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Article ; Online: How B cells drive T-cell responses: A key role for cross-presentation of antibody-targeted antigens.

Ossendorp, Ferry / Ho, Nataschja I / Van Montfoort, Nadine

2023 Volume 160, Page(s) 37–57

Abstract: In this review we discuss an underexposed mechanism in the adaptive immune system where B cell and T cell immunity collaborate. The main function of B cell immunity is the generation of antibodies which are well known for their high affinity and antigen- ... ...

Abstract	In this review we discuss an underexposed mechanism in the adaptive immune system where B cell and T cell immunity collaborate. The main function of B cell immunity is the generation of antibodies which are well known for their high affinity and antigen-specificity. Antibodies can bind antigens in soluble form making so-called immune complexes (ICs) or can opsonize antigen-exposing cells or particles for degradation. This leads to well-known effector mechanisms complement activation, antibody-dependent cytotoxicity and phagocytosis. What is less realized is that antibodies can play an important role in the targeting of antigen to dendritic cells (DCs) and thereby can drive T cell immunity. Here we summarize the studies that described this highly efficient process of antibody-mediated antigen uptake in DCs in vitro and in vivo. Only very low doses of antigen can be captured by circulating antibodies and subsequently trapped by DCs in vivo. We studied the handling of these ICs by DCs in subcellular detail. Upon immune complex engulfment DCs can sustain MHC class I and II antigen presentation for many days. Cell biological analysis showed that this function is causally related to intracellular antigen-storage compartments which are functional endolysosomal organelles present in DCs. We speculate that this function is immunologically very important as DCs require time to migrate from the site of infection to the draining lymph nodes to activate T cells. The implications of these findings and the consequences for the immune system, immunotherapy with tumor-specific antibodies and novel vaccination strategies are discussed.
MeSH term(s)	Humans ; T-Lymphocytes ; Cross-Priming ; Dendritic Cells ; Antigen Presentation ; Antigens/metabolism ; Antigen-Antibody Complex/metabolism
Chemical Substances	Antigens ; Antigen-Antibody Complex
Language	English
Publishing date	2023-11-18
Publishing country	United States
Document type	Review ; Journal Article
ZDB-ID	80226-8
ISSN	1557-8445 ; 0065-2776
ISSN (online)	1557-8445
ISSN	0065-2776
DOI	10.1016/bs.ai.2023.09.002
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Article ; Online: Saponin-based adjuvant-induced dendritic cell cross-presentation is dependent on PERK activation.

Huis In 't Veld, Lisa G M / Ho, Nataschja I / Wassink, Melisssa / den Brok, Martijn H / Adema, Gosse J

Cellular and molecular life sciences : CMLS

2022 Volume 79, Issue 5, Page(s) 231

Abstract: Saponin-based adjuvants (SBAs) are promising new adjuvants that stand out as they not only enforce CD4 + T cell-mediated immunity and antibody responses, but also induce an unprecedented level of antigen cross-presentation by dendritic cells (DC) and ... ...

Abstract	Saponin-based adjuvants (SBAs) are promising new adjuvants that stand out as they not only enforce CD4 + T cell-mediated immunity and antibody responses, but also induce an unprecedented level of antigen cross-presentation by dendritic cells (DC) and subsequent CD8 + T cell activation. We discovered that SBA's ability to boost cross-presentation depends on the induction of lipid bodies (LBs). Moreover, the MHCII
MeSH term(s)	Animals ; Antigen Presentation ; CD8-Positive T-Lymphocytes ; Cross-Priming ; Dendritic Cells/metabolism ; Endoplasmic Reticulum ; Mice ; Mice, Inbred C57BL ; Saponins/pharmacology
Chemical Substances	Saponins
Language	English
Publishing date	2022-04-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	1358415-7
ISSN	1420-9071 ; 1420-682X
ISSN (online)	1420-9071
ISSN	1420-682X
DOI	10.1007/s00018-022-04253-x
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Article ; Online: Autophagy regulates long-term cross-presentation by murine dendritic cells.

Ho, Nataschja I / Camps, Marcel G M / Verdoes, Martijn / Münz, Christian / Ossendorp, Ferry

European journal of immunology

2021 Volume 51, Issue 4, Page(s) 835–847

Abstract: Autophagy has been reported to be involved in supporting antigen cross-presentation by dendritic cells (DCs). We have shown that DCs have the ability to store antigen for a prolonged time in endolysosomal compartments and thereby sustain MHCI antigen ... ...

Abstract	Autophagy has been reported to be involved in supporting antigen cross-presentation by dendritic cells (DCs). We have shown that DCs have the ability to store antigen for a prolonged time in endolysosomal compartments and thereby sustain MHCI antigen cross-presentation to CD8
MeSH term(s)	Animals ; Antigen Presentation/drug effects ; Antigen Presentation/immunology ; Autophagosomes/immunology ; Autophagosomes/metabolism ; Autophagy/drug effects ; Autophagy/immunology ; Autophagy-Related Protein 5/genetics ; Autophagy-Related Protein 5/immunology ; Autophagy-Related Protein 5/metabolism ; CD8-Positive T-Lymphocytes/immunology ; Cell Line ; Cross-Priming/drug effects ; Cross-Priming/immunology ; Dendritic Cells/cytology ; Dendritic Cells/immunology ; Dendritic Cells/metabolism ; Histocompatibility Antigens Class I/immunology ; Histocompatibility Antigens Class I/metabolism ; Mice, Inbred C57BL ; Mice, Knockout ; Microscopy, Confocal ; Microtubule-Associated Proteins/immunology ; Microtubule-Associated Proteins/metabolism ; Wortmannin/pharmacology ; Mice
Chemical Substances	Autophagy-Related Protein 5 ; Histocompatibility Antigens Class I ; Map1lc3b protein, mouse ; Microtubule-Associated Proteins ; Wortmannin (XVA4O219QW)
Language	English
Publishing date	2021-02-10
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	120108-6
ISSN	1521-4141 ; 0014-2980
ISSN (online)	1521-4141
ISSN	0014-2980
DOI	10.1002/eji.202048961
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Zs.A 489: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article: Saponin-based adjuvant-induced dendritic cell cross-presentation is dependent on PERK activation

Huis in ’t Veld, Lisa G. M. / Ho, Nataschja I. / Wassink, Melisssa / den Brok, Martijn H. / Adema, Gosse J.

Cellular and molecular life sciences. 2022 May, v. 79, no. 5

2022

Abstract	Saponin-based adjuvants (SBAs) are promising new adjuvants that stand out as they not only enforce CD4 + T cell-mediated immunity and antibody responses, but also induce an unprecedented level of antigen cross-presentation by dendritic cells (DC) and subsequent CD8 + T cell activation. We discovered that SBA’s ability to boost cross-presentation depends on the induction of lipid bodies (LBs). Moreover, the MHCIIˡᵒCD11bʰⁱ DC subset was identified to be most responsive to SBA-induced cross-presentation. The aim is to further unravel the mechanisms behind the induction of DC cross-presentation by SBAs. Here we show that SBAs specifically induce the PKR-like Endoplasmic Reticulum kinase (PERK) pathway and that SBA-induced DC cross-presentation is dependent on activation of the PERK pathway. PERK activation and LB formation are both crucial for SBA-induced cross-presentation and PERK inhibition has little or no effect on SBA-induced LB formation. SBA’s responsiveness, LB formation and PERK activation are specific for the MHCIIˡᵒCD11bʰⁱ DCs. These findings contribute to understanding the pathways involved in SBA-induced cross-presentation and immune activation which will ultimately lead to the development of vaccines with improved efficiency and safety.
Keywords	T-lymphocytes ; antibodies ; antigens ; cell-mediated immunity ; dendritic cells ; endoplasmic reticulum ; lipids
Language	English
Dates of publication	2022-05
Size	p. 231.
Publishing place	Springer International Publishing
Document type	Article
ZDB-ID	1358415-7
ISSN	1420-9071 ; 1420-682X
ISSN (online)	1420-9071
ISSN	1420-682X
DOI	10.1007/s00018-022-04253-x
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Article ; Online: Saponin-based adjuvants enhance antigen cross-presentation in human CD11c

Ho, Nataschja I / Huis In 't Veld, Lisa G M / van Eck van der Sluijs, Jesper / Heuts, Branco M H / Looman, Maaike W G / Kers-Rebel, Esther D / van den Dries, Koen / Dolstra, Harry / Martens, Joost H A / Hobo, Willemijn / Adema, Gosse J

Journal for immunotherapy of cancer

2023 Volume 11, Issue 8

Abstract: Background: Adjuvants are key for effective vaccination against cancer and chronic infectious diseases. Saponin-based adjuvants (SBAs) are unique among adjuvants in their ability to induce robust cell-mediated immune responses in addition to antibody ... ...

Abstract	Background: Adjuvants are key for effective vaccination against cancer and chronic infectious diseases. Saponin-based adjuvants (SBAs) are unique among adjuvants in their ability to induce robust cell-mediated immune responses in addition to antibody responses. Recent preclinical studies revealed that SBAs induced cross-presentation and lipid bodies in otherwise poorly cross-presenting CD11b Method: Here, we investigated the response of human DC subsets to SBAs with RNA sequencing and pathway analyses, lipid body induction visualized by laser scanning microscopy, antigen translocation to the cytosol, and antigen cross-presentation to CD8 Results: RNA sequencing of SBA-treated conventional type 1 DC (cDC1) and type 2 DC (cDC2) subsets uncovered that SBAs upregulated lipid-related pathways in CD11c Conclusions: These data thus identify the CD163
MeSH term(s)	Humans ; Animals ; Mice ; Cross-Priming ; CD8-Positive T-Lymphocytes ; Adjuvants, Immunologic/pharmacology ; Dendritic Cells ; Saponins/pharmacology
Chemical Substances	CD163 antigen ; Adjuvants, Immunologic ; Saponins
Language	English
Publishing date	2023-08-23
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2719863-7
ISSN	2051-1426 ; 2051-1426
ISSN (online)	2051-1426
ISSN	2051-1426
DOI	10.1136/jitc-2023-007082
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Article ; Online: Distinct antigen uptake receptors route to the same storage compartments for cross-presentation in dendritic cells.

Ho, Nataschja I / Camps, Marcel G / Garcia-Vallejo, Juan J / Bos, Erik / Koster, Abraham J / Verdoes, Martijn / van Kooyk, Yvette / Ossendorp, Ferry

Immunology

2021 Volume 164, Issue 3, Page(s) 494–506

Abstract: An exclusive feature of dendritic cells (DCs) is their capacity to present exogenous antigens by MHC class I molecules, called cross-presentation. Here, we show that protein antigen can be conserved in mature murine DCs for several days in a lysosome- ... ...

Abstract	An exclusive feature of dendritic cells (DCs) is their capacity to present exogenous antigens by MHC class I molecules, called cross-presentation. Here, we show that protein antigen can be conserved in mature murine DCs for several days in a lysosome-like storage compartment, distinct from MHC class II and early endosomal compartments, as an internal source for the supply of MHC class I ligands. Using two different uptake routes via Fcγ receptors and C-type lectin receptors, we could show that antigens were routed towards the same endolysosomal compartments after 48 h. The antigen-containing compartments lacked co-expression of molecules involved in MHC class I processing and presentation including TAP and proteasome subunits as shown by single-cell imaging flow cytometry. Moreover, we observed the absence of cathepsin S but selective co-localization of active cathepsin X with protein antigen in the storage compartments. This indicates cathepsin S-independent antigen degradation and a novel but yet undefined role for cathepsin X in antigen processing and cross-presentation by DCs. In summary, our data suggest that these antigen-containing compartments in DCs can conserve protein antigens from different uptake routes and contribute to long-lasting antigen cross-presentation.
MeSH term(s)	Animals ; Antigen Presentation ; Antigens/immunology ; Antigens/metabolism ; Cathepsins/metabolism ; Cross-Priming ; Dendritic Cells/immunology ; Dendritic Cells/metabolism ; Dendritic Cells/ultrastructure ; Endosomes/immunology ; Endosomes/metabolism ; Endosomes/ultrastructure ; Histocompatibility Antigens Class I/metabolism ; Histocompatibility Antigens Class II/metabolism ; Lectins, C-Type/metabolism ; Lysosomes/immunology ; Lysosomes/metabolism ; Lysosomes/ultrastructure ; Mice ; Microscopy, Electron, Transmission ; Models, Animal ; NIH 3T3 Cells ; Primary Cell Culture ; Receptors, IgG/metabolism
Chemical Substances	Antigens ; Histocompatibility Antigens Class I ; Histocompatibility Antigens Class II ; Lectins, C-Type ; Receptors, IgG ; Cathepsins (EC 3.4.-) ; cathepsin X, mouse (EC 3.4.-)
Language	English
Publishing date	2021-06-30
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80124-0
ISSN	1365-2567 ; 0019-2805 ; 0953-4954
ISSN (online)	1365-2567
ISSN	0019-2805 ; 0953-4954
DOI	10.1111/imm.13382
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Article ; Online: Sustained cross-presentation capacity of murine splenic dendritic cell subsets in vivo.

Ho, Nataschja I / Camps, Marcel G M / de Haas, Edwin F E / Ossendorp, Ferry

European journal of immunology

2018 Volume 48, Issue 7, Page(s) 1164–1173

Abstract: An exclusive feature of dendritic cells (DCs) is their ability to cross-present exogenous antigens in MHC class I molecules. We analyzed the fate of protein antigen in antigen presenting cell (APC) subsets after uptake of naturally formed antigen- ... ...

Abstract	An exclusive feature of dendritic cells (DCs) is their ability to cross-present exogenous antigens in MHC class I molecules. We analyzed the fate of protein antigen in antigen presenting cell (APC) subsets after uptake of naturally formed antigen-antibody complexes in vivo. We observed that murine splenic DC subsets were able to present antigen in vivo for at least a week. After ex vivo isolation of four APC subsets, the presence of antigen in the storage compartments was visualized by confocal microscopy. Although all APC subsets stored antigen for many days, their ability and kinetics in antigen presentation was remarkably different. CD8α
MeSH term(s)	Animals ; Antigen Presentation ; CD8 Antigens/metabolism ; CD8-Positive T-Lymphocytes/immunology ; Cells, Cultured ; Cross-Priming ; Dendritic Cells/immunology ; Dendritic Cells/metabolism ; Histocompatibility Antigens Class I/metabolism ; Histocompatibility Antigens Class II/metabolism ; Lymphocyte Activation ; Macrophages/immunology ; Mice ; Mice, Inbred C57BL ; Microscopy, Confocal ; Spleen/immunology
Chemical Substances	CD8 Antigens ; CD8 antigen, alpha chain ; Histocompatibility Antigens Class I ; Histocompatibility Antigens Class II
Language	English
Publishing date	2018-05-17
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	120108-6
ISSN	1521-4141 ; 0014-2980
ISSN (online)	1521-4141
ISSN	0014-2980
DOI	10.1002/eji.201747372
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Article ; Online: Adjuvants Enhancing Cross-Presentation by Dendritic Cells: The Key to More Effective Vaccines?

Ho, Nataschja I / Huis In 't Veld, Lisa G M / Raaijmakers, Tonke K / Adema, Gosse J

Frontiers in immunology

2018 Volume 9, Page(s) 2874

Abstract: Over the last decades, vaccine development has advanced significantly in pursuing higher safety with less side effects. However, this is often accompanied by a reduction in vaccine immunogenicity and an increased dependency on adjuvants to enhance ... ...

Abstract	Over the last decades, vaccine development has advanced significantly in pursuing higher safety with less side effects. However, this is often accompanied by a reduction in vaccine immunogenicity and an increased dependency on adjuvants to enhance vaccine potency. Especially for diseases like cancer, it is important that therapeutic vaccines contain adjuvants that promote strong T cell responses. An important mode of action for such adjuvants is to prolong antigen exposure to dendritic cells (DCs) and to induce their maturation. These mature DCs are extremely effective in the activation of antigen-specific T cells, which is a pre-requisite for induction of potent and long-lasting cellular immunity. For the activation of CD8
MeSH term(s)	Adjuvants, Immunologic/administration & dosage ; Aluminum/administration & dosage ; Aluminum/immunology ; Antigen Presentation/drug effects ; Antigen Presentation/immunology ; Bacterial Infections/immunology ; Bacterial Infections/microbiology ; Bacterial Infections/prevention & control ; Cross-Priming/drug effects ; Cross-Priming/immunology ; Dendritic Cells/drug effects ; Dendritic Cells/immunology ; Humans ; Immunogenicity, Vaccine ; Ligands ; Lymphocyte Activation/drug effects ; Lymphocyte Activation/immunology ; Malaria/immunology ; Malaria/parasitology ; Malaria/prevention & control ; Nanoparticles/administration & dosage ; Neoplasms/immunology ; Neoplasms/therapy ; Saponins/administration & dosage ; Saponins/immunology ; T-Lymphocytes, Cytotoxic/drug effects ; T-Lymphocytes, Cytotoxic/immunology ; Toll-Like Receptors/immunology ; Toll-Like Receptors/metabolism ; Treatment Outcome ; Vaccines/administration & dosage ; Vaccines/immunology ; Virus Diseases/immunology ; Virus Diseases/prevention & control ; Virus Diseases/virology
Chemical Substances	Adjuvants, Immunologic ; Ligands ; Saponins ; Toll-Like Receptors ; Vaccines ; Aluminum (CPD4NFA903)
Language	English
Publishing date	2018-12-13
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2018.02874
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Article ; Online: C1q-Dependent Dendritic Cell Cross-Presentation of In Vivo-Formed Antigen-Antibody Complexes.

Ho, Nataschja I / Camps, Marcel G M / de Haas, Edwin F E / Trouw, Leendert A / Verbeek, J Sjef / Ossendorp, Ferry

Journal of immunology (Baltimore, Md. : 1950)

2017 Volume 198, Issue 11, Page(s) 4235–4243

Abstract: Dendritic cells (DCs) are specialized in Ag engulfment via a wide variety of uptake receptors on their cell surface. In the present study we investigated Ag uptake and presentation of in vivo-formed Ag-Ab complexes by i.v. injecting mice with Ag-specific ...

Abstract	Dendritic cells (DCs) are specialized in Ag engulfment via a wide variety of uptake receptors on their cell surface. In the present study we investigated Ag uptake and presentation of in vivo-formed Ag-Ab complexes by i.v. injecting mice with Ag-specific Abs followed by the cognate Ag. We show by this natural Ab-mediated Ag targeting system that uptake by splenic APC subsets is severely hampered in mice lacking complement factor C1q (C1qa
MeSH term(s)	Adaptive Immunity ; Animals ; Antigen Presentation ; Antigen-Antibody Complex/immunology ; CD8 Antigens/immunology ; Complement C1q/deficiency ; Complement C1q/genetics ; Complement C1q/immunology ; Cross-Priming ; Dendritic Cells/immunology ; Mice ; Mice, Inbred C57BL ; Receptors, IgG/immunology
Chemical Substances	Antigen-Antibody Complex ; CD8 Antigens ; Receptors, IgG ; Complement C1q (80295-33-6)
Language	English
Publishing date	2017-06-01
Publishing country	United States
Document type	Journal Article
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.1602169
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Ud II Zs.37: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 2021: Bestellungen von Artikeln über das Online-Bestellformular ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Simplified Monopalmitoyl Toll-like Receptor 2 Ligand Mini-UPam for Self-Adjuvanting Neoantigen-Based Synthetic Cancer Vaccines.

van den Ende, Thomas C / Heuts, Jeroen M M / Gential, Geoffroy P P / Visser, Marten / van de Graaff, Michel J / Ho, Nataschja I / Jiskoot, Wim / Valentijn, A Rob P M / Meeuwenoord, Nico J / Overkleeft, Herman S / Codée, Jeroen D C / van der Burg, Sjoerd H / Verdegaal, Els M E / van der Marel, Gijsbert A / Ossendorp, Ferry / Filippov, Dmitri V

Chembiochem : a European journal of chemical biology

2020 Volume 22, Issue 7, Page(s) 1215–1222

Abstract: Synthetic vaccines, based on antigenic peptides that comprise MHC-I and MHC-II T-cell epitopes expressed by tumors, show great promise for the immunotherapy of cancer. For optimal immunogenicity, the synthetic peptides (SPs) should be adjuvanted with ... ...

Abstract	Synthetic vaccines, based on antigenic peptides that comprise MHC-I and MHC-II T-cell epitopes expressed by tumors, show great promise for the immunotherapy of cancer. For optimal immunogenicity, the synthetic peptides (SPs) should be adjuvanted with suitable immunostimulatory additives. Previously, we have shown that improved immunogenicity in vivo is obtained with vaccine modalities in which an SP is covalently connected to an adjuvanting moiety, typically a ligand to Toll-like receptor 2 (TLR2). SPs were covalently attached to UPam, which is a derivative of the classic TLR2 ligand Pam
MeSH term(s)	Antigens, Neoplasm/chemistry ; Antigens, Neoplasm/immunology ; Cancer Vaccines/chemistry ; Cancer Vaccines/immunology ; Cell Line ; Dendritic Cells/cytology ; Dendritic Cells/metabolism ; Drug Design ; Humans ; Interleukin-8/metabolism ; Ligands ; Lipopeptides/chemical synthesis ; Lipopeptides/chemistry ; Lipopeptides/immunology ; Lipoylation ; Lymphocyte Activation ; Toll-Like Receptor 2/chemistry ; Toll-Like Receptor 2/metabolism ; Vaccines, Synthetic/chemistry ; Vaccines, Synthetic/immunology
Chemical Substances	Antigens, Neoplasm ; Cancer Vaccines ; Interleukin-8 ; Ligands ; Lipopeptides ; Toll-Like Receptor 2 ; Vaccines, Synthetic
Language	English
Publishing date	2020-12-22
Publishing country	Germany
Document type	Journal Article
ZDB-ID	2020469-3
ISSN	1439-7633 ; 1439-4227
ISSN (online)	1439-7633
ISSN	1439-4227
DOI	10.1002/cbic.202000687
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