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Article ; Online: A protocol for qualitative and quantitative measurement of endosomal processing using hot spot analysis.

Clement, Cristina C / Nanaware, Padma P / Stern, Lawrence J / Santambrogio, Laura

STAR protocols

2021 Volume 2, Issue 3, Page(s) 100648

Abstract: A detailed quantification of antigen processing by endosomal compartments provides important information on the pattern of protein fragmentation. Here, we describe a protocol that combines gradient purified endosomes, incubated with antigens, followed by ...

Abstract	A detailed quantification of antigen processing by endosomal compartments provides important information on the pattern of protein fragmentation. Here, we describe a protocol that combines gradient purified endosomes, incubated with antigens, followed by hot spot analysis of MS/MS-sequenced peptides. The analysis identifies differences in endosomal antigen processing by dendritic cells under diverse experimental conditions. For complete details on the use and execution of this protocol, please refer to Clement et al. (2021).
MeSH term(s)	Animals ; Antigens/metabolism ; Dendritic Cells/immunology ; Dendritic Cells/metabolism ; Endosomes/immunology ; Endosomes/metabolism ; Membrane Proteins/administration & dosage ; Mice ; Molecular Biology/methods ; Peptides/immunology ; Peptides/metabolism ; Tandem Mass Spectrometry
Chemical Substances	Antigens ; Membrane Proteins ; Peptides ; flt3 ligand protein
Language	English
Publishing date	2021-07-06
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	2666-1667
ISSN (online)	2666-1667
DOI	10.1016/j.xpro.2021.100648
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Article ; Online: Immunopeptidome profiling of human coronavirus OC43-infected cells identifies CD4 T-cell epitopes specific to seasonal coronaviruses or cross-reactive with SARS-CoV-2.

Becerra-Artiles, Aniuska / Nanaware, Padma P / Muneeruddin, Khaja / Weaver, Grant C / Shaffer, Scott A / Calvo-Calle, J Mauricio / Stern, Lawrence J

PLoS pathogens

2023 Volume 19, Issue 7, Page(s) e1011032

Abstract: Seasonal "common-cold" human coronaviruses are widely spread throughout the world and are mainly associated with mild upper respiratory tract infections. The emergence of highly pathogenic coronaviruses MERS-CoV, SARS-CoV, and most recently SARS-CoV-2 ... ...

Abstract	Seasonal "common-cold" human coronaviruses are widely spread throughout the world and are mainly associated with mild upper respiratory tract infections. The emergence of highly pathogenic coronaviruses MERS-CoV, SARS-CoV, and most recently SARS-CoV-2 has prompted increased attention to coronavirus biology and immunopathology, but the T-cell response to seasonal coronaviruses remains largely uncharacterized. Here we report the repertoire of viral peptides that are naturally processed and presented upon infection of a model cell line with seasonal coronavirus OC43. We identified MHC-bound peptides derived from each of the viral structural proteins (spike, nucleoprotein, hemagglutinin-esterase, membrane, and envelope) as well as non-structural proteins nsp3, nsp5, nsp6, and nsp12. Eighty MHC-II bound peptides corresponding to 14 distinct OC43-derived epitopes were identified, including many at very high abundance within the overall MHC-II peptidome. Fewer and less abundant MHC-I bound OC43-derived peptides were observed, possibly due to MHC-I downregulation induced by OC43 infection. The MHC-II peptides elicited low-abundance recall T-cell responses in most donors tested. In vitro assays confirmed that the peptides were recognized by CD4+ T cells and identified the presenting HLA alleles. T-cell responses cross-reactive between OC43, SARS-CoV-2, and the other seasonal coronaviruses were confirmed in samples of peripheral blood and peptide-expanded T-cell lines. Among the validated epitopes, spike protein S903-917 presented by DPA101:03/DPB104:01 and S1085-1099 presented by DRB115:01 shared substantial homology to other human coronaviruses, including SARS-CoV-2, and were targeted by cross-reactive CD4 T cells. Nucleoprotein N54-68 and hemagglutinin-esterase HE128-142 presented by DRB115:01 and HE259-273 presented by DPA101:03/DPB104:01 are immunodominant epitopes with low coronavirus homology that are not cross-reactive with SARS-CoV-2. Overall, the set of naturally processed and presented OC43 epitopes comprise both OC43-specific and human coronavirus cross-reactive epitopes, which can be used to follow CD4 T-cell cross-reactivity after infection or vaccination, and to guide selection of epitopes for inclusion in pan-coronavirus vaccines.
MeSH term(s)	Humans ; SARS-CoV-2 ; CD4-Positive T-Lymphocytes ; Coronavirus OC43, Human ; Epitopes, T-Lymphocyte ; COVID-19 ; Hemagglutinins ; Seasons ; Esterases ; Spike Glycoprotein, Coronavirus
Chemical Substances	Epitopes, T-Lymphocyte ; Hemagglutinins ; Esterases (EC 3.1.-) ; Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2
Language	English
Publishing date	2023-07-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1011032
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Article ; Online: A druggable pocket on PSMD10

M G, Mukund Sudharsan / Chikhale, Rupesh / Nanaware, Padma P / Dalvi, Somavally / Venkatraman, Prasanna

European journal of pharmacology

2021 Volume 915, Page(s) 174718

Abstract: Background: PSMD10: Methods: High throughput virtual screening was used to screen compounds against PSMD10: Results: We identified doxorubicin as the first-generation small molecule inhibitor of PSMD10: General significance: Drug design against ...

Abstract	Background: PSMD10 Methods: High throughput virtual screening was used to screen compounds against PSMD10 Results: We identified doxorubicin as the first-generation small molecule inhibitor of PSMD10 General significance: Drug design against protein interactions in general and PSMD10
MeSH term(s)	Proteasome Endopeptidase Complex ; Proto-Oncogene Proteins
Chemical Substances	PSMD10 protein, human ; Proto-Oncogene Proteins ; Proteasome Endopeptidase Complex (EC 3.4.25.1)
Language	English
Publishing date	2021-12-23
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	80121-5
ISSN	1879-0712 ; 0014-2999
ISSN (online)	1879-0712
ISSN	0014-2999
DOI	10.1016/j.ejphar.2021.174718
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Article ; Online: Distinguishing Signal From Noise in Immunopeptidome Studies of Limiting-Abundance Biological Samples: Peptides Presented by I-A

Nanaware, Padma P / Jurewicz, Mollie M / Clement, Cristina C / Lu, Liying / Santambrogio, Laura / Stern, Lawrence J

Frontiers in immunology

2021 Volume 12, Page(s) 658601

Abstract: Antigen presentation by MHC-II proteins in the thymus is central to selection of CD4 T cells, but analysis of the full repertoire of presented peptides responsible for positive and negative selection is complicated by the low abundance of antigen ... ...

Abstract	Antigen presentation by MHC-II proteins in the thymus is central to selection of CD4 T cells, but analysis of the full repertoire of presented peptides responsible for positive and negative selection is complicated by the low abundance of antigen presenting cells. A key challenge in analysis of limiting abundance immunopeptidomes by mass spectrometry is distinguishing true MHC-binding peptides from co-eluting non-specifically bound peptides present in the mixture eluted from immunoaffinity-purified MHC molecules. Herein we tested several approaches to minimize the impact of non-specific background peptides, including analyzing eluates from isotype-control antibody-conjugated beads, considering only peptides present in nested sets, and using predicted binding motif analysis to identify core epitopes. We evaluated these methods using well-understood human cell line samples, and then applied them to analysis of the I-A
MeSH term(s)	Amino Acid Motifs ; Amino Acid Sequence ; Animals ; Antigen Presentation/immunology ; B-Lymphocytes/immunology ; B-Lymphocytes/metabolism ; Cell Line ; Computational Biology/methods ; Dendritic Cells/immunology ; Dendritic Cells/metabolism ; Epitope Mapping/methods ; Epitopes/chemistry ; Epitopes/immunology ; HLA-DR Antigens/chemistry ; HLA-DR Antigens/immunology ; Histocompatibility Antigens Class II/chemistry ; Histocompatibility Antigens Class II/immunology ; Humans ; Mice ; Mice, Inbred C57BL ; Peptides/chemistry ; Peptides/immunology ; Protein Binding ; Spleen/immunology ; Spleen/metabolism ; Thymus Gland/immunology ; Thymus Gland/metabolism
Chemical Substances	Epitopes ; HLA-DR Antigens ; Histocompatibility Antigens Class II ; I-A(b) antigen, mouse ; Peptides
Language	English
Publishing date	2021-04-29
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2021.658601
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Article: Immunopeptidome profiling of human coronavirus OC43-infected cells identifies CD4 T cell epitopes specific to seasonal coronaviruses or cross-reactive with SARS-CoV-2.

Becerra-Artiles, Aniuska / Nanaware, Padma P / Muneeruddin, Khaja / Weaver, Grant C / Shaffer, Scott A / Calvo-Calle, J Mauricio / Stern, Lawrence J

bioRxiv : the preprint server for biology

2022

Abstract	Seasonal "common-cold" human coronaviruses are widely spread throughout the world and are mainly associated with mild upper respiratory tract infections. The emergence of highly pathogenic coronaviruses MERS-CoV, SARS-CoV, and most recently SARS-CoV-2 has prompted increased attention to coronavirus biology and immunopathology, but identification and characterization of the T cell response to seasonal human coronaviruses remain largely uncharacterized. Here we report the repertoire of viral peptides that are naturally processed and presented upon infection of a model cell line with seasonal human coronavirus OC43. We identified MHC-I and MHC-II bound peptides derived from the viral spike, nucleocapsid, hemagglutinin-esterase, 3C-like proteinase, and envelope proteins. Only three MHC-I bound OC43-derived peptides were observed, possibly due to the potent MHC-I downregulation induced by OC43 infection. By contrast, 80 MHC-II bound peptides corresponding to 14 distinct OC43-derived epitopes were identified, including many at very high abundance within the overall MHC-II peptidome. These peptides elicited low-abundance recall T cell responses in most donors tested. In vitro assays confirmed that the peptides were recognized by CD4+ T cells and identified the presenting HLA alleles. T cell responses cross-reactive between OC43, SARS-CoV-2, and the other seasonal coronaviruses were confirmed in samples of peripheral blood and peptide-expanded T cell lines. Among the validated epitopes, S Author summary: There is much current interest in cellular immune responses to seasonal common-cold coronaviruses because of their possible role in mediating protection against SARS-CoV-2 infection or pathology. However, identification of relevant T cell epitopes and systematic studies of the T cell responses responding to these viruses are scarce. We conducted a study to identify naturally processed and presented MHC-I and MHC-II epitopes from human cells infected with the seasonal coronavirus HCoV-OC43, and to characterize the T cell responses associated with these epitopes. We found epitopes specific to the seasonal coronaviruses, as well as epitopes cross-reactive between HCoV-OC43 and SARS-CoV-2. These epitopes should be useful in following immune responses to seasonal coronaviruses and identifying their roles in COVID-19 vaccination, infection, and pathogenesis.
Language	English
Publishing date	2022-12-01
Publishing country	United States
Document type	Preprint
DOI	10.1101/2022.12.01.518643
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Article ; Online: CD4 Effector TCR Avidity for Peptide on APC Determines the Level of Memory Generated.

Jones, Michael C / Castonguay, Catherine / Nanaware, Padma P / Weaver, Grant C / Stadinski, Brian / Kugler-Umana, Olivia A / Huseby, Eric S / Stern, Lawrence J / McKinstry, Karl Kai / Strutt, Tara M / Devarajan, Priyadharshini / Swain, Susan L

Journal of immunology (Baltimore, Md. : 1950)

2023 Volume 210, Issue 12, Page(s) 1950–1961

Abstract: Initial TCR affinity for peptide Ag is known to impact the generation of memory; however, its contributions later, when effectors must again recognize Ag at 5-8 d postinfection to become memory, is unclear. We examined whether the effector TCR affinity ... ...

Abstract	Initial TCR affinity for peptide Ag is known to impact the generation of memory; however, its contributions later, when effectors must again recognize Ag at 5-8 d postinfection to become memory, is unclear. We examined whether the effector TCR affinity for peptide at this "effector checkpoint" dictates the extent of memory and degree of protection against rechallenge. We made an influenza A virus nucleoprotein (NP)-specific TCR transgenic mouse strain, FluNP, and generated NP-peptide variants that are presented by MHC class II to bind to the FluNP TCR over a broad range of avidity. To evaluate the impact of avidity in vivo, we primed naive donor FluNP in influenza A virus-infected host mice, purified donor effectors at the checkpoint, and cotransferred them with the range of peptides pulsed on activated APCs into second uninfected hosts. Higher-avidity peptides yielded higher numbers of FluNP memory cells in spleen and most dramatically in lung and draining lymph nodes and induced better protection against lethal influenza infection. Avidity determined memory cell number, not cytokine profile, and already impacted donor cell number within several days of transfer. We previously found that autocrine IL-2 production at the checkpoint prevents default effector apoptosis and supports memory formation. Here, we find that peptide avidity determines the level of IL-2 produced by these effectors and that IL-2Rα expression by the APCs enhances memory formation, suggesting that transpresentation of IL-2 by APCs further amplifies IL-2 availability. Secondary memory generation was also avidity dependent. We propose that this regulatory pathway selects CD4 effectors of highest affinity to progress to memory.
MeSH term(s)	Mice ; Animals ; CD4-Positive T-Lymphocytes/metabolism ; Interleukin-2/metabolism ; Peptides/metabolism ; Mice, Transgenic ; Receptors, Antigen, T-Cell/metabolism ; Immunologic Memory ; Mice, Inbred C57BL
Chemical Substances	Interleukin-2 ; Peptides ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2023-10-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
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.2200337
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Article ; Online: Broadly recognized, cross-reactive SARS-CoV-2 CD4 T cell epitopes are highly conserved across human coronaviruses and presented by common HLA alleles.

Becerra-Artiles, Aniuska / Calvo-Calle, J Mauricio / Co, Mary Dawn / Nanaware, Padma P / Cruz, John / Weaver, Grant C / Lu, Liying / Forconi, Catherine / Finberg, Robert W / Moormann, Ann M / Stern, Lawrence J

Cell reports

2022 Volume 39, Issue 11, Page(s) 110952

Abstract: Sequence homology between SARS-CoV-2 and common-cold human coronaviruses (HCoVs) raises the possibility that memory responses to prior HCoV infection can affect T cell response in COVID-19. We studied T cell responses to SARS-CoV-2 and HCoVs in ... ...

Abstract	Sequence homology between SARS-CoV-2 and common-cold human coronaviruses (HCoVs) raises the possibility that memory responses to prior HCoV infection can affect T cell response in COVID-19. We studied T cell responses to SARS-CoV-2 and HCoVs in convalescent COVID-19 donors and identified a highly conserved SARS-CoV-2 sequence, S
MeSH term(s)	Alleles ; CD4-Positive T-Lymphocytes ; COVID-19 ; COVID-19 Vaccines ; Epitopes, T-Lymphocyte ; HLA Antigens ; Humans ; Receptors, Antigen, T-Cell ; SARS-CoV-2 ; mRNA Vaccines
Chemical Substances	COVID-19 Vaccines ; Epitopes, T-Lymphocyte ; HLA Antigens ; Receptors, Antigen, T-Cell ; mRNA Vaccines
Language	English
Publishing date	2022-05-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2022.110952
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Article ; Online: Immunopeptidome profiling of human coronavirus OC43-infected cells identifies CD4 T cell epitopes specific to seasonal coronaviruses or cross-reactive with SARS-CoV-2

Becerra-Artiles, Aniuska / Nanaware, Padma P. / Muneeruddin, Khaja / Weaver, Grant C. / Shaffer, Scott A. / Calvo-Calle, J. Mauricio / Stern, Lawrence J.

bioRxiv

Abstract	Seasonal "common-cold" human coronaviruses are widely spread throughout the world and are mainly associated with mild upper respiratory tract infections. The emergence of highly pathogenic coronaviruses MERS-CoV, SARS-CoV, and most recently SARS-CoV-2 has prompted increased attention to coronavirus biology and immunopathology, but identification and characterization of the T cell response to seasonal human coronaviruses remain largely uncharacterized. Here we report the repertoire of viral peptides that are naturally processed and presented upon infection of a model cell line with seasonal human coronavirus OC43. We identified MHC-I and MHC-II bound peptides derived from the viral spike, nucleocapsid, hemagglutinin-esterase, 3C-like proteinase, and envelope proteins. Only three MHC-I bound OC43-derived peptides were observed, possibly due to the potent MHC-I downregulation induced by OC43 infection. By contrast, 80 MHC-II bound peptides corresponding to 14 distinct OC43-derived epitopes were identified, including many at very high abundance within the overall MHC-II peptidome. These peptides elicited low-abundance recall T cell responses in most donors tested. In vitro assays confirmed that the peptides were recognized by CD4+ T cells and identified the presenting HLA alleles. T cell responses cross-reactive between OC43, SARS-CoV-2, and the other seasonal coronaviruses were confirmed in samples of peripheral blood and peptide-expanded T cell lines. Among the validated epitopes, S903-917 presented by DPA101:03/DPB104:01 and S1085-1099 presented by DRB115:01 shared substantial homology to other human coronaviruses, including SARS-CoV-2, and were targeted by cross-reactive CD4 T cells. N54-68 and HE128-142 presented by DRB115:01 and HE259-273 presented by DPA101:03/DPB104:01 are immunodominant epitopes with low coronavirus homology that are not cross-reactive with SARS-CoV-2. Overall, the set of naturally processed and presented OC43 epitopes comprise both OC43-specific and human coronavirus cross-reactive epitopes, which can be used to follow T cell cross-reactivity after infection or vaccination and could aid in the selection of epitopes for inclusion in pan-coronavirus vaccines.
Keywords	covid19
Language	English
Publishing date	2022-12-01
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2022.12.01.518643
Database	COVID19

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Article ; Online: Current Insights in Cutaneous Lupus Erythematosus Immunopathogenesis.

Garelli, Colton J / Refat, Maggi Ahmed / Nanaware, Padma P / Ramirez-Ortiz, Zaida G / Rashighi, Mehdi / Richmond, Jillian M

Frontiers in immunology

2020 Volume 11, Page(s) 1353

Abstract: Cutaneous Lupus Erythematosus (CLE) is a clinically diverse group of autoimmune skin diseases with shared histological features of interface dermatitis and autoantibodies deposited at the dermal-epidermal junction. Various genetic and environmental ... ...

Abstract	Cutaneous Lupus Erythematosus (CLE) is a clinically diverse group of autoimmune skin diseases with shared histological features of interface dermatitis and autoantibodies deposited at the dermal-epidermal junction. Various genetic and environmental triggers of CLE promote infiltration of T cells, B cells, neutrophils, antigen presenting cells, and NK cells into lesional skin. In this mini-review, we will discuss the clinical features of CLE, insights into CLE immunopathogenesis, and novel treatment approaches.
MeSH term(s)	Humans ; Lupus Erythematosus, Cutaneous/drug therapy ; Lupus Erythematosus, Cutaneous/immunology ; Lupus Erythematosus, Cutaneous/pathology
Language	English
Publishing date	2020-07-02
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2020.01353
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Article ; Online: HLA-DO Modulates the Diversity of the MHC-II Self-peptidome.

Nanaware, Padma P / Jurewicz, Mollie M / Leszyk, John D / Shaffer, Scott A / Stern, Lawrence J

Molecular & cellular proteomics : MCP

2018 Volume 18, Issue 3, Page(s) 490–503

Abstract: Presentation of antigenic peptides on MHC-II molecules is essential for tolerance to self and for initiation of immune responses against foreign antigens. DO (HLA-DO in humans, H2-O in mice) is a nonclassical MHC-II protein that has been implicated in ... ...

Abstract	Presentation of antigenic peptides on MHC-II molecules is essential for tolerance to self and for initiation of immune responses against foreign antigens. DO (HLA-DO in humans, H2-O in mice) is a nonclassical MHC-II protein that has been implicated in control of autoimmunity and regulation of neutralizing antibody responses to viruses. These effects likely are related to a role of DO in selecting MHC-II epitopes, but previous studies examining the effect of DO on presentation of selected CD4 T cell epitopes have been contradictory. To understand how DO modulates MHC-II antigen presentation, we characterized the full spectrum of peptides presented by MHC-II molecules expressed by DO-sufficient and DO-deficient antigen-presenting cells
MeSH term(s)	Animals ; Antigen Presentation ; Cell Line ; Epitopes, T-Lymphocyte/metabolism ; HLA-D Antigens/chemistry ; HLA-D Antigens/genetics ; Histocompatibility Antigens Class II/chemistry ; Histocompatibility Antigens Class II/genetics ; Humans ; Immunodominant Epitopes/metabolism ; Mice ; Mice, Inbred C57BL ; Peptides/metabolism
Chemical Substances	Epitopes, T-Lymphocyte ; H-2O antigen ; HLA-D Antigens ; HLA-DO antigens ; Histocompatibility Antigens Class II ; Immunodominant Epitopes ; Peptides
Language	English
Publishing date	2018-12-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2075924-1
ISSN	1535-9484 ; 1535-9476
ISSN (online)	1535-9484
ISSN	1535-9476
DOI	10.1074/mcp.RA118.000956
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