Antibodies generated in cats by a lipopeptide reproducing the membrane-proximal external region of the feline immunodeficiency virus transmembrane enhance virus infectivity

Clinical and Vaccine Immunology

Volumn 14, Issue 8, 2007, Pages 944-951

  Giannecchini, Simone ^a,b   D'Ursi, Anna Maria ^c   Esposito, Cinzia ^c   Scrima, Mario ^c   Zabogli, Elisa ^a   Freer, Giulia ^a   Rovero, Paolo ^b   Bendinelli, Mauro ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITY OF SALERNO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; LIPOPEPTIDE; LIPOPEPTIDE P59; OLIGOPEPTIDE; UNCLASSIFIED DRUG; LIPOPROTEIN; MEMBRANE PROTEIN; PEPTIDE; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN RECOGNITION; ARTICLE; CAT; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FELINE IMMUNODEFICIENCY VIRUS; FEMALE; IMMUNIZATION; LYMPHOID CELL LINE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION; ANIMAL; BLOOD; CELL MEMBRANE; CHEMISTRY; GERMFREE ANIMAL; IMMUNOLOGY; MICELLE; PATHOGENICITY; PROTEIN CONFORMATION; SERODIAGNOSIS; SYNTHESIS; VIRION;

ANIMALS; ANTIBODIES, VIRAL; CATS; CELL MEMBRANE; CIRCULAR DICHROISM; IMMUNIZATION; IMMUNODEFICIENCY VIRUS, FELINE; LIPOPROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE GLYCOPROTEINS; MICELLES; NEUTRALIZATION TESTS; PEPTIDES; PROTEIN CONFORMATION; SPECIFIC PATHOGEN-FREE ORGANISMS; VIRION;

EID: 35248848419     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00140-07     Document Type: Article

References (58)

1. Avrameas, A., A. D. Strosberg, A. Moraillon, P. Sonigo, and G. Pancino. 1993. Serological diagnosis of feline immunodeficiency virus infection based on synthetic peptides from Env glycoproteins. Res. Virol. 144:209-218.
2. Barbato, G., E. Bianchi, P. Ingallinella, W. H. Hurni, M. D. Miller, G. Ciliberto, R. Cortese, R. Bazzo, J. W. Shiver, and A. Pessi. 2003. Structural analysis of the epitope of the anti-HIV antibody 2F5 sheds light into its mechanism of neutralization and HIV fusion. J. Mol. Biol. 330:1101-1115.
3. Bax, A., and D. G. Davis. 1985. Mlev-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65:355-360.
4. Braunschweiler, L., and R. R. Ernst. 1983. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53:521-528.
5. Calarota, S., M. Jansson, M. Levi, K. Broliden, O. Libonatti, H. Wigzell, and B. Wahren. 1996. Immunodominant glycoprotein 41 epitope identified by seroreactivity in HIV type 1-infected individuals. AIDS Res. Hum. Retrovir. 12:705-713.
6. Chan, D. C., and P. S. Kim. 1998. HIV entry and its inhibition. Cell 93:681-684.
7. de Parseval, A., C. K. Grant, K. J. Sastry, and J. H. Elder. 2006. Sequential CD134-CXCR4 interactions in feline immunodeficiency virus (FIV): soluble CD134 activates FIV Env for CXCR4-dependent entry and reveals a cryptic neutralization epitope. J. Virol. 80:3088-3091.
8. de Ronde, A., J. G. Stam, P. Boers, H. Langedijk, R. Meloen, W. Hesselink, L. C. E. J. M. Keldermans, A. van Vliet, E. J. Verschoor, M. C. Horzinek, and H. F. Egberink. 1993. Antibody response in cats to the envelope proteins of feline immunodeficiency virus: identification of an immunodominant neutralization domain. Virology 198:257-264.
9. Dimitrov, A. S., A. Jacobs, C. M. Finnegan, G. Stiegler, H. Katinger, and R. Blumenthal. 2007. Exposure of the membrane-proximal external region of HIV-1 gp41 in the course of HIV-1 envelope glycoprotein-mediated fusion. Biochemistry 46:1398-1401.
10. Elder, J. H., G. A. Dean, E. A. Hoover, J. A. Hoxie, M. H. Malim, L. Mathes, J. C. Neil, T. W. North, E. Sparger, M. B. Tompkins, W. A. F. Tompkins, J. Yamamoto, N. Yuhki, N. C. Pedersen, and R. H. Miller. 1998. Lessons from the cat: feline immunodeficiency virus as a tool to develop intervention strategies against human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 14:797-801.
11. Esposito, C., G. D'Errico, M. R. Armenante, S. Giannecchini, M. Bendinelli, P. Rovero, and A. M. D'Ursi. 2006. Physicochemical characterization of a peptide deriving from the glycoprotein gp36 of the feline immunodeficiency virus and its lipoylated analogue in micellar systems. Biochim. Biophys. Acta 1758:1653-1661.
12. Freer, G., S. Giannecchini, A. Tissot, M. F. Bachmann, P. Rovero, P. F. Serres, and M. Bendinelli. 2004. Dissection of seroreactivity against the tryptophan-rich motif of the feline immunodeficiency virus transmembrane glycoprotein. Virology 322:360-369.
13. Gallo, S. A., C. M. Finnegan, M. Viard, Y. Raviv, A. Dimitrov, S. S. Rawt, A. Puri, S. Durell, and R. Blumenthal. 2003. The HIV Env-mediated fusion reaction. Biochim. Biophys. Acta 1614:36-50.
14. Garg, H., F. J. Fuller, and W. A. Tompkins. 2004. Mechanism of feline immunodeficiency virus envelope glycoprotein-mediated fusion. Virology 321:274-286.
15. Giannecchini, S., M. C. Alcaro, P. Isola, O. Sichi, M. Pistello, A. M. Papini, P. Rovero, and M. Bendinelli. 2005. Feline immunodeficiency virus plasma load reduction by a retroinverso octapeptide reproducing the Trp-rich motif of the transmembrane glycoprotein. Antivir. Ther. 10:671-680.
16. Giannecchini, S., F. Bonci, M. Pistello, D. Matteucci, O. Sichi, P. Rovero, and M. Bendinelli. 2004. The membrane-proximal tryptophan-rich region in the transmembrane glycoprotein ectodomain of feline immunodeficiency virus is important for cell entry. Virology 320:156-166.
17. Giannecchini, S., A. Di Fenza, A. M. D'Ursi, D. Matteucci, P. Rovero, and M. Bendinelli. 2003. Antiviral activity and conformational features of an octapeptide derived from the membrane-proximal ectodomain of the feline immunodeficiency virus transmembrane glycoprotein. J. Virol. 77:3724-3733.
18. Giannecchini, S., P. Isola, O. Sichi, D. Matteucci, M. Pistello, L. Zaccaro, D. Del Mauro, and M. Bendinelli. 2002. AIDS vaccination studies using an ex vivo feline immunodeficiency virus model: failure to protect and possible enhancement of challenge infection by four cell-based vaccines prepared with autologous lymphoblasts. J. Virol. 76:6882-6892.
19. Grundner, C., T. Mirzabekov, J. Sodroski, and R. Wyatt. 2002. Solid-phase proteoliposomes containing human immunodeficiency virus envelope glycoproteins. J. Virol. 76:3511-3521.
20. Guntert, P., C. Mumenthaler, and K. Wüthrich. 1997. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273:283-298.
21. Huisman, W., E. J. Schrauwen, S. D. Pas, J. A. Karlas, G. F. Rimmelzwaan, and A. D. M. E. Osterhaus. 2004. Antibodies specific for hypervariable regions 3 to 5 of the feline immunodeficiency virus envelope glycoprotein are not solely responsible for vaccine-induced acceleration of challenge infection in cats. J. Gen. Virol. 85:1833-1841.
22. Jeener, J., B. H. Meyer, P. Bachman, and R. R. Ernst. 1979. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71:4546-4553.
23. Joyce, J. G., W. M. Hurni, M. J. Bogusky, V. M. Garsky, X. Liang, M. P. Citron, R. C. Danzeisen, R. D. Miller, J. W. Shiver, and P. M. Keller. 2002. Enhancement of α-helicity in the HIV-1 inhibitory peptide DP178 leads to an increased affinity for human monoclonal antibody 2F5 but does not elicit neutralizing responses in vitro: implications for vaccine design. J. Biol. Chem. 277:45811-45820.
24. Karlas, J. A., K. H. Siebelink, M. A. Peer, W. Huisman, A. M. Cuisinier, G. F. Rimmelzwaan, and A. D. M. E. Osterhaus. 1999. Vaccination with experimental feline immunodeficiency virus vaccines, based on autologous infected cells, elicits enhancement of homologous challenge infection. J. Gen. Virol. 80:761-765.
25. Kim, M., Z. Qiao, J. Yu, D. Montefiori, and E. L. Reinherz. 2007. Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine 25:5102-5114.
26. Lauterwein, J., C. Bosch, L. R. Brown, and K. Wuthrich. 1979. Physiochemical studies of the protein-lipid interactions in melittin containing micelles. Biochim. Biophys. Acta 556:244-264.
27. Lenz, O., M. T. Dittmar, A. Wagner, B. Ferko, K. Vorauer-Uhl, G. Stiegler, and W. Weissenhorn. 2005. Trimeric membrane-anchored gp41 inhibits HIV membrane fusion. J. Biol. Chem. 280:4095-4101.
28. Lombardi, S., C. Garzelli, M. Pistello, C. Massi, D. Matteucci, F. Baldinotti, G. Cammarota, L. Da Prato, P. Bandecchi, F. Tozzini, and M. Bendinelli. 1994. A neutralizing antibody-inducing peptide of the V3 domain of feline immunodeficiency virus envelope glycoprotein does not induce protective immunity. J. Virol. 68:8374-8379.
29. Lorizate, M., A. Cruz, N. Huarte, R. Kunert, J. Pèrez-Gil, and J. L. Nieva. 2006. Recognition and blocking of HIV-1 gp41 pre-transmembrane sequence by monoclonal 4E10 antibody in a raft-like membrane environment. J. Biol. Chem. 281:39598-39606.
30. Lorizate, M., I. de la Arada, N. Huarte, S. Sanchez-Martinez, B. G. de la Torre, D. Andreu, J. L. Arrondo, and J. L. Nieva. 2006. Structural analysis and assembly of the HIV-1 gp41 amino-terminal fusion peptide and the pretransmembrane amphipathic-at-interface sequence. Biochemistry 45:14337-14346.
31. Macura, S., and R. R. Ernst. 1980. Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy. Mol. Phys. 41:95-117.
32. Massi, C., S. Lombardi, E. Indino, D. Matteucci, C. La Rosa, F. Esposito, C. Garzelli, and M. Bendinelli. 1997. Most potential linear B cell epitopes of Env glycoproteins of feline immunodeficiency virus are immunogenically silent in infected cats. AIDS Res. Hum. Retrovir. 13:1121-1129.
33. Matteucci, D., P. Mazzetti, F. Baldinotti, L. Zaccaro, and M. Bendinelli. 1995. The feline lymphoid cell line MBM and its use for feline immunodeficiency virus isolation and quantitation. Vet. Immunol. Immunopathol. 46:71-82.
34. McGaughey, G. B., M. Citron, R. C. Danzeisen, R. M. Freidinger, V. M. Garsky, W. M. Hurni, J. G. Joyce, X. Liang, M. Miller, J. Shiver, and M. J. Bogusky. 2003. HIV-1 vaccine development: constrained peptide immunogens show improved binding to the anti-HIV-1 gp41 MAb. Biochemistry 42:3214-3223.
35. Muñoz-Barroso, I., K. Salzwedel, E. Hunter, and R. Blumenthal. 1999. Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusion. J. Virol. 73:6089-6092.
36. Muster, T., F. Steindl, M. Purtscher, A. Trkola, A. Klima, G. Himmler, F. Rüker, and H. Katinger. 1993. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67:6642-6647.
37. Ofek, G., M. Tang, A. Sambor, H. Katinger, J. R. Mascola, R. Wyatt, and P. D. Kwong. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737.
38. Overbaugh, J., A. D. Miller, and M. V. Eiden. 2001. Receptors and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins. Microbiol. Mol. Biol. Rev. 65:371-389.
39. Pancino, G., C. Chappey, W. Saurin, and P. Sonigo. 1993. B epitopes and selection pressures in feline immunodeficiency virus envelope glycoproteins. J. Virol. 67:664-672.
40. Parker, C. E., L. J. Deterding, C. Hager-Braun, J. M. Binley, N. Schulke, H. Katinger, J. P. Moore, and K. B. Tomer. 2001. Fine definition of the epitope on the gp41 glycoprotein of human immunodeficiency virus type 1 for the neutralizing monoclonal antibody 2F5. J. Virol. 75:10906-10911.
41. Pedersen, N. C., E. W. Ho, M. L. Brown, and J. K. Yamamoto. 1987. Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 235:790-793.
42. Peisajovich, S. G., and Y. Shai. 2003. Viral fusion proteins: multiple regions contribute to membrane fusion. Biochim. Biophys. Acta 1614:122-129.
43. Piantini, U., O. W. Sorensen, and R. R. Ernst. 1982. Multiple quantum filters for elucidating NMR coupling networks. J. Am. Chem. Soc. 104:6800-6801.
44. Reed, L. J., and H. A. Müench. 1938. A simple method for estimating fifty percent end points. Am. J. Hyg. 27:493-497.
45. Richardson, J., A. Moraillon, S. Baud, A. M. Cuisinier, P. Sonigo, and G. Pancino. 1997. Enhancement of feline immunodeficiency virus (FIV) infection after DNA vaccination with the FIV envelope. J. Virol. 71:9640-9649.
46. Richardson, J., A. Moraillon, F. Crespeau, S. Baud, P. Sonigo, and G. Pancino. 1998. Delayed infection after immunisation with a peptide from the transmembrane glycoprotein of the feline immunodeficiency virus. J. Virol. 72:2406-2415.
47. Salzwedel, K., J. T. West, and E. Hunter. 1999. A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73:2469-2480.
48. Sanchez-Martinez, S., M. Lorizate, H. Katinger, R. Kunert, and J. L. Nieva. 2006. Membrane association and epitope recognition by HIV-1 neutralizing anti-gp41 2F5 and 4E10 antibodies. AIDS Res. Hum. Retrovir. 22:998-1006.
49. Schibli, D. J., R. C. Montelaro, and H. J. Vogel. 2001. The membrane-proximal tryptophan-rich region of the HIV glycoprotein, gp41, forms a well-defined helix in dodecylphosphocholine micelles. Biochemistry 40:9570-9578.
50. Shimojima, M., T. Miyazawa, Y. Ikeda, E. L. McMonagle, H. Haining, H. Akashi, Y. Takeuchi, M. J. Hosie, and B. J. Willett. 2004. Use of CD134 as a primary receptor by the feline immunodeficiency virus. Science 303:1192-1195.
51. Siebelink, K. H., E. Tijhaar, R. C. Huisman, W. Huisman, A. de Ronde, I. H. Darby, M. J. Francis, G. F. Rimmelzwaan, and A. D. M. E. Osterhaus. 1995. Enhancement of feline immunodeficiency virus infection after immunization with envelope glycoprotein subunit vaccines. J. Virol. 69:3704-3711.
52. Suárez, T., W. R. Gallaher, A. Agirre, F. M. Goni, and J. L. Nieva. 2000. Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J. Virol. 74:8038-8047.
53. Talbott, R. L., E. E. Sparger, K. M. Lovelace, W. M. Fitch, N. C. Pedersen, P. A. Luciw, and J. H. Elder. 1989. Nucleotide sequence and genomic organization of feline immunodeficiency virus. Proc. Natl. Acad. Sci. USA 86:5743-5747.
54. Whitmore, L., and B. A. Wallace. 2004. DICHROWEB, an online server for protein secondary structure analysis from circular dichroism spectroscopic data. Nucleic Acids Res. 32:668-673.
55. Willett, B. J., J. N. Flynn, and M. J. Hosie. 1997. FIV infection of the domestic cat: an animal model for AIDS. Immunol. Today 18:182-189.
56. Zhu, P., J. Liu, J. Bess, Jr., E. Chertova, J. D. Lifson, H. Grise, G. A. Ofek, K. A. Taylor, and K. H. Roux. 2006. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441:847-852.
57. Zwick, M. B. 2005. The membrane-proximal external region of HIV-1 gp41: a vaccine target worth exploring. AIDS 19:1725-1737.
58. Zwick, M. B., A. F. Labrijn, M. Wang, C. Spenlehauer, E. O. Saphire, J. M. Binley, J. P. Moore, G. Stiegler, H. Katinger, D. R. Burton, and P. W. H. I. Parren. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75:10892-10905.