Antibody-mimetic ligand selected by mRNA display targets DC-SIGN for dendritic cell-directed antigen delivery

ACS Chemical Biology

Volumn 8, Issue 5, 2013, Pages 967-977

  Xiao, Liang ^a   Hung, Kuo Chan ^b   Takahashi, Terry T ^b   Joo, Kye Il ^a   Lim, Matthew ^a   Roberts, Richard W ^a,b   Wang, Pin ^a,b  

^a University of Southern California   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; DENDRITIC CELL VACCINE; FIBRONECTIN; MESSENGER RNA; SIPULEUCEL T; ANTIBODY; ANTIGEN; BIOMIMETIC MATERIAL; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; FIBRONECTIN TYPE III LIKE PEPTIDE, HUMAN; LECTIN; LIGAND; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELL ASSAY; CYTOKINE RELEASE; DENDRITIC CELL; DRUG DELIVERY SYSTEM; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROSTATE CANCER; ANIMAL; BINDING SITE; CELL SURFACE DISPLAY; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROCEDURES;

ANIMALS; ANTIBODIES; ANTIGENS; BASE SEQUENCE; BINDING SITES; BIOMIMETIC MATERIALS; CELL ADHESION MOLECULES; CELL SURFACE DISPLAY TECHNIQUES; DENDRITIC CELLS; DRUG DELIVERY SYSTEMS; FIBRONECTINS; HUMANS; LECTINS, C-TYPE; LIGANDS; MICE; MOLECULAR SEQUENCE DATA; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; RNA, MESSENGER;

EID: 84878062442     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300680c     Document Type: Article

References (48)

1. Mellman, I. and Steinman, R. M. (2001) Dendritic cells: specialized and regulated antigen processing machines Cell 106, 255-258 (Pubitemid 32772607)
2. Fajardo-Moser, M., Berzel, S., and Moll, H. (2008) Mechanisms of dendritic cell-based vaccination against infection Int. J. Med. Microbiol. 298, 11-20 (Pubitemid 350216547)
3. Wei, H., Wang, H., Lu, B., Li, B., Hou, S., Qian, W., Fan, K., Dai, J., Zhao, J., and Guo, Y. (2008) Cancer immunotherapy using in vitro genetically modified targeted dendritic cells Cancer Res. 68, 3854-3862
4. Boudreau, J. E., Bonehill, A., Thielemans, K., and Wan, Y. (2011) Engineering dendritic cells to enhance cancer immunotherapy Mol. Ther. 19, 841-853
5. Cheever, M. A. and Higano, C. S. (2011) PROVENGE (Sipuleucel-T) in prostate cancer: the first FDA-approved therapeutic cancer vaccine Clin. Cancer Res. 17, 3520-3526
6. Kantoff, P. W., Higano, C. S., Shore, N. D., Berger, E. R., Small, E. J., Penson, D. F., Redfern, C. H., Ferrari, A. C., Dreicer, R., Sims, R. B., Xu, Y., Frohlich, M. W., and Schellhammer, P. F. (2010) Sipuleucel-T immunotherapy for castration-resistant prostate cancer N. Engl. J. Med. 363, 411-422
7. Plosker, G. L. (2011) Sipuleucel-T: in metastatic castration-resistant prostate cancer Drugs 71, 101-108
8. Hammerstrom, A. E., Cauley, D. H., Atkinson, B. J., and Sharma, P. (2011) Cancer immunotherapy: sipuleucel-T and beyond Pharmacotherapy 31, 813-828
9. Tacken, P. J., de Vries, I. J., Torensma, R., and Figdor, C. G. (2007) Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting Nat. Rev. Immunol. 7, 790-802 (Pubitemid 47480309)
10. Figdor, C. G., van Kooyk, Y., and Adema, G. J. (2002) C-type lectin receptors on dendritic cells and Langerhans cells Nat. Rev. Immunol. 2, 77-84 (Pubitemid 37323231)
11. Geijtenbeek, T. B., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Adema, G. J., van Kooyk, Y., and Figdor, C. G. (2000) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses Cell 100, 575-585
12. Tacken, P. J., de Vries, I. J., Gijzen, K., Joosten, B., Wu, D., Rother, R. P., Faas, S. J., Punt, C. J., Torensma, R., Adema, G. J., and Figdor, C. G. (2005) Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody Blood 106, 1278-1285 (Pubitemid 41129591)
13. Park, C. G., Takahara, K., Umemoto, E., Yashima, Y., Matsubara, K., Matsuda, Y., Clausen, B. E., Inaba, K., and Steinman, R. M. (2001) Five mouse homologues of the human dendritic cell C-type lectin, DC-SIGN Int. Immunol. 13, 1283-1290 (Pubitemid 32994528)
14. Powlesland, A. S., Ward, E. M., Sadhu, S. K., Guo, Y., Taylor, M. E., and Drickamer, K. (2006) Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins J. Biol. Chem. 281, 20440-20449 (Pubitemid 44065817)
15. Takahara, K., Yashima, Y., Omatsu, Y., Yoshida, H., Kimura, Y., Kang, Y. S., Steinman, R. M., Park, C. G., and Inaba, K. (2004) Functional comparison of the mouse DC-SIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins Int. Immunol. 16, 819-829 (Pubitemid 38786523)
16. Yang, L., Yang, H., Rideout, K., Cho, T., Joo, K. I., Ziegler, L., Elliot, A., Walls, A., Yu, D., Baltimore, D., and Wang, P. (2008) Engineered lentivector targeting of dendritic cells for in vivo immunization Nat. Biotechnol. 26, 326-334 (Pubitemid 351355129)
17. Dai, B., Yang, L., Yang, H., Hu, B., Baltimore, D., and Wang, P. (2009) HIV-1 Gag-specific immunity induced by a lentivector-based vaccine directed to dendritic cells Proc. Natl. Acad. Sci. U.S.A. 106, 20382-20387
18. Xiao, L., Kim, J., Lim, M., Dai, B., Yang, L., Reed, S. G., Baltimore, D., and Wang, P. (2012) A TLR4 agonist synergizes with dendritic cell-directed lentiviral vectors for inducing antigen-specific immune responses Vaccine 30, 2570-2581
19. Yang, H., Hu, B., Xiao, L., and Wang, P. (2011) Dendritic cell-directed lentivector vaccine induces antigen-specific immune responses against murine melanoma Cancer Gene Ther. 18, 370-380
20. Roberts, R. W. and Szostak, J. W. (1997) RNA-peptide fusions for the in vitro selection of peptides and proteins Proc. Natl. Acad. Sci. U.S.A. 94, 12297-12302 (Pubitemid 27492522)
21. Takahashi, T. T. and Roberts, R. W. (2009) In vitro selection of protein and peptide libraries using mRNA display Methods Mol. Biol. 535, 293-314
22. Takahashi, T. T., Austin, R. J., and Roberts, R. W. (2003) mRNA display: ligand discovery, interaction analysis and beyond Trends Biochem. Sci. 28, 159-165 (Pubitemid 36293854)
23. Hayashi, Y., Morimoto, J., and Suga, H. (2012) In vitro selection of anti-Akt2 thioether-macrocyclic peptides leading to isoform-selective inhibitors ACS Chem. Biol. 7, 607-613
24. Jackrel, M. E., Cortajarena, A. L., Liu, T. Y., and Regan, L. (2010) Screening libraries to identify proteins with desired binding activities using a split-GFP reassembly assay ACS Chem. Biol. 5, 553-562
25. Olson, C. A., Liao, H. I., Sun, R., and Roberts, R. W. (2008) mRNA display selection of a high-affinity, modification-specific phospho- IkappaBalpha-binding fibronectin ACS Chem. Biol. 3, 480-485
26. Xu, L., Aha, P., Gu, K., Kuimelis, R. G., Kurz, M., Lam, T., Lim, A. C., Liu, H., Lohse, P. A., Sun, L., Weng, S., Wagner, R. W., and Lipovsek, D. (2002) Directed evolution of high-affinity antibody mimics using mRNA display Chem. Biol. 9, 933-942 (Pubitemid 35240913)
27. Koide, A., Bailey, C. W., Huang, X. L., and Koide, S. (1998) The fibronectin type III domain as a scaffold for novel binding proteins J. Mol. Biol. 284, 1141-1151 (Pubitemid 28558562)
28. Olson, C. A., Adams, J. D., Takahashi, T. T., Qi, H., Howell, S. M., Wu, T. T., Roberts, R. W., Sun, R., and Soh, H. T. (2011) Rapid mRNA-display selection of an IL-6 inhibitor using continuous-flow magnetic separation Angew. Chem., Int. Ed. 50, 8295-8298
29. Dakappagari, N., Maruyama, T., Renshaw, M., Tacken, P., Figdor, C., Torensma, R., Wild, M. A., Wu, D., Bowdish, K., and Kretz-Rommel, A. (2006) Internalizing antibodies to the C-type lectins, L-SIGN and DC-SIGN, inhibit viral glycoprotein binding and deliver antigen to human dendritic cells for the induction of T cell responses J. Immunol. 176, 426-440 (Pubitemid 43023289)
30. Cambi, A., Beeren, I., Joosten, B., Fransen, J. A., and Figdor, C. G. (2009) The C-type lectin DC-SIGN internalizes soluble antigens and HIV-1 virions via a clathrin-dependent mechanism Eur. J. Immunol. 39, 1923-1928
31. Joo, K. I., Lei, Y. N., Lee, C. L., Lo, J., Xie, J. S., Hamm-Alvarez, S. F., and Wang, P. (2008) Site-specific labeling of enveloped viruses with quantum dots for single virus tracking ACS Nano 2, 1553-1562
32. Tacken, P. J., Ginter, W., Berod, L., Cruz, L. J., Joosten, B., Sparwasser, T., Figdor, C. G., and Cambi, A. (2011) Targeting DC-SIGN via its neck region leads to prolonged antigen residence in early endosomes, delayed lysosomal degradation, and cross-presentation Blood 118, 4111-4119
33. Nijman, H. W., Houbiers, J. G., Vierboom, M. P., van der Burg, S. H., Drijfhout, J. W., D'Amaro, J., Kenemans, P., Melief, C. J., and Kast, W. M. (1993) Identification of peptide sequences that potentially trigger HLA-A2.1-restricted cytotoxic T lymphocytes Eur. J. Immunol. 23, 1215-1219 (Pubitemid 23165680)
34. Sundaram, R., Sun, Y., Walker, C. M., Lemonnier, F. A., Jacobson, S., and Kaumaya, P. T. (2003) A novel multivalent human CTL peptide construct elicits robust cellular immune responses in HLA-A*0201 transgenic mice: implications for HTLV-1 vaccine design Vaccine 21, 2767-2781 (Pubitemid 36705529)
35. Bernhard, O. K., Lai, J., Wilkinson, J., Sheil, M. M., and Cunningham, A. L. (2004) Proteomic analysis of DC-SIGN on dendritic cells detects tetramers required for ligand binding but no association with CD4 J. Biol. Chem. 279, 51828-51835 (Pubitemid 39656549)
36. Trombetta, E. S. and Mellman, I. (2005) Cell biology of antigen processing in vitro and in vivo Annu. Rev. Immunol. 23, 975-1028 (Pubitemid 40563191)
37. Kagi, D., Vignaux, F., Ledermann, B., Burki, K., Depraetere, V., Nagata, S., Hengartner, H., and Golstein, P. (1994) Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity Science 265, 528-530 (Pubitemid 24264998)
38. Tanaka, H., Yoshizawa, H., Yamaguchi, Y., Ito, K., Kagamu, H., Suzuki, E., Gejyo, F., Hamada, H., and Arakawa, M. (1999) Successful adoptive immunotherapy of murine poorly immunogenic tumor with specific effector cells generated from gene-modified tumor-primed lymph node cells J. Immunol. 162, 3574-3582 (Pubitemid 29313610)
39. Wong, P. and Pamer, E. G. (2003) CD8 T cell responses to infectious pathogens Annu. Rev. Immunol. 21, 29-70 (Pubitemid 37174526)
40. Ackerman, A. L. and Cresswell, P. (2004) Cellular mechanisms governing cross-presentation of exogenous antigens Nat. Immunol. 5, 678-684 (Pubitemid 39023296)
41. Guermonprez, P., Saveanu, L., Kleijmeer, M., Davoust, J., Van Endert, P., and Amigorena, S. (2003) ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells Nature 425, 397-402 (Pubitemid 37187268)
42. Ramakrishna, V., Treml, J. F., Vitale, L., Connolly, J. E., O'Neill, T., Smith, P. A., Jones, C. L., He, L. Z., Goldstein, J., Wallace, P. K., Keler, T., and Endres, M. J. (2004) Mannose receptor targeting of tumor antigen pmel17 to human dendritic cells directs anti-melanoma T cell responses via multiple HLA molecules J. Immunol. 172, 2845-2852 (Pubitemid 38263669)
43. Bonifaz, L., Bonnyay, D., Mahnke, K., Rivera, M., Nussenzweig, M. C., and Steinman, R. M. (2002) Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance J. Exp. Med. 196, 1627-1638 (Pubitemid 36026474)
44. Olson, C. A. and Roberts, R. W. (2007) Design, expression, and stability of a diverse protein library based on the human fibronectin type III domain Protein Sci. 16, 476-484 (Pubitemid 46327558)
45. Benedict, C. A., MacKrell, A. J., and Anderson, W. F. (1997) Determination of the binding affinity of an anti-CD34 single-chain antibody using a novel, flow cytometry based assay J. Immunol. Methods 201, 223-231 (Pubitemid 27086719)
46. Sallusto, F. and Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha J. Exp. Med. 179, 1109-1118
47. Romani, N., Gruner, S., Brang, D., Kampgen, E., Lenz, A., Trockenbacher, B., Konwalinka, G., Fritsch, P. O., Steinman, R. M., and Schuler, G. (1994) Proliferating dendritic cell progenitors in human blood J. Exp. Med. 180, 83-93 (Pubitemid 24181058)
48. Hoffmann, T. K., Meidenbauer, N., Dworacki, G., Kanaya, H., and Whiteside, T. L. (2000) Generation of tumor-specific T-lymphocytes by cross-priming with human dendritic cells ingesting apoptotic tumor cells Cancer Res. 60, 3542-3549 (Pubitemid 30482175)