Induction of HIV-blocking anti-CCR5 IgA in peyers's patches without histopathological alterations

Journal of Virology

Volumn 88, Issue 7, 2014, Pages 3623-3635

  Pastori, Claudia ^a   Diomede, Lorenzo ^a   Venuti, Assunta ^a   Fisher, Gregory ^b   Jarvik, Jonathan ^b   Bomsel, Morgane ^c   Sanvito, Francesca ^a   Lopalco, Lucia ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CHEMOKINE RECEPTOR CCR5; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; PROTEIN PRECURSOR;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ANTIGEN BINDING; ANTIVIRAL ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DOWN REGULATION; DRUG DOSAGE FORM COMPARISON; DRUG EFFICACY; DRUG SAFETY; EX VIVO STUDY; FEMALE; FLOCK HOUSE VIRUS; HISTOPATHOLOGY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNIZATION; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NODAVIRUS; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TOXICITY TESTING; TRANSCYTOSIS; VIRUS NEUTRALIZATION;

ADJUVANTS, IMMUNOLOGIC; ANIMAL STRUCTURES; ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; B-LYMPHOCYTES; CAPSID PROTEINS; DRUG CARRIERS; HISTOCYTOCHEMISTRY; IMMUNIZATION; IMMUNOGLOBULIN A; MICE; NODAVIRIDAE; PEYER'S PATCHES; RECEPTORS, CCR5; RECEPTORS, HIV; RECOMBINANT FUSION PROTEINS;

EID: 84895446661     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03663-13     Document Type: Article

References (46)

1. Klasse PJ, Shattock R, Moore JP. 2008. Antiretroviral drug-based microbicides to prevent HIV-1 sexual transmission. Annu. Rev. Med. 59:455-471. http://dx.doi.org/10.1146/annurev.med.59.061206.112737.
2. Barassi C, Lazzarin A, Lopalco L. 2004. CCR5-specific mucosal IgA in saliva and genital fluids of HIV-exposed seronegative subjects. Blood 104: 2205-2206. http://dx.doi.org/10.1182/blood-2004-06-2134.
3. Barassi C, Soprana E, Pastori C, Longhi R, Buratti E, Lillo F, Marenzi C, Lazzarin A, Siccardi AG, Lopalco L. 2005. Induction of murine mucosal CCR5-reactive antibodies as an anti-human immunodeficiency virus strategy. J. Virol. 79:6848-6858. http://dx.doi.org/10.1128/JVI.79 .11.6848-6858.2005.
4. Lopalco L, Barassi C, Pastori C, Longhi R, Burastero SE, Tambussi G, Mazzotta F, Lazzarin A, Clerici M, Siccardi AG. 2000. CCR5-reactive antibodies in seronegative partners of HIV-seropositive individuals down-modulate surface CCR5 in vivo and neutralize the infectivity of R5 strains of HIV-1 in vitro. J. Immunol. 164:3426-3433.
5. Pastori C, Clivio A, Diomede L, Consonni R, De Mori GM, Longhi R, Colombo G, Lopalco L. 2008. Two amino acid substitutions within the first external loop of CCR5 induce human immunodeficiency virusblocking antibodies in mice and chickens. J. Virol. 82:4125-4134. http: //dx.doi.org/10.1128/JVI.02232-07.
6. Pastori C, Weiser B, Barassi C, Uberti-Foppa C, Ghezzi S, Longhi R, Calori G, Burger H, Kemal K, Poli G, Lazzarin A, Lopalco L. 2006. Long-lasting CCR5 internalization by antibodies in a subset of long-term nonprogressors: a possible protective effect against disease progression. Blood 107:4825-4833. http://dx.doi.org/10.1182/blood-2005-06-2463.
7. Bouhlal H, Latry V, Requena M, Aubry S, Kaveri SV, Kazatchkine MD, Belec L, Hocini H. 2005. Natural antibodies to CCR5 from breast milk block infection of macrophages and dendritic cells with primary R5-tropic HIV-1. J. Immunol. 174:7202-7209.
8. Eslahpazir J, Jenabian MA, Bouhlal H, Hocini H, Carbonneil C, Gresenguet G, Keou FX, LeGoff J, Saidi H, Requena M, Nasreddine N, de Dieu Longo J, Kaveri SV, Belec L. 2008. Infection of macrophages and dendritic cells with primary R5-tropic human immunodeficiency virus type 1 inhibited by natural polyreactive anti-CCR5 antibodies purified from cervicovaginal secretions. Clin. Vaccine Immunol. 15:872-884. http://dx.doi.org/10.1128/CVI.00463-07.
9. Blanpain C, Doranz BJ, Vakili J, Rucker J, Govaerts C, Baik SS, Lorthioir O, Migeotte I, Libert F, Baleux F, Vassart G, Doms RW, Parmentier M. 1999. Multiple charged and aromatic residues in CCR5 amino-terminal domain are involved in high affinity binding of both chemokines and HIV-1 Env protein. J. Biol. Chem. 274:34719-34727. http://dx.doi.org/10.1074/jbc.274.49.34719.
10. Blanpain C, Vanderwinden JM, Cihak J, Wittamer V, Le Poul E, Issafras H, Stangassinger M, Vassart G, Marullo S, Schlndorff D, Parmentier M, Mack M. 2002. Multiple active states and oligomerization of CCR5 revealed by functional properties of monoclonal antibodies. Mol. Biol. Cell 13:723-737. http://dx.doi.org/10.1091/mbc.01-03-0129.
11. Olson WC, Jacobson JM. 2009. CCR5 monoclonal antibodies for HIV-1 therapy. Curr. Opin. HIV AIDS 4:104-111. http://dx.doi.org/10.1097 /COH.0b013e3283224015.
12. Grene E, Pinto LA, Landay AL, Kessler HA, Anderson SA, Dolan MJ, Shearer GM. 2001. Anti-CCR5 antibodies in sera of HIV-positive individuals. Hum. Immunol. 62:143-145. http://dx.doi.org/10.1016/S0198-8859(00)00243-3.
13. Haynes BF, Moody MA, Verkoczy L, Kelsoe G, Alam SM. 2005. Antibody polyspecificity and neutralization of HIV-1: a hypothesis. Hum. Antibodies 14:59-67.
14. Bogers WM, Bergmeier LA, Oostermeijer H, ten Haaft P, Wang Y, Kelly CG, Singh M, Heeney JL, Lehner T. 2004. CCR5 targeted SIV vaccination strategy preventing or inhibiting SIV infection. Vaccine 22:2974-2984. http://dx.doi.org/10.1016/j.vaccine.2004.02.050.
15. Chackerian B, Briglio L, Albert PS, Lowy DR, Schiller JT. 2004. Induction of autoantibodies toCCR5in macaquesandsubsequent effectsuponchallenge with an R5-tropic simian/human immunodeficiency virus. J. Virol. 78:4037-4047. http://dx.doi.org/10.1128/JVI.78.8.4037-4047.2004.
16. Chain BM, Noursadeghi M, Gardener M, Tsang J, Wright E. 2008. HIV blocking antibodies following immunisation with chimaeric peptides coding a short N-terminal sequence of the CCR5 receptor. Vaccine 26: 5752-5759. http://dx.doi.org/10.1016/j.vaccine.2008.08.025.
17. Misumi S, Nakayama D, Kusaba M, Iiboshi T, Mukai R, Tachibana K, Nakasone T, Umeda M, Shibata H, Endo M, Takamune N, Shoji S. 2006. Effects of immunization with CCR5-based cycloimmunogen on simian/HIVSF162P3 challenge. J. Immunol. 176:463-471.
18. Buratti E, McLain L, Tisminetzky S, Cleveland SM, Dimmock NJ, Baralle FE. 1998. The neutralizing antibody response against a conserved region of human immunodeficiency virus type 1 gp41 (amino acid residues 731-752) is uniquely directed against a conformational epitope. J. Gen. Virol. 79:2709-2716.
19. Buratti E, Tisminetzky SG, Scodeller ES, Baralle FE. 1996. Conformational display of two neutralizing epitopes of HIV-1 gp41 on the Flock House virus capsid protein. J. Immunol. Methods 197:7-18. http://dx.doi .org/10.1016/0022-1759(96)00097-X.
20. Schiappacassi M, Buratti E, D'Agaro P, Ciani L, Scodeller ES, Tisminetzky SG, Baralle FE. 1997. V3 loop core region serotyping of HIV-1 infected patients using the FHV epitope presenting system. J. Virol. Methods 63:121-127. http://dx.doi.org/10.1016/S0166-0934(96)02120-9.
21. Scodeller EA, Tisminetzky SG, Porro F, Schiappacassi M, De Rossi A, Chiecco-Bianchi L, Baralle FE. 1995.Anewepitope presenting system displays aHIV-1V3 loop sequence and induces neutralizing antibodies. Vaccine 13:1233-1239. http: //dx.doi.org/10.1016/0264-410X(95)00058-9.
22. Speir J, Chen Z, Reddy VS, Johnson JE. 2012. Flock House Virus capsid structure Protein Data Bank (PDB at EMBL-EBI) 4fsj record (X-ray diffraction, resolution 2.5A). http://www.ebi.ac.uk/pdbe-srv/view/entry/4fsj /summary_details.html.
23. Fisher GW, Adler SA, Fuhrman MH, Waggoner AS, Bruchez MP, Jarvik JW. 2010. Detection and quantification of beta2AR internalization in living cells using FAP-based biosensor technology. J. Biomol. Screen. 15: 703-709. http://dx.doi.org/10.1177/1087057110370892.
24. Wu Y, Tapia PH, Fisher GW, Waggoner AS, Jarvik J, Sklar LA. 2013. High-throughput flow cytometry compatible biosensor based on fluorogen activating protein technology. CytometryA83:220-226. http://dx.doi .org/10.1002/cyto.a.22242.
25. Binley JM, Cayanan CS, Wiley C, Schulke N, Olson WC, Burton DR. 2003. Redox-triggered infection by disulfide-shackled human immunodeficiency virus type 1 pseudovirions. J. Virol. 77:5678-5684. http://dx .doi.org/10.1128/JVI.77.10.5678-5684.2003.
26. Bomsel M, Pastori C, Tudor D, Alberti C, Garcia S, Ferrari D, Lazzarin A, Lopalco L. 2007. Natural mucosal antibodies reactive with first extracellular loop of CCR5 inhibit HIV-1 transport across human epithelial cells. AIDS 21:13-22. http://dx.doi.org/10.1097/QAD.0b013e328011049b.
27. Hanly W, Bennet BT, Artwohl JE. 1994. Overview of adjuvants. U.S. Department of Agriculture, Washington, DC. http://www.nal.usda.gov /awic/pubs/antibody/overview.htm.
28. Vogel FR, Powell MF. 1995. A compendium of vaccine adjuvants and excipients. Pharm. Biotechnol. 6:141-228. http://dx.doi.org/10.1007/978-1-4615-1823-5_7.
29. Joshi A, Nyakeriga AM, Ravi R, Garg H. 2011. HIV ENV glycoproteinmediated bystander apoptosis depends on expression of the CCR5 coreceptor at the cell surface and ENV fusogenic activity. J. Biol. Chem. 286:36404-36413. http://dx.doi.org/10.1074/jbc.M111.281659.
30. Lopalco L. 2011. Natural anti-CCR5 antibodies in HIV-infection and-exposure. J. Transl. Med. 9(Suppl 1):S4. http://dx.doi.org/10.1186/1479-5876-9-S1-S4.
31. Lopalco L, Bomsel M. 2011. Protecting the initial site of viral entry: an alternative HIV vaccine target. Expert Rev. Vaccines 10:1253-1256. http: //dx.doi.org/10.1586/erv.11.98.
32. Peabody DS, Manifold-Wheeler B, Medford A, Jordan SK, do Carmo Caldeira J, Chackerian B. 2008. Immunogenic display of diverse peptides on virus-like particles of RNA phage MS2. J. Mol. Biol. 380:252-263. http: //dx.doi.org/10.1016/j.jmb.2008.04.049.
33. Pastori C, Tudor D, Diomede L, Drillet AS, Jegerlehner A, Rohn TA, Bomsel M, Lopalco L. 2012. Virus like particle based strategy to elicit HIV-protective antibodies to the alpha-helic regions of gp41. Virology 431:1-11. http://dx.doi.org/10.1016/j.virol.2012.05.005.
34. Visciano ML, Diomede L, Tagliamonte M, Tornesello ML, Asti V, Bomsel M, Buonaguro FM, Lopalco L, Buonaguro L. 2011. Generation of HIV-1 virus-like particles expressing different HIV-1 glycoproteins. Vaccine 29:4903-4912. http://dx.doi.org/10.1016/j.vaccine.2011.05.005.
35. Lee B, Sharron M, Blanpain C, Doranz BJ, Vakili J, Setoh P, Berg E, Liu G, Guy HR, Durell SR, Parmentier M, Chang CN, Price K, Tsang M, Doms RW. 1999. Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J. Biol. Chem. 274:9617-9626. http://dx.doi .org/10.1074/jbc.274.14.9617.
36. Barnett SW, Srivastava IK, Kan E, Zhou F, Goodsell A, Cristillo AD, Ferrai MG, Weiss DE, Letvin NL, Montefiori D, Pal R, Vajdy M. 2008. Protection of macaques against vaginal SHIV challenge by systemic or mucosal and systemic vaccinations with HIV-envelope. AIDS 22:339-348. http://dx.doi.org/10.1097/QAD.0b013e3282f3ca57.
37. Bomsel M, Tudor D, Drillet AS, Alfsen A, Ganor Y, Roger MG, Mouz N, Amacker M, Chalifour A, Diomede L, Devillier G, Cong Z, Wei Q, Gao H, Qin C, Yang GB, Zurbriggen R, Lopalco L, Fleury S. 2011. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV challenges. Immunity 34:269-280. http://dx.doi.org/10.1016/j.immuni.2011.01.015.
38. Leroux-Roels G, Maes C, Clement F, van Engelenburg F, van den Dobbelsteen M, Adler M, Amacker M, Lopalco L, Bomsel M, Chalifour A, Fleury S. 2013. Randomized phase I: safety, immunogenicity and mucosal antiviral activity in young healthy women vaccinated with HIV-1 Gp41 P1 peptide on virosomes. PLoS One 8:e55438. http://dx.doi.org/10 .1371/journal.pone.0055438.
39. Vajdy M, Singh M, Kazzaz J, Soenawan E, Ugozzoli M, Zhou F, Srivastava I, Bin Q, Barnett S, Donnelly J, Luciw P, Adamson L, Montefiori D, O'Hagan DT. 2004. Mucosal and systemic anti-HIV responses in rhesus macaques following combinations of intranasal and parenteral immunizations. AIDS Res. Hum. Retroviruses 20:1269-1281. http://dx.doi.org/10.1089/aid.2004.20.1269.
40. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P. 1995. Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 270: 1811-1815. http://dx.doi.org/10.1126/science.270.5243.1811.
41. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. 2008. The immune geography of IgA induction and function. Mucosal Immunol. 1:11-22. http://dx.doi.org/10.1038/mi.2007.6.
42. Pabst O. 2012. New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 12:821-832. http://dx.doi.org/10.1038/nri3322.
43. Plotkin SA. 2010. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 17:1055-1065. http://dx.doi.org/10.1128/CVI.00131-10.
44. Tudor D, Yu H, Maupetit J, Drillet AS, Bouceba T, Schwartz-Cornil I, Lopalco L, Tuffery P, Bomsel M. 2012. Isotype modulates epitope specificity, affinity, and antiviral activities of anti-HIV-1 human broadly neutralizing 2F5 antibody. Proc. Natl. Acad. Sci. U. S. A. 109:12680-12685. http://dx.doi.org/10.1073/pnas.1200024109.
45. Corbeau P, Reynes J. 2009. CCR5 antagonism in HIV infection: ways, effects, and side effects. AIDS 23:1931-1943. http://dx.doi.org/10.1097 /QAD.0b013e32832e71cd.
46. Telenti A. 2009. Safety concerns about CCR5 as an antiviral target. Curr. Opin. HIV AIDS 4:131-135. http://dx.doi.org/10.1097/COH .0b013e3283223d76.