Mitochondrial control of apoptosis through modulation of cardiolipin oxidation in hepatocellular carcinoma: A novel link between oxidative stress and cancer

Free Radical Biology and Medicine

Volumn 102, Issue , 2017, Pages 67-76

  Zhong, Huiqin ^a,b   Xiao, Mengqing ^a,b,h   Zarkovic, Kamelija ^c   Zhu, Mingjiang ^a   Sa, Rina ^a,b   Lu, Jianhong ^a,b   Tao, Yongzhen ^a   Chen, Qun ^a,b   Xia, Lin ^a   Cheng, Shuqun ^e   Waeg, Georg ^f   Zarkovic, Neven ^g   Yin, Huiyong ^a,b,d,h  

^a Chinese Academy of Sciences   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF ZAGREB   (Croatia)

^d BEIJING HOSPITAL   (China)

^e Eastern Hepatobiliary Surgery Hospital   (China)

^f UNIVERSITY OF GRAZ   (Austria)

^g RUDER BO KOVI INSTITUTE   (Croatia)

^h SHANGHAITECH UNIVERSITY   (China)

Author keywords

4 hydroxy 2 nonenal; Apoptosis; Cardiolipin; Hepatocellular carcinoma; Oxidative stress

Indexed keywords

13 HYDROXYOCTADECADIENOIC ACID CARDIOLIPIN; 4 HYDROXYNONENAL; CARDIOLIPIN; ELECTROPHILE; EPOXYALCOHOLALDEHYDE CARDIOLIPIN; GLYCEROPHOSPHOLIPID; SORAFENIB; STAUROSPORINE; TETRALINOLEOYLCARDIOLIPIN; UNCLASSIFIED DRUG; 4-HYDROXY-2-NONENAL; ALDEHYDE; LIPID; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CANCER GROWTH; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; LIPID METABOLISM; LIPID OXIDATION; LIPIDOMICS; LIVER CANCER CELL LINE; LIVER CELL CARCINOMA; MASS SPECTROMETRY; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; CHEMISTRY; GENETICS; LIPID PEROXIDATION; LIVER; LIVER TUMOR; METABOLISM; MITOCHONDRIAL MEMBRANE; OXIDATION REDUCTION REACTION; PATHOLOGY;

ALDEHYDES; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CARDIOLIPINS; HUMANS; LIPID PEROXIDATION; LIPIDS; LIVER; LIVER NEOPLASMS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84997327239     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.10.494     Document Type: Article

References (51)

1. [1] Harris IS, T.A., Inoue, S., Sasaki, M., et al. Glutathione and thioredoxin antioxidant pathways synergize to drive cancer initiation and progression. Cancer Cell 27 (2015), 211–222.
2. [2] Yin H, Z.M., Free radical oxidation of cardiolipin: chemical mechanisms, detection and implication in apoptosis, mitochondrial dysfunction and human disease. Free Radic. Res. 46 (2012), 959–974.
3. [3] Gonzalvez, E., F.G., Cardiolipin: setting the beat of apoptosis. Apoptosis 12:5 (2007), 877–885.
4. [4] Peyta, L., Jarnouen, K., Pinault, M., Guimaraes, C., Pais de Barros, J.-P., Chevalier, S., Dumas, J.-F., Maillot, F., Hatch, G.M., Loyer, P., Servais, S., Reduced cardiolipin content decreases respiratory chain capacities and increases ATP synthesis yield in the human HepaRG cells. Biochim. Biophys. Acta (BBA) – Bioenerg. 1857:4 (2016), 443–453.
5. [5] Peyta, L., Jarnouen, K., Pinault, M., Coulouarn, C., Guimaraes, C., Goupille, C., de Barros, J.-P.P., Chevalier, S., Dumas, J.-F., Maillot, F., Hatch, G.M., Loyer, P., Servais, S., Regulation of hepatic cardiolipin metabolism by TNFα: Implication in cancer cachexia. Biochim. Biophys. Acta (BBA) – Mol. Cell Biol. Lipids 1851:11 (2015), 1490–1500.
6. [6] Julienne, C.M., Tardieu, M., Chevalier, S., Pinault, M., Bougnoux, P., Labarthe, F., Couet, C., Servais, S., Dumas, J.F., Cardiolipin content is involved in liver mitochondrial energy wasting associated with cancer-induced cachexia without the involvement of adenine nucleotide translocase. Biochim. Biophys. Acta 1842:5 (2014), 726–733.
7. [7] Kiebish, M.A., Han, X., Cheng, H., Chuang, J.H., Seyfried, T.N., Cardiolipin and electron transport chain abnormalities in mouse brain tumor mitochondria: lipidomic evidence supporting the Warburg theory of cancer. J. Lipid Res. 49:12 (2008), 2545–2556.
8. [8] Kagan, V.E., Tyurin, V.A., Jiang, J., Tyurina, Y.Y., Ritov, V.B., Amoscato, A.A., Osipov, A.N., Belikova, N.A., Kapralov, A.A., Kini, V., Vlasova II, Zhao, Q., Zou, M., Di, P., Svistunenko, D.A., Kurnikov, I.V., Borisenko, G.G., Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 1:4 (2005), 223–232.
9. [9] Kagan, V.E., Bayir, H.A., Belikova, N.A., Kapralov, O., Tyurina, Y.Y., Tyurin, V.A., Jiang, J., Stoyanovsky, D.A., Wipf, P., Kochanek, P.M., Greenberger, J.S., Pitt, B., Shvedova, A.A., Borisenko, G., Cytochrome c/cardiolipin relations in mitochondria: a kiss of death. Free Radic. Biol. Med. 46:11 (2009), 1439–1453.
10. [10] Kagan, V.E., Chu, C.T., Tyurina, Y.Y., Cheikhi, A., Bayir, H., Cardiolipin asymmetry, oxidation and signaling. Chem. Phys. Lipids 179 (2014), 64–69.
11. [11] Kagan, V.E., Tyurina, Y.Y., Tyurin, V.A., Mohammadyani, D., Angeli, J.P., Baranov, S.V., Klein-Seetharaman, J., Friedlander, R.M., Mallampalli, R.K., Conrad, M., Bayir, H., Cardiolipin signaling mechanisms: collapse of asymmetry and oxidation. Antioxid. Redox Signal. 22:18 (2015), 1667–1680.
12. [12] Liu, W., Porter, N.A., Schneider, C., Brash, A.R., Yin, H., Formation of 4-hydroxynonenal from cardiolipin oxidation: Intramolecular peroxyl radical addition and decomposition. Free Radic. Biol. Med. 50:1 (2011), 166–178.
13. [13] Yin, H., Vergeade, A., Shi, Q., Zackert, W.E., Gruenberg, K.C., Bokiej, M., Amin, T., Ying, W., Masterson, T.S., Zinkel, S.S., Oates, J.A., Boutaud, O., Roberts, L.J. 2nd, Acetaminophen inhibits cytochrome c redox cycling induced lipid peroxidation. Biochem. Biophys. Res. Commun. 423:2 (2012), 224–228.
14. [14] 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. 2 (2014), 878–883.
15. [15] Marnett, J.D. Wa.L.J., Endogenous reactive intermediates as modulators of cell signaling and cell death. Chem. Res. Toxicol., 2006.
16. [16] Siems, W., Grune, T., Intracellular metabolism of 4-hydroxynonenal. Mol. Asp. Med. 24:4–5 (2003), 167–175.
17. [17] El-Serag, H.B., Rudolph, K.L., Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:7 (2007), 2557–2576.
18. [18] Portolani, N., Coniglio, A., Ghidoni, S., Giovanelli, M., Benetti, A., Tiberio, G.A., Giulini, S.M., Early and late recurrence after liver resection for hepatocellular carcinoma: prognostic and therapeutic implications. Ann. Surg. 243:2 (2006), 229–235.
19. [19] Chambers, A.F., Groom, A.C., MacDonald, I.C., Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2:8 (2002), 563–572.
20. [20] Christofk, H.R., Vander Heiden, M.G., Harris, M.H., Ramanathan, A., Gerszten, R.E., Wei, R., Fleming, M.D., Schreiber, S.L., Cantley, L.C., The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452:7184 (2008), 230–233.
21. [21] Furuta, E., Okuda, H., Kobayashi, A., Watabe, K., Metabolic genes in cancer: their roles in tumor progression and clinical implications. Biochim. Biophys. Acta 1805:2 (2010), 141–152.
22. [22] Huang, Q., Tan, Y., Yin, P., Ye, G., Gao, P., Lu, X., Wang, H., Xu, G., Metabolic characterization of hepatocellular carcinoma using nontargeted tissue metabolomics. Cancer Res. 73:16 (2013), 4992–5002.
23. [23] Allen, B.G., Bhatia, S.K., Buatti, J.M., Brandt, K.E., Lindholm, K.E., Button, A.M., Szweda, L.I., Smith, B.J., Spitz, D.R., Fath, M.A., Ketogenic diets enhance oxidative stress and radio-chemo-therapy responses in lung cancer xenografts. Clin. Cancer Res.: Off. J. Am. Assoc. Cancer Res. 19:14 (2013), 3905–3913.
24. [24] Baumgartner, M., Sturlan, S., Roth, E., Wessner, B., Bachleitner-Hofmann, T., Enhancement of arsenic trioxide-mediated apoptosis using docosahexaenoic acid in arsenic trioxide-resistant solid tumor cells. Int. J. Cancer 112:4 (2004), 707–712.
25. [25] Sovic, S., A.B., 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. 21 (2001), 1997–2004.
26. [26] K.J. Zarkovic, G., Waeg, G., Kolenc, D., Zarkovic, N., Immunohistochemical appearance of HNE-protein conjugates in human astrocytomas. Biofactors 24 (2005), 33–40.
27. [27] Han, X., Gross, R.W., Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom. Rev. 24:3 (2005), 367–412.
28. [28] Han, X., Yang, K., Yang, J., Cheng, H., Gross, R.W., Shotgun lipidomics of cardiolipin molecular species in lipid extracts of biological samples. J. Lipid Res. 47:4 (2006), 864–879.
29. [29] Colombini, M., Voltage gating in the mitochondrial channel, VDAC. J. Membr. Biol. 111 (1989), 103–111.
30. [30] Zhong, H., Yin, H., Role of lipid peroxidation derived 4-hydroxynonenal (4-HNE) in cancer: focusing on mitochondria. Redox Biol. 4 (2015), 193–199.
31. [31] Negre-Salvayre, N.A. Anne, Ayala, Victoria, Basaga, Huveyda, Boada, Jordi, Brenke, Rainer, et al. Pathological aspects of lipid peroxidation. Free Radic. Res. 44 (2010), 1125–1171.
32. [32] Zarkovic, N., 4-Hydroxynonenal as a bioactive marker of pathophysiological processes. Mol. Asp. Med. 24:4–5 (2003), 281–291.
33. [33] Llovet JM, R.S., Mazzaferro, V., Hilgard, P., Gane, E., Blanc, J.F., de Oliveira, A.C., Santoro, A., Raoul, J.L., Forner A, S.M., Porta, C., Zeuzem, S., Bolondi, L., Greten, T.F., Galle, P.R., Seitz, J.F., Borbath, I., Haussinger D, G.T., Shan, M., Moscovici, M., Voliotis, D., Bruix, J., Sorafenib in advanced hepatocellular carcinoma. N. Engl. J. Med. 359:4 (2008), 378–390.
34. [34] Fernando, J., Sancho, P., Fernandez-Rodriguez, C.M., Lledo, J.L., Caja, L., Campbell, J.S., Fausto, N., Fabregat, I., Sorafenib sensitizes hepatocellular carcinoma cells to physiological apoptotic stimuli. J. Cell. Physiol. 227:4 (2012), 1319–1325.
35. [35] D.a.W. Hanahan, R.A., The hallmarks of cancer. Cell 100 (2000), 57–70.
36. [36] Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E.S., Baehrecke, E.H., Blagosklonny, M.V., El-Deiry, W.S., Golstein, P., Green, D.R., Hengartner, M., Knight, R.A., Kumar, S., Lipton, S.A., Malorni, W., Nunez, G., Peter, M.E., Tschopp, J., Yuan, J., Piacentini, M., Zhivotovsky, B., Melino, D, G., Nomenclature committee on cell, classification of cell death: recommendations of the nomenclature committee on cell death 2009. Cell Death Differ. 16:1 (2009), 3–11.
37. [37] Green, D.R., Kroemer, G., The pathophysiology of mitochondrial cell death. Science 305 (2004), 626–629.
38. [38] Tyurina, Y.Y., Tungekar, M.A., Jung, M.Y., Tyurin, V.A., Greenberger, J.S., Stoyanovsky, D.A., Kagan, V.E., Mitochondria targeting of non-peroxidizable triphenylphosphonium conjugated oleic acid protects mouse embryonic cells against apoptosis: role of cardiolipin remodeling. FEBS Lett. 586:3 (2012), 235–241.
39. [39] Huang, Z., Jiang, J., Tyurin, V.A., Zhao, Q., Mnuskin, A., Ren, J., Belikova, N.A., Feng, W., Kurnikov, I.V., Kagan, V.E., Cardiolipin deficiency leads to decreased cardiolipin peroxidation and increased resistance of cells to apoptosis. Free Radic. Biol. Med. 44:11 (2008), 1935–1944.
40. [40] Asumendi, A., Morales, M.C., Alvarez, A., Arechaga, J., Perez-Yarza, G., Implication of mitochondria-derived ROS and cardiolipin peroxidation in N-(4-hydroxyphenyl)retinamide-induced apoptosis. Br. J. Cancer 86:12 (2002), 1951–1956.
41. [41] Barrera, G., Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol., 2012, 2012, 137289.
42. [42] Yin, H., Xu, L., Porter, N.A., Free radical lipid peroxidation: mechanisms and analysis. Chem.Rev. 111:10 (2011), 5944–5972.
43. [43] Zhao, Y., Miriyala, S., Miao, L., Mitov, M., Schnell, D., Dhar, S.K., Cai, J., Klein, J.B., Sultana, R., Butterfield, D.A., Vore, M., Batinic-Haberle, I., Bondada, S., Clair, D.K. St, Redox proteomic identification of HNE-bound mitochondrial proteins in cardiac tissues reveals a systemic effect on energy metabolism after doxorubicin treatment. Free Radic. Biol. Med. 72 (2014), 55–65.
44. [44] Poli, G., Schaur, R.J., Siems, W.G., Leonarduzzi, G., 4-hydroxynonenal: a membrane lipid oxidation product of medicinal interest. Med. Res. Rev. 28:4 (2008), 569–631.
45. [45] Awasthi, Y.C., Sharma, R., Sharma, A., Yadav, S., Singhal, S.S., Chaudhary, P., Awasthi, S., Self-regulatory role of 4-hydroxynonenal in signaling for stress-induced programmed cell death. Free Radic. Biol. Med. 45:2 (2008), 111–118.
46. [46] Hu, Z.F. Wenwei, Eveleigh, Jamie, Iyer, Ganesh, Pan, Jishen, Ami, Shantu, Chung, Fung-Lung, Tang, Moon-shong, The major lipid peroxidation product, trans- 4-hydroxy-2-nonenal,preferentially forms DNA adducts at codon 249 of humanp53 gene, a unique mutational hotspot in hepatocellular carcinoma. Carcinogenesis 23 (2002), 1781–1789.
47. [47] Schneider, C., Porter, N.A., Brash, A.R., Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. J. Biol. Chem. 283:23 (2008), 15539–15543.
48. [48] 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.
49. [49] Yang, Y.J., Baek, J.Y., Goo, J., Shin, Y., Park, J.K., Jang, J.Y., Wang, S.B., Jeong, W., Lee, H.J., Um, H.D., Lee, S.K., Choi, Y., Rhee, S.G., Chang, T.S., Effective killing of cancer cells through ROS-mediated mechanisms by AMRI-59 targeting peroxiredoxin I. Antioxid. Redox Signal. 24:8 (2016), 453–469.
50. [50] Coriat, R., Nicco, C., Chereau, C., Mir, O., Alexandre, J., Ropert, S., Weill, B., Chaussade, S., Goldwasser, F., Batteux, F., Sorafenib-induced hepatocellular carcinoma cell death depends on reactive oxygen species production in vitro and in vivo. Mol. Cancer Ther. 11:10 (2012), 2284–2293.
51. [51] Milder, J., Patel, M., Modulation of oxidative stress and mitochondrial function by the ketogenic diet. Epilepsy Res. 100:3 (2012), 295–303.