206
Views
40
CrossRef citations to date
0
Altmetric
Articles

Carbohydrate-functionalized nanovaccines preserve HIV-1 antigen stability and activate antigen presenting cells

, , , , &
Pages 1387-1406 | Received 01 May 2014, Accepted 27 Jun 2014, Published online: 28 Jul 2014

References

  • Geijtenbeek TB, Gringhuis SI. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 2009;9:465–479.10.1038/nri2569
  • Keler T, Ramakrishna V, Fanger MW. Mannose receptor-targeted vaccines. Expert Opin. Biol. Ther. 2004;4:1953–1962.10.1517/14712598.4.12.1953
  • Irache JM, Salman HH, Gamazo C, Espuelas S. Mannose-targeted systems for the delivery of therapeutics. Expert Opin. Drug Deliv. 2008;5:703–724.10.1517/edd.2008.5.issue-6
  • Deng Z, Li S, Jiang X, Narain R. Well-defined galactose-containing multi-functional copolymers and glyconanoparticles for biomolecular recognition processes. Macromolecules. 2009;42:6393–6405.10.1021/ma9010457
  • Song EH, Osanya AO, Petersen CA, Pohl NL. Synthesis of multivalent tuberculosis and Leishmania-associated capping carbohydrates reveals structure-dependent responses allowing immune evasion. J. Am. Chem. Soc. 2010;132:11428–11430.10.1021/ja103351m
  • Engering AJ, Cella M, Fluitsma D, Brockhaus M, Hoefsmit EC, Lanzavecchia A, Pieters J. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur. J. Immunol. 1997;27:2417–2425.10.1002/(ISSN)1521-4141
  • Upham JP, Pickett D, Irimura T, Anders EM, Reading PC. Macrophage receptors for influenza A virus: role of the macrophage galactose-type lectin and mannose receptor in viral entry. J. Virol. 2010;84:3730–3737.10.1128/JVI.02148-09
  • Jiang HL, Kang ML, Quan JS, Kang SG, Akaike T, Yoo HS, Cho CS. The potential of mannosylated chitosan microspheres to target macrophage mannose receptors in an adjuvant-delivery system for intranasal immunization. Biomaterials. 2008;29:1931–1939.10.1016/j.biomaterials.2007.12.025
  • Figdor CG, van Kooyk Y, Adema GJ. C-type lectin receptors on dendritic cells and Langerhans cells. Nat. Rev. Immunol. 2002;2:77–84.10.1038/nri723
  • Cambi A, Figdor CG. Dual function of C-type lectin-like receptors in the immune system. Curr. Opin. Cell Biol. 2003;15:539–546.10.1016/j.ceb.2003.08.004
  • Stahl PD. The mannose receptor and other macrophage lectins. Curr. Opin. Immunol. 1992;4:49–52.10.1016/0952-7915(92)90123-V
  • Pyż E, Marshall AS, Gordon S, Brown GD. C-type lectin-like receptors on myeloid cells. Ann. Med. 2006;38:242–251.10.1080/07853890600608985
  • Chehimi J, Luo Q, Azzoni L, Shawver L, Ngoubilly N, June R, Jerandi G, Farabaugh M, Montaner LJ. HIV-1 transmission and cytokine-induced expression of DC-SIGN in human monocyte-derived macrophages. J. Leukoc. Biol. 2003;74:757–763.10.1189/jlb.0503231
  • Herbein G, Gras G, Khan KA, Abbas W. Macrophage signaling in HIV-1 infection. Retrovirology. 2010;7:34.10.1186/1742-4690-7-34
  • Gringhuis SI, van der Vlist M, van den Berg LM, den Dunnen J, Litjens M, Geijtenbeek TB. HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 2010;11:419–426.10.1038/ni.1858
  • Mascola JR, Montefiori DC. The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 2010;28:413–444.10.1146/annurev-immunol-030409-101256
  • Zolla-Pazner S. Identifying epitopes of HIV-1 that induce protective antibodies. Nat. Rev. Immunol. 2004;4:199–210.10.1038/nri1307
  • UNAIDS. Global report: UNAIDS report on the global AIDS epidemic 2010. Geneva: United Nations; 2010.
  • McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. The immune response during acute HIV-1 infection: clues for vaccine development. Nat. Rev. Immunol. 2010;10:11–23.10.1038/nri2674
  • Catalfamo M, Di Mascio M, Hu Z, Srinivasula S, Thaker V, Adelsberger J, Rupert A, Baseler M, Tagaya Y, Roby G, Rehm C, Follmann D, Lane HC. HIV infection-associated immune activation occurs by two distinct pathways that differentially affect CD4 and CD8 T cells. Proc. Natl. Acad. Sci. U.S.A. 2008;105:19851–19856.10.1073/pnas.0810032105
  • Karlsson Hedestam GB, Fouchier RA, Phogat S, Burton DR, Sodroski J, Wyatt RT. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 2008;6:143–155.
  • Nguyen DG, Hildreth JE. Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages. Eur. J. Immunol. 2003;33:483–493.10.1002/immu.200310024
  • Sol-Foulon N, Moris A, Nobile C, Boccaccio C, Engering A, Abastado JP, Heard JM, van Kooyk Y, Schwartz O. HIV-1 NEF-induced upregulation of DC-SIGN in dendritic cells promotes lymphocyte clustering and viral spread. Immunity. 2002;16:145–155.10.1016/S1074-7613(02)00260-1
  • Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. 2000;100:587–597.10.1016/S0092-8674(00)80694-7
  • Chung NP, Matthews K, Klasse PJ, Sanders RW, Moore JP. HIV-1 gp120 impairs the induction of B cell responses by TLR9-activated plasmacytoid dendritic cells. J. Immunol. 2012;189:5257–5265.
  • Scanlan CN, Offer J, Zitzmann N, Dwek RA. Exploiting the defensive sugars of HIV-1 for drug and vaccine design. Nature. 2007;446:1038–1045.10.1038/nature05818
  • Shi W, Bohon J, Han DP, Habte H, Qin Y, Cho MW, Chance MR. Structural characterization of HIV gp41 with the membrane-proximal external region. J. Biol. Chem. 2010;285:24290–24298.10.1074/jbc.M110.111351
  • Conix A. Poly[1,3-bis(p-carboxyphenoxy)-propane anhydride]. Macromol. Synth. 1966;2:95–98.
  • Kumar N, Langer RS, Domb AJ. Polyanhydrides: an overview. Adv. Drug Deliv. Rev. 2002;54:889–910.10.1016/S0169-409X(02)00050-9
  • Torres MP, Vogel BM, Narasimhan B, Mallapragada SK. Synthesis and characterization of novel polyanhydrides with tailored erosion mechanisms. J. Biomed. Mater. Res. A. 2006;76A:102–110.10.1002/(ISSN)1552-4965
  • Petersen LK, Sackett CK, Narasimhan B. High-throughput analysis of protein stability in polyanhydride nanoparticles. Acta Biomater. 2010;6:3873–3881.10.1016/j.actbio.2010.04.004
  • Carrillo-Conde B, Schiltz E, Yu J, Chris Minion F, Phillips GJ, Wannemuehler MJ, Narasimhan B. Encapsulation into amphiphilic polyanhydride microparticles stabilizes Yersinia pestis antigens. Acta Biomater. 2010;6:3110–3119.10.1016/j.actbio.2010.01.040
  • Ulery BD, Kumar D, Ramer-Tait AE, Metzger DW, Wannemuehler MJ, Narasimhan B. Design of a protective single-dose intranasal nanoparticle-based vaccine platform for respiratory infectious diseases. PLoS One. 2011;6:e17642. doi:17610.11371/journal.pone.0017642.10.1371/journal.pone.0017642
  • Kipper MJ, Wilson JH, Wannemuehler MJ, Narasimhan B. Single dose vaccine based on biodegradable polyanhydride microspheres can modulate immune response mechanism. J. Biomed Mater. Res. A. 2006;76A:798–810.10.1002/(ISSN)1552-4965
  • Ulery BD, Petersen LK, Phanse Y, Kong CS, Broderick SR, Kumar D, Ramer-Tait AE, Carrillo-Conde B, Rajan K, Wannemuehler MJ, Bellaire BH, Metzger DW, Narasimhan B. Rational design of pathogen-mimicking amphiphilic materials as nanoadjuvants. Sci. Rep. 2011;1:198. doi:10.1038/srep00198.
  • Penn-Nicholson A, Han DP, Kim SJ, Park H, Ansari R, Montefiori DC, Cho MW. Assessment of antibody responses against gp41 in HIV-1-infected patients using soluble gp41 fusion proteins and peptides derived from M group consensus envelope. Virology. 2008;372:442–456.10.1016/j.virol.2007.11.009
  • Gaiha GD, Dong T, Palaniyar N, Mitchell DA, Reid KB, Clark HW. Surfactant protein A binds to HIV and inhibits direct infection of CD4+ cells, but enhances dendritic cell-mediated viral transfer. J. Immunol. 2008;181:601–609.10.4049/jimmunol.181.1.601
  • Fantuzzi L, Canini I, Belardelli F, Gessani S. HIV-1 gp120 stimulates the production of beta-chemokines in human peripheral blood monocytes through a CD4-independent mechanism. J. Immunol. 2001;166:5381–5387.10.4049/jimmunol.166.9.5381
  • Shan M, Klasse PJ, Banerjee K, Dey AK, Iyer SP, Dionisio R, Charles D, Campbell-Gardener L, Olson WC, Sanders RW, Moore JP. HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells. PLoS Pathog. 2007;3:e169.10.1371/journal.ppat.0030169
  • Shen E, Pizsczek R, Dziadul B, Narasimhan B. Microphase separation in bioerodible copolymers for drug delivery. Biomaterials. 2001;22:201–210.10.1016/S0142-9612(00)00175-7
  • Torres MP, Wilson-Welder JH, Lopac SK, Phanse Y, Carrillo-Conde B, Ramer-Tait AE, Bellaire BH, Wannemuehler MJ, Narasimhan B. Polyanhydride microparticles enhance dendritic cell antigen presentation and activation. Acta Biomater. 2011;7:2857–2864.10.1016/j.actbio.2011.03.023
  • Kipper MJ, Shen E, Determan A, Narasimhan B. Design of an injectable system based on bioerodible polyanhydride microspheres for sustained drug delivery. Biomaterials. 2002;23:4405–4412.10.1016/S0142-9612(02)00181-3
  • Ulery BD, Phanse Y, Sinha A, Wannemuehler MJ, Narasimhan B, Bellaire BH. Polymer chemistry influences monocytic uptake of polyanhydride nanospheres. Pharm. Res. 2009;26:683–690.10.1007/s11095-008-9760-7
  • Jaipuri FA, Pohl NL. Toward solution-phase automated iterative synthesis: fluorous-tag assisted solution-phase synthesis of linear and branched mannose oligomers. Org. Biomol. Chem. 2008;6:2686–2691.10.1039/b803451f
  • Curran DP, Luo Z. Fluorous synthesis with fewer fluorines (light fluorous synthesis): separation of tagged from untagged products by solid-phase extraction with fluorous reverse-phase silica gel. J. Am. Chem. Soc. 1999;121:9069–9072.10.1021/ja991496r
  • Zhang W. Fluorous linker-facilitated chemical synthesis. Chem. Rev. 2009;109:749–795.10.1021/cr800412s
  • Zhang W, Curran DP. Synthetic applications of fluorous solid-phase extraction (F-SPE). Tetrahedron. 2006;62:11837–11865.10.1016/j.tet.2006.08.051
  • Carrillo-Conde B, Song EH, Chavez-Santoscoy A, Phanse Y, Ramer-Tait AE, Pohl NL, Wannemuehler MJ, Bellaire BH, Narasimhan B. Mannose-functionalized “pathogen-like” polyanhydride nanoparticles target C-type lectin receptors on dendritic cells. Mol. Pharm. 2011;8:1877–1886.10.1021/mp200213r
  • Chavez-Santoscoy AV, Roychoudhury R, Pohl NL, Wannemuehler MJ, Narasimhan B, Ramer-Tait AE. Tailoring the immune response by targeting C-type lectin receptors on alveolar macrophages using ‘pathogen-like’ amphiphilic polyanhydride nanoparticles. Biomaterials. 2012;33:4762–4772.10.1016/j.biomaterials.2012.03.027
  • Carrillo-Conde BR, Roychoudhury R, Chavez-Santoscoy AV, Narasimhan B, Pohl NL. High-throughput synthesis of carbohydrates and functionalization of polyanhydride nanoparticles. J. Vis. Exp. 2012;64:e3884. doi:10.3791/3884.
  • Phanse Y, Carrillo-Conde BR, Ramer-Tait AE, Roychoudhury R, Pohl NL, Narasimhan B, Wannemuehler MJ, Bellaire BH. Functionalization of polyanhydride microparticles with di-mannose influences uptake by and intracellular fate within dendritic cells. Acta Biomater. 2013;9:8902–8909.10.1016/j.actbio.2013.06.024
  • Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S, Lee YC. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal. Biochem. 2005;339:69–72.10.1016/j.ab.2004.12.001
  • Lopac SK, Torres MP, Wilson-Welder JH, Wannemuehler MJ, Narasimhan B. Effect of polymer chemistry and fabrication method on protein release and stability from polyanhydride microspheres. J. Biomed. Mater. Res. B Appl. Biomater. 2009;91B:938–947.10.1002/jbm.b.v91b:2
  • Torres MP, Determan AS, Anderson GL, Mallapragada SK, Narasimhan B. Amphiphilic polyanhydrides for protein stabilization and release. Biomaterials. 2007;28:108–116.10.1016/j.biomaterials.2006.08.047
  • Carrillo-Conde BR, Ramer-Tait AE, Wannemuehler MJ, Narasimhan B. Chemistry-dependent adsorption of serum proteins onto polyanhydride microparticles differentially influences dendritic cell uptake and activation. Acta Biomater. 2012;8:3618–3628.10.1016/j.actbio.2012.06.001
  • Buchacher A, Predl R, Strutzenberger K, Steinfellner W, Trkola A, Purtscher M, Gruber G, Tauer C, Steindl F, Jungbauer A, Katinger H. Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein–Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res. Hum. Retroviruses. 1994;10:359–369.10.1089/aid.1994.10.359
  • Purtscher M, Trkola A, Grassauer A, Schulz PM, Klima A, Döpper S, Gruber G, Buchacher A, Muster T, Katinger H. Restricted antigenic variability of the epitope recognized by the neutralizing gp41 antibody 2F5. AIDS. 1996;10:587–593.10.1097/00002030-199606000-00003
  • Purtscher M, Trkola A, Gruber G, Buchacher A, Predl R, Steindl F, Tauer C, Berger R, Barrett N, Jungbauer A, Katinger H. A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses. 1994;10:1651–1658.10.1089/aid.1994.10.1651
  • Nelson JD, Brunel FM, Jensen R, Crooks ET, Cardoso RM, Wang M, Hessell A, Wilson IA, Binley JM, Dawson PE, Burton DR, Zwick MB. An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J. Virol. 2007;81:4033–4043.10.1128/JVI.02588-06
  • Stiegler G, Kunert R, Purtscher M, Wolbank S, Voglauer R, Steindl F, Katinger H. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses. 2001;17:1757–1765.10.1089/08892220152741450
  • Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, Binley JM, Moore JP, Stiegler G, Katinger H, Burton DR, Parren PW. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 2001;75:10892–10905.10.1128/JVI.75.22.10892-10905.2001
  • Petersen LK, Xue L, Wannemuehler MJ, Rajan K, Narasimhan B. The simultaneous effect of polymer chemistry and device geometry on the in vitro activation of murine dendritic cells. Biomaterials. 2009;30:5131–5142.10.1016/j.biomaterials.2009.05.069
  • Petersen LK, Ramer-Tait AE, Broderick SR, Kong CS, Ulery BD, Rajan K, Wannemuehler MJ, Narasimhan B. Activation of innate immune responses in a pathogen-mimicking manner by amphiphilic polyanhydride nanoparticle adjuvants. Biomaterials. 2011;32:6815–6822.10.1016/j.biomaterials.2011.05.063
  • Determan AS, Graham JR, Pfeiffer KA, Narasimhan B. The role of microsphere fabrication methods on the stability and release kinetics of ovalbumin encapsulated in polyanhydride microspheres. J. Microencapsul. 2006;23:832–843.10.1080/02652040601033841
  • Petersen LK, Phanse Y, Ramer-Tait AE, Wannemuehler MJ, Narasimhan B. Amphiphilic polyanhydride nanoparticles stabilize Bacillus anthracis protective antigen. Mol. Pharm. 2012;9:874–882.10.1021/mp2004059
  • Adams EW, Ratner DM, Seeberger PH, Hacohen N. Carbohydrate-mediated targeting of antigen to dendritic cells leads to enhanced presentation of antigen to T cells. Chembiochem. 2008;9:294–303.10.1002/(ISSN)1439-7633
  • Turville S, Wilkinson J, Cameron P, Dable J, Cunningham AL. The role of dendritic cell C-type lectin receptors in HIV pathogenesis. J. Leukoc. Biol. 2003;74:710–718.10.1189/jlb.0503208
  • Berzi A, Varga N, Sattin S, Antonazzo P, Biasin M, Cetin I, Trabattoni D, Bernardi A, Clerici M. Pseudo-mannosylated DC-SIGN ligands as potential adjuvants for HIV vaccines. Viruses. 2014;6:391–403.10.3390/v6020391
  • Jameson B, Baribaud F, Pohlmann S, Ghavimi D, Mortari F, Doms RW, Iwasaki A. Expression of DC-SIGN by dendritic cells of intestinal and genital mucosae in humans and rhesus macaques. J. Virol. 2002;76:1866–1875.10.1128/JVI.76.4.1866-1875.2002
  • Cunningham AL, Harman AN, Donaghy H. DC-SIGN ‘AIDS’ HIV immune evasion and infection. Nat. Immunol. 2007;8:556–558.10.1038/ni0607-556
  • Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat. Med. 2005;11:S45–S53.10.1038/nm1213
  • Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, Noelle RJ. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev. 2009;229:152–172.10.1111/imr.2009.229.issue-1
  • McKenzie EJ, Taylor PR, Stillion RJ, Lucas AD, Harris J, Gordon S, Martinez-Pomares L. Mannose receptor expression and function define a new population of murine dendritic cells. J. Immunol. 2007;178:4975–4983.10.4049/jimmunol.178.8.4975
  • Ohtani M, Iyori M, Saeki A, Tanizume N, Into T, Hasebe A, Totsuka Y, Shibata K. Involvement of suppressor of cytokine signalling-1-mediated degradation of MyD88-adaptor-like protein in the suppression of Toll-like receptor 2-mediated signalling by the murine C-type lectin SIGNR1-mediated signalling. Cell. Microbiol. 2012;14:40–57.10.1111/cmi.2012.14.issue-1
  • Lewis JS, Zaveri TD, Crooks CP 2nd, Keselowsky BG. Microparticle surface modifications targeting dendritic cells for non-activating applications. Biomaterials. 2012;33:7221–7232.10.1016/j.biomaterials.2012.06.049
  • Saunders SP, Barlow JL, Walsh CM, Bellsoi A, Smith P, McKenzie AN, Fallon PG. C-type lectin SIGN-R1 has a role in experimental colitis and responsiveness to lipopolysaccharide. J. Immunol. 2010;184:2627–2637.10.4049/jimmunol.0901970

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.