. 237.
82. Zarković N, Zarković K, Schaur RJ, Stolc S, Schlag G, Redl H, et al. 4-Hydroxynonenal as a second messenger of free radicals and growth modifying factor. Life Sci 1999; 65: 1901-1904.
83. Semlitsch T, Tillian HM, Zarkovic N, Borovic S, Purtscher M, Hohenwarter O, Schaur RJ. Differential influence of the lipid peroxidation product 4-hydroxynonenal on the growth of human lymphatic leukaemia cells and human periopherial blood lymphocytes. Anticancer Res 2002; 22: 1689-1697.
84. Chen Z-H, Saito Y, Yoshida Y, Sekine A, Noguchi N, Niki E. 4-Hydroxynonenal induces adaptive response and enhances PC12 cell tolerance primarily through induction of thioredoxin reductase 1 via activation of Nrf2. J Biol Chem 2005; 280: 41921-41927.
85. Mattson MP, Calabrese EJ (Eds.). Hormesis: A Revolution in Biology, Toxicology and Medicine. Humana Press; 2010.
86. Zarkovic N, Ilic Z, Jurin M, Schaur RJ, Puhl H, Esterbauer H. Stimulation of HeLa cell growth by physiological concentrations of 4-hydroxynonenal. Cell Biochem Funct 1993; 11: 279-286.
87. Cerbone A, Toaldo C, Laurora S, Briatore F, Pizzimenti S, Dianzani MU, Ferretti C, Barrera G. 4-Hydroxynonenal and PPARgamma ligands affect proliferation, differentiation, and apoptosis in colon cancer cells. Free Radic Biol Med 2007; 42: 1661-1670.
88. Sharma R, Sharma A, Dwivedi S, Zimniak P, Awasthi S, Awasthi YC. 4-Hydroxynonenal self-limits fas-mediated DISC-independent apoptosis by promoting export of Daxx from the nucleus to the cytosol and its binding to Fas. Biochemistry 2008; 47: 143-156.
89. Pizzimenti S, Ferracin M, Sabbioni S, Toaldo C, Pettazzoni P, Dianzani MU, et al. MicroRNA expression changes during human leukemic HL-60 cell differentiation induced by 4-hydroxynonenal, a product of lipid peroxidation. Free Radic Biol Med 2009; 46: 282-288.
90. Semlitsch T, Tillian HM, Zarkovic N, Borovic S, Purtscher M, Hohenwarter O, Schaur RJ. Differential influence of the lipid peroxidation product 4-hydroxynonenal on the growth of human lymphatic leukaemia cells and human periopherial blood lymphocytes. Anticancer Res 2002; 22: 1689-1697.
91. Esterbauer H. Cytotoxicity and genotoxicity of lipidoxidation products. Am J Clin Nutr 1993; 57: 779S - 785S; discussion 785S - 786S.
92. Zarkovic N, Jorg Schaur R, Puhl H, Jurin M, Esterbauer H. Mutual dependence of growth modifying effects of 4-hydroxynonenal and fetal calf serum in vitro. Free Radic Biol Med 1994; 16: 877-884.
93. Barrera G, Mauro C Di, Muraca R, Ferrero D, Cavalli G, Fazio VM, et al. Induction of differentiation in human HL-60 cells by 4-hydroxynonenal, a product of lipid peroxidation. Exp Cell Res 1991; 197: 148-152.
94. Sovic A, Borovic S, Loncaric I, Kreuzer T, Zarkovic K, Vukovic T, et al. The carcinostatic and proapoptotic potential of 4-hydroxynonenal in HeLa cells is associated with its conjugation to cellular proteins. Anticancer Res 2001; 21: 1997-2004.
95. Kreuzer T, Zarković N, Grube R, Schaur RJ. Inhibition of HeLa cell proliferation by 4-hydroxynonenal is associated with enhanced expression of the c-fos oncogene. Cancer Biother Radiopharm 1997; 12: 131-136.
96. Jaganjac M, Cacev T, Cipak A, Kapitanović S, Gall Troselj K, Zarković N. Even stressed cells are individuals: second messengers of free radicals in pathophysiology of cancer. Croat Med J 2012; 53: 304-309.
97. Shearn CT, Reigan P, Petersen DR. Inhibition of hydrogen peroxide signaling by 4-hydroxynonenal due to differential regulation of Akt1 and Akt2 contributes to decreases in cell survival and proliferation in hepatocellular carcinoma cells. Free Radic Biol Med 2012; 53: 1-11.
98. Li J, Sharma R, Patrick B, Sharma A, Jeyabal PV, Reddy PM, et al. Regulation of CD95 (Fas) expression and Fas-mediated apoptotic signaling in HLE B-3 cells by 4-hydroxynonenal. Biochemistry 2006; 45: 12253-12264.
99. Awasthi YC, Sharma R, Sharma A, Yadav S, Singhal SS, Chaudhary P, Awasthi S. Self-regulatory role of 4-hydroxynonenal in signaling for stress-induced programmed cell death. Free Radic Biol Med 2008; 45: 111-118.
100. McMahon M, Itoh K, Yamamoto M, Chanas SA, Henderson CJ, McLellan LI, et al. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res 2001; 61: 3299-3307.
101. Pettazzoni P, Ciamporcero E, Medana C, Pizzimenti S, Dal Bello F, Minero VG, et al. Nuclear factor erythroid 2-related factor-2 activity controls 4-hydroxynonenal metabolism and activity in prostate cancer cells. Free Radic Biol Med 2011; 51: 1610-1618.
102. Zarkovic K, Juric G, Waeg G, Kolenc D, Zarkovic N. Immunohistochemical appearance of HNE-protein conjugates in human astrocytomas. Biofactors 2005; 24: 33-40.
103. Kolenc D, Jakovčević A, Macan M, Žarković K. The co-expression of 4-hydroxynonenal and prominin-1 in glioblastomas. Transl Neurosci 2011; 2: 163-167.
104. Juric-Sekhar G, Zarkovic K, Waeg G, Cipak A, Zarkovic N. Distribution of 4-hydroxynonenal-protein conjugates as a marker of lipid peroxidation and parameter of malignancy in astrocytic and ependymal tumors of the brain. Tumori 2009; 95: 762-768.
105. Marquez-Quinones A, Cipak A, Zarkovic K, Fattel-Fazenda S, Villa-Trevino S, Waeg G, et al. HNE-protein adducts formation in different pre-carcinogenic stages of hepatitis in LEC rats. Free Radic Res 2010; 44: 119-127.
106. Karihtala P, Kauppila S, Puistola U, Jukkola-Vuorinen A. Divergent behaviour of oxidative stress markers 8-hydroxydeoxyguanosine (8-OHdG) and 4-hydroxy-2-nonenal (HNE) in breast carcinogenesis. Histopathology 2011; 58: 854-862.
107. Biasi F, Tessitore L, Zanetti D, Cutrin JC, Zingaro B, Chiarpotto E, et al. Associated changes of lipid peroxidation and transforming growth factor beta1 levels in human colon cancer during tumour progression. Gut 2002; 50: 361-367.
108. Obtu ł owicz T, Winczura A, Speina E, Swoboda M, Janik J, Janowska B, et al. Aberrant repair of etheno-DNA adducts in leukocytes and colon tissue of colon cancer patients. Free Radic Biol Med 2010; 49: 1064-1071.
109. Borovic S, Cipak A, Meinitzer A, Kejla Z, Perovic D, Waeg G, Zarkovic N. Differential sensitivity to 4-hydroxynonenal for normal and malignant mesenchymal cells. Redox Rep 2007; 12: 50-54.
110. Rudić M, Milković L, Zarković K, Borović-Šunjić S, Sterkers O, Waeg G, et al. The effects of angiotensin II and the oxidative stress mediator 4-hydroxynonenal on human osteoblast-like cell growth: possible relevance to otosclerosis. Free Radic Biol Med 2012; 57C: 22-28.
111. Chapple SJ, Cheng X, Mann GE. Effects of 4-hydroxynonenal on vascular endothelial and smooth muscle cell redox signaling and function in health and disease. Redox Biol 2013; 1: 319-331.
112. Cipak A, Borovic S, Scukanec-Spoljar M, Kirac I, Zarkovic N. Possible involvement of 4-hydroxynonenal in splenocyte regulated liver regeneration. Biofactors Oxford Engl 2005; 24: 217-226.
113. Cipak A, Borovic S, Jaganjac M, Bresgen N, Kirac I, Grbesa I, et al. Influence of 4-hydroxynonenal and spleen cells on primary hepatocyte culture and a novel liver-derived cell line resembling hepatocyte stem cells. Acta Biochim Pol 2010; 57: 185-191.
114. Zamara E, Novo E, Marra F, Gentilini A, Romanelli RG, Caligiuri A, et al. 4-Hydroxynonenal as a selective profibrogenic stimulus for activated human hepatic stellate cells. J Hepatol 2004; 40: 60-68.
115. Vatsyayan R, Chaudhary P, Sharma A, Sharma R, Rao Lelsani PC, Awasthi S, Awasthi YC. Role of 4-hydroxynonenal in epidermal growth factor receptor-mediated signaling in retinal pigment epithelial cells. Exp Eye Res 2011; 92: 147-154.
116. Ranjan D, Chen C, Johnston TD, Jeon H, Ibrahim M, Drake J, Butterfield DA. Stimulation of Epstein-Barr virus-infected human B cell growth by physiological concentrations of 4-hydroxynonenal. Cell Biochem Funct 2006; 24: 147-152.
117. Mattson MP, Haddon RC, Rao AM. Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J Mol Neurosci 2000; 14: 175-182.
118. Mrakovcic L, Wildburger R, Jaganjac M, Cindric M, Cipak A, Borovic-Sunjic S, et al. Lipid peroxidation product 4-hydroxynonenal as factor of oxidative homeostasis supporting bone regeneration with bioactive glasses. Acta Biochim Pol 2010; 57: 173-178.
119. Gaetke L. Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 2003; 189: 147-163.
120. Milkovic L, Hoppe A, Detsch R, Boccaccini AR, Zarkovic N. Effects of Cu-doped 45S5 bioactive glass on the lipid peroxidation-associated growth of human osteoblast-like cells in vitro. J Biomed Mater Res A 2013; 102: 3556-3561.
121. Milkovic L, Siems W, Siems R, Zarkovic N. Oxidative stress and antioxidants in carcinogenesis and integrative therapy of cancer. Curr Pharm Des 2014; 20: 6529-6542.
122. Gago-Dominguez M, Jiang X, Castelao JE. Lipid peroxidation, oxidative stress genes and dietary factors in breast cancer protection: a hypothesis. Breast Cancer Res 2007; 9: 201.