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Science 14 August 1992:
Vol. 257. no. 5072, pp. 971 - 973
DOI: 10.1126/science.1323879
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Articles

Science, Vol 257, Issue 5072, 971-973
Copyright © 1992 by American Association for the Advancement of Science

articles

Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation

C Meyers, MG Frattini, JB Hudson, and LA Laimins

Department of Molecular Genetics and Cell Biology, Howard Hughes Medical Institute, University of Chicago, IL 60637.

The study of the human pathogen papillomaviruses (HPVs) has been hampered by the inability to propagate the virus in tissue culture. The addition of 12-O-tetradecanoyl phorbol-13-acetate to the media of organotypic (raft) cultures increased expression of physiological markers of keratinocyte differentiation and concomitantly induced production of virions. Capsid production was detected in differentiated suprabasal cells. Virions approximately 54 nanometers in size were observed by electron microscopy in raft tissue cross sections in the suprabasal layers. Virions purified through isopycnic gradients were found to contain type 31b DNA and exhibited an icosahedral shape similar to that of papillomaviruses found in clinical samples.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
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X. Wang, H.-K. Wang, J. P. McCoy, N. S. Banerjee, J. S. Rader, T. R. Broker, C. Meyers, L. T. Chow, and Z.-M. Zheng (2009)
RNA 15, 637-647
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Human papillomaviruses: a growing field.
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Genes & Dev. 23, 138-142
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Robust production and passaging of infectious HPV in squamous epithelium of primary human keratinocytes.
H.-K. Wang, A. A. Duffy, T. R. Broker, and L. T. Chow (2009)
Genes & Dev. 23, 181-194
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Control of the Papillomavirus Early-to-Late Switch by Differentially Expressed SRp20.
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Expression Pattern and Subcellular Localization of Human Papillomavirus Minor Capsid Protein L2.
Z. Lin, A. V. Yemelyanova, R. Gambhira, S. Jagu, C. Meyers, R. Kirnbauer, B. M. Ronnett, P. E. Gravitt, and R. B.S. Roden (2009)
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Ras Modifies Proliferation and Invasiveness of Cells Expressing Human Papillomavirus Oncoproteins.
S. Yoshida, N. Kajitani, A. Satsuka, H. Nakamura, and H. Sakai (2008)
J. Virol. 82, 8820-8827
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How Does Tobacco Smoke Contribute to Cervical Carcinogenesis?.
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J. Virol. 82, 6084-6086
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The Cigarette Smoke Carcinogen Benzo[a]pyrene Enhances Human Papillomavirus Synthesis.
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Human Papillomavirus Type 31 Uses a Caveolin 1- and Dynamin 2-Mediated Entry Pathway for Infection of Human Keratinocytes.
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J. Virol. 81, 9922-9931
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Conditionally activated e7 proteins of high-risk and low-risk human papillomaviruses induce s phase in postmitotic, differentiated human keratinocytes..
N. S. Banerjee, N. J. Genovese, F. Noya, W.-M. Chien, T. R. Broker, and L. T. Chow (2006)
J. Virol. 80, 6517-6524
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Condom use and the risk of genital human papillomavirus infection in young women..
R. L. Winer, J. P. Hughes, Q. Feng, S. O'Reilly, N. B. Kiviat, K. K. Holmes, and L. A. Koutsky (2006)
N. Engl. J. Med. 354, 2645-2654
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Adeno-Associated Virus Type 2 Increases Proteosome-Dependent Degradation of p21WAF1 in a Human Papillomavirus Type 31b-Positive Cervical Carcinoma Line..
S. Alam, E. Sen, H. Brashear, and C. Meyers (2006)
J. Virol. 80, 4927-4939
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Activation of Kaposi's Sarcoma-Associated Herpesvirus Lytic Gene Expression during Epithelial Differentiation.
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J. Virol. 79, 13769-13777
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T. Nakahara, W. L. Peh, J. Doorbar, D. Lee, and P. F. Lambert (2005)
J. Virol. 79, 13150-13165
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Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation.
D. Pyeon, P. F. Lambert, and P. Ahlquist (2005)
PNAS 102, 9311-9316
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Human Papillomavirus Type 31b Infection of Human Keratinocytes Does Not Require Heparan Sulfate.
N. A. Patterson, J. L. Smith, and M. A. Ozbun (2005)
J. Virol. 79, 6838-6847
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The Minor Capsid Protein L2 Contributes to Two Steps in the Human Papillomavirus Type 31 Life Cycle.
S. C. Holmgren, N. A. Patterson, M. A. Ozbun, and P. F. Lambert (2005)
J. Virol. 79, 3938-3948
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Genetic Analysis of the Human Papillomavirus Type 31 Differentiation-Dependent Late Promoter.
J. M. Bodily and C. Meyers (2005)
J. Virol. 79, 3309-3321
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Role of the PDZ Domain-Binding Motif of the Oncoprotein E6 in the Pathogenesis of Human Papillomavirus Type 31.
C. Lee and L. A. Laimins (2004)
J. Virol. 78, 12366-12377
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Global Effects of Human Papillomavirus Type 18 E6/E7 in an Organotypic Keratinocyte Culture System.
P. A. Garner-Hamrick, J. M. Fostel, W.-M. Chien, N. S. Banerjee, L. T. Chow, T. R. Broker, and C. Fisher (2004)
J. Virol. 78, 9041-9050
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Pathogenesis of Human Papillomaviruses in Differentiating Epithelia.
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Propagation of infectious human papillomavirus type 16 by using an adenovirus and Cre/LoxP mechanism.
J. H. Lee, S. M. P. Yi, M. E. Anderson, K. L. Berger, M. J. Welsh, A. J. Klingelhutz, and M. A. Ozbun (2004)
PNAS 101, 2094-2099
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Genetic and Biochemical Analysis of cis Regulatory Elements within the Keratinocyte Enhancer Region of the Human Papillomavirus Type 31 Upstream Regulatory Region during Different Stages of the Viral Life Cycle.
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J. Virol. 78, 612-629
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Different Heparan Sulfate Proteoglycans Serve as Cellular Receptors for Human Papillomaviruses.
S. Shafti-Keramat, A. Handisurya, E. Kriehuber, G. Meneguzzi, K. Slupetzky, and R. Kirnbauer (2003)
J. Virol. 77, 13125-13135
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Keratinocyte Growth Conditions Modulate Telomerase Expression, Senescence, and Immortalization by Human Papillomavirus Type 16 E6 and E7 Oncogenes.
B. Fu, J. Quintero, and C. C. Baker (2003)
Cancer Res. 63, 7815-7824
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Induction of the Upstream Regulatory Region of Human Papillomavirus Type 31 by Dexamethasone Is Differentiation Dependent.
J. L. Bromberg-White, E. Sen, S. Alam, J. M. Bodily, and C. Meyers (2003)
J. Virol. 77, 10975-10983
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Toxicogenomics in Drug Development.
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Toxicol Pathol 31, 471-479
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Interaction of L2 with beta -Actin Directs Intracellular Transport of Papillomavirus and Infection.
R. Yang, W. H. Yutzy IV, R. P. Viscidi, and R. B. S. Roden (2003)
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Human Papillomavirus and Cervical Cancer.
E. M. Burd (2003)
Clin. Microbiol. Rev. 16, 1-17
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Infectious human papillomavirus type 31b: purification and infection of an immortalized human keratinocyte cell line.
M. A. Ozbun (2002)
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Saccharomyces cerevisiae Is Permissive for Replication of Bovine Papillomavirus Type 1.
K.-N. Zhao and I. H. Frazer (2002)
J. Virol. 76, 12265-12273
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Human Papillomavirus Type 31b Infection of Human Keratinocytes and the Onset of Early Transcription.
M. A. Ozbun (2002)
J. Virol. 76, 11291-11300
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The Upstream Regulatory Region of Human Papillomavirus Type 31 Is Insensitive to Glucocorticoid Induction.
J. L. Bromberg-White and C. Meyers (2002)
J. Virol. 76, 9702-9715
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Long-Term Effect of Interferon on Keratinocytes That Maintain Human Papillomavirus Type 31.
Y. E. Chang, L. Pena, G. C. Sen, J. K. Park, and L. A. Laimins (2002)
J. Virol. 76, 8864-8874
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Infectious Virions Produced from a Human Papillomavirus Type 18/16 Genomic DNA Chimera.
C. Meyers, J. L. Bromberg-White, J. Zhang, M. E. Kaupas, J. T. Bryan, R. S. Lowe, and K. U. Jansen (2002)
J. Virol. 76, 4723-4733
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Genetic Analysis of cis Regulatory Elements within the 5' Region of the Human Papillomavirus Type 31 Upstream Regulatory Region during Different Stages of the Viral Life Cycle.
E. Sen, J. L. Bromberg-White, and C. Meyers (2002)
J. Virol. 76, 4798-4809
   Abstract »    Full Text »    PDF »
Differentiation-Dependent Chromatin Rearrangement Coincides with Activation of Human Papillomavirus Type 31 Late Gene Expression.
L. d. M. Pena and L. A. Laimins (2001)
J. Virol. 75, 10005-10013
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Displacement of YY1 by Differentiation-Specific Transcription Factor hSkn-1a Activates the P670 Promoter of Human Papillomavirus Type 16.
I. Kukimoto and T. Kanda (2001)
J. Virol. 75, 9302-9311
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Early Polyadenylation Signals of Human Papillomavirus Type 31 Negatively Regulate Capsid Gene Expression.
S. S. Terhune, W. G. Hubert, J. T. Thomas, and L. A. Laimins (2001)
J. Virol. 75, 8147-8157
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Cellular Changes Induced by Low-Risk Human Papillomavirus Type 11 in Keratinocytes That Stably Maintain Viral Episomes.
J. T. Thomas, S. T. Oh, S. S. Terhune, and L. A. Laimins (2001)
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Human Papillomavirus Infection Requires Cell Surface Heparan Sulfate.
T. Giroglou, L. Florin, F. Schäfer, R. E. Streeck, and M. Sapp (2001)
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F. Stubenrauch, M. Hummel, T. Iftner, and L. A. Laimins (2000)
J. Virol. 74, 1178-1186
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Regulation of Human Papillomavirus Type 31 Polyadenylation during the Differentiation-Dependent Life Cycle.
S. S. Terhune, C. Milcarek, and L. A. Laimins (1999)
J. Virol. 73, 7185-7192
   Abstract »    Full Text »
Human papillomavirus type 31 oncoproteins E6 and E7 are required for the maintenance of episomes during the viral life cycle in normal human keratinocytes.
J. T. Thomas, W. G. Hubert, M. N. Ruesch, and L. A. Laimins (1999)
PNAS 96, 8449-8454
   Abstract »    Full Text »    PDF »
CCAAT Displacement Protein Binds to and Negatively Regulates Human Papillomavirus Type 6 E6, E7, and E1 Promoters.
W. Ai, E. Toussaint, and A. Roman (1999)
J. Virol. 73, 4220-4229
   Abstract »    Full Text »
Two Novel Promoters in the Upstream Regulatory Region of Human Papillomavirus Type 31b Are Negatively Regulated by Epithelial Differentiation.
M. A. Ozbun and C. Meyers (1999)
J. Virol. 73, 3505-3510
   Abstract »    Full Text »
DNA Replication of Human Papillomavirus Type 31 Is Modulated by Elements of the Upstream Regulatory Region That Lie 5' of the Minimal Origin.
W. G. Hubert, T. Kanaya, and L. A. Laimins (1999)
J. Virol. 73, 1835-1845
   Abstract »    Full Text »
The L1 Major Capsid Protein of Human Papillomavirus Type 11 Recombinant Virus-like Particles Interacts with Heparin and Cell-surface Glycosaminoglycans on Human Keratinocytes.
J. G. Joyce, J.-S. Tung, C. T. Przysiecki, J. C. Cook, E. D. Lehman, J. A. Sands, K. U. Jansen, and P. M. Keller (1999)
J. Biol. Chem. 274, 5810-5822
   Abstract »    Full Text »    PDF »
A Novel YY1-Independent Silencer Represses the Activity of the Human Papillomavirus Type 16 Enhancer.
M. J. O'Connor, W. Stunkel, H. Zimmermann, C.-H. Koh, and H.-U. Bernard (1998)
J. Virol. 72, 10083-10092
   Abstract »    Full Text »    PDF »
Transactivation by the E2 Protein of Oncogenic Human Papillomavirus Type 31 Is Not Essential for Early and Late Viral Functions.
F. Stubenrauch, A. M. E. Colbert, and L. A. Laimins (1998)
J. Virol. 72, 8115-8123
   Abstract »    Full Text »    PDF »
Activation of Papillomavirus Late Gene Transcription and Genome Amplification upon Differentiation in Semisolid Medium Is Coincident with Expression of Involucrin and Transglutaminase but Not Keratin-10.
M. N. Ruesch, F. Stubenrauch, and L. A. Laimins (1998)
J. Virol. 72, 5016-5024
   Abstract »    Full Text »    PDF »
Isolation and Propagation of Human Papillomavirus Type 16 in Human Xenografts Implanted in the Severe Combined Immunodeficiency Mouse.
W. Bonnez, C. DaRin, C. Borkhuis, K. de Mesy Jensen, R. C. Reichman, and R. C. Rose (1998)
J. Virol. 72, 5256-5261
   Abstract »    Full Text »    PDF »
Temporal Usage of Multiple Promoters during the Life Cycle of Human Papillomavirus Type 31b.
M. A. Ozbun and C. Meyers (1998)
J. Virol. 72, 2715-2722
   Abstract »    Full Text »    PDF »
Association of the Human Papillomavirus Type 11 E1 Protein with Histone H1.
C. S. Swindle and J. A. Engler (1998)
J. Virol. 72, 1994-2001
   Abstract »    Full Text »    PDF »
Differential Requirements for Conserved E2 Binding Sites in the Life Cycle of Oncogenic Human Papillomavirus Type 31.
F. Stubenrauch, H. B. Lim, and L. A. Laimins (1998)
J. Virol. 72, 1071-1077
   Abstract »    Full Text »    PDF »
Human Papillomavirus Oncoproteins E6 and E7 Independently Abrogate the Mitotic Spindle Checkpoint.
J. T. Thomas and L. A. Laimins (1998)
J. Virol. 72, 1131-1137
   Abstract »    Full Text »    PDF »
The Papillomavirus Minor Capsid Protein, L2, Induces Localization of the Major Capsid Protein, L1, and the Viral Transcription/Replication Protein, E2, to PML Oncogenic Domains.
P. M. Day, R. B. S. Roden, D. R. Lowy, and J. T. Schiller (1998)
J. Virol. 72, 142-150
   Abstract »    Full Text »    PDF »
Characterization of Skn-1a/i POU Domain Factors and Linkage to Papillomavirus Gene Expression.
B. Andersen, A. Hariri, M. R. Pittelkow, and M. G. Rosenfeld (1997)
J. Biol. Chem. 272, 15905-15913
   Abstract »    Full Text »    PDF »
A cellular 65-kDa protein recognizes the negative regulatory element of human papillomavirus late mRNA.
W. Dietrich-Goetz, I. M. Kennedy, B. Levins, M. A. Stanley, and J. B. Clements (1997)
PNAS 94, 163-168
   Abstract »    Full Text »    PDF »
Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes..
S Cheng, D C Schmidt-Grimminger, T Murant, T R Broker, and L T Chow (1995)
Genes & Dev. 9, 2335-2349
   Abstract »    PDF »
Transcriptional Control and Cell Type Specificity of HPV Gene Expression.
H.-U. Bernard and D. Apt (1994)
Arch Dermatol 130, 210-215
   Abstract »    PDF »


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