Viroporin potential of the lentivirus lytic peptide (LLP) domains of the HIV-1 gp41 protein

Virology Journal

Volumn 4, Issue , 2007, Pages

  Costin, Joshua M ^a   Rausch, Joshua M ^b   Garry, Robert F ^c   Wimley, William C ^d  

^a FLORIDA GULF COAST UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GP4I PROTEIN; LENTIVIRUS LYTIC PEPTIDE; PEPTIDE; UNCLASSIFIED DRUG; VIROPORIN; VIRUS PROTEIN; GLYCOPROTEIN GP 41; LENTIVIRAL LYTIC PEPTIDE TYPE 1, HUMAN IMMUNODEFICIENCY VIRUS 1; PEPTIDE FRAGMENT;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; CELL MEMBRANE; CYTOPATHOGENIC EFFECT; HUMAN IMMUNODEFICIENCY VIRUS 1; ION TRANSPORT; MEMBRANE PERMEABILITY; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; VIRUS REPLICATION; BIOLOGY; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PROTEIN MOTIF; PROTEOMICS;

CERCOPITHECINE HERPESVIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS;

AMINO ACID MOTIFS; COMPUTATIONAL BIOLOGY; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; PEPTIDE FRAGMENTS; PEPTIDES; PROTEOMICS;

EID: 38349181791     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-4-123     Document Type: Article

References (78)

1. A structural correlation between lentivirus transmembrane proteins and natural cytolytic peptides. MA Miller RF Garry JM Jaynes RC Montelaro, AIDS Res Hum Retroviruses 1991 7 511 519 1657072
2. Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. M Zasloff, Proc Natl Acad Sci USA 1987 84 5449 5453 3299384 10.1073/pnas.84.15.5449
3. Antimicrobial activity of synthetic magainin peptides and several analogues. M Zasloff B Martin HC Chen, Proc Natl Acad Sci USA 1988 85 910 913 3277183 10.1073/pnas.85.3.910
4. The most highly amphiphilic alpha-helices include two amino acid segments in human immunodeficiency virus glycoprotein 41. D Eisenberg M Wesson, Biopolymers 1990 29 171 177 10.1002/bip.360290122 2328285
5. Synthetic magainin analogues with improved antimicrobial activity. HC Chen JH Brown JL Morell CM Huang, FEBS Lett 1988 236 462 466 10.1016/0014-5793(88)80077-2 3410055
6. Magainin 2, a natural antibiotic from frog skin, forms ion channels in lipid bilayer membranes. RA Cruciani JL Barker SR Durell G Raghunathan HR Guy M Zasloff EF Stanley, Eur J Pharmacol 1992 226 287 296 10.1016/0922-4106(92)90045- W 1383011
7. A two-dimensional NMR study of the antimicrobial peptide magainin 2. D Marion M Zasloff A Bax, FEBS Lett 1988 227 21 26 10.1016/0014-5793(88)81405-4 3338566
8. Construction of a toroidal model for the magainin pore. K Murzyn M Pasenkiewicz-Gierula, J Mol Model (Online) 2003 9 217 224 10.1007/s00894-003- 0127-z
9. Barrel-stave model or toroidal model? A case study on melittin pores. L Yang TA Harroun TM Weiss L Ding HW Huang, Biophys J 2001 81 1475 1485 11509361
10. N-terminal analogues of cecropin A: synthesis, antibacterial activity, and conformational properties. D Andreu RB Merrifield H Steiner HG Boman, Biochemistry 1985 24 1683 1688 10.1021/bi00328a017 3924096
11. Membrane interactions of synthetic peptides corresponding to amphipathic helical segments of the human immunodeficiency virus type-1 envelope glycoprotein. SK Srinivas RV Srinivas GM Anantharamaiah JP Segrest RW Compans, J Biol Chem 1992 267 7121 7127 1551918
12. A molecular model for membrane fusion based on solution studies of an amphiphilic peptide from HIV gp41. G Fujii S Horvath S Woodward F Eiserling D Eisenberg, Protein Sci 1992 1 1454 1464 1303764
13. Interaction of peptide fragment 828-848 of the envelope glycoprotein of human immunodeficiency virus type I with lipid bilayers. K Gawrisch KH Han JS Yang LD Bergelson JA Ferretti, Biochemistry 1993 32 3112 3118 10.1021/bi00063a024 8457572
14. A leucine zipper-like sequence from the cytoplasmic tail of the HIV-1 envelope glycoprotein binds and perturbs lipid bilayers. Y Kliger Y Shai, Biochemistry 1997 36 5157 5169 10.1021/bi962935r 9136877
15. The membranotropic regions of the endo and ecto domains of HIV gp41 envelope glycoprotein. MR Moreno M Giudici J Villalain, Biochim Biophys Acta 2006 1758 111 123 10.1016/j.bbamem.2006.01.007 16483537
16. Identification of a calmodulin-binding and inhibitory peptide domain in the HIV-1 transmembrane glycoprotein. MA Miller TA Mietzner MW Cloyd WG Robey RC Montelaro, AIDS Res Hum Retroviruses 1993 9 1057 1066 8312049
17. Protective effect of glutathione in HIV-1 lytic peptide 1-induced cell death in human neuronal cells. JH Sung SA Shin HK Park RC Montelaro YH Chong, J Neurovirol 2001 7 454 465 10.1080/135502801753170318 11582518
18. Concentration-dependent differential induction of necrosis or apoptosis by HIV-1 lytic peptide 1. DR Plymale AM Comardelle CD Fermi DS Martin JM Costin CH Norris SB Tencza TA Mietzner RC Montelaro RF Garry, Peptides 1999 20 1275 1283 10.1016/S0196-9781(99)00132-1 10612441
19. Effect of amino acid substitutions on calmodulin binding and cytolytic properties of the LLP-1 peptide segment of human immunodeficiency virus type 1 transmembrane protein. SB Tencza MA Miller K Islam TA Mietzner RC Montelaro, J Virol 1995 69 5199 5202 7609094
20. Novel antimicrobial peptides derived from human immunodeficiency virus type 1 and other lentivirus transmembrane proteins. SB Tencza JP Douglass DJ Creighton Jr RC Montelaro TA Mietzner, Antimicrob Agents Chemother 1997 41 2394 2398 9371339
21. Alterations in cell membrane permeability by the lentivirus lytic peptide (LLP-1) of HIV-1 transmembrane protein. MA Miller MW Cloyd J Liebmann CR Rinaldo Jr KR Islam SZ Wang TA Mietzner RC Montelaro, Virology 1993 196 89 100 10.1006/viro.1993.1457 8356808
22. A synthetic peptide corresponding to the carboxy terminus of human immunodeficiency virus type 1 transmembrane glycoprotein induces alterations in the ionic permeability of Xenopus laevis oocytes. AM Comardelle CH Norris DR Plymale PJ Gatti B Choi CD Fermin AM Haislip SB Tencza TA Mietzner RC Montelaro RF Garry, AIDS Res Hum Retroviruses 1997 13 1525 1532 9390752
23. An amphipathic peptide from the C-terminal region of the human immunodeficiency virus envelope glycoprotein causes pore formation in membranes. L Chernomordik AN Chanturiya E Suss-Toby E Nora J Zimmerberg, J Virol 1994 68 7115 7123 7933093
24. Human immunodeficiency virus infection of T-lymphoblastoid cells reduces intracellular pH. A Makutonina TG Voss DR Plymale CD Fermin CH Norris S Vigh RF Garry, J Virol 1996 70 7049 7055 8794349
25. Role of Membrane Alterations in HIV-1 Infection. PJ Gatti, Ph.D. Tulane University, Department of Microbiology and Immunology 1998
26. Role of potassium in human immunodeficiency virus production and cytopathic effects. B Choi PJ Gatti AM Haislip CD Fermin RF Garry, Virology 1998 247 189 199 10.1006/viro.1998.9251 9705912
27. Alteration of intracellular potassium and sodium concentrations correlates with induction of cytopathic effects by human immunodeficiency virus. TG Voss CD Fermin JA Levy S Vigh B Choi RF Garry, J Virol 1996 70 5447 5454 8764056
28. Cell killing by ultraviolet-inactivated human immunodeficiency virus. S Rasheed AA Gottlieb RF Garry, Virology 1986 154 395 400 10.1016/0042-6822(86) 90465-4 3490050
29. Oligomerization of the hydrophobic heptad repeat of gp41. HB Bernstein SP Tucker SR Kar SA McPherson DT McPherson JW Dubay J Lebowitz RW Compans E Hunter, J Virol 1995 69 2745 2750 7707497
30. Similarities of viral proteins to toxins that interact with monovalent cation channels. RF Garry JJ Kort F Koch-Nolte G Koch, Aids 1991 5 1381 1384 10.1097/00002030-199111000-00017 1722677
31. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. WC Wimley SH White, Nat Struct Biol 1996 3 842 848 10.1038/nsb1096-842 8836100
32. Folding amphipathic helices into membranes: amphiphilicity trumps hydrophobicity. M Fernandez-Vidal S Jayasinghe AS Ladokhin SH White, J Mol Biol 2007 370 459 470 17532340 10.1016/j.jmb.2007.05.016
33. From "carpet" mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides. Y Shai Z Oren, Peptides 2001 22 1629 1641 10.1016/S0196-9781(01)00498-3 11587791
34. Mechanism of leakage of phospholipid vesicle contents induced by the peptide GALA. RA Parente S Nir FC Szoka Jr, Biochemistry 1990 29 8720 8728 10.1021/bi00489a031 2271552
35. Inhibition of HIV type 1 production by hygromycin B. PJ Gatti B Choi AM Haislip CD Fermin RF Garry, AIDS Res Hum Retroviruses 1998 14 885 892 9671217
36. Human immunodeficiency virus type 1 envelope glycoprotein oligomerization requires the gp41 amphipathic alpha-helical/leucine zipper-like sequence. P Poumbourios KA Wilson RJ Center W El Ahmar BE Kemp, J Virol 1997 71 2041 2049 9032336
37. Determinants of human immunodeficiency virus type 1 envelope glycoprotein oligomeric structure. P Poumbourios W el Ahmar DA McPhee BE Kemp, J Virol 1995 69 1209 1218 7815497
38. Genetic evidence for an interaction between human immunodeficiency virus type 1 matrix and alpha-helix 2 of the gp41 cytoplasmic tail. T Murakami EO Freed, J Virol 2000 74 3548 3554 10729129 10.1128/JVI.74.8.3548-3554.2000
39. The role of lipid microdomains in virus biology. DP Nayak EK Hui, Subcell Biochem 2004 37 443 491 15376630
40. Specific lipid requirements of membrane proteins-a putative bottleneck in heterologous expression. M Opekarova W Tanner, Biochim Biophys Acta 2003 1610 11 22 10.1016/S0005-2736(02)00708-3 12586375
41. Quantification of major classes of Xenopus phospholipids by high performance liquid chromatography with evaporative light scattering detection. BJ Stith J Hall P Ayres L Waggoner JD Moore WA Shaw, J Lipid Res 2000 41 1448 1454 10974052
42. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. M Lu SC Blacklow PS Kim, Nat Struct Biol 1995 2 1075 1082 10.1038/nsb1295-1075 8846219
43. The antigenic structure of the HIV gp120 envelope glycoprotein. R Wyatt PD Kwong E Desjardins RW Sweet J Robinson WA Hendrickson JG Sodroski, Nature 1998 393 705 711 10.1038/31514 9641684
44. Induction of anti-HIV neutralizing antibodies by synthetic peptides. TC Chanh GR Dreesman P Kanda GP Linette JT Sparrow DD Ho RC Kennedy, Embo J 1986 5 3065 3071 3466790
45. Properties of a neutralizing antibody that recognizes a conformational form of epitope ERDRD in the gp41 C-terminal tail of human immunodeficiency virus type 1. SM Cleveland TD Jones NJ Dimmock, J Gen Virol 2000 81 1251 1260 10769067
46. A region of the C-terminal tail of the gp41 envelope glycoprotein of human immunodeficiency virus type 1 contains a neutralizing epitope: evidence for its exposure on the surface of the virion. SM Cleveland L McLain L Cheung TD Jones M Hollier NJ Dimmock, J Gen Virol 2003 84 591 602 10.1099/vir.0.18630-0 12604810
47. Part of the C-terminal tail of the envelope gp41 transmembrane glycoprotein of human immunodeficiency virus type 1 is exposed on the surface of infected cells and is involved in virus-mediated cell fusion. L Cheung L McLain MJ Hollier SA Reading NJ Dimmock, J Gen Virol 2005 86 131 138 10.1099/vir.0.80439-0 15604440
48. Neutralization of diverse HIV-1 strains by monoclonal antibodies raised against a gp41 synthetic peptide. AG Dalgleish TC Chanh RC Kennedy P Kanda PR Clapham RA Weiss, Virology 1988 165 209 215 10.1016/0042-6822(88)90674-5 2838959
49. Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific, single amino acid substitutions in the human immunodeficiency virus type 1 matrix. EO Freed MA Martin, J Virol 1995 69 1984 1989 7853546
50. Membrane-permeabilizing motif in Semliki forest virus E1 glycoprotein. JL Nieva MA Sanz L Carrasco, FEBS Lett 2004 576 417 422 10.1016/j.febslet.2004.09. 061 15498572
51. Modification of membrane permeability by animal viruses. L Carrasco, Adv Virus Res 1995 45 61 112 7793329
52. The 6-kilodalton membrane protein of Semliki Forest virus is involved in the budding process. A Loewy J Smyth CH von Bonsdorff P Liljestrom MJ Schlesinger, J Virol 1995 69 469 475 7983743
53. The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. T Klimkait K Strebel MD Hoggan MA Martin JM Orenstein, J Virol 1990 64 621 629 2404139
54. Viroporins. ME Gonzalez L Carrasco, FEBS Lett 2003 552 28 34 10.1016/S0014-5793(03)00780-4 12972148
55. Molecular and biochemical analyses of human immunodeficiency virus type 1 vpu protein. K Strebel T Klimkait F Maldarelli MA Martin, J Virol 1989 63 3784 3791 2788224
56. Calmodulin-binding function of LLP segments from the HIV type 1 transmembrane protein is conserved among natural sequence variants. SB Tencza TA Mietzner RC Montelaro, AIDS Res Hum Retroviruses 1997 13 263 269 9115814
57. Pore-forming peptides induce rapid phospholipid flip-flop in membranes. E Fattal S Nir RA Parente FC Szoka Jr, Biochemistry 1994 33 6721 6731 10.1021/bi00187a044 8204607
58. Determining the membrane topology of peptides by fluorescence quenching. WC Wimley SH White, Biochemistry 2000 39 161 170 10.1021/bi991836l 10625491
59. The organization of the envelope projections on the surface of HIV. M Ozel G Pauli HR Gelderblom, Arch Virol 1988 100 255 266 10.1007/BF01487688 3401118
60. Envelope structure model of human immunodeficiency virus type 1. I Takahashi M Takama AM Ladhoff D Scholz, J Acquir Immune Defic Syndr 1989 2 136 140 2703954
61. Oligomeric organization of gp120 on infectious human immunodeficiency virus type 1 particles. CD Weiss JA Levy JM White, J Virol 1990 64 5674 5677 2214033
62. Endogenous reverse transcription of human immunodeficiency virus type 1 in physiological microenviroments: an important stage for viral infection of nondividing cells. H Zhang G Dornadula RJ Pomerantz, J Virol 1996 70 2809 2824 8627755
63. Impairment of excitatory amino acid transport in astroglial cells infected with the human immunodeficiency virus type 1. JJ Kort, AIDS Res Hum Retroviruses 1998 14 1329 1339 9788674
64. Immunohistochemical characterization of multinucleated giant cells in the brain of a Japanese AIDS patient. M Takeya M Naito K Eto K Takahashi, Acta Pathol Jpn 1991 41 212 216 2068946
65. Indirect mechanisms of HIV pathogenesis: how does HIV kill T cells? TH Finkel NK Banda, Curr Opin Immunol 1994 6 605 615 10.1016/0952-7915(94)90149-X 7946050
66. Death of bystander cells by a novel pathway involving early mitochondrial damage in human immunodeficiency virus-related lymphadenopathy. M Carbonari AM Pesce M Cibati A Modica L Dell'Anna G D'Offizi A Angelici S Uccini A Modesti M Fiorilli, Blood 1997 90 209 216 9207455
67. USAID. http://www.USAID.gov/our_work/global_health/aids/News/aidsfaq.html
68. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. D Finzi M Hermankova T Pierson LM Carruth C Buck RE Chaisson TC Quinn K Chadwick J Margolick R Brookmeyer, Science 1997 278 1295 1300 10.1126/science.278.5341.1295 9360927
69. Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry. JM Kilby S Hopkins TM Venetta B DiMassimo GA Cloud JY Lee L Alldredge E Hunter D Lambert D Bolognesi, Nat Med 1998 4 1302 1307 10.1038/3293 9809555
70. Membrane Protein Explorer. http://blanco.biomol.uci.edu/mpex/
71. Bona fide prediction of aspects of protein conformation. Assigning interior and surface residues from patterns of variation and conservation in homologous protein sequences. SA Benner I Badcoe MA Cohen DL Gerloff, J Mol Biol 1994 235 926 958 10.1006/jmbi.1994.1049 8289328
72. The PredictProtein server. http://biobug.life.nthu.edu.tw/predictprotein/ tools/helicalWheel/
73. Vesicles of variable sizes produced by a rapid extrusion procedure. LD Mayer MJ Hope PR Cullis, Biochim Biophys Acta 1986 858 161 168 10.1016/0005-2736(86)90302-0 3707960
74. Generation of large unilamellar vesicles from long-chain saturated phosphatidylcholines by extrusion technique. R Nayar MJ Hope PR Cullis, Biochim Biophys Acta 1989 986 200 206 10.1016/0005-2736(89)90468-9
75. A high-throughput screen for identifying transmembrane pore-forming peptides. JM Rausch WC Wimley, Anal Biochem 2001 293 258 263 10.1006/abio.2001.5137 11399041
76. Microdetermination of phosphorus. PS Chen TY Toribara H Warner, Anal Chem 1956 28 1756 1758 10.1021/ac60119a033
77. The colometric determination of phosphorus. CH Fiske Y Subbarow, J Biol Chem 1925 66 375 400
78. Protein folding in membranes: determining energetics of peptide-bilayer interactions. SH White WC Wimley AS Ladokhin K Hristova, Methods Enzymol 1998 295 62 87 9750214