The Wnt pathway: a key network in cell signalling dysregulated by viruses

Reviews in Medical Virology

Volumn 26, Issue 5, 2016, Pages 340-355

  van Zuylen, Wendy J ^a,b   Rawlinson, William D ^a,b   Ford, Caroline E ^b  

^a PRINCE OF WALES HOSPITAL   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MICRORNA; VIRUS RNA;

CARCINOGENESIS; CYTOMEGALOVIRUS; DISEASE ASSOCIATION; EPIGENETICS; EPSTEIN BARR VIRUS; GENE; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS; MODULATION; NONHUMAN; PATHOGENESIS; REVIEW; VIRUS CELL INTERACTION; WART VIRUS; WNT SIGNALING PATHWAY;

EID: 84985987004     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.1892     Document Type: Review

References (119)

1. de Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncology 2012; 13: 607–615. DOI:10.1016/s1470-2045(12)70137-7.
2. Fujiwara S, Imadome K, Takei M. Modeling EBV infection and pathogenesis in new-generation humanized mice. Experimental and Molecular Medicine 2015; 47: e135. DOI:10.1038/emm.2014.88.
3. Cobbs CS. Cytomegalovirus and brain tumor: epidemiology, biology and therapeutic aspects. Current Opinion in Oncology 2013; 25: 682–688. DOI:10.1097/cco.0000000000000005.
4. Kempkes B, Robertson ES. Epstein–Barr virus latency: current and future perspectives. Current Opinion Virology 2015; 14: 138–144. DOI:10.1016/j.coviro.2015.09.007.
5. Cobbs CS, Harkins L, Samanta M, et al. Human cytomegalovirus infection and expression in human malignant glioma. Cancer Research 2002; 62: 3347–3350.
6. Ranganathan P, Clark PA, Kuo JS, Salamat MS, Kalejta RF. Significant association of multiple human cytomegalovirus genomic Loci with glioblastoma multiforme samples. Journal of Virology 2012; 86: 854–864. DOI:10.1128/jvi.06097-11.
7. Bhutani M, Polizzotto MN, Uldrick TS, Yarchoan R. Kaposi sarcoma-associated herpesvirus-associated malignancies: epidemiology, pathogenesis, and advances in treatment. Seminars in Oncology 2015; 42: 223–246. DOI:10.1053/j.seminoncol.2014.12.027.
8. Chan SL, Wong VW, Qin S, Chan HL. Infection and cancer: the case of hepatitis B. Journal of Clinical Oncology 2016; 34: 83–90. DOI:10.1200/jco.2015.61.5724.
9. Tholey DM, Ahn J. Impact of hepatitis C virus infection on hepatocellular carcinoma. Gastroenterology Clinics of North America 2015; 44: 761–773. DOI:10.1016/j.gtc.2015.07.005.
10. Frazer IH, Leggatt GR, Mattarollo SR. Prevention and treatment of papillomavirus-related cancers through immunization. Annual Review of Immunology 2011; 29: 111–138. DOI:10.1146/annurev-immunol-031210-101308.
11. Weinberger PM, Yu Z, Kountourakis P, et al. Defining molecular phenotypes of human papillomavirus-associated oropharyngeal squamous cell carcinoma: validation of three-class hypothesis. Otolaryngology and Head and Neck Surgery 2009; 141: 382–389. DOI:10.1016/j.otohns.2009.04.014.
12. Borges AH, Silverberg MJ, Wentworth D, et al. Predicting risk of cancer during HIV infection: the role of inflammatory and coagulation biomarkers. AIDS 2013; 27: 1433–1441. DOI:10.1097/QAD.0b013e32835f6b0c.
13. Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nature Reviews Cancer 2013; 13: 11–26. DOI:10.1038/nrc3419.
14. Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell 2012; 149: 1192–1205. DOI:10.1016/j.cell.2012.05.012.
15. Voronkov A, Krauss S. Wnt/beta-catenin signaling and small molecule inhibitors. Current Pharmaceutical Design 2013; 19: 634–664.
16. Anastas JN. Functional crosstalk between WNT signaling and tyrosine kinase signaling in cancer. Seminars in Oncology 2015; 42: 820–831. DOI:10.1053/j.seminoncol.2015.09.020.
17. Shackelford J, Maier C, Pagano JS. Epstein–Barr virus activates beta-catenin in type III latently infected B lymphocyte lines: association with deubiquitinating enzymes. Proceedings of the National Academy of Sciences of the United States of America 2003; 100: 15572–15576. DOI:10.1073/pnas.2636947100.
18. Riley KJ, Rabinowitz GS, Yario TA, Luna JM, Darnell RB, Steitz JA. EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. EMBO Journal 2012; 31: 2207–2221. DOI:10.1038/emboj.2012.63.
19. Imig J, Motsch N, Zhu JY, et al. microRNA profiling in Epstein–Barr virus-associated B-cell lymphoma. Nucleic Acids Research 2011; 39: 1880–1893. DOI:10.1093/nar/gkq1043.
20. Dimitrova YN, Li J, Lee YT, et al. Direct ubiquitination of beta-catenin by Siah-1 and regulation by the exchange factor TBL1. Journal of Biological Chemistry 2010; 285: 13507–13516. DOI:10.1074/jbc.M109.049411.
21. Jang KL, Shackelford J, Seo SY, Pagano JS. Up-regulation of beta-catenin by a viral oncogene correlates with inhibition of the seven in absentia homolog 1 in B lymphoma cells. Proceedings of the National Academy of Sciences of the United States of America 2005; 102: 18431–18436. DOI:10.1073/pnas.0504054102.
22. Wong AM, Kong KL, Tsang JW, Kwong DL, Guan XY. Profiling of Epstein–Barr virus-encoded microRNAs in nasopharyngeal carcinoma reveals potential biomarkers and oncomirs. Cancer 2012; 118: 698–710. DOI:10.1002/cncr.26309.
23. Hsu C-Y, Yi Y-H, Chang K-P, Chang Y-S, Chen S-J, Chen H-C. The Epstein–Barr virus-encoded MicroRNA MiR-BART9 promotes tumor metastasis by targeting E-cadherin in nasopharyngeal carcinoma. PLoS Pathogens 2014; 10e1003974:. DOI:10.1371/journal.ppat.1003974.
24. You S, Zhang F, Meng F, et al. EBV-encoded LMP1 increases nuclear beta-catenin accumulation and its transcriptional activity in nasopharyngeal carcinoma. Tumour Biology 2011; 32: 623–630. DOI:10.1007/s13277-011-0161-x.
25. Webb N, Connolly G, Tellam J, Yap AS, Khanna R. Epstein–Barr virus associated modulation of Wnt pathway is not dependent on latent membrane protein-1. PLoS ONE [Electronic Resource] 2008; 3: e3254. DOI:10.1371/journal.pone.0003254.
26. QingLing Z, LiNa Y, Li L, et al. LMP1 antagonizes WNT/beta-catenin signalling through inhibition of WTX and promotes nasopharyngeal dysplasia but not tumourigenesis in LMP1(B95-8) transgenic mice. Journal of Pathology 2011; 223: 574–583. DOI:10.1002/path.2820.
27. Morrison JA, Klingelhutz AJ, Raab-Traub N. Epstein–Barr virus latent membrane protein 2A activates beta-catenin signaling in epithelial cells. Journal of Virology 2003; 77: 12276–12284.
28. Morrison JA, Raab-Traub N. Roles of the ITAM and PY motifs of Epstein–Barr virus latent membrane protein 2A in the inhibition of epithelial cell differentiation and activation of {beta}-catenin signaling. Journal of Virology 2005; 79: 2375–2382. DOI:10.1128/jvi.79.4.2375-2382.2005.
29. Yap LF, Ahmad M, Zabidi MM, et al. Oncogenic effects of WNT5A in Epstein–Barr virus-associated nasopharyngeal carcinoma. International Journal of Oncology 2014; 44: 1774–1780. DOI:10.3892/ijo.2014.2342.
30. Liu X, Wang Y, Wang X, et al. Epigenetic silencing of WNT5A in Epstein–Barr virus-associated gastric carcinoma. Archives of Virology 2013; 158: 123–132. DOI:10.1007/s00705-012-1481-x.
31. Zhao J, Liang Q, Cheung KF, et al. Genome-wide identification of Epstein–Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells. Cancer 2013; 119: 304–312. DOI:10.1002/cncr.27724.
32. Kang GH, Lee S, Kim WH, et al. Epstein–Barr virus-positive gastric carcinoma demonstrates frequent aberrant methylation of multiple genes and constitutes CpG island methylator phenotype-positive gastric carcinoma. American Journal of Pathology 2002; 160: 787–794. DOI:10.1016/s0002-9440(10)64901-2.
33. Lee HS, Chang MS, Yang HK, Lee BL, Kim WH. Epstein-barr virus-positive gastric carcinoma has a distinct protein expression profile in comparison with Epstein–Barr virus-negative carcinoma. Clinical Cancer Research 2004; 10: 1698–1705.
34. Kim B, Byun SJ, Kim YA, et al. Cell cycle regulators, APC/beta-catenin, NF-kappaB and Epstein–Barr virus in gastric carcinomas. Pathology 2010; 42: 58–65. DOI:10.3109/00313020903356392.
35. Fujimuro M, Hayward SD. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus manipulates the activity of glycogen synthase kinase-3beta. Journal of Virology 2003; 77: 8019–8030.
36. Hagen T. Characterization of the interaction between latency-associated nuclear antigen and glycogen synthase kinase 3beta. Journal of Virology 2009; 83: 6312–6317. DOI:10.1128/jvi.01671-08.
37. Angelova M, Ferris M, Swan KF, et al. Kaposi's sarcoma-associated herpesvirus G-protein coupled receptor activates the canonical Wnt/beta-catenin signaling pathway. Virology Journal 2014; 11: 218. DOI:10.1186/s12985-014-0218-8.
38. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nature Reviews Cancer 2010; 10: 550–560. DOI:10.1038/nrc2886.
39. Rampias T, Boutati E, Pectasides E, et al. Activation of Wnt signaling pathway by human papillomavirus E6 and E7 oncogenes in HPV16-positive oropharyngeal squamous carcinoma cells. Molecular Cancer Research 2010; 8: 433–443. DOI:10.1158/1541-7786.MCR-09-0345.
40. Lichtig H, Gilboa DA, Jackman A, et al. HPV16 E6 augments Wnt signaling in an E6AP-dependent manner. Virology 2010; 396: 47–58. DOI:10.1016/j.virol.2009.10.011.
41. Sominsky S, Kuslansky Y, Shapiro B, et al. HPV16 E6 and E6AP differentially cooperate to stimulate or augment Wnt signaling. Virology 2014; 468-470: 510–523. DOI:10.1016/j.virol.2014.09.007.
42. Bonilla-Delgado J, Bulut G, Liu X, et al. The E6 oncoprotein from HPV16 enhances the canonical Wnt/beta-catenin pathway in skin epidermis in vivo. Molecular Cancer Research 2012; 10: 250–258. DOI:10.1158/1541-7786.MCR-11-0287.
43. Ramirez-Salazar E, Centeno F, Nieto K, Valencia-Hernandez A, Salcedo M, Garrido E. HPV16 E2 could act as down-regulator in cellular genes implicated in apoptosis, proliferation and cell differentiation. Virology Journal 2011; 8: 247. DOI:10.1186/1743-422X-8-247.
44. Fadare O, Reddy H, Wang J, Hileeto D, Schwartz PE, Zheng W. E-Cadherin and beta-Catenin expression in early stage cervical carcinoma: a tissue microarray study of 147 cases. World Journal of Surgical Oncology 2005; 3: 38. DOI:10.1186/1477-7819-3-38.
45. Van de Putte G, Kristensen GB, Baekelandt M, Lie AK, Holm R. E-cadherin and catenins in early squamous cervical carcinoma. Gynecologic Oncology 2004; 94: 521–527. DOI:10.1016/j.ygyno.2004.05.046.
46. Pereira-Suarez AL, Meraz MA, Lizano M, et al. Frequent alterations of the beta-catenin protein in cancer of the uterine cervix. Tumour Biology 2002; 23: 45–53 48688.
47. Henken FE, Wilting SM, Overmeer RM, et al. Sequential gene promoter methylation during HPV-induced cervical carcinogenesis. British Journal of Cancer 2007; 97: 1457–1464. DOI:10.1038/sj.bjc.6604055.
48. Lee EJ, Jo M, Rho SB, et al. Dkk3, downregulated in cervical cancer, functions as a negative regulator of beta-catenin. International Journal of Cancer 2009; 124: 287–297. DOI:10.1002/ijc.23913.
49. Dong SM, Kim HS, Rha SH, Sidransky D. Promoter hypermethylation of multiple genes in carcinoma of the uterine cervix. Clinical Cancer Research 2001; 7: 1982–1986.
50. Lin YW, Chung MT, Lai HC, et al. Methylation analysis of SFRP genes family in cervical adenocarcinoma. Journal of Cancer Research and Clinical Oncology 2009; 135: 1665–1674. DOI:10.1007/s00432-009-0613-5.
51. Chung MT, Sytwu HK, Yan MD, et al. Promoter methylation of SFRPs gene family in cervical cancer. Gynecologic Oncology 2009; 112: 301–306. DOI:10.1016/j.ygyno.2008.10.004.
52. van der Meide WF, Snellenberg S, Meijer CJ, et al. Promoter methylation analysis of WNT/beta-catenin signaling pathway regulators to detect adenocarcinoma or its precursor lesion of the cervix. Gynecologic Oncology 2011; 123: 116–122. DOI:10.1016/j.ygyno.2011.06.015.
53. Fragoso-Ontiveros V, Maria Alvarez-Garcia R, Contreras-Paredes A, et al. Gene expression profiles induced by E6 from non-European HPV18 variants reveals a differential activation on cellular processes driving to carcinogenesis. Virology 2012; 432: 81–90. DOI:10.1016/j.virol.2012.05.029.
54. Chen L, Hu L, Li L, et al. Dysregulation of beta-catenin by hepatitis B virus X protein in HBV-infected human hepatocellular carcinomas. Frontiers of Medicine in China 2010; 4: 399–411. DOI:10.1007/s11684-010-0170-y.
55. Cha MY, Kim CM, Park YM, Ryu WS. Hepatitis B virus X protein is essential for the activation of Wnt/beta-catenin signaling in hepatoma cells. Hepatology 2004; 39: 1683–1693.
56. Srisuttee R, Koh SS, Kim SJ, et al. Hepatitis B virus X (HBX) protein upregulates beta-catenin in a human hepatic cell line by sequestering SIRT1 deacetylase. Oncology Reports 2012; 28: 276–282. DOI:10.3892/or.2012.1798.
57. Guerrieri F, Belloni L, Pediconi N, Levrero M. Molecular mechanisms of HBV-associated hepatocarcinogenesis. Seminars in Liver Disease 2013; 33: 147–156. DOI:10.1055/s-0033-1345721.
58. Hsieh A, Kim HS, Lim SO, Yu DY, Jung G. Hepatitis B viral X protein interacts with tumor suppressor adenomatous polyposis coli to activate Wnt/beta-catenin signaling. Cancer Letters 2011; 300: 162–172. DOI:10.1016/j.canlet.2010.09.018.
59. Xie Q, Chen L, Shan X, et al. Epigenetic silencing of SFRP1 and SFRP5 by hepatitis B virus X protein enhances hepatoma cell tumorigenicity through Wnt signaling pathway. International Journal of Cancer 2014; 135: 635–646. DOI:10.1002/ijc.28697.
60. Guo Y, Kang W, Lei X, et al. Hepatitis B viral core protein disrupts human host gene expression by binding to promoter regions. BMC Genomics 2012; 13: 563. DOI:10.1186/1471-2164-13-563.
61. Tian X, Li J, Ma ZM, Zhao C, Wan DF, Wen YM. Role of hepatitis B surface antigen in the development of hepatocellular carcinoma: regulation of lymphoid enhancer-binding factor 1. Journal of Experimental & Clinical Cancer Research 2009; 28: 58. DOI:10.1186/1756-9966-28-58.
62. Tian X, Zhao C, Ren J, Ma ZM, Xie YH, Wen YM. Gene-expression profiles of a hepatitis B small surface antigen-secreting cell line reveal upregulation of lymphoid enhancer-binding factor 1. Journal of General Virology 2007; 88: 2966–2976.
63. Lin X, Wang Q, Cao Z, Geng M, Cao Y, Liu X. Differential expression of Wnt pathway genes in sporadic hepatocellular carcinomas infected with hepatitis B virus identified with OligoGE arrays. Hepatitis Monthly 2013; 13: e6192. DOI:10.5812/hepatmon.6192.
64. Li J, Quan H, Liu Q, Si Z, He Z, Qi H. Alterations of axis inhibition protein 1 (AXIN1) in hepatitis B virus-related hepatocellular carcinoma and overexpression of AXIN1 induces apoptosis in hepatocellular cancer cells. Oncology Research 2013; 20: 281–288.
65. Li W, Zhu C, Wu Y, Wang Z, Zhu C. Increased Pygo2 expression in liver of patients with hepatitis B virus-related fibrosis. Liver International 2015. DOI:10.1111/liv.12877.
66. Wong CM, Fan ST, Ng IO. beta-Catenin mutation and overexpression in hepatocellular carcinoma: clinicopathologic and prognostic significance. Cancer 2001; 92: 136–145.
67. Tien LT, Ito M, Nakao M, et al. Expression of beta-catenin in hepatocellular carcinoma. World Journal of Gastroenterology 2005; 11: 2398–2401.
68. Kim CW, Yoon SK, Jung ES, et al. Correlation of hepatitis B core antigen and beta-catenin expression on hepatocytes in chronic hepatitis B virus infection: relevance to the severity of liver damage and viral replication. Journal of Gastroenterology and Hepatology 2007; 22: 1534–1542.
69. Edamoto Y, Hara A, Biernat W, et al. Alterations of RB1, p53 and Wnt pathways in hepatocellular carcinomas associated with hepatitis C, hepatitis B and alcoholic liver cirrhosis. International Journal of Cancer 2003; 106: 334–341.
70. Ding X, Yang Y, Han B, et al. Transcriptomic characterization of hepatocellular carcinoma with CTNNB1 mutation. PLoS ONE [Electronic Resource] 2014; 9e95307:. DOI:10.1371/journal.pone.0095307.
71. Kan Z, Zheng H, Liu X, et al. Whole-genome sequencing identifies recurrent mutations in hepatocellular carcinoma. Genome Research 2013; 23: 1422–1433. DOI:10.1101/gr.154492.113.
72. Boyault S, Rickman DS, de Reynies A, et al. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology 2007; 45: 42–52. DOI:10.1002/hep.21467.
73. Guichard C, Amaddeo G, Imbeaud S, et al. Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nature Genetics 2012; 44: 694–698. DOI:10.1038/ng.2256.
74. Lau CC, Sun T, Ching AK, et al. Viral-human chimeric transcript predisposes risk to liver cancer development and progression. Cancer Cell 2014; 25: 335–349. DOI:10.1016/j.ccr.2014.01.030.
75. Arzumanyan A, Reis HM, Feitelson MA. Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma. Nature Reviews Cancer 2013; 13: 123–135. DOI:10.1038/nrc3449.
76. Deng YB, Nagae G, Midorikawa Y, et al. Identification of genes preferentially methylated in hepatitis C virus-related hepatocellular carcinoma. Cancer Science 2010; 101: 1501–1510. DOI:10.1111/j.1349-7006.2010.01549.x.
77. Umer M, Qureshi SA, Hashmi ZY, et al. Promoter hypermethylation of Wnt pathway inhibitors in hepatitis C virus-induced multistep hepatocarcinogenesis. Virology Journal 2014; 11: 117. DOI:10.1186/1743-422X-11-117.
78. Quan H, Zhou F, Nie D, et al. Hepatitis C virus core protein epigenetically silences SFRP1 and enhances HCC aggressiveness by inducing epithelial–mesenchymal transition. Oncogene 2014; 33: 2826–2835. DOI:10.1038/onc.2013.225.
79. Fukutomi T, Zhou Y, Kawai S, Eguchi H, Wands JR, Li J. Hepatitis C virus core protein stimulates hepatocyte growth: correlation with upregulation of wnt-1 expression. Hepatology 2005; 41: 1096–1105.
80. Liu J, Wang Z, Tang J, et al. Hepatitis C virus core protein activates Wnt/beta-catenin signaling through multiple regulation of upstream molecules in the SMMC-7721 cell line. Archives of Virology 2011; 156: 1013–1023. DOI:10.1007/s00705-011-0943-x.
81. Liu J, Ding X, Tang J, et al. Enhancement of canonical Wnt/beta-catenin signaling activity by HCV core protein promotes cell growth of hepatocellular carcinoma cells. PLoS ONE [Electronic Resource] 2011; 6e27496:. DOI:10.1371/journal.pone.0027496.
82. Street A, Macdonald A, McCormick C, Harris M. Hepatitis C virus NS5A-mediated activation of phosphoinositide 3-kinase results in stabilization of cellular beta-catenin and stimulation of beta-catenin-responsive transcription. Journal of Virology 2005; 79: 5006–5016. DOI:10.1128/jvi.79.8.5006-5016.2005.
83. Park CY, Choi SH, Kang SM, et al. Nonstructural 5A protein activates beta-catenin signaling cascades: implication of hepatitis C virus-induced liver pathogenesis. Journal of Hepatology 2009; 51: 853–864. DOI:10.1016/j.jhep.2009.06.026.
84. Higgs MR, Lerat H, Pawlotsky JM. Hepatitis C virus-induced activation of beta-catenin promotes c-Myc expression and a cascade of pro-carcinogenetic events. Oncogene 2013; 32: 4683–4693. DOI:10.1038/onc.2012.484.
85. Zhang Y, Wei W, Cheng N, et al. Hepatitis C virus-induced up-regulation of microRNA-155 promotes hepatocarcinogenesis by activating Wnt signaling. Hepatology 2012; 56: 1631–1640. DOI:10.1002/hep.25849.
86. Shackel NA, McGuinness PH, Abbott CA, Gorrell MD, McCaughan GW. Insights into the pathobiology of hepatitis C virus-associated cirrhosis: analysis of intrahepatic differential gene expression. American Journal of Pathology 2002; 160: 641–654.
87. Huang H, Fujii H, Sankila A, et al. Beta-catenin mutations are frequent in human hepatocellular carcinomas associated with hepatitis C virus infection. American Journal of Pathology 1999; 155: 1795–1801.
88. Polakowski N, Gregory H, Mesnard JM, Lemasson I. Expression of a protein involved in bone resorption, Dkk1, is activated by HTLV-1 bZIP factor through its activation domain. Retrovirology 2010; 7: 61. DOI:10.1186/1742-4690-7-61.
89. Ma G, Yasunaga J, Fan J, Yanagawa S, Matsuoka M. HTLV-1 bZIP factor dysregulates the Wnt pathways to support proliferation and migration of adult T-cell leukemia cells. Oncogene 2013; 32: 4222–4230. DOI:10.1038/onc.2012.450.
90. Gan DD, Khalili K. Interaction between JCV large T-antigen and beta-catenin. Oncogene 2004; 23: 483–490.
91. Bhattacharyya R, Noch EK, Khalili K. A novel role of Rac1 GTPase in JCV T-antigen-mediated beta-catenin stabilization. Oncogene 2007; 26: 7628–7636.
92. Bongers G, Maussang D, Muniz LR, et al. The cytomegalovirus-encoded chemokine receptor US28 promotes intestinal neoplasia in transgenic mice. Journal of Clinical Investigation 2010; 120: 3969–3978. DOI:10.1172/JCI42563.
93. Langemeijer EV, Slinger E, de Munnik S, et al. Constitutive beta-catenin signaling by the viral chemokine receptor US28. PLoS ONE [Electronic Resource] 2012; 7e48935:. DOI:10.1371/journal.pone.0048935.
94. Fu M, Gao Y, Zhou Q, et al. Human cytomegalovirus latent infection alters the expression of cellular and viral microRNA. Gene 2014; 536: 272–278. DOI:10.1016/j.gene.2013.12.012.
95. Li Q, Yu P, Wang W, et al. Gene expression profiles of various cytokines in mesenchymal stem cells derived from umbilical cord tissue and bone marrow following infection with human cytomegalovirus. Cellular & Molecular Biology Letters 2014; 19: 140–157. DOI:10.2478/s11658-014-0187-3.
96. Mo X, Xu L, Yang Q, et al. Microarray profiling analysis uncovers common molecular mechanisms of rubella virus, human cytomegalovirus, and herpes simplex virus type 2 infections in ECV304 cells. Current Molecular Medicine 2011; 11: 481–488.
97. Kapoor A, He R, Venkatadri R, Forman M, Arav-Boger R. Wnt modulating agents inhibit human cytomegalovirus replication. Antimicrobial Agents and Chemotherapy 2013; 57: 2761–2767. DOI:10.1128/AAC.00029-13.
98. Angelova M, Zwezdaryk K, Ferris M, Shan B, Morris CA, Sullivan DE. Human cytomegalovirus infection dysregulates the canonical Wnt/beta-catenin signaling pathway. PLoS Pathogens 2012; 8e1002959:. DOI:10.1371/journal.ppat.1002959.
99. Ueland T, Rollag H, Hartmann A, et al. Secreted Wnt antagonists during eradication of cytomegalovirus infection in solid organ transplant recipients. American Journal of Transplantation 2014; 14: 210–215. DOI:10.1111/ajt.12506.
100. van Zuylen WJ, Ford CE, Wong DD, Rawlinson WD. Human cytomegalovirus modulates expression of noncanonical Wnt receptor ROR2 to alter trophoblast migration. Journal of Virology 2015; 90: 1108–1115. DOI:10.1128/jvi.02588-15.
101. Wortman B, Darbinian N, Sawaya BE, Khalili K, Amini S. Evidence for regulation of long terminal repeat transcription by Wnt transcription factor TCF-4 in human astrocytic cells. Journal of Virology 2002; 76: 11159–11165.
102. Luque MC, Santos CC, Mairena EC, et al. Gene expression profile in long-term non progressor HIV infected patients: in search of potential resistance factors. Molecular Immunology 2014; 62: 63–70. DOI:10.1016/j.molimm.2014.05.016.
103. Kumar A, Zloza A, Moon RT, Watts J, Tenorio AR, Al-Harthi L. Active beta-catenin signaling is an inhibitory pathway for human immunodeficiency virus replication in peripheral blood mononuclear cells. Journal of Virology 2008; 82: 2813–2820. DOI:10.1128/JVI.02498-07.
104. Orellana JA, Saez JC, Bennett MV, Berman JW, Morgello S, Eugenin EA. HIV increases the release of dickkopf-1 protein from human astrocytes by a Cx43 hemichannel-dependent mechanism. Journal of Neurochemistry 2014; 128: 752–763. DOI:10.1111/jnc.12492.
105. Wu JQ, Dwyer DE, Dyer WB, Yang YH, Wang B, Saksena NK. Genome-wide analysis of primary CD4+ and CD8+ T cell transcriptomes shows evidence for a network of enriched pathways associated with HIV disease. Retrovirology 2011; 8: 18. DOI:10.1186/1742-4690-8-18.
106. Weiser K, Barton M, Gershoony D, Dasgupta R, Cardozo T. HIV's Nef interacts with beta-catenin of the Wnt signaling pathway in HEK293 cells. PLoS ONE [Electronic Resource] 2013; 8e77865:. DOI:10.1371/journal.pone.0077865.
107. Butler JS, Dunning EC, Murray DW, Doran PP, O'Byrne JM. HIV-1 protein induced modulation of primary human osteoblast differentiation and function via a Wnt/beta-catenin-dependent mechanism. Journal of Orthopaedic Research 2013; 31: 218–226. DOI:10.1002/jor.22196.
108. Li B, Shi Y, Shu J, Gao J, Wu P, Tang SJ. Wingless-type mammary tumor virus integration site family, member 5A (Wnt5a) regulates human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein 120 (gp120)-induced expression of pro-inflammatory cytokines via the Ca2+/calmodulin-dependent protein kinase II (CaMKII) and c-Jun N-terminal kinase (JNK) signaling pathways. Journal of Biological Chemistry 2013; 288: 13610–13619. DOI:10.1074/jbc.M112.381046.
109. Narasipura SD, Henderson LJ, Fu SW, Chen L, Kashanchi F, Al-Harthi L. Role of beta-catenin and TCF/LEF family members in transcriptional activity of HIV in astrocytes. Journal of Virology 2012; 86: 1911–1921. DOI:10.1128/JVI.06266-11.
110. Henderson LJ, Sharma A, Monaco MC, Major EO, Al-Harthi L. Human immunodeficiency virus type 1 (HIV-1) transactivator of transcription through its intact core and cysteine-rich domains inhibits Wnt/beta-catenin signaling in astrocytes: relevance to HIV neuropathogenesis. Journal of Neuroscience 2012; 32: 16306–16313. DOI:10.1523/JNEUROSCI.3145-12.2012.
111. Sharma A, Hu XT, Napier TC, Al-Harthi L. Methamphetamine and HIV-1 Tat down regulate beta-catenin signaling: implications for methampetamine abuse and HIV-1 co-morbidity. Journal of Neuroimmune Pharmacology: The Official Journal of The Society on NeuroImmune Pharmacology 2011; 6: 597–607. DOI:10.1007/s11481-011-9295-2.
112. Richards MH, Narasipura SD, Kim S, Seaton MS, Lutgen V, Al-Harthi L. Dynamic interaction between astrocytes and infiltrating PBMCs in context of neuroAIDS. GLIA 2015; 63: 441–451. DOI:10.1002/glia.22763.
113. Modarresi R, Xiang Z, Yin M, Laurence J. WNT/beta-catenin signaling is involved in regulation of osteoclast differentiation by human immunodeficiency virus protease inhibitor ritonavir: relationship to human immunodeficiency virus-linked bone mineral loss. American Journal of Pathology 2009; 174: 123–135. DOI:10.2353/ajpath.2009.080484.
114. Santiago F, Oguma J, Brown AM, Laurence J. Noncanonical Wnt signaling promotes osteoclast differentiation and is facilitated by the human immunodeficiency virus protease inhibitor ritonavir. Biochemical and Biophysical Research Communications 2012; 417: 223–230. DOI:10.1016/j.bbrc.2011.11.089.
115. Mora S, Puzzovio M, Giacomet V, et al. Sclerostin and DKK-1: two important regulators of bone metabolism in HIV-infected youths. Endocrine 2015; 49: 783–790. DOI:10.1007/s12020-015-0527-8.
116. Zhao H, Granberg F, Pettersson U. How adenovirus strives to control cellular gene expression. Virology 2007; 363: 357–375.
117. Bian L, Wang Y, Liu Q, Xia J, Long JE. Prediction of signaling pathways involved in enterovirus 71 infection by algorithm analysis based on miRNA profiles and their target genes. Archives of Virology 2015; 160: 173–182. DOI:10.1007/s00705-014-2249-2.
118. Ye X, Hemida MG, Qiu Y, Hanson PJ, Zhang HM, Yang D. MiR-126 promotes coxsackievirus replication by mediating cross-talk of ERK1/2 and Wnt/beta-catenin signal pathways. Cellular and Molecular Life Sciences 2013; 70: 4631–4644. DOI:10.1007/s00018-013-1411-4.
119. Wang C, Yang W, Yan HX, et al. Hepatitis B virus X (HBx) induces tumorigenicity of hepatic progenitor cells in 3,5-diethoxycarbonyl-1,4-dihydrocollidine-treated HBx transgenic mice. Hepatology 2012; 55: 108–120. DOI:10.1002/hep.24675.