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4. CES2 sustains HNF4α expression to promote pancreatic adenocarcinoma progression through an epoxide hydrolase-dependent regulatory loop

Author

Chen, Yihui, Capello, Michela, Perez, Mayrim V Rios, Vykoukal, Jody V, Roife, David, Kang, Ya'an, Prakash, Laura R, Katayama, Hiroyuki, Irajizad, Ehsan, Fleury, Alia, Ferri-Borgogno, Sammy, Baluya, Dodge L, Dennison, Jennifer B, Do, Kim-Anh, Fiehn, Oliver, Maitra, Anirban, Wang, Huamin, Chiao, Paul J, Katz, Matthew HG, Fleming, Jason B, Hanash, Samir M, and Fahrmann, Johannes F

Subjects
Biochemistry and Cell Biology, Biological Sciences, Pancreatic Cancer, Cancer, Digestive Diseases, Rare Diseases, Biotechnology, Development of treatments and therapeutic interventions, 5.1 Pharmaceuticals, Adenocarcinoma, Animals, Carboxylesterase, Carcinoma, Pancreatic Ductal, Cell Line, Tumor, Epoxide Hydrolases, Humans, Mice, Pancreatic Neoplasms, PDAC, HNF4 alpha, CES2, Classical/progenitor subtype, Phospholipid catabolism, HNF4α, Physiology, Biochemistry and cell biology
Abstract

ObjectiveIntra-tumoral expression of the serine hydrolase carboxylesterase 2 (CES2) contributes to the activation of the pro-drug irinotecan in pancreatic ductal adenocarcinoma (PDAC). Given other potential roles of CES2, we assessed its regulation, downstream effects, and contribution to tumor development in PDAC.MethodsAssociation between the mRNA expression of CES2 in pancreatic tumors and overall survival was assessed using The Cancer Genome Atlas. Cell viability, clonogenic, and anchorage-independent growth assays as well as an orthotopic mouse model of PDAC were used to evaluate the biological relevance of CES2 in pancreatic cancer. CES2-driven metabolic changes were determined by untargeted and targeted metabolomic analyses.ResultsElevated tumoral CES2 mRNA expression was a statistically significant predictor of poor overall survival in PDAC patients. Knockdown of CES2 in PDAC cells reduced cell viability, clonogenic capacity, and anchorage-independent growth in vitro and attenuated tumor growth in an orthotopic mouse model of PDAC. Mechanistically, CES2 was found to promote the catabolism of phospholipids resulting in HNF4α activation through a soluble epoxide hydrolase (sEH)-dependent pathway. Targeting of CES2 via siRNA or small molecule inhibitors attenuated HNF4α protein expression and reduced gene expression of classical/progenitor markers and increased basal-like markers. Targeting of the CES2-sEH-HNF4α axis using small molecule inhibitors of CES2 or sEH reduced cell viability.ConclusionsWe establish a novel regulatory loop between CES2 and HNF4α to sustain the progenitor subtype and promote PDAC progression and highlight the potential utility of CES2 or sEH inhibitors for the treatment of PDAC as part of non-irinotecan-containing regimens.

Published
2022

5. CES2 Expression in Pancreatic Adenocarcinoma Is Predictive of Response to Irinotecan and Is Associated With Type 2 Diabetes.

Author

Capello, Michela, Fahrmann, Johannes, Rios Perez, Mayrim, Vykoukal, Jody, Irajizad, Ehsan, Tripathi, Satyendra, Roife, David, Bantis, Leonidas, Kang, Yaan, Kundnani, Deepali, Xu, Hanwen, Prakash, Laura, Long, James, Katayama, Hiroyuki, Fleury, Alia, Ferri-Borgogno, Sammy, Baluya, Dodge, Dennison, Jennifer, Aguilar-Bonavides, Clemente, Casabar, Julian, Celiktas, Muge, Do, Kim-Anh, Fiehn, Oliver, Maitra, Anirban, Wang, Huamin, Feng, Ziding, Chiao, Paul, Katz, Matthew, Fleming, Jason, and Hanash, Samir

Abstract

PURPOSE: The combination chemotherapy of fluorouracil, leucovorin, irinotecan, and oxaliplatin (FOLFIRINOX) has provided clinically meaningful improvement for pancreatic ductal adenocarcinoma (PDAC). We previously uncovered a role for the serine hydrolase carboxylesterase 2 (CES2) in mediating intratumoral activation of the prodrug irinotecan, a constituent of FOLFIRINOX. We aimed to further test the predictive value of CES2 for response to irinotecan using patient-derived xenograft (PDX) models and to elucidate the determinants of CES2 expression and response to FOLFIRINOX treatment among patients with PDAC. METHODS: PDXs were engrafted subcutaneously into nude mice and treated for 4 weeks with either saline control or irinotecan. CES2 and hepatocyte nuclear factor 4 alpha (HNF4A) expression in PDAC tissues was evaluated by immunohistochemical and Western blot analysis. Kaplan-Meier and Cox regression analyses were applied to assess the association between overall survival and hemoglobin A1C (HbA1C) levels in patients who underwent neoadjuvant FOLFIRINOX treatment. RESULTS: High CES2 activity in PDAC PDXs was associated with increased sensitivity to irinotecan. Integrated gene expression, proteomic analyses, and in vitro genetic experiments revealed that nuclear receptor HNF4A, which is upregulated in diabetes, is the upstream transcriptional regulator of CES2 expression. Elevated CES2 protein expression in PDAC tissues was positively associated with a history of type 2 diabetes (odds ratio, 4.84; P = .02). High HbA1C levels were associated with longer overall survival in patients who received neoadjuvant FOLFIRINOX treatment (P = .04). CONCLUSION: To our knowledge, we provide, for the first time, evidence that CES2 expression is associated with a history of type 2 diabetes in PDAC and that elevated HbA1C, by predicting tumor CES2 expression, may represent a novel marker for stratifying patients most likely to respond to FOLFIRINOX therapy.

Published
2020

9. Molecular, Metabolic, and Subcellular Mapping of the Tumor Immune Microenvironment via 3D Targeted and Non-Targeted Multiplex Multi-Omics Analyses

Author

Ferri-Borgogno, Sammy, primary, Burks, Jared K., additional, Seeley, Erin H., additional, McKee, Trevor D., additional, Stolley, Danielle L., additional, Basi, Akshay V., additional, Gomez, Javier A., additional, Gamal, Basant T., additional, Ayyadhury, Shamini, additional, Lawson, Barrett C., additional, Yates, Melinda S., additional, Birrer, Michael J., additional, Lu, Karen H., additional, and Mok, Samuel C., additional

Published
2024
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10. Data from Spatial Immunoprofiling of Adenoid Cystic Carcinoma Reveals B7-H4 Is a Therapeutic Target for Aggressive Tumors

Author

Sousa, Luana Guimaraes, primary, McGrail, Daniel J., primary, Lazar Neto, Felippe, primary, Li, Kaiyi, primary, Marques-Piubelli, Mario L., primary, Ferri-Borgogno, Sammy, primary, Dai, Hui, primary, Mitani, Yoshitsugu, primary, Spardy Burr, Nicole, primary, Cooper, Zachary A., primary, Kinneer, Krista, primary, Cortez, Maria Angelica, primary, Lin, Shiaw-Yih, primary, Bell, Diana, primary, El Naggar, Adel, primary, Burks, Jared, primary, and Ferrarotto, Renata, primary

Published
2023
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11. Supplementary Figures 1 from Spatial Immunoprofiling of Adenoid Cystic Carcinoma Reveals B7-H4 Is a Therapeutic Target for Aggressive Tumors

Author

Sousa, Luana Guimaraes, primary, McGrail, Daniel J., primary, Lazar Neto, Felippe, primary, Li, Kaiyi, primary, Marques-Piubelli, Mario L., primary, Ferri-Borgogno, Sammy, primary, Dai, Hui, primary, Mitani, Yoshitsugu, primary, Spardy Burr, Nicole, primary, Cooper, Zachary A., primary, Kinneer, Krista, primary, Cortez, Maria Angelica, primary, Lin, Shiaw-Yih, primary, Bell, Diana, primary, El Naggar, Adel, primary, Burks, Jared, primary, and Ferrarotto, Renata, primary

Published
2023
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12. Supplementary Data 1 from Spatial Immunoprofiling of Adenoid Cystic Carcinoma Reveals B7-H4 Is a Therapeutic Target for Aggressive Tumors

Author

Sousa, Luana Guimaraes, primary, McGrail, Daniel J., primary, Lazar Neto, Felippe, primary, Li, Kaiyi, primary, Marques-Piubelli, Mario L., primary, Ferri-Borgogno, Sammy, primary, Dai, Hui, primary, Mitani, Yoshitsugu, primary, Spardy Burr, Nicole, primary, Cooper, Zachary A., primary, Kinneer, Krista, primary, Cortez, Maria Angelica, primary, Lin, Shiaw-Yih, primary, Bell, Diana, primary, El Naggar, Adel, primary, Burks, Jared, primary, and Ferrarotto, Renata, primary

Published
2023
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13. Spatial Immunoprofiling of Adenoid Cystic Carcinoma Reveals B7-H4 Is a Therapeutic Target for Aggressive Tumors

Author

Sousa, Luana Guimaraes, primary, McGrail, Daniel J., additional, Lazar Neto, Felippe, additional, Li, Kaiyi, additional, Marques-Piubelli, Mario L., additional, Ferri-Borgogno, Sammy, additional, Dai, Hui, additional, Mitani, Yoshitsugu, additional, Spardy Burr, Nicole, additional, Cooper, Zachary A., additional, Kinneer, Krista, additional, Cortez, Maria Angelica, additional, Lin, Shiaw-Yih, additional, Bell, Diana, additional, El Naggar, Adel, additional, Burks, Jared, additional, and Ferrarotto, Renata, additional

Published
2023
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21. Table S1 from Comparative Tumor Microenvironment Analysis of Primary and Recurrent Ovarian Granulosa Cell Tumors

Author

Khlebus, Eleonora, primary, Vuttaradhi, Veena K., primary, Welte, Thomas, primary, Khurana, Namrata, primary, Celestino, Joseph, primary, Beird, Hannah C., primary, Gumbs, Curtis, primary, Little, Latasha, primary, Legarreta, Alejandra Flores, primary, Fellman, Bryan M., primary, Nguyen, Tri, primary, Lawson, Barrett, primary, Ferri-Borgogno, Sammy, primary, Mok, Samuel C., primary, Broaddus, Russell R., primary, Gershenson, David M., primary, Futreal, P. Andrew, primary, and Hillman, R. Tyler, primary

Published
2023
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22. Supplementary Figures 1-6 from Comparative Tumor Microenvironment Analysis of Primary and Recurrent Ovarian Granulosa Cell Tumors

Author

Khlebus, Eleonora, primary, Vuttaradhi, Veena K., primary, Welte, Thomas, primary, Khurana, Namrata, primary, Celestino, Joseph, primary, Beird, Hannah C., primary, Gumbs, Curtis, primary, Little, Latasha, primary, Legarreta, Alejandra Flores, primary, Fellman, Bryan M., primary, Nguyen, Tri, primary, Lawson, Barrett, primary, Ferri-Borgogno, Sammy, primary, Mok, Samuel C., primary, Broaddus, Russell R., primary, Gershenson, David M., primary, Futreal, P. Andrew, primary, and Hillman, R. Tyler, primary

Published
2023
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23. Data from Comparative Tumor Microenvironment Analysis of Primary and Recurrent Ovarian Granulosa Cell Tumors

Author

Khlebus, Eleonora, primary, Vuttaradhi, Veena K., primary, Welte, Thomas, primary, Khurana, Namrata, primary, Celestino, Joseph, primary, Beird, Hannah C., primary, Gumbs, Curtis, primary, Little, Latasha, primary, Legarreta, Alejandra Flores, primary, Fellman, Bryan M., primary, Nguyen, Tri, primary, Lawson, Barrett, primary, Ferri-Borgogno, Sammy, primary, Mok, Samuel C., primary, Broaddus, Russell R., primary, Gershenson, David M., primary, Futreal, P. Andrew, primary, and Hillman, R. Tyler, primary

Published
2023
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24. Comparative Tumor Microenvironment Analysis of Primary and Recurrent Ovarian Granulosa Cell Tumors

Author

Khlebus, Eleonora, primary, Vuttaradhi, Veena K., additional, Welte, Thomas, additional, Khurana, Namrata, additional, Celestino, Joseph, additional, Beird, Hannah C., additional, Gumbs, Curtis, additional, Little, Latasha, additional, Legarreta, Alejandra Flores, additional, Fellman, Bryan M., additional, Nguyen, Tri, additional, Lawson, Barrett, additional, Ferri-Borgogno, Sammy, additional, Mok, Samuel C., additional, Broaddus, Russell R., additional, Gershenson, David M., additional, Futreal, P. Andrew, additional, and Hillman, R. Tyler, additional

Published
2023
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26. Exosomes harbor B cell targets in pancreatic adenocarcinoma and exert decoy function against complement-mediated cytotoxicity

Author

Capello, Michela, Vykoukal, Jody V., Katayama, Hiroyuki, Bantis, Leonidas E., Wang, Hong, Kundnani, Deepali L., Aguilar-Bonavides, Clemente, Aguilar, Mitzi, Tripathi, Satyendra C., Dhillon, Dilsher S., Momin, Amin A., Peters, Haley, Katz, Matthew H., Alvarez, Hector, Bernard, Vincent, Ferri-Borgogno, Sammy, Brand, Randall, Adler, Douglas G., Firpo, Matthew A., Mulvihill, Sean J., Molldrem, Jeffrey J., Feng, Ziding, Taguchi, Ayumu, Maitra, Anirban, and Hanash, Samir M.

Published
2019
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29. Abstract 1248: Predictors of innate resistance to pembrolizumab in patients with microsatellite instability-high endometrial cancer

Author

How, Jeffrey A., primary, Dang, Minghao, additional, Ferri-Borgogno, Sammy, additional, Euscher, Elizabeth, additional, Yates, Melinda S., additional, Peng, Weiyi, additional, Patel, Shrina D., additional, Burks, Jared J., additional, Vletic, Ivo, additional, Gomez, Javier, additional, Lu, Karen, additional, Mok, Samuel C., additional, Wang, Linghua, additional, and Jazaeri, Amir A., additional

Published
2022
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32. Single-cell immune mapping of adenoid cystic carcinoma (ACC) reveals potential therapeutic targets for the aggressive solid subtype.

Author

Guimaraes de Sousa, Luana, primary, Lazar Neto, Felippe, additional, McGrail, Daniel James, additional, Li, Kaiyi, additional, Marques-Piubelli, Mario L., additional, Ferri Borgogno, Sammy, additional, Dai, Hui, additional, Mitani, Yoshitsugu, additional, Lin, Shiaw-Yih, additional, El-Naggar, Adel K., additional, Bell, Diana, additional, Burks, Jared, additional, and Ferrarotto, Renata, additional

Published
2022
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36. Spontaneous tumor regression following COVID-19 vaccination

Author

Sousa, Luana Guimaraes de, primary, McGrail, Daniel J, additional, Li, Kaiyi, additional, Marques-Piubelli, Mario L, additional, Gonzalez, Cipriano, additional, Dai, Hui, additional, Ferri-Borgogno, Sammy, additional, Godoy, Myrna, additional, Burks, Jared, additional, Lin, Shiaw-Yih, additional, Bell, Diana, additional, and Ferrarotto, Renata, additional

Published
2022
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37. CES2 sustains HNF4α expression to promote pancreatic adenocarcinoma progression through an epoxide hydrolase-dependent regulatory loop

Author

Chen, Yihui, primary, Capello, Michela, additional, Rios Perez, Mayrim V., additional, Vykoukal, Jody V., additional, Roife, David, additional, Kang, Ya'an, additional, Prakash, Laura R., additional, Katayama, Hiroyuki, additional, Irajizad, Ehsan, additional, Fleury, Alia, additional, Ferri-Borgogno, Sammy, additional, Baluya, Dodge L., additional, Dennison, Jennifer B., additional, Do, Kim-Anh, additional, Fiehn, Oliver, additional, Maitra, Anirban, additional, Wang, Huamin, additional, Chiao, Paul J., additional, Katz, Matthew H.G., additional, Fleming, Jason B., additional, Hanash, Samir M., additional, and Fahrmann, Johannes F., additional

Published
2022
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39. Ryanodine Receptor 1-mediated Ca2+ signaling and mitochondrial reprogramming modulate uterine serous cancer malignant phenotypes

Author

Zhang, Li, primary, Huang, Chunxian, additional, Yeung, Tsz-Lun, additional, Ferri-Borgogno, Sammy, additional, AuYeung, Chilam, additional, Lawson, Barrett C., additional, Kwan, Suet-Ying, additional, Thomas, Vienna, additional, Lu, Karen H., additional, Yip, Kay-Pong, additional, Sham, James S.K., additional, and Mok, Samuel, additional

Published
2021
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45. Ryanodine receptor 1-mediated Ca2+ signaling and mitochondrial reprogramming modulate uterine serous cancer malignant phenotypes.

Author

Zhang, Li, Au-Yeung, Chi-Lam, Huang, Chunxian, Yeung, Tsz-Lun, Ferri-Borgogno, Sammy, Lawson, Barrett C., Kwan, Suet-Ying, Yin, Zheng, Wong, Stephen T., Thomas, Vienna, Lu, Karen H., Yip, Kay-Pong, Sham, James S. K., and Mok, Samuel C.

Subjects
RYANODINE receptors, UTERINE cancer, PROTEIN microarrays, OVERALL survival, PHENOTYPES, REPERFUSION injury
Abstract

Background: Uterine serous cancer (USC) is the most common non-endometrioid subtype of uterine cancer, and is also the most aggressive. Most patients will die of progressively chemotherapy-resistant disease, and the development of new therapies that can target USC remains a major unmet clinical need. This study sought to determine the molecular mechanism by which a novel unfavorable prognostic biomarker ryanodine receptor 1 (RYR1) identified in advanced USC confers their malignant phenotypes, and demonstrated the efficacy of targeting RYR1 by repositioned FDA-approved compounds in USC treatment. Methods: TCGA USC dataset was analyzed to identify top genes that are associated with patient survival or disease stage, and can be targeted by FDA-approved compounds. The top gene RYR1 was selected and the functional role of RYR1 in USC progression was determined by silencing and over-expressing RYR1 in USC cells in vitro and in vivo. The molecular mechanism and signaling networks associated with the functional role of RYR1 in USC progression were determined by reverse phase protein arrays (RPPA), Western blot, and transcriptomic profiling analyses. The efficacy of the repositioned compound dantrolene on USC progression was determined using both in vitro and in vivo models. Results: High expression level of RYR1 in the tumors is associated with advanced stage of the disease. Inhibition of RYR1 suppressed proliferation, migration and enhanced apoptosis through Ca2+-dependent activation of AKT/CREB/PGC-1α and AKT/HK1/2 signaling pathways, which modulate mitochondrial bioenergetics properties, including oxidative phosphorylation, ATP production, mitochondrial membrane potential, ROS production and TCA metabolites, and glycolytic activities in USC cells. Repositioned compound dantrolene suppressed USC progression and survival in mouse models. Conclusions: These findings provided insight into the mechanism by which RYR1 modulates the malignant phenotypes of USC and could aid in the development of dantrolene as a repurposed therapeutic agent for the treatment of USC to improve patient survival. [ABSTRACT FROM AUTHOR]

Published
2022
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46. SIO: A Spatioimageomics Pipeline to Identify Prognostic Biomarkers Associated with the Ovarian Tumor Microenvironment

Author

Zhu, Ying, primary, Ferri-Borgogno, Sammy, additional, Sheng, Jianting, additional, Yeung, Tsz-Lun, additional, Burks, Jared K., additional, Cappello, Paola, additional, Jazaeri, Amir A., additional, Kim, Jae-Hoon, additional, Han, Gwan Hee, additional, Birrer, Michael J., additional, Mok, Samuel C., additional, and Wong, Stephen T. C., additional

Published
2021
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48. Correction: Hu, W., et al. Targeting Dopamine Receptor D2 by Imipridone Suppresses Uterine Serous Cancer Malignant Phenotype. Cancers 2020, 12, 2436

Author

Hu, Wen, primary, Zhang, Li, additional, Ferri-Borgogno, Sammy, additional, Kwan, Suet-Ying, additional, Lewis, Kelsey E., additional, Cun, Han T., additional, Yeung, Tsz-Lun, additional, Soliman, Pamela T., additional, Tarapore, Rohinton S., additional, Allen, Joshua E., additional, Guan, Xinyuan, additional, Lu, Karen H., additional, Mok, Samuel C., additional, and Au-Yeung, Chi-Lam, additional

Published
2021
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49. Paradoxical Role of AT-rich Interactive Domain 1A in Restraining Pancreatic Carcinogenesis

Author

Ferri-Borgogno, Sammy, Barui, Sugata, McGee, Amberly M., Griffiths, Tamara, Singh, Pankaj K., Piett, Cortt G., Ghosh, Bidyut, Bhattacharyya, Sanchari, Singhi, Aatur, Pradhan, Kith, Verma, Amit, Nagel, Zac, Maitra, Anirban, Gupta, Sonal, Ferri-Borgogno, Sammy, Barui, Sugata, McGee, Amberly M., Griffiths, Tamara, Singh, Pankaj K., Piett, Cortt G., Ghosh, Bidyut, Bhattacharyya, Sanchari, Singhi, Aatur, Pradhan, Kith, Verma, Amit, Nagel, Zac, Maitra, Anirban, and Gupta, Sonal

Abstract

Background & Aims: ARID1A is postulated to be a tumor suppressor gene owing to loss-of-function mutations in human pancreatic ductal adenocarcinomas (PDAC). However, its role in pancreatic pathogenesis is not clear despite recent studies using genetically engineered mouse (GEM) models. We aimed at further understanding of its direct functional role in PDAC, using a combination of GEM model and PDAC cell lines. Methods: Pancreas-specific mutant Arid1a-driven GEM model (Ptf1a-Cre; KrasG12D; Arid1af/f or “KAC”) was generated by crossing Ptf1a-Cre; KrasG12D (“KC”) mice with Arid1af/f mice and characterized histologically with timed necropsies. Arid1a was also deleted using CRISPR-Cas9 system in established human and murine PDAC cell lines to study the immediate effects of Arid1a loss in isogenic models. Cell lines with or without Arid1a expression were developed from respective autochthonous PDAC GEM models, compared functionally using various culture assays, and subjected to RNA-sequencing for comparative gene expression analysis. DNA damage repair was analyzed in cultured cells using immunofluorescence and COMET assay. Results: Retention of Arid1a is critical for early progression of mutant Kras-driven pre-malignant lesions into PDAC, as evident by lower Ki-67 and higher apoptosis staining in “KAC” as compared to “KC” mice. Enforced deletion of Arid1a in established PDAC cell lines caused suppression of cellular growth and migration, accompanied by compromised DNA damage repair. Despite early development of relatively indolent cystic precursor lesions called intraductal papillary mucinous neoplasms (IPMNs), a subset of “KAC” mice developed aggressive PDAC in later ages. PDAC cells obtained from older autochthonous “KAC” mice revealed various compensatory (“escaper”) mechanisms to overcome the growth suppressive effects of Arid1a loss. Conclusions: Arid1a is an essential survival gene whose loss impairs cellular growth, and thus, its expression is critical during early

Published
2020

50. CES2 Expression in Pancreatic Adenocarcinoma Is Predictive of Response to Irinotecan and Is Associated With Type 2 Diabetes

Author

Capello, Michela, primary, Fahrmann, Johannes F., additional, Rios Perez, Mayrim V., additional, Vykoukal, Jody V., additional, Irajizad, Ehsan, additional, Tripathi, Satyendra C., additional, Roife, David, additional, Bantis, Leonidas E., additional, Kang, Ya’an, additional, Kundnani, Deepali L., additional, Xu, Hanwen, additional, Prakash, Laura R., additional, Long, James P., additional, Katayama, Hiroyuki, additional, Fleury, Alia, additional, Ferri-Borgogno, Sammy, additional, Baluya, Dodge L., additional, Dennison, Jennifer B., additional, Aguilar-Bonavides, Clemente, additional, Casabar, Julian P., additional, Celiktas, Muge, additional, Do, Kim-Anh, additional, Fiehn, Oliver, additional, Maitra, Anirban, additional, Wang, Huamin, additional, Feng, Ziding, additional, Chiao, Paul J., additional, Katz, Matthew H., additional, Fleming, Jason B., additional, and Hanash, Samir M., additional

Published
2020
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