Insights into the Structure, Correlated Motions, and Electrostatic Properties of Two HIV-1 gp120 V3 Loops

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  López de Victoria, Aliana ^a   Tamamis, Phanourios ^a   Kieslich, Chris A ^a   Morikis, Dimitrios ^a  

^a University of California Riverside ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ASPARAGINE; GLUTAMIC ACID; GLYCOPROTEIN GP 120; UNCLASSIFIED DRUG; V3 LOOP;

AMINO ACID SEQUENCE; ARTICLE; CRYSTALLOGRAPHY; ELECTRIC POTENTIAL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RECEPTOR BINDING; SIMULATION; STATIC ELECTRICITY;

AMINO ACID SEQUENCE; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PEPTIDE FRAGMENTS; RECEPTORS, CXCR4; STATIC ELECTRICITY; STRUCTURE-ACTIVITY RELATIONSHIP;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84869784812     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049925     Document Type: Article

References (70)

1. Chan DC, Fass D, Berger JM, Kim PS, (1997) Core structure of gp41 from the HIV envelope glycoprotein. Cell 89: 263-273.
2. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human abtibody. Nature 393: 648-659.
3. Kwong PD, Wyatt R, Majeed S, Robinson J, Sweet RW, et al. (2000) Structures of HIV-1 gp120 Envelope Glycoproteins from Laboratory-Adapted and Primary Isolates. Structure 8: 1329-1339.
4. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, et al. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
5. Huang CC, Lam SN, Acharya P, Tang M, Xiang SH, et al. (2007) Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317: 1930-1934.
6. Dittmar MT, McKnight A, Simmons G, Clapham PR, Weiss RA, et al. (1997) HIV-1 tropism and co-receptor use. Nature 385: 495-496.
7. Xiao LH, Owen SM, Goldman I, Lal AA, DeJong JJ, et al. (1998) CCR5 coreceptor usage of non-syncytium-inducing primary HIV-1 is independent of phylogenetically distinct global HIV-1 isolates: Delineation of consensus motif in the V3 domain that predicts CCR-5 usage. Virology 240: 83-92.
8. Pollakis G, Kang S, Kliphuis A, Chalaby MI, Goudsmit J, et al. (2001) N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J Biol Chem 276: 13433-13441.
9. Cardozo T, Kimura T, Philpott S, Weiser B, Burger H, et al. (2007) Structural basis for coreceptor selectivity by the HIV type 1 V3 loop. AIDS Res Hum Retrov 23: 415-426.
10. Edo-Matas D, van Dort KA, Setiawan LC, Schuitemaker H, Kootstra NA, (2011) Comparison of in vivo and in vitro evolution of CCR5 to CXCR4 coreceptor use of primary human immunodeficiency virus type 1 variants. Virology 412: 269-277.
11. López de Victoria A, Kieslich CA, Rizos AK, Krambovitis E, Morikis D, (2012) Clustering of HIV-1 subtypes based on gp120 V3 loop electrostatic properties. BMC Biophys 5: 3.
12. Kieslich CA, Shin D, López de Victoria A, González-Rivera G, Morikis D (2012) A Predictive Model for HIV-1 co-receptor selectivity and disease progression. Aids Res Hum Retrov, Submitted.
13. Napier KB, Wang ZX, Peiper SC, Trent JO, (2007) CCR5 interactions with the variable 3 loop of gp120. J Mol Model 13: 29-41.
14. Liu S, Fan S, Sun Z, (2003) Structural and functional characterization of the human CCR5 receptor in complex with HIV gp120 envelope glycoprotein and CD4 receptor by molecular modeling studies. J Mol Model 9: 329-336.
15. Brelot A, Heveker N, Montes M, Alizon M, (2000) Identification of residues of CXCR4 critical for human immunodeficiency virus coreceptor and chemokine receptor activities. J Biol Chem 275: 23736-23744.
16. Wu B, Chien EYT, Mol CD, Fenalti G, Liu W, et al. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonist. Science 330: 1066-1071.
17. Cornier EG, Persuh M, Thompson DAD, Lin SW, Sakmar TP, et al. (2000) Specific interaction of CCR5 amino-terminal domain peptides containing sulfotyrosines with HIV-1 envelope glycoprotein gp120. Proc Natl Acad Sci USA 97: 5762-5767.
18. Krambovitis E, Zafiropoulos A, Baritaki S, Spandidos DA, (2004) Simple electrostatic interaction mechanism in the service of HIV-1 pathogenesis. Scand J Immunol 59: 231-234.
19. Baritaki S, Zafiropoulos A, Sioumpara M, Politis M, Spandidos DA, et al. (2002) Ionic interaction of the HIV-1 V3 domain with CCR5 and deregulation of T lymphocyte function. Biochem Biophys Res Commun 298: 574-580.
20. Morikis D, Rizos AK, Spandidos DA, Krambovitis E, (2007) Electrostatic modeling of peptides derived from the V3-loop of HIV-1 gp120: implications of the interaction with chemokine receptor CCR5. Int J Mol Med 19: 343-351.
21. Dragic T, (2001) An overview of the determinants of CCR5 and CXCR4 co-receptor function. J Gen Virol 82: 1807-1814.
22. Teoh TC, Heidelberg T, Rizman-Idid M, (2011) Systematic protein-protein docking and molecular dynamics studies of HIV-1 gp120 and CD4: insights for new drug development. DARU J Pharm Sci 19: 469-475.
23. Da LT, Wu YD, (2011) Theoretical studies on the interactions and interferences of HIV-1 glycoprotein gp120 and its coreceptor CCR5. J Chem Inf Model 51: 359-369.
24. Hsu STD, Bonvin AMJJ, (2004) Atomic insight into the CD4 binding-induced conformational changes in HIV-1 gp120. Proteins 55: 582-593.
25. Chandramouli B, Chillemi G, Abbate I, Capobianchi MR, Rozera G, et al. (2012) Importance of V3 Loop Flexibility and Net Charge in the Context of Co-Receptor Recognition. A Molecular Dynamics Study on HIV gp120. J Biomol Struct Dyn 29: 879-891.
26. Myszka DG, Sweet RW, Hensley P, Brigham-Burke M, Kwong PD, et al. (2000) Energetics of the HIV gp120-CD4 binding reaction. Proc Natl Acad Sci USA 97: 9026-9031.
27. Liu SQ, Liu CQ, Fu YX, (2007) Molecular motions in HIV-1 gp120 mutants reveal their preferences for different conformations. J Mol Graph Model 26: 306-318.
28. Liu SQ, Liu SX, Fu YX, (2008) Molecular motions of human HIV-1 gp120 envelope glycoproteins. J Mol Model 14: 857-870.
29. Yokoyama M, Naganawa S, Yoshimura K, Matsushita S, Sato H, (2012) Structural dynamics of HIV-1 envelope Gp120 outer domain with V3 loop. PLoS One 7: e37530.
30. Rosen O, Sharon M, Quadt-Akabayov SR, Anglister J, (2006) Molecular switch for alternative conformations of the HIV-1 V3 region: implications for phenotype conversion. Proc Natl Acad Sci USA 103: 13950-13955.
31. Galanakis PA, Kandias NG, Rizos AK, Morikis D, Krambovitis E, et al. (2009) NMR evidence of charge-dependent interaction between various PND V3 and CCR5 N-terminal peptides. Biopolymers 92: 94-109.
32. Berman HM, (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
33. Kale L, Skeel R, Bhandarkar M, Brunner R, Gursoy A, et al. (1999) NAMD2: Greater scalability for parallel molecular dynamics. J Comp Phys 151: 283-312.
34. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, et al. (1998) An all-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
35. Mackerell AD Jr, Feig M, Brooks CL III, (2003) Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25: 1400-1415.
36. Macias AT, MacKerell AD Jr, (2005) CH/pi interactions involving aromatic amino acids: refinement of the CHARMM tryptophan force field. J Comput Chem 26: 1452-1463.
37. Grant BJ, Rodrigues AP, ElSawy KM, McCammon JA, Caves LS, (2006) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22: 2695-2696.
38. Seeber M, Cecchini M, Rao F, Settanni G, Caflisch A, (2007) Wordom: a program for efficient analysis of molecular dynamics simulations. Bioinformatics 23: 2625-2627.
39. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF chimera- A visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
40. Humphrey W, Dalke A, Schulten K, (1996) VMD: Visual molecular dynamics. Journal of Molecular Graphics 14: 33-38.
41. Massova I, Kollman PA, (2000) Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Perspectives in Drug Discovery and Design 18: 113-135.
42. Hou T, Wang J, Li Y, Wang W, (2011) Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J Chem Inf Model 51: 69-82.
43. Gohlke H, Case DA, (2004) Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf. J Comput Chem 25: 238-250.
44. Tamamis P, Morikis D, Floudas CA, Archontis G, (2010) Species specificity of the complement inhibitor compstatin investigated by all-atom molecular dynamics simulations. Proteins 78: 2655-2667.
45. Tamamis P, Pierou P, Mytidou C, Floudas CA, Morikis D, et al. (2011) Design of a modified mouse protein with ligand binding properties of its human analog by molecular dynamics simulations: The case of C3 inhibition by compstatin. Proteins 79: 3166-3179.
46. Tamamis P, López de Victoria A, Gorham RD Jr, Bellows-Peterson ML, Pierou P, et al. (2012) Molecular dynamics in drug design: new generations of compstatin analogs. Chem Biol Drug Des 79: 703-718.
47. Lee MS, Feig M, Salsbury FR, Jr., Brooks CL 3rd (2003) New analytic approximation to the standard molecular volume definition and its application to generalized Born calculations. J Comput Chem 24: 1348-1356.
48. Chocholousova J, Feig M, (2006) Balancing an accurate representation of the molecular surface in generalized born formalisms with integrator stability in molecular dynamics simulations. J Comput Chem 27: 719-729.
49. Moustafa IM, Shen H, Morton B, Colina CM, Cameron CE, (2011) Molecular dynamics simulations of viral RNA polymerases link conserved and correlated motions of functional elements to fidelity. Journal of Molecular Biology 410: 159-181.
50. Wang X, Xu X, Zhu S, Xiao Z, Ma Z, et al. (2011) Molecular dynamics simulation of conformational heterogeneity in transportin 1. Proteins 80: 382-397.
51. Silla Y, Chandamouli B, Maiti S, Sengupta S, (2011) A single nucleotide polymorphism in transcobalamin II (I5V) induces structural changes in the protein as revealed by molecular modeling studies. Biochemistry 50: 1396-1402.
52. Falconi M, Biocca S, Novelli G, Desideri A, (2007) Molecular dynamics simulation of human LOX-1 provides an explanation for the lack of OxLDL binding to the Trp150Ala mutant. BMC Struct Biol 7: 73.
53. Lukman S, Grant BJ, Gorfe AA, Grant GH, McCammon JA, (2010) The distinct conformational dynamics of K-Ras and H-Ras A59G. PLoS Comput Biol 6: e1000922.
54. Matter H, Szilágyi L, Forgó P, Marinić Ž, Klaić B, (1997) Structure and Dynamics of a Peptidoglycan Monomer in Aqueous Solution Using NMR Spectroscopy and Simulated Annealing Calculations. Journal of the American Chemical Society 119: 2212-2223.
55. Papaleo E, Mereghetti P, Fantucci P, Grandori R, De Gioia L, (2009) Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: the myoglobin case. J Mol Graph Model 27: 889-899.
56. Kieslich CA, Yang J, Gunopulos D, Morikis D, (2010) Automated computational protocol for alanine scans and clustering of electrostatic potentials: application to C3d-CR2 association. Biotechnol Prog 27: 316-325.
57. Kieslich CA, Gorham RD Jr, Morikis D, (2010) Is the rigid-body assumption reasonable? Insights into the effects of dynamics on the electrostatic analysis of barnase-barstar. J Non-Cryst Solids 357: 707-716.
58. Gorham RD Jr, Kieslich CA, Nichols A, Sausman NU, Foronda M, et al. (2011) An evaluation of Poisson-Boltzmann electrostatic free energy calculations through comparison with experimental mutagenesis. Biopolymers 95: 746-754.
59. Gorham RD Jr, Kieslich CA, Morikis D, (2011) Complement inhibition by Staphylococcus aureus: electrostatics of C3d-EfbC and C3d-Ehp association. Cell Molec Bioeng 5: 32-43.
60. Hakkoymaz H, Kieslich CA, Gorham RD Jr, Gunopulos D, Morikis D, (2011) Electrostatic similarity determination using multi-resolution analysis. Mol Inf 30: 733-746.
61. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, et al. (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35: W522-525.
62. Sitkoff D, Sharp KA, Honig B, (1994) Accurate calculation of hydration free energies using macroscopic solvent models. J Phys Chem 98: 1978-1988.
63. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98: 10037-10041.
64. Tsibris A (2007) Update on CCR5 inhibitors: scientific rationale, clinical evidence, and anticipated uses. PRN Notebook 12.
65. Lobritz MA, Ratcliff AN, Arts EJ, (2010) HIV-1 Entry, Inhibitors, and Resistance. Viruses 2: 1069-1105.
66. Engelman A, Cherepanov P, (2012) The structural biology of HIV-1: mechanistic and therapeutic insights. Nat Rev Microbiol 10: 279-290.
67. Tilton JC, Doms RW, (2010) Entry inhibitors in the treatment of HIV-1 infection. Antiviral Res 85: 91-100.
68. Wilkin TJ, Gulick RM, (2012) CCR5 antagonism in HIV infection: current concepts and future opportunities. Annu Rev Med 63: 81-93.
69. Soriano V, Perno CF, Kaiser R, Calvez V, Gatell JM, et al. (2009) When and how to use maraviroc in HIV-infected patients. AIDS 23: 2377-2385.
70. Frishman D, Argos P, (1995) Kwoledge-based protein secondary structure assignment. Proteins 23: 566-579.