Instigation of Notch signaling in the pathogenesis of Kaposis sarcoma-associated herpesvirus and other human tumor viruses

Future Microbiology

Volumn 7, Issue 10, 2012, Pages 1191-1205

  Cheng, Fang ^a,b   Pekkonen, Pirita ^a   Ojala, Päivi M ^a,c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

^c Foundation for the Finnish Cancer Institute   (Finland)

Author keywords

EndMT; human tumor virus; KSHV; Notch pathway; RBP J; viral reactivation

Indexed keywords

EPSTEIN BARR VIRUS ANTIGEN 2; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH RECEPTOR; PROTEIN P53; VASCULOTROPIN A;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; DOWN REGULATION; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; EPSTEIN BARR VIRUS; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN HERPESVIRUS 8; NONHUMAN; NUCLEAR REPROGRAMMING; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN INDUCTION; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR VIRUS; VIRUS LATENCY; VIRUS REPLICATION; WART VIRUS;

ANIMALS; DISEASE MODELS, ANIMAL; HERPESVIRUS 8, HUMAN; HUMANS; LYMPHOPROLIFERATIVE DISORDERS; ONCOGENIC VIRUSES; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; VIRUS DISEASES;

HERPESVIRIDAE; HUMAN HERPESVIRUS 8;

EID: 84867096020     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.12.95     Document Type: Review

References (135)

1. Wen KW, Damania B. Kaposi sarcomaassociated herpesvirus (KSHV): molecular biology and oncogenesis. Cancer Lett. 289(2), 140-150 (2010).
2. Jarviluoma A, Ojala PM. Cell signaling pathways engaged by KSHV. Biochim. Biophys. Acta 1766(1), 140-158 (2006).
3. Ballon G, Chen K, Perez R, Tam W, Cesarman E. Kaposi sarcoma herpesvirus (KSHV) vFLIP oncoprotein induces B cell transdifferentiation and tumorigenesis in mice. J. Clin. Invest. 121(3), 1141-1153 (2011).
4. Montaner S, Sodhi A, Molinolo A et al. Endothelial infection with KSHV genes in vivo reveals that vGPCR initiates Kaposi's sarcomagenesis and can promote the tumorigenic potential of viral latent genes. Cancer Cell 3(1), 23-36 (2003).
5. Sodhi A, Montaner S, Gutkind JS. Does dysregulated expression of a deregulated viral GPCR trigger Kaposi's sarcomagenesis? FASEB J. 18(3), 422-427 (2004).
6. Mutlu AD, Cavallin LE, Vincent L et al. In vivo-restricted and reversible malignancy induced by human herpesvirus-8 KSHV: a cell and animal model of virally induced Kaposi's sarcoma. Cancer Cell 11(3), 245-258 (2007).
7. Gottwein E. Kaposi's sarcoma-associated herpesvirus microRNAs. Front. Microbiol. 3, 165 (2012).
8. Zhong W, Wang H, Herndier B, Ganem D. Restricted expression of Kaposi sarcomaassociated herpesvirus (human herpesvirus 8) genes in Kaposi sarcoma. Proc. Natl Acad. Sci. USA 93(13), 6641-6646 (1996).
9. Staskus KA, Zhong W, Gebhard K et al. Kaposi's sarcoma-associated herpesvirus gene expression in endothelial (spindle) tumor cells. J. Virol. 71(1), 715-719 (1997).
10. Staskus KA, Sun R, Miller G et al. Cellular tropism and viral interleukin-6 expression distinguish human herpesvirus 8 involvement in Kaposi's sarcoma, primary effusion lymphoma, and multicentric Castleman's disease. J. Virol. 73(5), 4181-4187 (1999).
11. Dupin N, Fisher C, Kellam P et al. Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma. Proc. Natl Acad. Sci. USA 96(8), 4546-4551 (1999).
12. Sun R, Lin SF, Staskus K et al. Kinetics of Kaposi's sarcoma-associated herpesvirus gene expression. J. Virol. 73(3), 2232-2242 (1999).
13. Renne R, Lagunoff M, Zhong W, Ganem D. The size and conformation of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) DNA in infected cells and virions. J. Virol. 70(11), 8151-8154 (1996).
14. Dittmer DP. Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by real-time PCR arrays. Cancer Res. 63(9), 2010-2015 (2003).
15. Lukac DM, Yuan Y. Reactivation and lytic replication of KSHV. In: Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. Arvin A, Campadelli-Fiume G, Mocarski E et al. (Eds). Cambridge University Press, UK, 26 (2007).
16. Zhu FX, Cusano T, Yuan Y. Identification of the immediate-early transcripts of Kaposi's sarcoma-associated herpesvirus. J. Virol. 73(7), 5556-5567 (1999).
17. Rimessi P, Bonaccorsi A, Sturzl M et al. Transcription pattern of human herpesvirus 8 open reading frame K3 in primary effusion lymphoma and Kaposi's sarcoma. J. Virol. 75(15), 7161-7174 (2001).
18. Lu KH, Wang DY, Lue KH et al. PCR and flow cytometric analysis of paclitaxelinhibited arylamine N-acetyltransferase activity and gene expression in human osteogenic sarcoma cells (U-2 OS). Anticancer Res. 24(1), 83-90 (2004).
19. Staudt MR, Dittmer DP. The Rta/Orf50 transactivator proteins of the gammaherpesviridae. Curr. Top. Microbiol. Immunol. 312, 71-100 (2007).
20. Lan K, Kuppers DA, Verma SC, Robertson ES. Kaposi's sarcoma-associated herpesvirusencoded latency-associated nuclear antigen inhibits lytic replication by targeting RTA: a potential mechanism for virus-mediated control of latency. J. Virol. 78(12), 6585-6594 (2004).
21. Ye F, Lei X, Gao SJ. Mechanisms of Kaposi's sarcoma-associated herpesvirus latency and reactivation. Adv. Virol. 2011, 193860 (2011).
22. Ganem D. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J. Clin. Invest. 120(4), 939-949 (2010).
23. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 284(5415), 770-776 (1999).
24. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell. Biol. 7(9), 678-689 (2006).
25. Borggrefe T, Oswald F. The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell. Mol. Life Sci. 66(10), 1631-1646 (2009).
26. Oswald F, Winkler M, Cao Y et al. RBP-Jkappa/SHARP recruits CtIP/CtBP corepressors to silence Notch target genes. Mol. Cell. Biol. 25(23), 10379-10390 (2005).
27. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137(2), 216-233 (2009).
28. Leong KG, Niessen K, Kulic I et al. Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J. Exp. Med. 204(12), 2935-2948 (2007).
29. Niessen K, Fu Y, Chang L, Hoodless PA, Mcfadden D, Karsan A. Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J. Cell. Biol. 182(2), 315-325 (2008).
30. Palomero T, Odom DT, O'Neil J et al. Transcriptional regulatory networks downstream of TAL1/SCL in T-cell acute lymphoblastic leukemia. Blood 108(3), 986-992 (2006).
31. Hamidi H, Gustafason D, Pellegrini M, Gasson J. Identification of novel targets of CSL-dependent Notch signaling in hematopoiesis. PLoS One 6(5), e20022 (2011).
32. Andersen P, Uosaki H, Shenje LT, Kwon C. Non-canonical Notch signaling: emerging role and mechanism. Trends Cell. Biol. 22(5), 257-265 (2012).
33. Fortini ME, Bilder D. Endocytic regulation of Notch signaling. Curr. Opin. Genet. Dev. 19(4), 323-328 (2009).
34. Dang TP. Notch, apoptosis and cancer. Adv. Exp. Med. Biol. 727, 199-209 (2012).
35. Ranganathan P, Weaver KL, Capobianco AJ. Notch signalling in solid tumours: a little bit of everything but not all the time. Nat. Rev. Cancer 11(5), 338-351 (2011).
36. Ellisen LW, Bird J, West DC et al. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66(4), 649-661 (1991).
37. Weng AP, Ferrando AA, Lee W et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306(5694), 269-271 (2004).
38. Koch U, Radtke F. Notch signaling in solid tumors. Curr. Top. Dev. Biol. 92, 411-455 (2010).
39. Sethi N, Kang Y. Notch signalling in cancer progression and bone metastasis. Br. J. Cancer 105(12), 1805-1810 (2011).
40. Wang Z, Li Y, Ahmad A et al. Targeting Notch signaling pathway to overcome drug resistance for cancer therapy. Biochim. Biophys. Acta 1806(2), 258-267 (2010).
41. Pannuti A, Foreman K, Rizzo P et al. Targeting Notch to target cancer stem cells. Clin. Cancer Res. 16(12), 3141-3152 (2010).
42. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 139(5), 871-890 (2009).
43. Demehri S, Turkoz A, Kopan R. Epidermal Notch1 loss promotes skin tumorigenesis by impacting the stromal microenvironment. Cancer Cell 16(1), 55-66 (2009).
44. Lobry C, Oh P, Aifantis I. Oncogenic and tumor suppressor functions of Notch in cancer: it's NOTCH what you think. J. Exp. Med. 208(10), 1931-1935 (2011).
45. Nicolas M, Wolfer A, Raj K et al. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33(3), 416-421 (2003).
46. Dotto GP. Notch tumor suppressor function. Oncogene 27(38), 5115-5123 (2008).
47. Dotto GP. Crosstalk of Notch with p53 and p63 in cancer growth control. Nat. Rev. Cancer 9(8), 587-595 (2009).
48. Dufraine J, Funahashi Y, Kitajewski J. Notch signaling regulates tumor angiogenesis by diverse mechanisms. Oncogene 27(38), 5132-5137 (2008).
49. Curry CL, Reed LL, Golde TE, Miele L, Nickoloff BJ, Foreman KE. Gamma secretase inhibitor blocks Notch activation and induces apoptosis in Kaposi's sarcoma tumor cells. Oncogene 24(42), 6333-6344 (2005).
50. Emuss V, Lagos D, Pizzey A, Gratrix F, Henderson SR, Boshoff C. KSHV manipulates Notch signaling by DLL4 and JAG1 to alter cell cycle genes in lymphatic endothelia. PLoS Pathog. 5(10), e1000616 (2009).
51. Curry CL, Reed LL, Broude E, Golde TE, Miele L, Foreman KE. Notch inhibition in Kaposi's sarcoma tumor cells leads to mitotic catastrophe through nuclear factor-kappaB signaling. Mol. Cancer Ther. 6(7), 1983-1992 (2007).
52. Haapasalo A, Kovacs DM. The many substrates of presenilin/gamma- secretase. J. Alzheimers Dis. 25(1), 3-28 (2011).
53. Lan K, Choudhuri T, Murakami M, Kuppers DA, Robertson ES. Intracellular activated Notch1 is critical for proliferation of Kaposi's sarcoma-associated herpesvirus-associated B-lymphoma cell lines in vitro. J. Virol. 80(13), 6411-6419 (2006).
54. Lan K, Verma SC, Murakami M, Bajaj B, Kaul R, Robertson ES. Kaposi's sarcoma herpesvirus-encoded latency-associated nuclear antigen stabilizes intracellular activated Notch by targeting the Sel10 protein. Proc. Natl Acad. Sci. USA 104(41), 16287-16292 (2007).
55. Lan K, Murakami M, Bajaj B et al. Inhibition of KSHV-infected primary effusion lymphomas in NOD/SCID mice by gamma-secretase inhibitor. Cancer Biol. Ther. 8(22), 2136-2143 (2009).
56. Johnston DA, Dong B, Hughes CC. TNF induction of jagged-1 in endothelial cells is NFkappaB-dependent. Gene 435(1-2), 36-44 (2009).
57. Liu R, Li X, Tulpule A et al. KSHV-induced Notch components render endothelial and mural cell characteristics and cell survival. Blood 115(4), 887-895 (2010).
58. Oliver G, Detmar M. The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev. 16(7), 773-783 (2002).
59. Johnson LA, Jackson DG. Cell traffic and the lymphatic endothelium. Ann. NY Acad. Sci. 1131, 119-133 (2008).
60. Cheng F, Pekkonen P, Laurinavicius S et al. KSHV-initiated notch activation leads to membrane-type-1 matrix metalloproteinasedependent lymphatic endothelial-tomesenchymal transition. Cell Host Microbe 10(6), 577-590 (2011).
61. Gasperini P, Espigol-Frigole G, McCormick PJ et al. Kaposi sarcoma herpesvirus promotes endothelial-to-mesenchymal transition through Notch-dependent signaling. Cancer Res. 72(5), 1157-1169 (2012).
62. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119(6), 1420-1428 (2009).
63. Grossmann C, Podgrabinska S, Skobe M, Ganem D. Activation of NF-kappaB by the latent vFLIP gene of Kaposi's sarcomaassociated herpesvirus is required for the spindle shape of virus-infected endothelial cells and contributes to their proinflammatory phenotype. J. Virol. 80(14), 7179-7185 (2006).
64. Mansouri M, Douglas J, Rose PP et al. Kaposi sarcoma herpesvirus K5 removes CD31/PECAM from endothelial cells. Blood 108(6), 1932-1940 (2006).
65. Qian LW, Greene W, Ye F, Gao SJ. Kaposi's sarcoma-associated herpesvirus disrupts adherens junctions and increases endothelial permeability by inducing degradation of VE-cadherin. J. Virol. 82(23), 11902-11912 (2008).
66. Wang HW, Trotter MW, Lagos D et al. Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma. Nat. Genet. 36(7), 687-693 (2004).
67. Di Tommaso L, Pasquinelli G, Damiani S. Smooth muscle cell differentiation in mammary stromo-epithelial lesions with evidence of a dual origin: stromal myofibroblasts and myoepithelial cells. Histopathology 42(5), 448-456 (2003).
68. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat. Med. 16(12), 1400-1406 (2010).
69. Garcia Campelo MR, Alonso Curbera G, Aparicio Gallego G, Grande Pulido E, Anton Aparicio LM. Stem cell and lung cancer development: blaming the Wnt, Hh and Notch signalling pathway. Clin. Transl. Oncol. 13(2), 77-83 (2011).
70. Bridges E, Oon CE, Harris A. Notch regulation of tumor angiogenesis. Future Oncol. 7(4), 569-588 (2011).
71. Hofmann JJ, Iruela-Arispe ML. Notch signaling in blood vessels: who is talking to whom about what? Circ. Res. 100(11), 1556-1568 (2007).
72. Tung JJ, Tattersall IW, Kitajewski J. Tips, stalks, tubes: Notch-mediated cell fate determination and mechanisms of tubulogenesis during angiogenesis. Cold Spring Harb. Perspect. Med. 2(2), a006601 (2012).
73. Benedito R, Rocha SF, Woeste M et al. Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484(7392), 110-114 (2012).
74. Ridgway J, Zhang G, Wu Y et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444(7122), 1083-1087 (2006).
75. Zheng W, Tammela T, Yamamoto M et al. Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood 118(4), 1154-1162 (2011).
76. Tvorogov D, Anisimov A, Zheng W et al. Effective suppression of vascular network formation by combination of antibodies blocking VEGFR ligand binding and receptor dimerization. Cancer Cell 18(6), 630-640 (2010).
77. Liang Y, Chang J, Lynch SJ, Lukac DM, Ganem D. The lytic switch protein of KSHV activates gene expression via functional interaction with RBP-Jkappa (CSL), the target of the Notch signaling pathway. Genes Dev. 16(15), 1977-1989 (2002).
78. Lu J, Verma SC, Cai Q, Saha A, Dzeng RK, Robertson ES. The RBP-Jkappa binding sites within the RTA promoter regulate KSHV latent infection and cell proliferation. PLoS Pathog. 8(1), e1002479 (2012).
79. Lan K, Kuppers DA, Robertson ES. Kaposi's sarcoma-associated herpesvirus reactivation is regulated by interaction of latency-associated nuclear antigen with recombination signal sequence-binding protein Jkappa, the major downstream effector of the Notch signaling pathway. J. Virol. 79(6), 3468-3478 (2005).
80. Liang Y, Ganem D. Lytic but not latent infection by Kaposi's sarcoma-associated herpesvirus requires host CSL protein, the mediator of Notch signaling. Proc. Natl Acad. Sci. USA 100(14), 8490-8495 (2003).
81. Carroll KD, Bu W, Palmeri D et al. Kaposi's sarcoma-associated herpesvirus lytic switch protein stimulates DNA binding of RBP-Jk/CSL to activate the Notch pathway. J. Virol. 80(19), 9697-9709 (2006).
82. Palmeri D, Carroll KD, Gonzalez-Lopez O, Lukac DM. Kaposi's sarcoma-associated herpesvirus Rta tetramers make high-affinity interactions with repetitive DNA elements in the Mta promoter to stimulate DNA binding of RBP-Jk/CSL. J. Virol. 85(22), 11901-11915 (2011).
83. Persson LM, Wilson AC. Wide-scale use of Notch signaling factor CSL/RBP-Jkappa in RTA-mediated activation of Kaposi's sarcoma-associated herpesvirus lytic genes. J. Virol. 84(3), 1334-1347 (2010).
84. Chang H, Dittmer DP, Shin YC, Hong Y, Jung JU. Role of Notch signal transduction in Kaposi's sarcoma-associated herpesvirus gene expression. J. Virol. 79(22), 14371-14382 (2005).
85. Lan K, Murakami M, Choudhuri T, Kuppers DA, Robertson ES. Intracellular-activated Notch1 can reactivate Kaposi's sarcomaassociated herpesvirus from latency. Virology 351(2), 393-403 (2006).
86. Heinzelmann K, Scholz BA, Nowak A et al. Kaposi's sarcoma-associated herpesvirus viral interferon regulatory factor 4 (vIRF4/K10) is a novel interaction partner of CSL/CBF1, the major downstream effector of Notch signaling. J. Virol. 84(23), 12255-12264 (2010).
87. Gao SJ, Kingsley L, Hoover DR et al. Seroconversion to antibodies against Kaposi's sarcoma-associated herpesvirus-related latent nuclear antigens before the development of Kaposi's sarcoma. N. Engl. J. Med. 335(4), 233-241 (1996).
88. Kedes DH, Operskalski E, Busch M, Kohn R, Flood J, Ganem D. The seroepidemiology of human herpesvirus 8 (Kaposi's sarcomaassociated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Nat. Med. 2(8), 918-924 (1996).
89. Ballestas ME, Chatis PA, Kaye KM. Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284(5414), 641-644 (1999).
90. Cotter MA 2nd, Robertson ES. The latencyassociated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells. Virology 264(2), 254-264 (1999).
91. Lan K, Kuppers DA, Verma SC, Sharma N, Murakami M, Robertson ES. Induction of Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen by the lytic transactivator RTA: a novel mechanism for establishment of latency. J. Virol. 79(12), 7453-7465 (2005).
92. Lu J, Verma SC, Cai Q, Robertson ES. The single RBP-Jkappa site within the LANA promoter is crucial for establishing Kaposi's sarcoma-associated herpesvirus latency during primary infection. J. Virol. 85(13), 6148-6161 (2011).
93. Jin Y, He Z, Liang D et al. Carboxyl-terminal amino acids 1052 to 1082 of the latencyassociated nuclear antigen (LANA) interact with RBP-Jkappa and are responsible for LANA-mediated RTA repression. J. Virol. 86(9), 4956-4969 (2012).
94. Chang H, Gwack Y, Kingston D et al. Activation of CD21 and CD23 gene expression by Kaposi's sarcoma-associated herpesvirus RTA. J. Virol. 79(8), 4651-4663 (2005).
95. Spadavecchia S, Gonzalez-Lopez O, Carroll KD, Palmeri D, Lukac DM. Convergence of Kaposi's sarcoma-associated herpesvirus reactivation with Epstein-Barr virus latency and cellular growth mediated by the notch signaling pathway in coinfected cells. J. Virol. 84(20), 10488-10500 (2010).
96. Ling PD, Rawlins DR, Hayward SD. The Epstein-Barr virus immortalizing protein EBNA-2 is targeted to DNA by a cellular enhancer-binding protein. Proc. Natl Acad. Sci. USA 90(20), 9237-9241 (1993).
97. Henkel T, Ling PD, Hayward SD, Peterson MG. Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa. Science 265(5168), 92-95 (1994).
98. Hsieh JJ, Hayward SD. Masking of the CBF1/RBPJ kappa transcriptional repression domain by Epstein-Barr virus EBNA2. Science 268(5210), 560-563 (1995).
99. Hsieh JJ, Henkel T, Salmon P, Robey E, Peterson MG, Hayward SD. Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol. Cell. Biol. 16(3), 952-959 (1996).
100. Hsieh JJ, Nofziger DE, Weinmaster G, Hayward SD. Epstein-Barr virus immortalization: Notch2 interacts with CBF1 and blocks differentiation. J. Virol. 71(3), 1938-1945 (1997).
101. Hofelmayr H, Strobl LJ, Stein C et al. Activated mouse Notch1 transactivates Epstein-Barr virus nuclear antigen 2-regulated viral promoters. J. Virol. 73(4), 2770-2780 (1999).
102. Strobl LJ, Hofelmayr H, Marschall G, Brielmeier M, Bornkamm GW, Zimber-Strobl U. Activated Notch1 modulates gene expression in B cells similarly to Epstein-Barr viral nuclear antigen 2. J. Virol. 74(4), 1727-1735 (2000).
103. Gordadze AV, Peng R, Tan J et al. Notch1IC partially replaces EBNA2 function in B cells immortalized by Epstein-Barr virus. J. Virol. 75(13), 5899-5912 (2001).
104. Hofelmayr H, Strobl LJ, Marschall G, Bornkamm GW, Zimber-Strobl U. Activated Notch1 can transiently substitute for EBNA2 in the maintenance of proliferation of LMP1-expressing immortalized B cells. J. Virol. 75(5), 2033-2040 (2001).
105. Kohlhof H, Hampel F, Hoffmann R et al. Notch1, Notch2, and Epstein-Barr virus-encoded nuclear antigen 2 signaling differentially affects proliferation and survival of Epstein-Barr virus-infected B cells. Blood 113(22), 5506-5515 (2009).
106. Zhang J, Chen H, Weinmaster G, Hayward SD. Epstein-Barr virus BamHi-a rightward transcript-encoded RPMS protein interacts with the CBF1-associated corepressor CIR to negatively regulate the activity of EBNA2 and NotchIC. J. Virol. 75(6), 2946-2956 (2001).
107. Robertson ES, Lin J, Kieff E. The aminoterminal domains of Epstein-Barr virus nuclear proteins 3A, 3B, and 3C interact with RBPJkappa. J. Virol. 70(5), 3068-3074 (1996).
108. Zhao B, Marshall DR, Sample CE. A conserved domain of the Epstein-Barr virus nuclear antigens 3A and 3C binds to a discrete domain of Jkappa. J. Virol. 70(7), 4228-4236 (1996).
109. Johannsen E, Miller CL, Grossman SR, Kieff E. EBNA-2 and EBNA-3C extensively and mutually exclusively associate with RBPJkappa in Epstein-Barr virustransformed B lymphocytes. J. Virol. 70(6), 4179-4183 (1996).
110. Radkov SA, Touitou R, Brehm A et al. Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J. Virol. 73(7), 5688-5697 (1999).
111. Kempkes B, Zimber-Strobl U, Eissner G et al. Epstein-Barr virus nuclear antigen 2 (EBNA2)-oestrogen receptor fusion proteins complement the EBNA2-deficient Epstein-Barr virus strain P3HR1 in transformation of primary B cells but suppress growth of human B cell lymphoma lines. J. Gen. Virol. 77(Pt 2), 227-237 (1996).
112. Anderson LJ, Longnecker R. An autoregulatory loop for EBV LMP2A involves activation of Notch. Virology 371(2), 257-266 (2008).
113. Anderson LJ, Longnecker R. Epstein-Barr virus latent membrane protein 2A exploits Notch1 to alter B-cell identity in vivo. Blood 113(1), 108-116 (2009).
114. Farrell CJ, Lee JM, Shin EC, Cebrat M, Cole PA, Hayward SD. Inhibition of Epstein-Barr virus-induced growth proliferation by a nuclear antigen EBNA2-TAT peptide. Proc. Natl Acad. Sci. USA 101(13), 4625-4630 (2004).
115. Man CH, Wei-Man Lun S, Wai-Ying Hui J et al. Inhibition of NOTCH3 signalling significantly enhances sensitivity to cisplatin in EBV-associated nasopharyngeal carcinoma. J. Pathol. 226(3), 471-481 (2012).
116. Zagouras P, Stifani S, Blaumueller CM, Carcangiu ML, Artavanis-Tsakonas S. Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc. Natl Acad. Sci. USA 92(14), 6414-6418 (1995).
117. Gray GE, Mann RS, Mitsiadis E et al. Human ligands of the Notch receptor. Am. J. Pathol. 154(3), 785-794 (1999).
118. Veeraraghavalu K, Subbaiah VK, Srivastava S, Chakrabarti O, Syal R, Krishna S. Complementation of human papillomavirus type 16 E6 and E7 by Jagged1-specific Notch1-phosphatidylinositol 3-kinase signaling involves pleiotropic oncogenic functions independent of CBF1;Su(H);Lag-1 activation. J. Virol. 79(12), 7889-7898 (2005).
119. Talora C, Sgroi DC, Crum CP, Dotto GP. Specific down-modulation of Notch1 signaling in cervical cancer cells is required for sustained HPV-E6/E7 expression and late steps of malignant transformation. Genes Dev. 16(17), 2252-2263 (2002).
120. Talora C, Cialfi S, Segatto O et al. Constitutively active Notch1 induces growth arrest of HPV-positive cervical cancer cells via separate signaling pathways. Exp. Cell. Res. 305(2), 343-354 (2005).
121. Weijzen S, Zlobin A, Braid M, Miele L, Kast WM. HPV16 E6 and E7 oncoproteins regulate Notch-1 expression and cooperate to induce transformation. J. Cell. Physiol. 194(3), 356-362 (2003).
122. Lathion S, Schaper J, Beard P, Raj K. Notch1 can contribute to viral-induced transformation of primary human keratinocytes. Cancer Res. 63(24), 8687-8694 (2003).
123. Maliekal TT, Bajaj J, Giri V, Subramanyam D, Krishna S. The role of Notch signaling in human cervical cancer: implications for solid tumors. Oncogene 27(38), 5110-5114 (2008).
124. Tan CL, Gunaratne J, Lai D et al. HPV-18 E2E4 chimera. 2 new spliced transcripts and proteins induced by keratinocyte differentiation. Virology 429(1), 47-56 (2012).
125. Brimer N, Lyons C, Wallberg AE, Vande Pol SB. Cutaneous papillomavirus E6 oncoproteins associate with MAML1 to repress transactivation and NOTCH signaling. Oncogene doi:10.1038/onc.2011.589 (2012) (Epub ahead of print).
126. Giovannini C, Lacchini M, Gramantieri L, Chieco P, Bolondi L. Notch3 intracellular domain accumulates in HepG2 cell line. Anticancer Res. 26(3A), 2123-2127 (2006).
127. Gramantieri L, Giovannini C, Lanzi A et al. Aberrant Notch3 and Notch4 expression in human hepatocellular carcinoma. Liver Int. 27(7), 997-1007 (2007).
128. Gao J, Chen C, Hong L et al. Expression of Jagged1 and its association with hepatitis B virus X protein in hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 356(2), 341-347 (2007).
129. Gao J, Song Z, Chen Y et al. Deregulated expression of Notch receptors in human hepatocellular carcinoma. Dig. Liver Dis. 40(2), 114-121 (2008).
130. Iwai A, Takegami T, Shiozaki T, Miyazaki T. Hepatitis C virus NS3 protein can activate the Notch-signaling pathway through binding to a transcription factor, SRCAP. PLoS One 6(6), e20718 (2011).
131. Fuchs M, Gerber J, Drapkin R et al. The p400 complex is an essential E1A transformation target. Cell 106(3), 297-307 (2001).
132. Eissenberg JC, Wong M, Chrivia JC. Human SRCAP and Drosophila melanogaster DOM are homologs that function in the notch signaling pathway. Mol. Cell. Biol. 25(15), 6559-6569 (2005).
133. Liu Z, Turkoz A, Jackson EN et al. Notch1 loss of heterozygosity causes vascular tumors and lethal hemorrhage in mice. J. Clin. Invest. 121(2), 800-808 (2011).
134. Mesri EA, Cesarman E, Boshoff C. Kaposi's sarcoma and its associated herpesvirus. Nat. Rev. Cancer 10(10), 707-719 (2010).
135. Grayson W, Pantanowitz L. Histological variants of cutaneous Kaposi sarcoma. Diagn. Pathol. 3, 31 (2008).