Allosteric modulation of protein oligomerization: An emerging approach to drug design

Frontiers in Chemistry

Volumn 2, Issue MAR, 2014, Pages

  Gabizon, Ronen ^a,b   Friedler, Assaf ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Allostery; Drug design; HIV 1; Peptides; Protein oligomerization; Shiftides

Indexed keywords

EID: 84987615742     PISSN: None     EISSN: 22962646     Source Type: Journal    
DOI: 10.3389/fchem.2014.00009     Document Type: Review

References (173)

1. Anastasiou, D., Yu, Y., Israelsen, W. J., Jiang, J., Boxer, M. B., Hong, B. S., et al. (2012). Pyruvate kinase M2 activators promote tetramer formation and suppress tumorigenesis. Nat. Chem. Biol. 8, 1008. doi: 10.1038/nchembio1212-1008b
2. Armon-Omer, A., Levin, A., Hayouka, Z., Butz, K., Hoppe-Seyler, F., Loya, S., et al. (2008). Correlation between shiftide activity and HIV-1 integrase inhibition by a peptide selected from a combinatorial library. J. Mol. Biol. 376, 971-982. doi: 10.1016/j.jmb.2007.11.095
3. Azdad, K., Gall, D., Woods, A. S., Ledent, C., Ferre, S., and Schiffmann, S. N. (2008). Dopamine D2 and Adenosine A2A Receptors Regulate NMDA-Mediated Excitation in Accumbens Neurons Through A2A-D2 Receptor Heteromerization. Neuropsychopharmacology 34, 972-986. doi: 10.1038/npp.2008.144
4. Bedrood, S., Li, Y., Isas, J. M., Hegde, B. G., Baxa, U., Haworth, I. S., et al. (2012). Fibril structure of human islet amyloid polypeptide. J. Biol. Chem. 287, 5235-5241. doi: 10.1074/jbc.M111.327817
5. Belluti, F., Rampa, A., Gobbi, S., and Bisi, A. (2013). Small-molecule inhibitors/modulators of amyloid-β peptide aggregation and toxicity for the treatment of Alzheimer's disease: a patent review (2010-2012). Expert Opin. Ther. Pat. 23, 581-596. doi: 10.1517/13543776.2013.772983
6. Blair, W. S., Pickford, C., Irving, S. L., Brown, D. G., Anderson, M., Bazin, R., et al. (2010). HIV Capsid is a Tractable Target for Small Molecule Therapeutic Intervention. PLoS Pathog. 6:e1001220. doi: 10.1371/journal.ppat.1001220
7. Bocanegra, R., Nevot, M., Doménech, R., López, I., Abián, O., Rodríguez-Huete, A., et al. (2011). Rationally designed interfacial peptides are efficient in vitro inhibitors of HIV-1 capsid assembly with antiviral activity. PLoS ONE 6:e23877. doi: 10.1371/journal.pone.0023877
8. Bonache, M.-C., Chamorro, C., Velázquez, S., De Clercq, E., Balzarini, J., Barrios, F. R., et al. (2005). Improving the antiviral efficacy and selectivity of HIV-1 reverse transcriptase inhibitor TSAO-T by the introduction of functional groups at the N-3 position. J. Med. Chem. 48, 6653-6660. doi: 10.1021/jm050437n
9. Bottcher, B., Wynne, S. A., and Crowther, R. A. (1997). Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386, 88-91. doi: 10.1038/386088a0
10. Cabo-Bilbao, A., Spinelli, S., Sot, B., Agirre, J., Mechaly, A. E., Muga, A., et al. (2006). Crystal structure of the temperature-sensitive and allosteric-defective chaperonin GroELE461K. J. Struct. Biol. 155, 482-492. doi: 10.1016/j.jsb.2006.06.008
11. Calebiro, D., Rieken, F., Wagner, J., Sungkaworn, T., Zabel, U., Borzi, A., et al. (2013). Single-molecule analysis of fluorescently labeled G-protein-coupled receptors reveals complexes with distinct dynamics and organization. Proc. Natl. Acad. Sci. U.S.A. 110, 743-748. doi: 10.1073/pnas.1205798110
12. Camarasa, M.-J., Velázquez, S., San-Félix, A., Pérez-Pérez, M.-J., and Gago, F. (2006). Dimerization inhibitors of HIV-1 reverse transcriptase, protease and integrase: a single mode of inhibition for the three HIV enzymes? Antiviral Res. 71, 260-267. doi: 10.1016/j.antiviral.2006.05.021
13. Chen, J. C., Krucinski, J., Miercke, L. J., Finer-Moore, J. S., Tang, A. H., Leavitt, A. D., et al. (2000). Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains: a model for viral DNA binding. Proc. Natl. Acad. Sci. U.S.A. 97, 8233-8238. doi: 10.1073/pnas.150220297
14. Chene, P. (2001). The role of tetramerization in p53 function. Oncogene 20, 2611-2617. doi: 10.1038/sj.onc.1204373
15. Cherepanov, P., Ambrosio, A. L. B., Rahman, S., Ellenberger, T., and Engelman, A. (2005). Structural basis for the recognition between HIV-1 integrase and transcriptional coactivator p75. Proc. Natl. Acad. Sci. U.S.A. 102, 17308-17313. doi: 10.1073/pnas.0506924102
16. Cherepanov, P., Maertens, G., Proost, P., Devreese, B., Van Beeumen, J., Engelborghs, Y., et al. (2003). HIV-1 Integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J. Biol. Chem. 278, 372-381. doi: 10.1074/jbc.M209278200
17. Christ, F., and Debyser, Z. (2013). The LEDGF/p75 integrase interaction, a novel target for anti-HIV therapy. Virology 435, 102-109. doi: 10.1016/j.virol.2012.09.033
18. Christ, F., Shaw, S., Demeulemeester, J., Desimmie, B. A., Marchand, A., Butler, S., et al. (2012). Small-molecule inhibitors of the LEDGF/p75 binding site of integrase block HIV replication and modulate integrase multimerization. Antimicrob. Agents Chemother. 56, 4365-4374. doi: 10.1128/AAC.00717-12
19. Christ, F., Voet, A., Marchand, A., Nicolet, S., Desimmie, B. A., Marchand, D., et al. (2010). Rational design of small-molecule inhibitors of the LEDGF/p75-integrase interaction and HIV replication. Nat. Chem. Biol. 6, 442-448. doi: 10.1038/nchembio.370
20. Clore, G. M., Omichinski, J. G., Sakaguchi, K., Zambrano, N., Sakamoto, H., Appella, E., et al. (1994). High-resolution structure of the oligomerization domain of p53 by multidimensional NMR. Science 265, 386-391. doi: 10.1126/science.8023159
21. Craig, R., and Woodhead, J. L. (2006). Structure and function of myosin filaments. Curr. Opin. Struct. Biol. 16, 204-212. doi: 10.1016/j.sbi.2006.03.006
22. Cramer, P., Bushnell, D. A., and Kornberg, R. D. (2001). Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science 292, 1863-1876. doi: 10.1126/science.1059493
23. Delelis, O., Carayon, K., Saïb, A., Deprez, E., and Mouscadet, J.-F. (2008). Integrase and integration: biochemical activities of HIV-1 integrase. Retrovirology 5, 114. doi: 10.1186/1742-4690-5-114
24. Delphin, C., Huang, K. P., Scotto, C., Chapel, A., Vincon, M., Chambaz, E., et al. (1997). The in vitro phosphorylation of p53 by calcium-dependent protein kinase C-characterization of a protein kinase C-binding site on p53. Eur. J. Biochem. 245, 684-692. doi: 10.1111/j.1432-1033.1997.t01-1-00684.x
25. De Meyts, P. (2008). The insulin receptor: a prototype for dimeric, allosteric membrane receptors? Trends Biochem. Sci. 33, 376-384. doi: 10.1016/j.tibs.2008.06.003
26. Depollier, J., Hourdou, M.-L., Aldrian-Herrada, G., Rothwell, P., Restle, T., and Divita, G. (2005). Insight into the mechanism of a peptide inhibitor of HIV reverse transcriptase dimerization. Biochemistry 44, 1909-1918. doi: 10.1021/bi0484264
27. Deprez, E., Tauc, P., Leh, H., Mouscadet, J.-F., Auclair, C., Hawkins, M. E., et al. (2001). DNA binding induces dissociation of the multimeric form of HIV-1 integrase: a time-resolved fluorescence anisotropy study. Proc. Natl. Acad. Sci. U.S.A. 98, 10090-10095. doi: 10.1073/pnas.181024498
28. Deres, K., Schröder, C. H., Paessens, A., Goldmann, S., Hacker, H. J., Weber, O., et al. (2003). Inhibition of hepatitis B virus replication by drug-induced depletion of nucleocapsids. Science 299, 893-896. doi: 10.1126/science.1077215
29. Derry, W. B., Wilson, L., and Jordan, M. A. (1995). Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry 34, 2203-2211. doi: 10.1021/bi00007a014
30. Divita, G., Restle, T., Goody, R. S., Chermann, J. C., and Baillon, J. G. (1994). Inhibition of human immunodeficiency virus type 1 reverse transcriptase dimerization using synthetic peptides derived from the connection domain. J. Biol. Chem. 269, 13080-13083.
31. Dong, Q.-G., Zhang, Y., Wang, M.-S., Feng, J., Zhang, H.-H., Wu, Y.-G., et al. (2012). Improvement of enzymatic stability and intestinal permeability of deuterohemin-peptide conjugates by specific multi-site N-methylation. Amino Acids 43, 2431-2441. doi: 10.1007/s00726-012-1322-y
32. Eisenstein, E., and Beckett, D. (1999). Dimerization of the Escherichia coli biotin repressor: corepressor function in protein assembly. Biochemistry 38, 13077-13084. doi: 10.1021/bi991241q
33. Emiliani, S., Mousnier, A., Busschots, K., Maroun, M., Van Maele, B., Tempé, D., et al. (2005). Integrase mutants defective for interaction with LEDGF/p75 are impaired in chromosome tethering and HIV-1 replication. J. Biol. Chem. 280, 25517-25523. doi: 10.1074/jbc.M501378200
34. Engelman, A., Kessl, J. J., and Kvaratskhelia, M. (2013). Allosteric inhibition of HIV-1 integrase activity. Curr. Opin. Chem. Biol. 17, 339-345. doi: 10.1016/j.cbpa.2013.04.010
35. Engelman, A., Mizuuchi, K., and Craigie, R. (1991). HIV-1 DNA integration: Mechanism of viral DNA cleavage and DNA strand transfer. Cell 67, 1211-1221. doi: 10.1016/0092-8674(91)90297-C
36. Fader, L. D., Malenfant, E., Parisien, M., Carson, R., Bilodeau, F., Landry, S., et al. (in press). Discovery of BI 224436, a Noncatalytic Site Integrase Inhibitor (NCINI) of HIV-1. ACS Med. Chem. Lett. doi: 10.1021/ml500002n
37. Feng, L., Sharma, A., Slaughter, A., Jena, N., Koh, Y., Shkriabai, N., et al. (2013). The A128T resistance mutation reveals aberrant protein multimerization as the primary mechanism of action of allosteric HIV-1 integrase inhibitors. J. Biol. Chem. 288, 15813-15820. doi: 10.1074/jbc.M112.443390
38. Fermi, G., Perutz, M. F., Shaanan, B., and Fourme, R. (1984). The crystal structure of human deoxyhaemoglobin at 1.74 Å resolution. J. Mol. Biol. 175, 159-174. doi: 10.1016/0022-2836(84)90472-8
39. Fernandez-Fernandez, M. R., Rutherford, T. J., and Fersht, A. R. (2008). Members of the S100 family bind p53 in two distinct ways. Protein Sci. 17, 1663-1670. doi: 10.1110/ps.035527.108
40. Fernandez-Fernandez, M. R., Veprintsev, D. B., and Fersht, A. R. (2005). Proteins of the S100 family regulate the oligomerization of p53 tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 102, 4735-4740. doi: 10.1073/pnas.0501459102
41. Ferré, S., Navarro, G., Casadó, V., Cortés, A., Mallol, J., Canela, E. I., et al. (2010). "Chapter 2-G protein-coupled receptor heteromers as new targets for drug development, " in Membrane Proteins as Drug Targets. Progress in molecular biology and translational science, ed C. A. Lunn (Waltham, MA: Academic Press), 41-52. doi: 10.1016/S1877-1173(10)91002-8
42. Gabizon, R., Brandt, T., Sukenik, S., Lahav, N., Lebendiker, M., Shalev, D. E., et al. (2012). Specific recognition of p53 tetramers by peptides derived from p53 interacting proteins. PLoS ONE 7:e38060. doi: 10.1371/journal.pone.0038060
43. Gabizon, R., Mor, M., Rosenberg, M. M., Britan, L., Hayouka, Z., Kotler, M., et al. (2008). Using peptides to study the interaction between the p53 tetramerization domain and HIV-1 Tat. Biopolymers 90, 105-116. doi: 10.1002/bip.20919
44. Gaglia, G., Guan, Y., Shah, J. V., and Lahav, G. (2013). Activation and control of p53 tetramerization in individual living cells. Proc. Natl. Acad. Sci. U.S.A. 110, 15497-15501. doi: 10.1073/pnas.1311126110
45. Gamble, T. R., Yoo, S., Vajdos, F. F., von Schwedler, U. K., Worthylake, D. K., Wang, H., et al. (1997). Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278, 849-853. doi: 10.1126/science.278.5339.849
46. Gilbert, B. J. (2013). The role of amyloid β in the pathogenesis of Alzheimer's disease. J. Clin. Pathol. 66, 362-366. doi: 10.1136/jclinpath-2013-201515
47. Gomez, R., Jolly, S. J., Williams, T., Vacca, J. P., Torrent, M., McGaughey, G., et al. (2011). Design and synthesis of conformationally constrained inhibitors of non-nucleoside reverse transcriptase. J. Med. Chem. 54, 7920-7933. doi: 10.1021/jm2010173
48. Goodsell, D. S., and Olson, A. J. (2000). Structual symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29, 105-153. doi: 10.1146/annurev.biophys.29.1.105
49. Gordo, S., Martos, V., Santos, E., Menendez, M., Bo, C., Giralt, E., et al. (2008). Stability and structural recovery of the tetramerization domain of p53-R337H mutant induced by a designed templating ligand. Proc. Natl. Acad. Sci. U.S.A. 105, 16426-16431. doi: 10.1073/pnas.0805658105
50. Gordo, S., Martos, V., Vilaseca, M., Menéndez, M., de Mendoza, J., and Giralt, E. (2011). On the role of flexibility in protein-ligand interactions: the example of p53 tetramerization domain. Chem. Asian J. 6, 1463-1469. doi: 10.1002/asia.201000938
51. Gotte, G., Mahmoud Helmy, A., Ercole, C., Spadaccini, R., Laurents, D. V., Donadelli, M., et al. (2012). Double domain swapping in bovine seminal RNase: formation of distinct N-and C-swapped Tetramers and multimers with increasing biological activities. PLoS ONE 7:e46804. doi: 10.1371/journal.pone.0046804
52. Gotz, C., Scholtes, P., Prowald, A., Schuster, N., Nastainczyk, W., and Montenarh, M. (1999). Protein kinase CK2 interacts with a multi-protein binding domain of p53. Mol. Cell. Biochem. 191, 111-120. doi: 10.1023/A:1006886727248
53. Goudreau, N., Coulombe, R., Faucher, A.-M., Grand-Maître, C., Lacoste, J.-E., Lemke, C. T., et al. (2013). Monitoring binding of HIV-1 capsid assembly inhibitors using 19F ligand-and 15N protein-based NMR and X-ray crystallography: early hit validation of a benzodiazepine series. ChemMedChem 8, 405-414. doi: 10.1002/cmdc.201200580
54. Graves, B., Thompson, T., Xia, M., Janson, C., Lukacs, C., Deo, D., et al. (2012). Activation of the p53 pathway by small-molecule-induced MDM2 and MDMX dimerization. Proc. Natl. Acad. Sci. U.S.A. 109, 11788-11793. doi: 10.1073/pnas.1203789109
55. Gray, T. A., Murray, E., Nowicki, M. W., Remnant, L., Scherl, A., Muller, P., et al. (2013). Development of a fluorescent monoclonal antibody-based assay to measure the allosteric effects of synthetic peptides on self-oligomerization of AGR2 protein. Protein Sci. 22, 1266-1278. doi: 10.1002/pro.2299
56. Grossman, S. R. (2001). p300/CBP/p53 interaction and regulation of the p53 response. Eur. J. Biochem. 268, 2773-2778. doi: 10.1046/j.1432-1327.2001.02226.x
57. Groulx, N., McGuire, H., Laprade, R., Schwartz, J.-L., and Blunck, R. (2011). Single Molecule fluorescence study of the Bacillus thuringiensis toxin Cry1Aa reveals tetramerization. J. Biol. Chem. 286, 42274-42282. doi: 10.1074/jbc.M111.296103
58. Guiot, E., Carayon, K., Delelis, O., Simon, F., Tauc, P., Zubin, E., et al. (2006). Relationship between the oligomeric status of HIV-1 integrase on DNA and enzymatic activity. J. Biol. Chem. 281, 22707-22719. doi: 10.1074/jbc.M602198200
59. Guo, W., Shi, L., Filizola, M., Weinstein, H., and Javitch, J. A. (2005). Crosstalk in G protein-coupled receptors: changes at the transmembrane homodimer interface determine activation. Proc. Natl. Acad. Sci. U.S.A. 102, 17495-17500. doi: 10.1073/pnas.0508950102
60. Hayouka, Z., Hurevich, M., Levin, A., Benyamini, H., Iosub, A., Maes, M., et al. (2010b). Cyclic peptide inhibitors of HIV-1 integrase derived from the LEDGF/p75 protein. Bioorg. Med. Chem. 18, 8388-8395. doi: 10.1016/j.bmc.2010.09.046
61. Hayouka, Z., Levin, A., Maes, M., Hadas, E., Shalev, D. E., Volsky, D. J., et al. (2010a). Mechanism of action of the HIV-1 integrase inhibitory peptide LEDGF 361-370. Biochem. Biophys. Res. Commun. 394, 260-265. doi: 10.1016/j.bbrc.2010.02.100
62. Hayouka, Z., Rosenbluh, J., Levin, A., Loya, S., Lebendiker, M., Veprintsev, D., et al. (2007). Inhibiting HIV-1 integrase by shifting its oligomerization equilibrium. Proc. Natl. Acad. Sci. U.S.A. 104, 8316-8321. doi: 10.1073/pnas.0700781104
63. Hayouka, Z., Rosenbluh, J., Levin, A., Maes, M., Loyter, A., and Friedler, A. (2008). Peptides derived from HIV-1 Rev inhibit HIV-1 integrase in a shiftide mechanism. Biopolymers 90, 481-487. doi: 10.1002/bip.20930
64. He, M. M., Smith, A. S., Oslob, J. D., Flanagan, W. M., Braisted, A. C., Whitty, A., et al. (2005). Small-Molecule Inhibition of TNF-a. Science 310, 1022-1025. doi: 10.1126/science.1116304
65. Jaffe, E. K. (2005). Morpheeins-a new structural paradigm for allosteric regulation. Trends Biochem. Sci. 30, 490-497. doi: 10.1016/j.tibs.2005.07.003
66. Jaffe, E. K., and Lawrence, S. H. (2012). Allostery and the dynamic oligomerization of porphobilinogen synthase. Arch. Biochem. Biophys. 519, 144-153. doi: 10.1016/j.abb.2011.10.010
67. Jeffrey, P. D., Gorina, S., and Pavletich, N. P. (1995). Crystal structure of the tetramerization domain of the p53 tumor suppressor at 1.7 angstroms. Science 267, 1498-1502. doi: 10.1126/science.7878469
68. Jones, K. A., Borowsky, B., Tamm, J. A., Craig, D. A., Durkin, M. M., Dai, M., et al. (1998). GABAB receptors function as a heteromeric assembly of the subunits GABABR1 and GABABR2. Nature 396, 674-679. doi: 10.1038/25348
69. Jones, S., and Thornton, J. M. (1996). Principles of protein-protein interactions. Proc. Natl. Acad. Sci. U.S.A. 93, 13-20. doi: 10.1073/pnas.93.1.13
70. Jordan, M. A., Toso, R. J., Thrower, D., and Wilson, L. (1993). Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Natl. Acad. Sci. U.S.A. 90, 9552-9556. doi: 10.1073/pnas.90.20.9552
71. Jurado, K. A., Wang, H., Slaughter, A., Feng, L., Kessl, J. J., Koh, Y., et al. (2013). Allosteric integrase inhibitor potency is determined through the inhibition of HIV-1 particle maturation. Proc. Natl. Acad. Sci. U.S.A. 110, 8690-8695. doi: 10.1073/pnas.1300703110
72. Kamada, R., Yoshino, W., Nomura, T., Chuman, Y., Imagawa, T., Suzuki, T., et al. (2010). Enhancement of transcriptional activity of mutant p53 tumor suppressor protein through stabilization of tetramer formation by calix[6]arene derivatives. Bioorg. Med. Chem. Lett. 20, 4412-4415. doi: 10.1016/j.bmcl.2010.06.053
73. Katen, S. P., Tan, Z., Chirapu, S. R., Finn, M. G., and Zlotnick, A. (2013). Assembly-directed antivirals differentially bind quasiequivalent pockets to modify hepatitis B virus capsid tertiary and quaternary structure. Structure 21, 1406-1416. doi: 10.1016/j.str.2013.06.013
74. Kelly, B. N., Kyere, S., Kinde, I., Tang, C., Howard, B. R., Robinson, H., et al. (2007). Structure of the antiviral assembly inhibitor CAP-1 complex with the HIV-1 CA protein. J. Mol. Biol. 373, 355-366. doi: 10.1016/j.jmb.2007.07.070
75. Kessl, J. J., Eidahl, J. O., Shkriabai, N., Zhao, Z., McKee, C. J., Hess, S., et al. (2009). An allosteric mechanism for inhibiting HIV-1 integrase with a small molecule. Mol. Pharmacol. 76, 824-832. doi: 10.1124/mol.109.058883
76. Kim, J., and Raushel, F. M. (2001). Allosteric control of the oligomerization of carbamoyl phosphate synthetase from Escherichia coli. Biochemistry 40, 11030-11036. doi: 10.1021/bi011121u
77. Koh, Y., Matsumi, S., Das, D., Amano, M., Davis, D. A., Li, J., et al. (2007). Potent Inhibition of HIV-1 replication by novel non-peptidyl small molecule inhibitors of protease dimerization. J. Biol. Chem. 282, 28709-28720. doi: 10.1074/jbc.M703938200
78. Krojer, T., Sawa, J., Huber, R., and Clausen, T. (2010). HtrA proteases have a conserved activation mechanism that can be triggered by distinct molecular cues. Nat. Struct. Mol. Biol. 17, 844-852. doi: 10.1038/nsmb.1840
79. Lamorte, L., Titolo, S., Lemke, C. T., Goudreau, N., Mercier, J.-F., Wardrop, E., et al. (2013). Discovery of novel small-molecule HIV-1 replication inhibitors that stabilize capsid complexes. Antimicrob. Agents Chemother. 57, 4622-4631. doi: 10.1128/AAC.00985-13
80. Lange-Savage, G., Berchtold, H., Liesum, A., Budt, K.-H., Peyman, A., Knolle, J., et al. (1997). Structure of HOE/BAY 793 complexed to human immunodeficiency virus (HIV-1) protease in two different crystal forms structure/function relationship and influence of crystal packing. Eur. J. Biochem. 248, 313-322. doi: 10.1111/j.1432-1033.1997.00313.x
81. Lawrence, S. H., Ramirez, U. D., Tang, L., Fazliyez, F., Kundrat, L., Markham, G. D., et al. (2008). Shape shifting leads to small-molecule allosteric drug discovery. Chem. Biol. 15, 586-596. doi: 10.1016/j.chembiol.2008.04.012
82. Lee, W., Harvey, T. S., Yin, Y., Yau, P., Litchfield, D., and Arrowsmith, C. H. (1994). Solution structure of the tetrameric minimum transforming domain of p53. Nat. Struct. Mol. Biol. 1, 877-890. doi: 10.1038/nsb1294-877
83. Lemke, C. T., Titolo, S., Goudreau, N., Faucher, A.-M., Mason, S. W., and Bonneau, P. (2013). A novel inhibitor-binding site on the HIV-1 capsid N-terminal domain leads to improved crystallization via compound-mediated dimerization. Acta Crystallogr. Sect. D 69, 1115-1123. doi: 10.1107/S0907444913006409
84. Lemke, C. T., Titolo, S., von Schwedler, U., Goudreau, N., Mercier, J.-F., Wardrop, E., et al. (2012). Distinct effects of two HIV-1 capsid assembly inhibitor families that bind the same site within the N-terminal domain of the viral CA protein. J. Virol. 86, 6643-6655. doi: 10.1128/JVI.00493-12
85. Leu, J. I.-J., Dumont, P., Hafey, M., Murphy, M. E., and George, D. L. (2004). Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat. Cell Biol. 6, 443-450. doi: 10.1038/ncb1123
86. Levine, A. J. (1997). p53, the cellular gatekeeper for growth and division. Cell 88, 323-331. doi: 10.1016/S0092-8674(00)81871-1
87. Li, M., and Craigie, R. (2005). Processing of viral DNA ends channels the HIV-1 integration reaction to concerted integration. J. Biol. Chem. 280, 29334-29339. doi: 10.1074/jbc.M505367200
88. Li, M., Mizuuchi, M., Burke, T. R., and Craigie, R. (2006). Retroviral DNA integration: reaction pathway and critical intermediates. EMBO J. 25, 1295-1304. doi: 10.1038/sj.emboj.7601005
89. Li, X., Zhang, Y.-K., Liu, Y., Ding, C. Z., Li, Q., Zhou, Y. et al. (2010). Synthesis and evaluation of novel a-amino cyclic boronates as inhibitors of HCV NS3 protease. Bioorg. Med. Chem. Lett. 20, 3550-3556. doi: 10.1016/j.bmcl.2010.04.129
90. Longo, F., Marchetti, M. A., Castagnoli, L., Battaglia, P. A., and Gigliani, F. (1995). A novel approach to protein-protein interaction: complex formation between the P53 tumor suppressor and the HIV tat proteins. Biochem. Biophys. Res. Commun. 206, 326-334. doi: 10.1006/bbrc.1995.1045
91. Löwe, J., Li, H., Downing, K. H., and Nogales, E. (2001). Refined structure of αβ-tubulin at 3.5 Å resolution. J. Mol. Biol. 313, 1045-1057. doi: 10.1006/jmbi.2001.5077
92. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997). Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 389, 251-260. doi: 10.1038/38444
93. Maertens, G., Cherepanov, P., Pluymers, W., Busschots, K., De Clercq, E., Debyser, Z., et al. (2003). LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J. Biol. Chem. 278, 33528-33539. doi: 10.1074/jbc.M303594200
94. Maes, M., Levin, A., Hayouka, Z., Shalev, D. E., Loyter, A., and Friedler, A. (2009). Peptide inhibitors of HIV-1 integrase: from mechanistic studies to improved lead compounds. Bioorg. Med. Chem. 17, 7635-7642. doi: 10.1016/j.bmc.2009.09.053
95. Maes, M., Loyter, A., and Friedler, A. (2012). Peptides that inhibit HIV-1 integrase by blocking its protein-protein interactions. FEBS J. 279, 2795-2809. doi: 10.1111/j.1742-4658.2012.08680.x
96. Marinho-Carvalho, M. M., Zancan, P., and Sola-Penna, M. (2006). Modulation of 6-phosphofructo-1-kinase oligomeric equilibrium by calmodulin: formation of active dimmers. Mol. Genet. Metab. 87, 253-261. doi: 10.1016/j.ymgme.2005.11.002
97. Maroun, R. G., Gayet, S., Benleulmi, M. S., Porumb, H., Zargarian, L., Merad, H., et al. (2001). Peptide inhibitors of HIV-1 integrase dissociate the enzyme oligomers. Biochemistry 40, 13840-13848. doi: 10.1021/bi011328n
98. Martinell, M., Salvatella, X., Fernández-Carneado, J., Gordo, S., Feliz, M., Menéndez, M., et al. (2006). Synthetic ligands able to interact with the p53 tetramerization domain. Towards understanding a protein surface recognition event. Chembiochem 7, 1105-1113. doi: 10.1002/cbic.200500555
99. Mateu, M. G. (2013). Assembly, stability and dynamics of virus capsids. Arch. Biochem. Biophys. 531, 65-79. doi: 10.1016/j.abb.2012.10.015
100. Mateu, M. G., and Fersht, A. R. (1998). Nine hydrophobic side chains are key determinants of the thermodynamic stability and oligomerization status of tumour suppressor p53 tetramerization domain. EMBO J. 17, 2748-2758. doi: 10.1093/emboj/17.10.2748
101. Menendez, D., Inga, A., and Resnick, M. A. (2009). The expanding universe of p53 targets. Nat. Rev. Cancer 9, 724-737. doi: 10.1038/nrc2730
102. Messiaen, P., Wensing, A. M. J., Fun, A., Nijhuis, M., Brusselaers, N., and Vandekerckhove, L. (2013). Clinical use of HIV integrase inhibitors: a systematic review and meta-analysis. PLoS ONE 8:e52562. doi: 10.1371/journal.pone.0052562
103. Michael, D., and Oren, M. (2002). The p53 and Mdm2 families in cancer. Curr. Opin. Genet. Dev. 12, 53-59. doi: 10.1016/S0959-437X(01)00264-7
104. Molineux, I. J., and Panja, D. (2013). Popping the cork: mechanisms of phage genome ejection. Nat. Rev. Microbiol. 11, 194-204. doi: 10.1038/nrmicro2988
105. Mora, P., Rubio, V., and Cervera, J. (2002). Mechanism of oligomerization of Escherichia coli carbamoyl phosphate synthetase and modulation by the allosteric effectors. A site-directed mutagenesis study. FEBS Lett. 511, 6-10. doi: 10.1016/S0014-5793(01)03246-X
106. Moretto, A., Crisma, M., Kaptein, B., Broxterman, Q. B., and Toniolo, C. (2006). N-methylation of N(alpha)-acylated, fully C(alpha)-methylated, linear, folded peptides: synthetic and conformational aspects. Biopolymers 84, 553-565. doi: 10.1002/bip.20560
107. Morris, M. C., Robert-Hebmann, V., Chaloin, L., Mery, J., Heitz, F., Devaux, C., et al. (1999). A new potent HIV-1 reverse transcriptase inhibitor: a synthetic peptide derived from the interface subunit domains. J. Biol. Chem. 274, 24941-24946. doi: 10.1074/jbc.274.35.24941
108. Mouscadet, J.-F., Delelis, O., Marcelin, A.-G., and Tchertanov, L. (2010). Resistance to HIV-1 integrase inhibitors: a structural perspective. Drug Resist. Updat. 13, 139-150. doi: 10.1016/j.drup.2010.05.001
109. Murugan, S., and Hung, H.-C. (2012). Biophysical characterization of the dimer and tetramer interface interactions of the human cytosolic malic enzyme. PLoS ONE 7:e50143. doi: 10.1371/journal.pone.0050143
110. Nam, H.-J., Gurda, B. L., McKenna, R., Potter, M., Byrne, B., Salganik, M., et al. (2011). Structural studies of adeno-associated virus serotype 8 capsid transitions associated with endosomal trafficking. J. Virol. 85, 11791-11799. doi: 10.1128/JVI.05305-11
111. Nomura, T., Kamada, R., Ito, I., Chuman, Y., Shimohigashi, Y., and Sakaguchi, K. (2009). Oxidation of methionine residue at hydrophobic core destabilizes p53 tetrameric structure. Biopolymers 91, 78-84. doi: 10.1002/bip.21084
112. Noviello, C. M., López, C. S., Kukull, B., McNett, H., Still, A., Eccles, J., et al. (2011). Second-site compensatory mutations of HIV-1 capsid mutations. J. Virol. 85, 4730-4738. doi: 10.1128/JVI.00099-11
113. Ono, S. (2007). "Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics, " in International Review of Cytology, Vol. 258, ed Kwang W. Jeon (Waltham, MA: Academic Press), 1-82.
114. Paredes, J. M., Casares, S., Ruedas-Rama, M. J., Fernandez, E., Castello, F., Varela, L., et al. (2012). Early amyloidogenic oligomerization studied through fluorescence lifetime correlation spectroscopy. Int. J. Mol. Sci. 13, 9400-9418. doi: 10.3390/ijms13089400
115. Pietsch, E. C., Perchiniak, E., Canutescu, A. A., Wang, G., Dunbrack, R. L., and Murphy, M. E. (2008). Oligomerization of BAK by p53 utilizes conserved residues of the p53 DNA binding domain. J. Biol. Chem. 283, 21294-21304. doi: 10.1074/jbc.M710539200
116. Plevka, P., Perera, R., Yap, M. L., Cardosa, J., Kuhn, R. J., and Rossmann, M. G. (2013). Structure of human enterovirus 71 in complex with a capsid-binding inhibitor. Proc. Natl. Acad. Sci. U.S.A. 110, 5463-5467. doi: 10.1073/pnas.1222379110
117. Pornillos, O., Ganser-Pornillos, B. K., Kelly, B. N., Hua, Y., Whitby, F. G., Stout, C. D., et al. (2009). X-Ray structures of the hexameric building block of the HIV capsid. Cell 137, 1282-1292. doi: 10.1016/j.cell.2009.04.063
118. Rajagopalan, S., Jaulent, A. M., Wells, M., Veprintsev, D. B., and Fersht, A. R. (2008). 14-3-3 activation of DNA binding of p53 by enhancing its association into tetramers. Nucleic Acids Res. 36, 5983-5991. doi: 10.1093/nar/gkn598
119. Rodríguez-Barrios, F., Pérez, C., Lobatón, E., Velázquez, S., Chamorro, C., San-Félix, A., et al. (2001). Identification of a putative binding site for [2', 5'-Bis-O-(tert-butyldimethylsilyl)-β-d-ribofuranosyl]-3'-spiro-5"-(4"-amino-1", 2"-oxathiole-2", 2"-dioxide)thymine (TSAO) Derivatives at the p51-p66 Interface of HIV-1 reverse transcriptase. J. Med. Chem. 44, 1853-1865. doi: 10.1021/jm001095i
120. Ronen, D., Rosenberg, M. M., Shalev, D. E., Rosenberg, M., Rotem, S., Friedler, A., et al. (2010). The positively charged region of the myosin IIC Non-helical tailpiece promotes filament assembly. J. Biol. Chem. 285, 7079-7086. doi: 10.1074/jbc.M109.049221
121. Rosenbluh, J., Hayouka, Z., Loya, S., Levin, A., Armon-Omer, A., Britan, E., et al. (2007). Interaction between HIV-1 Rev and integrase proteins: a basis for the development of anti-HIV peptides. J. Biol. Chem. 282, 15743-15753. doi: 10.1074/jbc.M609864200
122. Ryan, K. M., Phillips, A. C., and Vousden, K. H. (2001). Regulation and function of the p53 tumor suppressor protein. Curr. Opin. Cell Biol. 13, 332-337. doi: 10.1016/S0955-0674(00)00216-7
123. Salvatella, X. (2013). "Chapter four-structural aspects of amyloid formation, " in Oligomerization in Health and Disease. Progress in molecular biology and translational science, eds J. Giraldo and F. Ciruela (Waltham, MA: Academic Press), 73-101. doi: 10.1016/B978-0-12-386931-9.00004-0
124. Salvatella, X., Martinell, M., Gairí, M., Mateu, M. G., Feliz, M., Hamilton, A. D., et al. (2004). A tetraguanidinium ligand binds to the surface of the tetramerization domain of protein P53. Angew. Chemie Int. Ed. 43, 196-198. doi: 10.1002/anie.200352115
125. Sapienza, P. J., Rosenberg, J. M., and Jen-Jacobson, L. (2007). Structural and thermodynamic basis for enhanced dna binding by a promiscuous mutant EcoRI endonuclease. Structure 15, 1368-1382. doi: 10.1016/j.str.2007.09.014
126. Sato, T., Kienlen-Campard, P., Ahmed, M., Liu, W., Li, H., Elliott, J. I., et al. (2006). Inhibitors of amyloid toxicity based on β-sheet packing of Aβ 40 and Aβ 42. Biochemistry 45, 5503-5516. doi: 10.1021/bi052485f
127. Selwood, T., and Jaffe, E. K. (2012). Dynamic dissociating homo-oligomers and the control of protein function. Arch. Biochem. Biophys. 519, 131-143. doi: 10.1016/j.abb.2011.11.020
128. Selwood, T., Tang, L., Lawrence, S. H., Anokhina, Y., and Jaffe, E. K. (2008). Kinetics and thermodynamics of the interchange of the morpheein forms of human porphobilinogen synthase. Biochemistry 47, 3245-3257. doi: 10.1021/bi702113z
129. Semenova, G., and Chernoff, J. (2012). PKM2 enters the morpheein academy. Mol. Cell 45, 583-584. doi: 10.1016/j.molcel.2012.02.014
130. Serrao, E., Odde, S., Ramkumar, K., and Neamati, N. (2009). Raltegravir, elvitegravir, and metoogravir: the birth of "me-too" HIV-1 integrase inhibitors. Retrovirology 6, 25. doi: 10.1186/1742-4690-6-25
131. Sharma, M., Yi, M., Dong, H., Qin, H., Peterson, E., Busath, D. D., et al. (2010). Insight into the mechanism of the influenza a proton channel from a structure in a lipid bilayer. Science 330, 509-512. doi: 10.1126/science.1191750
132. Sherman, M. P., and Greene, W. C. (2002). Slipping through the door: HIV entry into the nucleus. Microbes Infect. 4, 67-73. doi: 10.1016/S1286-4579(01)01511-8
133. Shi, J., Zhou, J., Shah, V. B., Aiken, C., and Whitby, K. (2011). Small-molecule inhibition of human immunodeficiency virus type 1 infection by virus capsid destabilization. J. Virol. 85, 542-549. doi: 10.1128/JVI.01406-10
134. Sievers, S. A., Karanicolas, J., Chang, H. W., Zhao, A., Jiang, L., Zirafi, O., et al. (2011). Structure-based design of non-natural amino-acid inhibitors of amyloid fibril formation. Nature 475, 96-100. doi: 10.1038/nature10154
135. Slomnicki, E. P., Nawrot, B., and Leøeniak, W. (2009). S100A6 binds p53 and affects its activity. Int. J. Biochem. Cell Biol. 41, 784-790. doi: 10.1016/j.biocel.2008.08.007
136. Smerdon, S. J., Jäger, J., Wang, J., Kohlstaedt, L. A., Chirino, A. J., Friedman, J. M., et al. (1994). Structure of the binding site for nonnucleoside inhibitors of the reverse transcriptase of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U.S.A. 91, 3911-3915. doi: 10.1073/pnas.91.9.3911
137. Soto, C., and Estrada, L. (2005). "Amyloid inhibitors and β-sheet breakers, " in Alzheimer's Disease SE-18, eds J. R. Harris and F. Fahrenholz (New York, NY: Springer), 351-364.
138. Sourgen, F., Maroun, R. G., Frère, V., Bouziane, M., Auclair, C., Troalen, F., et al. (1996). A synthetic peptide from the human immunodeficiency virus type-1 integrase exhibits coiled-coil properties and interferes with the in vitro integration activity of the enzyme. Eur. J. Biochem. 240, 765-773. doi: 10.1111/j.1432-1033.1996.0765h.x
139. Sticht, J., Humbert, M., Findlow, S., Bodem, J., Muller, B., Dietrich, U., et al. (2005). A peptide inhibitor of HIV-1 assembly in vitro. Nat. Struct. Mol. Biol. 12, 671-677. doi: 10.1038/nsmb964
140. Stommel, J. M., Marchenko, N. D., Jimenez, G. S., Moll, U. M., Hope, T. J., and Wahl, G. M. (1999). A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J. 18, 1660-1672. doi: 10.1093/emboj/18.6.1660
141. Stray, S. J., Bourne, C. R., Punna, S., Lewis, W. G., Finn, M. G., and Zlotnick, A. (2005). A heteroaryldihydropyrimidine activates and can misdirect hepatitis B virus capsid assembly. Proc. Natl. Acad. Sci. U.S.A. 102, 8138-8143. doi: 10.1073/pnas.0409732102
142. Stray, S. J., and Zlotnick, A. (2006). BAY 41-4109 has multiple effects on Hepatitis B virus capsid assembly. J. Mol. Recognit. 19, 542-548. doi: 10.1002/jmr.801
143. Szymanski, M. R., Jezewska, M. J., and Bujalowski, W. (2013). The Escherichia coli primosomal DnaT protein exists in solution as a monomer-trimer equilibrium system. Biochemistry 52, 1845-1857. doi: 10.1021/bi301568w
144. Tan, Z., Maguire, M. L., Loeb, D. D., and Zlotnick, A. (2013). Genetically altering the thermodynamics and kinetics of hepatitis B virus capsid assembly has profound effects on virus replication in cell culture. J. Virol. 87, 3208-3216. doi: 10.1128/JVI.03014-12
145. Tang, C., Loeliger, E., Kinde, I., Kyere, S., Mayo, K., Barklis, E., et al. (2003). Antiviral inhibition of the HIV-1 capsid protein. J. Mol. Biol. 327, 1013-1020. doi: 10.1016/S0022-2836(03)00289-4
146. Ternois, F., Sticht, J., Duquerroy, S., Krausslich, H.-G., and Rey, F. A. (2005). The HIV-1 capsid protein C-terminal domain in complex with a virus assembly inhibitor. Nat. Struct. Mol. Biol. 12, 678-682. doi: 10.1038/nsmb967
147. Teufel, D. P., Freund, S. M., Bycroft, M., and Fersht, A. R. (2007). Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53. Proc. Natl. Acad. Sci. U.S.A. 104, 7009-7014. doi: 10.1073/pnas.0702010104
148. Thulin, E., Kesvatera, T., and Linse, S. (2011). Molecular determinants of S100B oligomer formation. PLoS ONE 6:e14768. doi: 10.1371/journal.pone.0014768
149. Tintori, C., Demeulemeester, J., Franchi, L., Massa, S., Debyser, Z., Christ, F., et al. (2012). Discovery of small molecule HIV-1 integrase dimerization inhibitors. Bioorg. Med. Chem. Lett. 22, 3109-3114. doi: 10.1016/j.bmcl.2012.03.064
150. Tjernberg, L. O., Näslund, J., Lindqvist, F., Johansson, J., Karlström, A. R., Thyberg, J., et al. (1996). Arrest of amyloid fibril formation by a pentapeptide ligand. J. Biol. Chem. 271, 8545-8548. doi: 10.1074/jbc.271.15.8545
151. Tremblay, M., Bonneau, P., Bousquet, Y., DeRoy, P., Duan, J., Duplessis, M., et al. (2012). Inhibition of HIV-1 capsid assembly: Optimization of the antiviral potency by site selective modifications at N1, C2 and C16 of a 5-(5-furan-2-yl-pyrazol-1-yl)-1H-benzimidazole scaffold. Bioorg. Med. Chem. Lett. 22, 7512-7517. doi: 10.1016/j.bmcl.2012.10.034
152. Tsantrizos, Y. S., Boes, M., Brochu, C., Fenwick, C., Malenfant, E., Mason, S., et al. (2007). Inhibitors of Human Immunodecifiency Virus Replication, International Patent PCT/CA2007/000845.
153. Tsiang, M., Jones, G. S., Niedziela-Majka, A., Kan, E., Lansdon, E. B., Huang, W., et al. (2012). New class of HIV-1 integrase (IN) inhibitors with a dual mode of action. J. Biol. Chem. 287, 21189-21203. doi: 10.1074/jbc.M112.347534
154. Unwin, N., Miyazawa, A., Li, J., and Fujiyoshi, Y. (2002). Activation of the nicotinic acetylcholine receptor involves a switch in conformation of the a subunits. J. Mol. Biol. 319, 1165-1176. doi: 10.1016/S0022-2836(02)00381-9
155. Van Dieck, J., Fernandez-Fernandez, M. R., Veprintsev, D. B., and Fersht, A. R. (2009a). Modulation of the oligomerization state of p53 by differential binding of proteins of the S100 family to p53 monomers and tetramers. J. Biol. Chem. 284, 13804-13811. doi: 10.1074/jbc.M901351200
156. Van Dieck, J., Teufel, D. P., Jaulent, A. M., Fernandez-Fernandez, M. R., Rutherford, T. J., Wyslouch-Cieszynska, A., et al. (2009b). Posttranslational modifications affect the interaction of S100 proteins with tumor suppressor p53. J. Mol. Biol. 394, 922-930. doi: 10.1016/j.jmb.2009.10.002
157. Vidu, A., Dufau, L., Bannwarth, L., Soulier, J.-L., Sicsic, S., Piarulli, U., et al. (2010). Toward the first nonpeptidic molecular tong inhibitor of wild-type and mutated HIV-1 protease dimerization. ChemMedChem 5, 1899-1906. doi: 10.1002/cmdc.201000308
158. Vogelstein, B., Lane, D., and Levine, A. J. (2000). Surfing the p53 network. Nature 408, 307-310. doi: 10.1038/35042675
159. Walters, K. J., Dayie, K. T., Reece, R. J., Ptashne, M., and Wagner, G. (1997). Structure and mobility of the PUT3 dimer. Nat. Struct. Mol. Biol. 4, 744-750. doi: 10.1038/nsb0997-744
160. Wang, F., Wang, Y., Zhang, X., Zhang, W., Guo, S., and Jin, F. (2014). Recent progress of cell-penetrating peptides as new carriers for intracellular cargo delivery. J. Control. Release 174, 126-136. doi: 10.1016/j.jconrel.2013.11.020
161. Wang, P., Reed, M., Wang, Y., Mayr, G., Stenger, J. E., Anderson, M. E., et al. (1994). p53 domains: structure, oligomerization, and transformation. Mol. Cell. Biol. 14, 5182-5191.
162. Wani, M. C., Taylor, H. L., Wall, M. E., Coggon, P., and McPhail, A. T. (1971). Plant antitumor agents. VI. Isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J. Am. Chem. Soc. 93, 2325-2327. doi: 10.1021/ja00738a045
163. Weinberg, R. L., Freund, S. M. V., Veprintsev, D. B., Bycroft, M., and Fersht, A. R. (2004b). Regulation of DNA binding of p53 by its C-terminal domain. J. Mol. Biol. 342, 801-811. doi: 10.1016/j.jmb.2004.07.042
164. Weinberg, R. L., Veprintsev, D. B., and Fersht, A. R. (2004a). Cooperative binding of tetrameric p53 to DNA. J. Mol. Biol. 341, 1145-1159. doi: 10.1016/j.jmb.2004.06.071
165. Whitson, S. R., LeStourgeon, W. M., and Krezel, A. M. (2005). Solution structure of the symmetric coiled coil tetramer formed by the oligomerization domain of hnRNP C: implications for biological function. J. Mol. Biol. 350, 319-337. doi: 10.1016/j.jmb.2005.05.002
166. Wu, H., and Rossmann, M. G. (1993). The canine parvovirus empty capsid structure. J. Mol. Biol. 233, 231-244. doi: 10.1006/jmbi.1993.1502
167. Yakovlev, V. A., Bayden, A. S., Graves, P. R., Kellogg, G. E., and Mikkelsen, R. B. (2010). Nitration of the tumor suppressor protein p53 at Tyrosine 327 promotes p53 oligomerization and activation. Biochemistry 49, 5331-5339. doi: 10.1021/bi100564w
168. Yu, L. P. C., Chou, C.-Y., Choi, P. H., and Tong, L. (2013). Characterizing the importance of the biotin carboxylase domain dimer for Staphylococcus aureus pyruvate carboxylase catalysis. Biochemistry 52, 488-496. doi: 10.1021/bi301294d
169. Yun, M.-K., Nourse, A., White, S. W., Rock, C. O., and Heath, R. J. (2007). Crystal structure and allosteric regulation of the cytoplasmic Escherichia coli l-Asparaginase I. J. Mol. Biol. 369, 794-811. doi: 10.1016/j.jmb.2007.03.061
170. Zhang, H., Zhao, Q., Bhattacharya, S., Waheed, A. A., Tong, X., Hong, A., et al. (2008). A cell-penetrating helical peptide as a potential HIV-1 inhibitor. J. Mol. Biol. 378, 565-580. doi: 10.1016/j.jmb.2008.02.066
171. Zhang, J., Baker, M. L., Schroder, G. F., Douglas, N. R., Reissmann, S., Jakana, J., et al. (2010). Mechanism of folding chamber closure in a group II chaperonin. Nature 463, 379-383. doi: 10.1038/nature08701
172. Zhao, G., Perilla, J. R., Yufenyuy, E. L., Meng, X., Chen, B., Ning, J., et al. (2013). Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497, 643-646. doi: 10.1038/nature12162
173. Zhao, L., O'Reilly, M. K., Shultz, M. D., and Chmielewski, J. (2003). Interfacial peptide inhibitors of HIV-1 integrase activity and dimerization. Bioorg. Med. Chem. Lett. 13, 1175-1177. doi: 10.1016/S0960-894X(03)00040-4