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Article ; Online: Hypoxia-activated prodrug and antiangiogenic therapies cooperatively treat pancreatic cancer but elicit immunosuppressive G-MDSC infiltration.

Liu, Arthur / Gammon, Seth T / Pisaneschi, Federica / Boda, Akash / Ager, Casey R / Piwnica-Worms, David / Hong, David S / Curran, Michael A

JCI insight

2024 Volume 9, Issue 1

Abstract: We previously showed that ablation of tumor hypoxia can sensitize tumors to immune checkpoint blockade (ICB). Here, we used a Kras+/G12D TP53+/R172H Pdx1-Cre-derived (KPC-derived) model of pancreatic adenocarcinoma to examine the tumor response and ... ...

Abstract	We previously showed that ablation of tumor hypoxia can sensitize tumors to immune checkpoint blockade (ICB). Here, we used a Kras+/G12D TP53+/R172H Pdx1-Cre-derived (KPC-derived) model of pancreatic adenocarcinoma to examine the tumor response and adaptive resistance mechanisms involved in response to 2 established methods of hypoxia-reducing therapy: the hypoxia-activated prodrug TH-302 and vascular endothelial growth factor receptor 2 (VEGFR-2) blockade. The combination of both modalities normalized tumor vasculature, increased DNA damage and cell death, and delayed tumor growth. In contrast with prior cancer models, the combination did not alleviate overall tissue hypoxia or sensitize these KPC tumors to ICB therapy despite qualitative improvements to the CD8+ T cell response. Bulk tumor RNA sequencing, flow cytometry, and adoptive myeloid cell transfer suggested that treated tumor cells increased their capacity to recruit granulocytic myeloid-derived suppressor cells (G-MDSCs) through CCL9 secretion. Blockade of the CCL9/CCR1 axis could limit G-MDSC migration, and depletion of Ly6G-positive cells could sensitize tumors to the combination of TH-302, anti-VEGFR-2, and ICB. Together, these data suggest that pancreatic tumors modulate G-MDSC migration as an adaptive response to vascular normalization and that these immunosuppressive myeloid cells act in a setting of persistent hypoxia to maintain adaptive immune resistance.
MeSH term(s)	Humans ; Pancreatic Neoplasms/pathology ; Myeloid-Derived Suppressor Cells ; Adenocarcinoma/pathology ; Vascular Endothelial Growth Factor A/metabolism ; Hypoxia/metabolism
Chemical Substances	TH 302 ; Vascular Endothelial Growth Factor A
Language	English
Publishing date	2024-01-09
Publishing country	United States
Document type	Journal Article
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.169150
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Article ; Online: Identification of Nonfunctional Alternatively Spliced Isoforms of STING in Human Acute Myeloid Leukemia.

Boda, Akash R / Liu, Arthur J / Castro-Pando, Susana / Whitfield, Benjamin T / Molldrem, Jeffrey J / Al-Atrash, Gheath / Di Francesco, Maria Emilia / Jones, Philip / Ager, Casey R / Curran, Michael A

Cancer research communications

2024 Volume 4, Issue 3, Page(s) 911–918

Abstract: Lack of robust activation of Stimulator of Interferon Genes (STING) pathway and subsequent induction of type I IFN responses is considered a barrier to antitumor immunity in acute myeloid leukemia (AML). Using common human AML cell lines as in vitro ... ...

Abstract	Lack of robust activation of Stimulator of Interferon Genes (STING) pathway and subsequent induction of type I IFN responses is considered a barrier to antitumor immunity in acute myeloid leukemia (AML). Using common human AML cell lines as in vitro tools to evaluate the efficacy of novel STING agonists, we found most AML lines to be poor producers of IFNs upon exposure to extremely potent agonists, suggesting cell-intrinsic suppression of STING signaling may occur. We observed unexpected patterns of response that did not correlate with levels of STING pathway components or of known enzymes associated with resistance. To identify a genetic basis for these observations, we cloned and sequenced STING from the cDNA of human AML cell lines and found both frequent mutations and deviations from normal RNA splicing. We identified two novel spliced isoforms of STING in these lines and validated their expression in primary human AML samples. When transduced into reporter cells, these novel STING isoforms exhibited complete insensitivity to agonist stimulation. These observations identify alternative splicing as a mechanism of STING pathway suppression and suggest that most AML silences the STING pathway through direct modification rather than through engagement of external inhibitory factors. Significance: We find that AML acquires resistance to innate immune activation via the STING pathway through aberrant splicing of the STING transcript including two novel forms described herein that act as dominant negatives. These data broaden understanding of how cancers evolve STING resistance, and suggest that the AML tumor microenvironment, not the cancer cell, should be the target of therapeutic interventions to activate STING.
MeSH term(s)	Humans ; Protein Isoforms/genetics ; Leukemia, Myeloid, Acute/genetics ; Alternative Splicing/genetics ; Interferon Type I/genetics ; Cell Line ; Tumor Microenvironment
Chemical Substances	Protein Isoforms ; Interferon Type I
Language	English
Publishing date	2024-03-13
Publishing country	United States
Document type	Journal Article
ISSN	2767-9764
ISSN (online)	2767-9764
DOI	10.1158/2767-9764.CRC-24-0095
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Article ; Online: High potency STING agonists engage unique myeloid pathways to reverse pancreatic cancer immune privilege.

Ager, Casey R / Boda, Akash / Rajapakshe, Kimal / Lea, Spencer Thomas / Di Francesco, Maria Emilia / Jayaprakash, Priyamvada / Slay, Ravaen B / Morrow, Brittany / Prasad, Rishika / Dean, Meghan A / Duffy, Colm R / Coarfa, Cristian / Jones, Philip / Curran, Michael A

Journal for immunotherapy of cancer

2021 Volume 9, Issue 8

Abstract: Background: Intratumoral injection of cyclic dinucleotide (CDN) agonists of the stimulator of interferon genes (STING) pathway engages innate immune activation and priming of adaptive immune effectors to foster local and distal tumor clearance. Despite ... ...

Abstract	Background: Intratumoral injection of cyclic dinucleotide (CDN) agonists of the stimulator of interferon genes (STING) pathway engages innate immune activation and priming of adaptive immune effectors to foster local and distal tumor clearance. Despite proven therapeutic efficacy in preclinical models, a thorough understanding of how CDNs reprogram suppressive myeloid stroma in mouse and man is lacking. Methods: Here, we perform deep transcript-level and protein-level profiling of myeloid-derived suppressor cells and M2 macrophages following stimulation with CDNs of ascending potency. Additionally, we leverage orthotopic Results: Highly potent synthetic STING agonists repolarize suppressive myeloid populations of human and murine origin in part through inhibition of Myc signaling, metabolic modulation, and antagonism of cell cycle. Surprisingly, high-potency synthetic agonists engage qualitatively unique pathways as compared with natural CDNs. Consistent with our mechanistic observations, we find that intratumoral injection of the highest activity STING agonist, IACS-8803, into orthotopic pancreatic adenocarcinoma lesions unmasks sensitivity to checkpoint blockade immunotherapy. Dimensionality reduction analyses of high parameter flow cytometry data reveals substantial contributions of both myeloid repolarization and T cell activation underlying the in vivo therapeutic benefit of this approach. Conclusions: This study defines the molecular basis of STING-mediated myeloid reprogramming, revealing previously unappreciated and qualitatively unique pathways engaged by CDNs of ascending potency during functional repolarization. Furthermore, we demonstrate the potential for high potency CDNs to overcome immunotherapy resistance in an orthotopic, multifocal model of PDAC.
MeSH term(s)	Animals ; Humans ; Immunotherapy/methods ; Male ; Membrane Proteins/pharmacology ; Membrane Proteins/therapeutic use ; Mice ; Myeloid-Derived Suppressor Cells/metabolism ; Pancreatic Neoplasms/drug therapy
Chemical Substances	Membrane Proteins ; Sting1 protein, mouse
Language	English
Publishing date	2021-07-31
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-2021-003246
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Article ; Online: RaftProt: mammalian lipid raft proteome database.

Shah, Anup / Chen, David / Boda, Akash R / Foster, Leonard J / Davis, Melissa J / Hill, Michelle M

Nucleic acids research

2015 Volume 43, Issue Database issue, Page(s) D335–8

Abstract: RaftProt (http://lipid-raft-database.di.uq.edu.au/) is a database of mammalian lipid raft-associated proteins as reported in high-throughput mass spectrometry studies. Lipid rafts are specialized membrane microdomains enriched in cholesterol and ... ...

Abstract	RaftProt (http://lipid-raft-database.di.uq.edu.au/) is a database of mammalian lipid raft-associated proteins as reported in high-throughput mass spectrometry studies. Lipid rafts are specialized membrane microdomains enriched in cholesterol and sphingolipids thought to act as dynamic signalling and sorting platforms. Given their fundamental roles in cellular regulation, there is a plethora of information on the size, composition and regulation of these membrane microdomains, including a large number of proteomics studies. To facilitate the mining and analysis of published lipid raft proteomics studies, we have developed a searchable database RaftProt. In addition to browsing the studies, performing basic queries by protein and gene names, searching experiments by cell, tissue and organisms; we have implemented several advanced features to facilitate data mining. To address the issue of potential bias due to biochemical preparation procedures used, we have captured the lipid raft preparation methods and implemented advanced search option for methodology and sample treatment conditions, such as cholesterol depletion. Furthermore, we have identified a list of high confidence proteins, and enabled searching only from this list of likely bona fide lipid raft proteins. Given the apparent biological importance of lipid raft and their associated proteins, this database would constitute a key resource for the scientific community.
MeSH term(s)	Animals ; Databases, Protein ; Humans ; Membrane Microdomains/chemistry ; Membrane Proteins/analysis ; Proteome/analysis
Chemical Substances	Membrane Proteins ; Proteome
Language	English
Publishing date	2015-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gku1131
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Article ; Online: ATR-mediated CD47 and PD-L1 up-regulation restricts radiotherapy-induced immune priming and abscopal responses in colorectal cancer.

Hsieh, Rodney Cheng-En / Krishnan, Sunil / Wu, Ren-Chin / Boda, Akash R / Liu, Arthur / Winkler, Michelle / Hsu, Wen-Hao / Lin, Steven Hsesheng / Hung, Mien-Chie / Chan, Li-Chuan / Bhanu, Krithikaa Rajkumar / Srinivasamani, Anupallavi / De Azevedo, Ricardo Alexandre / Chou, Yung-Chih / DePinho, Ronald A / Gubin, Matthew / Vilar, Eduardo / Chen, Chao Hsien / Slay, Ravaen /

Jayaprakash, Priyamvada / Hegde, Shweta Mahendra / Hartley, Genevieve / Lea, Spencer T / Prasad, Rishika / Morrow, Brittany / Couillault, Coline Agnes / Steiner, Madeline / Wang, Chun-Chieh / Venkatesulu, Bhanu Prasad / Taniguchi, Cullen / Kim, Yon Son Betty / Chen, Junjie / Rudqvist, Nils-Petter / Curran, Michael A

Science immunology

2022 Volume 7, Issue 72, Page(s) eabl9330

Abstract: Radiotherapy (RT) of colorectal cancer (CRC) can prime adaptive immunity against tumor-associated antigen (TAA)-expressing CRC cells systemically. However, abscopal tumor remissions are extremely rare, and the postirradiation immune escape mechanisms in ... ...

Abstract	Radiotherapy (RT) of colorectal cancer (CRC) can prime adaptive immunity against tumor-associated antigen (TAA)-expressing CRC cells systemically. However, abscopal tumor remissions are extremely rare, and the postirradiation immune escape mechanisms in CRC remain elusive. Here, we found that irradiated CRC cells used ATR-mediated DNA repair signaling pathway to up-regulate both CD47 and PD-L1, which through engagement of SIRPα and PD-1, respectively, prevented phagocytosis by antigen-presenting cells and thereby limited TAA cross-presentation and innate immune activation. This postirradiation CD47 and PD-L1 up-regulation was observed across various human solid tumor cells. Concordantly, rectal cancer patients with poor responses to neoadjuvant RT exhibited significantly elevated postirradiation CD47 levels. The combination of RT, anti-SIRPα, and anti-PD-1 reversed adaptive immune resistance and drove efficient TAA cross-presentation, resulting in robust TAA-specific CD8 T cell priming, functional activation of T effectors, and increased T cell clonality and clonal diversity. We observed significantly higher complete response rates to RT/anti-SIRPα/anti-PD-1 in both irradiated and abscopal tumors and prolonged survival in three distinct murine CRC models, including a cecal orthotopic model. The efficacy of triple combination therapy was STING dependent as knockout animals lost most benefit of adding anti-SIRPα and anti-PD-1 to RT. Despite activation across the myeloid stroma, the enhanced dendritic cell function accounts for most improvements in CD8 T cell priming. These data suggest ATR-mediated CD47 and PD-L1 up-regulation as a key mechanism restraining radiation-induced immune priming. RT combined with SIRPα and PD-1 blockade promotes robust antitumor immune priming, leading to systemic tumor regressions.
MeSH term(s)	Animals ; Antigens, Neoplasm ; Ataxia Telangiectasia Mutated Proteins/metabolism ; B7-H1 Antigen ; CD47 Antigen/metabolism ; Colorectal Neoplasms/radiotherapy ; Humans ; Mice ; Programmed Cell Death 1 Receptor ; Up-Regulation
Chemical Substances	Antigens, Neoplasm ; B7-H1 Antigen ; CD47 Antigen ; CD47 protein, human ; Programmed Cell Death 1 Receptor ; ATR protein, human (EC 2.7.11.1) ; Ataxia Telangiectasia Mutated Proteins (EC 2.7.11.1)
Language	English
Publishing date	2022-06-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ISSN	2470-9468
ISSN (online)	2470-9468
DOI	10.1126/sciimmunol.abl9330
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Article: Supporting evidence-based analysis for modified risk tobacco products through a toxicology data-sharing infrastructure.

Boué, Stéphanie / Exner, Thomas / Ghosh, Samik / Belcastro, Vincenzo / Dokler, Joh / Page, David / Boda, Akash / Bonjour, Filipe / Hardy, Barry / Vanscheeuwijck, Patrick / Hoeng, Julia / Peitsch, Manuel

F1000Research

2017 Volume 6, Page(s) 12

Abstract: The US FDA defines modified risk tobacco products (MRTPs) as products that aim to reduce harm or the risk of tobacco-related disease associated with commercially marketed tobacco products. Establishing a product's potential as an MRTP requires ... ...

Abstract	The US FDA defines modified risk tobacco products (MRTPs) as products that aim to reduce harm or the risk of tobacco-related disease associated with commercially marketed tobacco products. Establishing a product's potential as an MRTP requires scientific substantiation including toxicity studies and measures of disease risk relative to those of cigarette smoking. Best practices encourage verification of the data from such studies through sharing and open standards. Building on the experience gained from the OpenTox project, a proof-of-concept database and website ( INTERVALS) has been developed to share results from both
Language	English
Publishing date	2017
Publishing country	England
Document type	Journal Article
ZDB-ID	2699932-8
ISSN	2046-1402
ISSN	2046-1402
DOI	10.12688/f1000research.10493.2
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Article ; Online: The sbv IMPROVER Systems Toxicology Computational Challenge: Identification of Human and Species-Independent Blood Response Markers as Predictors of Smoking Exposure and Cessation Status

Belcastro, Vincenzo / Poussin, Carine / Xiang, Yang / Giordano, Maurizio / Tripathi, Kumar Parijat / Boda, Akash / Boué, Stéphanie / Guarracino, Mario / Martin, Florian / Peitsch, Manuel C. / Hoeng, Julia / Romero, Roberto / Tarca, Adi L. / Duan, Zhongqu / Yang, Hao / Gong, Xiaofeng / Wang, Peixuan / Zhang, Chenfang / Yeung, Man Shun /

Sarac, Omer Sinan / Bilgen, Ismail / Balci, Ali Tugrul / Rahul Kumar / Dhanda, Sandeep Kumar

Computational Toxicology. 2017,

2017

Abstract: Cigarette smoking entails chronic exposure to a mixture of harmful chemicals that trigger molecular changes over time, and is known to increase the risk of developing diseases. Risk assessment in the context of 21st century toxicology relies on the ... ...

Abstract	Cigarette smoking entails chronic exposure to a mixture of harmful chemicals that trigger molecular changes over time, and is known to increase the risk of developing diseases. Risk assessment in the context of 21st century toxicology relies on the elucidation of mechanisms of toxicity and the identification of exposure response markers, usually from high-throughput data, using advanced computational methodologies.The sbv IMPROVER Systems Toxicology computational challenge (Fall 2015-Spring 2016) aimed to evaluate whether robust and sparse (≤40 genes) human (sub-challenge 1, SC1) and species-independent (sub-challenge 2, SC2) exposure response markers (so called gene signatures) could be extracted from human and mouse blood transcriptomics data of current (S), former (FS) and never (NS) smoke-exposed subjects as predictors of smoking and cessation status. Best-performing computational methods were identified by scoring anonymized participants' predictions.Worldwide participation resulted in 12 (SC1) and six (SC2) final submissions qualified for scoring. The results showed that blood gene expression data were informative to predict smoking exposure (i.e. discriminating smoker versus never or former smokers) status in human and across species with a high level of accuracy. By contrast, the prediction of cessation status (i.e. distinguishing FS from NS) remained challenging, as reflected by lower classification performances. Participants successfully developed inductive predictive models and extracted human and species-independent gene signatures, including genes with high consensus across teams. Post-challenge analyses highlighted "feature selection" as a key step in the process of building a classifier and confirmed the importance of testing a gene signature in independent cohorts to ensure the generalized applicability of a predictive model at a population-based level.In conclusion, the Systems Toxicology challenge demonstrated the feasibility of extracting a consistent blood-based smoke exposure response gene signature and further stressed the importance of independent and unbiased data and method evaluations to provide confidence in systems toxicology-based scientific conclusions.
Keywords	Systems toxicology ; Computational challenge ; Gene signature ; Smoking biomarker ; Blood biomarkers
Language	English
Publishing place	Elsevier B.V.
Document type	Article ; Online
Note	Pre-press version
ISSN	2468-1113
DOI	10.1016/j.comtox.2017.07.004
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Identification of a novel PPARβ/δ/miR-21-3p axis in UV-induced skin inflammation.

Degueurce, Gwendoline / D'Errico, Ilenia / Pich, Christine / Ibberson, Mark / Schütz, Frédéric / Montagner, Alexandra / Sgandurra, Marie / Mury, Lionel / Jafari, Paris / Boda, Akash / Meunier, Julien / Rezzonico, Roger / Brembilla, Nicolò Costantino / Hohl, Daniel / Kolios, Antonios / Hofbauer, Günther / Xenarios, Ioannis / Michalik, Liliane

EMBO molecular medicine

2016 Volume 8, Issue 8, Page(s) 919–936

Abstract: Although excessive exposure to UV is widely recognized as a major factor leading to skin perturbations and cancer, the complex mechanisms underlying inflammatory skin disorders resulting from UV exposure remain incompletely characterized. The nuclear ... ...

Abstract	Although excessive exposure to UV is widely recognized as a major factor leading to skin perturbations and cancer, the complex mechanisms underlying inflammatory skin disorders resulting from UV exposure remain incompletely characterized. The nuclear hormone receptor PPARβ/δ is known to control mouse cutaneous repair and UV-induced skin cancer development. Here, we describe a novel PPARβ/δ-dependent molecular cascade involving TGFβ1 and miR-21-3p, which is activated in the epidermis in response to UV exposure. We establish that the passenger miRNA miR-21-3p, that we identify as a novel UV-induced miRNA in the epidermis, plays a pro-inflammatory function in keratinocytes and that its high level of expression in human skin is associated with psoriasis and squamous cell carcinomas. Finally, we provide evidence that inhibition of miR-21-3p reduces UV-induced cutaneous inflammation in ex vivo human skin biopsies, thereby underlining the clinical relevance of miRNA-based topical therapies for cutaneous disorders.
MeSH term(s)	Animals ; Humans ; Mice ; MicroRNAs/metabolism ; PPAR delta/metabolism ; PPAR-beta/metabolism ; Radiodermatitis/pathology ; Signal Transduction ; Skin/radiation effects ; Ultraviolet Rays
Chemical Substances	MIRN21 microRNA, human ; MicroRNAs ; PPAR delta ; PPAR-beta
Language	English
Publishing date	2016-08-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2467145-9
ISSN	1757-4684 ; 1757-4676
ISSN (online)	1757-4684
ISSN	1757-4676
DOI	10.15252/emmm.201505384
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Article: The sbv IMPROVER Systems Toxicology Computational Challenge: Identification of Human and Species-Independent Blood Response Markers as Predictors of Smoking Exposure and Cessation Status.

Belcastro, Vincenzo / Poussin, Carine / Xiang, Yang / Giordano, Maurizio / Tripathi, Kumar Parijat / Boda, Akash / Boué, Stéphanie / Guarracino, Mario / Martin, Florian / Peitsch, Manuel C / Hoeng, Julia / Romero, Roberto / Tarca, Adi L / Duan, Zhongqu / Yang, Hao / Gong, Xiaofeng / Wang, Peixuan / Zhang, Chenfang / Yang, Wenxin /

Sarac, Omer Sinan / Bilgen, Ismail / Balci, Ali Tugrul / Kumar, Rahul / Dhanda, Sandeep Kumar

Computational toxicology (Amsterdam, Netherlands)

2017 Volume 5, Page(s) 38–51

Abstract	Cigarette smoking entails chronic exposure to a mixture of harmful chemicals that trigger molecular changes over time, and is known to increase the risk of developing diseases. Risk assessment in the context of 21
Language	English
Publishing date	2017-07-14
Publishing country	Netherlands
Document type	Journal Article
ISSN	2468-1113
ISSN	2468-1113
DOI	10.1016/j.comtox.2017.07.004
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