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Science 15 March 1996:
Vol. 271. no. 5255, pp. 1579 - 1582
DOI: 10.1126/science.271.5255.1579
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Reports

Human Foamy Virus Replication: A Pathway Distinct from That of Retroviruses and Hepadnaviruses

Shuyuarn F. Yu, David N. Baldwin, Samuel R. Gwynn, Suneetha Yendapalli, Maxine L. Linial *

Human foamy virus (HFV) is the prototype of the Spumavirus genus of Retroviridae. In all other retroviruses, the pol gene products, including reverse transcriptase, are synthesized as Gag-Pol fusion proteins and are cleaved to functional enzymes during viral budding or release. In contrast, the Pol protein of HFV is translated from a spliced messenger RNA and lacks Gag domains. Infectious HFV particles contain double-stranded DNA similar in size to full-length provirus, suggesting that reverse transcription has taken place in viral particles before new rounds of infection, reminiscent of hepadnaviruses. These data suggest that foamy viruses possess a replication pathway containing features of both retroviruses and hepadnaviruses but distinct from both.

S. F. Yu and S. Yendapalli, Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98104, USA.
D. N. Baldwin and M. L. Linial, Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98104, and Department of Microbiology, University of Washington, Seattle, WA 98195, USA.
S. R. Gwynn, Interdisciplinary Program in Molecular and Cellular Biology, and Department of Microbiology, University of Washington, Seattle, WA 98195, USA.
* To whom correspondence should be addressed at the Fred Hutchinson Cancer Research Center.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
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Foamy virus-mediated gene transfer to canine repopulating cells.
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The Duck Hepatitis B Virus Reverse Transcriptase Functions as a Full-length Monomer.
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Foamy virus vector integration sites in normal human cells.
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Expanded Tissue Targets for Foamy Virus Replication with Simian Immunodeficiency Virus-Induced Immunosuppression.
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J. Virol. 80, 663-670
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Protease-Dependent Uncoating of a Complex Retrovirus.
J. Lehmann-Che, M.-L. Giron, O. Delelis, M. Lochelt, P. Bittoun, J. Tobaly-Tapiero, H. de The, and A. Saib (2005)
J. Virol. 79, 9244-9253
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RNA and Protein Requirements for Incorporation of the Pol Protein into Foamy Virus Particles.
K. Peters, T. Wiktorowicz, M. Heinkelein, and A. Rethwilm (2005)
J. Virol. 79, 7005-7013
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Identification of Domains in Gag Important for Prototypic Foamy Virus Egress.
G. S. Patton, S. A. Morris, W. Chung, P. D. Bieniasz, and M. O. McClure (2005)
J. Virol. 79, 6392-6399
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Role of the C Terminus of Foamy Virus Gag in RNA Packaging and Pol Expression.
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J. Virol. 78, 9423-9430
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Characterization of the Polymerase and RNase H Activities of Human Foamy Virus Reverse Transcriptase.
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J. Virol. 78, 6112-6121
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Cell Cycle Requirements for Transduction by Foamy Virus Vectors Compared to Those of Oncovirus and Lentivirus Vectors.
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J. Virol. 78, 2327-2335
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Feline Foamy Virus Genome and Replication Strategy.
J. Roy, W. Rudolph, T. Juretzek, K. Gartner, M. Bock, O. Herchenroder, D. Lindemann, M. Heinkelein, and A. Rethwilm (2003)
J. Virol. 77, 11324-11331
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Application of Chimeric Feline Foamy Virus-Based Retroviral Vectors for the Induction of Antiviral Immunity in Cats.
A. Schwantes, U. Truyen, J. Weikel, C. Weiss, and M. Lochelt (2003)
J. Virol. 77, 7830-7842
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Biphasic DNA Synthesis in Spumaviruses.
O. Delelis, A. Saib, and P. Sonigo (2003)
J. Virol. 77, 8141-8146
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Do lipid rafts mediate virus assembly and pseudotyping?.
J. A. G. Briggs, T. Wilk, and S. D. Fuller (2003)
J. Gen. Virol. 84, 757-768
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Bel1-mediated Transactivation of the Spumaretroviral Internal Promoter Is Repressed by Nuclear Factor I.
K. Kido, H. Bannert, R. M. Gronostajski, and R. M. Flugel (2003)
J. Biol. Chem. 278, 11836-11842
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Foamy Virus Envelope Glycoprotein Is Sufficient for Particle Budding and Release.
K. L. Shaw, D. Lindemann, M. J. Mulligan, and P. A. Goepfert (2003)
J. Virol. 77, 2338-2348
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Pregenomic RNA Is Required for Efficient Incorporation of Pol Polyprotein into Foamy Virus Capsids.
M. Heinkelein, C. Leurs, M. Rammling, K. Peters, H. Hanenberg, and A. Rethwilm (2002)
J. Virol. 76, 10069-10073
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Mutation of the Catalytic Domain of the Foamy Virus Reverse Transcriptase Leads to Loss of Processivity and Infectivity.
C. S. Rinke, P. L. Boyer, M. D. Sullivan, S. H. Hughes, and M. L. Linial (2002)
J. Virol. 76, 7560-7570
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Further Characterization of Equine Foamy Virus Reveals Unusual Features among the Foamy Viruses.
C.-H. Lecellier, M. Neves, M.-L. Giron, J. Tobaly-Tapiero, and A. Saib (2002)
J. Virol. 76, 7220-7227
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Transduction of human NOD/SCID-repopulating cells with both lymphoid and myeloid potential by foamy virus vectors.
N. C. Josephson, G. Vassilopoulos, G. D. Trobridge, G. V. Priestley, B. L. Wood, T. Papayannopoulou, and D. W. Russell (2002)
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Identification and Functional Characterization of an Intragenic DNA Binding Site for the Spumaretroviral trans-Activator in the Human p57Kip2 Gene.
K. Kido, A. Doerks, M. Lochelt, and R. M. Flugel (2002)
J. Biol. Chem. 277, 12032-12039
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Improved Primate Foamy Virus Vectors and Packaging Constructs.
M. Heinkelein, M. Dressler, G. Jarmy, M. Rammling, H. Imrich, J. Thurow, D. Lindemann, and A. Rethwilm (2002)
J. Virol. 76, 3774-3783
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Isolation and sequencing of infectious clones of feline foamy virus and a human/feline foamy virus Env chimera.
S. Hatama, K. Otake, S. Omoto, Y. Murase, A. Ikemoto, M. Mochizuki, E. Takahashi, H. Okuyama, and Y. Fujii (2001)
J. Gen. Virol. 82, 2999-3004
   Abstract »    Full Text »    PDF »
Specific Interaction of a Novel Foamy Virus Env Leader Protein with the N-Terminal Gag Domain.
T. Wilk, V. Geiselhart, M. Frech, S. D. Fuller, R. M. Flugel, and M. Lochelt (2001)
J. Virol. 75, 7995-8007
   Abstract »    Full Text »    PDF »
The R Region Found in the Human Foamy Virus Long Terminal Repeat Is Critical for both Gag and Pol Protein Expression.
R. A. Russell, Y. Zeng, O. Erlwein, B. R. Cullen, and M. O. McClure (2001)
J. Virol. 75, 6817-6824
   Abstract »    Full Text »
Identification of a Conserved Residue of Foamy Virus Gag Required for Intracellular Capsid Assembly.
S. W. Eastman and M. L. Linial (2001)
J. Virol. 75, 6857-6864
   Abstract »    Full Text »
Gene transfer into murine hematopoietic stem cells with helper-free foamy virus vectors.
G. Vassilopoulos, G. Trobridge, N. C. Josephson, and D. W. Russell (2001)
Blood 98, 604-609
   Abstract »    Full Text »    PDF »
Human Foamy Virus Capsid Formation Requires an Interaction Domain in the N Terminus of Gag.
J. Tobaly-Tapiero, P. Bittoun, M.-L. Giron, M. Neves, M. Koken, A. Saïb, and H. de Thé (2001)
J. Virol. 75, 4367-4375
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Palindromic Sequence Plays a Critical Role in Human Foamy Virus Dimerization.
D. Cain, O. Erlwein, A. Grigg, R. A. Russell, and M. O. McClure (2001)
J. Virol. 75, 3731-3739
   Abstract »    Full Text »
Primate foamy virus Pol proteins are imported into the nucleus.
H. Imrich, M. Heinkelein, O. Herchenröder, and A. Rethwilm (2000)
J. Gen. Virol. 81, 2941-2947
   Abstract »    Full Text »
Design of Retroviral Vectors and Helper Cells for Gene Therapy.
W.-S. Hu and V. K. Pathak (2000)
Pharmacol. Rev. 52, 493-512
   Abstract »    Full Text »    PDF »
Isolation and Characterization of an Equine Foamy Virus.
J. Tobaly-Tapiero, P. Bittoun, M. Neves, M.-C. Guillemin, C.-H. Lecellier, F. Puvion-Dutilleul, B. Gicquel, S. Zientara, M.-L. Giron, H. de Thé, et al. (2000)
J. Virol. 74, 4064-4073
   Abstract »    Full Text »
Complex Effects of Deletions in the 5' Untranslated Region of Primate Foamy Virus on Viral Gene Expression and RNA Packaging.
M. Heinkelein, J. Thurow, M. Dressler, H. Imrich, D. Neumann-Haefelin, M. O. McClure, and A. Rethwilm (2000)
J. Virol. 74, 3141-3148
   Abstract »    Full Text »
Multiple Integrations of Human Foamy Virus in Persistently Infected Human Erythroleukemia Cells.
C. D. Meiering, K. E. Comstock, and M. L. Linial (2000)
J. Virol. 74, 1718-1726
   Abstract »    Full Text »
Genetic Stability of Foamy Viruses: Long-Term Study in an African Green Monkey Population.
M. Schweizer, H. Schleer, M. Pietrek, J. Liegibel, V. Falcone, and D. Neumann-Haefelin (1999)
J. Virol. 73, 9256-9265
   Abstract »    Full Text »    PDF »
An Endoplasmic Reticulum Retrieval Signal Partitions Human Foamy Virus Maturation to Intracytoplasmic Membranes.
P. A. Goepfert, K. Shaw, G. Wang, A. Bansal, B. H. Edwards, and M. J. Mulligan (1999)
J. Virol. 73, 7210-7217
   Abstract »    Full Text »
Molecular Characterization of Proteolytic Processing of the Gag Proteins of Human Spumavirus.
K.-I. Pfrepper, M. Löchelt, H.-R. Rackwitz, M. Schnölzer, H. Heid, and R. M. Flügel (1999)
J. Virol. 73, 7907-7911
   Abstract »    Full Text »
Proteolytic Activity, the Carboxy Terminus of Gag, and the Primer Binding Site Are Not Required for Pol Incorporation into Foamy Virus Particles.
D. N. Baldwin and M. L. Linial (1999)
J. Virol. 73, 6387-6393
   Abstract »    Full Text »
Properties of human foamy virus relevant to its development as a vector for gene therapy.
C. L. Hill, P. D. Bieniasz, and M. O. McClure (1999)
J. Gen. Virol. 80, 2003-2009
   Abstract »    Full Text »
Replication of a foamy virus mutant with a constitutively active U3 promoter and deleted accessory genes.
T Schenk, J Enssle, N Fischer, and A Rethwilm (1999)
J. Gen. Virol. 80, 1591-1598
   Abstract »
An active foamy virus integrase is required for virus replication.
J Enssle, A Moebes, M Heinkelein, M Panhuysen, B Mauer, M Schweizer, D Neumann-Haefelin, and A Rethwilm (1999)
J. Gen. Virol. 80, 1445-1452
   Abstract »
Foamy Viruses Are Unconventional Retroviruses.
M. L. Linial (1999)
J. Virol. 73, 1747-1755
   Full Text »
Evidence that the Human Foamy Virus Genome Is DNA.
S. F. Yu, M. D. Sullivan, and M. L. Linial (1999)
J. Virol. 73, 1565-1572
   Abstract »    Full Text »
Gamma Interferon Is a Major Suppressive Factor Produced by Activated Human Peripheral Blood Lymphocytes That Is Able To Inhibit Foamy Virus-Induced Cytopathic Effects.
V. Falcone, M. Schweizer, A. Toniolo, D. Neumann-Haefelin, and A. Meyerhans (1999)
J. Virol. 73, 1724-1728
   Abstract »    Full Text »
Comparative sequence analysis and predictions for the envelope glycoproteins of foamy viruses.
G Wang and M. Mulligan (1999)
J. Gen. Virol. 80, 245-254
   Abstract »
Molecular Characterization of Proteolytic Processing of the Pol Proteins of Human Foamy Virus Reveals Novel Features of the Viral Protease.
K.-I. Pfrepper, H.-R. Rackwitz, M. Schnolzer, H. Heid, M. Lochelt, and R. M. Flugel (1998)
J. Virol. 72, 7648-7652
   Abstract »    Full Text »    PDF »
Characterization of a cis-Acting Sequence in the pol Region Required To Transfer Human Foamy Virus Vectors.
M. Heinkelein, M. Schmidt, N. Fischer, A. Moebes, D. Lindemann, J. Enssle, and A. Rethwilm (1998)
J. Virol. 72, 6307-6314
   Abstract »    Full Text »    PDF »
Sequences in pol Are Required for Transfer of Human Foamy Virus-Based Vectors.
O. Erlwein, P. D. Bieniasz, and M. O. McClure (1998)
J. Virol. 72, 5510-5516
   Abstract »    Full Text »    PDF »
An Evolutionarily Conserved Splice Generates a Secreted Env-Bet Fusion Protein during Human Foamy Virus Infection.
M.-L. Giron, H. de The, and A. Saib (1998)
J. Virol. 72, 4906-4910
   Abstract »    Full Text »    PDF »
The Roles of Pol and Env in the Assembly Pathway of Human Foamy Virus.
D. N. Baldwin and M. L. Linial (1998)
J. Virol. 72, 3658-3665
   Abstract »    Full Text »    PDF »
Characterization of a Human Foamy Virus 170-Kilodalton Env-Bet Fusion Protein Generated by Alternative Splicing.
D. Lindemann and A. Rethwilm (1998)
J. Virol. 72, 4088-4094
   Abstract »    Full Text »    PDF »
Mutations of the Human Immunodeficiency Virus Type 1 p6Gag Domain Result in Reduced Retention of Pol Proteins during Virus Assembly.
X.-F. Yu, L. Dawson, C.-J. Tian, C. Flexner, and M. Dettenhofer (1998)
J. Virol. 72, 3412-3417
   Abstract »    Full Text »    PDF »
cis-Acting Sequences Required for Simian Foamy Virus Type 1 Vectors.
M. Wu, S. Chari, T. Yanchis, and A. Mergia (1998)
J. Virol. 72, 3451-3454
   Abstract »    Full Text »    PDF »
The Nucleotide Sequence and Spliced pol mRNA Levels of the Nonprimate Spumavirus Bovine Foamy Virus.
D. L. Holzschu, M. A. Delaney, R. W. Renshaw, and J. W. Casey (1998)
J. Virol. 72, 2177-2182
   Abstract »    Full Text »    PDF »
Foamy Virus Particle Formation.
N. Fischer, M. Heinkelein, D. Lindemann, J. Enssle, C. Baum, E. Werder, H. Zentgraf, J. G. Muller, and A. Rethwilm (1998)
J. Virol. 72, 1610-1615
   Abstract »    Full Text »    PDF »
Evidence for Copurification of HERV-K-Related Transcripts and a Reverse Transcriptase Activity in Human Platelets From Patients With Essential Thrombocythemia.
M. T. Boyd, B. Foley, and I. Brodsky (1997)
Blood 90, 4022-4030
   Abstract »    Full Text »    PDF »


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