Abstract
Modification of vaccine carriers by decoration with glycans can enhance binding to and even targeting of dendritic cells (DCs), thus augmenting vaccine efficacy. To find a specific glycan-“vector” it is necessary to know glycan-binding profile of DCs. This task is not trivial; the small number of circulating blood DCs available for isolation hinders screening and therefore advancement of the profiling. It would be more convenient to employ long-term cell cultures or even primary DCs from murine blood. We therefore examined whether THP-1 (human monocyte cell line) and DC2.4 (immature murine DC-like cell line) could serve as a model for human DCs. These cells were probed with a set of glycans previously identified as binding to circulating human CD14low/-CD16+CD83+ DCs. In addition, we tested a subpopulation of murine CD14low/-CD80+СD11c+CD16+ cells reported as relating to the human CD14low/-CD16+CD83+ cells. Manα1–3(Manα1–6)Manβ1–4GlcNAcβ1–4GlcNAcβ bound to both the cell lines and the murine CD14low/-CD80+СD11c+CD16+ cells. Primary cells, but not the cell cultures, were capable of binding GalNAcα1–3Galβ (Adi), the most potent ligand for binding to human circulating DCs. In conclusion, not one of the studied cell lines proved an adequate model for DCs processes involving lectin binding. Although the glycan-binding profile of BYRB-Rb (8.17)1Iem mouse DCs could prove useful for assessing human DCs, important glycan interactions were missing, a situation which was aggravated when employing cells from the BALB/c strain. Accordingly, one must treat results from murine work with caution when seeking vaccine targeting of human DCs, and certainly should avoid cell lines such as THP-1 and DC2.4 cells.
Similar content being viewed by others
Abbreviations
- BSA:
-
Bovine serum albumin
- DCs:
-
Dendritic cells
- Glyc:
-
Glycan residue
- fluo:
-
Fluorescein residue
- LPS:
-
Lipopolysaccharide
- PAA:
-
Polyacrylamide
- PBS:
-
Phosphate buffer saline
- PMA:
-
Phorbol 12-myristate 13-acetate
- TBSCa:
-
tris-buffer, containing 2 mM CaCl2
- TBSACa:
-
TBSCa, containing 2 mM BSA
- Versene solution:
-
PBS containing 0.02% (w/v) EDTA
References
Johannssen, T., Lepenies, B.: Glycan-based cell targeting to modulate immune responses. Trends Biotechnol. 35, 334–346 (2017)
Project of foundation for assistance to small innovative enterprises “Self-replicating RNA vaccine against Hepatitis C virus genotype 2, targeted to dendritic cells” (8 #9889р/16992); ERA-NET-Rus project “HCRus”, grant number ERANetRUS 081
UniVaxA project “Universal influenza vaccine through synthetic dendritic cell-targeted self-replicating RNA vaccines” (EU FP7 Project UniVax (HEALTH-F3-2013-601738) Contract No. 601738), www.univax-fp7.eu
Lepenies, B., Lee, J., Sonkaria, S.: Targeting C-type lectin receptors with multivalent carbohydrate ligands. Adv. Drug Deliv. Rev. 65, 1271–1281 (2013)
Unger, W.W.J., van Beelen, A.J., Sven, C., Bruijns, S.C., Joshi, M., Fehres, C.M., van Bloois, L., Verstege, M.I., Ambrosini, M., Kalay, H., Nazmi, K., Bolscher, J.G., Hooijberg, E., de Gruijl, T.D., Storm, G., van Kooyk, Y.: Glycan-modified liposomes boost CD4+ and CD8+ T-cell responses by targeting DCS-SIGN on dendritic cells. J. Control. Release. 160, 88–95 (2012)
Garćia-Vallejo, J., Ambrosini, M., Overbeek, A., van Riel, W.E., Bloem, K., Unger, W.W.J., Chiodo, F., Bolscher, J.C., Nazmi, K., Kalay, H., van Kooyk, Y.: Multivalent glycopeptide dendrimers for the targeted delivery of antigens to dendritic cells. Mol. Imuunol. 53, 387–397 (2012)
Al-Barwani, F., Young, S.L., Baird, M.A., Larsen, D.S., Ward, V.K.: Mannosylation of virus-like particles enhances internalization by antigen presenting cells. PLoS. (2014). https://doi.org/10.1371/journal.pone.01045232014
Climent, N., García, I., Marradi, M., Chiodo, F., Maleno, M.J., Gatell, J.M., García, F., Penadés, S., Plana, M.: Loading dendritic cells with gold nanoparticles (GNPs) bearing HIV-peptides and mannosides enhance HIV-specific T cell responses. Nanomedicine. 14, 339–351 (2018)
Kawasaki, N., Rillahan, C.D., Cheng, T.-Y., van Rhijn, I., Macauley, M.S., Moody, D.B., Paulson, J.C.: Targeted delivery of mycobacterial antigens to human dendritic cells via Siglec-7 induces robust T cell activation. J. Immunol. 193, 1560–1566 (2014)
MacDonald, K., Munster, D., Clark, G., Dzionek, A., Schmitz, J., Hart, D.: Characterization of human blood dendritic cells subsets. Blood. 10, 4512–4520 (2002)
Harman, A., Bye, C., Nasr, N., Sandgren, K., Kim, M., Mercier, S.K., Botting, R., Lewin, S., Cunningham, A., Cameron, P.: Identification of lineage relationships and novel markers of blood and skin human dendritic cells. J. Immunol. 190, 66–79 (2013)
Satpathy, A., Wu, X., Albring, J., Murphy, K.: Re(de)fining the dendritic cell lineage. Nat. Immunol. 13, 1145–1154 (2012)
Hu, Z., Zaborski, M., MacLeod, R., Quentmeier, H., Drexler, H.: Establishment and characterization of two novel cytokine-responsive acute myeloid and monocytic leukemia cell lines, MUTZ-2 and MUTZ-3. Leukemia. 10, 1025–1040 (1996)
Quentemeier, H., Duschl, A., Hu, Z.-B., Schnaar, B., Zaborski, M., Drecler, H.G.: MUTZ-3, a monocytic model cell line for interleukin-4 and lipopolysaccharide studies. Immunology. 89, 606–612 (1996)
Masterson, A., Sombroek, C., de Gruijl, T., Graus, Y., van der Vliet, H., Lougheed, S., van den Eertwegh, A., Pinedo, H., Scheper, R.: MUTZ-3, a human cell line model for the cytokine-induced differentiation of dendritic cells from CD34+precursors. Blood. 100, 701–703 (2002)
Larsson, K., Lindstedt, M.C.: Functional and transcriptional profiling of MUTZ-3, a myeloid cell line acting as a model for dendritic cells. Immunology. 117, 156–166 (2006)
Santegoets, S., van den Eertwegh, A., van de Loosdrecht, A., Scheper, R., de Gruijl, T.: Human dendritic cell line models for DC differentiation and clinical DC vaccination studies. J. Leuk. Biol. 84, 1364–1373 (2008)
Hoefnagel, M., Vermeulen, J., Scheper, R., Vandebriel, R.: Response of MUTZ-3 dendritic cells to the different components of the Haemophilus influenzae type B conjugate vaccine: towards an in vitro assay for vaccine immunogenicity. Vaccine. 29, 5114–5121 (2011)
Shen, Z., Reznikoff, G., Dranoff, G., Rock, K.: Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158, 2723–2730 (1997)
Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T., Tada, K.: Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer. 26, 171–176 (1980)
Rapoport, E., Khaidukov, S., Gaponov, A., Pazynina, G., Tsygankova, S., Ryzhov, I., Belyanchikov, I., Milona, P., Bovin, N., McCullough, K.C.: Glycan recognition by human blood mononuclear cells with an emphasis on dendritic cells. Glycoconj. J. 35, 191–203 (2018)
Bovin, N., Korchagina, E., Zemlyanukhina, T., Byramova, N., Galanina, O., Zemlyakov, A., Ivanov, A., Zubov, V., Mochalova, L.: Synthesis of polymeric neoglycoconjugates based on N-substituted polyacrylamides. Glycoconj. J. 10, 142–151 (1993)
Moiseeva, E.V.: Anti-Breast Cancer Drug Testing. Lambert Academic Publishing, Saarbrücken, Original approaches. Novel set of mouse models (2009)
Ogasawara, N., Kojima, T., Go, M., Fuchimoto, J., Kamekura, R., Koizumi, J., Ohkuni, T., Masaki, T., Murata, M., Tanaka, S.: Induction of JAM-A during differentiation of human THP-1 dendritic cells. Biochem. Biophys. Res. Commun. 389, 543–549 (2009)
Butler, M., Morel, A.S., Jordan, W.J., Eren, E., Hue, S., Shrimpton, R.E., Ritter, M.A.: Altered expression and endocytic function of CD205 in human dendritic cells, and detection of a CD205-DCL-1 fusion protein upon dendritic cell maturation. Immunology. 120, 362–371 (2007)
Moyo, N.A., Marchi, E., Steinbach, F.: Differentiation and activation of equine monocyte-derived dendritic cells are not correlated with CD206 or CD83 expression. Immunology. 139, 472–483 (2013)
Rhule, A., Rase, B., Smith, J.R., Shepherd, D.M.: Toll-like receptor ligand-induced activation of murine DC2.4 cells is attenuated by Panax notoginseng. J. Ethnopharmacol. 116, 179–186 (2008)
Li, Y., Wang, L., Chen, S.: Endogenous toll-like receptor ligands and their biological significance. J. Cell. Mol. Med. 14, 2592–2503 (2010)
He, T., Tang, H., Xu, S., Moyana, T., Xiang, J.: Interferon γ stimulates cellular maturation of dendritic cell line DC2.4 leading to induction of efficient cytotoxic T cell. Cell. Mol. Immunol. 4, 105–111 (2007)
McCullough, K.C., Sharma, R.: Dendritic cell endocytosis essential for viruses and vaccines. In: Ghosh, A. (ed.) Biology of Myelomonocytic Cells, pp. 99–128. InTech, Rijeka (2017)
McCullough, K.C., Sáiz, M., Summerfield, A.: Innate to adaptive: immune defence handling of foot-and-mouth disease virus in Sobrino, F., Domingo, E. (eds.) Foot-and-mouth disease virus: current research and emerging trends, pp. 211–274. Caister Academic Press, Norfolk (2017)
Boltjes, A., van Wijk, F.: Human dendritic cell functional specialization in steady-state and inflammation. Front. Immunol. https://doi.org/10.3389/fimmu.2014.00131 (2014)
Data of Consortium for functional glycomics, http://www.functionalglycomics.org
Hartnell, A., Steel, J., Turley, H., Jones, M., Jackson, D., Crocker, P.: Characterization of human sialoadhesin, a sialic acid binding receptor expressed by resident and inflammatory macrophage populations. Blood. 97, 288–296 (2001)
Wielgat, P., Trofimiuk, E., Gsarmomysy, R., Holownia, A.: Braszko: Sialylation pattern in lung epithelial cell line and siglecs expression in monocytic THP-1 cells as cellular indicators of cigarette smoke – induced pathology in vitro. J. Exp. Lung Res. 44, 167–177 (2018)
Lahm, H., André, S., Hoeflich, A., Fischer, J., Sordat, B., Kaltner, H., Wolf, E., Gabius, H.-J.: Comprehesive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implicantions for diagnostic and therapeutic procedures. J. Cancer Res. Clin. Oncol. 127, 375–386 (2001)
Diaz-Silvestre, H., Espinosa-Cueto, P., Sanchez-Gonzalez, A., Esparza-Ceron, M., Pereira-Suarez, A., Bernal-Fernandez, G., Espitia, C., Mancilla, R.: The 19-kDa antigen of mycobacterium tuberculosis is a major adhesin that binds the mannose receptor of THP-1 monocytic cells and promotes phagocytosis of mycobacteria. Microb. Pathog. 39, 97–107 (2005)
Jin, C., Wu, L., Fang, M., Cheng, L., Wu, N.: Multiple signaling pathways are involved in the interleukine-4 regulated expression of DC-SIGN in THP-1 cell line. J. Biomed. Biotechnol. (2012). https://doi.org/10.1155/2012/357060
Higashi, N., Fujioka, K., Denda-Nagai, K., Hashimoto, S., Nagai, S., Sato, T., Fujita, Y., Morikawa, A., Tsuiji, M., Miyata-Takeuchi, M., Sano, Y., Suzuki, N., Yamamoto, K., Matsushima, K., Irimura, T.: The macrophage C-type lectin specificfor galactose/N-acetylgalactosamine is an endocytic receptor expressed onmonocyte-derived immature dendritic cells. J. Biol. Chem. 277, 20686–20693 (2002)
Tsuiji, M., Fujimori, M., Ohashi, Y., Higashi, N., Onami, T.M., Hedrick, S.M., Irimura, T.: Molecular cloning and characterization of a novel mouse macrophage C-type lectin, mMGL2, which has a distinct carbohydrate specificity from mMGL1. J. Biol. Chem. 277, 28892–28901 (2002)
McCullough, K.C., Bassi, I., Démoulins, T., Thomann-Harwood, L., Ruggli, N.: Functional RNA delivery targeted to dendritic cells by synthetic nanoparticles. Ther. Deliv. 3, 1077–1099 (2012)
McCullough, K.C., Milona, P., Thomann-Harwood, L., Démoulins, T., Englezou, P., Suter, R., Ruggli, N.: Self-amplifying replicon RNA vaccine delivery to dendritic cells by synthetic nanoparticles. Vaccines. 2, 735–754 (2014)
Acknowledgments
This work was generously supported in part by grant 16-04-01084 of the Russian Foundation for Basic Research (E.R., E. M., D.A., S. Kh., G.P., S.Ts.), and EU FP7 Project UniVax (HEALTH-F3-2013-60173), grant number 601738 (N.B., K.M., E.R.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflicts of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Thesaurus
•Classical dendritic cells – the DCs that are considered to be the most potent antigen-presenting cells, and therefore also referred to as “professional antigen-presenting cells”; also termed conventional DCs.
•Monocytes (Mo) – the cell population of myeloid origin characterized in humans as CD16neg with a CD14 expression relative to other cells described as CD14high.
•CD14low/-CD16+ CD83+ cells – the human blood mononuclear cells containing DC subpopulations
Electronic supplementary material
Fig. 1S
Probing of CD16+ and CD11c+ cells for Adi binding, assessed by flow cytometry. Flow cytometer plots show expression of CD11c+ and CD16+ on subpopulations of murine monocytes in terms of their SSC (A, B, E, F). Histograms show binding profiles of CD11c+ and CD16+ subpopulations to the glycoprobe Adi (C, D, G, H). The number given for the rectangle gate (A, B, E, F), and for the black histogram gate (C, D, G, H) represent the percentage of the positive CD16+ and CD11c+ cells within monocytes from blood of BALB/c and BYRB-Rb (8.17) strains. SSC, side scatter; FL, mean of fluorescence intensity. In the C, D, G, H histograms the logs of fluorescence intensity (x-axis) are plotted against cell number (y-axis, counts) (DOCX 143 kb)
Rights and permissions
About this article
Cite this article
Rapoport, E.M., Moiseeva, E.V., Aronov, D.A. et al. Glycan-binding profile of DC-like cells. Glycoconj J 37, 129–138 (2020). https://doi.org/10.1007/s10719-019-09897-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10719-019-09897-9