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Article ; Online: BTN1A1 is a novel immune checkpoint mutually exclusive to PD-L1.

Kim, Young-Seung / Lee, Seung-Hoon / Park, Andrew H / Wu, Chunai / Hong, Bong-Ki / Jung, Hyunjin / Lin, Steven H / Yoo, Stephen S

Journal for immunotherapy of cancer

2024 Volume 12, Issue 3

Abstract: Background: While Programmed cell death protein 1 (PD-1)/programmed cell death-ligand 1 (PD-L1) blockade is a potent antitumor treatment strategy, it is effective in only limited subsets of patients with cancer, emphasizing the need for the ... ...

Abstract	Background: While Programmed cell death protein 1 (PD-1)/programmed cell death-ligand 1 (PD-L1) blockade is a potent antitumor treatment strategy, it is effective in only limited subsets of patients with cancer, emphasizing the need for the identification of additional immune checkpoints. Butyrophilin 1A1 (BTN1A1) has been reported to exhibit potential immunoregulatory activity, but its ability to function as an immune checkpoint remains to be systematically assessed, and the mechanisms underlying such activity have yet to be characterized. Methods: BTN1A1 expression was evaluated in primary tumor tissue samples, and its ability to suppress T-cell activation and T cell-dependent tumor clearance was examined. The relationship between BTN1A1 and PD-L1 expression was further characterized, followed by the development of a BTN1A1-specific antibody that was administered to tumor-bearing mice to test the amenability of this target to immune checkpoint inhibition. Results: BTN1A1 was confirmed to suppress T-cell activation in vitro and in vivo. Robust BTN1A1 expression was detected in a range of solid tumor tissue samples, and BTN1A1 expression was mutually exclusive with that of PD-L1 as a consequence of its inhibition of Janus-activated kinase/signal transducer and activator of transcription signaling-induced PD-L1 upregulation. Antibody-mediated BTN1A1 blockade suppressed tumor growth and enhanced immune cell infiltration in syngeneic tumor-bearing mice. Conclusion: Together, these results confirm that the potential of BTN1A1 is a bona fide immune checkpoint and a viable immunotherapeutic target for the treatment of individuals with anti-PD-1/PD-L1 refractory or resistant disease, opening new avenues to improving survival outcomes for patients with a range of cancers.
MeSH term(s)	Animals ; Humans ; Mice ; B7-H1 Antigen ; Butyrophilins ; Lymphocyte Activation ; Neoplasms/drug therapy ; T-Lymphocytes ; Up-Regulation
Chemical Substances	B7-H1 Antigen ; BTN1A1 protein, human ; Butyrophilins ; CD274 protein, human
Language	English
Publishing date	2024-03-14
Publishing country	England
Document type	Journal Article
ZDB-ID	2719863-7
ISSN	2051-1426 ; 2051-1426
ISSN (online)	2051-1426
ISSN	2051-1426
DOI	10.1136/jitc-2023-008303
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Article: DNA binding site kinetics of a large antiviral polyamide

Niederschulte, Jacquelyn / Song, Yang / Park, Andrew H / Bashkin, James K / Dupureur, Cynthia M

Biochimie. 2021 June, v. 185

2021

Abstract: Polyamides (PAs) are powerful DNA ligands that can bind the minor groove of DNA with high affinity and specificity. While the characterization of PA-DNA behavior has focused principally on hairpin PAs 6–8 rings in size, there is increasing evidence that ... ...

Abstract	Polyamides (PAs) are powerful DNA ligands that can bind the minor groove of DNA with high affinity and specificity. While the characterization of PA-DNA behavior has focused principally on hairpin PAs 6–8 rings in size, there is increasing evidence that their behavior does not necessarily reflect the complexities that are emerging from studies of larger hairpin PAs, particularly concerning sequence mismatch tolerance and observed but unaddressed high PA-target site binding stoichiometries. To explore these complexities in more detail, kinetics studies of binding a large anti-HPV hairpin polyamide to an isolated DNA recognition site are described. Using a fluorescence assay, two distinct binding phases are observed for the first time in hairpin PA literature. PA14 concentration dependence analysis indicates that the faster binding event is diffusion-controlled; the apparent, second event is significantly slower (350–1500 fold). Both association phases are sampled in 1:1 complexes, consistent with cooperative binding of two PA molecules even under this condition. Fitting of the slow phase to a biexponential model yields two λₒₙ,ₐₚₚ that differ by 4-5-fold, which is consistent with the high mismatch tolerance and binding site stoichiometry previously observed. A/T patterns in the recognition sequence do not affect these decay constants significantly. Dissociation decay constants are among the slowest reported for hairpin PAs (10⁻³ s⁻¹), independent of A/T pattern, and may point to the efficacy of PA14 as an antiviral.
Keywords	DNA ; fluorescence ; ligands ; polyamides ; stoichiometry
Language	English
Dates of publication	2021-06
Size	p. 146-154.
Publishing place	Elsevier B.V.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	120345-9
ISSN	0300-9084
ISSN	0300-9084
DOI	10.1016/j.biochi.2021.03.015
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Article ; Online: DNA binding site kinetics of a large antiviral polyamide.

Niederschulte, Jacquelyn / Song, Yang / Park, Andrew H / Bashkin, James K / Dupureur, Cynthia M

Biochimie

2021 Volume 185, Page(s) 146–154

Abstract: Polyamides (PAs) are powerful DNA ligands that can bind the minor groove of DNA with high affinity and specificity. While the characterization of PA-DNA behavior has focused principally on hairpin PAs 6-8 rings in size, there is increasing evidence that ... ...

Abstract	Polyamides (PAs) are powerful DNA ligands that can bind the minor groove of DNA with high affinity and specificity. While the characterization of PA-DNA behavior has focused principally on hairpin PAs 6-8 rings in size, there is increasing evidence that their behavior does not necessarily reflect the complexities that are emerging from studies of larger hairpin PAs, particularly concerning sequence mismatch tolerance and observed but unaddressed high PA-target site binding stoichiometries. To explore these complexities in more detail, kinetics studies of binding a large anti-HPV hairpin polyamide to an isolated DNA recognition site are described. Using a fluorescence assay, two distinct binding phases are observed for the first time in hairpin PA literature. PA14 concentration dependence analysis indicates that the faster binding event is diffusion-controlled; the apparent, second event is significantly slower (350-1500 fold). Both association phases are sampled in 1:1 complexes, consistent with cooperative binding of two PA molecules even under this condition. Fitting of the slow phase to a biexponential model yields two λ
MeSH term(s)	Antiviral Agents/chemistry ; Binding Sites ; DNA/chemistry ; Kinetics ; Nylons/chemistry
Chemical Substances	Antiviral Agents ; Nylons ; DNA (9007-49-2)
Language	English
Publishing date	2021-03-29
Publishing country	France
Document type	Journal Article
ZDB-ID	120345-9
ISSN	1638-6183 ; 0300-9084
ISSN (online)	1638-6183
ISSN	0300-9084
DOI	10.1016/j.biochi.2021.03.015
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Article ; Online: DNA binding thermodynamics and site stoichiometry as a function of polyamide size.

Song, Yang / Niederschulte, Jacquelyn / Bales, Kristin N / Park, Andrew H / Bashkin, James K / Dupureur, Cynthia M

Biochimie

2019 Volume 165, Page(s) 170–178

Abstract: The interactions of 6-8 ring hairpin polyamides (PAs) with the minor groove of DNA have been investigated extensively. More recent studies of large antiviral PAs (14-20 rings) active against small DNA tumor viruses lead to questions regarding the extent ... ...

Abstract	The interactions of 6-8 ring hairpin polyamides (PAs) with the minor groove of DNA have been investigated extensively. More recent studies of large antiviral PAs (14-20 rings) active against small DNA tumor viruses lead to questions regarding the extent to which the DNA binding behaviors of the well studied, smaller PAs can be reliably extrapolated to the larger ones. Described here is the first reported study of hairpin PA-DNA binding thermodynamics as a function of PA size (6-20 rings). All PAs exhibit binding affinity in the low nM to upper pM range, which indicates that affinity is not a discriminator of antiviral activity. Unlike the smaller PAs, a 20-ring PA does not appreciably dissociate from DNA in competition experiments, which indicates very long residence time that is consistent with antiviral activity. While the DNA binding thermodynamics for the smaller antivirally inactive 6- and 8-ring PAs is clearly enthalpically driven, the larger antiviral PAs (14- and 20-rings) exhibit strongly entropically-driven DNA binding. These distinct energetic signatures indicate that different types of interactions drive these associations. In DNA binding site stoichiometry experiments conducted at both nM and μM concentrations, all PAs except the 6-ring PA bind an isolated site with site stoichiometry of at least two PAs per recognition sequence. Electrostatic contributions to DNA binding affinity are small for all PAs and not correlated with PA size but weakly correlated with the number of imidazole residues. Altogether, these results indicate that DNA binding behaviors of smaller hairpin PAs do not necessarily reflect those of larger PAs. These are vital considerations in the development of hairpin PAs for biological use.
MeSH term(s)	Antiviral Agents/chemistry ; Binding Sites ; DNA, Neoplasm/chemistry ; DNA, Viral/chemistry ; Imidazoles/chemistry ; Inverted Repeat Sequences ; Nucleic Acid Conformation ; Thermodynamics
Chemical Substances	Antiviral Agents ; DNA, Neoplasm ; DNA, Viral ; Imidazoles
Language	English
Publishing date	2019-07-31
Publishing country	France
Document type	Journal Article
ZDB-ID	120345-9
ISSN	1638-6183 ; 0300-9084
ISSN (online)	1638-6183
ISSN	0300-9084
DOI	10.1016/j.biochi.2019.07.021
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Article: DNA Binding Thermodynamics and Site Stoichiometry as a Function of Polyamide Size

Song, Yang / Bales, Kristin N / Bashkin, James K / Dupureur, Cynthia M / Niederschulte, Jacquelyn / Park, Andrew H

Biochimie. 2019 July 29,

2019

Abstract	The interactions of 6-8 ring hairpin polyamides (PAs) with the minor groove of DNA have been investigated extensively. More recent studies of large antiviral PAs (14-20 rings) active against small DNA tumor viruses lead to questions regarding the extent to which the DNA binding behaviors of the well studied, smaller PAs can be reliably extrapolated to the larger ones. Described here is the first reported study of hairpin PA-DNA binding thermodynamics as a function of PA size (6 to 20 rings). All PAs exhibit binding affinity in the low nM to upper pM range, which indicates that affinity is not a discriminator of antiviral activity. Unlike the smaller PAs, a 20-ring PA does not appreciably dissociate from DNA in competition experiments, which indicates very long residence time that is consistent with antiviral activity (the smaller PAs are inactive against human papillomavirus, HPV). While the DNA binding thermodynamics for the smaller antivirally inactive 6- and 8-ring PAs is clearly enthalpically driven, the larger antiviral PAs (14- and 20-rings) exhibit strongly entropically-driven DNA binding. These distinct energetic signatures indicate that different types of interactions drive these associations. In DNA binding site stoichiometry experiments conducted at both nM and μM concentrations, all PAs except the 6-ring PA bind an isolated site with site stoichiometry of at least two PAs per recognition sequence. Electrostatic contributions to DNA binding affinity are small for all PAs and not correlated with PA size but weakly correlated with the number of imidazole residues. Altogether, these results indicate that DNA binding behaviors of smaller hairpin PAs do not necessarily reflect those of larger PAs. These are vital considerations in the development of hairpin PAs for biological use.
Keywords	antiviral properties ; binding capacity ; binding sites ; DNA ; imidazole ; neoplasms ; Papillomaviridae ; polyamides ; stoichiometry ; thermodynamics ; viruses
Language	English
Dates of publication	2019-0729
Publishing place	Elsevier B.V.
Document type	Article
Note	Pre-press version
ZDB-ID	120345-9
ISSN	0300-9084
ISSN	0300-9084
DOI	10.1016/j.biochi.2019.07.021
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Article ; Online: Targeting Glycosylated PD-1 Induces Potent Antitumor Immunity.

Cancer research

2020 Volume 80, Issue 11, Page(s) 2298–2310

Abstract: Immunotherapies targeting programmed cell death protein 1 (PD-1) and programmed cell death 1 ligand 1 (PD-L1) immune checkpoints represent a major breakthrough in cancer treatment. PD-1 is an inhibitory receptor expressed on the surface of activated T ... ...

Abstract	Immunotherapies targeting programmed cell death protein 1 (PD-1) and programmed cell death 1 ligand 1 (PD-L1) immune checkpoints represent a major breakthrough in cancer treatment. PD-1 is an inhibitory receptor expressed on the surface of activated T cells that dampens T-cell receptor (TCR)/CD28 signaling by engaging with its ligand PD-L1 expressed on cancer cells. Despite the clinical success of PD-1 blockade using mAbs, most patients do not respond to the treatment, and the underlying regulatory mechanisms of PD-1 remain incompletely defined. Here we show that PD-1 is extensively N-glycosylated in T cells and the intensities of its specific glycoforms are altered upon TCR activation. Glycosylation was critical for maintaining PD-1 protein stability and cell surface localization. Glycosylation of PD-1, especially at the N58 site, was essential for mediating its interaction with PD-L1. The mAb STM418 specifically targeted glycosylated PD-1, exhibiting higher binding affinity to PD-1 than FDA-approved PD-1 antibodies, potently inhibiting PD-L1/PD-1 binding, and enhancing antitumor immunity. Together, these findings provide novel insights into the functional significance of PD-1 glycosylation and offer a rationale for targeting glycosylated PD-1 as a potential strategy for immunotherapy. SIGNIFICANCE: These findings demonstrate that glycosylation of PD-1 is functionally significant and targeting glycosylated PD-1 may serve as a means to improve immunotherapy response.
MeSH term(s)	Animals ; Antibodies, Monoclonal, Humanized/pharmacology ; Antineoplastic Agents, Immunological/pharmacology ; Breast Neoplasms/drug therapy ; Breast Neoplasms/immunology ; Breast Neoplasms/metabolism ; Female ; Glycosylation ; HEK293 Cells ; Heterografts ; Humans ; Jurkat Cells ; Leukemia, T-Cell/drug therapy ; Leukemia, T-Cell/immunology ; Leukemia, T-Cell/metabolism ; Lymphocyte Activation ; Mice ; Mice, Inbred NOD ; Mice, SCID ; Molecular Targeted Therapy ; Nivolumab/pharmacology ; Programmed Cell Death 1 Receptor/antagonists & inhibitors ; Programmed Cell Death 1 Receptor/immunology ; Programmed Cell Death 1 Receptor/metabolism ; T-Lymphocytes/immunology ; T-Lymphocytes/metabolism
Chemical Substances	Antibodies, Monoclonal, Humanized ; Antineoplastic Agents, Immunological ; PDCD1 protein, human ; Programmed Cell Death 1 Receptor ; Nivolumab (31YO63LBSN) ; pembrolizumab (DPT0O3T46P)
Language	English
Publishing date	2020-03-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1432-1
ISSN	1538-7445 ; 0008-5472
ISSN (online)	1538-7445
ISSN	0008-5472
DOI	10.1158/0008-5472.CAN-19-3133
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Article: ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana

Ko, Jae-Heung / Yang, Seung Hwan / Park, Andrew H / Lerouxel, Olivier / Han, Kyung-Hwan

Plant journal. 2007 June, v. 50, no. 6

2007

Abstract: Vascular plants evolved to have xylem that provides physical support for their growing body and serves as a conduit for water and nutrient transport. In a previous study, we used comparative-transcriptome analyses to select a group of genes that were ... ...

Abstract	Vascular plants evolved to have xylem that provides physical support for their growing body and serves as a conduit for water and nutrient transport. In a previous study, we used comparative-transcriptome analyses to select a group of genes that were upregulated in xylem of Arabidopsis plants undergoing secondary growth. Subsequent analyses identified a plant-specific NAC-domain transcription factor gene (ANAC012) as a candidate for genetic regulation of xylem formation. Promoter-GUS analyses showed that ANAC012 expression was preferentially localized in the (pro)cambium region of inflorescence stem and root. Using yeast transactivation analyses, we confirmed the function of ANAC012 as a transcriptional activator, and identified an activation domain in the C terminus. Ectopic overexpression of ANAC012 in Arabidopsis (35S::ANAC012 plants) dramatically suppressed secondary wall deposition in the xylary fiber and slightly increased cell-wall thickness in the xylem vessels. Cellulose compositions of the cell wall were decreased in the inflorescent stems and roots of 35S::ANAC012 plants, probably resulting from defects in xylary fiber formation. Our data suggest that ANAC012 may act as a negative regulator of secondary wall thickening in xylary fibers.
Keywords	xylem
Language	English
Dates of publication	2007-06
Size	p. 1035-1048.
Publisher	Blackwell Publishing Ltd
Publishing place	Oxford, UK
Document type	Article
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/j.1365-313X.2007.03109.x
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Article: ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana.

Ko, Jae-Heung / Yang, Seung Hwan / Park, Andrew H / Lerouxel, Olivier / Han, Kyung-Hwan

The Plant journal : for cell and molecular biology

2007 Volume 50, Issue 6, Page(s) 1035–1048

Abstract	Vascular plants evolved to have xylem that provides physical support for their growing body and serves as a conduit for water and nutrient transport. In a previous study, we used comparative-transcriptome analyses to select a group of genes that were upregulated in xylem of Arabidopsis plants undergoing secondary growth. Subsequent analyses identified a plant-specific NAC-domain transcription factor gene (ANAC012) as a candidate for genetic regulation of xylem formation. Promoter-GUS analyses showed that ANAC012 expression was preferentially localized in the (pro)cambium region of inflorescence stem and root. Using yeast transactivation analyses, we confirmed the function of ANAC012 as a transcriptional activator, and identified an activation domain in the C terminus. Ectopic overexpression of ANAC012 in Arabidopsis (35S::ANAC012 plants) dramatically suppressed secondary wall deposition in the xylary fiber and slightly increased cell-wall thickness in the xylem vessels. Cellulose compositions of the cell wall were decreased in the inflorescent stems and roots of 35S::ANAC012 plants, probably resulting from defects in xylary fiber formation. Our data suggest that ANAC012 may act as a negative regulator of secondary wall thickening in xylary fibers.
MeSH term(s)	Amino Acid Sequence ; Arabidopsis/genetics ; Arabidopsis/growth & development ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Cell Wall/metabolism ; Gene Expression ; Gene Expression Profiling ; Genes, Plant ; Molecular Sequence Data ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Transcriptional Activation ; Xylem/growth & development
Chemical Substances	ANAC012 protein, Arabidopsis ; Arabidopsis Proteins ; Transcription Factors
Language	English
Publishing date	2007-06
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/j.1365-313X.2007.03109.x
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Article ; Online: Eradication of Triple-Negative Breast Cancer Cells by Targeting Glycosylated PD-L1.

Li, Chia-Wei / Lim, Seung-Oe / Chung, Ezra M / Kim, Yong-Soo / Park, Andrew H / Yao, Jun / Cha, Jong-Ho / Xia, Weiya / Chan, Li-Chuan / Kim, Taewan / Chang, Shih-Shin / Lee, Heng-Huan / Chou, Chao-Kai / Liu, Yen-Liang / Yeh, Hsin-Chih / Perillo, Evan P / Dunn, Andrew K / Kuo, Chu-Wei / Khoo, Kay-Hooi /

Hsu, Jennifer L / Wu, Yun / Hsu, Jung-Mao / Yamaguchi, Hirohito / Huang, Tzu-Hsuan / Sahin, Aysegul A / Hortobagyi, Gabriel N / Yoo, Stephen S / Hung, Mien-Chie

Cancer cell

2018 Volume 33, Issue 2, Page(s) 187–201.e10

Abstract: Protein glycosylation provides proteomic diversity in regulating protein localization, stability, and activity; it remains largely unknown whether the sugar moiety contributes to immunosuppression. In the study of immune receptor glycosylation, we showed ...

Abstract	Protein glycosylation provides proteomic diversity in regulating protein localization, stability, and activity; it remains largely unknown whether the sugar moiety contributes to immunosuppression. In the study of immune receptor glycosylation, we showed that EGF induces programmed death ligand 1 (PD-L1) and receptor programmed cell death protein 1 (PD-1) interaction, requiring β-1,3-N-acetylglucosaminyl transferase (B3GNT3) expression in triple-negative breast cancer. Downregulation of B3GNT3 enhances cytotoxic T cell-mediated anti-tumor immunity. A monoclonal antibody targeting glycosylated PD-L1 (gPD-L1) blocks PD-L1/PD-1 interaction and promotes PD-L1 internalization and degradation. In addition to immune reactivation, drug-conjugated gPD-L1 antibody induces a potent cell-killing effect as well as a bystander-killing effect on adjacent cancer cells lacking PD-L1 expression without any detectable toxicity. Our work suggests targeting protein glycosylation as a potential strategy to enhance immune checkpoint therapy.
MeSH term(s)	Animals ; Antibodies, Monoclonal/pharmacology ; Cell Line, Tumor ; Female ; Humans ; Lymphocytes, Tumor-Infiltrating/drug effects ; Lymphocytes, Tumor-Infiltrating/immunology ; Mice, Inbred BALB C ; N-Acetylglucosaminyltransferases/drug effects ; N-Acetylglucosaminyltransferases/metabolism ; Programmed Cell Death 1 Receptor/immunology ; Triple Negative Breast Neoplasms/drug therapy ; Triple Negative Breast Neoplasms/immunology ; Triple Negative Breast Neoplasms/metabolism
Chemical Substances	Antibodies, Monoclonal ; Programmed Cell Death 1 Receptor ; N-Acetylglucosaminyltransferases (EC 2.4.1.-)
Language	English
Publishing date	2018-03-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2078448-X
ISSN	1878-3686 ; 1535-6108
ISSN (online)	1878-3686
ISSN	1535-6108
DOI	10.1016/j.ccell.2018.01.009
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