Differential inhibition of human immunodeficiency virus type 1 in peripheral blood mononuclear cells and TZM-bl cells by endotoxin-mediated chemokine and gamma interferon production

AIDS Research and Human Retroviruses

Volumn 26, Issue 3, 2010, Pages 279-291

  Geonnotti, Anthony R ^a   Bilska, Miroslawa ^a   Yuan, Xing ^a   Ochsenbauer, Christina ^b   Edmonds, Tara G ^c   Kappes, John C ^b,c   Liao, Hua Xin ^a   Haynes, Barton F ^a   Montefiori, David C ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BETA CHEMOKINE; CD14 ANTIGEN; GAMMA INTERFERON; PHYTOHEMAGGLUTININ;

ANTIVIRAL ACTIVITY; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MONOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; VIRUS NEUTRALIZATION;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; CELL LINE, TUMOR; CHEMOKINES, CC; EQUIPMENT CONTAMINATION; ESCHERICHIA COLI; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; NEUTRALIZATION TESTS; SALMONELLA ENTERICA;

EID: 77950196300     PISSN: 08892229     EISSN: None     Source Type: Journal    
DOI: 10.1089/aid.2009.0186     Document Type: Article

References (89)

1. Montefiori DC, Morris L, Ferrari G, and Mascola JR: Neutralizing and other antiviral antibodies in HIV-1 infection and vaccination. Curr Opin HIV AIDS 2007;2: 169-176.
2. Polonis VR, Brown BK, Borges AR, et al.: Recent advances in the characterization of HIV-1 neutralization assays for standardized evaluation of the antibody response to infection and vaccination. Virology 2008;375:315-320.
3. Li M, Gao F, Mascola JR, et al.: 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;79:10108-10125.
4. Mascola JR, D'Souza P, Gilbert P, et al.: Recommendations for the design and use of standard virus panels to assess neutralizing antibody responses elicited by candidate human immunodeficiency virus type 1 vaccines. J Virol 2005;79:10103-10107.
5. Montefiori D, Sattentau Q, Flores J, Esparza J, and Mascola J: Antibody-based HIV-1 vaccines: Recent developments and future directions. PLoS Med 2007;4:e348.
6. Montefiori DC: Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol Biol 2009;485:395-405.
7. Richman DD, Wrin T, Little SJ, and Petropoulos CJ: Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci USA 2003;100:4144-4149.
8. Binley JM, Wrin T, Korber B, et al.: Comprehensive crossclade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J Virol 2004;78:13232-13252.
9. Brown BK, Karasavvas N, Beck Z, et al.: Monoclonal antibodies to phosphatidylinositol phosphate neutralize human immunodeficiency virus type 1: Role of phosphate-binding subsites. J Virol 2007;81:2087-2091.
10. Choudhry V, Zhang M-Y, Sidorov IA, et al.: Cross-reactive HIV-1 neutralizing monoclonal antibodies selected by screening of an immune human phage library against an envelope glycoprotein (gp140) isolated from a patient (R2) with broadly HIV-1 neutralizing antibodies. Virology 2007;363:79-90.
11. Zhang M-Y, Vu BK, Choudhary A, et al.: Cross-reactive human immunodeficiency virus type 1-neutralizing human monoclonal antibody that recognizes a novel conformational epitope on gp41 and lacks reactivity against self-antigens. J Virol 2008;82:6869-6879.
12. Mann AM, Rusert P, Berlinger L, Kuster H, Gunthard HF, and Trkola A: HIV sensitivity to neutralization is determined by target and virus producer cell properties. AIDS 2009;23: 1659-1667.
13. Fenyo EM, Heath A, Dispinseri S, et al.: International network for comparison of HIV neutralization assays: The NeutNet report. PLoS ONE 2009;4:e4505.
14. Choudhry V, Zhang M-Y, Harris I, et al.: Increased efficacy of HIV-1 neutralization by antibodies at low CCR5 surface concentration. Biochem Biophys Res Commun 2006;348: 1107-1115.
15. Perez LG, Costa MR, Todd CA, Haynes BF, and Montefiori DC: Utilization of IgG Fc receptors by human immunodeficiency virus type 1: A specific role for antibodies against the membrane proximal external region of gp41. J Virol 2009;83:7397-7410.
16. Beausejour Y and Tremblay MJ: Susceptibility of HIV type 1 to the fusion inhibitor T-20 is reduced on insertion of host intercellular adhesion molecule 1 in the virus membrane. J Infect Dis 2004;190:894-902.
17. Losier M, Fortin JF, Cantin R, Bergeron MG, and Tremblay MJ: Virion-bound ICAM-1 and activated LFA-1: A combination of factors conferring resistance to neutralization by sera from human immunodeficiency virus type 1-infected individuals independently of the disease status and phase. Clin Immunol 2003;108:111-118.
18. Rizzuto CD and Sodroski JG: Contribution of virion ICAM-1 to human immunodeficiency virus infectivity and sensitivity to neutralization. J Virol 1997;71:4847-4851.
19. Louder MK, Sambor A, Chertova E, et al.: HIV-1 envelope pseudotyped viral vectors and infectious molecular clones expressing the same envelope glycoprotein have a similar neutralization phenotype, but culture in peripheral blood mononuclear cells is associated with decreased neutralization sensitivity. Virology 2005;339:226-238.
20. Miyauchi K, Kim Y, Latinovic O, Morozov V, and Melikyan GB: HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 2009;137:433-444.
21. Hoshino K, Takeuchi O, Kawai T, et al.: Cutting edge: Tolllike receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J Immunol 1999;162:3749-3752.
22. Nagai Y, Akashi S, Nagafuku M, et al.: Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol 2002;3:667-672.
23. Poltorak A, He X, Smirnova I, et al.: Defective LPS signaling in C3H=HeJ and C57BL=10ScCr mice: Mutations in Tlr4 gene. Science 1998;282:2085-2088.
24. Wright SD: CD14 and innate recognition of bacteria. J Immunol 1995;155:6-8.
25. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, and Mathison JC: CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 1990;249:1431-1433.
26. Bernstein MS, Tong-Starksen SE, and Locksley RM: Activation of human monocyte-derived macrophages with lipopolysaccharide decreases human immunodeficiency virus replication in vitro at the level of gene expression. J Clin Invest 1991;88:540-545.
27. Kornbluth RS, Oh PS, Munis JR, Cleveland PH, and Richman DD: Interferons and bacterial lipopolysaccharide protect macrophages from productive infection by human immunodeficiency virus in vitro. J Exp Med 1989;169:1137-1151.
28. Verani A, Scarlatti G, Comar M, et al.: C-C chemokines released by lipopolysaccharide (LPS)-stimulated human macrophages suppress HIV-1 infection in both macrophages and T cells. J Exp Med 1997;185:805-816.
29. Verani A, Sironi F, Siccardi AG, Lusso P, and Vercelli D: Inhibition of CXCR4-tropic HIV-1 infection by lipopolysaccharide: Evidence of different mechanisms in macrophages and T lymphocytes. J Immunol 2002;168:6388-6395.
30. Aquaro S, Menten P, Struyf S, et al.: The LD78b isoform of MIP-1a is the most potent CC-chemokine in inhibiting CCR5- dependent human immunodeficiency virus type 1 replication in human macrophages. J Virol 2001;75:4402-4406.
31. Menten P, Wuyts A, and Van Damme J: Macrophage inflammatory protein-1. Cytokine Growth Factor Rev 2002;13: 455-481.
32. Worgall S, Connor R, Kaner RJ, et al.: Expression and use of human immunodeficiency virus type 1 coreceptors by human alveolar macrophages. J Virol 1999;73:5865-5874.
33. Mikulak J, Gianolini M, Versmisse P, Pancino G, Lusso P, and Verani A: Biological and physical characterization of the X4 HIV-1 suppressive factor secreted by LPS-stimulated human macrophages. Virology 2009;390:37-44.
34. Thibault S, Tardif MR, Barat C, and Tremblay MJ: TLR2 signaling renders quiescent naive and memory CD4+ T cells more susceptible to productive infection with X4 and R5 HIV-Type 1. J Immunol 2007;179:4357-4366.
35. Wyllie DH, Kiss-Toth E, Visintin A, et al.: Evidence for an accessory protein function for toll-like receptor 1 in antibacterial responses. J Immunol 2000;165:7125-7132.
36. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, and Kabat D: Effects of CCR5 and CD4cell surface concentrations on infections by macrophage tropic isolates of human immunodeficiency virus type 1. J Virol 1998;72:2855-2864.
37. Wei X, Decker JM, Liu H, et al.: Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 2002;46:1896-1905.
38. Edmonds T, Ding D, Conway J, et al.: Rapid and quantitative analysis of HIV-1 neutralization in primary cells via Renilla luciferase-expressing infectious molecular clones. Presented at the Conference on Retroviruses and Opportunistic Infections, 2009, Montreal, Quebec, Canada.
39. Ochesenbauer C and Kappes JC: New virologic reagents for neutralizing antibody assays. Curr Opin HIV AIDS 2009;4: 418-425.
40. Keele BF, Giorgi EE, Salazar-Gonzalez JF, et al.: Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci USA 2008;105:7552-7557.
41. Salazar-Gonzalez JF, Salazar MG, Keele BF, et al.: Genetic identity, biological phenotype, and evolutionary pathways of transmitted=founder viruses in acute and early HIV-1 infection. J Exp Med 2009;206:1273-1289.
42. Ochsenbauer-Jambor C, Ding H, Keele BF, et al.: Generation and biological characterization of infectious molecular clones derived from clade B HIV-1 transmitted=founder viruses. Presented at the Conference on Retroviruses and Opportunistic Infections, 2009, Montreal, Quebec, Canada.
43. Godowski PJ: A smooth operator for LPS responses. Nat Immunol 2005;6:544-546.
44. Jiang Z, Georgel P, Du X, et al.: CD14 is required for MyD88-independent LPS signaling. Nat Immunol 2005;6: 565-570.
45. Montefiori DC: Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays, In: Current Protocols in Immunology (Coligan JE, Kruisbeek AM, Shevach EM, Strober W, Coico R, Eds.). John Wiley & Sons, 2004, New York, pp. 12.11.1-12.11.15
46. Bures R, Gaitan A, Zhu T, et al.: Immunization with recombinant canarypox vectors expressing membraneanchored 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;16:2019-2035.
47. Abdelwahab SF, Cocchi F, Bagley KC, et al.: HIV-1- suppressive factors are secreted by CD4+ T cells during primary immune responses. Proc Natl Acad Sci USA 2003;100:15006-15010.
48. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, and Lusso P: Identification of RANTES, MIP-1a, and MIP-1b as the major HIV-suppressive factors produced by CD8+ T cells. Science 1995;270:1811-1815.
49. Pal R, Garzino-Demo A, Markham PD, et al.: Inhibition of HIV-1 infection by the b-chemokine MDC. Science 1997;278: 695-698.
50. Urban TJ, Weintrob AC, Fellay J, et al.: CCL3L1 and HIV=AIDS susceptibility. Nat Med 2009;15:1110-1112.
51. Menten P, Struyf S, Schutyser E, et al.: The LD78beta isoform of MIP-1alpha is the most potent CCR5 agonist and HIV-1- inhibiting chemokine. J Clin Invest 1999;104:R1-5.
52. Nakao M, Nomiyama H, and Shimada K: Structures of human genes coding for cytokine LD78 and their expression. Mol Cell Biol 1990;10:3646-3658.
53. Nibbs RJ, Yang J, Landau NR, Mao JH, and Graham GJ: LD78b, a non-allelic variant of human MIP-1alpha (LD78alpha), has enhanced receptor interactions and potent HIV suppressive activity. J Biol Chem 1999;274:17478-17483.
54. Struyf S, Menten P, Lenaerts JP, et al.: Diverging binding capacities of natural LD78b isoforms of macrophage inflammatory protein-1a to the CC chemokine receptors 1, 3 and 5 affect their anti-HIV-1 activity and chemotactic potencies for neutrophils and eosinophils. Eur J Immunol 2001;31:2170-2178.
55. Burton DR, Pyati J, Koduri R, et al.: Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 1994;266:1024-1027.
56. Mo H, Stamatatos L, Ip JE, et al.: Human immunodeficiency virus type 1 mutants that escape neutralization by human monoclonal antibody IgG1b12. J Virol 1997;71:6869-6874.
57. Pantophlet R, Ollmann Saphire E, Poignard P, Parren PW, Wilson IA, and Burton DR: Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120. J Virol 2003;77:642-658.
58. Calarese DA, Scanlan CN, Zwick MB, et al.: Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 2003;300:2065-2071.
59. Sanders RW, Venturi M, Schiffner L, et al.: The mannosedependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J Virol 2002;76:7293-7305.
60. Scanlan CN, Pantophlet R, Wormald MR, et al.: 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;76:7306-7321.
61. Barbato G, Bianchi E, Ingallinella P, et al.: Structural analysis of the epitope of the anti-HIV antibody 2F5 sheds light into its mechanism of neutralization and HIV fusion. J Mol Biol 2003;330:1101-1115.
62. Muster T, Steindl F, Purtscher M, et al.: A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol 1993;67:6642-6647.
63. Purtscher M, Trkola A, Gruber G, et al.: A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 1994;10:1651-1658.
64. Stiegler G, Kunert R, Purtscher M, et al.: A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 2001;17:1757-1765.
65. Zwick MB, Labrijn AF, Wang M, et al.: Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol 2001;75:10892-10905.
66. Schmidtmayerova H, Sherry B, and Bukrinsky M: Chemokines and HIV replication. Nature 1996;382:767.
67. Dragic T, Litwin V, Allaway GP, et al.: HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CCCKR-5. Nature 1996;381:667-673.
68. Moriuchi H, Moriuchi M, Combadiere C, Murphy PM, and Fauci AS: CD8+ T-cell-derived soluble factor(s), but not beta-chemokines RANTES, MIP-1 alpha, and MIP-1 beta, suppress HIV-1 replication in monocyte=macrophages. Proc Natl Acad Sci USA 1996;93:15341-15345.
69. Morrison RP: Differential sensitivities of Chlamydia trachomatis strains to inhibitory effects of gamma interferon. Infect Immun 2000;68:6038-6040.
70. Um S-J, Kim E-J, Hwang E-S, Kim S-J, Namkoong S-E, and Park J-S: Antiproliferative effects of retinoic acid=interferon in cervical carcinoma cell lines: Cooperative growth suppression of IRF-1 and p53. Int J Cancer 2000;85:416-423.
71. Miller SI, Ernst RK, and Bader MW: LPS, TLR4 and infectious disease diversity. Nat Rev Microbiol 2005;3:36-46.
72. Arbour NC, Lorenz E, Schutte BC, et al.: TLR4 mutations are associated with endotoxin hyporesponsiveness in humans. Nat Genet 2000;25:187-191.
73. Picard C, Puel A, Bonnet M, et al.: Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 2003;299: 2076-2079.
74. Bleul CC, Farzan M, Choe H, et al.: The lymphocyte chemoattractant SDF-1 is a ligand for LESTR=fusin and blocks HIV-1 entry. Nature 1996;382:829-833.
75. Oberlin E, Amara A, Bachelerie F, et al.: The CXC chemokine SDF-1 is the ligand for LESTR=fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 1996;382:833-835.
76. Lee B, Rucker J, Doms RW, et al.: b-Chemokine MDC and HIV-1 infection. Science 1998;281:487a.
77. Ho DD, Hartshorn KL, Rota TR, et al.: Recombinant human interferon alpha-A suppresses HTLV-III replication in vitro. Lancet 1985;1:602-604.
78. Yamamoto JK, Barre-Sinoussi F, Bolton V, Pedersen NC, and Gardner MB: Human alpha- and beta-interferon but not gamma- suppress the in vitro replication of LAV, HTLV-III, and ARV-2. J Interferon Res 1986;6:143-152.
79. Triantafilou K, Triantafilou M, and Dedrick RL: A CD14- independent LPS receptor cluster. Nat Immunol 2001;2:338-345.
80. Triantafilou M, Lepper PM, Briault CD, et al.: Chemokine receptor 4 (CXCR4) is part of the lipopolysaccharide "sensing apparatus." Eur J Immunol 2008;38:192-203.
81. Magalhaes PO, Lopes AM, Mazzola PG, Rangel-Yagui C, Penna TC, and Pessoa A, Jr: Methods of endotoxin removal from biological preparations: A review. J Pharm Sci 2007;10: 388-404.
82. Forthal DN, Landucci G, Cole KS, Marthas M, Becerra JC, and Van Rompay K: Rhesus macaque polyclonal and monoclonal antibodies inhibit simian immunodeficiency virus in the presence of human or autologous Rhesus effector cells. J Virol 2006;80:9217-9225.
83. Ancuta P, Kamat A, Kunstman KJ, et al.: Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS ONE 2008;3:e2516.
84. Brenchley JM, Price DA, Schacker TW, et al.: Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006;12:1365-1371.
85. Lester RT, Yao X-D, Ball TB, et al.: HIV-1 RNA dysregulates the natural TLR response to subclinical endotoxemia in Kenyan female sex-workers. PLoS ONE 2009;4:e5644.
86. Jiang W, Lederman MM, Hunt P, et al.: Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis 2009;199: 1177-1185.
87. Mandl JN, Barry AP, Vanderford TH, et al.: Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 2008;14:1077-1087.
88. Pandrea I, Gaufin T, Brenchley JM, et al.: Cutting edge: Experimentally induced immune activation in natural hosts of simian immunodeficiency virus induces significant increases in viral replication and CD4+ T cell depletion. J Immunol 2008;181:6687-6691.
89. Marchetti G, Bellistri GM, Borghi E, et al.: Microbial translocation is associated with sustained failure in CD4+ T-cell reconstitution in HIV-infected patients on longterm highly active antiretroviral therapy. AIDS 2008;22: 2035-2038.