Home LiteratureArticle Details
PMID: 17580087 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

A comparative immunogenicity study of HIV-1 virus-like particles bearing various forms of envelope proteins, particles bearing no envelope and soluble monomeric gp120.

Virology ·Vol. 366 ·No. 2 ·2007-09-30 ·Pages 245-62

Crooks ET, Moore PL, Franti M, Cayanan CS, Zhu P, Jiang P, de Vries RP, Wiley C, Zharkikh I, Schülke N, Roux KH, Montefiori DC, Burton DR, Binley JM

Abstract

To assess the potential of native Envelope glycoprotein (Env) trimers as neutralizing antibody vaccines, we immunized guinea pigs with three types of VLPs and soluble gp120. Particles included "SOS-VLPs" (bearing disulfide-shackled functional trimers), "UNC-VLPs" (bearing uncleaved nonfunctional Env) and "naked VLPs" (bearing no Env). The SOS-VLPs were found to have a density of about 27 native trimers per particle, approximately twice that of live inactivated HIV-1 preparations. As immunogens, UNC- and SOS-VLP rapidly elicited anti-gp120 antibodies focused on the V3 loop and the gp120 coreceptor binding site. Reactivity to the gp41 immunodominant domain was absent in SOS-VLP sera, presumably because gp120-gp41 association is stabilized, effectively covering this epitope. Gp120-immune sera reacted with the receptor binding sites of gp120 and were less focused on the V3 loop. Some Env-VLP sera neutralized primary isolates at modest titers. The measurement of neutralization was found to be affected by the cell lines used. Depending on the assay particulars, non-Env specific antibodies in VLP sera could enhance infection, or nonspecifically neutralize. However, a neutralization assay using TZM-BL cells was essentially clear of these effects. We also describe a native trimer binding assay to confirm neutralization activity in a manner that completely eliminates nonspecific effects. Overall, our data suggests that Env-VLP sera were primarily focused on nonfunctional forms of Env on VLP surfaces, possibly gp120/gp41 monomers and not the trimers. Therefore, to make progress toward a more effective VLP-based vaccine, we will need to find ways to refocus the attention of B cells on native trimers.

MeSH Terms
AIDS Vaccines/immunology Animals Cell Line Guinea Pigs HIV Antibodies/blood HIV Envelope Protein gp120/genetics,immunology HIV Envelope Protein gp41/immunology HIV-1/immunology Humans Neutralization Tests
Chemicals
AIDS Vaccines HIV Antibodies HIV Envelope Protein gp120 HIV Envelope Protein gp41
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Crooks Emma T
Torrey Pines Institute for Molecular Studies, 3550 General Atomics Court, San Diego, CA 92121, USA.
Moore Penny L
Franti Michael
Cayanan Charmagne S
Zhu Ping
Jiang Pengfei
de Vries Robbert P
Wiley Cheryl
Zharkikh Irina
Schülke Norbert
Roux Kenneth H
Montefiori David C
Burton Dennis R
Binley James M
References (103)
103 references, click to expand
  1. Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies.
    J Virol. 2003 Jan;77(1):353-65 PMID: 12477840
  2. Changes in the immunogenic properties of soluble gp140 human immunodeficiency virus envelope constructs upon partial deletion of the second hypervariable region.
    J Virol. 2003 Feb;77(4):2310-20 PMID: 12551968
  3. Redox-triggered infection by disulfide-shackled human immunodeficiency virus type 1 pseudovirions.
    J Virol. 2003 May;77(10):5678-84 PMID: 12719560
  4. Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusion.
    J Virol. 2003 May;77(10):5829-36 PMID: 12719576
  5. Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1.
    J Virol. 2003 Oct;77(19):10557-65 PMID: 12970440
  6. Gp120 stability on HIV-1 virions and Gag-Env pseudovirions is enhanced by an uncleaved Gag core.
    Virology. 2003 Sep 30;314(2):636-49 PMID: 14554091
  7. Covalently linked human immunodeficiency virus type 1 gp120/gp41 is stably anchored in rhabdovirus particles and exposes critical neutralizing epitopes.
    J Virol. 2003 Dec;77(23):12782-94 PMID: 14610200
  8. Progress in the development of an HIV vaccine.
    Expert Opin Emerg Drugs. 2003 May;8(1):37-45 PMID: 14610910
  9. A single injection of recombinant measles virus vaccines expressing human immunodeficiency virus (HIV) type 1 clade B envelope glycoproteins induces neutralizing antibodies and cellular immune responses to HIV.
    J Virol. 2004 Jan;78(1):146-57 PMID: 14671096
  10. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15812-7 PMID: 14668432
  11. Removal of N-linked glycosylation sites in the V1 region of simian immunodeficiency virus gp120 results in redirection of B-cell responses to V3.
    J Virol. 2004 Feb;78(3):1525-39 PMID: 14722307
  12. Crystal structure of the broadly cross-reactive HIV-1-neutralizing Fab X5 and fine mapping of its epitope.
    Biochemistry. 2004 Feb 17;43(6):1410-7 PMID: 14769016
  13. AIDS/HIV. Developing an AIDS vaccine: need, uncertainty, hope.
    Science. 2004 Jun 25;304(5679):1913-4 PMID: 15218131
  14. Prospects for an AIDS vaccine: three big questions, no easy answers.
    Lancet Infect Dis. 2004 Jul;4(7):397-413 PMID: 15219551
  15. Evaluation of the safety, immunogenicity, and protective efficacy of whole inactivated simian immunodeficiency virus (SIV) vaccines with conformationally and functionally intact envelope glycoproteins.
    AIDS Res Hum Retroviruses. 2004 Jul;20(7):772-87 PMID: 15307924
  16. Polio vaccines and polioviruses.
    Br Med J. 1977 Sep 17;2(6089):765 PMID: 912286
  17. Synthesis and assembly of hepatitis B virus surface antigen particles in yeast.
    Nature. 1982 Jul 22;298(5872):347-50 PMID: 7045698
  18. Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):648-52 PMID: 2300552
  19. Differential loss of envelope glycoprotein gp120 from virions of human immunodeficiency virus type 1 isolates: effects on infectivity and neutralization.
    J Virol. 1991 Feb;65(2):852-60 PMID: 1898972
  20. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1-->2 mannose residues on the outer face of gp120.
    J Virol. 2002 Jul;76(14):7306-21 PMID: 12072529
  21. HIV-specific humoral and cellular immunity in rabbits vaccinated with recombinant human immunodeficiency virus-like gag-env particles.
    Virology. 1991 Aug;183(2):487-95 PMID: 1906660
  22. The ability of certain SIV vaccines to provoke reactions against normal cells.
    Science. 1992 Jan 17;255(5042):292-3 PMID: 1549775
  23. Effects of deletions in the cytoplasmic domain on biological functions of human immunodeficiency virus type 1 envelope glycoproteins.
    J Virol. 1992 Jun;66(6):3306-15 PMID: 1583717
  24. Efficient isolation of novel human monoclonal antibodies with neutralizing activity against HIV-1 from transgenic mice expressing human Ig loci.
    J Immunol. 2002 Jul 1;169(1):595-605 PMID: 12077293
  25. Efficacy of inactivated whole-virus and subunit vaccines in preventing infection and disease caused by equine infectious anemia virus.
    J Virol. 1992 Jun;66(6):3398-408 PMID: 1316455
  26. Protection in simian immunodeficiency virus-vaccinated monkeys correlates with anti-HLA class I antibody response.
    J Exp Med. 1992 Oct 1;176(4):1203-7 PMID: 1402662
  27. Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines.
    Science. 1992 Dec 18;258(5090):1935-8 PMID: 1470916
  28. Cryptic nature of envelope V3 region epitopes protects primary monocytotropic human immunodeficiency virus type 1 from antibody neutralization.
    J Virol. 1994 Sep;68(9):6006-13 PMID: 8057475
  29. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody.
    Science. 1994 Nov 11;266(5187):1024-7 PMID: 7973652
  30. High-titer immune responses elicited by recombinant vaccinia virus priming and particle boosting are ineffective in preventing virulent SIV infection.
    AIDS Res Hum Retroviruses. 1994 Jul;10(7):839-51 PMID: 7986589
  31. An experimental chemically inactivated HIV-1 vaccine induces antibodies that neutralize homologous and heterologous viruses.
    Vaccine. 1995 Jan;13(1):54-60 PMID: 7762278
  32. Assembly of SIV virus-like particles containing envelope proteins using a baculovirus expression system.
    Virology. 1995 Dec 1;214(1):50-8 PMID: 8525638
  33. Virus-like particles as a rotavirus subunit vaccine.
    J Infect Dis. 1996 Sep;174 Suppl 1:S88-92 PMID: 8752296
  34. Maternal monoclonal antibody to the V3 loop alters specificity of the response to a human immunodeficiency virus vaccine.
    J Infect Dis. 1996 Oct;174(4):866-9 PMID: 8843232
  35. Safety and immunogenicity of recombinant human immunodeficiency virus-like particles in rodents and rhesus macaques.
    Intervirology. 1996;39(1-2):93-103 PMID: 8957675
  36. Differential regulation of the antibody responses to Gag and Env proteins of human immunodeficiency virus type 1.
    J Virol. 1997 Apr;71(4):2799-809 PMID: 9060635
  37. Truncation of the human immunodeficiency virus type 1 envelope glycoprotein allows efficient pseudotyping of Moloney murine leukemia virus particles and gene transfer into CD4+ cells.
    J Virol. 1997 Apr;71(4):3341-5 PMID: 9060707
  38. Antibodies with specificity to native gp120 and neutralization activity against primary human immunodeficiency virus type 1 isolates elicited by immunization with oligomeric gp160.
    J Virol. 1997 Jun;71(6):4319-30 PMID: 9151820
  39. Refocusing neutralizing antibody response by targeted dampening of an immunodominant epitope.
    J Immunol. 1997 Jul 1;159(1):279-89 PMID: 9200464
  40. Immunogenicity of recombinant vaccinia viruses that display the HIV type 1 envelope glycoprotein on the surface of infectious virions.
    AIDS Res Hum Retroviruses. 1997 Nov 20;13(17):1497-500 PMID: 9390748
  41. Cytotoxic T cells and neutralizing antibodies induced in rhesus monkeys by virus-like particle HIV vaccines in the absence of protection from SHIV infection.
    Virology. 1998 May 25;245(1):65-74 PMID: 9614868
  42. Stabilization of human immunodeficiency virus type 1 envelope glycoprotein trimers by disulfide bonds introduced into the gp41 glycoprotein ectodomain.
    J Virol. 1998 Sep;72(9):7620-5 PMID: 9696864
  43. Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins.
    J Virol. 1998 Oct;72(10):7992-8001 PMID: 9733838
  44. Studies of the neutralizing activity and avidity of anti-human immunodeficiency virus type 1 Env antibody elicited by DNA priming and protein boosting.
    J Virol. 1998 Nov;72(11):9092-100 PMID: 9765454
  45. Mapping of epitopes exposed on intact human immunodeficiency virus type 1 (HIV-1) virions: a new strategy for studying the immunologic relatedness of HIV-1.
    J Virol. 1998 Nov;72(11):9384-91 PMID: 9765494
  46. Fusion-competent vaccines: broad neutralization of primary isolates of HIV.
    Science. 1999 Jan 15;283(5400):357-62 PMID: 9888845
  47. Inhibition of the anti-V3 loop response to a recombinant gp120SF2 vaccine by preexisting monoclonal antibody.
    AIDS Res Hum Retroviruses. 1999 Jun 10;15(9):855-60 PMID: 10381174
  48. Modifications of HIV-1 retrovirus-like particles to enhance safety and immunogenicity.
    Biologicals. 1998 Dec;26(4):255-65 PMID: 10403029
  49. Role of immune responses against the envelope and the core antigens of simian immunodeficiency virus SIVmne in protection against homologous cloned and uncloned virus challenge in Macaques.
    J Virol. 1999 Oct;73(10):8201-15 PMID: 10482571
  50. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies.
    J Virol. 2004 Dec;78(23):13232-52 PMID: 15542675
  51. The cytoplasmic tail slows the folding of human immunodeficiency virus type 1 Env from a late prebundle configuration into the six-helix bundle.
    J Virol. 2005 Jan;79(1):106-15 PMID: 15596806
  52. Neutralizing as well as non-neutralizing polyclonal immunoglobulin (Ig)G from infected patients capture HIV-1 via antibodies directed against the principal immunodominant domain of gp41.
    Virology. 2005 Mar 1;333(1):102-13 PMID: 15708596
  53. Immunogenicity and safety of a combined hepatitis A and B vaccine administered concomitantly with either a measles-mumps-rubella or a diphtheria-tetanus-acellular pertussis-inactivated poliomyelitis vaccine mixed with a Haemophilus influenzae type b conjugate vaccine in infants aged 12-18 months.
    Vaccine. 2005 Apr 8;23(20):2602-6 PMID: 15780442
  54. Induction of humoral immune responses following vaccination with envelope-containing, formaldehyde-treated, thermally inactivated human immunodeficiency virus type 1.
    J Virol. 2005 Apr;79(8):4927-35 PMID: 15795278
  55. Antigenic conservation and immunogenicity of the HIV coreceptor binding site.
    J Exp Med. 2005 May 2;201(9):1407-19 PMID: 15867093
  56. Induction of systemic and mucosal cross-clade neutralizing antibodies in BALB/c mice immunized with human immunodeficiency virus type 1 clade A virus-like particles administered by different routes of inoculation.
    J Virol. 2005 Jun;79(11):7059-67 PMID: 15890945
  57. Immunization of macaques with single-cycle simian immunodeficiency virus (SIV) stimulates diverse virus-specific immune responses and reduces viral loads after challenge with SIVmac239.
    J Virol. 2005 Jun;79(12):7707-20 PMID: 15919923
  58. Evaluating the immunogenicity of a disulfide-stabilized, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1.
    J Virol. 2005 Jul;79(14):8812-27 PMID: 15994775
  59. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies.
    J Virol. 2005 Aug;79(16):10108-25 PMID: 16051804
  60. Formaldehyde-treated, heat-inactivated virions with increased human immunodeficiency virus type 1 env can be used to induce high-titer neutralizing antibody responses.
    J Virol. 2005 Aug;79(16):10210-7 PMID: 16051814
  61. Comparing antigenicity and immunogenicity of engineered gp120.
    J Virol. 2005 Oct;79(19):12148-63 PMID: 16160142
  62. Induction of neutralizing antibodies against human immunodeficiency virus type 1 primary isolates by Gag-Env pseudovirion immunization.
    J Virol. 2005 Dec;79(23):14804-14 PMID: 16282480
  63. Characterization of antibody responses elicited by human immunodeficiency virus type 1 primary isolate trimeric and monomeric envelope glycoproteins in selected adjuvants.
    J Virol. 2006 Feb;80(3):1414-26 PMID: 16415019
  64. Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1.
    J Virol. 2006 Mar;80(5):2515-28 PMID: 16474158
  65. Characterizing anti-HIV monoclonal antibodies and immune sera by defining the mechanism of neutralization.
    Hum Antibodies. 2005;14(3-4):101-13 PMID: 16720980
  66. Neutralizing antibody responses against autologous and heterologous viruses in acute versus chronic human immunodeficiency virus (HIV) infection: evidence for a constraint on the ability of HIV to completely evade neutralizing antibody responses.
    J Virol. 2006 Jun;80(12):6155-64 PMID: 16731954
  67. Distribution and three-dimensional structure of AIDS virus envelope spikes.
    Nature. 2006 Jun 15;441(7095):847-52 PMID: 16728975
  68. Antibody responses elicited in macaques immunized with human immunodeficiency virus type 1 (HIV-1) SF162-derived gp140 envelope immunogens: comparison with those elicited during homologous simian/human immunodeficiency virus SHIVSF162P4 and heterologous HIV-1 infection.
    J Virol. 2006 Sep;80(17):8745-62 PMID: 16912322
  69. Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ.
    PLoS Pathog. 2006 Aug;2(8):e83 PMID: 16933990
  70. Modulation of DNA vaccine-elicited CD8+ T-lymphocyte epitope immunodominance hierarchies.
    J Virol. 2006 Dec;80(24):11991-7 PMID: 17005652
  71. Membrane embedded HIV-1 envelope on the surface of a virus-like particle elicits broader immune responses than soluble envelopes.
    Virology. 2007 Feb 20;358(2):334-46 PMID: 17011011
  72. Specific amino acids in the N-terminus of the gp41 ectodomain contribute to the stabilization of a soluble, cleaved gp140 envelope glycoprotein from human immunodeficiency virus type 1.
    Virology. 2007 Mar 30;360(1):199-208 PMID: 17092531
  73. A comparative immunogenicity study in rabbits of disulfide-stabilized, proteolytically cleaved, soluble trimeric human immunodeficiency virus type 1 gp140, trimeric cleavage-defective gp140 and monomeric gp120.
    Virology. 2007 Apr 10;360(2):329-40 PMID: 17126869
  74. Immunogenicity of full length and truncated SIV envelope proteins.
    Viral Immunol. 1999;12(3):205-15 PMID: 10532649
  75. A DNA immunization model study with constructs expressing the tick-borne encephalitis virus envelope protein E in different physical forms.
    J Immunol. 1999 Dec 15;163(12):6756-61 PMID: 10586074
  76. Immunogenic and antigenic dominance of a nonneutralizing epitope over a highly conserved neutralizing epitope in the gp41 envelope glycoprotein of human immunodeficiency virus type 1: its deletion leads to a strong neutralizing response.
    Virology. 2000 Jan 5;266(1):66-78 PMID: 10612661
  77. 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 Virol. 2000 Jan;74(2):627-43 PMID: 10623724
  78. Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus.
    J Virol. 2000 Feb;74(4):1961-72 PMID: 10644369
  79. Vaccines and the induction of functional antibodies: time to look beyond the molecules of natural infection?
    Nat Med. 2000 Feb;6(2):123-5 PMID: 10655088
  80. Production and characterization of simian--human immunodeficiency virus-like particles.
    AIDS Res Hum Retroviruses. 2000 Feb 10;16(3):227-36 PMID: 10710211
  81. Modifications that stabilize human immunodeficiency virus envelope glycoprotein trimers in solution.
    J Virol. 2000 May;74(10):4746-54 PMID: 10775613
  82. Enhanced binding of antibodies to neutralization epitopes following thermal and chemical inactivation of human immunodeficiency virus type 1.
    J Virol. 2000 Jul;74(13):5802-9 PMID: 10846059
  83. Characterization and epitope mapping of neutralizing monoclonal antibodies produced by immunization with oligomeric simian immunodeficiency virus envelope protein.
    J Virol. 2000 Sep;74(17):7922-35 PMID: 10933700
  84. [Macaque immunization with virions purified from a primary isolate of the human immunodeficiency virus type 1 induced enhancement antibodies].
    Bull Acad Natl Med. 2000;184(1):67-84; discussion 85-7 PMID: 10989532
  85. Processing, stability, and receptor binding properties of oligomeric envelope glycoprotein from a primary HIV-1 isolate.
    J Biol Chem. 2000 Nov 10;275(45):35137-45 PMID: 10926931
  86. Immunogenicity and protective efficacy of oligomeric human immunodeficiency virus type 1 gp140.
    J Virol. 2001 Jan;75(2):645-53 PMID: 11134278
  87. Increased neutralization sensitivity of CD4-independent human immunodeficiency virus variants.
    J Virol. 2001 Mar;75(5):2041-50 PMID: 11160708
  88. AIDS vaccination studies using an ex vivo feline immunodeficiency virus model: reevaluation of neutralizing antibody levels elicited by a protective and a nonprotective vaccine after removal of antisubstrate cell antibodies.
    J Virol. 2001 May;75(9):4424-9 PMID: 11287594
  89. A Phase 1 study of a recombinant viruslike particle vaccine against human papillomavirus type 11 in healthy adult volunteers.
    J Infect Dis. 2001 May 15;183(10):1485-93 PMID: 11319684
  90. Induction of neutralizing antibodies and gag-specific cellular immune responses to an R5 primary isolate of human immunodeficiency virus type 1 in rhesus macaques.
    J Virol. 2001 Jul;75(13):5879-90 PMID: 11390589
  91. Expression, purification, and characterization of recombinant HIV gp140. The gp41 ectodomain of HIV or simian immunodeficiency virus is sufficient to maintain the retroviral envelope glycoprotein as a trimer.
    J Biol Chem. 2001 Oct 26;276(43):39577-85 PMID: 11514580
  92. Systemic, mucosal, and heterotypic immune induction in mice inoculated with Venezuelan equine encephalitis replicons expressing Norwalk virus-like particles.
    J Virol. 2002 Jan;76(2):730-42 PMID: 11752163
  93. Enhancing the proteolytic maturation of human immunodeficiency virus type 1 envelope glycoproteins.
    J Virol. 2002 Mar;76(6):2606-16 PMID: 11861826
  94. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein.
    J Virol. 2002 Mar;76(6):2683-91 PMID: 11861835
  95. Purification and characterization of oligomeric envelope glycoprotein from a primary R5 subtype B human immunodeficiency virus.
    J Virol. 2002 Mar;76(6):2835-47 PMID: 11861851
  96. Solid-phase proteoliposomes containing human immunodeficiency virus envelope glycoproteins.
    J Virol. 2002 Apr;76(7):3511-21 PMID: 11884575
  97. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus.
    J Virol. 2002 Jun;76(11):5315-25 PMID: 11991960
  98. Modifications of the human immunodeficiency virus envelope glycoprotein enhance immunogenicity for genetic immunization.
    J Virol. 2002 Jun;76(11):5357-68 PMID: 11991964
  99. Broadly cross-reactive HIV-1-neutralizing human monoclonal Fab selected for binding to gp120-CD4-CCR5 complexes.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):6913-8 PMID: 11997472
  100. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120.
    J Virol. 2002 Jul;76(14):7293-305 PMID: 12072528
  101. Oligomeric and conformational properties of a proteolytically mature, disulfide-stabilized human immunodeficiency virus type 1 gp140 envelope glycoprotein.
    J Virol. 2002 Aug;76(15):7760-76 PMID: 12097589
  102. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1.
    J Virol. 2002 Sep;76(17):8875-89 PMID: 12163607
  103. A controlled trial of a human papillomavirus type 16 vaccine.
    N Engl J Med. 2002 Nov 21;347(21):1645-51 PMID: 12444178
Article Info
Journal
Virology
Abbr.
Virology
ISSN
0042-6822
Published
2007-09-30
Epub
2007-00-19
Pages
245-62
Language
English
Region
United States
NLM ID
0110674
PMCID
PMC2080857
Subset
IM
Grants
NIAID NIH HHS · R01 AI058763-01A1 · United States
NIAID NIH HHS · AI55461 · United States
NIAID NIH HHS · R01 AI058763-04 · United States
NIAID NIH HHS · R21 AI049566-02 · United States
NIAID NIH HHS · R01 AI055461 · United States
NIAID NIH HHS · R01 AI058763-02 · United States
NIAID NIH HHS · R56 AI058763 · United States
NIAID NIH HHS · AI32292 · United States
NIAID NIH HHS · R01 AI058763 · United States
NIAID NIH HHS · R21 AI049566-03 · United States
FIC NIH HHS · D43 TW000231 · United States
NIAID NIH HHS · R01 AI100790 · United States
FIC NIH HHS · D43 TW00231 · United States
NIAID NIH HHS · R21 AI049566-01 · United States
NIAID NIH HHS · AI58763 · United States
NIAID NIH HHS · AI49566 · United States
NIAID NIH HHS · R01 AI058763-03 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com