Identification of Novel Interactions in HIV-1 Capsid Protein Assembly by High-resolution Mass Spectrometry
Abstract
The pleomorphic nature of the immature and mature HIV-1 virions has made it difficult to characterize intersubunit interactions using traditional approaches. While the structures of isolated domains are known, the challenge is to identify intersubunit interactions and thereby pack these domains into supramolecular structures. Using high-resolution mass spectrometry, we have measured the amide hydrogen exchange protection factors for the soluble capsid protein (CA) and CA assembled in vitro. Comparison of the protection factors as well as chemical crosslinking experiments has led to a map of the subunit/subunit interfaces in the assembled tubes. This analysis provides direct biochemical evidence for the homotypic N domain and C domain interactions proposed from cryo-electron microscopy image reconstruction of CA tubes. Most significantly, we have identified a previously unrecognized intersubunit N domain-C domain interaction. The detection of this interaction reconciles previously discrepant biophysical and genetic data.
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An interface is also present between each CA-CTD and the CA-NTD of the neighbouring CA molecule in the hexameric ring.
“An interface is also present between each CA-CTD and the CA-NTD of the neighbouring CA molecule in the hexameric ring”
From Retrovirus maturation-an extraordinary structural transformation (2016) · cites this paper as [55]
Cites
Handbook of Proteolytic Enzymes
(2004) · Elsevier eBooks · doi:10.1016/c2009-0-03628-9 · Cited by 2,627 · see citing works
Fourier transform ion cyclotron resonance mass spectrometry: A primer
Marshall, A. G., Hendrickson, C. L., & Jackson, G. S. (1998) · Mass Spectrometry Reviews · doi:10.1002/(sici)1098-2787(1998)17:1 · Cited by 1,992 · see citing works
Self-citationFourier transform ion cyclotron resonance spectroscopy
Comisarow, M. B., & Marshall, A. G. (1974) · Chemical Physics Letters · doi:10.1016/0009-2614(74)89137-2 · Cited by 1,038 · see citing works
Self-citationZhang, Z., & Smith, D. L. (1993) · Protein Science · doi:10.1002/pro.5560020404 · Cited by 1,017 · see citing works
PROTEINS, AMINO ACIDS AND PEPTIDES as Ions and Dipolar Ions
Cohn, E. J., Edsall, J. T., Kirkwood, J. G., Mueller, H., Oncley, J. L., & Scatchard, G. (1943) · The American Journal of the Medical Sciences · doi:10.1097/00000441-194306000-00035 · Cited by 912 · see citing works
Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques
Johnson, M. L., Correia, J. J., Yphantis, D. A., & Halvorson, H. R. (1981) · Biophysical Journal · doi:10.1016/s0006-3495(81)84753-4 · Cited by 844 · see citing works
HIV-1 Gag proteins: diverse functions in the virus life cycle
Freed, E. O. (1998) · Virology · doi:10.1006/viro.1998.9398 · Cited by 717 · see citing works
Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein
Gamble, T. R., Yoo, S., Vajdos, F. F., von Schwedler, U. K., Worthylake, D. K., Wang, H., McCutcheon, J. P., Sundquist, W. I., & Hill, C. P. (1997) · Science · doi:10.1126/science.278.5339.849 · Cited by 598 · see citing works
Chiu, W. K., Burnett, R. M., & Garcea, R. L. (1997) · Oxford University Press eBooks · Cited by 532 · see citing works
Forshey, B. M., von Schwedler, U. K., Sundquist, W. I., & Aiken, C. (2002) · Journal of Virology · doi:10.1128/jvi.76.11.5667-5677.2002 · Cited by 514 · see citing works
Micro-electrospray mass spectrometry: Ultra-high-sensitivity analysis of peptides and proteins
Emmett, M. R., & Caprioli, R. M. (1994) · Journal of the American Society for Mass Spectrometry · doi:10.1016/1044-0305(94)85001-1 · Cited by 512 · see citing works
Self-citationImage reconstructions of helical assemblies of the HIV-1 CA protein
Li, S., Hill, C. P., Sundquist, W. I., & Finch, J. T. (2000) · Nature · doi:10.1038/35030177 · Cited by 500 · see citing works
Structural biology of HIV 1 1Edited by P. E. Wright
Turner, B. G., & Summers, M. F. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2354 · Cited by 470 · see citing works
Senko, M. W., Hendrickson, C. L., Emmett, M. R., Shi, S. D. ‐., & Marshall, A. G. (1997) · Journal of the American Society for Mass Spectrometry · doi:10.1016/s1044-0305(97)00126-8 · Cited by 461 · see citing works
Self-citationStructure of the Amino-Terminal Core Domain of the HIV-1 Capsid Protein
Gitti, R. K., Lee, B. M., Walker, J., Summers, M. F., Yoo, S., & Sundquist, W. I. (1996) · Science · doi:10.1126/science.273.5272.231 · Cited by 459 · see citing works
Probing the Non-covalent Structure of Proteins by Amide Hydrogen Exchange and Mass Spectrometry
Smith, D. L., Deng, Y., & Zhang, Z. (1997) · Journal of Mass Spectrometry · doi:10.1002/(sici)1096-9888(199702)32:2 · Cited by 426 · see citing works
Mechanisms and uses of hydrogen exchange
Englander, S. W., Sosnick, T. R., Englander, J. J., & Mayne, L. C. (1996) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(96)80090-x · Cited by 383 · see citing works
Amarasinghe, G., Guzman, R. D. D., Turner, R. B., Chancellor, K. J., Wu, Z.-R., & Summers, M. F. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3979 · Cited by 337 · see citing works
Proteolytic refolding of the HIV‐1 capsid protein amino‐terminus facilitates viral core assembly
von Schwedler, U. K., Stemmler, T. L., Klishko, V. Y., Li, S., Albertine, K. H., Davis, D. R., & Sundquist, W. I. (1998) · The EMBO Journal · doi:10.1093/emboj/17.6.1555 · Cited by 337 · see citing works
Crystal structure of dimeric HIV-1 capsid protein
Momany, C., Kovari, L. C., Prongay, A., Keller, W., Gitti, R. K., Lee, B. M., Gorbalenya, A. E., Tong, L., McClure, J., Ehrlich, L. S., et al. (1996) · Nature Structural & Molecular Biology · doi:10.1038/nsb0996-763 · Cited by 313 · see citing works
Mervis, R. J., Ahmad, N., Lillehoj, E. P., Raum, M. G., Salazar, F. H., Chan, H. W., & Venkatesan, S. (1988) · Journal of Virology · doi:10.1128/jvi.62.11.3993-4002.1988 · Cited by 309 · see citing works
Molecular recognition in the HIV-1 capsid/cyclophilin A complex 1 1Edited by J. A. Wells
Yoo, S., Myszka, D. G., Yeh, C.-Y., McMurray, M., Hill, C. P., & Sundquist, W. I. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.1051 · Cited by 259 · see citing works
Senko, M. W., Canterbury, J. D., Guan, S., & Marshall, A. G. (1996) · Rapid Communications in Mass Spectrometry · doi:10.1002/(sici)1097-0231(199611)10:14 · Cited by 256 · see citing works
Self-citationCryo-electron microscopy reveals ordered domains in the immature HIV-1 particle
Fuller, S. D., Wilk, T., Gowen, B. E., Kräusslich, H., & Vogt, V. M. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00331-9 · Cited by 246 · see citing works
Functional domains of the capsid protein of human immunodeficiency virus type 1
Dorfman, T., Bukovský, A., Öhagen, Å., Höglund, S., & Göttlinger, H. G. (1994) · Journal of Virology · doi:10.1128/jvi.68.12.8180-8187.1994 · Cited by 218 · see citing works
Identification of protein–protein interfaces by decreased amide proton solvent accessibility
Mandell, J. G., Falick, A. M., & Komives, E. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14705 · Cited by 209 · see citing works
Structure of the N-terminal 283-residue fragment of the immature HIV-1 Gag polyprotein
Tang, C., Ndassa, Y., & Summers, M. F. (2002) · Nature Structural Biology · doi:10.1038/nsb806 · Cited by 205 · see citing works
Berthet-Colominas, C., Monaco, S., Novelli, A., Sibaı̈, G., Mallet, F., & Cusack, S. (1999) · The EMBO Journal · doi:10.1093/emboj/18.5.1124 · Cited by 191 · see citing works
Assembly, processing, and infectivity of human immunodeficiency virus type 1 gag mutants
Wang, C. T., & Barklis, E. (1993) · Journal of Virology · doi:10.1128/jvi.67.7.4264-4273.1993 · Cited by 184 · see citing works
Organization of Immature Human Immunodeficiency Virus Type 1
Wilk, T., Gross, I., Gowen, B. E., Rutten, T. L. M., de Haas, F., Welker, R., Kräusslich, H., Boulanger, P. A., & Fuller, S. D. (2001) · Journal of Virology · doi:10.1128/jvi.75.2.759-771.2001 · Cited by 179 · see citing works
Determinants of protein hydrogen exchange studied in equine cytochrome c
Milne, J. S., Mayne, L. C., Röder, H., Wand, A. J., & Englander, S. W. (1998) · Protein Science · doi:10.1002/pro.5560070323 · Cited by 177 · see citing works
Macromolecular interactions in the assembly of HIV and other retroviruses
Hunter, E. (1994) · Seminars in Virology · doi:10.1006/smvy.1994.1008 · Cited by 172 · see citing works
Reicin, A., Paik, S., Berkowitz, R., Luban, J., Lowy, I., & Goff, S. (1995) · Journal of Virology · doi:10.1128/jvi.69.2.642-650.1995 · Cited by 155 · see citing works
Tang, S., Murakami, T., Agresta, B. E., Campbell, S., Freed, E. O., & Levin, J. G. (2001) · Journal of Virology · doi:10.1128/jvi.75.19.9357-9366.2001 · Cited by 142 · see citing works
Two-dimensional proton NMR studies of cytochrome c: hydrogen exchange in the N-terminal helix
Wand, A. J., Röder, H., & Englander, S. W. (1986) · Biochemistry · doi:10.1021/bi00353a025 · Cited by 127 · see citing works
Reicin, A. S., Öhagen, Å., Yin, L., Höglund, S., & Goff, S. P. (1996) · Journal of Virology · doi:10.1128/jvi.70.12.8645-8652.1996 · Cited by 125 · see citing works
Lanman, J. K., Sexton, J., Sakalian, M., & Prevelige, P. E. (2002) · Journal of Virology · doi:10.1128/jvi.76.14.6900-6908.2002 · Cited by 123 · see citing works
Self-citationAmide Hydrogen Exchange Determined by Mass Spectrometry: Application to Rabbit Muscle Aldolase
Zhang, Z., Post, C. B., & Smith, D. L. (1996) · Biochemistry · doi:10.1021/bi952227q · Cited by 117 · see citing works
Fitzon, T., Leschonsky, B., Bieler, K., Paulus, C., Schröder, J., Wolf, H. J., & Wagner, R. (2000) · Virology · doi:10.1006/viro.1999.0178 · Cited by 100 · see citing works
Dharmasiri, K., & Smith, D. L. (1996) · Analytical Chemistry · doi:10.1021/ac9601526 · Cited by 99 · see citing works
Zhang, Z., Li, W., Logan, T. M., Li, M., & Marshall, A. G. (1997) · Protein Science · doi:10.1002/pro.5560061015 · Cited by 87 · see citing works
Self-citationDetecting structural changes in viral capsids by hydrogen exchange and mass spectrometry
Wang, L., Lane, L. C., & Smith, D. L. (2001) · Protein Science · doi:10.1110/ps.100101 · Cited by 75 · see citing works
Ma, Y. M., & Vogt, V. M. (2002) · Journal of Virology · doi:10.1128/jvi.76.11.5452-5462.2002 · Cited by 74 · see citing works
Modeling deuterium exchange behavior of ERK2 using pepsin mapping to probe secondary structure
Resing, K. A., Hoofnagle, A. N., & Ahn, N. G. (1999) · Journal of the American Society for Mass Spectrometry · doi:10.1016/s1044-0305(99)00037-9 · Cited by 71 · see citing works
Massiah, M. A., Worthylake, D. K., Christensen, A. M., Sundquist, W. I., Hill, C. P., & Summers, M. F. (1996) · Protein Science · doi:10.1002/pro.5560051202 · Cited by 65 · see citing works
Hughes, C. A. N., Mandell, J. G., Anand, G. S., Stock, A., & Komives, E. A. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4523 · Cited by 65 · see citing works
Wang, F., Li, W., Emmett, M. R., Hendrickson, C. L., Marshall, A. G., Zhang, Y., Wu, L., & Zhang, Z. (1998) · Biochemistry · doi:10.1021/bi981481q · Cited by 61 · see citing works
Self-citationComparative morphology and structural classification of retroviruses.
Nermut, M., & Hockley, D. (1996) · Current Topics in Microbiology and Immunology · doi:10.1007/978-3-642-80145-7_1 · Cited by 60 · see citing works
Second-Site Suppressors of Rous Sarcoma Virus CA Mutations: Evidence for Interdomain Interactions
Bowzard, J. B., Wills, J. W., & Craven, R. C. (2001) · Journal of Virology · doi:10.1128/jvi.75.15.6850-6856.2001 · Cited by 58 · see citing works
Characterization of HIV‐1 p24 self‐association using analytical affinity chromatography
Rosé, S. D., Hensley, P., O'Shannessy, D. J., Culp, J. S., Debouck, C. M., & CHAIKEN, I. M. (1992) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340130204 · Cited by 54 · see citing works
Lam, T. T., Lanman, J. K., Emmett, M. R., Hendrickson, C. L., Marshall, A. G., & Prevelige, P. E. (2002) · Journal of Chromatography A · doi:10.1016/s0021-9673(02)01357-2 · Cited by 53 · see citing works
Self-citationTuma, R., Coward, L. U., Kirk, M. C., Barnes, S., & Prevelige, P. E. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4383 · Cited by 53 · see citing works
Self-citationKragelund, B. B., Knudsen, J., & Poulsen, F. M. (1995) · Journal of Molecular Biology · doi:10.1006/jmbi.1995.0409 · Cited by 48 · see citing works
Wang, F., Li, W., Emmett, M. R., Marshall, A. G., Corson, D. C., & Sykes, B. D. (1999) · Journal of the American Society for Mass Spectrometry · doi:10.1016/s1044-0305(99)00039-2 · Cited by 26 · see citing works
Self-citationTuengler, P., Long, G. L., & Durchschlag, H. (1979) · Analytical Biochemistry · doi:10.1016/0003-2697(79)90171-4 · Cited by 24 · see citing works
Flagged first, then by citations
1 of the 56 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity
Um, S. H., Frigerio, F., Watanabe, M., Picard, F., Joaquin, M., Sticker, M., Fumagalli, S., Allegrini, P. R., Kozma, S. C., Auwerx, J., et al. (2004) · Nature · doi:10.1038/nature02866 · Cited by 1,677 · see citing works
Hydrogen exchange mass spectrometry for the analysis of protein dynamics
Wales, T. E., & Engen, J. R. (2005) · Mass Spectrometry Reviews · doi:10.1002/mas.20064 · Cited by 864 · see citing works
Sinz, A. (2006) · Mass Spectrometry Reviews · doi:10.1002/mas.20082 · Cited by 648 · see citing works
X-Ray Structures of the Hexameric Building Block of the HIV Capsid
Pornillos, O., Ganser-Pornillos, B. K., Kelly, B. N., Hua, Y., Whitby, F. G., Stout, C. D., Sundquist, W. I., Hill, C. P., & Yeager, M. (2009) · Cell · doi:10.1016/j.cell.2009.04.063 · Cited by 523 · see citing works
The structural biology of HIV assembly
Ganser‐Pornillos, B. K., Yeager, M. J., & Sundquist, W. I. (2008) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2008.02.001 · Cited by 500 · see citing works
Probing Native Protein Structures by Chemical Cross-linking, Mass Spectrometry, and Bioinformatics
Leitner, A., Walzthoeni, T., Kahraman, A., Herzog, F., Rinner, O., Beck, M., & Aebersold, R. H. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r000001-mcp201 · Cited by 459 · see citing works
Functional Surfaces of the Human Immunodeficiency Virus Type 1 Capsid Protein
von Schwedler, U. K., Stray, K. M., Garrus, J. E., & Sundquist, W. I. (2003) · Journal of Virology · doi:10.1128/jvi.77.9.5439-5450.2003 · Cited by 421 · see citing works
Structures of the CCR5 N Terminus and of a Tyrosine-Sulfated Antibody with HIV-1 gp120 and CD4
Huang, C.-C., Lam, S. N., Acharya, P., Tang, M., Xiang, S.-H., Shahzad‐ul‐Hussan, S., Stanfield, R. L., Robinson, J. E., Sodroski, J., Wilson, I. A., et al. (2007) · Science · doi:10.1126/science.1145373 · Cited by 416 · see citing works
Structure of Full-Length HIV-1 CA: A Model for the Mature Capsid Lattice
Ganser-Pornillos, B. K., Cheng, A., & Yeager, M. (2007) · Cell · doi:10.1016/j.cell.2007.08.018 · Cited by 321 · see citing works
Assembly Properties of the Human Immunodeficiency Virus Type 1 CA Protein
Ganser-Pornillos, B. K., von Schwedler, U. K., Stray, K. M., Aiken, C., & Sundquist, W. I. (2004) · Journal of Virology · doi:10.1128/jvi.78.5.2545-2552.2004 · Cited by 302 · see citing works
Sinz, A. (2003) · Journal of Mass Spectrometry · doi:10.1002/jms.559 · Cited by 276 · see citing works
A structural perspective on protein?protein interactions
Russell, R. B., Alber, F., Aloy, P., Davis, F. P., Korkin, D., Pichaud, M., Topf, M., & Šali, A. (2004) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2004.04.006 · Cited by 263 · see citing works
Byeon, I.-J. L., Meng, X., Jung, J., Zhao, G., Yang, R., Ahn, J., Shi, J., Concel, J., Aiken, C., Zhang, P., et al. (2009) · Cell · doi:10.1016/j.cell.2009.10.010 · Cited by 253 · see citing works
Chemical Cross-linking and Mass Spectrometry for Protein Structural Modeling
Back, J. W., de Jong, L., Muijsers, A. O., & de Koster, C. G. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(03)00721-6 · Cited by 240 · see citing works
A peptide inhibitor of HIV-1 assembly in vitro
Sticht, J., Humbert, M., Findlow, S. C., Bodem, J., Müller, B., Dietrich, U., Werner, J. M., & Kräusslich, H. (2005) · Nature Structural & Molecular Biology · doi:10.1038/nsmb964 · Cited by 224 · see citing works
Antiviral Inhibition of the HIV-1 Capsid Protein
Tang, C., Loeliger, E., Kinde, I., Kyere, S., Mayo, K., Barklis, E., Sun, Y., Huang, M., & Summers, M. F. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(03)00289-4 · Cited by 218 · see citing works
Mass Spectrometry Identifiable Cross-Linking Strategy for Studying Protein−Protein Interactions
Tang, X., Munske, G. R., Siems, W. F., & Bruce, J. E. (2004) · Analytical Chemistry · doi:10.1021/ac0488762 · Cited by 218 · see citing works
A Cell-penetrating Helical Peptide as a Potential HIV-1 Inhibitor
Zhang, H., Zhao, Q., Bhattacharya, S., Waheed, A. A., Tong, X., Hong, A. L., Heck, S., Curreli, F., Goger, M. J., Cowburn, D., et al. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.02.066 · Cited by 215 · see citing works
Pan, J., Han, J., Borchers, C. H., & Konermann, L. (2009) · Journal of the American Chemical Society · doi:10.1021/ja904379w · Cited by 202 · see citing works
Konermann, L., Tong, X., & Pan, Y. H. (2008) · Journal of Mass Spectrometry · doi:10.1002/jms.1435 · Cited by 197 · see citing works
Extreme Genetic Fragility of the HIV-1 Capsid
Rihn, S. J., Wilson, S. J., Loman, N. J., Alim, M., Bakker, S. E., Bhella, D., Gifford, R. J., Rixon, F. J., & Bieniasz, P. D. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003461 · Cited by 190 · see citing works
High-resolution structure of a retroviral capsid hexameric amino-terminal domain
Mortuza, G. B., Haire, L. F., Stevens, A., Smerdon, S. J., Stoye, J. P., & Taylor, I. A. (2004) · Nature · doi:10.1038/nature02915 · Cited by 185 · see citing works
Human immunodeficiency virus type 1 assembly, release, and maturation
Adamson, C. S., & Freed, E. O. (2007) · Advances in Pharmacology · doi:10.1016/s1054-3589(07)55010-6 · Cited by 179 · see citing works
Assembly and Architecture of HIV
Ganser‐Pornillos, B. K., Yeager, M. J., & Pornillos, O. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-0980-9_20 · Cited by 161 · see citing works
Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange
Lanman, J., Lam, T. T., Emmett, M. R., Marshall, A. G., Sakalian, M., & Prevelige, P. E. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb790 · Cited by 164 · see citing works
Self-citationStructure of the Antiviral Assembly Inhibitor CAP-1 Complex with the HIV-1 CA Protein
Kelly, B. N., Kyere, S. K., Kinde, I., Tang, C., Howard, B. R., Robinson, H. H., Sundquist, W. I., Summers, M. F., & Hill, C. P. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.07.070 · Cited by 152 · see citing works
Mass spectrometry based tools to investigate protein–ligand interactions for drug discovery
Pacholarz, K. J., Garlish, R. A., Taylor, R. J., & Barran, P. E. (2012) · Chemical Society Reviews · doi:10.1039/c2cs35035a · Cited by 140 · see citing works
Interactions between HIV-1 Gag Molecules in Solution: An Inositol Phosphate-mediated Switch
Datta, S. A. K., Zhao, Z., Clark, P. K., Tarasov, S. G., Alexandratos, J. N., Campbell, S. J., Kvaratskhelia, M., Lebowitz, J., & Rein, A. R. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.10.072 · Cited by 132 · see citing works
Disulfide Bond Stabilization of the Hexameric Capsomer of Human Immunodeficiency Virus
Pornillos, O., Ganser‐Pornillos, B. K., Sankaran, B., Hua, Y., & Yeager, M. J. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.06.042 · Cited by 132 · see citing works
Alfadhli, A., Barklis, R. L., & Barklis, E. (2009) · Virology · doi:10.1016/j.virol.2009.02.048 · Cited by 125 · see citing works
Zhang, Q., Willison, L. N., Tripathi, P., Sathe, S. K., Roux, K. H., Emmett, M. R., Blakney, G. T., Zhang, H., & Marshall, A. G. (2011) · Analytical Chemistry · doi:10.1021/ac201501z · Cited by 121 · see citing works
Self-citationRole of HIV-1 Gag domains in viral assembly
Scarlata, S., & Carter, C. (2003) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(03)00163-9 · Cited by 111 · see citing works
Solid-State NMR Studies of HIV-1 Capsid Protein Assemblies
Han, Y. H., Ahn, J., Concel, J., Byeon, I. L., Gronenborn, A. M., Yang, J., & Polenova, T. E. (2010) · Journal of the American Chemical Society · doi:10.1021/ja908687k · Cited by 111 · see citing works
Fitness Costs Limit Viral Escape from Cytotoxic T Lymphocytes at a Structurally Constrained Epitope
Peyerl, F. W., Bazick, H. S., Newberg, M. H., Barouch, D. H., Sodroski, J., & Letvin, N. L. (2004) · Journal of Virology · doi:10.1128/jvi.78.24.13901-13910.2004 · Cited by 108 · see citing works
del Álamo, M., Rivas, G., & Mateu, M. G. (2005) · Journal of Virology · doi:10.1128/jvi.79.22.14271-14281.2005 · Cited by 100 · see citing works
HIV-1 Maturation: Lessons Learned from Inhibitors
Kleinpeter, A. B., & Freed, E. O. (2020) · Viruses · doi:10.3390/v12090940 · Cited by 95 · see citing works
Zhang, H., Kazazić, S., Schaub, T. M., Tipton, J. D., Emmett, M. R., & Marshall, A. G. (2008) · Analytical Chemistry · doi:10.1021/ac801417d · Cited by 96 · see citing works
Self-citationVisualization of a missing link in retrovirus capsid assembly
Giovanni Cardone, A., Purdy, J. G., Cheng, N., Craven, R. C., & Steven, A. C. (2009) · Nature · doi:10.1038/nature07724 · Cited by 95 · see citing works
Ako-adjei, D., Johnson, M. C., & Vogt, V. M. (2005) · Journal of Virology · doi:10.1128/jvi.79.21.13463-13472.2005 · Cited by 92 · see citing works
Peyerl, F. W., Barouch, D. H., Yeh, W. W., Bazick, H. S., Kunstman, J., Kunstman, K., Wolinsky, S. M., & Letvin, N. L. (2003) · Journal of Virology · doi:10.1128/jvi.77.23.12572-12578.2003 · Cited by 91 · see citing works
Uetrecht, C., & Heck, A. J. R. (2011) · Angewandte Chemie International Edition · doi:10.1002/anie.201008120 · Cited by 86 · see citing works
Kellersberger, K. A., Yu, E. T., Kruppa, G. H., Young, M. M., & Fabris, D. (2004) · Analytical Chemistry · doi:10.1021/ac0355045 · Cited by 86 · see citing works
Gardner, M. W., Vasicek, L. A., Shabbir, S. H., Anslyn, E. V., & Brodbelt, J. S. (2008) · Analytical Chemistry · doi:10.1021/ac800625x · Cited by 82 · see citing works
Feixia Chu, C., Shan, S., Moustakas, D. T., Alber, F., Egea, P. F., Stroud, R. M., Walter, P., & Burlingame, A. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407456101 · Cited by 82 · see citing works
HIV Type 1 Gag as a Target for Antiviral Therapy
Waheed, A. A., & Freed, E. O. (2011) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2011.0230 · Cited by 81 · see citing works
Automated extraction of backbone deuteration levels from amide H/2H mass spectrometry experiments
Hotchko, M., Anand, G. S., Komives, E. A., & Eyck, L. F. T. (2006) · Protein Science · doi:10.1110/ps.051774906 · Cited by 79 · see citing works
Bartonova, V., Igonet, S., Sticht, J., Glass, B., Habermann, A., Vaney, M.-C., Sehr, P., Lewis, J., Rey, F. A., & Kraüsslich, H.-G. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m804230200 · Cited by 76 · see citing works
Chavez, J. D., Cilia, M., Weisbrod, C. R., Ju, H.-J., Eng, J. K., Gray, S. M., & Bruce, J. E. (2012) · Journal of Proteome Research · doi:10.1021/pr300041t · Cited by 69 · see citing works
Retrovirus maturation-an extraordinary structural transformation
Mattei, S., Schur, F. K., & Briggs, J. A. (2016) · Current Opinion in Virology · doi:10.1016/j.coviro.2016.02.008 · Cited by 72 · see citing works
“An interface is also present between each CA-CTD and the CA-NTD of the neighbouring CA molecule in the hexameric ring [55].”
BackgroundVirus maturation as a new HIV-1 therapeutic target
Adamson, C. S., Salzwedel, K., & Freed, E. O. (2009) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728220903039714 · Cited by 72 · see citing works
Ma, Y. M., & Vogt, V. M. (2003) · Journal of Virology · doi:10.1128/jvi.78.1.52-60.2004 · Cited by 70 · see citing works
Maturation inhibitors: a new therapeutic class targets the virus structure.
Salzwedel, K., Martin, D. E., & Sakalian, M. (2007) · PubMed · Cited by 69 · see citing works
Self-citationKeller, P. W., Huang, R. K., England, M. R., Waki, K., Cheng, N., Heymann, J. B., Craven, R. C., Freed, E. O., & Steven, A. C. (2013) · Journal of Virology · doi:10.1128/jvi.01408-13 · Cited by 67 · see citing works
del Álamo, M., Neira, J. L., & Mateu, M. G. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304466200 · Cited by 67 · see citing works
Uncoating of HIV-1 requires cellular activation
Auewarakul, P., Wacharapornin, P., Srichatrapimuk, S., Chutipongtanate, S., & Puthavathana, P. (2005) · Virology · doi:10.1016/j.virol.2005.02.028 · Cited by 64 · see citing works
Hydrogen/Deuterium Exchange Mass Spectrometry for Investigating Protein-Ligand Interactions
Garcia, R. A., Pantazatos, D., & Villarreal, F. J. (2004) · Assay and Drug Development Technologies · doi:10.1089/154065804322966342 · Cited by 64 · see citing works
Synthesis of biotin‐tagged chemical cross‐linkers and their applications for mass spectrometry
Kang, S., Mou, L., Lanman, J. K., Velu, S. E., Brouillette, W. J., & Prevelige, P. E. (2009) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.4066 · Cited by 62 · see citing works
Self-citationMolecular recognition by mass spectrometry
Tullio, A. D., Reale, S., & Angelis, F. D. (2005) · Journal of Mass Spectrometry · doi:10.1002/jms.896 · Cited by 61 · see citing works
Kazazić, S., Zhang, H., Schaub, T. M., Emmett, M. R., Hendrickson, C. L., Blakney, G. T., & Marshall, A. G. (2010) · Journal of the American Society for Mass Spectrometry · doi:10.1016/j.jasms.2009.12.016 · Cited by 60 · see citing works
Self-citationdel Álamo, M., & Mateu, M. G. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.10.086 · Cited by 60 · see citing works
Yang, R., Shi, J., Byeon, I. L., Ahn, J., Sheehan, J. H., Meiler, J., Gronenborn, A. M., & Aiken, C. (2012) · Retrovirology · doi:10.1186/1742-4690-9-30 · Cited by 56 · see citing works
The capsid protein of human immunodeficiency virus: intersubunit interactions during virus assembly
Mateu, M. G. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07313.x · Cited by 56 · see citing works
Mortuza, G. B., Dodding, M. P., Goldstone, D. C., Haire, L. F., Stoye, J. P., & Taylor, I. A. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.12.043 · Cited by 56 · see citing works
High-sensitivity mass spectrometry for imaging subunit interactions: hydrogen/deuterium exchange
Lanman, J. K., & Prevelige, P. E. (2004) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2004.03.006 · Cited by 56 · see citing works
Self-citationInsights into virus capsid assembly from non‐covalent mass spectrometry
Morton, V. L., Stockley, P. G., Stonehouse, N. J., & Ashcroft, A. E. (2008) · Mass Spectrometry Reviews · doi:10.1002/mas.20176 · Cited by 55 · see citing works
Yufenyuy, E. L., & Aiken, C. (2013) · Retrovirology · doi:10.1186/1742-4690-10-29 · Cited by 54 · see citing works
Characterization of the In Vitro HIV-1 Capsid Assembly Pathway
Barklis, E., Alfadhli, A., McQuaw, C. M., Yalamuri, S. M., Still, A., Barklis, R. L., Kukull, B., & López, C. S. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.01.058 · Cited by 53 · see citing works
Kang, S., Hawkridge, A. M., Johnson, K. L., Muddiman, D. C., & Prevelige, P. E. (2006) · Journal of Proteome Research · doi:10.1021/pr050356f · Cited by 52 · see citing works
Self-citationJiang, J., Ablan, S. D., Derebail, S. S., Hercík, K., Soheilian, F., Thomas, J. A., Tang, S., HEWLETT, I. K., Nagashima, K., Gorelick, R. J., et al. (2011) · Virology · doi:10.1016/j.virol.2011.09.012 · Cited by 52 · see citing works
HIV Capsid Assembly, Mechanism, and Structure
Chen, B. (2016) · Biochemistry · doi:10.1021/acs.biochem.6b00159 · Cited by 51 · see citing works
Investigation of N-Terminal Domain Charged Residues on the Assembly and Stability of HIV-1 CA
Douglas, C. C., Thomas, D. R., Lanman, J. K., & Prevelige, P. E. (2004) · Biochemistry · doi:10.1021/bi049359g · Cited by 51 · see citing works
Self-citationTang, S., Murakami, T., Cheng, N., Steven, A. C., Freed, E. O., & Levin, J. G. (2003) · Journal of Virology · doi:10.1128/jvi.77.23.12592-12602.2003 · Cited by 52 · see citing works
Novel Amidinating Cross-Linker for Facilitating Analyses of Protein Structures and Interactions
Lauber, M. A., & Reilly, J. P. (2010) · Analytical Chemistry · doi:10.1021/ac101586z · Cited by 51 · see citing works
Purdy, J. G., Flanagan, J. M., Ropson, I. J., Rennoll-Bankert, K. E., & Craven, R. C. (2008) · Journal of Virology · doi:10.1128/jvi.00214-08 · Cited by 50 · see citing works
Hydrogen/Deuterium Exchange Analysis of HIV-1 Capsid Assembly and Maturation
Monroe, E. B., Kang, S., Kyere, S. K., Li, R., & Prevelige, P. E. (2010) · Structure · doi:10.1016/j.str.2010.08.016 · Cited by 49 · see citing works
Self-citationPotluri, S., Yan, A. K., Chou, J. J., Donald, B. R., & Bailey‐Kellogg, C. (2006) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.21091 · Cited by 48 · see citing works
In Vitro Assembly of Retroviruses
Bush, D. L., & Vogt, V. M. (2014) · Annual Review of Virology · doi:10.1146/annurev-virology-031413-085427 · Cited by 48 · see citing works
Dual-acting stapled peptides target both HIV-1 entry and assembly
Zhang, H., Curreli, F., Waheed, A. A., Mercredi, P. Y., Mehta, M., Bhargava, P., Scacalossi, D., Tong, X., Lee, S., Cooper, A., et al. (2013) · Retrovirology · doi:10.1186/1742-4690-10-136 · Cited by 48 · see citing works
VSV-G pseudotyping rescues HIV-1 CA mutations that impair core assembly or stability
Brun, S., Solignat, M., Gay, B., Bernard, É., Chaloin, L., Fenard, D., Devaux, C. A., Chazal, N., & Briant, L. (2008) · Retrovirology · doi:10.1186/1742-4690-5-57 · Cited by 46 · see citing works
Wong, H. C., Shin, R., & Krishna, N. R. (2008) · Biochemistry · doi:10.1021/bi7022128 · Cited by 46 · see citing works
Dimeric Rous Sarcoma Virus Capsid Protein Structure Relevant to Immature Gag Assembly
Nandhagopal, N., Simpson, A. A., Johnson, M. C., Francisco, A. B., Schatz, G. W., Rossmann, M. G., & Vogt, V. M. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.10.034 · Cited by 44 · see citing works
Molecular recognition in the human immunodeficiency virus capsid and antiviral design
Bocanegra, R., Rodríguez‐Huete, A., Fuertes, M. A., del Álamo, M., & Mateu, M. G. (2012) · Virus Research · doi:10.1016/j.virusres.2012.06.016 · Cited by 43 · see citing works
Protease Cleavage Leads to Formation of Mature Trimer Interface in HIV-1 Capsid
Meng, X., Zhao, G., Yufenyuy, E. L., Ke, D., Ning, J., DeLucia, M., Ahn, J., Gronenborn, A. M., Aiken, C., & Zhang, P. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002886 · Cited by 43 · see citing works
Krishna, V., Ayton, G. S., & Voth, G. A. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2009.09.049 · Cited by 42 · see citing works
Frantom, P. A., Zhang, H. M., Emmett, M. R., Marshall, A. G., & Blanchard, J. S. (2009) · Biochemistry · doi:10.1021/bi900851q · Cited by 42 · see citing works
Self-citationSecond-Site Compensatory Mutations of HIV-1 Capsid Mutations
Noviello, C., López, C., Kukull, B., McNett, H., Still, A., Eccles, J., Sloan, R., & Barklis, E. (2011) · Journal of Virology · doi:10.1128/jvi.00099-11 · Cited by 40 · see citing works
Catalysis and Binding of Cyclophilin A with Different HIV-1 Capsid Constructs
Bosco, D. A., & Kern, D. (2004) · Biochemistry · doi:10.1021/bi049841z · Cited by 41 · see citing works
Keller, P. W., Johnson, M. C., & Vogt, V. M. (2008) · Journal of Virology · doi:10.1128/jvi.00213-08 · Cited by 40 · see citing works
New Approaches for Antiviral Targeting of HIV Assembly
Prevelige, P. E. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.03.074 · Cited by 40 · see citing works
Self-citationKang, S., & Prevelige, P. E. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.02.021 · Cited by 39 · see citing works
Self-citationProton-Linked Dimerization of a Retroviral Capsid Protein Initiates Capsid Assembly
Bailey, G. D., Hyun, J., MITRA, A. K., & Kingston, R. L. (2009) · Structure · doi:10.1016/j.str.2009.03.010 · Cited by 38 · see citing works
A Trimer of Dimers Is the Basic Building Block for Human Immunodeficiency Virus-1 Capsid Assembly
Tsiang, M., Niedziela‐Majka, A., Hung, M., Jin, D., Hu, E. Y., Yant, S. R., Samuel, D., Liu, X., & Sakowicz, R. (2012) · Biochemistry · doi:10.1021/bi300052h · Cited by 38 · see citing works
Tong, X., Wren, J. C., & Konermann, L. (2008) · Analytical Chemistry · doi:10.1021/ac702321r · Cited by 38 · see citing works
A Mass Spectrometry View of Stable and Transient Protein Interactions
Budayeva, H. G., & Cristea, I. M. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-06068-2_11 · Cited by 37 · see citing works
The effect of capsid mutations on HIV-1 uncoating
Wacharapornin, P., Lauhakirti, D., & Auewarakul, P. (2006) · Virology · doi:10.1016/j.virol.2006.08.031 · Cited by 37 · see citing works
Protease-Dependent Uncoating of a Complex Retrovirus
Lehmann‐Che, J., Giron, M.-L., Delelis, O., Löchelt, M., Bittoun, P., Tobaly-Tapiero, J., de Thé, H., & Saı̈b, A. (2005) · Journal of Virology · doi:10.1128/jvi.79.14.9244-9253.2005 · Cited by 37 · see citing works
3D Visualization of HIV Virions by Cryoelectron Tomography
Liu, J., Wright, E. R., & Winkler, H. (2010) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(10)83014-9 · Cited by 34 · see citing works
Preparation and characterization of three monoclonal antibodies against HIV-1 p24 capsid protein.
Liu, G. J., Wang, J., Xiao, J. C., Zhao, Z. W., & Zheng, Y. T. (2007) · PubMed · Cited by 36 · see citing works
Phosphorylation of the HIV-1 capsid by MELK triggers uncoating to promote viral cDNA synthesis
Takeuchi, H., Saito, H., Noda, T., Miyamoto, T., Yoshinaga, T., Terahara, K., Ishii, H., Tsunetsugu‐Yokota, Y., & Yamaoka, S. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006441 · Cited by 34 · see citing works
Identification of novel quaternary domain interactions in the Hsp90 chaperone, GRP94
Feixia Chu, C., Maynard, J. C., Chiosis, G., Nicchitta, C. V., & Burlingame, A. L. (2006) · Protein Science · doi:10.1110/ps.052065106 · Cited by 34 · see citing works
- Authors
- Lanman, J., Lam, T. T., Barnes, S., Sakalian, M., Emmett, M. R., Marshall, A. G., & Prevelige, P. E.
- Affiliations
- University of Alabama at Birmingham (US)
- Florida State University (US)
- University of Oklahoma Health Sciences Center (US)
- Corresponding author
- Prevelige, Peter E.
- Venue
- Journal of Molecular Biology
- Publisher
- Elsevier BV
- Published
- 2003-01
- Volume
- 325
- Issue
- 4
- Pages
- 759-772
- ISSN
- 0022-2836 (ISSN-L)
- OpenAlex
- W1968718594
- Cited by
- 206
- References
- 56
- Citations by year
- 2026: 1 · 2023: 1 · 2022: 3 · 2021: 2 · 2020: 3 · 2019: 3 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 6 · 2014: 7 · 2013: 14 · 2012: 8
- FWCI
- 5.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- National High Magnetic Field Laboratory
- National Institutes of Health (5r01gm031683-17)
- National Cancer Institute (T32 CA 09467, T32CA009467)
- National Institute of General Medical Sciences (GM 31683)
- National Institute of Allergy and Infectious Diseases (AI 44626, R01AI044626)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Physical Sciences › Chemistry › Spectroscopy › Mass Spectrometry Techniques and Applications
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Keywords
- HIV-1 capsid protein, intersubunit interactions, amide hydrogen exchange, N-domain, C-domain, subunit interface, chemical crosslinking, supramolecular structure
- MeSH terms
- Amides, Cross-Linking Reagents, Deuterium, Hydrogen, Models, Molecular, Mass Spectrometry, HIV-1, Mutagenesis, Site-Directed, Protein Structure, Tertiary, Dimerization, Protein Structure, Quaternary, Protein Subunits, Capsid Proteins, Macromolecular Substances
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