A species-specific amino acid difference in the macaque CD4 receptor restricts replication by global circulating HIV-1 variants representing viruses from recent infection

Journal of Virology

Volumn 86, Issue 23, 2012, Pages 12472-12483

  Humes, Daryl ^a,b   Emery, Sandra ^a   Laws, Elizabeth ^a   Overbaugh, Julie ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 RECEPTOR; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; DISEASE MARKER; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MACACA; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSITIVITY ANALYSIS; SPECIES DIFFERENCE; VIRUS CELL INTERACTION; VIRUS CULTURE; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS REPLICATION;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, CD4; CELL LINE; DISEASE MODELS, ANIMAL; DNA PRIMERS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GREEN FLUORESCENT PROTEINS; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA MULATTA; MUTAGENESIS, SITE-DIRECTED; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIES SPECIFICITY; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; MACACA NEMESTRINA; PRIMATES;

EID: 84869215739     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02176-12     Document Type: Article

References (61)

1. Arthos J, et al. 1989. Identification of the residues in human CD4 critical for the binding of HIV. Cell 57:469-481.
2. Bartz SR, Vodicka MA. 1997. Production of high-titer human immunodeficiency virus type 1 pseudotyped with vesicular stomatitis virus glycoprotein. Methods 12:337-342.
3. Blish CA, et al. 2009. Cross-subtype neutralization sensitivity despite monoclonal antibody resistance among early subtype A, C, and D envelope variants of human immunodeficiency virus type 1. J. Virol. 83:7783-7788.
4. Burton DR, et al. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266: 1024-1027.
5. Camerini D, Seed B. 1990. A CD4 domain important for HIV-mediated syncytium formation lies outside the virus binding site. Cell 60:747-754.
6. Capon DJ, Ward RH. 1991. The CD4-gp120 interaction and AIDS pathogenesis. Annu. Rev. Immunol. 9:649-678.
7. Chen Z, et al. 2000. 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). J. Virol. 74:6501-6510.
8. Chen Z, Zhou P, Ho DD, Landau NT, Marx PA. 1997. Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. J. Virol. 71:2705-2714.
9. Cheng-Mayer C, Weiss C, Seto D, Levy JA. 1989. Isolates of human immunodeficiency virus type 1 from the brain may constitute a special group of the AIDS virus. Proc. Natl. Acad. Sci. U. S. A. 86:8575-8579.
10. Collman R, et al. 1992. An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1. J. Virol. 66:7517-7521.
11. Deminie CA, Emerman M. 1993. Incorporation of human immunodeficiency virus type 1 Gag proteins into murine leukemia virus virions. J. Virol. 67:6499-6506.
12. Duenas-Decamp MJ, Peters PJ, Burton D, Clapham PR. 2009. Determinants flanking the CD4 binding loop modulate macrophage tropism of human immunodeficiency virus type 1 R5 envelopes. J. Virol. 83:2575-2583.
13. Dunfee RL, Thomas ER, Gabuzda D. 2009. Enhanced macrophage tropism of HIV in brain and lymphoid tissues is associated with sensitivity to the broadly neutralizing CD4 binding site antibody b12. Retrovirology. 6:69.
14. Dunfee RL, et al. 2006. The HIV Env variant N283 enhances macrophage tropism and is associated with brain infection and dementia. Proc. Natl. Acad. Sci. U. S. A. 103:15160-15165.
15. Dunfee RL, et al. 2007. Loss of the N-linked glycosylation site at position 386 in the HIV envelope V4 region enhances macrophage tropism and is associated with dementia. Virology 367:222-234.
16. Fomsgaard A, Hirsch VM, Johnson PR. 1992. Cloning and sequences of primate CD4 molecules: diversity of the. Eur. J. Immunol. 22:2973-2981.
17. Fomsgaard A, et al. 1995. Receptor function of CD4 structures from African green monkey and pig-tail macaque for simian immunodeficiency virus, SIVsm, SIVagm, and human immunodeficiency virus type-1. Viral Immunol. 8:121-133.
18. Gorry PR, et al. 2002. Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J. Virol. 76:6277-6292.
19. Harouse JM, et al. 2001. Mucosal transmission and induction of simian AIDS by CCR5-specific simian/human immunodeficiency virus SHIV(SF162P3). J. Virol. 75:1990-1995.
20. Harouse JM, Gettie A, Tan RC, Blanchard J, Cheng-Mayer C. 1999. Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 284:816-819.
21. Hemelaar J, et al. 2011. Global trends in molecular epidemiology of HIV-1 during 2000-2007. AIDS 25:679-689.
22. Himathongkham S, et al. 2002. Species tropism of chimeric SHIV clones containing HIV-1 subtype-A and subtype-E envelope genes. Virology 298: 189-199.
23. Himathongkham S, et al. 2000. Simian-human immunodeficiency virus containing a human immunodeficiency virus type 1 subtype-E envelope gene: persistent infection, CD4T-cell depletion, and mucosal membrane transmission in macaques. J. Virol. 74:7851-7860.
24. Hsu M, et al. 2003. Increased mucosal transmission but not enhanced pathogenicity of the CCR5-tropic, simian AIDS-inducing simian/human immunodeficiency virus SHIV(SF162P3) maps to envelope gp120. J. Virol. 77:989-998.
25. Huang CC, et al. 2005. Structure of a V3-containing HIV-1 gp120 core. Science 310:1025-1028.
26. Humes D, Overbaugh J. 2011. Adaptation of subtype A human immunodeficiency virus type 1 envelope to pig-tailed macaque cells. J. Virol. 85:4409-4420.
27. Joag SV, et al. 1996. Chimeric simian/human immunodeficiency virus that causes progressive loss of CD4 T cells and AIDS in pig-tailed macaques. J. Virol. 70:3189-3197.
28. Korber BT, Letvin NL, Haynes BF. 2009. T-cell vaccine strategies for human immunodeficiency virus, the virus with a thousand faces. J. Virol. 83:8300-8314.
29. Kwong PD, et al. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
30. Li J, Lord CI, Haseltine W, Letvin NL, Sodroski J. 1992. Infection of cynomolgus monkeys with a chimeric HIV-1/SIVmac virus. J. Acquir. Immune Defic. Syndr. 5:639-646.
31. Li M, et al. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125.
32. Li M, et al. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J. Virol. 80:11776-11790.
33. Li Y, et al. 1992. Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectiveness and complementation. J. Virol. 66:6587-6600.
34. Li Y, et al. 2006. Characterization of antibody responses elicited by human immunodeficiency virus type 1 primary isolate trimeric and monomeric envelope glycoproteins in selected adjuvants. J. Virol. 80:1414-1426.
35. Long EM, Rainwater SM, Lavreys L, Mandaliya K, Overbaugh J. 2002. HIV type 1 variants transmitted to women in Kenya require the CCR5 coreceptor for entry, regardless of the genetic complexity of the infecting virus. AIDS Res. Hum. Retrovir. 18:567-576.
36. Luciw PA, Pratt-Lowe E, Shaw KES, Levy JA, Cheng-Mayer C. 1995. Persistent infection of rhesus macaque with T-cell-line-tropic and macrophage-tropic clones of simian/human immunodeficiency viruses (SHIV). Proc. Natl. Acad. Sci. U. S. A. 92:7490-7494.
37. Miller AD, Rosman GJ. 1989. Improved retroviral vectors for gene transfer and expression. Biotechniques 7:980-982.
38. Mirzabekov T, et al. 1999. Enhanced expression, native purification, and characterization of CCR5, a principal HIV-1 coreceptor. J. Biol. Chem. 274:28745-28750.
39. Moir S, Perreault J, Poulin L. 1996. Postbinding events mediated by human immunodeficiency virus type 1 are sensitive to modifications in the D4-transmembrane linker region of CD4. J. Virol. 70:8019-8028.
40. Morgenstern JP, Land H. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18: 3587-3596.
41. Naldini L, Blomer U, Gage FH, Trono D, Verma IM. 1996. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U. S. A. 93:11382-11388.
42. Ndung'u T, et al. 2001. Infectious simian/human immunodeficiency virus with human immunodeficiency virus type 1 subtype C from an African isolate: rhesus macaque model. J. Virol. 75:11417-11425.
43. Nishimura Y, et al. 2010. Generation of the pathogenic R5-tropic simian/ human immunodeficiency virus SHIVAD8 by serial passaging in rhesus macaques. J. Virol. 84:4769-4781.
44. Overbaugh J, Rudensey LM, Papenhausen MD, Benveniste RE, Morton WR. 1991. Variation in simian immunodeficiency virus env is confined to V1 and V4 during progression to simian AIDS. J. Virol. 65:7025-7031.
45. Pal R, et al. 2003. Characterization of a simian human immunodeficiency virus encoding the envelope gene from the CCR5-tropic HIV-1 Ba-L. J. Acquir. Immune Defic. Syndr. 33:300-307.
46. Pineda MJ, Orton BR, Overbaugh J. 2007. A TRIM5alpha-independent post-entry restriction to HIV-1 infection of macaque cells that is dependent on the path of entry. Virology 363:310-318.
47. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D. 1998. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophage-tropic isolates of human immunodeficiency virus type 1. J. Virol. 72:2855-2864.
48. Puffer BA, et al. 2002. CD4 independence of simian immunodeficiency virus Envs is associated with macrophage tropism, neutralization sensitivity, and attenuated pathogenicity. J. Virol. 76:2595-2605.
49. Reimann KA, et al. 1996. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate Env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J. Virol. 70:6922-6928.
50. Reimann KA, et al. 1996. An env gene derived from a primary human immunodeficiency virus type 1 isolate confers high in vivo replicative capacity to a chimeric simian/human immunodeficiency virus in rhesus monkeys. J. Virol. 70:3198-3206.
51. Roben P, et al. 1994. Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1. J. Virol. 68:4821-4828.
52. Rossi F, et al. 2008. The V1-V3 region of a brain-derived HIV-1 envelope glycoprotein determines macrophage tropism, low CD4 dependence, increased fusogenicity and altered sensitivity to entry inhibitors. Retrovirology 5:89.
53. Sakuragi S, et al. 1992. Infection of macaque monkeys with a chimeric human and simian immunodeficiency virus. J. Gen. Virol. 73:2983-2987.
54. Shibata R, et al. 1991. Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J. Virol. 65:3514-3520.
55. Siddappa NB, et al. 2009. Neutralization-sensitive R5-tropic simianhuman immunodeficiency virus SHIV-2873Nip, which carries env isolated from an infant with a recent HIV clade C infection. J. Virol. 83:1422-1432.
56. Song RJ, et al. 2006. Molecularly cloned SHIV-1157ipd3N4: a highly replication-competent, mucosally transmissible R5 simian-human immunodeficiency virus encoding HIV clade C Env. J. Virol. 80:8729-8738.
57. Sterjovski J, et al. 2007. Asn 362 in gp120 contributes to enhanced fusogenicity by CCR5-restricted HIV-1 envelope glycoprotein variants from patients with AIDS. Retrovirology 4:89.
58. Sterjovski J, et al. 2011. CD4-binding site alterations in CCR5-using HIV-1 envelopes influencing gp120-CD4 interactions and fusogenicity. Virology 410:418-428.
59. Thippeshappa R, et al. 2011. Vif substitution enables persistent infection of pig-tailed macaques by human immunodeficiency virus type 1. J. Virol. 85:3767-3779.
60. Wu X, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
61. Zhang ZD, Weinstock G, Gerstein M. 2008. Rapid evolution by positive Darwinian selection in T-cell antigen CD4 in primates. J. Mol. Evol. 66: 446-456.