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Science 1 June 1990:
Vol. 248. no. 4959, pp. 1109 - 1112
DOI: 10.1126/science.2160735

Articles

Science, Vol 248, Issue 4959, 1109-1112
Copyright © 1990 by American Association for the Advancement of Science


articles

Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus

H Kestler, T Kodama, D Ringler, M Marthas, N Pedersen, A Lackner, D Regier, P Sehgal, M Daniel, N King, and al. et

New England Regional Primate Research Center, Harvard Medical School, Southborough, MA 01772.

Better understanding of the pathogenesis of acquired immunodeficiency syndrome (AIDS) would be greatly facilitated by a relevant animal model that uses molecularly cloned virus of defined sequence to induce the disease. Such a system would also be of great value for AIDS vaccine research. An infectious molecular clone of simian immunodeficiency virus (SIV) was identified that induces AIDS in common rhesus monkeys in a time frame suitable for laboratory investigation. These results provide another strong link in the chain of evidence for the viral etiology of AIDS. More importantly, they define a system for molecular dissection of the determinants of AIDS pathogenesis.


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E. Yung, M. Sorin, E.-J. Wang, S. Perumal, D. Ott, and G. V. Kalpana (2004)
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P. Blancou, N. Chenciner, R. H. T. Fang, V. Monceaux, M.-C. Cumont, D. Guetard, B. Hurtrel, and S. Wain-Hobson (2004)
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Multispecific Vaccine-Induced Mucosal Cytotoxic T Lymphocytes Reduce Acute-Phase Viral Replication but Fail in Long-Term Control of Simian Immunodeficiency Virus SIVmac239.
T. U. Vogel, M. R. Reynolds, D. H. Fuller, K. Vielhuber, T. Shipley, J. T. Fuller, K. J. Kunstman, G. Sutter, M. L. Marthas, V. Erfle, et al. (2003)
J. Virol. 77, 13348-13360
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Simian-Human Immunodeficiency Virus Escape from Cytotoxic T-Lymphocyte Recognition at a Structurally Constrained Epitope.
F. W. Peyerl, D. H. Barouch, W. W. Yeh, H. S. Bazick, J. Kunstman, K. J. Kunstman, S. M. Wolinsky, and N. L. Letvin (2003)
J. Virol. 77, 12572-12578
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The emergence and characterization of macrophage-tropic SIV/HIV chimeric viruses (SHIVs) present in CD4+ T cell-depleted rhesus monkeys.
T. Igarashi, H. Imamichi, C. R. Brown, V. M. Hirsch, and M. A. Martin (2003)
J. Leukoc. Biol. 74, 772-780
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Early Control of Highly Pathogenic Simian Immunodeficiency Virus/Human Immunodeficiency Virus Chimeric Virus Infections in Rhesus Monkeys Usually Results in Long-Lasting Asymptomatic Clinical Outcomes.
T. Igarashi, Y. Endo, Y. Nishimura, C. Buckler, R. Sadjadpour, O. K. Donau, M.-J. Dumaurier, R. J. Plishka, A. Buckler-White, and M. A. Martin (2003)
J. Virol. 77, 10829-10840
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Down-Modulation of Mature Major Histocompatibility Complex Class II and Up-Regulation of Invariant Chain Cell Surface Expression Are Well-Conserved Functions of Human and Simian Immunodeficiency Virus nef Alleles.
M. Schindler, S. Wurfl, P. Benaroch, T. C. Greenough, R. Daniels, P. Easterbrook, M. Brenner, J. Munch, and F. Kirchhoff (2003)
J. Virol. 77, 10548-10556
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DNA vaccination of macaques by a full-genome simian/human immunodeficiency virus type 1 plasmid chimera that produces non-infectious virus particles.
W. Akahata, E. Ido, H. Akiyama, H. Uesaka, Y. Enose, R. Horiuchi, T. Kuwata, T. Goto, H. Takahashi, and M. Hayami (2003)
J. Gen. Virol. 84, 2237-2244
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Hydrogen Bonding at a Conserved Threonine in Lentivirus Capsid Is Required for Virus Replication.
S. M. Rue, J. W. Roos, L. M. Amzel, J. E. Clements, and S. A. Barber (2003)
J. Virol. 77, 8009-8018
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Determinants of Increased Replicative Capacity of Serially Passaged Simian Immunodeficiency Virus with nef Deleted in Rhesus Monkeys.
L. Alexander, P. O. Illyinskii, S. M. Lang, R. E. Means, J. Lifson, K. Mansfield, and R. C. Desrosiers (2003)
J. Virol. 77, 6823-6835
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Expression of Simian Immunodeficiency Virus (SIV) Nef in Astrocytes during Acute and Terminal Infection and Requirement of Nef for Optimal Replication of Neurovirulent SIV In Vitro.
E. D. Overholser, G. D. Coleman, J. L. Bennett, R. J. Casaday, M. C. Zink, S. A. Barber, and J. E. Clements (2003)
J. Virol. 77, 6855-6866
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Mutational analysis of two zinc-finger motifs in the nucleocapsid protein of simian immunodeficiency virus mac239.
W. Akahata, E. Ido, and M. Hayami (2003)
J. Gen. Virol. 84, 1641-1648
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Unique Pattern of Convergent Envelope Evolution in Simian Immunodeficiency Virus-Infected Rapid Progressor Macaques: Association with CD4-Independent Usage of CCR5.
H. Dehghani, B. A. Puffer, R. W. Doms, and V. M. Hirsch (2003)
J. Virol. 77, 6405-6418
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In Situ Hybridization AT-Tailing with Catalyzed Signal Amplification for Sensitive and Specific in Situ Detection of Human Immunodeficiency Virus-1 mRNA in Formalin-Fixed and Paraffin-Embedded Tissues.
N. Nakajima, P. Ionescu, Y. Sato, M. Hashimoto, T. Kuroita, H. Takahashi, H. Yoshikura, and T. Sata (2003)
Am. J. Pathol. 162, 381-389
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Control of Viremia and Prevention of Simian-Human Immunodeficiency Virus-Induced Disease in Rhesus Macaques Immunized with Recombinant Vaccinia Viruses plus Inactivated Simian Immunodeficiency Virus and Human Immunodeficiency Virus Type 1 Particles.
R. L. Willey, R. Byrum, M. Piatak, Y. B. Kim, M. W. Cho, J. L. Rossio Jr., J. Bess Jr., T. Igarashi, Y. Endo, L. O. Arthur, et al. (2003)
J. Virol. 77, 1163-1174
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Importance of B-Cell Responses for Immunological Control of Variant Strains of Simian Immunodeficiency Virus.
W. E. Johnson, J. D. Lifson, S. M. Lang, R. P. Johnson, and R. C. Desrosiers (2003)
J. Virol. 77, 375-381
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Effects of Cytotoxic T Lymphocytes (CTL) Directed against a Single Simian Immunodeficiency Virus (SIV) Gag CTL Epitope on the Course of SIVmac239 Infection.
T. M. Allen, P. Jing, B. Calore, H. Horton, D. H. O'Connor, T. Hanke, M. Piekarczyk, R. Ruddersdorf, B. R. Mothe, C. Emerson, et al. (2002)
J. Virol. 76, 10507-10511
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Primary replication of a recombinant Sendai virus vector in macaques.
M. Kano, T. Matano, A. Kato, H. Nakamura, A. Takeda, Y. Suzaki, Y. Ami, K. Terao, and Y. Nagai (2002)
J. Gen. Virol. 83, 1377-1386
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CD4 Independence of Simian Immunodeficiency Virus Envs Is Associated with Macrophage Tropism, Neutralization Sensitivity, and Attenuated Pathogenicity.
B. A. Puffer, S. Pohlmann, A. L. Edinger, D. Carlin, M. D. Sanchez, J. Reitter, D. D. Watry, H. S. Fox, R. C. Desrosiers, and R. W. Doms (2002)
J. Virol. 76, 2595-2605
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T. Igarashi, C. R. Brown, R. A. Byrum, Y. Nishimura, Y. Endo, R. J. Plishka, C. Buckler, A. Buckler-White, G. Miller, V. M. Hirsch, et al. (2002)
J. Virol. 76, 379-391
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L. Holterman, R. Dubbes, J. Mullins, G. Learn, H. Niphuis, W. Koornstra, G. Koopman, E.-M. Kuhn, A. Wade-Evans, B. Rosenwirth, et al. (2001)
J. Virol. 75, 9328-9338
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Simian Immunodeficiency Virus in Which nef and U3 Sequences Do Not Overlap Replicates Efficiently In Vitro and In Vivo in Rhesus Macaques.
J. Munch, N. Adam, N. Finze, N. Stolte, C. Stahl-Hennig, D. Fuchs, P. Ten Haaft, J. L. Heeney, and F. Kirchhoff (2001)
J. Virol. 75, 8137-8146
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Protection against Simian Immunodeficiency Virus Vaginal Challenge by Using Sabin Poliovirus Vectors.
S. Crotty, C. J. Miller, B. L. Lohman, M. R. Neagu, L. Compton, D. Lu, F. X.-S. Lu, L. Fritts, J. D. Lifson, and R. Andino (2001)
J. Virol. 75, 7435-7452
   Abstract »    Full Text »    PDF »
Induction of Disseminated Mycobacterium avium in Simian AIDS Is Dependent upon Simian Immunodeficiency Virus Strain and Defective Granuloma Formation.
K. G. Mansfield, R. S. Veazey, A. Hancock, A. Carville, M. Elliott, K.-C. Lin, and A. A. Lackner (2001)
Am. J. Pathol. 159, 693-702
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Primate and Feline Lentivirus Vector RNA Packaging and Propagation by Heterologous Lentivirus Virions.
M. T. Browning, R. D. Schmidt, K. A. Lew, and T. A. Rizvi (2001)
J. Virol. 75, 5129-5140
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Construction and In Vitro Properties of a Series of Attenuated Simian Immunodeficiency Viruses with All Accessory Genes Deleted.
Y. Guan, J. B. Whitney, M. Detorio, and M. A. Wainberg (2001)
J. Virol. 75, 4056-4067
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Ability of the V3 Loop of Simian Immunodeficiency Virus To Serve as a Target for Antibody-Mediated Neutralization: Correlation of Neutralization Sensitivity, Growth in Macrophages, and Decreased Dependence on CD4.
R. E. Means, T. Matthews, J. A. Hoxie, M. H. Malim, T. Kodama, and R. C. Desrosiers (2001)
J. Virol. 75, 3903-3915
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Suboptimal Nucleotides in the Infectious, Pathogenic Simian Immunodeficiency Virus Clone SIVmac239.
L. Alexander, L. Denekamp, S. Czajak, and R. C. Desrosiers (2001)
J. Virol. 75, 4019-4022
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Novel, Live Attenuated Simian Immunodeficiency Virus Constructs Containing Major Deletions in Leader RNA Sequences.
Y. Guan, J. B. Whitney, C. Liang, and M. A. Wainberg (2001)
J. Virol. 75, 2776-2785
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Activation of NFAT-Dependent Gene Expression by Nef: Conservation among Divergent Nef Alleles, Dependence on SH3 Binding and Membrane Association, and Cooperation with Protein Kinase C-{theta}.
A. Manninen, P. Huotari, M. Hiipakka, G. H. Renkema, and K. Saksela (2001)
J. Virol. 75, 3034-3037
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Identification of Enteropathogenic Escherichia coli in Simian Immunodeficiency Virus-Infected Infant and Adult Rhesus Macaques.
K. G. Mansfield, K.-C. Lin, J. Newman, D. Schauer, J. MacKey, A. A. Lackner, and A. Carville (2001)
J. Clin. Microbiol. 39, 971-976
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In Vivo Attenuation of Simian Immunodeficiency Virus by Disruption of a Tyrosine-Dependent Sorting Signal in the Envelope Glycoprotein Cytoplasmic Tail.
P. N. Fultz, P. J. Vance, M. J. Endres, B. Tao, J. D. Dvorin, I. C. Davis, J. D. Lifson, D. C. Montefiori, M. Marsh, M. H. Malim, et al. (2001)
J. Virol. 75, 278-291
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The Level of CD4 Expression Limits Infection of Primary Rhesus Monkey Macrophages by a T-Tropic Simian Immunodeficiency Virus and Macrophagetropic Human Immunodeficiency Viruses.
N. Bannert, D. Schenten, S. Craig, and J. Sodroski (2000)
J. Virol. 74, 10984-10993
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Naturally Occurring V1-env Region Variants Mediate Simian Immunodeficiency Virus SIVmac Escape from High-Titer Neutralizing Antibodies Induced by a Protective Subunit Vaccine.
H. Petry, K. Pekrun, G. Hunsmann, E. Jurkiewicz, and W. Luke (2000)
J. Virol. 74, 11145-11152
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Human T-Lymphotropic Virus Type 1 Open Reading Frame I p12I Is Required for Efficient Viral Infectivity in Primary Lymphocytes.
B. Albrecht, N. D. Collins, M. T. Burniston, J. W. Nisbet, L. Ratner, P. L. Green, and M. D. Lairmore (2000)
J. Virol. 74, 9828-9835
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Leader Sequences Downstream of the Primer Binding Site Are Important for Efficient Replication of Simian Immunodeficiency Virus.
Y. Guan, J. B. Whitney, K. Diallo, and M. A. Wainberg (2000)
J. Virol. 74, 8854-8860
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Induction of Mucosal Homing Virus-Specific CD8+ T Lymphocytes by Attenuated Simian Immunodeficiency Virus.
M. A. Cromwell, R. S. Veazey, J. D. Altman, K. G. Mansfield, R. Glickman, T. M. Allen, D. I. Watkins, A. A. Lackner, and R. P. Johnson (2000)
J. Virol. 74, 8762-8766
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Mechanisms Associated with Thymocyte Apoptosis Induced by Simian Immunodeficiency Virus.
M. Rosenzweig, M. Connole, A. Forand-Barabasz, M.-P. Tremblay, R. P. Johnson, and A. A. Lackner (2000)
J. Immunol. 165, 3461-3468
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Short- and Long-Term Clinical Outcomes in Rhesus Monkeys Inoculated with a Highly Pathogenic Chimeric Simian/Human Immunodeficiency Virus.
Y. Endo, T. Igarashi, Y. Nishimura, C. Buckler, A. Buckler-White, R. Plishka, D. S. Dimitrov, and M. A. Martin (2000)
J. Virol. 74, 6935-6945
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Enhanced Infectivity of an R5-Tropic Simian/Human Immunodeficiency Virus Carrying Human Immunodeficiency Virus Type 1 Subtype C Envelope after Serial Passages in Pig-Tailed Macaques (Macaca nemestrina).
Z. Chen, Y. Huang, X. Zhao, E. Skulsky, D. Lin, J. Ip, A. Gettie, and D. D. Ho (2000)
J. Virol. 74, 6501-6510
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Simian Immunodeficiency Virus Utilizes Human and Sooty Mangabey but Not Rhesus Macaque STRL33 for Efficient Entry.
S. Pohlmann, B. Lee, S. Meister, M. Krumbiegel, G. Leslie, R. W. Doms, and F. Kirchhoff (2000)
J. Virol. 74, 5075-5082
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Simian Immunodeficiency Virus Containing Mutations in N-Terminal Tyrosine Residues and in the PxxP Motif in Nef Replicates Efficiently in Rhesus Macaques.
S. Carl, A. J. Iafrate, S. M. Lang, N. Stolte, C. Stahl-Hennig, K. Matz-Rensing, D. Fuchs, J. Skowronski, and F. Kirchhoff (2000)
J. Virol. 74, 4155-4164
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Experimental Infection of Rhesus and Pig-Tailed Macaques with Macaque Rhadinoviruses.
K. G. Mansfield, S. V. Westmoreland, C. D. DeBakker, S. Czajak, A. A. Lackner, and R. C. Desrosiers (1999)
J. Virol. 73, 10320-10328
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Mucosal Immunization of Cynomolgus Macaques with Two Serotypes of Live Poliovirus Vectors Expressing Simian Immunodeficiency Virus Antigens: Stimulation of Humoral, Mucosal, and Cellular Immunity.
S. Crotty, B. L. Lohman, F. X.-S. Lu, S. Tang, C. J. Miller, and R. Andino (1999)
J. Virol. 73, 9485-9495
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Protection by Live, Attenuated Simian Immunodeficiency Virus against Heterologous Challenge.
M. S. Wyand, K. Manson, D. C. Montefiori, J. D. Lifson, R. P. Johnson, and R. C. Desrosiers (1999)
J. Virol. 73, 8356-8363
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The Human Immunodeficiency Virus Type 1 nef Gene Can to a Large Extent Replace Simian Immunodeficiency Virus nef In Vivo.
F. Kirchhoff, J. Munch, S. Carl, N. Stolte, K. Matz-Rensing, D. Fuchs, P. Ten Haaft, J. L. Heeney, T. Swigut, J. Skowronski, et al. (1999)
J. Virol. 73, 8371-8383
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Neuropathogenesis of Simian Immunodeficiency Virus in Neonatal Rhesus Macaques.
S. V. Westmoreland, K. C. Williams, M. A. Simon, M. E. Bahn, A. E. Rullkoetter, M. W. Elliott, C. D. deBakker, H. L. Knight, and A. A. Lackner (1999)
Am. J. Pathol. 155, 1217-1228
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Effects of Soluble CD4 on Simian Immunodeficiency Virus Infection of CD4-Positive and CD4-Negative Cells.
D. Schenten, L. Marcon, G. B. Karlsson, C. Parolin, T. Kodama, N. Gerard, and J. Sodroski (1999)
J. Virol. 73, 5373-5380
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Improved Mg2+-Based Reverse Transcriptase Assay for Detection of Primate Retroviruses.
J. F. Sears, R. Repaske, and A. S. Khan (1999)
J. Clin. Microbiol. 37, 1704-1708
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Effect of the Attenuating Deletion and of Sequence Alterations Evolving In Vivo on Simian Immunodeficiency Virus C8-Nef Function.
S. Carl, A. J. Iafrate, J. Skowronski, C. Stahl-Hennig, and F. Kirchhoff (1999)
J. Virol. 73, 2790-2797
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Association of Simian Virus 40 with a Central Nervous System Lesion Distinct from Progressive Multifocal Leukoencephalopathy in Macaques with AIDS.
M. A. Simon, P. O. Ilyinskii, G. B. Baskin, H. Y. Knight, D. R. Pauley, and A. A. Lackner (1999)
Am. J. Pathol. 154, 437-446
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Diverse Host Responses and Outcomes following Simian Immunodeficiency Virus SIVmac239 Infection in Sooty Mangabeys and Rhesus Macaques.
A. Kaur, R. M. Grant, R. E. Means, H. McClure, M. Feinberg, and R. P. Johnson (1998)
J. Virol. 72, 9597-9611
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Rhesus Macaques Infected with Macrophage-Tropic Simian Immunodeficiency Virus (SIVmacR71/17E) Exhibit Extensive Focal Segmental and Global Glomerulosclerosis.
E. B. Stephens, C. Tian, Z. Li, O. Narayan, and V. H. Gattone II (1998)
J. Virol. 72, 8820-8832
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Inhibition of Simian Immunodeficiency Virus (SIV) Replication by CD8+ T Lymphocytes from Macaques Immunized with Live Attenuated SIV.
M.-C. Gauduin, R. L. Glickman, R. Means, and R. P. Johnson (1998)
J. Virol. 72, 6315-6324
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Viral Genetic Evolution in Macaques Infected with Molecularly Cloned Simian Immunodeficiency Virus Correlates with the Extent of Persistent Viremia.
V. M. Hirsch, G. Dapolito, A. Hahn, J. Lifson, D. Montefiori, C. R. Brown, and R. Goeken (1998)
J. Virol. 72, 6482-6489
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Neutralizing Antibodies in Sera from Macaques Immunized with Attenuated Simian Immunodeficiency Virus.
A. J. Langlois, R. C. Desrosiers, M. G. Lewis, V. N. KewalRamani, D. R. Littman, J. Y. Zhou, K. Manson, M. S. Wyand, D. P. Bolognesi, and D. C. Montefiori (1998)
J. Virol. 72, 6950-6955
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Simian-Human Immunodeficiency Virus (SHIV) Containing the nef/Long Terminal Repeat Region of the Highly Virulent SIVsmmPBj14 Causes PBj-Like Activation of Cultured Resting Peripheral Blood Mononuclear Cells, but the Chimera Showed No Increase in Virulence.
E. B. Stephens, S. Mukherjee, Z. Q. Liu, D. Sheffer, R. Lamb-Wharton, K. Leung, W. Zhuge, S. V. Joag, Z. Li, L. Foresman, et al. (1998)
J. Virol. 72, 5207-5214
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Early Regeneration of Thymic Progenitors in Rhesus Macaques Infected with Simian Immunodeficiency Virus.
J. J. Wykrzykowska, M. Rosenzweig, R. S. Veazey, M. A. Simon, K. Halvorsen, R. C. Desrosiers, R. P. Johnson, and A. A. Lackner (1998)
J. Exp. Med. 187, 1767-1778
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Gastrointestinal Tract as a Major Site of CD4+ T Cell Depletion and Viral Replication in SIV Infection.
R. S. Veazey, M. DeMaria, L. V. Chalifoux, D. E. Shvetz, D. R. Pauley, H. L. Knight, M. Rosenzweig, R. P. Johnson, R. C. Desrosiers, and A. A. Lackner (1998)
Science 280, 427-431
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In Vivo Replication Capacity Rather Than In Vitro Macrophage Tropism Predicts Efficiency of Vaginal Transmission of Simian Immunodeficiency Virus or Simian/Human Immunodeficiency Virus in Rhesus Macaques.
C. J. Miller, M. Marthas, J. Greenier, D. Lu, P. J. Dailey, and Y. Lu (1998)
J. Virol. 72, 3248-3258
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The U3 Promoter and the nef Gene of Simian Immunodeficiency Virus (SIV) smmPBj1.9 Do Not Confer Acute Pathogenicity upon SIVagm.
S. Wagener, M. T. Dittmar, B. Beer, R. Konig, R. Plesker, S. Norley, R. Kurth, and K. Cichutek (1998)
J. Virol. 72, 3446-3450
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Identification of Highly Attenuated Mutants of Simian Immunodeficiency Virus.
R. C. Desrosiers, J. D. Lifson, J. S. Gibbs, S. C. Czajak, A. Y. M. Howe, L. O. Arthur, and R. P. Johnson (1998)
J. Virol. 72, 1431-1437
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Administration of an Anti-CD8 Monoclonal Antibody Interferes with the Clearance of Chimeric Simian/Human Immunodeficiency Virus during Primary Infections of Rhesus Macaques.
T. Matano, R. Shibata, C. Siemon, M. Connors, H. C. Lane, and M. A. Martin (1998)
J. Virol. 72, 164-169
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A Lymph Node-Derived Cytopathic Simian Immunodeficiency Virus Mne Variant Replicates in Nonstimulated Peripheral Blood Mononuclear Cells.
J. T. Kimata, A. Mozaffarian, and J. Overbaugh (1998)
J. Virol. 72, 245-256
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Evolution of a Simian Immunodeficiency Virus Pathogen.
P. Edmonson, M. Murphey-Corb, L. N. Martin, C. Delahunty, J. Heeney, H. Kornfeld, P. R. Donahue, G. H. Learn, L. Hood, and J. I. Mullins (1998)
J. Virol. 72, 405-414
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Intracellular Immunization of Rhesus CD34+ Hematopoietic Progenitor Cells With a Hairpin Ribozyme Protects T Cells and Macrophages From Simian Immunodeficiency Virus Infection.
M. Rosenzweig, D. F. Marks, D. Hempel, M. Heusch, G. Kraus, F. Wong-Staal, and R. P. Johnson (1997)
Blood 90, 4822-4831
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