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Science 27 February 1987:
Vol. 235. no. 4792, pp. 1056 - 1059
DOI: 10.1126/science.2434993
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Articles

Science, Vol 235, Issue 4792, 1056-1059
Copyright © 1987 by American Association for the Advancement of Science

articles

RNA complementary to a herpesvirus alpha gene mRNA is prominent in latently infected neurons

JG Stevens, EK Wagner, GB Devi-Rao, ML Cook, and LT Feldman

In initial attempts to define the molecular events responsible for the latent state of herpes simplex virus, in situ hybridization was utilized to search for virally encoded RNA transcripts in latently infected sensory neurons. The use of cloned probes representing the entire viral genome indicated that transcripts encoded within terminal repeats were present. When the alpha genes encoding ICP-0, ICP-4, and ICP-27 and the gamma 1 gene encoding VP-5 were employed, only RNA transcripts hybridizing to the ICP-0 probe were detected. In latently infected cells, the ICP-0--related transcripts were localized principally in the nucleus; this was not the case in acutely (productively) infected neurons or in neurons probed for RNA transcripts coding for actin. In Northern blotting experiments, an RNA of 2.6 kilobases was detected with the ICP-0 probe. When single-stranded DNAs from the ICP-0 region were used as probes, RNA from the strand complementary to that encoding ICP-0 messenger RNA (mRNA) was the major species detected. This RNA species may play a significant role in maintaining the latent infection.


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An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor.
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J. Virol. 81, 1872-1878
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Tissue-Specific Splicing of the Herpes Simplex Virus Type 1 Latency-Associated Transcript (LAT) Intron in LAT Transgenic Mice.
A. M. Gussow, N. V. Giordani, R. K. Tran, Y. Imai, D. L. Kwiatkowski, G. F. Rall, T. P. Margolis, and D. C. Bloom (2006)
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Herpes Simplex Virus Type 1 Latently Infected Neurons Differentially Express Latency-Associated and ICP0 Transcripts..
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J. Virol. 80, 9310-9321
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A. L. Amelio, N. V. Giordani, N. J. Kubat, J. E. O'Neil, and D. C. Bloom (2006)
J. Virol. 80, 2063-2068
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Qa-1b and CD94-NKG2a Interaction Regulate Cytolytic Activity of Herpes Simplex Virus-Specific Memory CD8+ T Cells in the Latently Infected Trigeminal Ganglia.
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J. Immunol. 176, 1703-1711
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Herpes Simplex Virus 1 Immediate-Early and Early Gene Expression during Reactivation from Latency under Conditions That Prevent Infectious Virus Production.
J. M. Pesola, J. Zhu, D. M. Knipe, and D. M. Coen (2005)
J. Virol. 79, 14516-14525
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K. Wang, T. Y. Lau, M. Morales, E. K. Mont, and S. E. Straus (2005)
J. Virol. 79, 14079-14087
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The Herpes Simplex Virus Type 1 Locus That Encodes the Latency-Associated Transcript Enhances the Frequency of Encephalitis in Male BALB/c Mice.
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J. Virol. 79, 12286-12295
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The Locus Encompassing the Latency-Associated Transcript of Herpes Simplex Virus Type 1 Interferes with and Delays Interferon Expression in Productively Infected Neuroblastoma Cells and Trigeminal Ganglia of Acutely Infected Mice.
W. Peng, G. Henderson, M. Inman, L. BenMohamed, G.-C. Perng, S. L. Wechsler, and C. Jones (2005)
J. Virol. 79, 6162-6171
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Construction of a Herpes Simplex Virus Type 1 Mutant with Only a Three-Nucleotide Change in the Branchpoint Region of the Latency-Associated Transcript (LAT) and the Stability of Its Two-Kilobase LAT Intron.
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J. Virol. 78, 12097-12106
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The Herpes Simplex Virus Type 1 Latency-Associated Transcript (LAT) Enhancer/rcr Is Hyperacetylated during Latency Independently of LAT Transcription.
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J. Virol. 78, 12508-12518
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The bovine herpesvirus-1 LR ORF2 is critical for this gene's ability to restore the high wild-type reactivation phenotype to a herpes simplex virus-1 LAT null mutant.
K. R. Mott, N. Osorio, L. Jin, D. J. Brick, J. Naito, J. Cooper, G. Henderson, M. Inman, C. Jones, S. L. Wechsler, et al. (2003)
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Capsaicin-induced reactivation of latent herpes simplex virus type 1 in sensory neurons in culture.
E. A. Hunsperger and C. L. Wilcox (2003)
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The Stable 2.0-Kilobase Intron of the Herpes Simplex Virus Type 1 Latency-Associated Transcript Does Not Function as an Antisense Repressor of ICP0 in Nonneuronal Cells.
E. A. Burton, C.-S. Hong, and J. C. Glorioso (2003)
J. Virol. 77, 3516-3530
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Herpes Simplex Virus Type 1 and Bovine Herpesvirus 1 Latency.
C. Jones (2003)
Clin. Microbiol. Rev. 16, 79-95
   Abstract »    Full Text »    PDF »
Herpes simplex virus type 1 mutants containing the KOS strain ICP34.5 gene in place of the McKrae ICP34.5 gene have McKrae-like spontaneous reactivation but non-McKrae-like virulence.
G.-C. Perng, K. R. Mott, N. Osorio, A. Yukht, S. Salina, Q.-H. Nguyen, A. B. Nesburn, and S. L. Wechsler (2002)
J. Gen. Virol. 83, 2933-2942
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Susceptibility of sensory neurons to apoptosis following infection by bovine herpesvirus type 1.
G. A. Delhon, M. J. Gonzalez, and P. R. Murcia (2002)
J. Gen. Virol. 83, 2257-2267
   Abstract »    Full Text »    PDF »
A Novel Herpes Simplex Virus Type 1 Transcript (AL-RNA) Antisense to the 5' End of the Latency-Associated Transcript Produces a Protein in Infected Rabbits.
G.-C. Perng, B. Maguen, L. Jin, K. R. Mott, J. Kurylo, L. BenMohamed, A. Yukht, N. Osorio, A. B. Nesburn, G. Henderson, et al. (2002)
J. Virol. 76, 8003-8010
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A Mutation in the Latency-Related Gene of Bovine Herpesvirus 1 Disrupts the Latency Reactivation Cycle in Calves.
M. Inman, L. Lovato, A. Doster, and C. Jones (2002)
J. Virol. 76, 6771-6779
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Herpes simplex virus type 1 infection prevents detachment of nerve growth factor-differentiated PC12 cells in culture.
M. J. Moxley, T. M. Block, H.-C. Liu, N. W. Fraser, G.-C. Perng, S. L. Wechsler, and Y.-H. Su (2002)
J. Gen. Virol. 83, 1591-1600
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Neither LAT nor Open Reading Frame P Mutations Increase Expression of Spliced or Intron-Containing ICP0 Transcripts in Mouse Ganglia Latently Infected with Herpes Simplex Virus.
S.-H. Chen, L. Y. Lee, D. A. Garber, P. A. Schaffer, D. M. Knipe, and D. M. Coen (2002)
J. Virol. 76, 4764-4772
   Abstract »    Full Text »    PDF »
A Protein Encoded by the Herpes Simplex Virus (HSV) Type 1 2-Kilobase Latency-Associated Transcript Is Phosphorylated, Localized to the Nucleus, and Overcomes the Repression of Expression from Exogenous Promoters When Inserted into the Quiescent HSV Genome.
S. K. Thomas, C. E. Lilley, D. S. Latchman, and R. S. Coffin (2002)
J. Virol. 76, 4056-4067
   Abstract »    Full Text »    PDF »
A Gene Capable of Blocking Apoptosis Can Substitute for the Herpes Simplex Virus Type 1 Latency-Associated Transcript Gene and Restore Wild-Type Reactivation Levels.
G.-C. Perng, B. Maguen, L. Jin, K. R. Mott, N. Osorio, S. M. Slanina, A. Yukht, H. Ghiasi, A. B. Nesburn, M. Inman, et al. (2002)
J. Virol. 76, 1224-1235
   Abstract »    Full Text »    PDF »
The 2-Kilobase Intron of the Herpes Simplex Virus Type 1 Latency-Associated Transcript Has a Half-Life of Approximately 24 Hours in SY5Y and COS-1 Cells.
D. L. Thomas, M. Lock, J. M. Zabolotny, B. R. Mohan, and N. W. Fraser (2002)
J. Virol. 76, 532-540
   Abstract »    Full Text »    PDF »
Regions of the Herpes Simplex Virus Type 1 Latency-Associated Transcript That Protect Cells from Apoptosis In Vitro and Protect Neuronal Cells In Vivo.
M. Ahmed, M. Lock, C. G. Miller, and N. W. Fraser (2002)
J. Virol. 76, 717-729
   Abstract »    Full Text »    PDF »
Herpes Simplex Virus Type 1 2-Kilobase Latency-Associated Transcript Intron Associates with Ribosomal Proteins and Splicing Factors.
M. Ahmed and N. W. Fraser (2001)
J. Virol. 75, 12070-12080
   Abstract »    Full Text »    PDF »
Book Review: Gene Therapy with Herpes Simplex Virus Vectors: Progress and Prospects for Clinical Neuroscience.
D. S. Latchman (2001)
Neuroscientist 7, 528-537
   Abstract »    PDF »
The Transgenic ICP4 Promoter Is Activated in Schwann Cells in Trigeminal Ganglia of Mice Latently Infected with Herpes Simplex Virus Type 1.
N. S. Taus and W. J. Mitchell (2001)
J. Virol. 75, 10401-10408
   Abstract »    Full Text »    PDF »
Three Herpes Simplex Virus Type 1 Latency-Associated Transcript Mutants with Distinct and Asymmetric Effects on Virulence in Mice Compared with Rabbits.
G.-C. Perng, D. Esmaili, S. M. Slanina, A. Yukht, H. Ghiasi, N. Osorio, K. R. Mott, B. Maguen, L. Jin, A. B. Nesburn, et al. (2001)
J. Virol. 75, 9018-9028
   Abstract »    Full Text »    PDF »
The 2.2-Kilobase Latency-Associated Transcript of Herpes Simplex Virus Type 2 Does Not Modulate Viral Replication, Reactivation, or Establishment of Latency in Transgenic Mice.
K. Wang, L. Pesnicak, E. Guancial, P. R. Krause, and S. E. Straus (2001)
J. Virol. 75, 8166-8172
   Abstract »    Full Text »    PDF »
Multiple Applications For Replication-Defective Herpes Simplex Virus Vectors.
E. A. Burton, J. B. Wechuck, S. K. Wendell, W. F. Goins, D. J. Fink, and J. C. Glorioso (2001)
Stem Cells 19, 358-377
   Abstract »    Full Text »    PDF »
Herpes Simplex Virus Type 1 Latency-Associated Transcript Gene Promotes Neuronal Survival.
R. L. Thompson and N. M. Sawtell (2001)
J. Virol. 75, 6660-6675
   Abstract »    Full Text »
ICP0, ICP4, or VP16 Expressed from Adenovirus Vectors Induces Reactivation of Latent Herpes Simplex Virus Type 1 in Primary Cultures of Latently Infected Trigeminal Ganglion Cells.
W. P. Halford, C. D. Kemp, J. A. Isler, D. J. Davido, and P. A. Schaffer (2001)
J. Virol. 75, 6143-6153
   Abstract »    Full Text »    PDF »
Cutting Edge: A NK Complex-Linked Locus Governs Acute Versus Latent Herpes Simplex Virus Infection of Neurons.
R. A. Pereira, A. Scalzo, and A. Simmons (2001)
J. Immunol. 166, 5869-5873
   Abstract »    Full Text »    PDF »
Multiple Immediate-Early Gene-Deficient Herpes Simplex Virus Vectors Allowing Efficient Gene Delivery to Neurons in Culture and Widespread Gene Delivery to the Central Nervous System In Vivo.
C. E. Lilley, F. Groutsi, Z. Han, J. A. Palmer, P. N. Anderson, D. S. Latchman, and R. S. Coffin (2001)
J. Virol. 75, 4343-4356
   Abstract »    Full Text »
Enhancer and Long-Term Expression Functions of Herpes Simplex Virus Type 1 Latency-Associated Promoter Are both Located in the Same Region.
H. Berthomme, J. Thomas, P. Texier, A. Epstein, and L. T. Feldman (2001)
J. Virol. 75, 4386-4393
   Abstract »    Full Text »
Region of Herpes Simplex Virus Type 1 Latency-Associated Transcript Sufficient for Wild-Type Spontaneous Reactivation Promotes Cell Survival in Tissue Culture.
M. Inman, G.-C. Perng, G. Henderson, H. Ghiasi, A. B. Nesburn, S. L. Wechsler, and C. Jones (2001)
J. Virol. 75, 3636-3646
   Abstract »    Full Text »
Herpes Simplex Virus Type 1 Promoter Activity during Latency Establishment, Maintenance, and Reactivation in Primary Dorsal Root Neurons In Vitro.
J. L. Arthur, C. G. Scarpini, V. Connor, R. H. Lachmann, A. M. Tolkovsky, and S. Efstathiou (2001)
J. Virol. 75, 3885-3895
   Abstract »    Full Text »
Analysis of Protein Expression from within the Region Encoding the 2.0-Kilobase Latency-Associated Transcript of Herpes Simplex Virus Type 1.
M. Lock, C. Miller, and N. W. Fraser (2001)
J. Virol. 75, 3413-3426
   Abstract »    Full Text »
Analysis of Individual Human Trigeminal Ganglia for Latent Herpes Simplex Virus Type 1 and Varicella-Zoster Virus Nucleic Acids Using Real-Time PCR.
R. J. Cohrs, J. Randall, J. Smith, D. H. Gilden, C. Dabrowski, H. van der Keyl, and R. Tal-Singer (2000)
J. Virol. 74, 11464-11471
   Abstract »    Full Text »
Gene Therapy for Cardiovascular Disease.
S. L. Meyerson, C. L. Skelly, M. A. Curi, and L. B. Schwartz (2000)
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   Abstract »    PDF »
Herpes Simplex Virus 1 Open Reading Frames O and P Are Not Necessary for Establishment of Latent Infection in Mice.
G. Randall, M. Lagunoff, and B. Roizman (2000)
J. Virol. 74, 9019-9027
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Identification of the Pseudorabies Virus Promoter Required for Latency-Associated Transcript Gene Expression in the Natural Host.
L. Jin, W. M. Schnitzlein, and G. Scherba (2000)
J. Virol. 74, 6333-6338
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Development and Optimization of Herpes Simplex Virus Vectors for Multiple Long-Term Gene Delivery to the Peripheral Nervous System.
J. A. Palmer, R. H. Branston, C. E. Lilley, M. J. Robinson, F. Groutsi, J. Smith, D. S. Latchman, and R. S. Coffin (2000)
J. Virol. 74, 5604-5618
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Evidence for a Bidirectional Element Located Downstream from the Herpes Simplex Virus Type 1 Latency-Associated Promoter That Increases Its Activity during Latency.
H. Berthomme, J. Lokensgard, L. Yang, T. Margolis, and L. T. Feldman (2000)
J. Virol. 74, 3613-3622
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Expression from the herpes simplex virus type 1 latency-associated promoter in the murine central nervous system.
C. Smith, R. H. Lachmann, and S. Efstathiou (2000)
J. Gen. Virol. 81, 649-662
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Virus-Induced Neuronal Apoptosis Blocked by the Herpes Simplex Virus Latency-Associated Transcript.
G. Perng, C. Jones, J. Ciacci-Zanella, M. Stone, G. Henderson, A. Yukht, S. M. Slanina, F. M. Hofman, H. Ghiasi, A. B. Nesburn, et al. (2000)
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The Latency-Associated Transcript Gene Enhances Establishment of Herpes Simplex Virus Type 1 Latency in Rabbits.
G.-C. Perng, S. M. Slanina, A. Yukht, H. Ghiasi, A. B. Nesburn, and S. L. Wechsler (2000)
J. Virol. 74, 1885-1891
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Repression of viral transcription during herpes simplex virus latency.
C. M. Preston (2000)
J. Gen. Virol. 81, 1-19
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Long-Term Transgene Expression in Mice Infected with a Herpes Simplex Virus Type 1 Mutant Severely Impaired for Immediate-Early Gene Expression.
K. R. Marshall, R. H. Lachmann, S. Efstathiou, A. Rinaldi, and C. M. Preston (2000)
J. Virol. 74, 956-964
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Replication of Herpes Simplex Virus Type 1 within Trigeminal Ganglia Is Required for High Frequency but Not High Viral Genome Copy Number Latency.
R. L. Thompson and N. M. Sawtell (2000)
J. Virol. 74, 965-974
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Quantitation of Latent Varicella-Zoster Virus and Herpes Simplex Virus Genomes in Human Trigeminal Ganglia.
S. R. Pevenstein, R. K. Williams, D. McChesney, E. K. Mont, J. E. Smialek, and S. E. Straus (1999)
J. Virol. 73, 10514-10518
   Abstract »    Full Text »
Behavioural changes in the rat following infection with varicella-zoster virus.
S. M. Fleetwood-Walker, J. P. Quinn, C. Wallace, G. Blackburn-Munro, B. G. Kelly, C. E. Fiskerstrand, A. A. Nash, and R. G. Dalziel (1999)
J. Gen. Virol. 80, 2433-2436
   Abstract »    Full Text »
Herpes Simplex Virus Latency-Associated Transcript Encodes a Protein Which Greatly Enhances Virus Growth, Can Compensate for Deficiencies in Immediate-Early Gene Expression, and Is Likely To Function during Reactivation from Virus Latency.
S. K. Thomas, G. Gough, D. S. Latchman, R. S. , and Coffin (1999)
J. Virol. 73, 6618-6625
   Abstract »    Full Text »
Herpes simplex virus type 1 infection has two separate modes of spread in three-dimensional keratinocyte culture.
V. Hukkanen, H. Mikola, M. Nykänen, and S. Syrjänen (1999)
J. Gen. Virol. 80, 2149-2155
   Abstract »    Full Text »
Human Corneal Cells and Other Fibroblasts Can Stimulate the Appearance of Herpes Simplex Virus from Quiescently Infected PC12 Cells.
Y.-H. Su, R. L. Meegalla, R. Chowhan, C. Cubitt, J. E. Oakes, R. N. Lausch, N. W. Fraser, and T. M. Block (1999)
J. Virol. 73, 4171-4180
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Identical 371-Base-Pair Deletion Mutations in the LAT Genes of Herpes Simplex Virus Type 1 McKrae and 17syn+ Result in Different In Vivo Reactivation Phenotypes.
J. M. Loutsch, G.-C. Perng, J. M. Hill, X. Zheng, M. E. Marquart, T. M. Block, H. Ghiasi, A. B. Nesburn, and S. L. Wechsler (1999)
J. Virol. 73, 767-771
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The Polyserine Tract of Herpes Simplex Virus ICP4 Is Required for Normal Viral Gene Expression and Growth in Murine Trigeminal Ganglia.
P. A. Bates and N. A. DeLuca (1998)
J. Virol. 72, 7115-7124
   Abstract »    Full Text »    PDF »
UL27.5 Is a Novel gamma 2 Gene Antisense to the Herpes Simplex Virus 1 Gene Encoding Glycoprotein B.
Y. E. Chang, L. Menotti, F. Filatov, G. Campadelli-Fiume, and B. Roizman (1998)
J. Virol. 72, 6056-6064
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T Lymphocytes Are Required for Protection of the Vaginal Mucosae and Sensory Ganglia of Immune Mice Against Reinfection with Herpes Simplex Virus Type 2.
G. N. Milligan, D. I. Bernstein, and N. Bourne (1998)
J. Immunol. 160, 6093-6100
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Herpes Simplex Virus Type 1 Latency-Associated Transcripts Suppress Viral Replication and Reduce Immediate-Early Gene mRNA Levels in a Neuronal Cell Line.
N. Mador, D. Goldenberg, O. Cohen, A. Panet, and I. Steiner (1998)
J. Virol. 72, 5067-5075
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The TAATGARAT Motif in the Herpes Simplex Virus Immediate-Early Gene Promoters Can Confer both Positive and Negative Responses to Cellular Octamer-Binding Proteins When It Is Located within the Viral Genome.
S. Thomas, R. S. Coffin, P. Watts, G. Gough, and D. S. Latchman (1998)
J. Virol. 72, 3495-3500
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A 2.9-Kilobase Noncoding Nuclear RNA Functions in the Establishment of Persistent Hz-1 Viral Infection.
Y.-C. Chao, S.-T. Lee, M.-C. Chang, H.-H. Chen, S.-S. Chen, T.-Y. Wu, F.-H. Liu, E.-L. Hsu, and R. F. Hou (1998)
J. Virol. 72, 2233-2245
   Abstract »    Full Text »    PDF »
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