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Article: The ER-Mitochondria Interface as a Dynamic Hub for T Cell Efficacy in Solid Tumors.

Hunt, Elizabeth G / Andrews, Alex M / Larsen, Sydney R / Thaxton, Jessica E

Frontiers in cell and developmental biology

2022 Volume 10, Page(s) 867341

Abstract: The endoplasmic reticulum (ER) is a large continuous membranous organelle that plays a central role as the hub of protein and lipid synthesis while the mitochondria is the principal location for energy production. T cells are an immune subset exhibiting ... ...

Abstract	The endoplasmic reticulum (ER) is a large continuous membranous organelle that plays a central role as the hub of protein and lipid synthesis while the mitochondria is the principal location for energy production. T cells are an immune subset exhibiting robust dependence on ER and mitochondrial function based on the need for protein synthesis and secretion and metabolic dexterity associated with foreign antigen recognition and cytotoxic effector response. Intimate connections exist at mitochondrial-ER contact sites (MERCs) that serve as the structural and biochemical platforms for cellular metabolic homeostasis through regulation of fission and fusion as well as glucose, Ca
Language	English
Publishing date	2022-04-27
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2737824-X
ISSN	2296-634X
ISSN	2296-634X
DOI	10.3389/fcell.2022.867341
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Article ; Online: Stress relief for cancer immunotherapy: implications for the ER stress response in tumor immunity.

Andrews, Alex M / Tennant, Megan D / Thaxton, Jessica E

Cancer immunology, immunotherapy : CII

2020 Volume 70, Issue 5, Page(s) 1165–1175

Abstract: The solid tumor microenvironment is replete with factors that present a stress to infiltrating immune cells. Endoplasmic reticulum (ER) stress sensor PKR-like ER kinase (PERK) is primed to sense and respond to the burden of misfolded proteins in the ER ... ...

Abstract	The solid tumor microenvironment is replete with factors that present a stress to infiltrating immune cells. Endoplasmic reticulum (ER) stress sensor PKR-like ER kinase (PERK) is primed to sense and respond to the burden of misfolded proteins in the ER lumen induced by cell stressors. PERK has documented roles as a master regulator of acute and chronic responses to cell stress as well as in the regulation of cell metabolism. Here, we provide an overview of the roles of PERK based on what is known and remains to be tested in immune cells in tumors and impacts on tumor control. PERK is one of several ER kinases able to preferentially induce activating transcription factor 4 (ATF4) as a response to cell stress. ATF4 orchestrates the oxidative stress response and governs amino acid metabolism. We discuss the tested role of ATF4 in tumor immunity and provide insight on the dueling protective and deleterious roles that ATF4 may play in the stress of solid tumors.
MeSH term(s)	Activating Transcription Factor 4/genetics ; Activating Transcription Factor 4/metabolism ; Animals ; Endoplasmic Reticulum Stress/immunology ; Humans ; Immunity ; Immunotherapy/methods ; Neoplasms/immunology ; T-Lymphocytes/immunology ; Tumor Microenvironment ; eIF-2 Kinase/metabolism
Chemical Substances	Activating Transcription Factor 4 (145891-90-3) ; PERK kinase (EC 2.7.11.1) ; eIF-2 Kinase (EC 2.7.11.1)
Language	English
Publishing date	2020-10-26
Publishing country	Germany
Document type	Journal Article ; Review
ZDB-ID	195342-4
ISSN	1432-0851 ; 0340-7004
ISSN (online)	1432-0851
ISSN	0340-7004
DOI	10.1007/s00262-020-02740-3
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Article ; Online: Acetyl-CoA carboxylase obstructs CD8

Hunt, Elizabeth G / Hurst, Katie E / Riesenberg, Brian P / Kennedy, Andrew S / Gandy, Evelyn J / Andrews, Alex M / Del Mar Alicea Pauneto, Coral / Ball, Lauren E / Wallace, Emily D / Gao, Peng / Meier, Jeremy / Serody, John J / Coleman, Michael F / Thaxton, Jessica E

Cell metabolism

2024 Volume 36, Issue 5, Page(s) 969–983.e10

Abstract: The solid tumor microenvironment (TME) imprints a compromised metabolic state in tumor-infiltrating T cells (TILs), hallmarked by the inability to maintain effective energy synthesis for antitumor function and survival. T cells in the TME must catabolize ...

Abstract	The solid tumor microenvironment (TME) imprints a compromised metabolic state in tumor-infiltrating T cells (TILs), hallmarked by the inability to maintain effective energy synthesis for antitumor function and survival. T cells in the TME must catabolize lipids via mitochondrial fatty acid oxidation (FAO) to supply energy in nutrient stress, and it is established that T cells enriched in FAO are adept at cancer control. However, endogenous TILs and unmodified cellular therapy products fail to sustain bioenergetics in tumors. We reveal that the solid TME imposes perpetual acetyl-coenzyme A (CoA) carboxylase (ACC) activity, invoking lipid biogenesis and storage in TILs that opposes FAO. Using metabolic, lipidomic, and confocal imaging strategies, we find that restricting ACC rewires T cell metabolism, enabling energy maintenance in TME stress. Limiting ACC activity potentiates a gene and phenotypic program indicative of T cell longevity, engendering T cells with increased survival and polyfunctionality, which sustains cancer control.
MeSH term(s)	Acetyl-CoA Carboxylase/metabolism ; Tumor Microenvironment ; Animals ; CD8-Positive T-Lymphocytes/metabolism ; CD8-Positive T-Lymphocytes/immunology ; Mice ; Lipid Metabolism ; Mice, Inbred C57BL ; Humans ; Fatty Acids/metabolism ; Female ; Cell Line, Tumor ; Lymphocytes, Tumor-Infiltrating/immunology ; Lymphocytes, Tumor-Infiltrating/metabolism ; Mitochondria/metabolism
Chemical Substances	Acetyl-CoA Carboxylase (EC 6.4.1.2) ; Fatty Acids
Language	English
Publishing date	2024-03-14
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2176834-1
ISSN	1932-7420 ; 1550-4131
ISSN (online)	1932-7420
ISSN	1550-4131
DOI	10.1016/j.cmet.2024.02.009
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Article ; Online: To affinity and beyond: harnessing the T cell receptor for cancer immunotherapy.

Thaxton, Jessica E / Li, Zihai

Human vaccines & immunotherapeutics

2014 Volume 10, Issue 11, Page(s) 3313–3321

Abstract: T cell adoptive therapies for immune-mediated regression of cancers have attracted a great deal of recent attention. Clinical results are glamorous, yet much remains to be uncovered behind the basic science that allows us to engineer T cells and T cell ... ...

Abstract	T cell adoptive therapies for immune-mediated regression of cancers have attracted a great deal of recent attention. Clinical results are glamorous, yet much remains to be uncovered behind the basic science that allows us to engineer T cells and T cell receptors (TCRs) for clinical use. We discuss the development of TCRs for therapeutic use in the context of thymic selection toward central tolerance and we review therapies based on tumor infiltrating lymphocytes (TILs), endogenous antigen specific TCRs, and engineered TCRs. Further we discuss the development of low and high affinity TCRs and the extent to which each challenges central tolerance. Current results suggest that adaptation of TCR engineering of moderate affinity TCRs coupled with co-regulatory and stimulatory molecules may be the safest and most efficacious road for TCR development aimed at tumor abolition.
MeSH term(s)	Humans ; Immunotherapy, Adoptive/methods ; Lymphocytes, Tumor-Infiltrating/immunology ; Neoplasms/immunology ; Neoplasms/therapy ; Protein Engineering ; Receptors, Antigen, T-Cell, alpha-beta/genetics ; Receptors, Antigen, T-Cell, alpha-beta/immunology ; T-Lymphocytes, Cytotoxic/immunology ; T-Lymphocytes, Cytotoxic/transplantation ; T-Lymphocytes, Regulatory/immunology ; Tumor Escape/immunology
Chemical Substances	Receptors, Antigen, T-Cell, alpha-beta
Language	English
Publishing date	2014
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	2664176-8
ISSN	2164-554X ; 2164-5515
ISSN (online)	2164-554X
ISSN	2164-5515
DOI	10.4161/21645515.2014.973314
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Article ; Online: An observational study and randomized trial of stress reactivity in cancer disparities.

Halbert, Chanita Hughes / Jefferson, Melanie S / Danielson, Carla / Froeliger, Brett / Giordano, Antonio / Thaxton, Jessica E

Health psychology : official journal of the Division of Health Psychology, American Psychological Association

2020 Volume 39, Issue 9, Page(s) 745–757

Abstract: Objectives: Physiological stress responses have been suggested as a mechanism through which social and biological factors contribute to racial disparities in breast cancer outcomes. Many African Americans experience stressful life events and ... ...

Abstract	Objectives: Physiological stress responses have been suggested as a mechanism through which social and biological factors contribute to racial disparities in breast cancer outcomes. Many African Americans experience stressful life events and circumstances. These social factors may contribute to an increased risk of advanced stage disease at diagnosis and/or faster progression, but not all African American women exposed to adverse social factors develop advanced stage disease. Similarly, women who have a limited number of stressors can develop advanced stage breast cancer. Highly individualized stress reactivity may account for these inconsistent associations. Method: This report describes the rationale, design, and methods for an exploratory study that uses the experimental medicine approach to: (a) characterize the nature and distribution of stress reactivity among African American breast cancer survivors based on socioeconomic, clinical, and social stressors; (b) examine the impact of stress reactivity on temporal discounting; and (c) determine the extent to which stress reactivity and temporal discounting are associated with adherence to recommendations for cancer control behaviors and treatment compliance as part of the Science of Behavior Change Network. Results: This study addresses several empirical gaps about the most effective ways to develop behavior change interventions for a medically underserved population that continues to experience disparities in cancer morbidity and mortality. Conclusions: Results from this research will provide the empirical and conceptual basis for future intervention protocols that target mechanisms that are critical to disparities in African American breast cancer survivors. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
MeSH term(s)	Adult ; Cancer Survivors/psychology ; Female ; Healthcare Disparities/standards ; Humans ; Stress, Psychological/psychology
Language	English
Publishing date	2020-09-08
Publishing country	United States
Document type	Journal Article ; Randomized Controlled Trial
ZDB-ID	226369-5
ISSN	1930-7810 ; 0278-6133
ISSN (online)	1930-7810
ISSN	0278-6133
DOI	10.1037/hea0000882
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Article: The degree of T cell stemness differentially impacts the potency of adoptive cancer immunotherapy in a Lef-1 and Tcf-1 dependent manner.

Rangel Rivera, Guillermo O / Dwyer, Connor J / Knochelmann, Hannah M / Smith, Aubrey S / Aksoy, Arman / Cole, Anna C / Wyatt, Megan M / Thaxton, Jessica E / Lesinski, Gregory B / Paulos, Chrystal M

bioRxiv : the preprint server for biology

2023

Abstract: Generating stem memory T cells ( ... ...

Abstract	Generating stem memory T cells (T
Language	English
Publishing date	2023-03-10
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.08.531589
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Article ; Online: Progressively Enhancing Stemness of Adoptively Transferred T Cells with PI3Kδ Blockade Improves Metabolism and Antitumor Immunity.

Rangel Rivera, Guillermo O / Dwyer, Connor J / Knochelmann, Hannah M / Smith, Aubrey S / Aksoy, Bülent Arman / Cole, Anna C / Wyatt, Megan M / Kumaresan, Soundharya / Thaxton, Jessica E / Lesinski, Gregory B / Paulos, Chrystal M

Cancer research

2023 Volume 84, Issue 1, Page(s) 69–83

Abstract: Generating stem-like memory T cells (TSCM) is a potential strategy to improve adoptive immunotherapy. Elucidating optimal ways to modulate signaling pathways that enrich TSCM properties could identify approaches to achieve this goal. We discovered herein ...

Abstract	Generating stem-like memory T cells (TSCM) is a potential strategy to improve adoptive immunotherapy. Elucidating optimal ways to modulate signaling pathways that enrich TSCM properties could identify approaches to achieve this goal. We discovered herein that blocking the PI3Kδ pathway pharmaceutically to varying degrees can generate T cells with increasingly heightened stemness properties, based on the progressive enrichment of the transcription factors Tcf1 and Lef1. T cells with enhanced stemness features exhibited metabolic plasticity, marked by improved mitochondrial function and glucose uptake after tumor recognition. Conversely, T cells with low or medium stemness were less metabolically dynamic, vulnerable to antigen-induced cell death, and expressed more inhibitory checkpoint receptors. Only T-cell receptor-specific or chimeric antigen receptor (CAR)-specific T cells with high stemness persisted in vivo and mounted protective immunity to tumors. Likewise, the strongest level of PI3Kδ blockade in vitro generated human tumor-infiltrating lymphocytes and CAR T cells with elevated stemness properties, in turn bolstering their capacity to regress human solid tumors. The stemness level of T cells in vitro was important, ultimately impacting their efficacy in mice bearing three distinct solid tumors. Lef1 and Tcf1 sustained antitumor protection by donor high CD8+ TSCM or CD4+ Th17SCM, as deletion of either one compromised the therapeutic efficacy. Collectively, these findings highlight the importance of strategic modulation of PI3Kδ signaling in T cells to induce stemness and lasting protective responses to solid tumors. Significance: Elevating T-cell stemness by progressively blocking PI3Kδ signaling during ex vivo manufacturing of adoptive cell therapies alters metabolic and functional properties to enhance antitumor immunity dependent on Tcf1 and Lef1.
MeSH term(s)	Humans ; Mice ; Animals ; T-Lymphocytes ; Neoplasms ; Immunotherapy, Adoptive ; Lymphocytes, Tumor-Infiltrating ; Receptors, Antigen, T-Cell ; CD8-Positive T-Lymphocytes
Chemical Substances	Receptors, Antigen, T-Cell
Language	English
Publishing date	2023-10-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	1432-1
ISSN	1538-7445 ; 0008-5472
ISSN (online)	1538-7445
ISSN	0008-5472
DOI	10.1158/0008-5472.CAN-23-0801
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Article ; Online: Stress-Mediated Attenuation of Translation Undermines T-cell Activity in Cancer.

Riesenberg, Brian P / Hunt, Elizabeth G / Tennant, Megan D / Hurst, Katie E / Andrews, Alex M / Leddy, Lee R / Neskey, David M / Hill, Elizabeth G / Rivera, Guillermo O Rangel / Paulos, Chrystal M / Gao, Peng / Thaxton, Jessica E

Cancer research

2022 Volume 82, Issue 23, Page(s) 4386–4399

Abstract: Protein synthesis supports robust immune responses. Nutrient competition and global cell stressors in the tumor microenvironment (TME) may impact protein translation in T cells and antitumor immunity. Using human and mouse tumors, we demonstrated here ... ...

Abstract	Protein synthesis supports robust immune responses. Nutrient competition and global cell stressors in the tumor microenvironment (TME) may impact protein translation in T cells and antitumor immunity. Using human and mouse tumors, we demonstrated here that protein translation in T cells is repressed in solid tumors. Reduced glucose availability to T cells in the TME led to activation of the unfolded protein response (UPR) element eIF2α (eukaryotic translation initiation factor 2 alpha). Genetic mouse models revealed that translation attenuation mediated by activated p-eIF2α undermines the ability of T cells to suppress tumor growth. Reprograming T-cell metabolism was able to alleviate p-eIF2α accumulation and translational attenuation in the TME, allowing for sustained protein translation. Metabolic and pharmacological approaches showed that proteasome activity mitigates induction of p-eIF2α to support optimal antitumor T-cell function, protecting from translation attenuation and enabling prolonged cytokine synthesis in solid tumors. Together, these data identify a new therapeutic avenue to fuel the efficacy of tumor immunotherapy. Significance: Proteasome function is a necessary cellular component for endowing T cells with tumor killing capacity by mitigating translation attenuation resulting from the unfolded protein response induced by stress in the tumor microenvironment.
MeSH term(s)	Humans ; Mice ; Animals ; T-Lymphocytes/metabolism ; Proteasome Endopeptidase Complex ; Neoplasms/therapy ; Tumor Microenvironment ; Immunotherapy/methods ; Eukaryotic Initiation Factor-2/genetics ; Eukaryotic Initiation Factor-2/metabolism
Chemical Substances	Proteasome Endopeptidase Complex (EC 3.4.25.1) ; Eukaryotic Initiation Factor-2
Language	English
Publishing date	2022-09-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1432-1
ISSN	1538-7445 ; 0008-5472
ISSN (online)	1538-7445
ISSN	0008-5472
DOI	10.1158/0008-5472.CAN-22-1744
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Article ; Online: Remodeling Translation Primes CD8

Hurst, Katie E / Lawrence, Kiley A / Robino, Rob A / Ball, Lauren E / Chung, Dongjun / Thaxton, Jessica E

Cancer immunology research

2020 Volume 8, Issue 5, Page(s) 587–595

Abstract: The requisites for protein translation in T cells are poorly understood and how translation shapes the antitumor efficacy of T cells is unknown. Here we demonstrated that IL15-conditioned T cells were primed by the metabolic energy sensor AMP-activated ... ...

Abstract	The requisites for protein translation in T cells are poorly understood and how translation shapes the antitumor efficacy of T cells is unknown. Here we demonstrated that IL15-conditioned T cells were primed by the metabolic energy sensor AMP-activated protein kinase to undergo diminished translation relative to effector T cells. However, we showed that IL15-conditioned T cells exhibited a remarkable capacity to enhance their protein translation in tumors, which effector T cells were unable to duplicate. Studying the modulation of translation for applications in cancer immunotherapy revealed that direct
MeSH term(s)	Animals ; CD8-Positive T-Lymphocytes/immunology ; Cell Line, Tumor ; Coculture Techniques ; Disease Models, Animal ; Female ; Immunotherapy/methods ; Interleukin-15/metabolism ; Lymphocyte Activation/immunology ; Mice ; Mice, Inbred C57BL ; Neoplasms/immunology ; Neoplasms/metabolism ; Neoplasms/therapy ; Peptide Elongation Factor 2/metabolism ; Protein Biosynthesis
Chemical Substances	Interleukin-15 ; Peptide Elongation Factor 2
Language	English
Publishing date	2020-02-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2732489-8
ISSN	2326-6074 ; 2326-6066
ISSN (online)	2326-6074
ISSN	2326-6066
DOI	10.1158/2326-6066.CIR-19-0516
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Article ; Online: Interleukin-10: a multi-faceted agent of pregnancy.

Thaxton, Jessica E / Sharma, Surendra

American journal of reproductive immunology (New York, N.Y. : 1989)

2010 Volume 63, Issue 6, Page(s) 482–491

Abstract: It is widely accepted that pregnancy constitutes a unique developmental event. Unprecedented intrauterine actions of angiogenesis, immunity, and neuroendocrine regulation are juxtaposed to mechanisms of senescence that enable fetal growth and protection. ...

Abstract	It is widely accepted that pregnancy constitutes a unique developmental event. Unprecedented intrauterine actions of angiogenesis, immunity, and neuroendocrine regulation are juxtaposed to mechanisms of senescence that enable fetal growth and protection. The suppressive and regulatory factors that facilitate healthy pregnancy are under investigation. In non-pregnant systems of infection and inflammation, the cytokine interleukin-10 (IL-10) has been widely investigated because of its potential as a key immunosuppressant in response to a multitude of inflammatory events. In the context of pregnancy, IL-10 levels increase markedly in women during early pregnancy and remain elevated well into the third trimester immediately prior to onset of labor. The role of IL-10 during pregnancy as a suppressor of active maternal immunity to allow acceptance of the fetal allograft has been a point of study. Moreover, secretion of IL-10 by a diverse set of maternal and fetal cells has proven to aid in the orchestration of normal processes of pregnancy. Interestingly, some of the more profound findings regarding the actions of IL-10 during pregnancy have manifested from research that focuses on aberrant pregnancy outcomes as a result of inflammation, hormonal imbalances, or gene-environment interactions. This review focuses on the role of IL-10 as a facilitator of successful pregnancy both as an immune suppressive agent and a mediator of cross talk between the placenta and the decidua. Importantly, we discuss investigations on adverse pregnancy conditions to further elucidate the multifarious role of IL-10 at the maternal-fetal interface.
MeSH term(s)	Animals ; Decidua/immunology ; Decidua/metabolism ; Female ; Humans ; Inflammation ; Interleukin-10/immunology ; Interleukin-10/metabolism ; Mice ; Mice, Inbred CBA ; Mice, Inbred DBA ; Placenta/immunology ; Placenta/metabolism ; Pregnancy/immunology ; Pregnancy Outcome
Chemical Substances	Interleukin-10 (130068-27-8)
Language	English
Publishing date	2010-02-16
Publishing country	Denmark
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	604542-x
ISSN	1600-0897 ; 0271-7352 ; 8755-8920 ; 1046-7408
ISSN (online)	1600-0897
ISSN	0271-7352 ; 8755-8920 ; 1046-7408
DOI	10.1111/j.1600-0897.2010.00810.x
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