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Published in: BMC Cancer 1/2023

Open Access 01-12-2023 | Hepatocellular Carcinoma | Research

SUV39H1 is a novel biomarker targeting oxidative phosphorylation in hepatitis B virus-associated hepatocellular carcinoma

Authors: Yanping Zhang, Wanwen Lao, Kaming Yang, Xinyi Kong, Yuetong Li, Xin Yu, Xumeng Wang, Yang Liu, Zhenlin Li, Yilin Deng, Shuping Nie, Changlong Bi, Chao Wu, Aixia Zhai

Published in: BMC Cancer | Issue 1/2023

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Abstract

Background

As a histone methyltransferase, suppressor of variegation 3–9 homolog 1 (SUV39H1) plays an important role in the occurrence and development of cancer. To explore the mechanism and biological function of SUV39H1 in hepatitis B virus-associated hepatocellular carcinoma (HBV-HCC) can gain an insight into the pathogenesis of HBV-HCC.

Methods

The effect of HBV infection on SUV39H1 in hepatoma cells was detected. CCK-8, colony growth assay and wound healing assay were used to assess the proliferation and migration of HBV-positive hepatoma cells. RNA sequencing (RNA-seq) was applied to find differential genes and enriched pathways. The serum SUV39H1 level in HBV-HCC patients was detected and its correlation with clinical indicators was analyzed.

Results

SUV39H1 was increased by HBV infection and promoted the proliferation and migration of hepatoma cells. SUV39H1 could upregulate the expression of mitochondrial oxidative phosphorylation (OXPHOS) pathway-related genes. OXPHOS pathway inhibitors could reduce the capacity of proliferation and migration of hepatoma cells after overexpressing SUV39H1. Serum SUV39H1 levels were higher in chronic hepatitis B (CHB) patients than in healthy controls and higher in HBV-HCC patients than in CHB patients. In the diagnosis of HCC, the predictive value of SUV39H1 combined with alpha-fetoprotein (AFP) was better than that of AFP alone.

Conclusion

SUV39H1 is regulated by HBV infection and promotes the proliferation and migration of hepatoma cells by targeting OXPHOS pathway. It indicates that SUV39H1 may be a new biomarker of the diagnosis of HCC.
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Literature
1.
go back to reference Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer statistics 2020: GLOBOCAN estimates of incidence and Mortality Worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.PubMedCrossRef Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer statistics 2020: GLOBOCAN estimates of incidence and Mortality Worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.PubMedCrossRef
2.
go back to reference Foerster F, Gairing SJ, Ilyas SI, Galle PR. Emerging immunotherapy for HCC: a guide for hepatologists. Hepatology. 2022;75(6):1604–26.PubMedCrossRef Foerster F, Gairing SJ, Ilyas SI, Galle PR. Emerging immunotherapy for HCC: a guide for hepatologists. Hepatology. 2022;75(6):1604–26.PubMedCrossRef
3.
go back to reference Kulik L, El-Serag HB. Epidemiology and management of Hepatocellular Carcinoma. Gastroenterology. 2019;156(2):477–491e471.PubMedCrossRef Kulik L, El-Serag HB. Epidemiology and management of Hepatocellular Carcinoma. Gastroenterology. 2019;156(2):477–491e471.PubMedCrossRef
5.
go back to reference Fernández-Barrena MG, Arechederra M, Colyn L, Berasain C, Avila MA. Epigenetics in hepatocellular carcinoma development and therapy: the tip of the iceberg. JHEP Rep. 2020;2(6):100167.PubMedPubMedCentralCrossRef Fernández-Barrena MG, Arechederra M, Colyn L, Berasain C, Avila MA. Epigenetics in hepatocellular carcinoma development and therapy: the tip of the iceberg. JHEP Rep. 2020;2(6):100167.PubMedPubMedCentralCrossRef
6.
go back to reference Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 2000;406(6796):593–9.PubMedCrossRef Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 2000;406(6796):593–9.PubMedCrossRef
7.
go back to reference Liu B, Wang Z, Zhang L, Ghosh S, Zheng H, Zhou Z. Depleting the methyltransferase Suv39h1 improves DNA repair and extends lifespan in a progeria mouse model. Nat Commun. 2013;4:1868.PubMedCrossRef Liu B, Wang Z, Zhang L, Ghosh S, Zheng H, Zhou Z. Depleting the methyltransferase Suv39h1 improves DNA repair and extends lifespan in a progeria mouse model. Nat Commun. 2013;4:1868.PubMedCrossRef
8.
go back to reference Rodrigues C, Pattabiraman C, Vijaykumar A, Arora R, Narayana SM, Kumar RV, Notani D, Varga-Weisz P, Krishna S. A SUV39H1-low chromatin state characterises and promotes migratory properties of Cervical cancer cells. Exp Cell Res. 2019;378(2):206–16.PubMedCrossRef Rodrigues C, Pattabiraman C, Vijaykumar A, Arora R, Narayana SM, Kumar RV, Notani D, Varga-Weisz P, Krishna S. A SUV39H1-low chromatin state characterises and promotes migratory properties of Cervical cancer cells. Exp Cell Res. 2019;378(2):206–16.PubMedCrossRef
9.
go back to reference Yang YJ, Han JW, Youn HD, Cho EJ. The Tumor suppressor, parafibromin, mediates histone H3 K9 methylation for cyclin D1 repression. Nucleic Acids Res. 2010;38(2):382–90.PubMedCrossRef Yang YJ, Han JW, Youn HD, Cho EJ. The Tumor suppressor, parafibromin, mediates histone H3 K9 methylation for cyclin D1 repression. Nucleic Acids Res. 2010;38(2):382–90.PubMedCrossRef
10.
go back to reference Chu Y, Chen Y, Guo H, Li M, Wang B, Shi D, Cheng X, Guan J, Wang X, Xue C, et al. SUV39H1 regulates the progression of MLL-AF9-induced acute Myeloid Leukemia. Oncogene. 2020;39(50):7239–52.PubMedPubMedCentralCrossRef Chu Y, Chen Y, Guo H, Li M, Wang B, Shi D, Cheng X, Guan J, Wang X, Xue C, et al. SUV39H1 regulates the progression of MLL-AF9-induced acute Myeloid Leukemia. Oncogene. 2020;39(50):7239–52.PubMedPubMedCentralCrossRef
11.
go back to reference Lu C, Klement JD, Yang D, Albers T, Lebedyeva IO, Waller JL, Liu K. SUV39H1 regulates human colon carcinoma apoptosis and cell cycle to promote Tumor growth. Cancer Lett. 2020;476:87–96.PubMedPubMedCentralCrossRef Lu C, Klement JD, Yang D, Albers T, Lebedyeva IO, Waller JL, Liu K. SUV39H1 regulates human colon carcinoma apoptosis and cell cycle to promote Tumor growth. Cancer Lett. 2020;476:87–96.PubMedPubMedCentralCrossRef
12.
go back to reference Kim G, Kim JY, Lim SC, Lee KY, Kim O, Choi HS. SUV39H1/DNMT3A-dependent methylation of the RB1 promoter stimulates PIN1 expression and Melanoma development. Faseb j. 2018;32(10):5647–60.PubMedCrossRef Kim G, Kim JY, Lim SC, Lee KY, Kim O, Choi HS. SUV39H1/DNMT3A-dependent methylation of the RB1 promoter stimulates PIN1 expression and Melanoma development. Faseb j. 2018;32(10):5647–60.PubMedCrossRef
13.
go back to reference Chiba T, Saito T, Yuki K, Zen Y, Koide S, Kanogawa N, Motoyama T, Ogasawara S, Suzuki E, Ooka Y, et al. Histone lysine methyltransferase SUV39H1 is a potent target for epigenetic therapy of hepatocellular carcinoma. Int J Cancer. 2015;136(2):289–98.PubMedCrossRef Chiba T, Saito T, Yuki K, Zen Y, Koide S, Kanogawa N, Motoyama T, Ogasawara S, Suzuki E, Ooka Y, et al. Histone lysine methyltransferase SUV39H1 is a potent target for epigenetic therapy of hepatocellular carcinoma. Int J Cancer. 2015;136(2):289–98.PubMedCrossRef
14.
go back to reference Takeuchi Y, Tsuge M, Tsushima K, Suehiro Y, Fujino H, Ono A, Yamauchi M, Makokha GN, Nakahara T, Murakami E, et al. Signal activation of Hepatitis B Virus-Related Hepatocarcinogenesis by Up-regulation of SUV39h1. J Infect Dis. 2020;222(12):2061–70.PubMedCrossRef Takeuchi Y, Tsuge M, Tsushima K, Suehiro Y, Fujino H, Ono A, Yamauchi M, Makokha GN, Nakahara T, Murakami E, et al. Signal activation of Hepatitis B Virus-Related Hepatocarcinogenesis by Up-regulation of SUV39h1. J Infect Dis. 2020;222(12):2061–70.PubMedCrossRef
15.
go back to reference Guo S, Li F, Liang Y, Zheng Y, Mo Y, Zhao D, Jiang Z, Cui M, Qi L, Chen J, et al. AIFM2 promotes hepatocellular carcinoma Metastasis by enhancing mitochondrial biogenesis through activation of SIRT1/PGC-1α signaling. Oncogenesis. 2023;12(1):46.PubMedPubMedCentralCrossRef Guo S, Li F, Liang Y, Zheng Y, Mo Y, Zhao D, Jiang Z, Cui M, Qi L, Chen J, et al. AIFM2 promotes hepatocellular carcinoma Metastasis by enhancing mitochondrial biogenesis through activation of SIRT1/PGC-1α signaling. Oncogenesis. 2023;12(1):46.PubMedPubMedCentralCrossRef
16.
go back to reference Vaquero A, Scher M, Erdjument-Bromage H, Tempst P, Serrano L, Reinberg D. SIRT1 regulates the histone methyl-transferase SUV39H1 during heterochromatin formation. Nature. 2007;450(7168):440–4.PubMedCrossRef Vaquero A, Scher M, Erdjument-Bromage H, Tempst P, Serrano L, Reinberg D. SIRT1 regulates the histone methyl-transferase SUV39H1 during heterochromatin formation. Nature. 2007;450(7168):440–4.PubMedCrossRef
17.
go back to reference Martínez-Reyes I, Chandel NS. Cancer metabolism: looking forward. Nat Rev Cancer. 2021;21(10):669–80.PubMedCrossRef Martínez-Reyes I, Chandel NS. Cancer metabolism: looking forward. Nat Rev Cancer. 2021;21(10):669–80.PubMedCrossRef
18.
go back to reference Schöpf B, Weissensteiner H, Schäfer G, Fazzini F, Charoentong P, Naschberger A, Rupp B, Fendt L, Bukur V, Giese I, et al. OXPHOS remodeling in high-grade Prostate cancer involves mtDNA mutations and increased succinate oxidation. Nat Commun. 2020;11(1):1487.PubMedPubMedCentralCrossRef Schöpf B, Weissensteiner H, Schäfer G, Fazzini F, Charoentong P, Naschberger A, Rupp B, Fendt L, Bukur V, Giese I, et al. OXPHOS remodeling in high-grade Prostate cancer involves mtDNA mutations and increased succinate oxidation. Nat Commun. 2020;11(1):1487.PubMedPubMedCentralCrossRef
19.
go back to reference Roth KG, Mambetsariev I, Kulkarni P, Salgia R. The Mitochondrion as an emerging therapeutic target in Cancer. Trends Mol Med. 2020;26(1):119–34.PubMedCrossRef Roth KG, Mambetsariev I, Kulkarni P, Salgia R. The Mitochondrion as an emerging therapeutic target in Cancer. Trends Mol Med. 2020;26(1):119–34.PubMedCrossRef
20.
go back to reference Knowles BB, Howe CC, Aden DP. Human hepatocellular carcinoma cell lines secrete the major plasma proteins and Hepatitis B surface antigen. Science. 1980;209(4455):497–9.PubMedCrossRef Knowles BB, Howe CC, Aden DP. Human hepatocellular carcinoma cell lines secrete the major plasma proteins and Hepatitis B surface antigen. Science. 1980;209(4455):497–9.PubMedCrossRef
21.
go back to reference Yu X, Chen Y, Cui L, Yang K, Wang X, Lei L, Zhang Y, Kong X, Lao W, Li Z, et al. CXCL8, CXCL9, CXCL10, and CXCL11 as biomarkers of liver injury caused by chronic Hepatitis B. Front Microbiol. 2022;13:1052917.PubMedPubMedCentralCrossRef Yu X, Chen Y, Cui L, Yang K, Wang X, Lei L, Zhang Y, Kong X, Lao W, Li Z, et al. CXCL8, CXCL9, CXCL10, and CXCL11 as biomarkers of liver injury caused by chronic Hepatitis B. Front Microbiol. 2022;13:1052917.PubMedPubMedCentralCrossRef
24.
go back to reference Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 2023;51(D1):D587–d592.PubMedCrossRef Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 2023;51(D1):D587–d592.PubMedCrossRef
25.
go back to reference Cui F, Shen L, Li L, Wang H, Wang F, Bi S, Liu J, Zhang G, Wang F, Zheng H, et al. Prevention of Chronic Hepatitis B after 3 decades of escalating Vaccination Policy, China. Emerg Infect Dis. 2017;23(5):765–72.PubMedPubMedCentralCrossRef Cui F, Shen L, Li L, Wang H, Wang F, Bi S, Liu J, Zhang G, Wang F, Zheng H, et al. Prevention of Chronic Hepatitis B after 3 decades of escalating Vaccination Policy, China. Emerg Infect Dis. 2017;23(5):765–72.PubMedPubMedCentralCrossRef
26.
go back to reference Liu Z, Jiang Y, Yuan H, Fang Q, Cai N, Suo C, Jin L, Zhang T, Chen X. The trends in incidence of primary Liver cancer caused by specific etiologies: results from the global burden of Disease Study 2016 and implications for Liver cancer prevention. J Hepatol. 2019;70(4):674–83.PubMedCrossRef Liu Z, Jiang Y, Yuan H, Fang Q, Cai N, Suo C, Jin L, Zhang T, Chen X. The trends in incidence of primary Liver cancer caused by specific etiologies: results from the global burden of Disease Study 2016 and implications for Liver cancer prevention. J Hepatol. 2019;70(4):674–83.PubMedCrossRef
29.
go back to reference Wang J, Yan W, Peng X, Jiang Y, He L, Peng Y, Chen X, Ye M, Zhuo H. Functional role of SUV39H1 in human renal tubular epithelial cells under high-glucose ambiance. Inflammation. 2018;41(1):1–10.PubMedCrossRef Wang J, Yan W, Peng X, Jiang Y, He L, Peng Y, Chen X, Ye M, Zhuo H. Functional role of SUV39H1 in human renal tubular epithelial cells under high-glucose ambiance. Inflammation. 2018;41(1):1–10.PubMedCrossRef
30.
go back to reference Li J, Yang G, Liu S, Wang L, Liang Z, Zhang H. Suv39h1 promotes facet joint chondrocyte proliferation by targeting miR-15a/Bcl2 in idiopathic scoliosis patients. Clin Epigenetics. 2019;11(1):107.PubMedPubMedCentralCrossRef Li J, Yang G, Liu S, Wang L, Liang Z, Zhang H. Suv39h1 promotes facet joint chondrocyte proliferation by targeting miR-15a/Bcl2 in idiopathic scoliosis patients. Clin Epigenetics. 2019;11(1):107.PubMedPubMedCentralCrossRef
31.
go back to reference Miao Y, Lv Q, Qiao S, Yang L, Tao Y, Yan W, Wang P, Cao N, Dai Y, Wei Z. Alpinetin improves intestinal barrier homeostasis via regulating AhR/suv39h1/TSC2/mTORC1/autophagy pathway. Toxicol Appl Pharmacol. 2019;384:114772.PubMedCrossRef Miao Y, Lv Q, Qiao S, Yang L, Tao Y, Yan W, Wang P, Cao N, Dai Y, Wei Z. Alpinetin improves intestinal barrier homeostasis via regulating AhR/suv39h1/TSC2/mTORC1/autophagy pathway. Toxicol Appl Pharmacol. 2019;384:114772.PubMedCrossRef
32.
go back to reference Saha N, Muntean AG. Insight into the multi-faceted role of the SUV family of H3K9 methyltransferases in carcinogenesis and cancer progression. Biochim Biophys Acta Rev Cancer. 2021;1875(1):188498.PubMedCrossRef Saha N, Muntean AG. Insight into the multi-faceted role of the SUV family of H3K9 methyltransferases in carcinogenesis and cancer progression. Biochim Biophys Acta Rev Cancer. 2021;1875(1):188498.PubMedCrossRef
33.
go back to reference Wang J, Yin X, He W, Xue W, Zhang J, Huang Y. SUV39H1 deficiency suppresses clear cell renal cell carcinoma growth by inducing ferroptosis. Acta Pharm Sin B. 2021;11(2):406–19.PubMedCrossRef Wang J, Yin X, He W, Xue W, Zhang J, Huang Y. SUV39H1 deficiency suppresses clear cell renal cell carcinoma growth by inducing ferroptosis. Acta Pharm Sin B. 2021;11(2):406–19.PubMedCrossRef
34.
go back to reference Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11(5):325–37.PubMedCrossRef Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11(5):325–37.PubMedCrossRef
36.
go back to reference Zhang G, Frederick DT, Wu L, Wei Z, Krepler C, Srinivasan S, Chae YC, Xu X, Choi H, Dimwamwa E, et al. Targeting mitochondrial biogenesis to overcome drug resistance to MAPK inhibitors. J Clin Invest. 2016;126(5):1834–56.PubMedPubMedCentralCrossRef Zhang G, Frederick DT, Wu L, Wei Z, Krepler C, Srinivasan S, Chae YC, Xu X, Choi H, Dimwamwa E, et al. Targeting mitochondrial biogenesis to overcome drug resistance to MAPK inhibitors. J Clin Invest. 2016;126(5):1834–56.PubMedPubMedCentralCrossRef
37.
go back to reference Jagust P, de Luxán-Delgado B, Parejo-Alonso B, Sancho P. Metabolism-based therapeutic strategies targeting Cancer Stem cells. Front Pharmacol. 2019;10:203.PubMedPubMedCentralCrossRef Jagust P, de Luxán-Delgado B, Parejo-Alonso B, Sancho P. Metabolism-based therapeutic strategies targeting Cancer Stem cells. Front Pharmacol. 2019;10:203.PubMedPubMedCentralCrossRef
38.
go back to reference Zhao Y, Zhou L, Li H, Sun T, Wen X, Li X, Meng Y, Li Y, Liu M, Liu S, et al. Nuclear-encoded lncRNA MALAT1 epigenetically controls metabolic reprogramming in HCC cells through the Mitophagy Pathway. Mol Ther Nucleic Acids. 2021;23:264–76.PubMedCrossRef Zhao Y, Zhou L, Li H, Sun T, Wen X, Li X, Meng Y, Li Y, Liu M, Liu S, et al. Nuclear-encoded lncRNA MALAT1 epigenetically controls metabolic reprogramming in HCC cells through the Mitophagy Pathway. Mol Ther Nucleic Acids. 2021;23:264–76.PubMedCrossRef
39.
go back to reference Chang H, Li J, Qu K, Wan Y, Liu S, Zheng W, Zhang Z, Liu C. CRIF1 overexpression facilitates Tumor growth and Metastasis through inducing ROS/NFκB pathway in hepatocellular carcinoma. Cell Death Dis. 2020;11(5):332.PubMedPubMedCentralCrossRef Chang H, Li J, Qu K, Wan Y, Liu S, Zheng W, Zhang Z, Liu C. CRIF1 overexpression facilitates Tumor growth and Metastasis through inducing ROS/NFκB pathway in hepatocellular carcinoma. Cell Death Dis. 2020;11(5):332.PubMedPubMedCentralCrossRef
40.
go back to reference Turcios L, Vilchez V, Acosta LF, Poyil P, Butterfield DA, Mitov M, Marti F, Gedaly R. Sorafenib and FH535 in combination act synergistically on hepatocellular carcinoma by targeting cell bioenergetics and mitochondrial function. Dig Liver Dis. 2017;49(6):697–704.PubMedCrossRef Turcios L, Vilchez V, Acosta LF, Poyil P, Butterfield DA, Mitov M, Marti F, Gedaly R. Sorafenib and FH535 in combination act synergistically on hepatocellular carcinoma by targeting cell bioenergetics and mitochondrial function. Dig Liver Dis. 2017;49(6):697–704.PubMedCrossRef
41.
go back to reference Turcios L, Marti F, Watt DS, Kril LM, Khurana A, Chapelin F, Liu C, Zwischenberger JB, Evers BM, Gedaly R. Mitochondrial uncoupling and the disruption of the metabolic network in hepatocellular carcinoma. Oncotarget. 2020;11(31):3013–24.PubMedPubMedCentralCrossRef Turcios L, Marti F, Watt DS, Kril LM, Khurana A, Chapelin F, Liu C, Zwischenberger JB, Evers BM, Gedaly R. Mitochondrial uncoupling and the disruption of the metabolic network in hepatocellular carcinoma. Oncotarget. 2020;11(31):3013–24.PubMedPubMedCentralCrossRef
42.
go back to reference Tsuchiya N, Sawada Y, Endo I, Saito K, Uemura Y, Nakatsura T. Biomarkers for the early diagnosis of hepatocellular carcinoma. World J Gastroenterol. 2015;21(37):10573–83.PubMedPubMedCentralCrossRef Tsuchiya N, Sawada Y, Endo I, Saito K, Uemura Y, Nakatsura T. Biomarkers for the early diagnosis of hepatocellular carcinoma. World J Gastroenterol. 2015;21(37):10573–83.PubMedPubMedCentralCrossRef
43.
go back to reference Trevisani F, D’Intino PE, Morselli-Labate AM, Mazzella G, Accogli E, Caraceni P, Domenicali M, De Notariis S, Roda E, Bernardi M. Serum alpha-fetoprotein for diagnosis of hepatocellular carcinoma in patients with chronic Liver Disease: influence of HBsAg and anti-HCV status. J Hepatol. 2001;34(4):570–5.PubMedCrossRef Trevisani F, D’Intino PE, Morselli-Labate AM, Mazzella G, Accogli E, Caraceni P, Domenicali M, De Notariis S, Roda E, Bernardi M. Serum alpha-fetoprotein for diagnosis of hepatocellular carcinoma in patients with chronic Liver Disease: influence of HBsAg and anti-HCV status. J Hepatol. 2001;34(4):570–5.PubMedCrossRef
44.
go back to reference Lok AS, Sterling RK, Everhart JE, Wright EC, Hoefs JC, Di Bisceglie AM, Morgan TR, Kim HY, Lee WM, Bonkovsky HL, et al. Des-gamma-carboxy prothrombin and alpha-fetoprotein as biomarkers for the early detection of hepatocellular carcinoma. Gastroenterology. 2010;138(2):493–502.PubMedCrossRef Lok AS, Sterling RK, Everhart JE, Wright EC, Hoefs JC, Di Bisceglie AM, Morgan TR, Kim HY, Lee WM, Bonkovsky HL, et al. Des-gamma-carboxy prothrombin and alpha-fetoprotein as biomarkers for the early detection of hepatocellular carcinoma. Gastroenterology. 2010;138(2):493–502.PubMedCrossRef
45.
go back to reference Baudi I, Inoue T, Tanaka Y. Novel biomarkers of Hepatitis B and Hepatocellular Carcinoma: clinical significance of HBcrAg and M2BPGi. Int J Mol Sci. 2020;21(3):949.PubMedPubMedCentralCrossRef Baudi I, Inoue T, Tanaka Y. Novel biomarkers of Hepatitis B and Hepatocellular Carcinoma: clinical significance of HBcrAg and M2BPGi. Int J Mol Sci. 2020;21(3):949.PubMedPubMedCentralCrossRef
46.
go back to reference Jun T, Hsu YC, Ogawa S, Huang YT, Yeh ML, Tseng CH, Huang CF, Tai CM, Dai CY, Huang JF, et al. Mac-2 binding protein glycosylation isomer as a Hepatocellular Carcinoma Marker in patients with chronic Hepatitis B or C Infection. Hepatol Commun. 2019;3(4):493–503.PubMedPubMedCentralCrossRef Jun T, Hsu YC, Ogawa S, Huang YT, Yeh ML, Tseng CH, Huang CF, Tai CM, Dai CY, Huang JF, et al. Mac-2 binding protein glycosylation isomer as a Hepatocellular Carcinoma Marker in patients with chronic Hepatitis B or C Infection. Hepatol Commun. 2019;3(4):493–503.PubMedPubMedCentralCrossRef
47.
go back to reference Wang H, Hou L, Li A, Duan Y, Gao H, Song X. Expression of serum exosomal microRNA-21 in human hepatocellular carcinoma. Biomed Res Int. 2014;2014:864894.PubMedPubMedCentral Wang H, Hou L, Li A, Duan Y, Gao H, Song X. Expression of serum exosomal microRNA-21 in human hepatocellular carcinoma. Biomed Res Int. 2014;2014:864894.PubMedPubMedCentral
48.
go back to reference Xu H, Dong X, Chen Y, Wang X. Serum exosomal hnRNPH1 mRNA as a novel marker for hepatocellular carcinoma. Clin Chem Lab Med. 2018;56(3):479–84.PubMedCrossRef Xu H, Dong X, Chen Y, Wang X. Serum exosomal hnRNPH1 mRNA as a novel marker for hepatocellular carcinoma. Clin Chem Lab Med. 2018;56(3):479–84.PubMedCrossRef
49.
go back to reference Wang D, Hu X, Long G, Xiao L, Wang ZM, Zhou LD. The clinical value of total plasma cell-free DNA in Hepatitis B virus-related hepatocellular carcinoma. Ann Transl Med. 2019;7(22):650.PubMedPubMedCentralCrossRef Wang D, Hu X, Long G, Xiao L, Wang ZM, Zhou LD. The clinical value of total plasma cell-free DNA in Hepatitis B virus-related hepatocellular carcinoma. Ann Transl Med. 2019;7(22):650.PubMedPubMedCentralCrossRef
Metadata
Title
SUV39H1 is a novel biomarker targeting oxidative phosphorylation in hepatitis B virus-associated hepatocellular carcinoma
Authors
Yanping Zhang
Wanwen Lao
Kaming Yang
Xinyi Kong
Yuetong Li
Xin Yu
Xumeng Wang
Yang Liu
Zhenlin Li
Yilin Deng
Shuping Nie
Changlong Bi
Chao Wu
Aixia Zhai
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2023
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-023-11633-4

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