Previous Article | Next Article 
Journal of Virology, October 2000, p. 9680-9693, Vol. 74, No. 20
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Multi-PDZ Domain Protein MUPP1 Is a Cellular Target
for both Adenovirus E4-ORF1 and High-Risk Papillomavirus Type 18 E6 Oncoproteins
Siu Sylvia
Lee,1
Britt
Glaunsinger,1
Fiamma
Mantovani,2
Lawrence
Banks,2 and
Ronald T.
Javier1,*
Department of Molecular Virology and
Microbiology, Baylor College of Medicine, Houston, Texas
77030,1 and International Center for
Genetic Engineering and Biotechnology, I-34012 Trieste,
Italy2
Received 10 April 2000/Accepted 13 July 2000
A general theme that has emerged from studies of DNA tumor viruses
is that otherwise unrelated oncoproteins encoded by these viruses often
target the same important cellular factors. Major oncogenic
determinants for human adenovirus type 9 (Ad9) and high-risk human
papillomaviruses (HPV) are the E4-ORF1 and E6 oncoproteins, respectively, and although otherwise unrelated, both of these viral
proteins possess a functional PDZ domain-binding motif that is
essential for their transforming activity and for binding to the PDZ
domain-containing and putative tumor suppressor protein DLG. We report
here that the PDZ domain-binding motifs of Ad9 E4-ORF1 and high-risk
HPV-18 E6 also mediate binding to the widely expressed cellular factor
MUPP1, a large multi-PDZ domain protein predicted to function as an
adapter in signal transduction. With regard to the consequences of
these interactions in cells, we showed that Ad9 E4-ORF1 aberrantly
sequesters MUPP1 within the cytoplasm of cells whereas HPV-18 E6
targets this cellular protein for degradation. These effects were
specific because mutant viral proteins unable to bind MUPP1 lack these
activities. From these results, we propose that the multi-PDZ domain
protein MUPP1 is involved in negatively regulating cellular
proliferation and that the transforming activities of two different
viral oncoproteins depend, in part, on their ability to inactivate this
cellular factor.
*
Corresponding author. Mailing address: Department of
Molecular Virology and Microbiology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030. Phone: (713) 798-3898. Fax: (713) 798-3586. E-mail: rjavier{at}bcm.tmc.edu.
Journal of Virology, October 2000, p. 9680-9693, Vol. 74, No. 20
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
McCrea, P. D., Gu, D., Balda, M. S.
(2009). Junctional Music that the Nucleus Hears: Cell-Cell Contact Signaling and the Modulation of Gene Activity. Cold Spring Harb. Perspect. Biol.
1: a002923-a002923
[Abstract]
[Full Text]
-
Vos, R. M., Altreuter, J., White, E. A., Howley, P. M.
(2009). The Ubiquitin-Specific Peptidase USP15 Regulates Human Papillomavirus Type 16 E6 Protein Stability. J. Virol.
83: 8885-8892
[Abstract]
[Full Text]
-
Bulgakova, N. A., Knust, E.
(2009). The Crumbs complex: from epithelial-cell polarity to retinal degeneration. J. Cell Sci.
122: 2587-2596
[Abstract]
[Full Text]
-
Katzenellenbogen, R. A., Vliet-Gregg, P., Xu, M., Galloway, D. A.
(2009). NFX1-123 Increases hTERT Expression and Telomerase Activity Posttranscriptionally in Human Papillomavirus Type 16 E6 Keratinocytes. J. Virol.
83: 6446-6456
[Abstract]
[Full Text]
-
Adachi, M., Hamazaki, Y., Kobayashi, Y., Itoh, M., Tsukita, S., Furuse, M., Tsukita, S.
(2009). Similar and Distinct Properties of MUPP1 and Patj, Two Homologous PDZ Domain-Containing Tight-Junction Proteins. Mol. Cell. Biol.
29: 2372-2389
[Abstract]
[Full Text]
-
Thomas, M. A., Broughton, R. S., Goodrum, F. D., Ornelles, D. A.
(2009). E4orf1 Limits the Oncolytic Potential of the E1B-55K Deletion Mutant Adenovirus. J. Virol.
83: 2406-2416
[Abstract]
[Full Text]
-
Lanaspa, M. A., Andres-Hernando, A., Rivard, C. J., Dai, Y., Berl, T.
(2008). Hypertonic stress increases claudin-4 expression and tight junction integrity in association with MUPP1 in IMCD3 cells. Proc. Natl. Acad. Sci. USA
105: 15797-15802
[Abstract]
[Full Text]
-
Guillaume, J.-L., Daulat, A. M., Maurice, P., Levoye, A., Migaud, M., Brydon, L., Malpaux, B., Borg-Capra, C., Jockers, R.
(2008). The PDZ Protein Mupp1 Promotes Gi Coupling and Signaling of the Mt1 Melatonin Receptor. J. Biol. Chem.
283: 16762-16771
[Abstract]
[Full Text]
-
Spanos, W. C., Hoover, A., Harris, G. F., Wu, S., Strand, G. L., Anderson, M. E., Klingelhutz, A. J., Hendriks, W., Bossler, A. D., Lee, J. H.
(2008). The PDZ Binding Motif of Human Papillomavirus Type 16 E6 Induces PTPN13 Loss, Which Allows Anchorage-Independent Growth and Synergizes with Ras for Invasive Growth. J. Virol.
82: 2493-2500
[Abstract]
[Full Text]
-
Liu, X., Disbrow, G. L., Yuan, H., Tomaic, V., Schlegel, R.
(2007). Myc and Human Papillomavirus Type 16 E7 Genes Cooperate To Immortalize Human Keratinocytes. J. Virol.
81: 12689-12695
[Abstract]
[Full Text]
-
Chung, S.-H., Frese, K. K., Weiss, R. S., Prasad, B. V. V., Javier, R. T.
(2007). A New Crucial Protein Interaction Element That Targets the Adenovirus E4-ORF1 Oncoprotein to Membrane Vesicles. J. Virol.
81: 4787-4797
[Abstract]
[Full Text]
-
Filippova, M., Johnson, M. M., Bautista, M., Filippov, V., Fodor, N., Tungteakkhun, S. S., Williams, K., Duerksen-Hughes, P. J.
(2007). The Large and Small Isoforms of Human Papillomavirus Type 16 E6 Bind to and Differentially Affect Procaspase 8 Stability and Activity. J. Virol.
81: 4116-4129
[Abstract]
[Full Text]
-
Storrs, C. H., Silverstein, S. J.
(2007). PATJ, a Tight Junction-Associated PDZ Protein, Is a Novel Degradation Target of High-Risk Human Papillomavirus E6 and the Alternatively Spliced Isoform 18 E6. J. Virol.
81: 4080-4090
[Abstract]
[Full Text]
-
Zhang, Y., Dasgupta, J., Ma, R. Z., Banks, L., Thomas, M., Chen, X. S.
(2007). Structures of a Human Papillomavirus (HPV) E6 Polypeptide Bound to MAGUK Proteins: Mechanisms of Targeting Tumor Suppressors by a High-Risk HPV Oncoprotein. J. Virol.
81: 3618-3626
[Abstract]
[Full Text]
-
Sugihara-Mizuno, Y., Adachi, M., Kobayashi, Y., Hamazaki, Y., Nishimura, M., Imai, T., Furuse, M., Tsukita, S.
(2007). Molecular characterization of angiomotin/JEAP family proteins: interaction with MUPP1/Patj and their endogenous properties. GENES CELLS
12: 473-486
[Abstract]
[Full Text]
-
Jing, M., Bohl, J., Brimer, N., Kinter, M., Vande Pol, S. B.
(2007). Degradation of Tyrosine Phosphatase PTPN3 (PTPH1) by Association with Oncogenic Human Papillomavirus E6 Proteins. J. Virol.
81: 2231-2239
[Abstract]
[Full Text]
-
Handa, K., Yugawa, T., Narisawa-Saito, M., Ohno, S.-i., Fujita, M., Kiyono, T.
(2007). E6AP-Dependent Degradation of DLG4/PSD95 by High-Risk Human Papillomavirus Type 18 E6 Protein. J. Virol.
81: 1379-1389
[Abstract]
[Full Text]
-
Rehtanz, M., Ghim, S.-j., Rector, A., Van Ranst, M., Fair, P. A., Bossart, G. D., Jenson, A. B.
(2006). Isolation and characterization of the first American bottlenose dolphin papillomavirus: Tursiops truncatus papillomavirus type 2. J. Gen. Virol.
87: 3559-3565
[Abstract]
[Full Text]
-
James, M. A., Lee, J. H., Klingelhutz, A. J.
(2006). Human Papillomavirus Type 16 E6 Activates NF-{kappa}B, Induces cIAP-2 Expression, and Protects against Apoptosis in a PDZ Binding Motif-Dependent Manner.. J. Virol.
80: 5301-5307
[Abstract]
[Full Text]
-
Heydecke, D., Meyer, D., Ackermann, F., Wilhelm, B., Gudermann, T., Boekhoff, I.
(2006). The Multi PDZ Domain Protein MUPP1 as a Putative Scaffolding Protein for Organizing Signaling Complexes in the Acrosome of Mammalian Spermatozoa. J Androl
27: 390-404
[Abstract]
[Full Text]
-
Wei, Q.
(2005). Pitx2a Binds to Human Papillomavirus Type 18 E6 Protein and Inhibits E6-mediated P53 Degradation in HeLa Cells. J. Biol. Chem.
280: 37790-37797
[Abstract]
[Full Text]
-
Simonson, S. J.S., Difilippantonio, M. J., Lambert, P. F.
(2005). Two Distinct Activities Contribute to Human Papillomavirus 16 E6's Oncogenic Potential. Cancer Res.
65: 8266-8273
[Abstract]
[Full Text]
-
Latorre, I. J., Roh, M. H., Frese, K. K., Weiss, R. S., Margolis, B., Javier, R. T.
(2005). Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J. Cell Sci.
118: 4283-4293
[Abstract]
[Full Text]
-
Favre-Bonvin, A., Reynaud, C., Kretz-Remy, C., Jalinot, P.
(2005). Human Papillomavirus Type 18 E6 Protein Binds the Cellular PDZ Protein TIP-2/GIPC, Which Is Involved in Transforming Growth Factor {beta} Signaling and Triggers Its Degradation by the Proteasome. J. Virol.
79: 4229-4237
[Abstract]
[Full Text]
-
Liu, X., Yuan, H., Fu, B., Disbrow, G. L., Apolinario, T., Tomaic, V., Kelley, M. L., Baker, C. C., Huibregtse, J., Schlegel, R.
(2005). The E6AP Ubiquitin Ligase Is Required for Transactivation of the hTERT Promoter by the Human Papillomavirus E6 Oncoprotein. J. Biol. Chem.
280: 10807-10816
[Abstract]
[Full Text]
-
Kelley, M. L., Keiger, K. E., Lee, C. J., Huibregtse, J. M.
(2005). The Global Transcriptional Effects of the Human Papillomavirus E6 Protein in Cervical Carcinoma Cell Lines Are Mediated by the E6AP Ubiquitin Ligase. J. Virol.
79: 3737-3747
[Abstract]
[Full Text]
-
Magal, S. S., Jackman, A., Ish-Shalom, S., Botzer, L. E., Gonen, P., Schlegel, R., Sherman, L.
(2005). Downregulation of Bax mRNA expression and protein stability by the E6 protein of human papillomavirus 16. J. Gen. Virol.
86: 611-621
[Abstract]
[Full Text]
-
Lee, C., Laimins, L. A.
(2004). Role of the PDZ Domain-Binding Motif of the Oncoprotein E6 in the Pathogenesis of Human Papillomavirus Type 31. J. Virol.
78: 12366-12377
[Abstract]
[Full Text]
-
Coyne, C. B., Voelker, T., Pichla, S. L., Bergelson, J. M.
(2004). The Coxsackievirus and Adenovirus Receptor Interacts with the Multi-PDZ Domain Protein-1 (MUPP-1) within the Tight Junction. J. Biol. Chem.
279: 48079-48084
[Abstract]
[Full Text]
-
Filippova, M., Parkhurst, L., Duerksen-Hughes, P. J.
(2004). The Human Papillomavirus 16 E6 Protein Binds to Fas-associated Death Domain and Protects Cells from Fas-triggered Apoptosis. J. Biol. Chem.
279: 25729-25744
[Abstract]
[Full Text]
-
Longworth, M. S., Laimins, L. A.
(2004). Pathogenesis of Human Papillomaviruses in Differentiating Epithelia. Microbiol. Mol. Biol. Rev.
68: 362-372
[Abstract]
[Full Text]
-
Stewart, D., Kazemi, S., Li, S., Massimi, P., Banks, L., Koromilas, A. E., Matlashewski, G.
(2004). Ubiquitination and proteasome degradation of the E6 proteins of human papillomavirus types 11 and 18. J. Gen. Virol.
85: 1419-1426
[Abstract]
[Full Text]
-
Schneeberger, E. E., Lynch, R. D.
(2004). The tight junction: a multifunctional complex. Am. J. Physiol. Cell Physiol.
286: C1213-C1228
[Abstract]
[Full Text]
-
Oh, S. T., Longworth, M. S., Laimins, L. A.
(2004). Roles of the E6 and E7 Proteins in the Life Cycle of Low-Risk Human Papillomavirus Type 11. J. Virol.
78: 2620-2626
[Abstract]
[Full Text]
-
Nguyen, M. M., Nguyen, M. L., Caruana, G., Bernstein, A., Lambert, P. F., Griep, A. E.
(2003). Requirement of PDZ-Containing Proteins for Cell Cycle Regulation and Differentiation in the Mouse Lens Epithelium. Mol. Cell. Biol.
23: 8970-8981
[Abstract]
[Full Text]
-
Watson, R. A., Thomas, M., Banks, L., Roberts, S.
(2003). Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes. J. Cell Sci.
116: 4925-4934
[Abstract]
[Full Text]
-
McMurray, H. R., McCance, D. J.
(2003). Human Papillomavirus Type 16 E6 Activates TERT Gene Transcription through Induction of c-Myc and Release of USF-Mediated Repression. J. Virol.
77: 9852-9861
[Abstract]
[Full Text]
-
Nguyen, M. L., Nguyen, M. M., Lee, D., Griep, A. E., Lambert, P. F.
(2003). The PDZ Ligand Domain of the Human Papillomavirus Type 16 E6 Protein Is Required for E6's Induction of Epithelial Hyperplasia In Vivo. J. Virol.
77: 6957-6964
[Abstract]
[Full Text]
-
Nguyen, M., Song, S., Liem, A., Androphy, E., Liu, Y., Lambert, P. F.
(2002). A Mutant of Human Papillomavirus Type 16 E6 Deficient in Binding {alpha}-Helix Partners Displays Reduced Oncogenic Potential In Vivo. J. Virol.
76: 13039-13048
[Abstract]
[Full Text]
-
Kumar, A., Zhao, Y., Meng, G., Zeng, M., Srinivasan, S., Delmolino, L. M., Gao, Q., Dimri, G., Weber, G. F., Wazer, D. E., Band, H., Band, V.
(2002). Human Papillomavirus Oncoprotein E6 Inactivates the Transcriptional Coactivator Human ADA3. Mol. Cell. Biol.
22: 5801-5812
[Abstract]
[Full Text]
-
Filippova, M., Song, H., Connolly, J. L., Dermody, T. S., Duerksen-Hughes, P. J.
(2002). The Human Papillomavirus 16 E6 Protein Binds to Tumor Necrosis Factor (TNF) R1 and Protects Cells from TNF-induced Apoptosis. J. Biol. Chem.
277: 21730-21739
[Abstract]
[Full Text]
-
Gao, Q., Kumar, A., Singh, L., Huibregtse, J. M., Beaudenon, S., Srinivasan, S., Wazer, D. E., Band, H., Band, V.
(2002). Human Papillomavirus E6-induced Degradation of E6TP1 Is Mediated by E6AP Ubiquitin Ligase. Cancer Res.
62: 3315-3321
[Abstract]
[Full Text]
-
Gardiol, D., Galizzi, S., Banks, L.
(2002). Mutational analysis of the discs large tumour suppressor identifies domains responsible for human papillomavirus type 18 E6-mediated degradation. J. Gen. Virol.
83: 283-289
[Abstract]
[Full Text]
-
Vaccaro, P., Brannetti, B., Montecchi-Palazzi, L., Philipp, S., Citterich, M. H., Cesareni, G., Dente, L.
(2001). Distinct Binding Specificity of the Multiple PDZ Domains of INADL, a Human Protein with Homology to INAD from Drosophila melanogaster. J. Biol. Chem.
276: 42122-42130
[Abstract]
[Full Text]
-
Thomas, D. L., Schaack, J., Vogel, H., Javier, R.
(2001). Several E4 Region Functions Influence Mammary Tumorigenesis by Human Adenovirus Type 9. J. Virol.
75: 557-568
[Abstract]
[Full Text]
-
Hamazaki, Y., Itoh, M., Sasaki, H., Furuse, M., Tsukita, S.
(2002). Multi-PDZ Domain Protein 1 (MUPP1) Is Concentrated at Tight Junctions through Its Possible Interaction with Claudin-1 and Junctional Adhesion Molecule. J. Biol. Chem.
277: 455-461
[Abstract]
[Full Text]