Cytomegalovirus as an oncomodulatory agent in the progression of glioma

Cancer Letters

Volumn 384, Issue , 2017, Pages 79-85

  Joseph, Gabriel P ^a   McDermott, Ryan ^b   Baryshnikova, Maria A ^c   Cobbs, Charles S ^a   Ulasov, Ilya V ^a,c  

^a SWEDISH MEDICAL CENTER   (United States)

^b University of San Antonio   (United States)

^c N N BLOKHIN RUSSIAN CANCER RESEARCH CENTER   (Russian Federation)

Author keywords

Brain tumor; CMV; Glioblastoma; Oncomodulatory agent

Indexed keywords

APOPTOSIS; AUTOPHAGY; CANCER CELL DESTRUCTION; CANCER RECURRENCE; CANCER STEM CELL; CANCER SURVIVAL; CELL CYCLE; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; GLIOMA; HUMAN; IMMUNOMODULATION; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; TUMOR GROWTH; TUMOR VASCULARIZATION; ANIMAL; BRAIN NEOPLASMS; CELL PROLIFERATION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DISEASE COURSE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PATHOLOGY; TUMOR ESCAPE; TUMOR VIRUS INFECTIONS; VIROLOGY; VIRUS CELL TRANSFORMATION;

AUTACOID;

ANIMALS; APOPTOSIS; BRAIN NEOPLASMS; CELL CYCLE; CELL PROLIFERATION; CELL TRANSFORMATION, VIRAL; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DISEASE PROGRESSION; GLIOMA; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION MEDIATORS; TUMOR ESCAPE; TUMOR VIRUS INFECTIONS;

EID: 84994047651     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.10.022     Document Type: Review

References (100)

1. [1] Polley, M.Y., Lamborn, K.R., Chang, S.M., Butowski, N., Clarke, J.L., Prados, M., Conditional probability of survival in patients with newly diagnosed glioblastoma. J. Clin. Oncol. 29 (2011), 4175–4180.
2. [2] Lehrer, S., Cytomegalovirus infection in early childhood may be protective against glioblastoma multiforme, while later infection is a risk factor. Med. Hypotheses 78 (2012), 657–658.
3. [3] Muquit, S., Parks, R., Basu, S., Socio-economic characteristics of patients with glioblastoma multiforme. J. Neurooncol. 125 (2015), 325–329.
4. [4] Anic, G.M., Madden, M.H., Sincich, K., Thompson, R.C., Nabors, L.B., Olson, J.J., LaRocca, R.V., Browning, J.E., Pan, E., Egan, K.M., Early life exposures and the risk of adult glioma. Eur. J. Epidemiol. 28 (2013), 753–758.
5. [5] Cobbs, C.S., Harkins, L., Samanta, M., Gillespie, G.Y., Bharara, S., King, P.H., Nabors, L.B., Cobbs, C.G., Britt, W.J., Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res. 62 (2002), 3347–3350.
6. [6] Wick, W., Wick, A., Platten, M., Challenging cytomegalovirus data in glioblastoma. Neuro Oncol., 16, 2014, 165.
7. [7] Soderberg-Naucler, C., Rahbar, A., Stragliotto, G., Survival in patients with glioblastoma receiving valganciclovir. N. Engl. J. Med. 369 (2013), 985–986.
8. [8] Saccoccio, F.M., Gallagher, M.K., Adler, S.P., McVoy, M.A., Neutralizing activity of saliva against cytomegalovirus. Clin. Vaccine Immunol. 18 (2011), 1536–1542.
9. [9] Ryckman, B.J., Rainish, B.L., Chase, M.C., Borton, J.A., Nelson, J.A., Jarvis, M.A., Johnson, D.C., Characterization of the human cytomegalovirus gH/gL/UL128-131 complex that mediates entry into epithelial and endothelial cells. J. Virol. 82 (2008), 60–70.
10. [10] Preece, P.M., Blount, J.M., Glover, J., Fletcher, G.M., Peckham, C.S., Griffiths, P.D., The consequences of primary cytomegalovirus infection in pregnancy. Arch. Dis. Child. 58 (1983), 970–975.
11. [11] Huang, E.S., Roche, J.K., Cytomegalovirus D.N.A. and adenocarcinoma of the colon: evidence for latent viral infection. Lancet 1 (1978), 957–960.
12. [12] Salyakina, D., Tsinoremas, N.F., Viral expression associated with gastrointestinal adenocarcinomas in TCGA high-throughput sequencing data. Hum. Genomics, 7, 2013, 23.
13. [13] Boldogh, I., Fons, M.P., Albrecht, T., Increased levels of sequence-specific DNA-binding proteins in human cytomegalovirus-infected cells. Biochem. Biophys. Res. Commun. 197 (1993), 1505–1510.
14. [14] Harkins, L.E., Matlaf, L.A., Soroceanu, L., Klemm, K., Britt, W.J., Wang, W., Bland, K.I., Cobbs, C.S., Detection of human cytomegalovirus in normal and neoplastic breast epithelium. Herpesviridae, 1, 2010, 8.
15. [15] Melnick, M., Sedghizadeh, P.P., Allen, C.M., Jaskoll, T., Human cytomegalovirus and mucoepidermoid carcinoma of salivary glands: cell-specific localization of active viral and oncogenic signaling proteins is confirmatory of a causal relationship. Exp. Mol. Pathol. 92 (2012), 118–125.
16. [16] Taher, C., de Boniface, J., Mohammad, A.A., Religa, P., Hartman, J., Yaiw, K.C., Frisell, J., Rahbar, A., Soderberg-Naucler, C., High prevalence of human cytomegalovirus proteins and nucleic acids in primary breast cancer and metastatic sentinel lymph nodes. PLoS One, 8, 2013, e56795.
17. [17] Bishop, R.K., Valle Oseguera, C.A., Spencer, J.V., Human cytomegalovirus interleukin-10 promotes proliferation and migration of MCF-7 breast cancer cells. Cancer Cell Microenviron., 2, 2015.
18. [18] Cimino, P.J., Zhao, G., Wang, D., Sehn, J.K., Lewis, J.S. Jr., Duncavage, E.J., Detection of viral pathogens in high grade gliomas from unmapped next-generation sequencing data. Exp. Mol. Pathol. 96 (2014), 310–315.
19. [19] Tang, K.W., Hellstrand, K., Larsson, E., Absence of cytomegalovirus in high-coverage DNA sequencing of human glioblastoma multiforme. Int. J. Cancer 136 (2015), 977–981.
20. [20] Yamashita, Y., Ito, Y., Isomura, H., Takemura, N., Okamoto, A., Motomura, K., Tsujiuchi, T., Natsume, A., Wakabayashi, T., Toyokuni, S., Tsurumi, T., Lack of presence of the human cytomegalovirus in human glioblastoma. Mod. Pathol. 27 (2014), 922–929.
21. [21] Dziurzynski, K., Wei, J., Qiao, W., Hatiboglu, M.A., Kong, L.Y., Wu, A., Wang, Y., Cahill, D., Levine, N., Prabhu, S., Rao, G., Sawaya, R., Heimberger, A.B., Glioma-associated cytomegalovirus mediates subversion of the monocyte lineage to a tumor propagating phenotype. Clin. Cancer Res. 17 (2011), 4642–4649.
22. [22] Ho, K.L., Gottlieb, C., Zarbo, R.J., Cytomegalovirus infection of cerebral astrocytoma in an AIDS patient. Clin. Neuropathol. 10 (1991), 127–133.
23. [23] Lau, S.K., Chen, Y.Y., Chen, W.G., Diamond, D.J., Mamelak, A.N., Zaia, J.A., Weiss, L.M., Lack of association of cytomegalovirus with human brain tumors. Mod. Pathol. 18 (2005), 838–843.
24. [24] Cobbs, C., Response to “Human cytomegalovirus infection in tumor cells of the nervous system is not detectable with standardized pathologico-virological diagnostics”. Neuro Oncol. 16 (2014), 1435–1436.
25. [25] Soroceanu, L., Matlaf, L., Bezrookove, V., Harkins, L., Martinez, R., Greene, M., Soteropoulos, P., Cobbs, C.S., Human cytomegalovirus US28 found in glioblastoma promotes an invasive and angiogenic phenotype. Cancer Res. 71 (2011), 6643–6653.
26. [26] Bhattacharjee, B., Renzette, N., Kowalik, T.F., Genetic analysis of cytomegalovirus in malignant gliomas. J. Virol. 86 (2012), 6815–6824.
27. [27] Ranganathan, P., Clark, P.A., Kuo, J.S., Salamat, M.S., Kalejta, R.F., Significant association of multiple human cytomegalovirus genomic Loci with glioblastoma multiforme samples. J. Virol. 86 (2012), 854–864.
28. [28] Cobbs, C., Khan, S., Matlaf, L., McAllister, S., Zider, A., Yount, G., Rahlin, K., Harkins, L., Bezrookove, V., Singer, E., Soroceanu, L., HCMV glycoprotein B is expressed in primary glioblastomas and enhances growth and invasiveness via PDGFR-alpha activation. Oncotarget 5 (2014), 1091–1100.
29. [29] Smith, M.G., Propagation in tissue cultures of a cytopathogenic virus from human salivary gland virus (SGV) disease. Proc. Soc. Exp. Biol. Med. 92 (1956), 424–430.
30. [30] Craig, J.M., Macauley, J.C., Weller, T.H., Wirth, P., Isolation of intranuclear inclusion producing agents from infants with illnesses resembling cytomegalic inclusion disease. Proc. Soc. Exp. Biol. Med. 94 (1957), 4–12.
31. [31] Brennan, D.C., Cytomegalovirus in renal transplantation. J. Am. Soc. Nephrol. 12 (2001), 848–855.
32. [32] Babu, S.G., Pandeya, A., Verma, N., Shukla, N., Kumar, R.V., Saxena, S., Role of HCMV miR-UL70-3p and miR-UL148D in overcoming the cellular apoptosis. Mol. Cell Biochem., 2014.
33. [33] Soderberg-Naucler, C., Johnsen, J.I., Cytomegalovirus infection in brain tumors: a potential new target for therapy?. Oncoimmunology 1 (2012), 739–740.
34. [34] Soroceanu, L., Cobbs, C.S., Is HCMV a tumor promoter?. Virus Res. 157 (2011), 193–203.
35. [35] Jault, F.M., Jault, J.M., Ruchti, F., Fortunato, E.A., Clark, C., Corbeil, J., Richman, D.D., Spector, D.H., Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J. Virol. 69 (1995), 6697–6704.
36. [36] Frolov, M.V., Dyson, N.J., Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J. Cell Sci. 117 (2004), 2173–2181.
37. [37] McLaughlin-Drubin, M.E., Munger, K., The human papillomavirus E7 oncoprotein. Virology 384 (2009), 335–344.
38. [38] Dittmer, D., Mocarski, E.S., Human cytomegalovirus infection inhibits G1/S transition. J. Virol. 71 (1997), 1629–1634.
39. [39] Fry, A.M., Meraldi, P., Nigg, E.A., A centrosomal function for the human Nek2 protein kinase, a member of the NIMA family of cell cycle regulators. EMBO J. 17 (1998), 470–481.
40. [40] Tschopp, J., Thome, M., Hofmann, K., Meinl, E., The fight of viruses against apoptosis. Curr. Opin. Genet. Dev. 8 (1998), 82–87.
41. [41] Zhu, H., Shen, Y., Shenk, T., Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J. Virol. 69 (1995), 7960–7970.
42. [42] Paulus, C., Nevels, M., The human cytomegalovirus major immediate-early proteins as antagonists of intrinsic and innate antiviral host responses. Viruses 1 (2009), 760–779.
43. [43] Lukac, D.M., Alwine, J.C., Effects of human cytomegalovirus major immediate-early proteins in controlling the cell cycle and inhibiting apoptosis: studies with ts13 cells. J. Virol. 73 (1999), 2825–2831.
44. [44] Cobbs, C.S., Soroceanu, L., Denham, S., Zhang, W., Britt, W.J., Pieper, R., Kraus, M.H., Human cytomegalovirus induces cellular tyrosine kinase signaling and promotes glioma cell invasiveness. J. Neurooncol. 85 (2007), 271–280.
45. [45] Kroemer, G., Galluzzi, L., Brenner, C., Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87 (2007), 99–163.
46. [46] Goldmacher, V.S., Bartle, L.M., Skaletskaya, A., Dionne, C.A., Kedersha, N.L., Vater, C.A., Han, J.W., Lutz, R.J., Watanabe, S., Cahir McFarland, E.D., Kieff, E.D., Mocarski, E.S., Chittenden, T., A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 12536–12541.
47. [47] Hertel, L., Mocarski, E.S., Global analysis of host cell gene expression late during cytomegalovirus infection reveals extensive dysregulation of cell cycle gene expression and induction of Pseudomitosis independent of US28 function. J. Virol. 78 (2004), 11988–12011.
48. [48] Sharon-Friling, R., Goodhouse, J., Colberg-Poley, A.M., Shenk, T., Human cytomegalovirus pUL37x1 induces the release of endoplasmic reticulum calcium stores. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 19117–19122.
49. [49] Poncet, D., Pauleau, A.L., Szabadkai, G., Vozza, A., Scholz, S.R., Le Bras, M., Briere, J.J., Jalil, A., Le Moigne, R., Brenner, C., Hahn, G., Wittig, I., Schagger, H., Lemaire, C., Bianchi, K., Souquere, S., Pierron, G., Rustin, P., Goldmacher, V.S., Rizzuto, R., Palmieri, F., Kroemer, G., Cytopathic effects of the cytomegalovirus-encoded apoptosis inhibitory protein vMIA. J. Cell Biol. 174 (2006), 985–996.
50. [50] Arnoult, D., Bartle, L.M., Skaletskaya, A., Poncet, D., Zamzami, N., Park, P.U., Sharpe, J., Youle, R.J., Goldmacher, V.S., Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 7988–7993.
51. [51] Isler, J.A., Skalet, A.H., Alwine, J.C., Human cytomegalovirus infection activates and regulates the unfolded protein response. J. Virol. 79 (2005), 6890–6899.
52. [52] Fliss, P.M., Brune, W., Prevention of cellular suicide by cytomegaloviruses. Viruses 4 (2012), 1928–1949.
53. [53] Szegezdi, E., Logue, S.E., Gorman, A.M., Samali, A., Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7 (2006), 880–885.
54. [54] Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H.P., Ron, D., Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287 (2000), 664–666.
55. [55] Kang, R., Zeh, H.J., Lotze, M.T., Tang, D., The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18 (2011), 571–580.
56. [56] Zhang, T., Li, Y., Park, K.A., Byun, H.S., Won, M., Jeon, J., Lee, Y., Seok, J.H., Choi, S.W., Lee, S.H., Man Kim, J., Lee, J.H., Son, C.G., Lee, Z.W., Shen, H.M., Hur, G.M., Cucurbitacin induces autophagy through mitochondrial ROS production which counteracts to limit caspase-dependent apoptosis. Autophagy 8 (2012), 559–576.
57. [57] Chaumorcel, M., Souquere, S., Pierron, G., Codogno, P., Esclatine, A., Human cytomegalovirus controls a new autophagy-dependent cellular antiviral defense mechanism. Autophagy 4 (2008), 46–53.
58. [58] Chaumorcel, M., Lussignol, M., Mouna, L., Cavignac, Y., Fahie, K., Cotte-Laffitte, J., Geballe, A., Brune, W., Beau, I., Codogno, P., Esclatine, A., The human cytomegalovirus protein TRS1 inhibits autophagy via its interaction with Beclin 1. J. Virol. 86 (2012), 2571–2584.
59. [59] McFarlane, S., Aitken, J., Sutherland, J.S., Nicholl, M.J., Preston, V.G., Preston, C.M., Early induction of autophagy in human fibroblasts after infection with human cytomegalovirus or herpes simplex virus 1. J. Virol. 85 (2011), 4212–4221.
60. [60] Streblow, D.N., Kreklywich, C.N., Andoh, T., Moses, A.V., Dumortier, J., Smith, P.P., Defilippis, V., Fruh, K., Nelson, J.A., Orloff, S.L., The role of angiogenic and wound repair factors during CMV-accelerated transplant vascular sclerosis in rat cardiac transplants. Am. J. Transpl. 8 (2008), 277–287.
61. [61] Botto, S., Streblow, D.N., DeFilippis, V., White, L., Kreklywich, C.N., Smith, P.P., Caposio, P., IL-6 in human cytomegalovirus secretome promotes angiogenesis and survival of endothelial cells through the stimulation of survivin. Blood 117 (2011), 352–361.
62. [62] Fiorentini, S., Luganini, A., Dell'Oste, V., Lorusso, B., Cervi, E., Caccuri, F., Bonardelli, S., Landolfo, S., Caruso, A., Gribaudo, G., Human cytomegalovirus productively infects lymphatic endothelial cells and induces a secretome that promotes angiogenesis and lymphangiogenesis through interleukin-6 and granulocyte-macrophage colony-stimulating factor. J. Gen. Virol. 92 (2011), 650–660.
63. [63] Maussang, D., Langemeijer, E., Fitzsimons, C.P., Stigter-van Walsum, M., Dijkman, R., Borg, M.K., Slinger, E., Schreiber, A., Michel, D., Tensen, C.P., van Dongen, G.A., Leurs, R., Smit, M.J., The human cytomegalovirus-encoded chemokine receptor US28 promotes angiogenesis and tumor formation via cyclooxygenase-2. Cancer Res. 69 (2009), 2861–2869.
64. [64] Matlaf, L.A., Harkins, L.E., Bezrookove, V., Cobbs, C.S., Soroceanu, L., Cytomegalovirus pp71 protein is expressed in human glioblastoma and promotes pro-angiogenic signaling by activation of stem cell factor. PLoS One, 8, 2013, e68176.
65. [65] Zhang, S., Liu, L., Wang, R., Tuo, H., Guo, Y., Yi, L., Wang, D., Wang, J., MicroRNA-217 promotes angiogenesis of human cytomegalovirus-infected endothelial cells through downregulation of SIRT1 and FOXO3A. PLoS One, 8, 2013, e83620.
66. [66] Zhang, S., Liu, L., Wang, R., Tuo, H., Guo, Y., Yi, L., Wang, J., Wang, D., MiR-199a-5p promotes migration and tube formation of human cytomegalovirus-infected endothelial cells through downregulation of SIRT1 and eNOS. Arch. Virol. 158 (2013), 2443–2452.
67. [67] Powers, C., DeFilippis, V., Malouli, D., Fruh, K., Cytomegalovirus immune evasion. Curr. Top. Microbiol. Immunol. 325 (2008), 333–359.
68. [68] Jarvis, M.A., Borton, J.A., Keech, A.M., Wong, J., Britt, W.J., Magun, B.E., Nelson, J.A., Human cytomegalovirus attenuates interleukin-1beta and tumor necrosis factor alpha proinflammatory signaling by inhibition of NF-kappaB activation. J. Virol. 80 (2006), 5588–5598.
69. [69] Montag, C., Wagner, J., Gruska, I., Hagemeier, C., Human cytomegalovirus blocks tumor necrosis factor alpha- and interleukin-1beta-mediated NF-kappaB signaling. J. Virol. 80 (2006), 11686–11698.
70. [70] Taylor, R.T., Bresnahan, W.A., Human cytomegalovirus immediate-early 2 gene expression blocks virus-induced beta interferon production. J. Virol. 79 (2005), 3873–3877.
71. [71] Taylor, R.T., Bresnahan, W.A., Human cytomegalovirus immediate-early 2 protein IE86 blocks virus-induced chemokine expression. J. Virol. 80 (2006), 920–928.
72. [72] Gealy, C., Humphreys, C., Dickinson, V., Stinski, M., Caswell, R., An activation-defective mutant of the human cytomegalovirus IE2p86 protein inhibits NF-kappaB-mediated stimulation of the human interleukin-6 promoter. J. Gen. Virol. 88 (2007), 2435–2440.
73. [73] Boehme, K.W., Singh, J., Perry, S.T., Compton, T., Human cytomegalovirus elicits a coordinated cellular antiviral response via envelope glycoprotein B. J. Virol. 78 (2004), 1202–1211.
74. [74] Yoo, Y.D., Chiou, C.J., Choi, K.S., Yi, Y., Michelson, S., Kim, S., Hayward, G.S., Kim, S.J., The IE2 regulatory protein of human cytomegalovirus induces expression of the human transforming growth factor beta1 gene through an Egr-1 binding site. J. Virol. 70 (1996), 7062–7070.
75. [75] Cheeran, M.C., Hu, S., Yager, S.L., Gekker, G., Peterson, P.K., Lokensgard, J.R., Cytomegalovirus induces cytokine and chemokine production differentially in microglia and astrocytes: antiviral implications. J. Neurovirol. 7 (2001), 135–147.
76. [76] Weinshenker, B.G., Wilton, S., Rice, G.P., Phorbol ester-induced differentiation permits productive human cytomegalovirus infection in a monocytic cell line. J. Immunol. 140 (1988), 1625–1631.
77. [77] Zou, Y., Bresnahan, W., Taylor, R.T., Stastny, P., Effect of human cytomegalovirus on expression of MHC class I-related chains A. J. Immunol. 174 (2005), 3098–3104.
78. [78] Cheeran, M.C., Hu, S., Ni, H.T., Sheng, W., Palmquist, J.M., Peterson, P.K., Lokensgard, J.R., Neural precursor cell susceptibility to human cytomegalovirus diverges along glial or neuronal differentiation pathways. J. Neurosci. Res. 82 (2005), 839–850.
79. [79] Odeberg, J., Wolmer, N., Falci, S., Westgren, M., Seiger, A., Soderberg-Naucler, C., Human cytomegalovirus inhibits neuronal differentiation and induces apoptosis in human neural precursor cells. J. Virol. 80 (2006), 8929–8939.
80. [80] Odeberg, J., Wolmer, N., Falci, S., Westgren, M., Sundtrom, E., Seiger, A., Soderberg-Naucler, C., Late human cytomegalovirus (HCMV) proteins inhibit differentiation of human neural precursor cells into astrocytes. J. Neurosci. Res. 85 (2007), 583–593.
81. [81] Pan, X., Li, X.J., Liu, X.J., Yuan, H., Li, J.F., Duan, Y.L., Ye, H.Q., Fu, Y.R., Qiao, G.H., Wu, C.C., Yang, B., Tian, X.H., Hu, K.H., Miao, L.F., Chen, X.L., Zheng, J., Rayner, S., Schwartz, P.H., Britt, W.J., Xu, J., Luo, M.H., Later passages of neural progenitor cells from neonatal brain are more permissive for human cytomegalovirus infection. J. Virol. 87 (2013), 10968–10979.
82. [82] Luo, M.H., Schwartz, P.H., Fortunato, E.A., Neonatal neural progenitor cells and their neuronal and glial cell derivatives are fully permissive for human cytomegalovirus infection. J. Virol. 82 (2008), 9994–10007.
83. [83] Fiallos, E., Judkins, J., Matlaf, L., Prichard, M., Dittmer, D., Cobbs, C., Soroceanu, L., Human cytomegalovirus gene expression in long-term infected glioma stem cells. PLoS One, 9, 2014, e116178.
84. [84] Soroceanu, L., Matlaf, L., Khan, S., Akhavan, A., Singer, E., Bezrookove, V., Decker, S., Ghanny, S., Hadaczek, P., Bengtsson, H., Ohlfest, J., Luciani-Torres, M.G., Harkins, L., Perry, A., Guo, H., Soteropoulos, P., Cobbs, C.S., Cytomegalovirus immediate-early proteins promote stemness properties in glioblastoma. Cancer Res. 75 (2015), 3065–3076.
85. [85] Fielding, C.A., Aicheler, R., Stanton, R.J., Wang, E.C., Han, S., Seirafian, S., Davies, J., McSharry, B.P., Weekes, M.P., Antrobus, P.R., Prod'homme, V., Blanchet, F.P., Sugrue, D., Cuff, S., Roberts, D., Davison, A.J., Lehner, P.J., Wilkinson, G.W., Tomasec, P., Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLoS Pathog., 10, 2014, e1004058.
86. [86] Hook, L.M., Grey, F., Grabski, R., Tirabassi, R., Doyle, T., Hancock, M., Landais, I., Jeng, S., McWeeney, S., Britt, W., Nelson, J.A., Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe 15 (2014), 363–373.
87. [87] Shen, Z.Z., Pan, X., Miao, L.F., Ye, H.Q., Chavanas, S., Davrinche, C., McVoy, M., Luo, M.H., Comprehensive analysis of human cytomegalovirus microRNA expression during lytic and quiescent infection. PLoS One, 9, 2014, e88531.
88. [88] Huang, Y., Qi, Y., Ma, Y., He, R., Ji, Y., Sun, Z., Ruan, Q., Down-regulation of human cytomegalovirus UL138, a novel latency-associated determinant, by hcmv-miR-UL36. J. Biosci. 38 (2013), 479–485.
89. [89] Skaletskaya, A., Bartle, L.M., Chittenden, T., McCormick, A.L., Mocarski, E.S., Goldmacher, V.S., A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 7829–7834.
90. [90] Qi, M., Qi, Y., Ma, Y., He, R., Ji, Y., Sun, Z., Ruan, Q., Over-expression of human cytomegalovirus miR-US25-2-3p downregulates eIF4A1 and inhibits HCMV replication. FEBS Lett. 587 (2013), 2266–2271.
91. [91] Wang, Y.P., Qi, Y., Huang, Y.J., Qi, M.L., Ma, Y.P., He, R., Ji, Y.H., Sun, Z.R., Ruan, Q., Identification of immediate early gene X-1 as a cellular target gene of hcmv-mir-UL148D. Int. J. Mol. Med. 31 (2013), 959–966.
92. [92] Huang, Y., Qi, Y., Ma, Y., He, R., Ji, Y., Sun, Z., Ruan, Q., The expression of interleukin-32 is activated by human cytomegalovirus infection and down regulated by hcmv-miR-UL112-1. Virol. J., 10, 2013, 51.
93. [93] Cobbs, C.S., Soroceanu, L., Denham, S., Zhang, W., Kraus, M.H., Modulation of oncogenic phenotype in human glioma cells by cytomegalovirus IE1-mediated mitogenicity. Cancer Res. 68 (2008), 724–730.
94. [94] Zydek, M., Hagemeier, C., Wiebusch, L., Cyclin-dependent kinase activity controls the onset of the HCMV lytic cycle. PLoS Pathog., 6, 2010, e1001096.
95. [95] Xuan, B., Qian, Z., Torigoi, E., Yu, D., Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death. J. Virol. 83 (2009), 3463–3474.
96. [96] Stropes, M.P., Schneider, O.D., Zagorski, W.A., Miller, J.L., Miller, W.E., The carboxy-terminal tail of human cytomegalovirus (HCMV) US28 regulates both chemokine-independent and chemokine-dependent signaling in HCMV-infected cells. J. Virol. 83 (2009), 10016–10027.
97. [97] Slinger, E., Maussang, D., Schreiber, A., Siderius, M., Rahbar, A., Fraile-Ramos, A., Lira, S.A., Soderberg-Naucler, C., Smit, M.J., HCMV-encoded chemokine receptor US28 mediates proliferative signaling through the IL-6-STAT3 axis. Sci. Signal, 3, 2010, ra58.
98. [98] Park, B., Spooner, E., Houser, B.L., Strominger, J.L., Ploegh, H.L., The HCMV membrane glycoprotein US10 selectively targets HLA-G for degradation. J. Exp. Med. 207 (2010), 2033–2041.
99. [99] Arcangeletti, M.C., Rodighiero, I., Mirandola, P., De Conto, F., Covan, S., Germini, D., Razin, S., Dettori, G., Chezzi, C., Cell-cycle-dependent localization of human cytomegalovirus UL83 phosphoprotein in the nucleolus and modulation of viral gene expression in human embryo fibroblasts in vitro. J. Cell Biochem. 112 (2011), 307–317.
100. [100] Stahl, S., Burkhart, J.M., Hinte, F., Tirosh, B., Mohr, H., Zahedi, R.P., Sickmann, A., Ruzsics, Z., Budt, M., Brune, W., Cytomegalovirus downregulates IRE1 to repress the unfolded protein response. PLoS Pathog., 9, 2013, e1003544.