Human Viral Oncogenesis: a Cancer Hallmarks Analysis

Overview

Journal Cell Host Microbe

Publisher Cell Press

Specialties Infectious Diseases
Microbiology

Date 2014 Mar 18

PMID 24629334

Citations 331

Authors

Enrique A Mesri

Mark A Feitelson

Karl Munger

Affiliations

Soon will be listed here.

Abstract

Approximately 12% of all human cancers are caused by oncoviruses. Human viral oncogenesis is complex, and only a small percentage of the infected individuals develop cancer, often many years to decades after the initial infection. This reflects the multistep nature of viral oncogenesis, host genetic variability, and the fact that viruses contribute to only a portion of the oncogenic events. In this review, the Hallmarks of Cancer framework of Hanahan and Weinberg (2000 and 2011) is used to dissect the viral, host, and environmental cofactors that contribute to the biology of multistep oncogenesis mediated by established human oncoviruses. The viruses discussed include Epstein-Barr virus (EBV), high-risk human papillomaviruses (HPVs), hepatitis B and C viruses (HBV and HCV, respectively), human T cell lymphotropic virus-1 (HTLV-1), and Kaposi's sarcoma herpesvirus (KSHV).

Citing Articles

BRN3A, a transcription factor, regulates the expression of genes involved in biological processes shaping the HPV induced cervical cancer.

Prakash A, Patel Y, Roy J Genes Genomics. 2025; .

PMID: 39873931 DOI: 10.1007/s13258-025-01620-3.

A Landscape of Cancer Initiation and Cancer Stem Cells.

Seno M Cancers (Basel). 2025; 17(2).

PMID: 39857984 PMC: 11764454. DOI: 10.3390/cancers17020203.

Mouse models of Kaposi sarcoma-associated herpesvirus (KSHV).

Shifflett K, Dittmer D Virology. 2025; 603:110384.

PMID: 39837218 PMC: 11788063. DOI: 10.1016/j.virol.2024.110384.

Identifying the key regulators orchestrating Epstein-Barr virus reactivation.

Wang Y, Yu J, Pei Y Front Microbiol. 2024; 15:1505191.

PMID: 39703703 PMC: 11655498. DOI: 10.3389/fmicb.2024.1505191.

The Role of microRNA Expression and DNA Methylation in HPV-Related Cervical Cancer: A Systematic Review.

Pulliero A, Cassatella G, Astuni P, Khalid Z, Fiordoro S, Izzotti A Int J Mol Sci. 2024; 25(23).

PMID: 39684425 PMC: 11641737. DOI: 10.3390/ijms252312714.

References

Martinez-Pastor B, Cosentino C, Mostoslavsky R . A tale of metabolites: the cross-talk between chromatin and energy metabolism. Cancer Discov. 2013; 3(5):497-501. PMC: 3652636. DOI: 10.1158/2159-8290.CD-13-0059. View

Schiller J, Lowy D . Vaccines to prevent infections by oncoviruses. Annu Rev Microbiol. 2010; 64:23-41. PMC: 6264788. DOI: 10.1146/annurev.micro.112408.134019. View

Nakamura H, Li M, Zarycki J, Jung J . Inhibition of p53 tumor suppressor by viral interferon regulatory factor. J Virol. 2001; 75(16):7572-82. PMC: 114992. DOI: 10.1128/JVI.75.16.7572-7582.2001. View

Karki R, Lang S, Means R . The MARCH family E3 ubiquitin ligase K5 alters monocyte metabolism and proliferation through receptor tyrosine kinase modulation. PLoS Pathog. 2011; 7(4):e1001331. PMC: 3072377. DOI: 10.1371/journal.ppat.1001331. View

Brechot C . Pathogenesis of hepatitis B virus-related hepatocellular carcinoma: old and new paradigms. Gastroenterology. 2004; 127(5 Suppl 1):S56-61. DOI: 10.1053/j.gastro.2004.09.016. View

Maruyama M, Shibuya H, Harada H, Hatakeyama M, Seiki M, Fujita T . Evidence for aberrant activation of the interleukin-2 autocrine loop by HTLV-1-encoded p40x and T3/Ti complex triggering. Cell. 1987; 48(2):343-50. DOI: 10.1016/0092-8674(87)90437-5. View

Zhao P, Han T, Guo J, Zhu S, Wang J, Ao F . HCV NS4B induces apoptosis through the mitochondrial death pathway. Virus Res. 2012; 169(1):1-7. DOI: 10.1016/j.virusres.2012.04.006. View

Cai Q, Knight J, Verma S, Zald P, Robertson E . EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors. PLoS Pathog. 2006; 2(10):e116. PMC: 1626105. DOI: 10.1371/journal.ppat.0020116. View

Feitelson M, Lee J . Hepatitis B virus integration, fragile sites, and hepatocarcinogenesis. Cancer Lett. 2006; 252(2):157-70. DOI: 10.1016/j.canlet.2006.11.010. View

10.

Keith B, Simon M . Hypoxia-inducible factors, stem cells, and cancer. Cell. 2007; 129(3):465-72. PMC: 3150586. DOI: 10.1016/j.cell.2007.04.019. View

11.

Cheng F, Pekkonen P, Laurinavicius S, Sugiyama N, Henderson S, Gunther T . KSHV-initiated notch activation leads to membrane-type-1 matrix metalloproteinase-dependent lymphatic endothelial-to-mesenchymal transition. Cell Host Microbe. 2011; 10(6):577-90. DOI: 10.1016/j.chom.2011.10.011. View

12.

Vogelstein B, Kinzler K . The multistep nature of cancer. Trends Genet. 1993; 9(4):138-41. DOI: 10.1016/0168-9525(93)90209-z. View

13.

Duffy C, Phillips S, Klingelhutz A . Microarray analysis identifies differentiation-associated genes regulated by human papillomavirus type 16 E6. Virology. 2003; 314(1):196-205. DOI: 10.1016/s0042-6822(03)00390-8. View

14.

Hofelmayr H, Strobl L, Marschall G, Bornkamm G, Zimber-Strobl U . Activated Notch1 can transiently substitute for EBNA2 in the maintenance of proliferation of LMP1-expressing immortalized B cells. J Virol. 2001; 75(5):2033-40. PMC: 114787. DOI: 10.1128/JVI.75.5.2033-2040.2001. View

15.

Bais C, Van Geelen A, Eroles P, Mutlu A, Chiozzini C, Dias S . Kaposi's sarcoma associated herpesvirus G protein-coupled receptor immortalizes human endothelial cells by activation of the VEGF receptor-2/ KDR. Cancer Cell. 2003; 3(2):131-43. DOI: 10.1016/s1535-6108(03)00024-2. View

16.

Rochford R, Cannon M, Moormann A . Endemic Burkitt's lymphoma: a polymicrobial disease?. Nat Rev Microbiol. 2005; 3(2):182-7. DOI: 10.1038/nrmicro1089. View

17.

Wang W, London W, Lega L, Feitelson M . HBxAg in the liver from carrier patients with chronic hepatitis and cirrhosis. Hepatology. 1991; 14(1):29-37. DOI: 10.1002/hep.1840140106. View

18.

Hanahan D, Weinberg R . Hallmarks of cancer: the next generation. Cell. 2011; 144(5):646-74. DOI: 10.1016/j.cell.2011.02.013. View

19.

Paul A, Sharma-Walia N, Kerur N, White C, Chandran B . Piracy of prostaglandin E2/EP receptor-mediated signaling by Kaposi's sarcoma-associated herpes virus (HHV-8) for latency gene expression: strategy of a successful pathogen. Cancer Res. 2010; 70(9):3697-708. PMC: 2862142. DOI: 10.1158/0008-5472.CAN-09-3934. View

20.

Stine J, Wood C, Hill M, Epp A, Raport C, Schweickart V . KSHV-encoded CC chemokine vMIP-III is a CCR4 agonist, stimulates angiogenesis, and selectively chemoattracts TH2 cells. Blood. 2000; 95(4):1151-7. View