Cited by 295HIV Research and TreatmentCellular transport and secretionT-cell and Retrovirus Studies

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Human immunodeficiency virus infection of CD4-bearing cells occurs by a pH-independent mechanism

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McClure, M. O., Marsh, M., Weiss, R. A.·1988·The EMBO Journal

DOI 10.1002/j.1460-2075.1988.tb02839.xPMC PMC454348

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Abstract

The effect of weak bases (NH4Cl and amantadine) and carboxylic ionophores (monensin) on the infection of CD4 (T4) positive human cell lines by HIV-1 is examined. These reagents, which raise the pH of acidic intracellular organelles, fail to inhibit HIV-1 entry and the events leading to viral protein synthesis at concentrations inhibitory for low pH-dependent fusogenic enveloped viruses. The infectivity of VSV (HIV-1) pseudotypes is unaffected by weak bases at concentrations causing 95% plaque reduction of VSV in its own envelope. HIV-1 dependent cell--cell fusion (syncytium formation) occurs in medium maintained at pH 7.4-7.6, and virions are not irreversibly inactivated by incubation in acid medium. Our results show that HIV-1 entry and membrane fusion do not require exposure to low pH. The production of infectious HIV-1 particles, however, is inhibited in cells treated with NH4Cl.

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Items 101–200 of 295

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Background
Analysis of hemagglutinin-mediated entry tropism of H5N1 avian influenza
Guo, Y., Rumschlag-Booms, E., Wang, J., Xiao, H., Yu, J., Wang, J., Guo, L., Gao, G. F., Cao, Y., Caffrey, M. S., et al. (2009) · Virology Journal · doi:10.1186/1743-422x-6-39 · Cited by 64
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Background
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Berger, E. A., Lifson, J. D., & Eiden, L. E. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.18.8082 · Cited by 60
Duck hepatitis B virus infection of hepatocytes is not dependent on low pH
Rigg, R., & Schaller, H. (1992) · Journal of Virology · doi:10.1128/jvi.66.5.2829-2836.1992 · Cited by 59
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Method
CD4 molecules with a diversity of mutations encompassing the CDR3 region efficiently support human immunodeficiency virus type 1 envelope glycoprotein-mediated cell fusion
Broder, C. C., & Berger, E. A. (1993) · Journal of Virology · doi:10.1128/jvi.67.2.913-926.1993 · Cited by 59
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Background
The Avian Retrovirus Avian Sarcoma/Leukosis Virus Subtype A Reaches the Lipid Mixing Stage of Fusion at Neutral pH
Earp, L. J., Delos, S. E., Netter, R. C., Bates, P. F., & White, J. M. (2003) · Journal of Virology · doi:10.1128/jvi.77.5.3058-3066.2003 · Cited by 58
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Background
Initial Stages of HIV-1 Envelope Glycoprotein-Mediated Cell Fusion Monitored by a New Assay Based on Redistribution of Fluorescent Dyes
Dimitrov, D. S., Golding, H., & Blumenthal, R. (1991) · AIDS Research and Human Retroviruses · doi:10.1089/aid.1991.7.799 · Cited by 58
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The life-cycle of human immunodeficiency virus type 1.
Goto, T., Nakai, M., & Ikuta, K. (1998) · Micron · doi:10.1016/s0968-4328(98)00002-x · Cited by 69
Proteolytic cleavage of the murine coronavirus surface glycoprotein is not required for fusion activity
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Autographa californica Multicapsid Nucleopolyhedrovirus Efficiently Infects Sf9 Cells and Transduces Mammalian Cells via Direct Fusion with the Plasma Membrane at Low pH
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Background
Role of complement and Fc receptors in the pathogenesis of HIV-1 infection
Montefiori, D. C. (1997) · Springer Seminars in Immunopathology · doi:10.1007/bf00813504 · Cited by 54
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Self-citation
Herpes simplex virus glycoprotein D is sufficient to induce spontaneous pH-independent fusion in a cell line that constitutively expresses the glycoprotein
Campadelli‐Fiume, G., Avitabile, E., Fini, S., Stirpe, D., Arsenakis, M., & Roizman, B. (1988) · Virology · doi:10.1016/0042-6822(88)90533-8 · Cited by 53
Imaging Single Retrovirus Entry through Alternative Receptor Isoforms and Intermediates of Virus-Endosome Fusion
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“[4,5,6,7,8,9,10].”
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The complete Consensus V3 loop peptide of the envelope protein gp120 of HIV‐1 shows pronounced helical character in solution
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Method
Human immunodeficiency virus type 1 envelope gp120 is cleaved after incubation with recombinant soluble CD4
Werner, A., & Levy, J. A. (1993) · Journal of Virology · doi:10.1128/jvi.67.5.2566-2574.1993 · Cited by 50
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Background
Kinetics of soluble CD4 binding to cells expressing human immunodeficiency virus type 1 envelope glycoprotein
Dimitrov, D. S., Hillman, K., Manischewitz, J. F., Blumenthal, R., & Golding, H. (1992) · Journal of Virology · doi:10.1128/jvi.66.1.132-138.1992 · Cited by 50
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Background
Investigation of Human Immunodeficiency Virus Fusion Peptides. Analysis of Interrelations Between Their Structure and Function
Slepushkin, V., Andreev, S. M., Sidorova, M. V., Melikyan, G. B., Grigoriev, V. B., Chumakov, V. M., Grinfeldt, A. E., MANUKYAN, R. A., & Ev, K. (1992) · AIDS Research and Human Retroviruses · doi:10.1089/aid.1992.8.9 · Cited by 50
“Such a model could explain the difference between P415 and P491 (similar structures but different length), as well as between P388 and P491 (the same length and different structures) (Tables 1,2,4).”
Fusion of Mature HIV-1 Particles Leads to Complete Release of a Gag-GFP-Based Content Marker and Raises the Intraviral pH
Padilla‐Parra, S., Marin, M., Gahlaut, N., Suter, R., Kondo, N., & Melikyan, G. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071002 · Cited by 50
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Background
Kinetics of HIV-1 interactions with sCD4 and CD4+ cells: Implications for inhibition of virus infection and initial steps of virus entry into cells
Dimitrov, D. S., Willey, R. L., Martin, M. A., & Blumenthal, R. (1992) · Virology · doi:10.1016/0042-6822(92)90441-q · Cited by 49
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Self-citation
Antigenic Properties of the Human Immunodeficiency Virus Envelope Glycoprotein Gp120 on Virions Bound to Target Cells
Mengistu, M., Ray, K., Lewis, G. K., & DeVico, A. L. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004772 · Cited by 47
“Nevertheless, the occurrence of these particles is consistent with conventional models of virion fusion with the plasma membrane [151–160].”
Result
Betaretroviral Envelope Subunits Are Noncovalently Associated and Restricted to the Mammalian Class
Henzy, J. E., & Coffin, J. M. (2012) · Journal of Virology · doi:10.1128/jvi.01442-12 · Cited by 48
The trinity of the cortical actin in the initiation of HIV-1 infection
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“If the endocytic pathway [21] is defective in resting T cells [19,20], HIV envelope-mediated membrane fusion would directly deliver the viral core in front of the cortical actin [22-26]; an encounter and engagement with the cortical actin is unavoidable, either actively or passively.”
Background
Receptor-Mediated Moloney Murine Leukemia Virus Entry Can Occur Independently of the Clathrin-Coated-Pit-Mediated Endocytic Pathway
Lee, S., Zhao, Y., & Anderson, W. F. (1999) · Journal of Virology · doi:10.1128/jvi.73.7.5994-6005.1999 · Cited by 47
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Background
Receptor-Mediated Entry by Equine Infectious Anemia Virus Utilizes a pH-Dependent Endocytic Pathway
Jin, S., Zhang, B., Weisz, O. A., & Montelaro, R. C. (2005) · Journal of Virology · doi:10.1128/jvi.79.23.14489-14497.2005 · Cited by 46
Replication of human immunodeficiency virus type 1 in primary cultured placental cells
MANO, H., & Chermann, J. (1991) · Research in Virology · doi:10.1016/0923-2516(91)90044-4 · Cited by 46
Several CD4 domains can play a role in human immunodeficiency virus infection in cells
Poulin, L., Evans, L. A., Tang, S., Barboza, A., Legg, H. S., Littman, D. R., & Levy, J. A. (1991) · Journal of Virology · doi:10.1128/jvi.65.9.4893-4901.1991 · Cited by 45
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Background
Soluble CD4 enhances simian immunodeficiency virus SIVagm infection
Werner, A., Winskowsky, G., & Kurth, R. (1990) · Journal of Virology · doi:10.1128/jvi.64.12.6252-6256.1990 · Cited by 44
Inhibition of Human Immunodeficiency Virus Type 1 Env-Mediated Fusion by DC-SIGN
Nobile, C., Moris, A., Porrot, F., Sol‐Foulon, N., & Schwartz, O. (2003) · Journal of Virology · doi:10.1128/jvi.77.9.5313-5323.2003 · Cited by 43
“HIV-1 infection is a pH-independent process (24, 32) that is not inhibited by weak bases or by inhibitors of vesicular acidification, such as bafilomycin A1 (22).”
Background
Lentiviral Vectors
Lever, A. M. L., Strappe, P., & Zhao, J. (2004) · Journal of Biomedical Science · doi:10.1007/bf02256092 · Cited by 43
Effect of Mutations in the V3 Loop of HIV-1 gp120 on Infectivity and Susceptibility to Proteolytic Cleavage
Schulz, T. F., Reeves, J. D., Hoad, J. G., Tailor, C. S., Stephens, P. E., Clements, G., ORTLEPP, S., Page, K. A., Moore, J. P., & Weiss, R. A. (1993) · AIDS Research and Human Retroviruses · doi:10.1089/aid.1993.9.159 · Cited by 42
Self-citation
Understanding retroviral life cycle and its genomic RNA packaging
Chameettachal, A., Mustafa, F., & Rizvi, T. A. (2023) · Journal of Molecular Biology · doi:10.1016/j.jmb.2022.167924 · Cited by 41
A molecular model for membrane fusion based on solution studies of an amphiphilic peptide from HIV gp41
Fujii, G., Horvath, S. J., Woodward, S., Eiserling, F. A., & Eisenberg, D. S. (1992) · Protein Science · doi:10.1002/pro.5560011107 · Cited by 41
A Critical Role for CD63 in HIV Replication and Infection of Macrophages and Cell Lines
Chen, H., Dziuba, N., Friedrich, B. M., von Lindern, J. J., Murray, J., Rojo, D. R., Hodge, T., O'Brien, W., & Ferguson, M. (2008) · Virology · doi:10.1016/j.virol.2008.06.029 · Cited by 42
“Although early studies indicated that HIV infection is pH-independent and does not require endocytosis of the CD4 receptor (Maddon et al., 1988; McClure et al., 1988; Stein et al., 1987), HIV can enter through clathrin-coated vesicles which fuse with endosomal membranes (Bourinbaiar et al.”
Background
Role of basic residues in the subgroup-determining region of the subgroup A avian sarcoma and leukosis virus envelope in receptor binding and infection
Rong, L., Edinger, A. L., & Bates, P. F. (1997) · Journal of Virology · doi:10.1128/jvi.71.5.3458-3465.1997 · Cited by 40
“Entry into host cells by most retroviruses, including the avian sarcoma and leukosis viruses (ASLV), does not depend on low pH (12, 16, 17, 24).”
Background
Retrovirus Entry by Endocytosis and Cathepsin Proteases
Kubo, Y., Hayashi, H., Matsuyama, T., Sato, H., & Yamamoto, N. (2012) · Advances in Virology · doi:10.1155/2012/640894 · Cited by 39
“Early reports indicate that the acidification inhibitors enhance [89–91] or do not affect CD4-dependent HIV infection [92, 93], suggesting that the HIV does not enter into host cells via acidic vesicles.”
The transmembrane glycoprotein of human immunodeficiency virus type 1 induces syncytium formation in the absence of the receptor binding glycoprotein
Perez, L. G., O'Donnell, M. A., & Stephens, E. B. (1992) · Journal of Virology · doi:10.1128/jvi.66.7.4134-4143.1992 · Cited by 39
“Subsequently, the transmembrane protein mediates a pHindependent membrane fusion event at the cell surface, permitting release of the viral nucleocapsid into the cell (14, 18, 24, 33).”
Background
Furin is important but not essential for the proteolytic maturation of gp160 of HIV‐1
Gu, M., Rappapor, J., & Leppla, S. H. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)00447-h · Cited by 38
Role of the N-terminal peptides of viral envelope proteins in membrane fusion
Martin, I., Ruysschaert, J., & Epand, R. M. (1999) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(99)00031-9 · Cited by 38
Primate lentiviruses are differentially inhibited by interferon-induced transmembrane proteins
Qian, J., Duff, Y. L., Wang, Y., Pan, Q., Ding, S., Zheng, Y.-M., Liu, S., & Liang, C. (2014) · Virology · doi:10.1016/j.virol.2014.10.015 · Cited by 37
“HIV and SIV are known as pH-independent viruses (McClure et al., 1988).”
Recent progress in lentiviral vector mass production
Ansorge, S., Henry, O., & Kamen, A. (2009) · Biochemical Engineering Journal · doi:10.1016/j.bej.2009.10.017 · Cited by 37
Jaagsiekte Sheep Retrovirus Utilizes a pH-Dependent Endocytosis Pathway for Entry
Bertrand, P., Côté, M., Zheng, Y.-M., Albritton, L. M., & Liu, S. (2007) · Journal of Virology · doi:10.1128/jvi.01853-07 · Cited by 37
“While human immunodeficiency virus type 1 (23, 37) and amphotropic 10A1 murine leukemia virus (MLV) (18, 24, 27) use a pH-independent pathway, other retroviruses, including mouse mammary tumor virus, avian leukosis and sarcoma virus (ASLV) subgroups A and B, equine infectious anemia virus, foamy virus, and ecotropic M…”
Background
To fuse or not to fuse: the effects of electrostatic interactions, hydrophobic forces, and structural amphiphilicity on protein-mediated membrane destabilization
Fujii, G. (1999) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(99)00032-0 · Cited by 38
MOLECULAR BIOLOGY OF HEPATITIS B VIRUS
Yu, W., & Tiollais, P. (1999) · Clinics in Liver Disease · doi:10.1016/s1089-3261(05)70065-9 · Cited by 37
Cationic liposomes (Lipofectin) mediate retroviral infection in the absence of specific receptors
Innes, C. L., Smith, P. B., Langenbach, R. J., Tindall, K. R., & Boone, L. R. (1990) · Journal of Virology · doi:10.1128/jvi.64.2.957-961.1990 · Cited by 36
“Most of the recent studies with retroviruses favor a direct fusion mechanism (17, 19, 20, 29, 40).”
Result
Δ20 IFITM2 differentially restricts X4 and R5 HIV-1
Wu, W., Grotefend, C. R., Tsai, M.-T., Wang, Y., Radic, V., Eoh, H., & Huang, I. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619640114 · Cited by 35
“Nevertheless, HIV-1 entry does not require a low pH environment, and fusion between viral membrane and plasma membrane of CD4 T cells has been well documented (19, 20).”
Background
An Envelope-Determined, pH-Independent Endocytic Route of Viral Entry Determines the Susceptibility of Human Immunodeficiency Virus Type 1 (HIV-1) and HIV-2 to Lv2 Restriction
Marchant, D., Neil, S. J. D., Aubin, K., Schmitz, C., & McKnight, Á. (2005) · Journal of Virology · doi:10.1128/jvi.79.15.9410-9418.2005 · Cited by 36
“HIV-1/2-mediated fusion is pH independent (21).”
Analysis of the murine ecotropic leukemia virus receptor reveals a common biochemical determinant on diverse cell surface receptors that is essential to retrovirus entry
Malhotra, S., Scott, A. G., Zavorotinskaya, T., & Albritton, L. M. (1996) · Journal of Virology · doi:10.1128/jvi.70.1.321-326.1996 · Cited by 35
Insights into neutralization of animal viruses gained from study of influenza virus
Outlaw, M. C., & Dimmock, N. J. (1991) · Epidemiology and Infection · doi:10.1017/s0950268800048354 · Cited by 35
“Other enveloped viruses (e.g. HIV [13], Newcastle Disease Virus [14]) enter cells by fusing with the plasma membrane itself at neutral pH.”
Human immunodeficiency virus type 1 (HIV-1) fusion with model membranes: kinetic analysis and the role of lipid composition, pH and divalent cations
Larsen, C. E., Nir, S., Alford, D. R., Jennings, M. B., Lee, K., & Düzgüneş, N. (1993) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(93)90007-m · Cited by 35
Entry of human immunodeficiency virus (HIV) into MT-2, human T cell leukemia virus carrier cell line
Goto, T., Harada, S., Yamamoto, N., & Nakai, M. (1988) · Archives of Virology · doi:10.1007/bf01315560 · Cited by 34
Glycosylphosphatidylinositol-anchored CD4/Thy-1 chimeric molecules serve as human immunodeficiency virus receptors in human, but not mouse, cells and are modulated by gangliosides
Jasin, M., Page, K. A., & Littman, D. R. (1991) · Journal of Virology · doi:10.1128/jvi.65.1.440-444.1991 · Cited by 34
“In addition, they occur at neutral pH and so are unlikely to require receptor-mediated endocytosis (17).”
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BackgroundInfluential
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“…which fuse with the plasma membrane, e.g. cytomegalovirus (CMV) (Compton et al., 1992), human immunodeficiency virus (HIV) (Freed & Martin, 1995 ; McClure et al., 1988) and paramyxovirus (Lamb, 1993), are rich in disulfide bonds and it is tempting to speculate on the role that disulfide bonds…”
Background

Authors: McClure, M. O., Marsh, M., & Weiss, R. A.
Affiliations: Institute of Cancer Research (GB)
ORCID: McClure, M. O.
Marsh, M.
Weiss, R. A.
Venue: The EMBO Journal
Publisher: Springer Science and Business Media LLC
Published: 1988-02-01
Volume: 7
Issue: 2
Pages: 513-518
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.1002/j.1460-2075.1988.tb02839.x
PMC: PMC454348
OpenAlex: W108460990
Cited by: 295
References: 46
Citations by year: 2026: 1 · 2025: 5 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 5 · 2019: 2 · 2018: 1 · 2017: 4 · 2016: 2 · 2015: 3 · 2014: 6 · 2013: 7 · 2012: 11
FWCI: 6.89
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: The EMBO Journal (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Funders: Wellcome Trust
Medical Research Council
Topics: Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Immunology and Microbiology › Immunology › T-cell and Retrovirus Studies
Keywords: HIV-1 infection, CD4+ T cells, membrane fusion, syncytium formation, ammonium chloride, amantadine, monensin, carboxylic ionophores, weak bases, viral protein synthesis
MeSH terms: Antigens, Differentiation, T-Lymphocyte, Cell Line, Cell Transformation, Viral, HIV, Humans, Hydrogen-Ion Concentration, Viral Envelope Proteins

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Human immunodeficiency virus infection of CD4-bearing cells occurs by a pH-independent mechanism

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