Protective versus pathogenic anti-CD4 immunity: Insights from the study of natural resistance to HIV infection

Journal of Translational Medicine

Volumn 7, Issue , 2009, Pages

  Burastero, Samuele E ^a   Figini, Mariangela ^b   Frigerio, Barbara ^b   Lusso, Paolo ^c   Mollica, Luca ^d   Lopalco, Lucia ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b IRCCS   (Italy)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d DULBECCO TELETHON INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; EPITOPE; GLYCOPROTEIN GP 120; IBALIZUMAB; AUTOANTIBODY; CD4 ANTIGEN;

ANTIGEN BINDING; ANTIVIRAL ACTIVITY; APOPTOSIS; AUTOIMMUNITY; BINDING SITE; CD4+ T LYMPHOCYTE; CLINICAL TRIAL; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE FUNCTION; NONHUMAN; PHARMACOLOGICAL BLOCKING; PSORIASIS; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; PROTEIN TERTIARY STRUCTURE;

ANTIGENS, CD4; AUTOANTIBODIES; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY;

EID: 71949116318     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-7-101     Document Type: Review

References (76)

1. Papagno L, Spina CA, Marchant A, Salio M, Rufer N, Little S, Dong T, Chesney G, Waters A, Easterbrook P, Dunbar PR, Shepherd D, Cerundolo V, Emery V, Griffiths P, Conlon C, McMichael AJ, Richman DD, Rowland-Jones SL, Appay V. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol 2004, 2:E20. 340937, 14966528, 10.1371/journal.pbio.0020020.
2. Silvestri G, Sodora DL, Koup RA, Paiardini M, O'Neil SP, McClure HM, Staprans SI, Feinberg MB. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 2003, 18:441-452. 10.1016/S1074-7613(03)00060-8, 12648460.
3. Rowland-Jones SL, Whittle HC. Out of Africa: what can we learn from HIV-2 about protective immunity to HIV-1?. Nat Immunol 2007, 8:329-331. 10.1038/ni0407-329, 17375091.
4. Keiser P, Keay S, Wasserman S, Wecksler W. Anti-CD4 antibodies are associated with HIV-1 seroconversion and may be detectable before anti-HIV-1 antibodies. The Multicenter AIDS Cohort Study. AIDS Res Hum Retroviruses 1992, 8:1919-1927. 10.1089/aid.1992.8.1919, 1489580.
5. Tomaras GD, Yates NL, Liu P, Qin L, Fouda GG, Chavez LL, Decamp AC, Parks RJ, Ashley VC, Lucas JT, Cohen M, Eron J, Hicks CB, Liao HX, Self SG, Landucci G, Forthal DN, Weinhold KJ, Keele BF, Hahn BH, Greenberg ML, Morris L, Karim SS, Blattner WA, Montefiori DC, Shaw GM, Perelson AS, Haynes BF. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J Virol 2008, 82:12449-12463. 2593361, 18842730, 10.1128/JVI.01708-08.
6. Davis KL, Gray ES, Moore PL, Decker JM, Salomon A, Montefiori DC, Graham BS, Keefer MC, Pinter A, Morris L, Hahn BH, Shaw GM. High titer HIV-1 V3-specific antibodies with broad reactivity but low neutralizing potency in acute infection and following vaccination. Virology 2009, 387:414-426. 10.1016/j.virol.2009.02.022, 19298995.
7. Oswald-Richter K, Grill SM, Shariat N, Leelawong M, Sundrud MS, Haas DW, Unutmaz D. HIV infection of naturally occurring and genetically reprogrammed human regulatory T-cells. PLoS Biol 2004, 2:E198. 449855, 15252446, 10.1371/journal.pbio.0020198.
8. Rawson PM, Molette C, Videtta M, Altieri L, Franceschini D, Donato T, Finocchi L, Propato A, Paroli M, Meloni F, Mastroianni CM, d'Ettorre G, Sidney J, Sette A, Barnaba V. Cross-presentation of caspase-cleaved apoptotic self antigens in HIV infection. Nat Med 2007, 13:1431-1439. 10.1038/nm1679, 18026114.
9. Ansari AA. Autoimmunity, anergy, lentiviral immunity and disease. Autoimmun Rev 2004, 3:530-540. 10.1016/j.autrev.2004.07.009, 15546802.
10. Klatt NR, Villinger F, Bostik P, Gordon SN, Pereira L, Engram JC, Mayne A, Dunham RM, Lawson B, Ratcliffe SJ, Sodora DL, Else J, Reimann K, Staprans SI, Haase AT, Estes JD, Silvestri G, Ansari AA. Availability of activated CD4+ T cells dictates the level of viremia in naturally SIV-infected sooty mangabeys. J Clin Invest 2008, 118:2039-2049. 2391063, 18497876.
11. Kuwata T, Nishimura Y, Whitted S, Ourmanov I, Brown CR, Dang Q, Buckler-White A, Iyengar R, Brenchley JM, Hirsch VM. Association of progressive CD4(+) T cell decline in SIV infection with the induction of autoreactive antibodies. PLoS Pathog 2009, 5:e1000372. 2662887, 19360097, 10.1371/journal.ppat.1000372.
12. Zarling JM, Ledbetter JA, Sias J, Fultz P, Eichberg J, Gjerset G, Moran PA. HIV-infected humans, but not chimpanzees, have circulating cytotoxic T lymphocytes that lyse uninfected CD4+ cells. J Immunol 1990, 144:2992-2998.
13. Kaufmann GR, Perrin L, Pantaleo G, Opravil M, Furrer H, Telenti A, Hirschel B, Ledergerber B, Vernazza P, Bernasconi E, Rickenbach M, Egger M, Battegay M. CD4 T-lymphocyte recovery in individuals with advanced HIV-1 infection receiving potent antiretroviral therapy for 4 years: the Swiss HIV Cohort Study. Arch Intern Med 2003, 163:2187-2195. 10.1001/archinte.163.18.2187, 14557216.
14. Salemi S, Caporossi AP, Boffa L, Longobardi MG, Barnaba V. HIVgp120 activates autoreactive CD4-specific T cell responses by unveiling of hidden CD4 peptides during processing. J Exp Med 1995, 181:2253-2257. 2192056, 7760011, 10.1084/jem.181.6.2253.
15. Caporossi AP, Bruno G, Salemi S, Mastroianni C, Falciano M, Salotti A, Bergami N, Santilio I, Nisini R, Barnaba V. Autoimmune T-cell response to the CD4 molecule in HIV-infected patients. Viral Immunol 1998, 11:9-17. 10.1089/vim.1998.11.9, 9586693.
16. Abulafia-Lapid R, Mayan S, Bentwich Z, Keren-Zur Y, Avbramovitz Y, Cohen IR, Atlan H. T-cell vaccination against anti-CD4 autoimmunity in HIV-1 subtypes B and C-infected patients--an extended open trial. Vaccine 2005, 23:2149-2153. 10.1016/j.vaccine.2005.01.054, 15755585.
17. Schubert U, Bour S, Willey RL, Strebel K. Regulation of virus release by the macrophage-tropic human immunodeficiency virus type 1 AD8 isolate is redundant and can be controlled by either Vpu or Env. J Virol 1999, 73:887-896. 103908, 9882289.
18. Fujita K, Omura S, Silver J. Rapid degradation of CD4 in cells expressing human immunodeficiency virus type 1 Env and Vpu is blocked by proteasome inhibitors. J Gen Virol 1997, 78(Pt 3):619-625.
19. Kerkau T, Bacik I, Bennink JR, Yewdell JW, Hunig T, Schimpl A, Schubert U. The human immunodeficiency virus type 1 (HIV-1) Vpu protein interferes with an early step in the biosynthesis of major histocompatibility complex (MHC) class I molecules. J Exp Med 1997, 185:1295-1305. 2196253, 9104816, 10.1084/jem.185.7.1295.
20. Paul M, Jabbar MA. Phosphorylation of both phosphoacceptor sites in the HIV-1 Vpu cytoplasmic domain is essential for Vpu-mediated ER degradation of CD4. Virology 1997, 232:207-216. 10.1006/viro.1997.8541, 9185604.
21. D'Aloja P, Olivetta E, Bona R, Nappi F, Pedacchia D, Pugliese K, Ferrari G, Verani P, Federico M. gag, vif, and nef genes contribute to the homologous viral interference induced by a nonproducer human immunodeficiency virus type 1 (HIV-1) variant: identification of novel HIV-1-inhibiting viral protein mutants. J Virol 1998, 72:4308-4319. 109661, 9557721.
22. Manca F, Seravalli E, Valle MT, Fenoglio D, Kunkl A, Li Pira G, Zolla-Pazner S, Celada F. Non-covalent complexes of HIV gp120 with CD4 and/or mAbs enhance activation of gp120-specific T clones and provide intermolecular help for anti-CD4 antibody production. Int Immunol 1993, 5:1109-1117. 10.1093/intimm/5.9.1109, 7902128.
23. Manca F, Fenoglio D, Li Pira G, Kunkl A, Celada F. Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies. J Exp Med 1991, 173:37-48. 2118742, 1985125, 10.1084/jem.173.1.37.
24. Manca F, Fenoglio D, Kunkl A, Cambiaggi C, Sasso M, Celada F. Differential activation of T cell clones stimulated by macrophages exposed to antigen complexed with monoclonal antibodies. J Immunol 1988, 140:2893-2898.
25. Hasler P. Biological therapies directed against cells in autoimmune disease. Springer Semin Immunopathol 2006, 27:443-456. 10.1007/s00281-006-0013-8, 16738955.
26. Moreland LW, Pratt PW, Bucy RP, Jackson BS, Feldman JW, Koopman WJ. Treatment of refractory rheumatoid arthritis with a chimeric anti-CD4 monoclonal antibody. Arthritis Rheum 1994, 37:834-838. 10.1002/art.1780370610, 7911664.
27. Jabado N, Pallier A, Le Deist F, Bernard F, Fischer A, Hivroz C. CD4 ligands inhibit the formation of multifunctional transduction complexes involved in T cell activation. J Immunol 1997, 158:94-103.
28. Tsygankov AY, Broker BM, Guse AH, Meinke U, Roth E, Rossmann C, Emmrich F. Preincubation with anti-CD4 influences activation of human T cells by subsequent co-cross-linking of CD4 with CD3. J Leukoc Biol 1993, 54:430-438.
29. Carrel S, Moretta A, Pantaleo G, Tambussi G, Isler P, Perussia B, Cerottini JC. Stimulation and proliferation of CD4+ peripheral blood T lymphocytes induced by an anti-CD4 monoclonal antibody. Eur J Immunol 1988, 18:333-339. 10.1002/eji.1830180303, 3258562.
30. Herzog C, Walker C, Muller W, Rieber P, Reiter C, Riethmuller G, Wassmer P, Stockinger H, Madic O, Pichler WJ. Anti-CD4 antibody treatment of patients with rheumatoid arthritis: I. Effect on clinical course and circulating T cells. J Autoimmun 1989, 2:627-642. 10.1016/S0896-8411(89)80002-2, 2572230.
31. Horneff G, Burmester GR, Emmrich F, Kalden JR. Treatment of rheumatoid arthritis with an anti-CD4 monoclonal antibody. Arthritis Rheum 1991, 34:129-140. 10.1002/art.1780340202, 1994909.
32. Epstein WV. Expectation bias in rheumatoid arthritis clinical trials. The anti-CD4 monoclonal antibody experience. Arthritis Rheum 1996, 39:1773-1780. 10.1002/art.1780391102, 8912498.
33. Choy EH, Connolly DJ, Rapson N, Jeal S, Brown JC, Kingsley GH, Panayi GS, Johnston JM. Pharmacokinetic, pharmacodynamic and clinical effects of a humanized IgG1 anti-CD4 monoclonal antibody in the peripheral blood and synovial fluid of rheumatoid arthritis patients. Rheumatology (Oxford) 2000, 39:1139-1146. 10.1093/rheumatology/39.10.1139, 11035136.
34. Qin SX, Cobbold S, Benjamin R, Waldmann H. Induction of classical transplantation tolerance in the adult. J Exp Med 1989, 169:779-794. 2189271, 2647894, 10.1084/jem.169.3.779.
35. Gutstein NL, Seaman WE, Scott JH, Wofsy D. Induction of immune tolerance by administration of monoclonal antibody to L3T4. J Immunol 1986, 137:1127-1132.
36. Benjamin RJ, Waldmann H. Induction of tolerance by monoclonal antibody therapy. Nature 1986, 320:449-451. 10.1038/320449a0, 2938014.
37. Morel P, Revillard JP, Nicolas JF, Wijdenes J, Rizova H, Thivolet J. Anti-CD4 monoclonal antibody therapy in severe psoriasis. J Autoimmun 1992, 5:465-477. 10.1016/0896-8411(92)90006-C, 1384529.
38. Hiepe F, Volk HD, Apostoloff E, von Baehr R, Emmrich F. Treatment of severe systemic lupus erythematosus with anti-CD4 monoclonal antibody. Lancet 1991, 338:1529-1530. 10.1016/0140-6736(91)92353-4, 1683954.
39. Racadot E, Rumbach L, Bataillard M, Galmiche J, Henlin JL, Truttmann M, Herve P, Wijdenes J. Treatment of multiple sclerosis with anti-CD4 monoclonal antibody. A preliminary report on B-F5 in 21 patients. J Autoimmun 1993, 6:771-786. 10.1006/jaut.1993.1063, 8155256.
40. Pohlers D, Schmidt-Weber CB, Franch A, Kuhlmann J, Brauer R, Emmrich F, Kinne RW. Differential clinical efficacy of anti-CD4 monoclonal antibodies in rat adjuvant arthritis is paralleled by differential influence on NF-kappaB binding activity and TNF-alpha secretion of T cells. Arthritis Res 2002, 4:184-189. 111020, 12010568, 10.1186/ar404.
41. Skov L, Kragballe K, Zachariae C, Obitz ER, Holm EA, Jemec GB, Solvsten H, Ibsen HH, Knudsen L, Jensen P, Petersen JH, Menne T, Baadsgaard O. HuMax-CD4: a fully human monoclonal anti-CD4 antibody for the treatment of psoriasis vulgaris. Arch Dermatol 2003, 139:1433-1439. 10.1001/archderm.139.11.1433, 14623703.
42. Di Somma MM, Majolini MB, Burastero SE, Telford JL, Baldari CT. Cyclosporin A sensitivity of the HIV-1 long terminal repeat identifies distinct p56lck-dependent pathways activated by CD4 triggering. Eur J Immunol 1996, 26:2181-2188. 10.1002/eji.1830260933, 8814265.
43. Cron RQ, Bartz SR, Clausell A, Bort SJ, Klebanoff SJ, Lewis DB. NFAT1 enhances HIV-1 gene expression in primary human CD4 T cells. Clin Immunol 2000, 94:179-191. 10.1006/clim.1999.4831, 10692237.
44. Schwarz A, Offermann G, Keller F, Bennhold I, L'Age-Stehr J, Krause PH, Mihatsch MJ. The effect of cyclosporine on the progression of human immunodeficiency virus type 1 infection transmitted by transplantation--data on four cases and review of the literature. Transplantation 1993, 55:95-103. 10.1097/00007890-199301000-00019, 8420072.
45. Denisova G, Lideman L, Spectorman E, Abulafia-Lapid R, Burke M, Yust I, Gershoni JM. Characterization of new monoclonal antibodies that discriminate between soluble and membrane CD4 and compete with human anti-CD4 autoimmune sera. Mol Immunol 2003, 40:231-239. 10.1016/S0161-5890(03)00147-0, 12943795.
46. Jacobson JM, Kuritzkes DR, Godofsky E, Dejesus E, Larson JA, Weinheimer SP, Lewis ST. Safety, Pharmacokinetics, and Antiretroviral Activity of Multiple Doses of Ibalizumab (formerly TNX-355), an Anti-CD4 Monoclonal Antibody, in HIV-1 Infected Adults. Antimicrob Agents Chemother 2008,
47. Boon L, Holland B, Gordon W, Liu P, Shiau F, Shanahan W, Reimann KA, Fung M. Development of anti-CD4 MAb hu5A8 for treatment of HIV-1 infection: preclinical assessment in non-human primates. Toxicology 2002, 172:191-203. 10.1016/S0300-483X(02)00002-1, 11893418.
48. Burkly LC, Olson D, Shapiro R, Winkler G, Rosa JJ, Thomas DW, Williams C, Chisholm P. Inhibition of HIV infection by a novel CD4 domain 2-specific monoclonal antibody. Dissecting the basis for its inhibitory effect on HIV-induced cell fusion. J Immunol 1992, 149:1779-1787.
49. Visciano ML, Tuen M, Gorny MK, Hioe CE. In vivo alteration of humoral responses to HIV-1 envelope glycoprotein gp120 by antibodies to the CD4-binding site of gp120. Virology 2008, 372:409-420. 2288784, 18054978, 10.1016/j.virol.2007.10.044.
50. Kalyanaraman VS, Rausch DM, Osborne J, Padgett M, Hwang KM, Lifson JD, Eiden LE. Evidence by peptide mapping that the region CD4(81-92) is involved in gp120/CD4 interaction leading to HIV infection and HIV-induced syncytium formation. J Immunol 1990, 145:4072-4078.
51. Moebius U, Clayton LK, Abraham S, Harrison SC, Reinherz EL. The human immunodeficiency virus gp120 binding site on CD4: delineation by quantitative equilibrium and kinetic binding studies of mutants in conjunction with a high-resolution CD4 atomic structure. J Exp Med 1992, 176:507-517. 2119328, 1500858, 10.1084/jem.176.2.507.
52. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, Hendrickson WA. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 1998, 393:648-659. 10.1038/31405, 9641677.
53. Gay D, Maddon P, Sekaly R, Talle MA, Godfrey M, Long E, Goldstein G, Chess L, Axel R, Kappler J. Functional interaction between human T-cell protein CD4 and the major histocompatibility complex HLA-DR antigen. Nature 1987, 328:626-629. 10.1038/328626a0, 3112582.
54. Xiang SH, Doka N, Choudhary RK, Sodroski J, Robinson JE. Characterization of CD4-induced epitopes on the HIV type 1 gp120 envelope glycoprotein recognized by neutralizing human monoclonal antibodies. AIDS Res Hum Retroviruses 2002, 18:1207-1217. 10.1089/08892220260387959, 12487827.
55. Lusso P, Earl PL, Sironi F, Santoro F, Ripamonti C, Scarlatti G, Longhi R, Berger EA, Burastero SE. Cryptic nature of a conserved, CD4-inducible V3 loop neutralization epitope in the native envelope glycoprotein oligomer of CCR5-restricted, but not CXCR4-using, primary human immunodeficiency virus type 1 strains. J Virol 2005, 79:6957-6968. 1112133, 15890935, 10.1128/JVI.79.11.6957-6968.2005.
56. Sullivan N, Sun Y, Sattentau Q, Thali M, Wu D, Denisova G, Gershoni J, Robinson J, Moore J, Sodroski J. CD4-Induced conformational changes in the human immunodeficiency virus type 1 gp120 glycoprotein: consequences for virus entry and neutralization. J Virol 1998, 72:4694-4703. 109994, 9573233.
57. Gershoni JM, Denisova G, Raviv D, Smorodinsky NI, Buyaner D. HIV binding to its receptor creates specific epitopes for the CD4/gp120 complex. FASEB J 1993, 7:1185-1187.
58. Celada F, Cambiaggi C, Maccari J, Burastero S, Gregory T, Patzer E, Porter J, McDanal C, Matthews T. Antibody raised against soluble CD4-rgp120 complex recognizes the CD4 moiety and blocks membrane fusion without inhibiting CD4-gp120 binding. J Exp Med 1990, 172:1143-1150. 2188612, 2212945, 10.1084/jem.172.4.1143.
59. Burastero SE. anti-human CD4-HIV-1-gp120 complex DB81 monoclonal antibody immunoglobulin kappa chain [Mus musculus]. 2008,
60. Burastero SE. anti-human CD4-HIV-1-gp120 complex DB81 monoclonal antibody immunoglobulin heavy chain [Mus musculus]. 2008,
61. Chams V, Jouault T, Fenouillet E, Gluckman JC, Klatzmann D. Detection of anti-CD4 autoantibodies in the sera of HIV-infected patients using recombinant soluble CD4 molecules. AIDS 1988, 2:353-361. 10.1097/00002030-198810000-00004, 3146263.
62. Sekigawa I, Groopmen JE, Allan JD, Ikeuchi K, Biberfield G, Takatsuki K, Byrn RA. Characterization of autoantibodies to the CD4 molecule in human immunodeficiency virus infection. Clin Immunol Immunopathol 1991, 58:145-153. 10.1016/0090-1229(91)90156-5, 1983967.
63. Kowalski M, Ardman B, Basiripour L, Lu YC, Blohm D, Haseltine W, Sodroski J. Antibodies to CD4 in individuals infected with human immunodeficiency virus type 1. Proc Natl Acad Sci USA 1989, 86:3346-3350. 287129, 2541442, 10.1073/pnas.86.9.3346.
64. Abulafia-Lapid R, Keren-Zur Y, Yachnin Y, Atlan H. Major CD4 epitopes involved in anti-CD4 T-cell autoimmunity in HIV-1 patients. Vaccine 2007, 25:3192-3199. 10.1016/j.vaccine.2007.01.040, 17298856.
65. Burastero SE, Gaffi D, Lopalco L, Tambussi G, Borgonovo B, De Santis C, Abecasis C, Robbioni P, Gasparri A, Lazzarin A, Celada F, Siccardi AG, Beretta A. Autoantibodies to CD4 in HIV type 1-exposed seronegative individuals. AIDS Res Hum Retroviruses 1996, 12:273-280. 10.1089/aid.1996.12.273, 8906987.
66. Furci L, Beretta A, Siccardi A, Lazzarin A, Confetti C, Magnani Z, Scarpellini P, Lopalco L, Burastero SE. Human immunodeficiency virus type 1 glycoprotein 120-specific T lymphocytes provide intermolecular help for anti-CD4 autoantibody production in exposed uninfected subjects. AIDS Res Hum Retroviruses 1997, 13:1461-1469. 10.1089/aid.1997.13.1461, 9390745.
67. Lopalco L, Magnani Z, Confetti C, Brianza M, Saracco A, Ferraris G, Lillo F, Vegni C, Lazzarin A, Siccardi AG, Burastero SE. Anti-CD4 antibodies in exposed seronegative adults and in newborns of HIV type 1-seropositive mothers: a follow-up study. AIDS Res Hum Retroviruses 1999, 15:1079-1085. 10.1089/088922299310377, 10461828.
68. Lopalco L, Barassi C, Paolucci C, Breda D, Brunelli D, Nguyen M, Nouhin J, Luong TT, Truong LX, Clerici M, Calori G, Lazzarin A, Pancino G, Burastero SE. Predictive value of anti-cell and anti-human immunodeficiency virus (HIV) humoral responses in HIV-1-exposed seronegative cohorts of European and Asian origin. J Gen Virol 2005, 86:339-348. 10.1099/vir.0.80585-0, 15659753.
69. Burastero SE, Casoli C, Paolucci C, Breda D, Alberti C, Pastori C, Lopalco L. Anti-CD4-gp120 complex antibodies in long-term non-progressors HIV-1 positive patients: a role in slowing disease progression?. Retrivirology 2006, 3(suppl 1):36.
70. Lopalco L, Burastero SE. HIV-1 and the self-nonself connection: how to sleep with the enemy and be much better off. AIDS Rev 2008, 10:162-171.
71. Novotny J, Handschumacher M, Haber E, Bruccoleri RE, Carlson WB, Fanning DW, Smith JA, Rose GD. Antigenic determinants in proteins coincide with surface regions accessible to large probes (antibody domains). Proc Natl Acad Sci USA 1986, 83:226-230. 322830, 2417241, 10.1073/pnas.83.2.226.
72. Pastori C, Clivio A, Diomede L, Consonni R, De Mori GM, Longhi R, Colombo G, Lopalco L. Two amino acid substitutions within the first external loop of CCR5 induce human immunodeficiency virus-blocking antibodies in mice and chickens. J Virol 2008, 82:4125-4134. 2293020, 18256149, 10.1128/JVI.02232-07.
73. Kang CY, Hariharan K, Nara PL, Sodroski J, Moore JP. Immunization with a soluble CD4-gp120 complex preferentially induces neutralizing anti-human immunodeficiency virus type 1 antibodies directed to conformation-dependent epitopes of gp120. J Virol 1994, 68:5854-5862. 236990, 7520095.
74. Fouts TR, Tuskan R, Godfrey K, Reitz M, Hone D, Lewis GK, DeVico AL. Expression and characterization of a single-chain polypeptide analogue of the human immunodeficiency virus type 1 gp120-CD4 receptor complex. J Virol 2000, 74:11427-11436. 112421, 11090138, 10.1128/JVI.74.24.11427-11436.2000.
75. Martin L, Stricher F, Misse D, Sironi F, Pugniere M, Barthe P, Prado-Gotor R, Freulon I, Magne X, Roumestand C, Menez A, Lusso P, Veas F, Vita C. Rational design of a CD4 mimic that inhibits HIV-1 entry and exposes cryptic neutralization epitopes. Nat Biotechnol 2003, 21:71-76. 10.1038/nbt768, 12483221.
76. Pulito VL, Roberts VA, Adair JR, Rothermel AL, Collins AM, Varga SS, Martocello C, Bodmer M, Jolliffe LK, Zivin RA. Humanization and molecular modeling of the anti-CD4 monoclonal antibody, OKT4A. J Immunol 1996, 156:2840-2850.