MDM2-Dependent Inhibition of p53 Is Required for Epstein-Barr Virus B-Cell Growth Transformation and Infected-Cell Survival
Open accessAbstract
Epstein-Barr virus (EBV) growth transformation of primary B lymphocytes into indefinitely proliferating lymphoblastoid cell lines (LCLs) depends on the concerted activities of a subset of viral proteins expressed during latency. EBV drives quiescent B cells into S phase, and consequently, a host response is activated that includes expression of p53 and its target genes. Since LCLs retain wild-type p53, it was of interest to determine what contribution the p53 pathway may have in controlling established LCL growth and EBV-mediated transformation of primary B cells. We found that liberation of p53 through chemical antagonism of one of its major ubiquitin ligases, MDM2, using the small-molecule Nutlin-3 led to apoptosis of established LCLs and suppressed EBV-mediated transformation of primary B cells. The activation of latent p53 induced target genes associated with apoptosis. Furthermore, MDM2 antagonism synergized with NF-κB inhibition in killing LCLs. NF-κB was important to increase steady-state MDM2 protein levels rather than in affecting p53-dependent transcription, suggesting a unique mechanism by which LCLs survive in the presence of a primed p53 pathway. Nutlin sensitivity of EBV-infected cells provides a novel system for studying the pathways that dictate LCL survival and regulate EBV transformation. Finally, MDM2 antagonists may be considered for therapeutic intervention in EBV-associated malignancies expressing wild-type p53.
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EBV expresses latency antigens that stabilize MDM2.
“EBV is associated with several tumour types, and it expresses latency antigens that stabilize MDM2 (Ref. 56).”
From MDM2, MDMX and p53 in oncogenesis and cancer therapy (2013) · cites this paper as [56]
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Cites
In Vivo Activation of the p53 Pathway by Small-Molecule Antagonists of MDM2
Vassilev, L. T., Vu, B. T., Graves, B., Carvajal, D., Podlaski, F., Filipovic, Z., Kong, N., Kammlott, U., Lukacs, C., Klein, C., et al. (2004) · Science · doi:10.1126/science.1092472 · Cited by 4,661 · see citing works
Wang, C.-Y., Mayo, M., Korneluk, R., Goeddel, D., & Baldwin, A. (1998) · Science · doi:10.1126/science.281.5383.1680 · Cited by 2,950 · see citing works
DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis
Bartkova, J., Hořejší, Z., Koed, K., Krämer, A., Tort, F., Zieger, K., Guldberg, P., Sehested, M., Nesland, J. M., Lukas, C., et al. (2005) · Nature · doi:10.1038/nature03482 · Cited by 2,688 · see citing works
Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions
Gorgoulis, V. G., Vassiliou, L.-V. F., Karakaidos, P., Zacharatos, P., Kotsinas, A., Liloglou, T., Venere, M., DiTullio, R. A., Kastrinakis, N. G., Levy, B., et al. (2005) · Nature · doi:10.1038/nature03485 · Cited by 2,009 · see citing works
Epstein-Barr virus and its replication
Kieff, E. D. (1996) · Medical Entomology and Zoology · Cited by 1,627 · see citing works
Stable replication of plasmids derived from Epstein–Barr virus in various mammalian cells
Yates, J. L., Warren, N., & Sugden, B. (1985) · Nature · doi:10.1038/313812a0 · Cited by 1,305 · see citing works
An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells
Wang, D., Liebowitz, D. N., & Kieff, E. D. (1985) · Cell · doi:10.1016/0092-8674(85)90256-9 · Cited by 1,253 · see citing works
Small-molecule MDM2 antagonists reveal aberrant p53 signaling in cancer: implications for therapy
Tovar, C., Rosinski, J., Filipovic, Z., Higgins, B., Kolinsky, K., Hilton, H., Zhao, X., Vu, B. T., Qing, W., Packman, K., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507493103 · Cited by 708 · see citing works
[29] Mitochondrial membrane potential monitored by JC-1 dye
Reers, M., Smiley, S. T., Mottola-Hartshorn, C., Chen, A., Mei, L., & Chen, L. B. (1995) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(95)60154-6 · Cited by 682 · see citing works
Transcriptional Cross Talk between NF-κB and p53
Webster, G. A., & Perkins, N. D. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.5.3485 · Cited by 598 · see citing works
Wang, C.-Y., D, D. C. G., Mayo, M. W., & Baldwin, A. S. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.9.5923 · Cited by 586 · see citing works
Kulwichit, W., Edwards, R. H., Davenport, E. M., Baskar, J. F., Godfrey, V., & Raab‐Traub, N. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11963 · Cited by 414 · see citing works
Juven‐Gershon, T., Barak, Y., Zauberman, A., George, D. L., & Oren, M. (1993) · PubMed · Cited by 332 · see citing works
The p53 response to DNA damage
Meek, D. W. (2004) · DNA Repair · doi:10.1016/j.dnarep.2004.03.027 · Cited by 329 · see citing works
Sinclair, A. J., Palmero, I., Peters, G., & Farrell, P. J. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06634.x · Cited by 299 · see citing works
NF-κB inhibition causes spontaneous apoptosis in Epstein–Barr virus-transformed lymphoblastoid cells
Cahir-McFarland, E. D., Davidson, D. M., Schauer, S. L., Duong, J., & Kieff, E. D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.100119497 · Cited by 259 · see citing works
Fries, K., Miller, W. E., & Raab‐Traub, N. (1996) · Journal of Virology · doi:10.1128/jvi.70.12.8653-8659.1996 · Cited by 253 · see citing works
MDMX overexpression prevents p53 activation by the MDM2 inhibitor Nutlin
Hu, B., Gilkes, D. M., Farooqi, B., Sebti, S. M., & Chen, J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.c600147200 · Cited by 236 · see citing works
Cahir-McFarland, E. D., Carter, K. L., Rosenwald, A., Giltnane, J. M., Henrickson, S. E., Staudt, L. M., & Kieff, E. D. (2004) · Journal of Virology · doi:10.1128/jvi.78.8.4108-4119.2004 · Cited by 233 · see citing works
Levels of HdmX expression dictate the sensitivity of normal and transformed cells to Nutlin-3
Patton, J. T., Mayo, L. D., Singhi, A. D., Gudkov, A. V., Stark, G. R., & Jackson, M. W. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3832 · Cited by 189 · see citing works
CREB-binding Protein Is a Nuclear Integrator of Nuclear Factor-κB and p53 Signaling
Wadgaonkar, R., Phelps, K. M., Haque, Z. K., Williams, A. J., Silverman, E. S., & Collins, T. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.4.1879 · Cited by 188 · see citing works
An shRNA barcode screen provides insight into cancer cell vulnerability to MDM2 inhibitors
Brummelkamp, T. R., Fabius, A. W. M., Mullenders, J., Madiredjo, M., Velds, A., Kerkhoven, R. M., Bernards, R., & Beijersbergen, R. L. (2006) · Nature Chemical Biology · doi:10.1038/nchembio774 · Cited by 187 · see citing works
Hdmx modulates the outcome of p53 activation in human tumor cells
Wade, M., Wong, E. T., Tang, M., Stommel, J. M., & Wahl, G. M. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605405200 · Cited by 163 · see citing works
McFarland, E. C., Izumi, K. M., & Mosialos, G. (1999) · Oncogene · doi:10.1038/sj.onc.1203217 · Cited by 159 · see citing works
p53-mediated repression of nuclear factor-kappaB RelA via the transcriptional integrator p300.
Ravi, R. K., Mookerjee, B., van Hensbergen, Y., Bedi, G. C., Giordano, A., El‐Deiry, W. S., Fuchs, E. J., & Bedi, A. (1998) · PubMed · Cited by 156 · see citing works
Altmann, M., Pich, D., Ruiss, R., Wang, J.-D., Sugden, B., & Hammerschmidt, W. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605985103 · Cited by 146 · see citing works
Reactivation of the p53 pathway as a treatment modality for KSHV-induced lymphomas
Sarek, G., Kurki, S., Enbäck, J., Iotzova, G., Haas, J., Laakkonen, P. M., Laiho, M., & Ojala, P. M. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30945 · Cited by 141 · see citing works
Genetic Evidence that EBNA-1 Is Needed for Efficient, Stable Latent Infection by Epstein-Barr Virus
Lee, M.-A., Diamond, M. E., & Yates, J. L. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.2974-2982.1999 · Cited by 134 · see citing works
Petre, C. E., Sin, S., & Dittmer, D. P. (2006) · Journal of Virology · doi:10.1128/jvi.01757-06 · Cited by 121 · see citing works
Epstein‐Barr virus efficiently immortalizes human B cells without neutralizing the function of p53.
Allday, M. J., Sinclair, A. J., Parker, G. A., Crawford, D., & Farrell, P. J. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07124.x · Cited by 107 · see citing works
Viral interactions with the Notch pathway
Hayward, S. D. (2004) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2004.04.018 · Cited by 95 · see citing works
The EBV-encoded LMP1 protein inhibits p53-triggered apoptosis but not growth arrest.
Okan, İ., Wang, Y., Chen, F., HU, L., Imreh, S., Klein, G., & Wiman, K. G. (1995) · PubMed · Cited by 77 · see citing works
Nutlin-3 inhibits the NFκB Pathway in a p53 Dependent Manner: Implications in Lung Cancer Therapy
Dey, A., Wong, E. T., Bist, P., Tergaonkar, V., & Lane, D. (2007) · Cell Cycle · doi:10.4161/cc.6.17.4643 · Cited by 70 · see citing works
Cannell, E., Farrell, P. J., & Sinclair, A. J. (1996) · PubMed · Cited by 44 · see citing works
O’Nions, J., & Allday, M. J. (2003) · Oncogene · doi:10.1038/sj.onc.1206838 · Cited by 29 · see citing works
Tamm, K. P., Okan, İ., Kashuba, E., L√∂wbeer, M., Klein, G., & Székely, L. (1999) · Journal of General Virology · doi:10.1099/0022-1317-80-4-987 · Cited by 18 · see citing works
Wild-type p53 reduces radiation hypermutability in p53-mutated human lymphoblast cells
Zhang, Q., Liu, Y., Zhou, J.-C., Chen, W., Zhang, Y., & Liber, H. L. (2007) · Mutagenesis · doi:10.1093/mutage/gem021 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mapping and analysis of chromatin state dynamics in nine human cell types
Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., et al. (2011) · Nature · doi:10.1038/nature09906 · Cited by 2,898 · see citing works
MDM2, MDMX and p53 in oncogenesis and cancer therapy
Wade, M., Li, Y.-C., & Wahl, G. M. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3430 · Cited by 1,279 · see citing works
Gene expression changes with age in skin, adipose tissue, blood and brain
Glass, D., Viñuela, A., Davies, M. N., Ramasamy, A., Parts, L., Knowles, D. A., Brown, A. A., Hedman, Å. K., Small, K. S., Buil, A., et al. (2013) · Genome biology · doi:10.1186/gb-2013-14-7-r75 · Cited by 281 · see citing works
Baldwin, A. S. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01095.x · Cited by 277 · see citing works
Apoptosis: why and how does it occur in biology?
Ulukaya, E., Açılan, C., & Yilmaz, Y. N. (2011) · Cell Biochemistry and Function · doi:10.1002/cbf.1774 · Cited by 229 · see citing works
A Human Herpesvirus MicroRNA Inhibits p21 Expression and Attenuates p21-Mediated Cell Cycle Arrest
Gottwein, E., & Cullen, B. R. (2010) · Journal of Virology · doi:10.1128/jvi.00202-10 · Cited by 158 · see citing works
CRISPR/Cas9 Screens Reveal Epstein-Barr Virus-Transformed B Cell Host Dependency Factors
Ma, Y., Walsh, M. J., Bernhardt, K., Ashbaugh, C. W., Trudeau, S. J., Ashbaugh, I. Y., Jiang, S., Jiang, C., Zhao, B., Root, D. E., et al. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.04.005 · Cited by 137 · see citing works
Tumor viruses and cancer biology: Modulating signaling pathways for therapeutic intervention
Saha, A., Kaul, R., Murakami, M., & Robertson, E. S. (2010) · Cancer Biology & Therapy · doi:10.4161/cbt.10.10.13923 · Cited by 123 · see citing works
Epstein–Barr Virus: Diseases Linked to Infection and Transformation
Jha, H. C., Pei, Y., & Robertson, E. S. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01602 · Cited by 111 · see citing works
Human Oncoviruses and p53 Tumor Suppressor Pathway Deregulation at the Origin of Human Cancers
Tornesello, M. L., Annunziata, C., Tornesello, A. L., Buonaguro, L., & Buonaguro, F. M. (2018) · Cancers · doi:10.3390/cancers10070213 · Cited by 87 · see citing works
Hagemeier, S. R., Barlow, E. A., Meng, Q., & Kenney, S. C. (2012) · Journal of Virology · doi:10.1128/jvi.01850-12 · Cited by 82 · see citing works
EBV and Apoptosis: The Viral Master Regulator of Cell Fate?
Fitzsimmons, L., & Kelly, G. L. (2017) · Viruses · doi:10.3390/v9110339 · Cited by 79 · see citing works
Dolcetti, R., Col, J. D., Martorelli, D., Carbone, A., & Klein, E. (2013) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.07.005 · Cited by 66 · see citing works
Krasavin, M. (2014) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2014.11.028 · Cited by 64 · see citing works
Epstein-Barr Virus Nuclear Antigen 3C Stabilizes Gemin3 to Block p53-mediated Apoptosis
Cai, Q., Guo, Y., Xiao, B., Banerjee, S., Saha, A., Lu, J. L., Glisovic, T., & Robertson, E. S. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002418 · Cited by 64 · see citing works
RetractedSoRelle, E. D., Reinoso-Vizcaíno, N. M., Horn, G. Q., & Luftig, M. A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1001145 · Cited by 63 · see citing works
Self-citationGallo, A., Vella, S., Miele, M., Timoneri, F., Bella, M. D., Bosi, S. R. A., Sciveres, M., & Conaldi, P. G. (2016) · Cancer Letters · doi:10.1016/j.canlet.2016.12.003 · Cited by 58 · see citing works
Mdm2 Promotes Systemic Lupus Erythematosus and Lupus Nephritis
Allam, R., Sayyed, S. G., Kulkarni, O. P., Lichtnekert, J., & Anders, H. (2011) · Journal of the American Society of Nephrology · doi:10.1681/asn.2011010045 · Cited by 52 · see citing works
Genetic transformation of lignin degrading fungi facilitated by Agrobacterium tumefaciens
Sharma, K. K., & Kuhad, R. C. (2010) · BMC Biotechnology · doi:10.1186/1472-6750-10-67 · Cited by 50 · see citing works
HIV-1 Vif promotes the G1- to S-phase cell-cycle transition
Wang, J., Reuschel, E. L., Shackelford, J. M., Jeang, L. J., Shivers, D. K., Diehl, J. A., Yu, X.-F., & Finkel, T. H. (2010) · Blood · doi:10.1182/blood-2010-06-289215 · Cited by 43 · see citing works
Extracellular circulating viral microRNAs: current knowledge and perspectives
Laganà, A., Russo, F., Veneziano, D., Bella, S. D., Giugno, R., Pulvirenti, A., Croce, C. M., & Ferro, A. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00120 · Cited by 43 · see citing works
Interference with p53 functions in human viral infections, a target for novel antiviral strategies?
Lazo, P. A., & Santos, C. R. (2011) · Reviews in Medical Virology · doi:10.1002/rmv.696 · Cited by 41 · see citing works
Impact of EBV Essential Nuclear Protein EBNA-3C on B-Cell Proliferation and Apoptosis
Saha, A., & Robertson, E. S. (2013) · Future Microbiology · doi:10.2217/fmb.12.147 · Cited by 39 · see citing works
Role of EBNA-3 Family Proteins in EBV Associated B-cell Lymphomagenesis
Bhattacharjee, S., Roy, S. G., Bose, P., & Saha, A. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00457 · Cited by 32 · see citing works
Lee, J., Nam, H. ‐., Shim, S.-M., Bae, G. ‐., Han, B. G., & Jeon, J. P. (2010) · Cell Proliferation · doi:10.1111/j.1365-2184.2010.00687.x · Cited by 28 · see citing works
EBNA3C regulates p53 through induction of Aurora kinase B
Jha, H. C., Yang, K., El-Naccache, D. W., Sun, Z., & Robertson, E. S. (2015) · Oncotarget · doi:10.18632/oncotarget.3310 · Cited by 28 · see citing works
Hayashida, K., Kajino, K., Hattori, M., Wallace, M., Morrison, I. W., Greene, M. I., & Sugimoto, C. (2012) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2012.08.008 · Cited by 28 · see citing works
Aspesi, A., Monteleone, V., Betti, M., Actis, C., Morleo, G., Sculco, M., Guarrera, S., Włodarski, M. W., Ramenghi, U., Santoro, C., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-12307-5 · Cited by 25 · see citing works
Mdm2 protein Expression is Strongly Associated with Survival in Malignant Pleural Mesothelioma
Mairinger, F. D., Walter, R. F. H., Ting, S. C., Vollbrecht, C., Kollmeier, J., Griff, S., Hager, T., Mairinger, T., Christoph, D. C., Theegarten, D., et al. (2014) · Future Oncology · doi:10.2217/fon.13.261 · Cited by 24 · see citing works
At a Crossroads: Human DNA Tumor Viruses and the Host DNA Damage Response
Nikitin, P. A., & Luftig, M. A. (2011) · Future Virology · doi:10.2217/fvl.11.55 · Cited by 23 · see citing works
Self-citationSoRelle, E. D., Reinoso-Vizcaíno, N. M., Dai, J., Barry, A. P., Chan, C. C. W., & Luftig, M. A. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112958 · Cited by 23 · see citing works
Self-citationIdentification of Host Biomarkers of Epstein-Barr Virus Latency IIb and Latency III
Messinger, J. E., Dai, J., Stanland, L. J., Price, A. M., & Luftig, M. A. (2019) · mBio · doi:10.1128/mbio.01006-19 · Cited by 19 · see citing works
Self-citationLi, H., Li, Y., Hu, J., Liu, S., Luo, X., Tang, M., Bode, A. M., Dong, Z., Liu, X., Liao, W., et al. (2021) · Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics · doi:10.3727/096504021x16135618512563 · Cited by 21 · see citing works
In utero cell transfer between porcine littermates
McConico, A. L., Butters, K. A., Lien, K. R., Knudsen, B. E., Wu, X., Platt, J. L., & Ogle, B. M. (2011) · Reproduction Fertility and Development · doi:10.1071/rd10165 · Cited by 21 · see citing works
Montani, M. S. G., Tarquini, G. D., Santarelli, R., Gonnella, R., Romeo, M. A., Benedetti, R., Arena, A., Faggioni, A., & Cirone, M. (2021) · Carcinogenesis · doi:10.1093/carcin/bgab116 · Cited by 19 · see citing works
Mitra, B., Beri, N. R., Guo, R., Burton, E. M., Murray‐Nerger, L. A., & Gewurz, B. E. (2023) · mBio · doi:10.1128/mbio.02338-23 · Cited by 17 · see citing works
Pujals, A., Renouf, B., Robert, A., Chelouah, S., Hollville, É., & Wiels, J. (2011) · Cell Death and Disease · doi:10.1038/cddis.2011.67 · Cited by 17 · see citing works
Forst, C. V., Zhou, B., Wang, M., Chou, T.-W., Mason, G., Song, W., Schadt, E. E., Ghedin, E., & Zhang, B. (2017) · npj Systems Biology and Applications · doi:10.1038/s41540-017-0036-x · Cited by 16 · see citing works
Maurer‐Granofszky, M., Müller, A. C., Parapatics, K., Pickl, W. F., Wagner, C., Rudashevskaya, E. L., Breitwieser, F. P., Colinge, J., Garg, K., Griss, J., et al. (2014) · Journal of Proteome Research · doi:10.1021/pr401270y · Cited by 15 · see citing works
Advances in Laser Scanning Imaging Cytometry for High-Content Screening
Wylie, P. G., Onley, D. J., Hammerstein, A. F., & Bowen, W. P. (2015) · Assay and Drug Development Technologies · doi:10.1089/adt.2014.607 · Cited by 13 · see citing works
Everly, D. N., Mainou, B. A., & Raab‐Traub, N. (2009) · Journal of Virology · doi:10.1128/jvi.01422-09 · Cited by 13 · see citing works
Lv, D., Zhong, J., Zhang, K., Pandey, A., & Li, R. (2017) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2016.0158 · Cited by 12 · see citing works
Autoantibody to MDM2: A Potential Serological Marker of Systemic Lupus Erythematosus
Liu, Y., Dai, L., Liu, W., Shi, G., & Zhang, J. (2015) · Journal of Immunology Research · doi:10.1155/2015/963568 · Cited by 11 · see citing works
Ressel, S., Kumar, S., Bermúdez‐Barrientos, J. R., Gordon, K., Lane, J., Wu, J. C., Abreu‐Goodger, C., Schwarze, J., & Buck, A. H. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae116 · Cited by 11 · see citing works
Dangerous Liaisons: Gammaherpesvirus Subversion of the Immunoglobulin Repertoire
Zelazowska, M. A., McBride, K. M., & Krug, L. T. (2020) · Viruses · doi:10.3390/v12080788 · Cited by 9 · see citing works
Liu, L. G., Chang, C. R., Dai, J., Nikitin, P. A., Jima, D. D., Davé, S. S., & Luftig, M. A. (2017) · mSphere · doi:10.1128/msphere.00305-17 · Cited by 9 · see citing works
Self-citationCable, J. M., Wongwiwat, W., Grabowski, J. C., White, R. E., & Luftig, M. A. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2426339122 · Cited by 8 · see citing works
Self-citationEpstein Barr virus–positive B-cell lymphoma is highly vulnerable to MDM2 inhibitors in vivo
Zhang, X., Zhang, R., Ren, C., Xu, Y., Wu, S., Meng, C., Pataer, A., Song, X., Zhang, J., Yao, Y., et al. (2021) · Blood Advances · doi:10.1182/bloodadvances.2021006156 · Cited by 8 · see citing works
Epstein-Barr virus latent membrane protein 1 subverts IMPDH pathways to drive B-cell oncometabolism
Burton, E. M., Maestri, D., White, S., Liang, J., Mitra, B., Asara, J. M., & Gewurz, B. E. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1013092 · Cited by 8 · see citing works
Owens, S. M., Sifford, J. M., Li, G., Murdock, S. J., Salinas, E., Oldenburg, D. G., Ghosh, D., Stumhofer, J. S., Nookaew, I., Manzano, M., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-56247-5 · Cited by 6 · see citing works
Sp140L Is a Novel Herpesvirus Restriction FactorPreprint
Cable, J. M., Wongwiwat, W., Grabowski, J. C., White, R. E., & Luftig, M. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.13.628399 · Cited by 6 · see citing works
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Mund, R., & Whitehurst, C. B. (2024) · Viruses · doi:10.3390/v16101523 · Cited by 5 · see citing works
Liu, M., Zou, G., Fu, J., Fu, J., Chen, H., Pan, C., Liu, H., & Fu, L. (2025) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2025.119935 · Cited by 5 · see citing works
Bonglack, E. N., Hill, K. K., Barry, A. P., Bartlett, A., Castellano‐Escuder, P., Hirschey, M. D., & Luftig, M. A. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1012685 · Cited by 3 · see citing works
Self-citationMiao, M., Chen, Y., Wang, X., Li, S., & Hu, R. (2025) · Virulence · doi:10.1080/21505594.2025.2497908 · Cited by 4 · see citing works
Satoh, J., Kawana, N., & Yamamoto, Y. (2013) · Clinical and Experimental Neuroimmunology · doi:10.1111/cen3.12035 · Cited by 2 · see citing works
SoRelle, E. D., Dai, J., Reinoso-Vizcaíno, N. M., Barry, A. P., Chan, C. C. W., & Luftig, M. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.23.481342 · Cited by 2 · see citing works
Self-citationA study of inter-individual differences in the DNA damage response
Sefta, M. (2011) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 1 · see citing works
DNA Damage Response Suppresses Epstein-Barr Virus-Driven Proliferation of Primary Human B Cells
Nikitin, P. A. (2012) · DukeSpace (Duke University)
Computational regulatory genomics: motifs, networks, and dynamics
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Beta Actin Antibody Review and FAQs
Johnson, M. (2013) · Materials and Methods · doi:10.13070/mm.en.3.179
Li, H., Luo, X., Hu, J., Liu, S., Li, N., Tang, M., Weng, X., Wei, Y., Gao, J., Bode, A. M., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/383497
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Messinger, J. E., Dai, J., Stanland, L. J., Price, A. M., & Luftig, M. A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/616359
Self-citationOwens, S. M., Sifford, J. M., Li, G., Salinas, E., Ghosh, D., Miller, A. D., Stumhofer, J. S., & Forrest, J. C. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.02.233148
Discovery of Inhibitors of MDM2 Against Nasopharyngeal Cancer: An In-Silico Investigation
(2023) · Journal of Smart Science and Technology · doi:10.24191/jsst.v3i2.55
- Authors
- Forte, E., & Luftig, M. A.
- Affiliations
- Duke Medical Center (US)
- Corresponding author
- Luftig, Micah A.
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2009-03-15
- Volume
- 83
- Issue
- 6
- Pages
- 2491-2499
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC2648290
- OpenAlex
- W2107244203
- Cited by
- 65
- References
- 37
- Citations by year
- 2025: 6 · 2024: 3 · 2023: 3 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 6 · 2016: 3 · 2015: 3 · 2014: 3 · 2013: 7 · 2012: 5
- FWCI
- 3.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (P30AI064518)
- Topics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
- Health Sciences › Medicine › Epidemiology › Cytomegalovirus and herpesvirus research
- Keywords
- Epstein-Barr virus, MDM2, p53, lymphoblastoid cell lines, Nutlin-3, NF-κB, apoptosis, viral latency, p53 target genes, EBV-associated malignancies
- MeSH terms
- B-Lymphocytes, Cell Line, Cell Survival, Cell Transformation, Viral, Enzyme Inhibitors, Herpesvirus 4, Human, Humans, Imidazoles, Piperazines, Virus Replication, Tumor Suppressor Protein p53, NF-kappa B, Apoptosis, Proto-Oncogene Proteins c-mdm2
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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