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Front. Biol.    2014, Vol. 9 Issue (6) : 423-436    https://doi.org/10.1007/s11515-014-1332-0
REVIEW
Functional implications of mitochondrial reactive oxygen species generated by oncogenic viruses
Young Bong CHOI(),Edward William HARHAJ()
Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins School of Medicine, Baltimore, MD 21287, USA
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Abstract

Between 15% and 20% of human cancers are associated with infection by oncogenic viruses. Oncogenic viruses, including HPV, HBV, HCV and HTLV-1, target mitochondria to influence cell proliferation and survival. Oncogenic viral gene products also trigger the production of reactive oxygen species which can elicit oxidative DNA damage and potentiate oncogenic host signaling pathways. Viral oncogenes may also subvert mitochondria quality control mechanisms such as mitophagy and metabolic adaptation pathways to promote virus replication. Here, we will review recent progress on viral regulation of mitophagy and metabolic adaptation and their roles in viral oncogenesis.
Keywords mitochondria      mitophagy      virus      ROS      oncogenes     
Corresponding Author(s): Young Bong CHOI   
Just Accepted Date: 12 September 2014   Online First Date: 28 October 2014    Issue Date: 13 January 2015
 Cite this article:   
Young Bong CHOI,Edward William HARHAJ. Functional implications of mitochondrial reactive oxygen species generated by oncogenic viruses[J]. Front. Biol., 2014, 9(6): 423-436.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-014-1332-0
https://academic.hep.com.cn/fib/EN/Y2014/V9/I6/423
Fig.1  Regulation of ROS homeostasis by mitophagy and metabolic adaptation. Mitochondrial ROS induced by virus infection can lead to mitochondrial dysfunction or damage. Accumulation of damaged mitochondria generates excessive mROS, which promotes oxidative stress, DNA damage and cell death. To mitigate the harmful effects of mROS and reduce mROS levels, cells induce mitophagy, by which damaged mitochondria are cleared, via the PINK1/Parkin complex (Youle and Narendra, 2011; Novak, 2012) and presumably HIF-1 activation of mitophagy receptors NIX and BINP3 or FUNDC1 (Ding and Yin, 2012). PINK1 phosphorylates ubiquitin (Ub) to activate Parkin (Koyano et al., 2014; Kane et al., 2014), which in turn induces the ubiquitination of mitochondrial proteins. The p62/SQSTM1 adaptor links the ubiquitinated mitochondria to the Atg8 family proteins (LC3/GABARAP) essential for the autophagosome maturation. Also, HIF-1 promotes metabolic adaptation (aerobic glycolysis) via the activation of PDK1 and LDHA (Kim et al., 2006; Cuninghame et al., 2014) to bypass mitochondrial oxidative phosphorylation generating mROS or presumably generate ATP in cells actively undergoing mitophagy or containing a few mitochondria.
Fig.2  Possible role of HBV HBx-induced mROS in mitophagy and metabolic adaptation. HBV infection induces the production of mROS via its gene product HBx and regulates mitophagy. The anti-apoptotic role of HBx may be dependent on the ability of HBx to eliminate damaged mitochondria via mitophagy. HBx, presumably the anti-apoptotic form phosphorylated by Akt (Lee et al., 2012b), can upregulate the expression of mitophagic proteins including PINK1, Parkin, Beclin, LC3 and also induce the phosphorylation of Drp1 to promote mitophagy (Kim et al., 2013b). However, the functional significance of HBx activation of HIF-1 is largely unknown.
Fig.3  Possible role of HCV core-induced mROS in mitophagy and metabolic adaptation. HCV infection promotes mROS production mainly via its gene product core, and regulates mitophagy through the upregulation of PINK1 and Parkin (Kim et al., 2013c). However, there is no direct evidence that HCV core regulates mitophagy although it upregulates LC3B and Atg5 through ER-stress-induced signaling (Wang et al., 2014). HCV core activates and stabilizes HIF-1 by ROS or several cellular signaling pathways such as NF-κB, STAT3, Akt and Erk and then promotes metabolic adaptation (Ivanov et al., 2013).
Fig.4  HPV-18 E2 regulates ROS production. High-risk HPV-18 E2 localizes to mitochondria and induces ROS that stabilizes HIF-1, which in turn activates PDK1 and CAIX enzymes to promote aerobic glycolysis (Lai et al., 2013). HPV can also promote aerobic glycolysis by inhibition of gC1qR through E6 and E7 (Gao et al., 2011). There is no evidence that HPV infection and its gene products including E2, E6, and E7 induce mitophagy.
Fig.5  HTLV-1 p13 and Tax proteins regulate ROS production. HTLV-1 p13 localizes in the mitochondria and induces an inward K+ current that triggers mitochondrial depolarization, an increase in respiratory chain activation and ROS production (Silic-Benussi et al., 2009; Biasiotto et al., 2010). HTLV-1 Tax increases ROS production via CREB and NF-κB activation, interaction with USP10 (Takahashi et al., 2013) and/or localization in mitochondria. Increased ROS by p13 and Tax results in increased DNA damage, senescence and possibly cell death.
1 Adinolfi L E, Restivo L, Zampino R, Lonardo A, Loria P (2011). Metabolic alterations and chronic hepatitis C: treatment strategies. Expert Opin Pharmacother, 12(14): 2215–2234
https://doi.org/10.1517/14656566.2011.597742 pmid: 21883025
2 Anupam R, Doueiri R, Green P L (2013). The need to accessorize: molecular roles of HTLV-1 p30 and HTLV-2 p28 accessory proteins in the viral life cycle. Front Microbiol, 4: 275
https://doi.org/10.3389/fmicb.2013.00275 pmid: 24062732
3 Arrese M, Riquelme A, Soza A (2010). Insulin resistance, hepatic steatosis and hepatitis C: a complex relationship with relevant clinical implications. Ann Hepatol, 9(Suppl.): 112–118
pmid: 20714007
4 Ashfaq U A, Javed T, Rehman S, Nawaz Z, Riazuddin S (2011). An overview of HCV molecular biology, replication and immune responses. Virol J, 8(1): 161–171
https://doi.org/10.1186/1743-422X-8-161 pmid: 21477382
5 Babusikova E, Evinova A, Hatok J (2013). Oxidative changes and possible effects of polymorphism of antioxidant enzymes in neurodegenerative disease. In Tech, Chapter 18: 421–455
6 Bai X T, Nicot C (2012). Overview on HTLV-1 p12, p8, p30, p13: accomplices in persistent infection and viral pathogenesis. Front Microbiol, 3: 400
https://doi.org/10.3389/fmicb.2012.00400 pmid: 23248621
7 Bai X T, Sinha-Datta U, Ko N L, Bellon M, Nicot C (2012). Nuclear export and expression of human T-cell leukemia virus type 1 tax/rex mRNA are RxRE/Rex dependent. J Virol, 86(8): 4559–4565
https://doi.org/10.1128/JVI.06361-11 pmid: 22318152
8 Bellanger S, Tan C L, Xue Y Z, Teissier S, Thierry F (2011). Tumor suppressor or oncogene? A critical role of the human papillomavirus (HPV) E2 protein in cervical cancer progression. Am J Cancer Res, 1(3): 373–389
pmid: 21968515
9 Benali-Furet N L, Chami M, Houel L, De Giorgi F, Vernejoul F, Lagorce D, Buscail L, Bartenschlager R, Ichas F, Rizzuto R, Paterlini-Bréchot P (2005). Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene, 24(31): 4921–4933
https://doi.org/10.1038/sj.onc.1208673 pmid: 15897896
10 Bernard B A, Bailly C, Lenoir M C, Darmon M, Thierry F, Yaniv M (1989). The human papillomavirus type 18 (HPV18) E2 gene product is a repressor of the HPV18 regulatory region in human keratinocytes. J Virol, 63(10): 4317–4324
pmid: 2476572
11 Bernard J J, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J, Borkowski A W, Martinez L, Greidinger E L, Yu B D, Gallo R L (2012). Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med, 18(8): 1286–1290
https://doi.org/10.1038/nm.2861 pmid: 22772463
12 Biasiotto R, Aguiari P, Rizzuto R, Pinton P, D’Agostino D M, Ciminale V (2010). The p13 protein of human T cell leukemia virus type 1 (HTLV-1) modulates mitochondrial membrane potential and calcium uptake. Biochim Biophys Acta, 1797(6-7): 945–951
https://doi.org/10.1016/j.bbabio.2010.02.023 pmid: 20188695
13 Bonekamp N A, V?lkl A, Fahimi H D, Schrader M (2009). Reactive oxygen species and peroxisomes: struggling for balance. Biofactors, 35(4): 346–355
https://doi.org/10.1002/biof.48 pmid: 19459143
14 Brieger K, Schiavone S, Miller F J Jr, Krause K H (2012). Reactive oxygen species: from health to disease. Swiss Med Wkly, 142: w13659
https://doi.org/10.4414/smw.2012.13659 pmid: 22903797
15 Bruick R K (2000). Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci USA, 97(16): 9082–9087
https://doi.org/10.1073/pnas.97.16.9082 pmid: 10922063
16 Burzio V A, Villota C, Villegas J, Landerer E, Boccardo E, Villa L L, Martínez R, Lopez C, Gaete F, Toro V, Rodriguez X, Burzio L O (2009). Expression of a family of noncoding mitochondrial RNAs distinguishes normal from cancer cells. Proc Natl Acad Sci USA, 106(23): 9430–9434
https://doi.org/10.1073/pnas.0903086106 pmid: 19470459
17 Carbone A, Gloghini A (2008). KSHV/HHV8-associated lymphomas. Br J Haematol, 140(1): 13–24
https://doi.org/10.1111/j.1365-2141.2007.06879.x pmid: 17991301
18 Chandel N S, Maltepe E, Goldwasser E, Mathieu C E, Simon M C, Schumacker P T (1998). Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA, 95(20): 11715–11720
https://doi.org/10.1073/pnas.95.20.11715 pmid: 9751731
19 Chatterjee A, Dasgupta S, Sidransky D (2011). Mitochondrial subversion in cancer. Cancer Prev Res (Phila), 4(5): 638–654
https://doi.org/10.1158/1940-6207.CAPR-10-0326 pmid: 21543342
20 Chen D, Gao F, Li B, Wang H, Xu Y, Zhu C, Wang G (2010). Parkin mono-ubiquitinates Bcl-2 and regulates autophagy. J Biol Chem, 285(49): 38214–38223
https://doi.org/10.1074/jbc.M110.101469 pmid: 20889974
21 Clippinger A J, Bouchard M J (2008). Hepatitis B virus HBx protein localizes to mitochondria in primary rat hepatocytes and modulates mitochondrial membrane potential. J Virol, 82(14): 6798–6811
https://doi.org/10.1128/JVI.00154-08 pmid: 18448529
22 Cooke M S, Evans M D, Dizdaroglu M, Lunec J (2003). Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J, 17(10): 1195–1214
https://doi.org/10.1096/fj.02-0752rev pmid: 12832285
23 Cuezva J M, Krajewska M, de Heredia M L, Krajewski S, Santamaría G, Kim H, Zapata J M, Marusawa H, Chamorro M, Reed J C (2002). The bioenergetic signature of cancer: a marker of tumor progression. Cancer Res, 62(22): 6674–6681
pmid: 12438266
24 Cuninghame S, Jackson R, Zehbe I (2014). Hypoxia-inducible factor 1 and its role in viral carcinogenesis. Virology, 456–457: 370–383
https://doi.org/10.1016/j.virol.2014.02.027 pmid: 24698149
25 D’Agostino D, Bernardi P, Chieco-Bianchi L, Ciminale V (2005). Mitochondria as functional targets of proteins coded by human tumor viruses. Adv Cancer Res, 94: 87–142
https://doi.org/10.1016/S0065-230X(04)94003-1
26 Danos O, Katinka M, Yaniv M (1982). Human papillomavirus 1a complete DNA sequence?: genome organization among Papovaviridae novel type of. EMBO J, 1: 231–236
pmid: 6325156
27 Dayaram T, Marriott S J (2008). Effect of transforming viruses on molecular mechanisms associated with cancer. J Cell Physiol, 216(2): 309–314
https://doi.org/10.1002/jcp.21439 pmid: 18366075
28 Demple B, Harrison L (1994). Repair of oxidative damage to DNA: enzymology and biology. Annu Rev Biochem, 63(1): 915–948
https://doi.org/10.1146/annurev.bi.63.070194.004411 pmid: 7979257
29 Ding W X, Yin X M (2012). Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol Chem, 393(7): 547–564
https://doi.org/10.1515/hsz-2012-0119 pmid: 22944659
30 Dizdaroglu M (1992). Oxidative damage to DNA in mammalian chromatin. Mutat Res, 275(3–6): 331–342
https://doi.org/10.1016/0921-8734(92)90036-O pmid: 1383774
31 Fader C M, Colombo M I (2006). Multivesicular bodies and autophagy in erythrocyte maturation. Autophagy, 2(2): 122–125
pmid: 16874060
32 Fantin V R, St-Pierre J, Leder P (2006). Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell, 9(6): 425–434
https://doi.org/10.1016/j.ccr.2006.04.023 pmid: 16766262
33 Feitelson M A, Bonamassa B, Arzumanyan A (2014). The roles of hepatitis B virus-encoded X protein in virus replication and the pathogenesis of chronic liver disease. Expert Opin Ther Targets, 18(3): 293–306
https://doi.org/10.1517/14728222.2014.867947 pmid: 24387282
34 Feng D, Liu L, Zhu Y, Chen Q (2013). Molecular signaling toward mitophagy and its physiological significance. Exp Cell Res, 319(12): 1697–1705
https://doi.org/10.1016/j.yexcr.2013.03.034 pmid: 23603281
35 Feng H, Shuda M, Chang Y, Moore P S (2008). Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science, 319(5866): 1096–1100
https://doi.org/10.1126/science.1152586 pmid: 18202256
36 Fogal V, Richardson A D, Karmali P P, Scheffler I E, Smith J W, Ruoslahti E (2010). Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Mol Cell Biol, 30(6): 1303–1318
https://doi.org/10.1128/MCB.01101-09 pmid: 20100866
37 Francis D A, Schmid S I, Howley P M (2000). Repression of the integrated papillomavirus E6/E7 promoter is required for growth suppression of cervical cancer cells. J Virol, 74(6): 2679–2686
https://doi.org/10.1128/JVI.74.6.2679-2686.2000 pmid: 10684283
38 Gabriela A, Adriana P, Coralia B, Anca B, Mariana A, Lorelei I B, Mihai S (2013). Human Papillomaviruses Oncoproteins. InTech, Chapter 8: 183–206
39 Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G (2008). Viral control of mitochondrial apoptosis. PLoS Pathog, 4(5): e1000018
https://doi.org/10.1371/journal.ppat.1000018 pmid: 18516228
40 Ganem D (2006). KSHV infection and the pathogenesis of Kaposi’s sarcoma. Annu Rev Pathol, 1(1): 273–296
https://doi.org/10.1146/annurev.pathol.1.110304.100133 pmid: 18039116
41 Gao L, Harhaj E W (2013). HSP90 protects the human T-cell leukemia virus type 1 (HTLV-1) tax oncoprotein from proteasomal degradation to support NF-κB activation and HTLV-1 replication. J Virol, 87(24): 13640–13654
https://doi.org/10.1128/JVI.02006-13 pmid: 24109220
42 Gao L J, Gu P Q, Fan W M, Liu Z, Qiu F, Peng Y Z, Guo X R (2011). The role of gC1qR in regulating survival of human papillomavirus 16 oncogene-transfected cervical cancer cells. Int J Oncol, 39(5): 1265–1272
https://doi.org/10.3892/ijo.2011.1108 pmid: 21725590
43 Geisler S, Holmstr?m K M, Skujat D, Fiesel F C, Rothfuss O C, Kahle P J, Springer W (2010). PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol, 12(2): 119–131
https://doi.org/10.1038/ncb2012 pmid: 20098416
44 Gravitz L (2011). Introduction: a smouldering public-health crisis. Nature, 474(7350): S2–S4
https://doi.org/10.1038/474S2a pmid: 21666731
45 Greene A W, Grenier K, Aguileta M A, Muise S, Farazifard R, Haque M E, McBride H M, Park D S, Fon E A (2012). Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep, 13(4): 378–385
https://doi.org/10.1038/embor.2012.14 pmid: 22354088
46 Gruhne B, Sompallae R, Marescotti D, Kamranvar S A, Gastaldello S, Masucci M G (2009). The Epstein-Barr virus nuclear antigen-1 promotes genomic instability via induction of reactive oxygen species. Proc Natl Acad Sci USA, 106(7): 2313–2318
https://doi.org/10.1073/pnas.0810619106 pmid: 19139406
47 Guzy R D, Hoyos B, Robin E, Chen H, Liu L, Mansfield K D, Simon M C, Hammerling U, Schumacker P T (2005). Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab, 1(6): 401–408
https://doi.org/10.1016/j.cmet.2005.05.001 pmid: 16054089
48 Ha H L, Yu D Y (2010). HBx-induced reactive oxygen species activates hepatocellular carcinogenesis via dysregulation of PTEN/Akt pathway. World J Gastroenterol, 16(39): 4932–4937
https://doi.org/10.3748/wjg.v16.i39.4932 pmid: 20954279
49 H?gg M, Wennstr?m S (2005). Activation of hypoxia-induced transcription in normoxia. Exp Cell Res, 306(1): 180–191
https://doi.org/10.1016/j.yexcr.2005.01.017 pmid: 15878343
50 Hamanaka R B, Chandel N S (2009). Mitochondrial reactive oxygen species regulate hypoxic signaling. Curr Opin Cell Biol, 21(6): 894–899
https://doi.org/10.1016/j.ceb.2009.08.005 pmid: 19781926
51 Harrod R, Tang Y, Nicot C, Lu H S, Vassilev A, Nakatani Y, Giam C Z (1998). An exposed KID-like domain in human T-cell lymphotropic virus type 1 Tax is responsible for the recruitment of coactivators CBP/p300. Mol Cell Biol, 18(9): 5052–5061
pmid: 9710589
52 Hartridge-Lambert S K, Stein E M, Markowitz A J, Portlock C S (2012). Hepatitis C and non-Hodgkin lymphoma: the clinical perspective. Hepatology, 55(2): 634–641
https://doi.org/10.1002/hep.25499 pmid: 22120959
53 Henkler F, Hoare J, Waseem N, Goldin R D, McGarvey M J, Koshy R, King I A (2001). Intracellular localization of the hepatitis B virus HBx protein. J Gen Virol, 82(4): 871–882
pmid: 11257193
54 Hirsil? M, Koivunen P, Günzler V, Kivirikko K I, Myllyharju J (2003). Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem, 278(33): 30772–30780
https://doi.org/10.1074/jbc.M304982200 pmid: 12788921
55 Hsu P P, Sabatini D M (2008). Cancer cell metabolism: Warburg and beyond. Cell, 134(5): 703–707
https://doi.org/10.1016/j.cell.2008.08.021 pmid: 18775299
56 Huang C, Andres A M, Ratliff E P, Hernandez G, Lee P, Gottlieb R A (2011). Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS ONE, 6(6): e20975
https://doi.org/10.1371/journal.pone.0020975 pmid: 21687634
57 Huh K W, Siddiqui A (2002). Characterization of the mitochondrial association of hepatitis B virus X protein, HBx. Mitochondrion, 1(4): 349–359
https://doi.org/10.1016/S1567-7249(01)00040-X pmid: 16120289
58 Ivanov A V, Bartosch B, Smirnova O A, Isaguliants M G, Kochetkov S N (2013). HCV and oxidative stress in the liver. Viruses, 5(2): 439–469
https://doi.org/10.3390/v5020439 pmid: 23358390
59 Jin D Y (2007). Molecular pathogenesis of hepatitis C virus-associated hepatocellular carcinoma. Front Biosci, 12(1): 222–233
https://doi.org/10.2741/2060 pmid: 17127295
60 Jin S M, Lazarou M, Wang C, Kane L A, Narendra D P, Youle R J (2010). Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol, 191(5): 933–942
https://doi.org/10.1083/jcb.201008084 pmid: 21115803
61 Jin S M, Youle R J (2012). PINK1- and Parkin-mediated mitophagy at a glance. J Cell Sci, 125(4): 795–799
https://doi.org/10.1242/jcs.093849 pmid: 22448035
62 Jung S Y, Kim Y J (2013). C-terminal region of HBx is crucial for mitochondrial DNA damage. Cancer Lett, 331(1): 76–83
https://doi.org/10.1016/j.canlet.2012.12.004 pmid: 23246371
63 Kane L A, Lazarou M, Fogel A I, Li Y, Yamano K, Sarraf S A, Banerjee S, Youle R J (2014). PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol, 205(2): 143–153
https://doi.org/10.1083/jcb.201402104 pmid: 24751536
64 Kato N (2000). Genome of human hepatitis C virus (HCV): gene organization, sequence diversity, and variation. Microb Comp Genomics, 5(3): 129–151
https://doi.org/10.1089/omi.1.2000.5.129 pmid: 11252351
65 Kim J W, Tchernyshyov I, Semenza G L, Dang C V (2006). HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab, 3(3): 177–185
https://doi.org/10.1016/j.cmet.2006.02.002 pmid: 16517405
66 Kim S, Kim H Y, Lee S, Kim S W, Sohn S, Kim K, Cho H (2007). Hepatitis B virus X protein induces perinuclear mitochondrial clustering in microtubule- and dynein-dependent manners. J Virol, 81(4): 1714–1726
https://doi.org/10.1128/JVI.01863-06 pmid: 17151129
67 Kim S J, Khan M, Quan J, Till A, Subramani S, Siddiqui A (2013a). Hepatitis B virus disrupts mitochondrial dynamics: induces fission and mitophagy to attenuate apoptosis. PLoS Pathog, 9(12): e1003722
https://doi.org/10.1371/journal.ppat.1003722 pmid: 24339771
68 Kim S J, Khan M, Quan J, Till A, Subramani S, Siddiqui A (2013b). Hepatitis B virus disrupts mitochondrial dynamics: induces fission and mitophagy to attenuate apoptosis. PLoS Pathog, 9(12): e1003722
https://doi.org/10.1371/journal.ppat.1003722 pmid: 24339771
69 Kim S J, Syed G H, Siddiqui A (2013c). Hepatitis C virus induces the mitochondrial translocation of Parkin and subsequent mitophagy. PLoS Pathog, 9(3): e1003285
https://doi.org/10.1371/journal.ppat.1003285 pmid: 23555273
70 Kinjo T, Ham-Terhune J, Peloponese J M Jr, Jeang K T (2010). Induction of reactive oxygen species by human T-cell leukemia virus type 1 tax correlates with DNA damage and expression of cellular senescence marker. J Virol, 84(10): 5431–5437
https://doi.org/10.1128/JVI.02460-09 pmid: 20219913
71 Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N (1998). Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature, 392(6676): 605–608
https://doi.org/10.1038/33416 pmid: 9560156
72 Koike K (2009). Hepatitis B virus X gene is implicated in liver carcinogenesis. Cancer Lett, 286(1): 60–68
https://doi.org/10.1016/j.canlet.2009.04.010 pmid: 19464104
73 Korenaga M, Wang T, Li Y, Showalter L A, Chan T, Sun J, Weinman S A (2005). Hepatitis C virus core protein inhibits mitochondrial electron transport and increases reactive oxygen species (ROS) production. J Biol Chem, 280(45): 37481–37488
https://doi.org/10.1074/jbc.M506412200 pmid: 16150732
74 Koyano F, Okatsu K, Kosako H, Tamura Y, Go E, Kimura M, Kimura Y, Tsuchiya H, Yoshihara H, Hirokawa T, Endo T, Fon E A, Trempe J F, Saeki Y, Tanaka K, Matsuda N (2014). Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature, 510(7503): 162–166
pmid: 24784582
75 Kroemer G (2006). Mitochondria in cancer. Oncogene, 25(34): 4630–4632
https://doi.org/10.1038/sj.onc.1209589 pmid: 16892077
76 Lai D, Tan C L, Gunaratne J, Quek L S, Nei W, Thierry F, Bellanger S (2013). Localization of HPV-18 E2 at mitochondrial membranes induces ROS release and modulates host cell metabolism. PLoS ONE, 8(9): e75625
https://doi.org/10.1371/journal.pone.0075625 pmid: 24086592
77 LaJeunesse D R, Brooks K, Adamson A L (2005). Epstein-Barr virus immediate-early proteins BZLF1 and BRLF1 alter mitochondrial morphology during lytic replication. Biochem Biophys Res Commun, 333(2): 438–442
https://doi.org/10.1016/j.bbrc.2005.05.120 pmid: 15950179
78 Lee J, Giordano S, Zhang J (2012a). Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J, 441(2): 523–540
https://doi.org/10.1042/BJ20111451 pmid: 22187934
79 Lee W P, Lan K H, Li C P, Chao Y, Lin H C, Lee S D (2012b). Pro-apoptotic or anti-apoptotic property of X protein of hepatitis B virus is determined by phosphorylation at Ser31 by Akt. Arch Biochem Biophys, 528(2): 156–162
https://doi.org/10.1016/j.abb.2012.08.008 pmid: 22982405
80 Lee Y I, Hwang J M, Im J H, Lee Y I, Kim N S, Kim D G, Yu D Y, Moon H B, Park S K (2004). Human hepatitis B virus-X protein alters mitochondrial function and physiology in human liver cells. J Biol Chem, 279(15): 15460–15471
https://doi.org/10.1074/jbc.M309280200 pmid: 14724286
81 Li S K, Ho S F, Tsui K W, Fung K P, Waye M Y M (2008). Identification of functionally important amino acid residues in the mitochondria targeting sequence of hepatitis B virus X protein. Virology, 381(1): 81–88
https://doi.org/10.1016/j.virol.2008.07.037 pmid: 18805561
82 Li W, Zhang X, Zhuang H, Chen H G, Chen Y, Tian W, Wu W, Li Y, Wang S, Zhang L, Chen Y, Li L, Zhao B, Sui S, Hu Z, Feng D (2014). MicroRNA-137 is a novel hypoxia-responsive microRNA that inhibits mitophagy via regulation of two mitophagy receptors FUNDC1 and NIX. J Biol Chem, 289(15): 10691–10701
https://doi.org/10.1074/jbc.M113.537050 pmid: 24573672
83 Li X, Fang P, Mai J, Choi E T, Wang H, Yang X F (2013). Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J Hematol Oncol, 6(1): 19
https://doi.org/10.1186/1756-8722-6-19 pmid: 23442817
84 Li Y, Boehning D F, Qian T, Popov V L, Weinman S A (2007). Hepatitis C virus core protein increases mitochondrial ROS production by stimulation of Ca2+ uniporter activity. FASEB J, 21(10): 2474–2485
https://doi.org/10.1096/fj.06-7345com pmid: 17392480
85 Li Y P, Schwartz R J, Waddell I D, Holloway B R, Reid M B (1998). Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kappaB activation in response to tumor necrosis factor alpha. FASEB J, 12(10): 871–880
pmid: 9657527
86 Liu L, Feng D, Chen G, Chen M, Zheng Q, Song P, Ma Q, Zhu C, Wang R, Qi W, Huang L, Xue P, Li B, Wang X, Jin H, Wang J, Yang F, Liu P, Zhu Y, Sui S, Chen Q (2012). Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol, 14(2): 177–185
https://doi.org/10.1038/ncb2422 pmid: 22267086
87 Liu L P, Hu B G, Ye C, Ho R L K, Chen G G, Lai P B S (2014). HBx mutants differentially affect the activation of hypoxia-inducible factor-1α in hepatocellular carcinoma. Br J Cancer, 110(4): 1066–1073
https://doi.org/10.1038/bjc.2013.787 pmid: 24346287
88 Liu X H, Zhou X, Zhu C L, Song H, Liu F (2011). Effects of HCV core protein on the expression of hypoxia-inducible factor 1 alpha and vascular endothelial growth factor. Zhonghua Gan Zang Bing Za Zhi, 19(10): 751–754
pmid: 22409847
89 Lu A L, Li X, Gu Y, Wright P M, Chang D Y (2001). Repair of oxidative DNA damage: mechanisms and functions. Cell Biochem Biophys, 35: 141–70
https://doi.org/10.1385/CBB:35:2:141
90 Ma Q, Cavallin L E, Leung H J, Chiozzini C, Goldschmidt-Clermont P J, Mesri E A (2013). A role for virally induced reactive oxygen species in Kaposi’s sarcoma herpesvirus tumorigenesis. Antioxid Redox Signal, 18(1): 80–90
https://doi.org/10.1089/ars.2012.4584 pmid: 22746102
91 Machida K, Cheng K T H, Lai C K, Jeng K S, Sung V M H, Lai M M C (2006). Hepatitis C virus triggers mitochondrial permeability transition with production of reactive oxygen species, leading to DNA damage and STAT3 activation. J Virol, 80(14): 7199–7207
https://doi.org/10.1128/JVI.00321-06 pmid: 16809325
92 Madkan V K, Cook-Norris R H, Steadman M C, Arora A, Mendoza N, Tyring S K (2007). The oncogenic potential of human papillomaviruses: a review on the role of host genetics and environmental cofactors. Br J Dermatol, 157(2): 228–241
https://doi.org/10.1111/j.1365-2133.2007.07961.x pmid: 17553059
93 Mao Y, Da L, Tang H, Yang J, Lei Y, Tiollais P, Li T, Zhao M (2011). Hepatitis B virus X protein reduces starvation-induced cell death through activation of autophagy and inhibition of mitochondrial apoptotic pathway. Biochem Biophys Res Commun, 415(1): 68–74
https://doi.org/10.1016/j.bbrc.2011.10.013 pmid: 22020078
94 Martin K R, Barrett J C (2002). Reactive oxygen species as double-edged swords in cellular processes: low-dose cell signaling versus high-dose toxicity. Hum Exp Toxicol, 21(2): 71–75
https://doi.org/10.1191/0960327102ht213oa pmid: 12102499
95 Matsuoka M, Jeang K T (2007). Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer, 7(4): 270–280
https://doi.org/10.1038/nrc2111 pmid: 17384582
96 McLaughlin-Drubin M E, Munger K (2008). Viruses associated with human cancer. Biochim Biophys Acta, 1782(3): 127–150
https://doi.org/10.1016/j.bbadis.2007.12.005 pmid: 18201576
97 Melser S, Chatelain E H, Lavie J, Mahfouf W, Jose C, Obre E, Goorden S, Priault M, Elgersma Y, Rezvani H R, Rossignol R, Bénard G (2013). Rheb regulates mitophagy induced by mitochondrial energetic status. Cell Metab, 17(5): 719–730
https://doi.org/10.1016/j.cmet.2013.03.014 pmid: 23602449
98 Mohd Hanafiah K, Groeger J, Flaxman A D, Wiersma S T (2013). Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology, 57(4): 1333–1342
https://doi.org/10.1002/hep.26141 pmid: 23172780
99 Moreno-Sánchez R, Rodríguez-Enríquez S, Marín-Hernández A, Saavedra E (2007). Energy metabolism in tumor cells. FEBS J, 274(6): 1393–1418
https://doi.org/10.1111/j.1742-4658.2007.05686.x pmid: 17302740
100 Münger K, Howley P M (2002). Human papillomavirus immortalization and transformation functions. Virus Res, 89(2): 213–228
https://doi.org/10.1016/S0168-1702(02)00190-9 pmid: 12445661
101 Narendra D, Kane L A, Hauser D N, Fearnley I M, Youle R J (2010). p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy, 6(8): 1090–1106
https://doi.org/10.4161/auto.6.8.13426 pmid: 20890124
102 Narendra D, Tanaka A, Suen D F, Youle R J (2008). Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol, 183(5): 795–803
https://doi.org/10.1083/jcb.200809125 pmid: 19029340
103 Nasimuzzaman M, Waris G, Mikolon D, Stupack D G, Siddiqui A (2007). Hepatitis C virus stabilizes hypoxia-inducible factor 1alpha and stimulates the synthesis of vascular endothelial growth factor. J Virol, 81(19): 10249–10257
https://doi.org/10.1128/JVI.00763-07 pmid: 17626077
104 Ney P A (2011). Normal and disordered reticulocyte maturation. Curr Opin Hematol, 18(3): 152–157
https://doi.org/10.1097/MOH.0b013e328345213e pmid: 21423015
105 Nicot C, Dundr M, Johnson J M, Fullen J R, Alonzo N, Fukumoto R, Princler G L, Derse D, Misteli T, Franchini G (2004). HTLV-1-encoded p30II is a post-transcriptional negative regulator of viral replication. Nat Med, 10(2): 197–201
https://doi.org/10.1038/nm984 pmid: 14730358
106 Novak I (2012). Mitophagy: a complex mechanism of mitochondrial removal. Antioxid Redox Signal, 17(5): 794–802
https://doi.org/10.1089/ars.2011.4407 pmid: 22077334
107 Novak I, Kirkin V, McEwan D G, Zhang J, Wild P, Rozenknop A, Rogov V, L?hr F, Popovic D, Occhipinti A, Reichert A S, Terzic J, D?tsch V, Ney P A, Dikic I (2010). Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep, 11(1): 45–51
https://doi.org/10.1038/embor.2009.256 pmid: 20010802
108 Ohta A, Nishiyama Y (2011). Mitochondria and viruses. Mitochondrion, 11(1): 1–12
https://doi.org/10.1016/j.mito.2010.08.006 pmid: 20813204
109 Okatsu K, Saisho K, Shimanuki M, Nakada K, Shitara H, Sou Y S, Kimura M, Sato S, Hattori N, Komatsu M, Tanaka K, Matsuda N (2010). p62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria. Genes Cells, 15(8): 887–900
pmid: 20604804
110 Okuda M, Li K, Beard M R, Showalter L A, Scholle F, Lemon S M, Weinman S A (2002). Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology, 122(2): 366–375
https://doi.org/10.1053/gast.2002.30983 pmid: 11832451
111 Pal A D, Basak N P, Banerjee A S, Banerjee S (2014). Epstein-Barr virus latent membrane protein-2A alters mitochondrial dynamics promoting cellular migration mediated by Notch signaling pathway. Carcinogenesis, 35(7): 1592–1601
https://doi.org/10.1093/carcin/bgu069 pmid: 24632494
112 Pan J S, Hong M Z, Ren J L (2009). Reactive oxygen species: a double-edged sword in oncogenesis. World J Gastroenterol, 15(14): 1702–1707
https://doi.org/10.3748/wjg.15.1702 pmid: 19360913
113 Pankiv S, Clausen T H, Lamark T, Brech A, Bruun J A, Outzen H, ?vervatn A, Bj?rk?y G, Johansen T (2007). p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem, 282(33): 24131–24145
https://doi.org/10.1074/jbc.M702824200 pmid: 17580304
114 Papandreou I, Cairns R A, Fontana L, Lim A L, Denko N C (2006). HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab, 3(3): 187–197
https://doi.org/10.1016/j.cmet.2006.01.012 pmid: 16517406
115 Paracha U Z, Fatima K, Alqahtani M, Chaudhary A, Abuzenadah A, Damanhouri G, Qadri I (2013). Oxidative stress and hepatitis C virus. Virol J, 10(1): 251
https://doi.org/10.1186/1743-422X-10-251 pmid: 23923986
116 Ramqvist T, Dalianis T (2010). Oropharyngeal cancer epidemic and human papillomavirus. Emerg Infect Dis, 16(11): 1671–1677
https://doi.org/10.3201/eid1611.100452 pmid: 21029523
117 Rawat S, Clippinger A J, Bouchard M J (2012). Modulation of apoptotic signaling by the hepatitis B virus X protein. Viruses, 4(11): 2945–2972
https://doi.org/10.3390/v4112945 pmid: 23202511
118 Ray P D, Huang B W, Tsuji Y (2012). Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal, 24(5): 981–990
https://doi.org/10.1016/j.cellsig.2012.01.008 pmid: 22286106
119 Ripoli M, D’Aprile A, Quarato G, Sarasin-Filipowicz M, Gouttenoire J, Scrima R, Cela O, Boffoli D, Heim M H, Moradpour D, Capitanio N, Piccoli C (2010). Hepatitis C virus-linked mitochondrial dysfunction promotes hypoxia-inducible factor 1 alpha-mediated glycolytic adaptation. J Virol, 84(1): 647–660
https://doi.org/10.1128/JVI.00769-09 pmid: 19846525
120 Saggioro D, Silic-Benussi M, Biasiotto R, D’Agostino D M, Ciminale V (2009). Control of cell death pathways by HTLV-1 proteins. Front Biosci (Landmark Ed), 14(14): 3338–3351
https://doi.org/10.2741/3456 pmid: 19273278
121 Sawada M, Carlson J C (1987). Changes in superoxide radical and lipid peroxide formation in the brain, heart and liver during the lifetime of the rat. Mech Ageing Dev, 41(1-2): 125–137
https://doi.org/10.1016/0047-6374(87)90057-1 pmid: 2828774
122 Schrader M, Fahimi H D (2006). Peroxisomes and oxidative stress. Biochim Biophys Acta, 1763(12): 1755–1766
https://doi.org/10.1016/j.bbamcr.2006.09.006 pmid: 17034877
123 Schwer B, Ren S, Pietschmann T, Kartenbeck J, Kaehlcke K, Bartenschlager R, Yen T S, Ott M (2004). Targeting of hepatitis C virus core protein to mitochondria through a novel C-terminal localization motif. J Virol, 78(15): 7958–7968
https://doi.org/10.1128/JVI.78.15.7958-7968.2004 pmid: 15254168
124 Seagroves T N, Ryan H E, Lu H, Bradly G, Knapp M, Thibault P, Laderoute K, Johnson R S, Lu H A N, Wouters B G (2001). Transcription factor HIF-1 is a necessary mediator of the pasteur effect in mammalian cells transcription factor HIF-1 is a necessary mediator of the pasteur effect in mammalian cells. Mol Cell Biol, 21(10): 3436–3444
https://doi.org/10.1128/MCB.21.10.3436
125 Semenza G L (2007). HIF-1 mediates the Warburg effect in clear cell renal carcinoma. J Bioenerg Biomembr, 39(3): 231–234
https://doi.org/10.1007/s10863-007-9081-2 pmid: 17551816
126 Semenza G L (2011). Regulation of metabolism by hypoxia-inducible factor 1. Cold Spring Harb Symp Quant Biol, 76(0): 347–353
https://doi.org/10.1101/sqb.2011.76.010678 pmid: 21785006
127 Semenza G L, Jiang B H, Leung S W, Passantino R, Concordet J P, Maire P, Giallongo A (1996). Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem, 271(51): 32529–32537
https://doi.org/10.1074/jbc.271.51.32529 pmid: 8955077
128 Sena L A, Chandel N S (2012). Physiological roles of mitochondrial reactive oxygen species. Mol Cell, 48(2): 158–167
https://doi.org/10.1016/j.molcel.2012.09.025 pmid: 23102266
129 Shiba-Fukushima K, Imai Y, Yoshida S, Ishihama Y, Kanao T, Sato S, Hattori N (2012). PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep, 2: 1002
https://doi.org/10.1038/srep01002 pmid: 23256036
130 Shirakata Y, Koike K (2003). Hepatitis B virus X protein induces cell death by causing loss of mitochondrial membrane potential. J Biol Chem, 278(24): 22071–22078
https://doi.org/10.1074/jbc.M301606200 pmid: 12676947
131 Silic-Benussi M, Biasiotto R, Andresen V, Franchini G, D’Agostino D M, Ciminale V (2010a). HTLV-1 p13, a small protein with a busy agenda. Mol Aspects Med, 31(5): 350–358
https://doi.org/10.1016/j.mam.2010.03.001 pmid: 20332002
132 Silic-Benussi M, Cannizzaro E, Venerando A, Cavallari I, Petronilli V, La Rocca N, Marin O, Chieco-Bianchi L, Di Lisa F, D’Agostino D M, Bernardi P, Ciminale V (2009). Modulation of mitochondrial K(+) permeability and reactive oxygen species production by the p13 protein of human T-cell leukemia virus type 1. Biochim Biophys Acta, 1787(7): 947–954
https://doi.org/10.1016/j.bbabio.2009.02.001 pmid: 19366603
133 Silic-Benussi M, Cavallari I, Vajente N, Vidali S, Chieco-Bianchi L, Di Lisa F, Saggioro D, D’Agostino D M, Ciminale V (2010b). Redox regulation of T-cell turnover by the p13 protein of human T-cell leukemia virus type 1: distinct effects in primary versus transformed cells. Blood, 116(1): 54–62
https://doi.org/10.1182/blood-2009-07-235861 pmid: 20395415
134 Silic-Benussi M, Marin O, Biasiotto R, D’Agostino D M, Ciminale V (2010c). Effects of human T-cell leukemia virus type 1 (HTLV-1) p13 on mitochondrial K+ permeability: A new member of the viroporin family? FEBS Lett, 584(10): 2070–2075
https://doi.org/10.1016/j.febslet.2010.02.030 pmid: 20170654
135 Simonnet H, Alazard N, Pfeiffer K, Gallou C, Béroud C, Demont J, Bouvier R, Sch?gger H, Godinot C (2002). Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma. Carcinogenesis, 23(5): 759–768
https://doi.org/10.1093/carcin/23.5.759 pmid: 12016148
136 Soeda E, Ferran M C, Baker C C, McBride A A (2006). Repression of HPV16 early region transcription by the E2 protein. Virology, 351(1): 29–41
https://doi.org/10.1016/j.virol.2006.03.016 pmid: 16624362
137 Stubbs M, Griffiths J R (2010). The altered metabolism of tumors: HIF-1 and its role in the Warburg effect. Adv Enzyme Regul, 50(1): 44–55
https://doi.org/10.1016/j.advenzreg.2009.10.027 pmid: 19896967
138 Takahashi M, Higuchi M, Makokha G N, Matsuki H, Yoshita M, Tanaka Y, Fujii M (2013). HTLV-1 Tax oncoprotein stimulates ROS production and apoptosis in T cells by interacting with USP10. Blood, 122(5): 715–725
https://doi.org/10.1182/blood-2013-03-493718 pmid: 23775713
139 Tal M C, Sasai M, Lee H K, Yordy B, Shadel G S, Iwasaki A (2009). Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci USA, 106(8): 2770–2775
https://doi.org/10.1073/pnas.0807694106 pmid: 19196953
140 Tanaka A, Cleland M M, Xu S, Narendra D P, Suen D F, Karbowski M, Youle R J (2010). Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol, 191(7): 1367–1380
https://doi.org/10.1083/jcb.201007013 pmid: 21173115
141 Tsutsumi T, Matsuda M, Aizaki H, Moriya K, Miyoshi H, Fujie H, Shintani Y, Yotsuyanagi H, Miyamura T, Suzuki T, Koike K (2009). Proteomics analysis of mitochondrial proteins reveals overexpression of a mitochondrial protein chaperon, prohibitin, in cells expressing hepatitis C virus core protein. Hepatology, 50(2): 378–386
https://doi.org/10.1002/hep.22998 pmid: 19591124
142 Turrens J F (2003). Mitochondrial formation of reactive oxygen species. J Physiol, 552(2): 335–344
https://doi.org/10.1113/jphysiol.2003.049478 pmid: 14561818
143 Valente E M, Abou-Sleiman P M, Caputo V, Muqit M M K, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio A R, Healy D G, Albanese A, Nussbaum R, González-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks W P, Latchman D S, Harvey R J, Dallapiccola B, Auburger G, Wood N W (2004). Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science, 304(5674): 1158–1160
https://doi.org/10.1126/science.1096284 pmid: 15087508
144 Vander Heiden M G, Cantley L C, Thompson C B (2009). Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 324(5930): 1029–1033
https://doi.org/10.1126/science.1160809 pmid: 19460998
145 Villota C, Campos A, Vidaurre S, Oliveira-Cruz L, Boccardo E, Burzio V A, Varas M, Villegas J, Villa L L, Valenzuela P D, Socías M, Roberts S, Burzio L O (2012). Expression of mitochondrial non-coding RNAs (ncRNAs) is modulated by high risk human papillomavirus (HPV) oncogenes. J Biol Chem, 287(25): 21303–21315
https://doi.org/10.1074/jbc.M111.326694 pmid: 22539350
146 Wang H, Song P, Du L, Tian W, Yue W, Liu M, Li D, Wang B, Zhu Y, Cao C, Zhou J, Chen Q (2011). Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J Biol Chem, 286(13): 11649–11658
https://doi.org/10.1074/jbc.M110.144238 pmid: 21292769
147 Wang J, Kang R, Huang H, Xi X, Wang B, Wang J, Zhao Z (2014). Hepatitis C virus core protein activates autophagy through EIF2AK3 and ATF6 UPR pathway-mediated MAP1LC3B and ATG12 expression. Autophagy, 10(5): 766–784
https://doi.org/10.4161/auto.27954 pmid: 24589849
148 Wang P, Guo Q S, Wang Z W, Qian H X (2013a). HBx induces HepG-2 cells autophagy through PI3K/Akt-mTOR pathway. Mol Cell Biochem, 372(1-2): 161–168
https://doi.org/10.1007/s11010-012-1457-x pmid: 23001846
149 Wang P, Wang Z W, Qian H X, Guo Q S (2013b). Role of autophagy in HepG-2 cells induced by hepatitis B virus x protein. Zhonghua Yi Xue Za Zhi, 93(44): 3556–3558
pmid: 24521902
150 Wang Y, Liu V W S, Xue W C, Cheung A N, Ngan H Y (2006). Association of decreased mitochondrial DNA content with ovarian cancer progression. Br J Cancer, 95(8): 1087–1091
https://doi.org/10.1038/sj.bjc.6603377 pmid: 17047655
151 Wang Y, Nartiss Y, Steipe B, McQuibban G A, Kim P K (2012). ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy, 8(10): 1462–1476
https://doi.org/10.4161/auto.21211 pmid: 22889933
152 Waris G, Ahsan H (2006). Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog, 5(1): 14
https://doi.org/10.1186/1477-3163-5-14 pmid: 16689993
153 Wilson G K, Brimacombe C L, Rowe I A, Reynolds G M, Fletcher N F, Stamataki Z, Bhogal R H, Sim?es M L, Ashcroft M, Afford S C, Mitry R R, Dhawan A, Mee C J, Hübscher S G, Balfe P, McKeating J A (2012). A dual role for hypoxia inducible factor-1α in the hepatitis C virus lifecycle and hepatoma migration. J Hepatol, 56(4): 803–809
https://doi.org/10.1016/j.jhep.2011.11.018 pmid: 22178269
154 Yamano K, Youle R J (2013). PINK1 is degraded through the N-end rule pathway. Autophagy, 9(11): 1758–1769
https://doi.org/10.4161/auto.24633 pmid: 24121706
155 Yoo Y G, Lee M O (2004). Hepatitis B virus X protein induces expression of Fas ligand gene through enhancing transcriptional activity of early growth response factor. J Biol Chem, 279(35): 36242–36249
https://doi.org/10.1074/jbc.M401290200 pmid: 15173177
156 Yoo Y G, Na T Y, Seo H W, Seong J K, Park C K, Shin Y K, Lee M O (2008). Hepatitis B virus X protein induces the expression of MTA1 and HDAC1, which enhances hypoxia signaling in hepatocellular carcinoma cells. Oncogene, 27(24): 3405–3413
https://doi.org/10.1038/sj.onc.1211000 pmid: 18264140
157 Yoo Y G, Oh S H, Park E S, Cho H, Lee N, Park H, Kim D K, Yu D Y, Seong J K, Lee M O (2003). Hepatitis B virus X protein enhances transcriptional activity of hypoxia-inducible factor-1alpha through activation of mitogen-activated protein kinase pathway. J Biol Chem, 278(40): 39076–39084
https://doi.org/10.1074/jbc.M305101200 pmid: 12855680
158 Youle R J, Narendra D P (2011). Mechanisms of mitophagy. Nat Rev Mol Cell Biol, 12(1): 9–14
https://doi.org/10.1038/nrm3028 pmid: 21179058
159 Young L S, Rickinson A B (2004). Epstein-Barr virus: 40 years on. Nat Rev Cancer, 4(10): 757–768
https://doi.org/10.1038/nrc1452 pmid: 15510157
160 Zhang J, Ney P A (2009). Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ, 16(7): 939–946
https://doi.org/10.1038/cdd.2009.16 pmid: 19229244
161 Zhao T, Matsuoka M (2012). HBZ and its roles in HTLV-1 oncogenesis. Front Microbiol, 3: 247
https://doi.org/10.3389/fmicb.2012.00247 pmid: 22787458
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