Home LiteratureArticle Details
PMID: 11462019 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Postnatal passive immunization of neonatal macaques with a triple combination of human monoclonal antibodies against oral simian-human immunodeficiency virus challenge.

Journal of virology ·Vol. 75 ·No. 16 ·2001-08-00 ·Pages 7470-80

Hofmann-Lehmann R, Vlasak J, Rasmussen RA, Smith BA, Baba TW, Liska V, Ferrantelli F, Montefiori DC, McClure HM, Anderson DC, Bernacky BJ, Rizvi TA, Schmidt R, Hill LR, Keeling ME, Katinger H, Stiegler G, Cavacini LA, Posner MR, Chou TC, Andersen J, Ruprecht RM

Abstract

To develop prophylaxis against mother-to-child human immunodeficiency virus (HIV) transmission, we established a simian-human immunodeficiency virus (SHIV) infection model in neonatal macaques that mimics intrapartum mucosal virus exposure (T. W. Baba et al., AIDS Res. Hum. Retroviruses 10:351-357, 1994). Using this model, neonates were protected from mucosal SHIV-vpu(+) challenge by pre- and postnatal treatment with a combination of three human neutralizing monoclonal antibodies (MAbs), F105, 2G12, and 2F5 (Baba et al., Nat. Med. 6:200-206, 2000). In the present study, we used this MAb combination only postnatally, thereby significantly reducing the quantity of antibodies necessary and rendering their potential use in humans more practical. We protected two neonates with this regimen against oral SHIV-vpu(+) challenge, while four untreated control animals became persistently infected. Thus, synergistic MAbs protect when used as immunoprophylaxis without the prenatal dose. We then determined in vitro the optimal MAb combination against the more pathogenic SHIV89.6P, a chimeric virus encoding env of the primary HIV89.6. Remarkably, the most potent combination included IgG1b12, which alone does not neutralize SHIV89.6P. We administered the combination of MAbs IgG1b12, 2F5, and 2G12 postnatally to four neonates. One of the four infants remained uninfected after oral challenge with SHIV89.6P, and two infants had no or a delayed CD4(+) T-cell decline. In contrast, all control animals had dramatic drops in their CD4(+) T cells by 2 weeks postexposure. We conclude that our triple MAb combination partially protected against mucosal challenge with the highly pathogenic SHIV89.6P. Thus, combination immunoprophylaxis with passively administered synergistic human MAbs may play a role in the clinical prevention of mother-to-infant transmission of HIV type 1.

MeSH Terms
Administration, Oral Animals Animals, Newborn Antibodies, Monoclonal/administration & dosage,immunology Drug Synergism Humans Immunity, Mucosal Immunization, Passive Macaca Simian Acquired Immunodeficiency Syndrome/immunology,prevention & control,transmission Simian Immunodeficiency Virus/immunology
Chemicals
Antibodies, Monoclonal
Authors & Affiliations
22 authors, click to expand affiliations / ORCID
Hofmann-Lehmann R
Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA.
Vlasak J
Rasmussen R A
Smith B A
Baba T W
Liska V
Ferrantelli F
Montefiori D C
McClure H M
Anderson D C
Bernacky B J
Rizvi T A
Schmidt R
Hill L R
Keeling M E
Katinger H
Stiegler G
Cavacini L A
Posner M R
Chou T C
Andersen J
Ruprecht R M
References (62)
62 references, click to expand
  1. 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. 1996 Oct;70(10):6922-8 PMID: 8794335
  2. Viral burden and disease progression in rhesus monkeys infected with chimeric simian-human immunodeficiency viruses.
    Virology. 1999 Mar 30;256(1):15-21 PMID: 10087222
  3. 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
  4. Viremia and AIDS in rhesus macaques after intramuscular inoculation of plasmid DNA encoding full-length SIVmac239.
    AIDS Res Hum Retroviruses. 1999 Mar 20;15(5):445-50 PMID: 10195754
  5. Protection of Macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies.
    J Virol. 1999 May;73(5):4009-18 PMID: 10196297
  6. A recombinant vaccinia virus based ELISPOT assay detects high frequencies of Pol-specific CD8 T cells in HIV-1-positive individuals.
    AIDS. 1999 May 7;13(7):767-77 PMID: 10357375
  7. HIV transmission through breastfeeding: a study in Malawi.
    JAMA. 1999 Aug 25;282(8):744-9 PMID: 10463709
  8. Protection by live, attenuated simian immunodeficiency virus against heterologous challenge.
    J Virol. 1999 Oct;73(10):8356-63 PMID: 10482586
  9. Determinants of neutralization resistance in the envelope glycoproteins of a simian-human immunodeficiency virus passaged in vivo.
    J Virol. 1999 Oct;73(10):8873-9 PMID: 10482646
  10. Intravenous immune globulin in symptomatic paediatric human immunodeficiency virus infection.
    Eur J Pediatr. 1988 Apr;147(3):300-3 PMID: 3134244
  11. Characterization of primary isolate-like variants of simian-human immunodeficiency virus.
    J Virol. 1999 Dec;73(12):10199-207 PMID: 10559336
  12. Role of apoptosis induction in both peripheral lymph nodes and thymus in progressive loss of CD4+ cells in SHIV-infected macaques.
    AIDS Res Hum Retroviruses. 2000 Jan 1;16(1):9-18 PMID: 10628812
  13. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection.
    Nat Med. 2000 Feb;6(2):200-6 PMID: 10655110
  14. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies.
    Nat Med. 2000 Feb;6(2):207-10 PMID: 10655111
  15. Effect of breastfeeding and formula feeding on transmission of HIV-1: a randomized clinical trial.
    JAMA. 2000 Mar 1;283(9):1167-74 PMID: 10703779
  16. Passive infusion of immune serum into simian immunodeficiency virus-infected rhesus macaques undergoing a rapid disease course has minimal effect on plasma viremia.
    Virology. 2000 Apr 25;270(1):237-49 PMID: 10772996
  17. Sensitive and robust one-tube real-time reverse transcriptase-polymerase chain reaction to quantify SIV RNA load: comparison of one- versus two-enzyme systems.
    AIDS Res Hum Retroviruses. 2000 Sep 1;16(13):1247-57 PMID: 10957722
  18. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination.
    Science. 2000 Oct 20;290(5491):486-92 PMID: 11039923
  19. Immunization with recombinant canarypox vectors expressing membrane-anchored glycoprotein 120 followed by glycoprotein 160 boosting fails to generate antibodies that neutralize R5 primary isolates of human immunodeficiency virus type 1.
    AIDS Res Hum Retroviruses. 2000 Dec 10;16(18):2019-35 PMID: 11153085
  20. Transforming activity and antigenicity of an Epstein-Barr-like virus from lymphoblastoid cell lines of baboons with lymphoid disease.
    Intervirology. 1977;8(4):240-9 PMID: 194867
  21. Generalized equations for the analysis of inhibitions of Michaelis-Menten and higher-order kinetic systems with two or more mutually exclusive and nonexclusive inhibitors.
    Eur J Biochem. 1981 Mar 16;115(1):207-16 PMID: 7227366
  22. Prevention of perinatally transmitted hepatitis B virus infections with hepatitis B immune globulin and hepatitis B vaccine.
    Lancet. 1983 Nov 12;2(8359):1099-102 PMID: 6138642
  23. Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS.
    Science. 1984 May 4;224(4648):500-3 PMID: 6200936
  24. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors.
    Adv Enzyme Regul. 1984;22:27-55 PMID: 6382953
  25. Evaluation of antiviral drugs and neutralizing antibodies to human immunodeficiency virus by a rapid and sensitive microtiter infection assay.
    J Clin Microbiol. 1988 Feb;26(2):231-5 PMID: 3422647
  26. Designing CD4 immunoadhesins for AIDS therapy.
    Nature. 1989 Feb 9;337(6207):525-31 PMID: 2536900
  27. High concentrations of recombinant soluble CD4 are required to neutralize primary human immunodeficiency virus type 1 isolates.
    Proc Natl Acad Sci U S A. 1990 Sep;87(17):6574-8 PMID: 2395859
  28. An IgG human monoclonal antibody that reacts with HIV-1/GP120, inhibits virus binding to cells, and neutralizes infection.
    J Immunol. 1991 Jun 15;146(12):4325-32 PMID: 1710248
  29. Intravenous immune globulin for the prevention of bacterial infections in children with symptomatic human immunodeficiency virus infection.
    N Engl J Med. 1991 Jul 11;325(2):73-80 PMID: 1675763
  30. Statistical analysis of sparse infection data and its implications for retroviral treatment trials in primates.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7581-5 PMID: 1323844
  31. Functional activity of an HIV-1 neutralizing IgG human monoclonal antibody: ADCC and complement-mediated lysis.
    AIDS Res Hum Retroviruses. 1992 May;8(5):553-8 PMID: 1381201
  32. An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1.
    J Virol. 1992 Dec;66(12):7517-21 PMID: 1433527
  33. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1.
    J Virol. 1993 Nov;67(11):6642-7 PMID: 7692082
  34. Resistance to neutralization by broadly reactive antibodies to the human immunodeficiency virus type 1 gp120 glycoprotein conferred by a gp41 amino acid change.
    J Virol. 1994 Feb;68(2):674-80 PMID: 7507184
  35. Neutralization of divergent human immunodeficiency virus type 1 variants and primary isolates by IAM-41-2F5, an anti-gp41 human monoclonal antibody.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3348-52 PMID: 7512731
  36. 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. 1994 Aug;68(8):4821-8 PMID: 7518527
  37. Mucosal infection of neonatal rhesus monkeys with cell-free SIV.
    AIDS Res Hum Retroviruses. 1994 Apr;10(4):351-7 PMID: 8068415
  38. Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization.
    AIDS Res Hum Retroviruses. 1994 Apr;10(4):359-69 PMID: 7520721
  39. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody.
    Science. 1994 Nov 11;266(5187):1024-7 PMID: 7973652
  40. Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120.
    J Virol. 1995 Jan;69(1):101-9 PMID: 7527081
  41. Cross-clade neutralization of primary isolates of human immunodeficiency virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG.
    J Virol. 1995 Nov;69(11):6609-17 PMID: 7474069
  42. Persistent infection of macaques with simian-human immunodeficiency viruses.
    J Virol. 1995 Nov;69(11):7061-7 PMID: 7474126
  43. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1.
    J Virol. 1996 Feb;70(2):1100-8 PMID: 8551569
  44. 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. 1996 May;70(5):3198-206 PMID: 8627800
  45. Utility of SHIV for testing HIV-1 vaccine candidates in macaques.
    J Acquir Immune Defic Syndr Hum Retrovirol. 1996 Jun 1;12(2):99-106 PMID: 8680896
  46. Simultaneous detection of simian retrovirus type D serotypes 1, 2, and 3 by polymerase chain reaction.
    AIDS Res Hum Retroviruses. 1997 Mar 20;13(5):433-7 PMID: 9075485
  47. Evaluation of monoclonal antibodies to human immunodeficiency virus type 1 primary isolates by neutralization assays: performance criteria for selecting candidate antibodies for clinical trials. AIDS Clinical Trials Group Antibody Selection Working Group.
    J Infect Dis. 1997 May;175(5):1056-62 PMID: 9129066
  48. Characterization of molecularly cloned simian-human immunodeficiency viruses causing rapid CD4+ lymphocyte depletion in rhesus monkeys.
    J Virol. 1997 Jun;71(6):4218-25 PMID: 9151808
  49. Characterization of the pathogenic KU-SHIV model of acquired immunodeficiency syndrome in macaques.
    AIDS Res Hum Retroviruses. 1997 May 20;13(8):635-45 PMID: 9168232
  50. Synergistic neutralization of a chimeric SIV/HIV type 1 virus with combinations of human anti-HIV type 1 envelope monoclonal antibodies or hyperimmune globulins.
    AIDS Res Hum Retroviruses. 1997 May 20;13(8):647-56 PMID: 9168233
  51. A human IgG1 (b12) specific for the CD4 binding site of HIV-1 neutralizes by inhibiting the virus fusion entry process, but b12 Fab neutralizes by inhibiting a postfusion event.
    Virology. 1997 Jul 7;233(2):313-26 PMID: 9217055
  52. Infection and pathogenicity of chimeric simian-human immunodeficiency viruses in macaques: determinants of high virus loads and CD4 cell killing.
    J Infect Dis. 1997 Aug;176(2):362-73 PMID: 9237701
  53. Human immunodeficiency virus type 1 mutants that escape neutralization by human monoclonal antibody IgG1b12. off.
    J Virol. 1997 Sep;71(9):6869-74 PMID: 9261412
  54. Detection of simian T cell leukemia virus type I infection in seronegative macaques.
    AIDS Res Hum Retroviruses. 1997 Sep 1;13(13):1147-53 PMID: 9282820
  55. Synergistic neutralization of simian-human immunodeficiency virus SHIV-vpu+ by triple and quadruple combinations of human monoclonal antibodies and high-titer anti-human immunodeficiency virus type 1 immunoglobulins.
    J Virol. 1998 Apr;72(4):3235-40 PMID: 9525650
  56. Neutralizing antibodies in sera from macaques infected with chimeric simian-human immunodeficiency virus containing the envelope glycoproteins of either a laboratory-adapted variant or a primary isolate of human immunodeficiency virus type 1.
    J Virol. 1998 Apr;72(4):3427-31 PMID: 9525675
  57. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens.
    Science. 1998 Jun 19;280(5371):1884-8 PMID: 9632381
  58. Rhesus macaques that become systemically infected with pathogenic SHIV 89.6-PD after intravenous, rectal, or vaginal inoculation and fail to make an antiviral antibody response rapidly develop AIDS.
    J Acquir Immune Defic Syndr Hum Retrovirol. 1998 Sep 1;19(1):6-18 PMID: 9732063
  59. Antibody neutralization-resistant primary isolates of human immunodeficiency virus type 1.
    J Virol. 1998 Dec;72(12):10270-4 PMID: 9811774
  60. A pathogenic threshold of virus load defined in simian immunodeficiency virus- or simian-human immunodeficiency virus-infected macaques.
    J Virol. 1998 Dec;72(12):10281-5 PMID: 9811776
  61. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys.
    Nat Med. 1999 Feb;5(2):204-10 PMID: 9930869
  62. Neutralization of the human immunodeficiency virus type 1 primary isolate JR-FL by human monoclonal antibodies correlates with antibody binding to the oligomeric form of the envelope glycoprotein complex.
    J Virol. 1997 Apr;71(4):2779-85 PMID: 9060632
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2001-08-00
Pages
7470-80
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC114982
Subset
IM
Grants
NIAID NIH HHS · R01 AI034266 · United States
NIAID NIH HHS · KO8-AI01327 · United States
NIAID NIH HHS · AI45320 · United States
NIAID NIH HHS · R21 AI046177 · United States
NIAID NIH HHS · P01 AI048240 · United States
NCRR NIH HHS · P51 RR000165 · United States
NIAID NIH HHS · R21 AI46177 · United States
NIAID NIH HHS · P01 AI48240 · United States
NIAID NIH HHS · N01 AI85343 · United States
NIAID NIH HHS · AI26926 · United States
NIAID NIH HHS · R01 AI026926 · United States
NIAID NIH HHS · R01 AI34266 · United States
NCRR NIH HHS · RR00165 · 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