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Science 15 May 1987:
Vol. 236. no. 4803, pp. 819 - 822
DOI: 10.1126/science.3646751
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Articles

Science, Vol 236, Issue 4803, 819-822
Copyright © 1987 by American Association for the Advancement of Science

articles

Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms

Y Koyanagi, S Miles, RT Mitsuyasu, JE Merrill, HV Vinters, and IS Chen

Human immunodeficiency virus (HIV) is the causative agent of the acquired immune deficiency syndrome (AIDS). A large number of AIDS patients show evidence of neurologic involvement, known as AIDS-related subacute encephalopathy, which has been correlated with the presence of HIV in the brain. In this study, two genetically distinct but related viruses were isolated from one patient from two different sources in the central nervous system: brain tissue and cerebrospinal fluid. Both viruses were found to replicate in peripheral blood lymphocytes, but only virus from brain tissue will efficiently infect macrophage/monocytes. The viruses also differ in their ability to infect a brain glioma explant culture. This infection of the brain-derived cells in vitro is generally nonproductive, and appears to be some form of persistent or latent infection. These results indicate that genetic variation of HIV in vivo may result in altered cell tropisms and possibly implicate strains of HIV with glial cell tropism in the pathogenesis of some neurologic disorders of AIDS.


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J. Virol. 77, 3777-3784
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Tumor necrosis factor-related apoptosis-inducing ligand induces neuronal death in a murine model of HIV central nervous system infection.
Y. Miura, N. Misawa, Y. Kawano, H. Okada, Y. Inagaki, N. Yamamoto, M. Ito, H. Yagita, K. Okumura, H. Mizusawa, et al. (2003)
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Genetic Characterization of Rebounding Human Immunodeficiency Virus Type 1 in Plasma during Multiple Interruptions of Highly Active Antiretroviral Therapy.
M. Dybul, M. Daucher, M. A. Jensen, C. W. Hallahan, T.-W. Chun, M. Belson, B. Hidalgo, D. C. Nickle, C. Yoder, J. A. Metcalf, et al. (2003)
J. Virol. 77, 3229-3237
   Abstract »    Full Text »    PDF »
Human immunodeficiency virus type 1 (HIV-1) induces activation of multiple STATs in CD4+ cells of lymphocyte or monocyte/macrophage lineages.
J. J. Kohler, D. L. Tuttle, C. R. Coberley, J. W. Sleasman, and M. M. Goodenow (2003)
J. Leukoc. Biol. 73, 407-416
   Abstract »    Full Text »    PDF »
Heterogeneity of Envelope Molecules Expressed on Primary Human Immunodeficiency Virus Type 1 Particles as Probed by the Binding of Neutralizing and Nonneutralizing Antibodies.
P. Poignard, M. Moulard, E. Golez, V. Vivona, M. Franti, S. Venturini, M. Wang, P. W. H. I. Parren, and D. R. Burton (2003)
J. Virol. 77, 353-365
   Abstract »    Full Text »    PDF »
Fine Mapping of the Interaction of Neutralizing and Nonneutralizing Monoclonal Antibodies with the CD4 Binding Site of Human Immunodeficiency Virus Type 1 gp120.
R. Pantophlet, E. Ollmann Saphire, P. Poignard, P. W. H. I. Parren, I. A. Wilson, and D. R. Burton (2003)
J. Virol. 77, 642-658
   Abstract »    Full Text »    PDF »
Selection for Human Immunodeficiency Virus Type 1 Recombinants in a Patient with Rapid Progression to AIDS.
S.-L. Liu, J. E. Mittler, D. C. Nickle, T. M. Mulvania, D. Shriner, A. G. Rodrigo, B. Kosloff, X. He, L. Corey, and J. I. Mullins (2002)
J. Virol. 76, 10674-10684
   Abstract »    Full Text »    PDF »
TCR{gamma}{delta}+ and CD161+ Thymocytes Express HIV-1 in the SCID-hu Mouse, Potentially Contributing to Immune Dysfunction in HIV Infection.
K. B. Gurney, O. O. Yang, S. B. Wilson, and C. H. Uittenbogaart (2002)
J. Immunol. 169, 5338-5346
   Abstract »    Full Text »    PDF »
Effects of Prostratin on T-Cell Activation and Human Immunodeficiency Virus Latency.
Y. D. Korin, D. G. Brooks, S. Brown, A. Korotzer, and J. A. Zack (2002)
J. Virol. 76, 8118-8123
   Abstract »    Full Text »    PDF »
Impact of Cytokines on Replication in the Thymus of Primary Human Immunodeficiency Virus Type 1 Isolates from Infants.
L. Pedroza-Martins, W. J. Boscardin, D. J. Anisman-Posner, D. Schols, Y. J. Bryson, and C. H. Uittenbogaart (2002)
J. Virol. 76, 6929-6943
   Abstract »    Full Text »    PDF »
HIV envelope induces a cascade of cell signals in non-proliferating target cells that favor virus replication.
C. Cicala, J. Arthos, S. M. Selig, G. Dennis Jr., D. A. Hosack, D. Van Ryk, M. L. Spangler, T. D. Steenbeke, P. Khazanie, N. Gupta, et al. (2002)
PNAS 99, 9380-9385
   Abstract »    Full Text »    PDF »
Efficient Isolation of Novel Human Monoclonal Antibodies with Neutralizing Activity Against HIV-1 from Transgenic Mice Expressing Human Ig Loci.
Y. He, W. J. Honnen, C. P. Krachmarov, M. Burkhart, S. C. Kayman, J. Corvalan, and A. Pinter (2002)
J. Immunol. 169, 595-605
   Abstract »    Full Text »    PDF »
Hemofiltrate CC Chemokine 1[9-74] Causes Effective Internalization of CCR5 and Is a Potent Inhibitor of R5-Tropic Human Immunodeficiency Virus Type 1 Strains in Primary T Cells and Macrophages.
J. Munch, L. Standker, S. Pohlmann, F. Baribaud, A. Papkalla, O. Rosorius, R. Stauber, G. Sass, N. Heveker, K. Adermann, et al. (2002)
Antimicrob. Agents Chemother. 46, 982-990
   Abstract »    Full Text »    PDF »
Retrocyclin: A primate peptide that protects cells from infection by T- and M-tropic strains of HIV-1.
A. M. Cole, T. Hong, L. M. Boo, T. Nguyen, C. Zhao, G. Bristol, J. A. Zack, A. J. Waring, O. O. Yang, and R. I. Lehrer (2002)
PNAS 99, 1813-1818
   Abstract »    Full Text »    PDF »
Effector Function Activities of a Panel of Mutants of a Broadly Neutralizing Antibody against Human Immunodeficiency Virus Type 1.
M. Hezareh, A. J. Hessell, R. C. Jensen, J. G. J. van de Winkel, and P. W. H. I. Parren (2001)
J. Virol. 75, 12161-12168
   Abstract »    Full Text »    PDF »
Neutralization Synergy of Human Immunodeficiency Virus Type 1 Primary Isolates by Cocktails of Broadly Neutralizing Antibodies.
M. B. Zwick, M. Wang, P. Poignard, G. Stiegler, H. Katinger, D. R. Burton, and P. W. H. I. Parren (2001)
J. Virol. 75, 12198-12208
   Abstract »    Full Text »    PDF »
Unique Monoclonal Antibody Recognizing the Third Extracellular Loop of CXCR4 Induces Lymphocyte Agglutination and Enhances Human Immunodeficiency Virus Type 1-Mediated Syncytium Formation and Productive Infection.
R. Tanaka, A. Yoshida, T. Murakami, E. Baba, J. Lichtenfeld, T. Omori, T. Kimura, N. Tsurutani, N. Fujii, Z.-X. Wang, et al. (2001)
J. Virol. 75, 11534-11543
   Abstract »    Full Text »    PDF »
Identification of Shared Populations of Human Immunodeficiency Virus Type 1 Infecting Microglia and Tissue Macrophages outside the Central Nervous System.
T. H. Wang, Y. K. Donaldson, R. P. Brettle, J. E. Bell, and P. Simmonds (2001)
J. Virol. 75, 11686-11699
   Abstract »    Full Text »    PDF »
Induction of Rapid and Extensive beta -Chemokine Synthesis in Macrophages by Human Immunodeficiency Virus Type 1 and gp120, Independently of Their Coreceptor Phenotype.
W. Choe, D. J. Volsky, and M. J. Potash (2001)
J. Virol. 75, 10738-10745
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Mononuclear Phagocyte Differentiation, Activation, and Viral Infection Regulate Matrix Metalloproteinase Expression: Implications for Human Immunodeficiency Virus Type 1-Associated Dementia.
A. Ghorpade, R. Persidskaia, R. Suryadevara, M. Che, X. J. Liu, Y. Persidsky, and H. E. Gendelman (2001)
J. Virol. 75, 6572-6583
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Characterization of Human Immunodeficiency Virus Type 1 in Saliva and Blood Plasma by V3-Specific Heteroduplex Tracking Assay and Genotype Analyses.
S. A. Freel, J. M. Williams, J. A. E. Nelson, L. L. Patton, S. A. Fiscus, R. Swanstrom, and D. C. Shugars (2001)
J. Virol. 75, 4936-4940
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Elevated cerebrospinal fluid quinolinic acid levels are associated with region-specific cerebral volume loss in HIV infection.
M. P. Heyes, R. J. Ellis, L. Ryan, M. E. Childers, I. Grant, T. Wolfson, S. Archibald, and T. L. Jernigan (2001)
Brain 124, 1033-1042
   Abstract »    Full Text »    PDF »
Genetic and Functional Diversity of Human Immunodeficiency Virus Type 1 Subtype B Nef Primary Isolates.
J. L. Foster, R. P. Molina, T. Luo, V. K. Arora, Y. Huang, D. D. Ho, and J. V. Garcia (2001)
J. Virol. 75, 1672-1680
   Abstract »    Full Text »    PDF »
Mechanisms for Adaptation of Simian Immunodeficiency Virus to Replication in Alveolar Macrophages.
K. Mori, M. Rosenzweig, and R. C. Desrosiers (2000)
J. Virol. 74, 10852-10859
   Abstract »    Full Text »    PDF »
Effects of Genital Tract Inflammation on Human Immunodeficiency Virus Type 1 V3 Populations in Blood and Semen.
L.-H. Ping, M. S. Cohen, I. Hoffman, P. Vernazza, F. Seillier-Moiseiwitsch, H. Chakraborty, P. Kazembe, D. Zimba, M. Maida, S. A. Fiscus, et al. (2000)
J. Virol. 74, 8946-8952
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Sensitivity of Human Immunodeficiency Virus Type 1 to the Fusion Inhibitor T-20 Is Modulated by Coreceptor Specificity Defined by the V3 Loop of gp120.
C. A. Derdeyn, J. M. Decker, J. N. Sfakianos, X. Wu, W. A. O'Brien, L. Ratner, J. C. Kappes, G. M. Shaw, and E. Hunter (2000)
J. Virol. 74, 8358-8367
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Patterns of Changes in Human Immunodeficiency Virus Type 1 V3 Sequence Populations Late in Infection.
J. A. E. Nelson, F. Baribaud, T. Edwards, and R. Swanstrom (2000)
J. Virol. 74, 8494-8501
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CCR5 Signal Transduction in Macrophages by Human Immunodeficiency Virus and Simian Immunodeficiency Virus Envelopes.
J. Arthos, A. Rubbert, R. L. Rabin, C. Cicala, E. Machado, K. Wildt, M. Hanbach, T. D. Steenbeke, R. Swofford, J. M. Farber, et al. (2000)
J. Virol. 74, 6418-6424
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Inhibition of Human Immunodeficiency Virus Type 1 Replication in Primary CD4+ T Lymphocytes, Monocytes, and Dendritic Cells by Cytotoxic T Lymphocytes.
M. E. Severino, N. V. Sipsas, P. T. Nguyen, S. A. Kalams, B. D. Walker, R. P. Johnson, and O. O. Yang (2000)
J. Virol. 74, 6695-6699
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Linkage of the CCR5{Delta}32 Mutation with a Functional Polymorphism of CD45RA.
H.-X. Liao, D. C. Montefiori, D. D. Patel, D. M. Lee, W. K. Scott, M. Pericak-Vance, and B. F. Haynes (2000)
J. Immunol. 165, 148-157
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Induction of Indolamine 2,3-Dioxygenase in Primary Human Macrophages by Human Immunodeficiency Virus Type 1 Is Strain Dependent.
R. S. Grant, H. Naif, S. J. Thuruthyil, N. Nasr, T. Littlejohn, O. Takikawa, and V. Kapoor (2000)
J. Virol. 74, 4110-4115
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Human Immunodeficiency Virus Type 1 Pathogenesis in SCID-hu Mice Correlates with Syncytium-Inducing Phenotype and Viral Replication.
D. Camerini, H.-P. Su, G. Gamez-Torre, M. L. Johnson, J. A. Zack, and I. S. Y. Chen (2000)
J. Virol. 74, 3196-3204
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A Recombinant Human Immunodeficiency Virus Type 1 Envelope Glycoprotein Complex Stabilized by an Intermolecular Disulfide Bond between the gp120 and gp41 Subunits Is an Antigenic Mimic of the Trimeric Virion-Associated Structure.
J. M. Binley, R. W. Sanders, B. Clas, N. Schuelke, A. Master, Y. Guo, F. Kajumo, D. J. Anselma, P. J. Maddon, W. C. Olson, et al. (2000)
J. Virol. 74, 627-643
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Determinants of Syncytium Formation in Microglia by Human Immunodeficiency Virus Type 1: Role of the V1/V2 Domains.
J. T. C. Shieh, J. Martin, G. Baltuch, M. H. Malim, and F. Gonzalez-Scarano (2000)
J. Virol. 74, 693-701
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Persistent CCR5 Utilization and Enhanced Macrophage Tropism by Primary Blood Human Immunodeficiency Virus Type 1 Isolates from Advanced Stages of Disease and Comparison to Tissue-Derived Isolates.
S. Li, J. Juarez, M. Alali, D. Dwyer, R. Collman, A. Cunningham, and H. M. Naif (1999)
J. Virol. 73, 9741-9755
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High Viral Load in the Cerebrospinal Fluid and Brain Correlates with Severity of Simian Immunodeficiency Virus Encephalitis.
M. C. Zink, K. Suryanarayana, J. L. Mankowski, A. Shen, M. Piatak Jr., J. P. Spelman, D. L. Carter, R. J. Adams, J. D. Lifson, and J. E. Clements (1999)
J. Virol. 73, 10480-10488
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Role of CXCR4 in Cell-Cell Fusion and Infection of Monocyte-Derived Macrophages by Primary Human Immunodeficiency Virus Type 1 (HIV-1) Strains: Two Distinct Mechanisms of HIV-1 Dual Tropism.
Y. Yi, S. N. Isaacs, D. A. Williams, I. Frank, D. Schols, E. De Clercq, D. L. Kolson, and R. G. Collman (1999)
J. Virol. 73, 7117-7125
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Inhibitory Mechanism of the CXCR4 Antagonist T22 against Human Immunodeficiency Virus Type 1 Infection.
T. Murakami, T.-Y. Zhang, Y. Koyanagi, Y. Tanaka, J. Kim, Y. Suzuki, S. Minoguchi, H. Tamamura, M. Waki, A. Matsumoto, et al. (1999)
J. Virol. 73, 7489-7496
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An Inducible Human Immunodeficiency Virus Type 1 (HIV-1) Vector Which Effectively Suppresses HIV-1 Replication.
D. S. An, K. Morizono, Q.-X. Li, S. H. Mao, S. Lu, and I. S. Y. Chen (1999)
J. Virol. 73, 7671-7677
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R5 Strains of Human Immunodeficiency Virus Type 1 from Rapid Progressors Lacking X4 Strains Do Not Possess X4-Type Pathogenicity in Human Thymus.
R. D. Berkowitz, A. B. van 't Wout, N. A. Kootstra, M. E. Moreno, V. D. Linquist-Stepps, C. Bare, C. A. Stoddart, H. Schuitemaker, and J. M. McCune (1999)
J. Virol. 73, 7817-7822
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Expanded Tropism of Primary Human Immunodeficiency Virus Type 1 R5 Strains to CD4+ T-Cell Lines Determined by the Capacity To Exploit Low Concentrations of CCR5.
N. Dejucq, G. Simmons, and P. R. Clapham (1999)
J. Virol. 73, 7842-7847
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Progesterone-Induced Inhibition of Chemokine Receptor Expression on Peripheral Blood Mononuclear Cells Correlates with Reduced HIV-1 Infectability In Vitro.
N. Vassiliadou, L. Tucker, and D. J. Anderson (1999)
J. Immunol. 162, 7510-7518
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Enhanced Inhibition of Human Immunodeficiency Virus Type 1 by Met-Stromal-Derived Factor 1beta Correlates with Down-Modulation of CXCR4.
O. O. Yang, S. L. Swanberg, Z. Lu, M. Dziejman, J. McCoy, A. D. Luster, B. D. Walker, and S. H. Herrmann (1999)
J. Virol. 73, 4582-4589
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CCR5-Mediated Human Immunodeficiency Virus Entry Depends on an Amino-Terminal gp120-Binding Site and on the Conformational Integrity of All Four Extracellular Domains.
S. Genoud, F. Kajumo, Y. Guo, D. Thompson, and T. Dragic (1999)
J. Virol. 73, 1645-1648
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CXCR4 utilization is sufficient to trigger CD4+ T cell depletion in HIV-1-infected human lymphoid tissue.
M. L. Penn, J.-C. Grivel, B. Schramm, M. A. Goldsmith, and L. Margolis (1999)
PNAS 96, 663-668
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Determinant in Human Immunodeficiency Virus Type 1 for Efficient Replication under Cytokine-Induced CD4+ T-Helper 1 (Th1)- and Th2-Type Conditions.
Y. Suzuki, Y. Koyanagi, Y. Tanaka, T. Murakami, N. Misawa, N. Maeda, T. Kimura, H. Shida, J. A. Hoxie, W. A. O'Brien, et al. (1999)
J. Virol. 73, 316-324
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Differential Tropism and Replication Kinetics of Human Immunodeficiency Virus Type 1 Isolates in Thymocytes: Coreceptor Expression Allows Viral Entry, but Productive Infection of Distinct Subsets Is Determined at the Postentry Level.
L. Pedroza-Martins, K. B. Gurney, B. E. Torbett, and C. H. Uittenbogaart (1998)
J. Virol. 72, 9441-9452
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CCR5- and CXCR4-Utilizing Strains of Human Immunodeficiency Virus Type 1 Exhibit Differential Tropism and Pathogenesis In Vivo.
R. D. Berkowitz, S. Alexander, C. Bare, V. Linquist-Stepps, M. Bogan, M. E. Moreno, L. Gibson, E. D. Wieder, J. Kosek, C. A. Stoddart, et al. (1998)
J. Virol. 72, 10108-10117
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Natural Killer Cells from HIV-1+ Patients Produce C-C Chemokines and Inhibit HIV-1 Infection.
T. A. Fehniger, G. Herbein, H. Yu, M. I. Para, Z. P. Bernstein, W. A. O'Brien, and M. A. Caligiuri (1998)
J. Immunol. 161, 6433-6438
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Neuronal Death Induced by Brain-Derived Human Immunodeficiency Virus Type 1 Envelope Genes Differs between Demented and Nondemented AIDS Patients.
C. Power, J. C. McArthur, A. Nath, K. Wehrly, M. Mayne, J. Nishio, T. Langelier, R. T. Johnson, and B. Chesebro (1998)
J. Virol. 72, 9045-9053
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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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Rabbit Cells Expressing Human CD4 and Human CCR5 Are Highly Permissive for Human Immunodeficiency Virus Type 1 Infection.
R. F. Speck, M. L. Penn, J. Wimmer, U. Esser, B. F. Hague, T. J. Kindt, R. E. Atchison, and M. A. Goldsmith (1998)
J. Virol. 72, 5728-5734
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Exclusive and Persistent Use of the Entry Coreceptor CXCR4 by Human Immunodeficiency Virus Type 1 from a Subject Homozygous for CCR5 Delta 32.
N. L. Michael, J. A. E. Nelson, V. N. KewalRamani, G. Chang, S. J. O'Brien, J. R. Mascola, B. Volsky, M. Louder, G. C. White II, D. R. Littman, et al. (1998)
J. Virol. 72, 6040-6047
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Sources of the neurotoxin quinolinic acid in the brain of HIV-1-infected patients and retrovirus-infected macaques.
M. P. Heyes, K. Saito, A. Lackner, C. A. Wiley, C. L. Achim, and S. P. Markey (1998)
FASEB J 12, 881-896
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Spontaneous and Ligand-induced Trafficking of CXC-Chemokine Receptor 4.
N. I. Tarasova, R. H. Stauber, and C. J. Michejda (1998)
J. Biol. Chem. 273, 15883-15886
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Human Immunodeficiency Virus Inhibits Multilineage Hematopoiesis In Vivo.
P. S. Koka, J. K. Fraser, Y. Bryson, G. C. Bristol, G. M. Aldrovandi, E. S. Daar, and J. A. Zack (1998)
J. Virol. 72, 5121-5127
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Determinants of Entry Cofactor Utilization and Tropism in a Dualtropic Human Immunodeficiency Virus Type 1 Primary Isolate.
R. J. Smyth, Y. Yi, A. Singh, and R. G. Collman (1998)
J. Virol. 72, 4478-4484
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Effects of CCR5 and CD4 Cell Surface Concentrations on Infections by Macrophagetropic Isolates of Human Immunodeficiency Virus Type 1.
E. J. Platt, K. Wehrly, S. E. Kuhmann, B. Chesebro, and D. Kabat (1998)
J. Virol. 72, 2855-2864
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Human Immunodeficiency Virus Neurotropism: an Analysis of Viral Replication and Cytopathicity for Divergent Strains in Monocytes and Microglia.
A. Ghorpade, A. Nukuna, M. Che, S. Haggerty, Y. Persidsky, E. Carter, L. Carhart, L. Shafer, and H. E. Gendelman (1998)
J. Virol. 72, 3340-3350
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Alanine Substitutions of Polar and Nonpolar Residues in the Amino-Terminal Domain of CCR5 Differently Impair Entry of Macrophage- and Dualtropic Isolates of Human Immunodeficiency Virus Type 1.
G. E. E. Rabut, J. A. Konner, F. Kajumo, J. P. Moore, and T. Dragic (1998)
J. Virol. 72, 3464-3468
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CD4-Immunoglobulin G2 Protects Hu-PBL-SCID Mice against Challenge by Primary Human Immunodeficiency Virus Type 1 Isolates.
M.-C. Gauduin, G. P. Allaway, W. C. Olson, R. Weir, P. J. Maddon, and R. A. Koup (1998)
J. Virol. 72, 3475-3478
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The Cell Tropism of Human Immunodeficiency Virus Type 1 Determines the Kinetics of Plasma Viremia in SCID Mice Reconstituted with Human Peripheral Blood Leukocytes.
G. R. Picchio, R. J. Gulizia, K. Wehrly, B. Chesebro, and D. E. Mosier (1998)
J. Virol. 72, 2002-2009
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Cells with High Cyclophilin A Content Support Replication of Human Immunodeficiency Virus Type 1 Gag Mutants with Decreased Ability To Incorporate Cyclophilin A.
B. Ackerson, O. Rey, J. Canon, and P. Krogstad (1998)
J. Virol. 72, 303-308
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Human Immunodeficiency Virus Type 1 Populations in Blood and Semen.
E. L. Delwart, J. I. Mullins, P. Gupta, G. H. Learn Jr., M. Holodniy, D. Katzenstein, B. D. Walker, and M. K. Singh (1998)
J. Virol. 72, 617-623
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Detection and Delineation of CXCR-4 (Fusin) as an Entry and Fusion Cofactor for T Cell-Tropic HIV-1 by Three Different Monoclonal Antibodies.
T. Hori, H. Sakaida, A. Sato, T. Nakajima, H. Shida, O. Yoshie, and T. Uchiyama (1998)
J. Immunol. 160, 180-188
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