Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 6468342, 9 pages
http://dx.doi.org/10.1155/2016/6468342
Review Article

DNA Tumor Viruses and Cell Metabolism

1Department of Microbiology, Tumor and Cell Biology (MTC), Karolinska Institute, 17177 Stockholm, Sweden
2R.E. Kavetsky Institute of Experimental Pathology, Oncology and Radiobiology, NASU, Kyiv 03022, Ukraine

Received 28 November 2015; Accepted 8 February 2016

Academic Editor: Alexander V. Ivanov

Copyright © 2016 Muhammad Mushtaq et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar
  2. B. Ríhová, “Infectious causes of cancer: targets for intervention J.J. Goedert (Ed.),” Folia Microbiologica, vol. 45, no. 3, pp. 279–280, 2000. View at Publisher · View at Google Scholar
  3. B. H. Sweet and M. R. Hilleman, “The vacuolating virus, S.V. 40,” Proceedings of the Society for Experimental Biology and Medicine, vol. 105, pp. 420–427, 1960. View at Google Scholar
  4. A. J. Girardi, B. H. Sweet, V. B. Slotnick, and M. R. Hilleman, “Development of tumors in hamsters inoculated in the neonatal period with vacuolating virus, SV40,” Experimental Biology and Medicine, vol. 109, no. 3, pp. 649–660, 1962. View at Publisher · View at Google Scholar
  5. Y. Yabe, J. J. Trentin, and G. Taylor, “Cancer induction in hamsters by human type 12 adenovirus. Effect of age and of virus dose,” Experimental Biology and Medicine, vol. 111, no. 2, pp. 343–344, 1962. View at Publisher · View at Google Scholar
  6. M. G. V. Heiden, L. C. Cantley, and C. B. Thompson, “Understanding the warburg effect: the metabolic requirements of cell proliferation,” Science, vol. 324, no. 5930, pp. 1029–1033, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Nathan and A. Ding, “SnapShot: Reactive Oxygen Intermediates (ROI),” Cell, vol. 140, no. 6, p. 951.e2, 2010. View at Publisher · View at Google Scholar
  8. R. J. DeBerardinis, J. J. Lum, G. Hatzivassiliou, and C. B. Thompson, “The biology of cancer: metabolic reprogramming fuels cell growth and proliferation,” Cell Metabolism, vol. 7, no. 1, pp. 11–20, 2008. View at Publisher · View at Google Scholar
  9. R. J. Gillies, I. Robey, and R. A. Gatenby, “Causes and consequences of increased glucose metabolism of cancers,” Journal of Nuclear Medicine, vol. 49, supplement 2, pp. 24S–42S, 2008. View at Publisher · View at Google Scholar
  10. V. Fritz and L. Fajas, “Metabolism and proliferation share common regulatory pathways in cancer cells,” Oncogene, vol. 29, no. 31, pp. 4369–4377, 2010. View at Publisher · View at Google Scholar
  11. G. D. Dakubo, Mitochondrial Genetics and Cancer, Springer Science & Business Media, 2010.
  12. R. Moreno-Sánchez, S. Rodríguez-Enríquez, A. Marín-Hernández, and E. Saavedra, “Energy metabolism in tumor cells,” The FEBS Journal, vol. 274, no. 6, pp. 1393–1418, 2007. View at Publisher · View at Google Scholar
  13. N. Bellance, G. Benard, F. Furt et al., “Bioenergetics of lung tumors: alteration of mitochondrial biogenesis and respiratory capacity,” The International Journal of Biochemistry & Cell Biology, vol. 41, no. 12, pp. 2566–2577, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. G. Vander Heiden, “Targeting cancer metabolism: a therapeutic window opens,” Nature Reviews Drug Discovery, vol. 10, no. 9, pp. 671–684, 2011. View at Publisher · View at Google Scholar
  15. R. A. Cairns, I. S. Harris, and T. W. Mak, “Regulation of cancer cell metabolism,” Nature Reviews Cancer, vol. 11, no. 2, pp. 85–95, 2011. View at Publisher · View at Google Scholar
  16. G. L. Semenza, “HIF-1: upstream and downstream of cancer metabolism,” Current Opinion in Genetics & Development, vol. 20, no. 1, pp. 51–56, 1994. View at Publisher · View at Google Scholar
  17. C. V. Dang, “Rethinking the Warburg effect with Myc micromanaging glutamine metabolism,” Cancer Research, vol. 70, no. 3, pp. 859–862, 2010. View at Publisher · View at Google Scholar
  18. K. Bensaad, A. Tsuruta, M. A. Selak et al., “TIGAR, a p53-inducible regulator of glycolysis and apoptosis,” Cell, vol. 126, no. 1, pp. 107–120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Matoba, J.-G. Kang, W. D. Patino et al., “p53 regulates mitochondrial respiration,” Science, vol. 312, no. 5780, pp. 1650–1653, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Klein, E. Klein, and E. Kashuba, “Interaction of Epstein-Barr virus (EBV) with human B-lymphocytes,” Biochemical and Biophysical Research Communications, vol. 396, no. 1, pp. 67–73, 2010. View at Publisher · View at Google Scholar
  21. J. L. Hecht and J. C. Aster, “Molecular biology of Burkitt's lymphoma,” Journal of Clinical Oncology, vol. 18, no. 21, pp. 3707–3721, 2000. View at Google Scholar · View at Scopus
  22. A. ar-Rushdi, K. Nishikura, J. Erikson, R. Watt, G. Rovera, and C. M. Croce, “Differential expression of the translocated and the untranslocated c-myc oncogene in Burkitt lymphoma,” Science, vol. 222, no. 4622, pp. 390–393, 1983. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Mushtaq, S. Darekar, G. Klein, and E. Kashuba, “Different mechanisms of regulation of the Warburg effect in lymphoblastoid and Burkitt lymphoma cells,” PLoS ONE, vol. 10, no. 8, Article ID e0136142, 2015. View at Publisher · View at Google Scholar
  24. S. Darekar, K. Georgiou, M. Yurchenko et al., “Epstein-barr virus immortalization of human B-cells leads to stabilization of hypoxia-induced factor 1 alpha, congruent with the Warburg effect,” PLoS ONE, vol. 7, no. 7, Article ID e42072, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. P. H. Maxwell, M. S. Wiesener, G. W. Chang et al., “The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis,” Nature, vol. 399, no. 6733, pp. 271–275, 1999. View at Publisher · View at Google Scholar
  26. P. Jaakkola, D. R. Mole, Y.-M. Tian et al., “Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation,” Science, vol. 292, no. 5516, pp. 468–472, 2001. View at Publisher · View at Google Scholar
  27. M. Ivan, K. Kondo, H. Yang et al., “HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing,” Science, vol. 292, no. 5516, pp. 464–468, 2001. View at Publisher · View at Google Scholar
  28. M. A. McDonough, V. Li, E. Flashman et al., “Cellular oxygen sensing: crystal structure of hypoxia-inducible factor prolyl hydroxylase (PHD2),” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 26, pp. 9814–9819, 2006. View at Publisher · View at Google Scholar
  29. E. L. Page, D. A. Chan, A. J. Giaccia, M. Levine, and D. E. Richard, “Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion,” Molecular Biology of the Cell, vol. 19, no. 1, pp. 86–94, 2008. View at Publisher · View at Google Scholar
  30. O. Yogev, D. Lagos, T. Enver, C. Boshoff, and B. R. Cullen, “Kaposi's sarcoma herpesvirus microRNAs induce metabolic transformation of infected cells,” PLoS Pathogens, vol. 10, no. 9, Article ID e1004400, 2014. View at Publisher · View at Google Scholar
  31. T. Delgado, P. A. Carroll, A. S. Punjabi, D. Margineantu, D. M. Hockenbery, and M. Lagunoff, “Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells,” Proceedings of the National Academy of Sciences, vol. 107, no. 23, pp. 10696–10701, 2010. View at Publisher · View at Google Scholar
  32. A. Bravard, J. Beaumatin, C. Luccioni et al., “Chromosomal, mitochondrial and metabolic alterations in SV40-transformed rabbit chondrocytes,” Carcinogenesis, vol. 13, no. 5, pp. 767–772, 1992. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Ramanathan, C. Wang, and S. L. Schreiber, “Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 17, pp. 5992–5997, 2005. View at Publisher · View at Google Scholar
  34. P. Rodriguez-Viciana, C. Collins, and M. Fried, “Polyoma and SV40 proteins differentially regulate PP2A to activate distinct cellular signaling pathways involved in growth control,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 51, pp. 19290–19295, 2006. View at Publisher · View at Google Scholar
  35. R. L. Elstrom, D. E. Bauer, M. Buzzai et al., “Akt stimulates aerobic glycolysis in cancer cells,” Cancer Research, vol. 64, no. 11, pp. 3892–3899, 2004. View at Publisher · View at Google Scholar
  36. E. Noch, I. K. Sariyer, J. Gordon, and K. Khalili, “JC virus T-antigen regulates glucose metabolic pathways in brain tumor cells,” PLoS ONE, vol. 7, no. 4, Article ID e35054, 2012. View at Publisher · View at Google Scholar
  37. E. Madan, R. Gogna, M. Bhatt, U. Pati, P. Kuppusamy, and A. A. Mahdi, “Regulation of glucose metabolism by p53: emerging new roles for the tumor suppressor,” Oncotarget, vol. 2, no. 12, pp. 948–957, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. S. H. Ali and J. A. DeCaprio, “Cellular transformation by SV40 large T antigen: interaction with host proteins,” Seminars in Cancer Biology, vol. 11, no. 1, pp. 15–23, 2001. View at Publisher · View at Google Scholar
  39. C. Staib, J. Pesch, R. Gerwig et al., “p53 inhibits JC virus DNA replication in vivo and interacts with JC virus large T-antigen,” Virology, vol. 219, no. 1, pp. 237–246, 1996. View at Publisher · View at Google Scholar · View at Scopus
  40. C. V. Shivakumar and G. C. Das, “Interaction of human polyomavirus BK with the tumor-suppressor protein p53,” Oncogene, vol. 13, no. 2, pp. 323–332, 1996. View at Google Scholar · View at Scopus
  41. D. Lai, C. L. Tan, J. Gunaratne et al., “Localization of HPV-18 E2 at mitochondrial membranes induces ROS release and modulates host cell metabolism,” PLoS ONE, vol. 8, no. 9, Article ID e75625, 2013. View at Publisher · View at Google Scholar
  42. Y. Guo, X. Meng, J. Ma et al., “Human papillomavirus 16 E6 contributes HIF-1alpha induced Warburg effect by attenuating the VHL-HIF-1alpha interaction,” International Journal of Molecular Sciences, vol. 15, no. 5, pp. 7974–7986, 2014. View at Publisher · View at Google Scholar
  43. A. Ageyenko, I. Knm, V. T. Rimofeyev, I. Ya. Kogan, and A. N. Saprin, Glycolysis in Adenovirus Infected Rat Cell Cultures and in Adenovirus Type 12 Induced Hamster Sarcoma Cells, National Aeronautics and Space Administration, 1971.
  44. M. Thai, N. A. Graham, D. Braas et al., “Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication,” Cell Metabolism, vol. 19, no. 4, pp. 694–701, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. R. A. Gatenby and R. J. Gillies, “Why do cancers have high aerobic glycolysis?” Nature Reviews Cancer, vol. 4, no. 11, pp. 891–899, 2004. View at Publisher · View at Google Scholar
  46. M. J. Weber, “Hexose transport in normal and in Rous sarcoma virus-transformed cells,” The Journal of Biological Chemistry, vol. 248, no. 9, pp. 2978–2983, 1973. View at Google Scholar · View at Scopus
  47. M. B. Calvo, A. Figueroa, E. G. Pulido, R. G. Campelo, and L. A. Aparicio, “Potential role of sugar transporters in cancer and their relationship with anticancer therapy,” International Journal of Endocrinology, vol. 2010, Article ID 205357, 14 pages, 2010. View at Publisher · View at Google Scholar
  48. C. Barron, E. Tsiani, and T. Tsakiridis, “Expression of the glucose transporters GLUT1, GLUT3, GLUT4 and GLUT12 in human cancer cells,” BMC Proceedings, vol. 6, supplement 3, p. P4, 2012. View at Publisher · View at Google Scholar
  49. C. Chen, N. Pore, A. Behrooz, F. Ismail-Beigi, and A. Maity, “Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia,” Journal of Biological Chemistry, vol. 276, no. 12, pp. 9519–9525, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Yu, T. G. Maguire, and J. C. Alwine, “Human cytomegalovirus activates glucose transporter 4 expression to increase glucose uptake during infection,” Journal of Virology, vol. 85, no. 4, pp. 1573–1580, 2011. View at Publisher · View at Google Scholar
  51. R. Gonnella, R. Santarelli, A. Farina et al., “Kaposi sarcoma associated herpesvirus (KSHV) induces AKT hyperphosphorylation, bortezomib-resistance and GLUT-1 plasma membrane exposure in THP-1 monocytic cell line,” Journal of Experimental & Clinical Cancer Research, vol. 32, article 79, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. T. G. Sommermann, K. O'Neill, D. R. Plas, and E. Cahir-McFarland, “IKKκ and NF-κB transcription govern lymphoma cell survival through AKT-induced plasma membrane trafficking of GLUT1,” Cancer Research, vol. 71, no. 23, pp. 7291–7300, 2011. View at Publisher · View at Google Scholar
  53. N. Leiprecht, C. Munoz, I. Alesutan et al., “Regulation of Na+-coupled glucose carrier SGLT1 by human papillomavirus 18 E6 protein,” Biochemical and Biophysical Research Communications, vol. 404, no. 2, pp. 695–700, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Kitagawa, H. Nishino, and A. Iwashima, “Analysis of hexose transport in untransformed and sarcoma virus-transformed mouse 3T3 cells by photoaffinity binding of cytochalasin B,” Biochimica et Biophysica Acta (BBA)–Biomembranes, vol. 821, no. 1, pp. 63–66, 1985. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Stern, S. Shuster, B. A. Neudecker, and B. Formby, “Lactate stimulates fibroblast expression of hyaluronan and CD44: the Warburg effect revisited,” Experimental Cell Research, vol. 276, no. 1, pp. 24–31, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Nasi, T. Fekete, A. Krishnamurthy et al., “Dendritic cell reprogramming by endogenously produced lactic acid,” The Journal of Immunology, vol. 191, no. 6, pp. 3090–3099, 2013. View at Publisher · View at Google Scholar
  57. E. Gottfried, L. A. Kunz-Schughart, S. Ebner et al., “Tumor-derived lactic acid modulates dendritic cell activation and antigen expression,” Blood, vol. 107, no. 5, pp. 2013–2021, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. K. Brand, J. F. Williams, and M. J. Weidemann, “Glucose and glutamine metabolism in rat thymocytes,” Biochemical Journal, vol. 221, no. 2, pp. 471–475, 1984. View at Publisher · View at Google Scholar
  59. K. Brand, W. Leibold, P. Luppa, C. Schoerner, and A. Schulz, “Metabolic alterations associated with proliferation of mitogen-activated lymphocytes and of lymphoblastoid cell lines: evaluation of glucose and glutamine metabolism,” Immunobiology, vol. 173, no. 1, pp. 23–34, 1986. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Brand, R. Netzker, U. Aulwurm et al., “Control of thymocyte proliferation via redox-regulated expression of glycolytic genes,” Redox Report, vol. 5, no. 1, pp. 52–54, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Fischer, P. Hoffmann, S. Voelkl et al., “Inhibitory effect of tumor cell-derived lactic acid on human T cells,” Blood, vol. 109, no. 9, pp. 3812–3819, 2007. View at Publisher · View at Google Scholar
  62. S. Beckert, F. Farrahi, R. S. Aslam et al., “Lactate stimulates endothelial cell migration,” Wound Repair and Regeneration, vol. 14, no. 3, pp. 321–324, 2006. View at Publisher · View at Google Scholar
  63. G.-X. Ruan and A. Kazlauskas, “Lactate engages receptor tyrosine kinases Axl, Tie2, and vascular endothelial growth factor receptor 2 to activate phosphoinositide 3-kinase/AKT and promote angiogenesis,” The Journal of Biological Chemistry, vol. 288, no. 29, pp. 21161–21172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. B. Deuticke, “Monocarboxylate transport in erythrocytes,” The Journal of Membrane Biology, vol. 70, no. 2, pp. 89–103, 1982. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Bonen, M. Tonouchi, D. Miskovic, C. Heddle, J. J. Heikkila, and A. P. Halestrap, “Isoform-specific regulation of the lactate transporters MCT1 and MCT4 by contractile activity,” American Journal of Physiology—Endocrinology and Metabolism, vol. 279, no. 5, pp. E1131–E1138, 2000. View at Google Scholar · View at Scopus
  66. S. Bröer, A. Bröer, H.-P. Schneider, C. Stegen, A. P. Halestrap, and J. W. Deitmer, “Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes,” Biochemical Journal, vol. 341, part 3, pp. 529–535, 1999. View at Publisher · View at Google Scholar · View at Scopus
  67. E. F. Grollman, N. J. Philp, P. McPhie, R. D. Ward, and B. Sauer, “Determination of transport kinetics of chick MCT3 monocarboxylate transporter from retinal pigment epithelium by expression in genetically modified yeast,” Biochemistry, vol. 39, no. 31, pp. 9351–9357, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. A. P. Halestrap and D. Meredith, “The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond,” Pflugers Archiv, vol. 447, no. 5, pp. 619–628, 2004. View at Publisher · View at Google Scholar · View at Scopus
  69. B. Amit-Cohen, M. M. Rahat, and M. A. Rahat, “Tumor cell-macrophage interactions increase angiogenesis through secretion of EMMPRIN,” Frontiers in Physiology, vol. 4, article 178, 2013. View at Publisher · View at Google Scholar
  70. N. Dupin, C. Fisher, P. Kellam et al., “Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 8, pp. 4546–4551, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. A. J. Barbera, J. V. Chodaparambil, B. Kelley-Clarke et al., “The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA,” Science, vol. 311, no. 5762, pp. 856–861, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Pinheiro, E. A. Garcia, F. Morais-Santos et al., “Lactate transporters and vascular factors in HPV-induced squamous cell carcinoma of the uterine cervix,” BMC Cancer, vol. 14, article 751, 2014. View at Publisher · View at Google Scholar