Cancer growth regulation by 4-hydroxynonenal

Free Radical Biology and Medicine

Volumn 111, Issue , 2017, Pages 226-234

  Gasparovic, Ana Cipak ^a   Milkovic, Lidija ^a   Sunjic, Suzana Borovic ^a   Zarkovic, Neven ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

Author keywords

4 Hydroxynonenal (HNE); Cancer; Cancer therapy; Carcinogenesis; Growth regulation; Lipid peroxidation; Oxidative stress; Pathophysiology; Signaling

Indexed keywords

4 HYDROXYNONENAL; ANTINEOPLASTIC AGENT; ANTIOXIDANT; LIPID; 4-HYDROXY-2-NONENAL; ABC TRANSPORTER; ALDEHYDE; CARDIOLIPIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NFE2L2 PROTEIN, HUMAN; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN P53; RALBP1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR NRF2;

CANCER CELL; CANCER CHEMOTHERAPY; CANCER CONTROL; CANCER GROWTH; CANCER RESISTANCE; CELL DIFFERENTIATION; DETOXIFICATION; GROWTH REGULATION; HUMAN; INFLAMMATION; LIPID PEROXIDATION; MALIGNANT NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANTAGONISTS AND INHIBITORS; CARCINOGENESIS; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; OXIDATION REDUCTION REACTION; PATHOLOGY; SIGNAL TRANSDUCTION;

ALDEHYDES; ATP-BINDING CASSETTE TRANSPORTERS; CARCINOGENESIS; CARDIOLIPINS; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GTPASE-ACTIVATING PROTEINS; HUMANS; NEOPLASMS; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OXIDATION-REDUCTION; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 85010931258     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2017.01.030     Document Type: Review

References (91)

1. Niki, E., Oxidative stress and antioxidants: distress or eustress?. Arch. Biochem. Biophys. 595 (2016), 19–24, 10.1016/j.abb.2015.11.017.
2. Panieri, E., Santoro, M.M., ROS homeostasis and metabolism: a dangerous liaison in cancer cells. Cell Death Dis., 7, 2016, e2253, 10.1038/cddis.2016.105.
3. Esterbauer, H., Schaur, R.J., Zollner, H., Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11 (1991), 81–128.
4. Schaur, R.J., Basic aspects of the biochemical reactivity of 4-hydroxynonenal. Mol. Asp. Med. 24 (2003), 149–159, 10.1016/S0098-2997(03)00009-8.
5. Schaur, R.J., Siems, W., Bresgen, N., Eckl, P.M., 4-Hydroxy-nonenal-A bioactive lipid peroxidation product. Biomolecules 5 (2015), 2247–2337, 10.3390/biom5042247.
6. Stossel, T.P., Mason, R.J., Smith, A.L., Lipid peroxidation by human blood phagocytes. J. Clin. Invest. 54 (1974), 638–645, 10.1172/JCI107801.
7. Esterbauer, H., Cytotoxicity and genotoxicity of lipid-oxidation products. Am. J. Clin. Nutr. 57 (1993), 779S–785S (discussion 785S–786S) 〈http://www.ncbi.nlm.nih.gov/pubmed/8475896〉.
8. Esterbauer, H., Schaur, R.J., Zollner, H., Review Article. Free Radic. Biol. Med 11 (1991), 81–128 〈http://www.sciencedirect.com/science/article/pii/0891584991901926〉 (accessed 20.03.13).
9. Dianzani, M.U., Barrera, G., Parola, M., 4-Hydroxy-2,3-nonenal as a signal for cell function and differentiation. Acta Biochim. Pol. 46 (1999), 61–75 〈http://www.ncbi.nlm.nih.gov/pubmed/10453982〉 (accessed 18.08.16).
10. Zarkovic, N., Ilic, Z., Jurin, M., Schaur, R.J., Puhl, H., Esterbauer, H., Stimulation of HeLa cell growth by physiological concentrations of 4-hydroxynonenal. Cell Biochem. Funct. 11 (1993), 279–286, 10.1002/cbf.290110409.
11. Milkovic, L., Cipak Gasparovic, A., Zarkovic, N., Overview on major lipid peroxidation bioactive factor 4-hydroxynonenal as pluripotent growth-regulating factor. Free Radic. Res. 49 (2015), 850–860, 10.3109/10715762.2014.999056.
12. Hanahan, D., Weinberg, R. a., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674, 10.1016/j.cell.2011.02.013.
13. Oberley, T.D., Toyokuni, S., Szweda, L.I., Localization of hydroxynonenal protein adducts in normal human kidney and selected human kidney cancers. Free Radic. Biol. Med. 27 (1999), 695–703 〈http://www.ncbi.nlm.nih.gov/pubmed/10490290〉 (accessed 19.08.16).
14. Biasi, F., Tessitore, L., Zanetti, D., Cutrin, J.C., Zingaro, B., Chiarpotto, E., Zarkovic, N., Serviddio, G., Poli, G., Associated changes of lipid peroxidation and transforming growth factor beta1 levels in human colon cancer during tumour progression. Gut 50 (2002), 361–367 〈http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1773152&tool=pmcentrez&rendertype=abstract〉 (accessed 25.09.14).
15. 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 95 (2009), 762–768 〈http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20210242〉.
16. Zarkovic, K., Juric, G., Waeg, G., Kolenc, D., Zarkovic, N., Immunohistochemical appearance of HNE-protein conjugates in human astrocytomas. Biofactors 24 (2005), 33–40 〈http://www.ncbi.nlm.nih.gov/pubmed/16403961〉 (accessed 24.09.14).
17. Yelisyeyeva, O., Cherkas, A., Zarkovic, K., Semen, K., Kaminskyy, D., Waeg, G., Zarkovic, N., The distribution of 4-hydroxynonenal-modified proteins in gastric mucosa of duodenal peptic ulcer patients. Free Radic. Res. 42 (2008), 205–211, 10.1080/10715760801975743.
18. Marquez-Quiñones, A., Cipak, A., Zarkovic, K., Fattel-Fazenda, S., Villa-Treviño, S., Waeg, G., Zarkovic, N., Guéraud, F., HNE-protein adducts formation in different pre-carcinogenic stages of hepatitis in LEC rats. Free Radic. Res. 44 (2010), 119–127 〈http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19886749〉.
19. Forman, H.J., Fukuto, J.M., 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. 477 (2008), 183–195, 10.1016/j.abb.2008.06.011.
20. Lushchak, V.I., Glutathione homeostasis and functions: potential targets for medical interventions. J. Amino Acids, 2012, 2012, 10.1155/2012/736837.
21. Awasthi, S., Singhal, S.S., Awasthi, Y.C., Martin, B., Woo, J.-H., Cunningham, C.C., Frankel, A.E., RLIP76 and cancer. Clin. Cancer Res. 14 (2008), 4372–4377, 10.1158/1078-0432.CCR-08-0145.
22. Baradat, M., Jouanin, I., Dalleau, S., Taché, S., Gieules, M., Debrauwer, L., Canlet, C., Huc, L., Dupuy, J., Pierre, F.H.F., Guéraud, F., 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. 24 (2011), 1984–1993, 10.1021/tx2003036.
23. Canuto, R.A., Muzio, G., Maggiora, M., Poli, G., Biasi, F., Dianzani, M.U., Ferro, M., Bassi, A.M., Penco, S., Marinari, U.M., Ability of different hepatoma cells to metabolize 4-hydroxynonenal. Cell Biochem. Funct. 11 (1993), 79–86, 10.1002/cbf.290110202.
24. Awasthi, Y.C., Sharma, R., Cheng, J.Z., Yang, Y., Sharma, A., Singhal, S.S., Awasthi, S., Role of 4-hydroxynonenal in stress-mediated apoptosis signaling. Mol. Asp. Med. 24 (2003), 219–230, 10.1016/S0098-2997(03)00017-7.
25. Barrera, G., Martinotti, S., Fazio, V., Manzari, V., Paradisi, L., Parola, M., Frati, L., Dianzani, M.U., Effect of 4-hydroxynonenal on c-myc expression. Toxicol. Pathol. 15 (1987), 238–240 〈http://www.ncbi.nlm.nih.gov/pubmed/3475758〉 (accessed 05.10.16).
26. Barrera, G., Di Mauro, C., Muraca, R., Ferrero, D., Cavalli, G., Fazio, V.M., Paradisi, L., Dianzani, M.U., Induction of differentiation in human HL-60 cells by 4-hydroxynonenal, a product of lipid peroxidation. Exp. Cell Res. 197 (1991), 148–152 〈http://www.ncbi.nlm.nih.gov/pubmed/1959552〉 (accessed 05.10.16).
27. Pizzimenti, S., Laurora, S., Briatore, F., Ferretti, C., Dianzani, M.U., Barrera, G., Synergistic effect of 4-hydroxynonenal and PPAR ligands in controlling human leukemic cell growth and differentiation. Free Radic. Biol. Med. 32 (2002), 233–245 〈http://www.ncbi.nlm.nih.gov/pubmed/11827749〉 (accessed 05.10.16).
28. Lowell, B.B., PPARgamma: an essential regulator of adipogenesis and modulator of fat cell function. Cell 99 (1999), 239–242 〈http://www.ncbi.nlm.nih.gov/pubmed/10555139〉 (accessed 11.10.16).
29. Cerbone, A., Toaldo, C., Laurora, S., Briatore, F., Pizzimenti, S., Dianzani, M.U., Ferretti, C., Barrera, G., 4-Hydroxynonenal and PPARgamma ligands affect proliferation, differentiation, and apoptosis in colon cancer cells. Free Radic. Biol. Med. 42 (2007), 1661–1670, 10.1016/j.freeradbiomed.2007.02.009.
30. Kliewer, S.A., Lenhard, J.M., Willson, T.M., Patel, I., Morris, D.C., Lehmann, J.M., A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 83 (1995), 813–819 〈http://www.ncbi.nlm.nih.gov/pubmed/8521498〉 (accessed 11.10.16).
31. Laurora, S., Tamagno, E., Briatore, F., Bardini, P., Pizzimenti, S., Toaldo, C., Reffo, P., Costelli, P., Dianzani, M.U., Danni, O., Barrera, G., 4-Hydroxynonenal modulation of p53 family gene expression in the SK-N-BE neuroblastoma cell line. Free Radic. Biol. Med. 38 (2005), 215–225, 10.1016/j.freeradbiomed.2004.10.014.
32. Rinaldi, M., Barrera, G., Aquino, A., Spinsanti, P., Pizzimenti, S., Farace, M.G., Dianzani, M.U., Fazio, V.M., 4-Hydroxynonenal-induced MEL cell differentiation involves PKC activity translocation. Biochem. Biophys. Res. Commun. 272 (2000), 75–80, 10.1006/bbrc.2000.2691.
33. Marinari, U.M., Nitti, M., Pronzato, M.A., Domenicotti, C., Role of PKC-dependent pathways in HNE-induced cell protein transport and secretion. Mol. Asp. Med. 24 (2003), 205–211, 10.1016/S0098-2997(03)00015-3.
34. Yu, Y.-H., Liao, P.-R., Guo, C.-J., Chen, C.-H., Mochly-Rosen, D., Chuang, L.-M., PKC-ALDH2 pathway plays a novel role in adipocyte differentiation. PLoS One, 11, 2016, e0161993, 10.1371/journal.pone.0161993.
35. Reuter, S., Gupta, S.C., Chaturvedi, M.M., Aggarwal, B.B., Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic. Biol. Med. 49 (2010), 1603–1616, 10.1016/j.freeradbiomed.2010.09.006.
36. Sunjic, S.B., 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 24 (2005), 141–148 〈http://www.ncbi.nlm.nih.gov/pubmed/16403974〉.
37. Semlitsch, T., Tillian, H.M., Zarkovic, N., Borovic, S., Purtscher, M., Hohenwarter, O., Schaur, R.J., Differential influence of the lipid peroxidation product 4-hydroxynonenal on the growth of human lymphatic leukaemia cells and human periopherial blood lymphocytes. Anticancer Res. 22 (2014), 1689–1697 〈http://www.ncbi.nlm.nih.gov/pubmed/12168855〉 (accessed 30.09.17).
38. Parola, M., Robino, G., Marra, F., Pinzani, M., Bellomo, G., Leonarduzzi, G., Chiarugi, P., Camandola, S., Poli, G., Waeg, G., Gentilini, P., Dianzani, M.U., HNE interacts directly with JNK isoforms in human hepatic stellate cells. J. Clin. Invest. 102 (1998), 1942–1950, 10.1172/JCI1413.
39. Kreuzer, T., Zarković, N., Grube, R., Schaur, R.J., Inhibition of HeLa cell proliferation by 4-hydroxynonenal is associated with enhanced expression of the c-fos oncogene. Cancer Biother. Radiopharm. 12 (1997), 131–136 〈http://www.ncbi.nlm.nih.gov/pubmed/10851457〉 (accessed 30.09.14).
40. 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. Commun. Free Radic. Res. 12 (2007), 50–54 〈http://www.ncbi.nlm.nih.gov/pubmed/17263909〉.
41. Dalleau, S., Baradat, M., Guéraud, F., Huc, L., Cell death and diseases related to oxidative stress: 4-hydroxynonenal (HNE) in the balance. Cell Death Differ. 20 (2013), 1615–1630, 10.1038/cdd.2013.138.
42. Zarkovic, N., Jörg 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. 16 (1994), 877–884, 10.1016/0891-5849(94)90208-9.
43. Kreuzer, T., Grube, R., Wutte, A., Zarkovic, N., Schaur, R.J., 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. 25 (1998), 42–49 〈http://www.ncbi.nlm.nih.gov/pubmed/9655520〉 (accessed 30.09.14).
44. Shearn, C.T., Reigan, P., Petersen, D.R., 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. 53 (2012), 1–11, 10.1016/j.freeradbiomed.2012.04.021.
45. Sovic, A., Borovic, S., Loncaric, I., Kreuzer, T., Zarkovic, K., Vukovic, T., Wäg, G., Hrascan, R., Wintersteiger, R., Klinger, R., Zurak, N., Schaub, R.J., Zarkovic, N., The carcinostatic and proapoptotic potential of 4-hydroxynonenal in HeLa cells is associated with its conjugation to cellular proteins. Anticancer Res. 21 (2014), 1997–2004 〈http://www.ncbi.nlm.nih.gov/pubmed/11497289〉 (accessed 30.09.17).
46. Bauer, G., Zarkovic, N., Revealing mechanisms of selective, concentration-dependent potentials of 4-hydroxy-2-nonenal to induce apoptosis in cancer cells through inactivation of membrane-associated catalase. Free Radic. Biol. Med. 81 (2015), 128–144, 10.1016/j.freeradbiomed.2015.01.010.
47. Jaganjac, M., Poljak-Blazi, M., Zarkovic, K., Schaur, R.J., Zarkovic, N., The involvement of granulocytes in spontaneous regression of Walker 256 carcinoma. Cancer Lett. 260 (2008), 180–186, 10.1016/j.canlet.2007.10.039.
48. Jaganjac, M., Poljak-Blazi, M., Kirac, I., Borovic, S., Joerg Schaur, R., Zarkovic, N., Granulocytes as effective anticancer agent in experimental solid tumor models. Immunobiology 215 (2010), 1015–1020, 10.1016/j.imbio.2010.01.002.
49. Jaganjac, M., Poljak-Blazi, M., Schaur, R.J., Zarkovic, K., Borovic, S., Cipak, a., Cindric, M., Uchida, K., Waeg, G., Zarkovic, N., Elevated neutrophil elastase and acrolein-protein adducts are associated with W256 regression. Clin. Exp. Immunol. 170 (2012), 178–185, 10.1111/j.1365-2249.2012.04639.x.
50. Maki, A., Kono, H., Gupta, M., Asakawa, M., Suzuki, T., Matsuda, M., Fujii, H., Rusyn, I., Predictive power of biomarkers of oxidative stress and inflammation in patients with hepatitis C virus-associated hepatocellular carcinoma. Ann. Surg. Oncol. 14 (2007), 1182–1190, 10.1245/s10434-006-9049-1.
51. Tammali, R., Ramana, K.V., Singhal, S.S., Awasthi, S., Srivastava, S.K., Aldose reductase regulates growth factor-induced cyclooxygenase-2 expression and prostaglandin E2 production in human colon cancer cells. Cancer Res., 66, 2006.
52. Ramana, K.V., Srivastava, S.K., Aldose reductase: a novel therapeutic target for inflammatory pathologies. Int. J. Biochem. Cell Biol. 42 (2010), 17–20, 10.1016/j.biocel.2009.09.009.
53. Biasi, F., Vizio, B., Mascia, C., Gaia, E., Zarkovic, N., Chiarpotto, E., Leonarduzzi, G., Poli, G., 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. 41 (2006), 443–454, 10.1016/j.freeradbiomed.2006.04.005.
54. Cipak, A., Mrakovcic, L., Ciz, M., Lojek, A., Mihaylova, B., Goshev, I., Jaganjac, M., Cindric, M., Sitic, S., Margaritoni, M., Waeg, G., Balic, M., Zarkovic, N., Growth suppression of human breast carcinoma stem cells by lipid peroxidation product 4-hydroxy-2-nonenal and hydroxyl radical-modified collagen. Acta Biochim. Pol. 57 (2010), 165–171 〈http://www.ncbi.nlm.nih.gov/pubmed/20559572〉.
55. Yadav, U.C.S., Ramana, K.V., Regulation of NF-κB-induced inflammatory signaling by lipid peroxidation-derived aldehydes. Oxid. Med. Cell. Longev., 2013, 2013, 10.1155/2013/690545.
56. Ghosh, S., May, M.J., Kopp, E.B., NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16 (1998), 225–260, 10.1146/annurev.immunol.16.1.225.
57. Wu, S., Flint, J.K., Rezvani, G., De Luca, F., Nuclear factor-kappaB p65 facilitates longitudinal bone growth by inducing growth plate chondrocyte proliferation and differentiation and by preventing apoptosis. J. Biol. Chem. 282 (2007), 33698–33706, 10.1074/jbc.M702991200.
58. Mudipalli, A., Li, Z., Hromchak, R., Bloch, A., NF-kappaB (p65/RelA) as a regulator of TNFalpha-mediated ML-1 cell differentiation. Leukemia 15 (2001), 808–813 〈http://www.ncbi.nlm.nih.gov/pubmed/11368442〉 (accessed 18.10.16).
59. Tharappel, J.C., Nalca, A., Owens, A.B., Ghabrial, L., Konz, E.C., Glauert, H.P., Spear, B.T., Cell proliferation and apoptosis are altered in mice deficient in the NF-kappaB p50 subunit after treatment with the peroxisome proliferator ciprofibrate. Toxicol. Sci. 75 (2003), 300–308, 10.1093/toxsci/kfg201.
60. Tong, X., Yin, L., Washington, R., Rosenberg, D.W., Giardina, C., The p50-p50 NF-kappaB complex as a stimulus-specific repressor of gene activation. Mol. Cell. Biochem. 265 (2004), 171–183 〈http://www.ncbi.nlm.nih.gov/pubmed/15543947〉 (accessed 18.10.16).
61. Hoesel, B., Schmid, J.A., The complexity of NF-κB signaling in inflammation and cancer. Mol. Cancer, 12, 2013, 86, 10.1186/1476-4598-12-86.
62. Ben-Neriah, Y., Karin, M., Inflammation meets cancer, with NF-κB as the matchmaker. Nat. Immunol. 12 (2011), 715–723, 10.1038/ni.2060.
63. Huber, M.A., Azoitei, N., Baumann, B., Grünert, S., Sommer, A., Pehamberger, H., Kraut, N., Beug, H., Wirth, T., NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J. Clin. Invest. 114 (2004), 569–581, 10.1172/JCI21358.
64. Ji, C., Kozak, K.R., Marnett, L.J., IkappaB kinase, a molecular target for inhibition by 4-hydroxy-2-nonenal. J. Biol. Chem. 276 (2001), 18223–18228, 10.1074/jbc.M101266200.
65. Taguchi, K., Motohashi, H., Yamamoto, M., Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16 (2011), 123–140, 10.1111/j.1365-2443.2010.01473.x.
66. Kansanen, E., Kuosmanen, S.M., Leinonen, H., Levonen, A.-L., The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox Biol. 1 (2013), 45–49, 10.1016/j.redox.2012.10.001.
67. Levonen, A.-L., Landar, A., Ramachandran, A., Ceaser, E.K., Dickinson, D. a., Zanoni, G., Morrow, J.D., Darley-Usmar, V.M., Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem. J. 378 (2004), 373–382, 10.1042/BJ20031049.
68. Numazawa, S., Ishikawa, M., Yoshida, A., Tanaka, S., Yoshida, T., Atypical protein kinase C mediates activation of NF-E2-related factor 2 in response to oxidative stress. Am. J. Physiol. Cell Physiol. 285 (2003), C334–C342, 10.1152/ajpcell.00043.2003.
69. Huang, Y., Li, W., Kong, A.-N.T., 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., 2, 2012, 40, 10.1186/2045-3701-2-40.
70. Pettazzoni, P., Ciamporcero, E., Medana, C., Pizzimenti, S., Dal Bello, F., Minero, V.G., Toaldo, C., Minelli, R., Uchida, K., Dianzani, M.U., Pili, R., Barrera, G., Nuclear factor erythroid 2-related factor-2 activity controls 4-hydroxynonenal metabolism and activity in prostate cancer cells. Free Radic. Biol. Med. 51 (2011), 1610–1618, 10.1016/j.freeradbiomed.2011.07.009.
71. Singh, A., Misra, V., Thimmulappa, R.K., Lee, H., Ames, S., Hoque, M.O., Herman, J.G., Baylin, S.B., Sidransky, D., Gabrielson, E., Brock, M.V., Biswal, S., Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med., 3, 2006, e420, 10.1371/journal.pmed.0030420.
72. Zhang, P., Singh, A., Yegnasubramanian, S., Esopi, D., Kombairaju, P., Bodas, M., Wu, H., Bova, S.G., Biswal, S., Loss of Kelch-like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol. Cancer Ther. 9 (2010), 336–346, 10.1158/1535-7163.MCT-09-0589.
73. Pizzimenti, S., Daga, M., Ciamporcero, E., Toaldo, C., Pettazzoni, P., Osella-Abate, S., Novelli, M., Minelli, R., Bisazza, A., Gamba, P., Testa, G., Ullio, C., Ferruti, P., Ranucci, E., Bernengo, M.G., Ferretti, C., Dianzani, C., Biasi, F., Barrera, G., Cavalli, R., Improved anti-tumoral therapeutic efficacy of 4-hydroxynonenal incorporated in novel lipid nanocapsules in 2D and 3D models. J. Biomed. Nanotechnol. 11 (2015), 2169–2185 〈http://www.ncbi.nlm.nih.gov/pubmed/26510311〉 (accessed 19.10.16).
74. Pizzimenti, S., Ciamporcero, E., Pettazzoni, P., Osella-Abate, S., Novelli, M., Toaldo, C., Husse, M., Daga, M., Minelli, R., Bisazza, A., Ferruti, P., Ranucci, E., Grazia Bernengo, M., Dianzani, C., Biasi, F., Cavalli, R., Barrera, G., The inclusion complex of 4-hydroxynonenal with a polymeric derivative of β-cyclodextrin enhances the antitumoral efficacy of the aldehyde in several tumor cell lines and in a three-dimensional human melanoma model. Free Radic. Biol. Med. 65 (2013), 765–777, 10.1016/j.freeradbiomed.2013.06.035.
75. Sharma, R., Sharma, A., Chaudhary, P., Sahu, M., Jaiswal, S., Awasthi, S., Awasthi, Y.C., Role of 4-hydroxynonenal in chemopreventive activities of sulforaphane. Free Radic. Biol. Med. 52 (2012), 2177–2185, 10.1016/j.freeradbiomed.2012.04.012.
76. Singhal, S.S., Awasthi, Y.C., Awasthi, S., Regression of melanoma in a murine model by RLIP76 depletion. Cancer Res. 66 (2006), 2354–2360, 10.1158/0008-5472.CAN-05-3534.
77. Awasthi, S., Singhal, S.S., Awasthi, Y.C., Martin, B., Woo, J.-H., Cunningham, C.C., Frankel, A.E., RLIP76 and cancer. Clin. Cancer Res. 14 (2008), 4372–4377, 10.1158/1078-0432.CCR-08-0145.
78. Singhal, S.S., Singhal, J., Yadav, S., Dwivedi, S., Boor, P.J., Awasthi, Y.C., Awasthi, S., Regression of lung and colon cancer xenografts by depleting or inhibiting RLIP76 (Ral-binding protein 1). Cancer Res. 67 (2007), 4382–4389, 10.1158/0008-5472.CAN-06-4124.
79. Singhal, S.S., Singhal, J., Yadav, S., Sahu, M., Awasthi, Y.C., Awasthi, S., RLIP76: a target for kidney cancer therapy. Cancer Res. 69 (2009), 4244–4251, 10.1158/0008-5472.CAN-08-3521.
80. Zhong, H., Yin, H., Role of lipid peroxidation derived 4-hydroxynonenal (4-HNE) in cancer: focusing on mitochondria. Redox Biol. 4 (2015), 193–199, 10.1016/j.redox.2014.12.011.
81. Negre-Salvayre, A., Auge, N., Ayala, V., Basaga, H., Boada, J., Brenke, R., Chapple, S., Cohen, G., Feher, J., Grune, T., Lengyel, G., Mann, G.E., Pamplona, R., Poli, G., Portero-Otin, M., Riahi, Y., Salvayre, R., Sasson, S., Serrano, J., Shamni, O., Siems, W., Siow, R.C.M., Wiswedel, I., Zarkovic, K., Zarkovic, N., Pathological aspects of lipid peroxidation. Free Radic. Res. 44 (2010), 1125–1171, 10.3109/10715762.2010.498478.
82. Li, Y.-P., Tian, F.-G., Shi, P.-C., Guo, L.-Y., Wu, H.-M., Chen, R.-Q., Xue, J.-M., 4-Hydroxynonenal promotes growth and angiogenesis of breast cancer cells through HIF-1α stabilization. Asian Pac. J. Cancer Prev. 15 (2014), 10151–10156 〈http://www.ncbi.nlm.nih.gov/pubmed/25556440〉 (accessed 12.10.16).
83. Zarkovic, K., Uchida, K., Kolenc, D., Hlupic, L., Zarkovic, N., Tissue distribution of lipid peroxidation product acrolein in human colon carcinogenesis. Free Radic. Res. 40 (2006), 543–552, 10.1080/10715760500370048.
84. Moniuszko-Malinowska, A., Łuczaj, W., Jarocka-Karpowicz, I., Pancewicz, S., Zajkowska, J., Andrisic, L., Zarkovic, N., Skrzydlewska, E., Lipid peroxidation in the pathogenesis of neuroborreliosis. Free Radic. Biol. Med. 96 (2016), 255–263, 10.1016/j.freeradbiomed.2016.04.032.
85. Piskač Živković, M., Petrovečki, N., Tomasović Lončarić, Č., Nikolić, I., Waeg, G., Žarković, K., Žarković, N., Comparison of PET/CT findings and 4-hydroxynonenal-specific immunohistochemistry reveal differential onset of lipid peroxidation in lung cancer and pulmonary metastasis of remote malignancies. Redox Biol., 2017 in press.
86. Jaganjac, M., Cipak, A., Schaur, R.J., Zarkovic, N., Pathophysiology of neutrophil-mediated extracellular redox reactions. (Landmark Ed) Front. Biosci. 21 (2016), 839–855 〈http://www.ncbi.nlm.nih.gov/pubmed/26709808〉 (accessed 04.11.16).
87. Zarković, N., Zarković, K., Schaur, R.J., Stolc, S., Schlag, G., Redl, H., Waeg, G., Borović, S., Loncarić, I., Jurić, G., Hlavka, V., 4-Hydroxynonenal as a second messenger of free radicals and growth modifying factor. Life Sci. 65 (1999), 1901–1904.
88. Zarkovic, K., 4-Hydroxynonenal and neurodegenerative diseases. Mol. Asp. Med. 24 (2003), 293–303, 10.1016/S0098-2997(03)00024-4.
89. 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. 53 (2012), 304–309 〈http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3428817&tool=pmcentrez&rendertype=abstract〉 (accessed 29.08.13).
90. Zhong, H., Xiao, M., Zarkovic, K., Zhu, M., Sa, R., Lu, J., Tao, Y., Chen, Q., Xia, L., Cheng, S., Waeg, G., Zarkovic, N., Huiyong, mitochondrial control of apoptosis through modulation of cardiolipin oxidation in hepatocellular carcinoma: a novel link between oxidative stress and cancer. Free Radic. Biol. Med. 176 (2017), 67–76.
91. Mouthuy, P., Snelling, S., Dakin, S., Milkovic, L., Cipak Gasparovic, A., Carr, A., Zarkovic, N., Biocompatibility of implantable materials: an oxidative stress viewpoint. Biomaterials 109 (2016), 55–68.