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Nuclear protein 1 promotes pancreatic cancer development and protects cells from stress by inhibiting apoptosis

Tewfik Hamidi, … , Roland Michael Schmid, Juan Lucio Iovanna

Tewfik Hamidi, … , Roland Michael Schmid, Juan Lucio Iovanna

Published May 8, 2012
Citation Information: J Clin Invest. 2012;122(6):2092-2103. https://doi.org/10.1172/JCI60144.

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c-Rel drives pancreatic cancer metastasis through Fibronectin-Integrin signaling-induced isolation stress resistance and EMT activation Bakırdöğen D, Görgülü K, Xin J, Alcalá S, Ruiz-Cañas L, Frank K, Wu N, Diakopoulos KN, Dai C, Öztürk H, Demircioğlu D, Peschke K, Ranjan R, Fusco F, Martinez-Useros J, Fernandez-Aceñero MJ, Chhabra NF, López-Gil JC, Ai J, Ruess DA, Kaya-Aksoy E, Steiger K, Schmidt F, Kohlmann L, Berninger A, Schmid RM, Reichert M, Adli M, Lesina M, Sainz B Jr, Algül H	bioRxiv	2025
IER3: exploring its dual function as an oncogene and tumor suppressor Kanduri M, Subhash S, Putino R, Mahale S, Kanduri C	Cancer Gene Therapy	2025
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NEMO/NF-κB signaling functions as a double-edged sword in PanIN formation versus progression to pancreatic cancer. Tsesmelis M, Büttner UFG, Gerstenlauer M, Manfras U, Tsesmelis K, Du Z, Sperb N, Weissinger SE, Möller P, Barth TFE, Maier HJ, Chan LK, Wirth T	Molecular Cancer	2024
Exploring Hypertrophic Cardiomyopathy Biomarkers through Integrated Bioinformatics Analysis: Uncovering Novel Diagnostic Candidates Li G, Lin D, Fan X, Peng B	Cardiology Research and Practice	2024
Correlation study of NF-κB, IER3, and Recurrence of Ovarian Endometrioid Cysts. Fan X, Yang N, Huang G, Dong Y, Zhu P	Reproductive sciences (Thousand Oaks, Calif.)	2024
Fuzzy Drug Targets: Disordered Proteins in the Drug-Discovery Realm Saurabh S, Nadendla K, Purohit SS, Sivakumar PM, Cetinel S	ACS Omega	2023
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Microgravity triggers ferroptosis and accelerates senescence in the MG-63 cell model of osteoblastic cells. Garbacki N, Willems J, Neutelings T, Lambert C, Deroanne C, Adrian A, Franz M, Maurer M, De Gieter P, Nusgens B, Colige A	npj Microgravity	2023
The impact of SBF2 on taxane-induced peripheral neuropathy G Cunningham, F Shen, , E L., L Gardner, S Philips, G Jiang, C Bales, Z Tan, Y Liu, J Wan, J Fehrenbacher, B Schneider, H Orr	PLoS genetics	2022
Histone methyltransferase Dot1L inhibits pancreatic cancer cell apoptosis by promoting NUPR1 expression Shan L, Hao C, Jun Z, Qinghe C		2022
NUPR1 protects against hyperPARylation-dependent cell death Santofimia-Castaño P, Huang C, Liu X, Xia Y, Audebert S, Camoin L, Peng L, Lomberk G, Urrutia R, Soubeyran P, Neira JL, Iovanna J	Communications biology	2022
Effects of TP53 Mutations and miRs on Immune Responses in the Tumor Microenvironment Important in Pancreatic Cancer Progression McCubrey JA, Yang LV, Abrams SL, Steelman LS, Follo MY, Cocco L, Ratti S, Martelli AM, Augello G, Cervello M	Cells	2022
Construction of prognostic signature of patients with oral squamous cell carcinoma based on pyroptosis-related long non-coding RNAs Xin Y, Zhang J, Jiang Q, Qiu J	Frontiers in Surgery	2022
NUPR1 is a critical repressor of ferroptosis J Liu, X Song, F Kuang, Q Zhang, Y Xie, R Kang, G Kroemer, D Tang	Nature Communications	2021
Intrinsically Disordered Proteins as Regulators of Transient Biological Processes and as Untapped Drug Targets Y Hosoya, J Ohkanda	Molecules (Basel, Switzerland)	2021
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Short-term transcriptomic response to plasma membrane injury SC Häger, C Dias, SL Sønder, AV Olsen, I da Piedade, AS Heitmann, E Papaleo, J Nylandsted	Scientific Reports	2021
NUPR1 inhibitor ZZW-115 induces ferroptosis in a mitochondria-dependent manner C Huang, P Santofimia-Castaño, , Y Xia, L Peng, C Gotorbe, JL Neira, D Tang, J Pouyssegur, J Iovanna	Cell Death Discovery	2021
CHK1 protects oncogenic KRAS-expressing cells from DNA damage and is a target for pancreatic cancer treatment JE Klomp, YS Lee, CM Goodwin, B Papke, JA Klomp, AM Waters, CA Stalnecker, JM DeLiberty, K Drizyte-Miller, R Yang, JN Diehl, HH Yin, M Pierobon, E Baldelli, MB Ryan, S Li, J Peterson, AR Smith, JT Neal, AK McCormick, CJ Kuo, CM Counter, EF Petricoin, AD Cox, KL Bryant, CJ Der	Cell Reports	2021
ZZW-115-dependent inhibition of NUPR1 nuclear translocation sensitizes cancer cells to genotoxic agents Wenjun Lan, Patricia Santofimia-Castaño, Mirna Swayden, Yi Xia, Zhengwei Zhou, Stephane Audebert, Luc Camoin, Can Huang, Ling Peng, Ana Jiménez-Alesanco, Adrián Velázquez-Campoy, Olga Abian, Gwen Lomberk, Raul Urrutia, Bruno Rizzuti, Vincent Geli, Philippe Soubeyran, Jose Luis Neira, Juan L. Iovanna	JCI Insight	2020
The Paralogue of the Intrinsically Disordered Nuclear Protein 1 Has a Nuclear Localization Sequence that Binds to Human Importin α3 JL Neira, B Rizzuti, A Jiménez-Alesanco, O Abián, A Velázquez-Campoy, JL Iovanna	International journal of molecular sciences	2020
Pancreatic duct ligation reduces premalignant pancreatic lesions in a Kras model of pancreatic adenocarcinoma in mice M Cáceres, R Quesada, M Iglesias, FX Real, M Villamonte, JM de Villarreal, M Pérez, A Andaluz, X Moll, E Berjano, D Dorcaratto, PS Velazquez, L Grande, F Burdío	Scientific Reports	2020
Oncogenic Role of NUPR1 in Ovarian Cancer J Yu, H Zhu, R Li, Q Jiang, W Luan, J Shi, P Liu	OncoTargets and therapy	2020
Regulatory Potential of Long Non-Coding RNAs (lncRNAs) in Boar Spermatozoa with Good and Poor Freezability L Fraser, Ł Paukszto, A Mańkowska, P Brym, P Gilun, JP Jastrzębski, CS Pareek, D Kumar, M Pierzchała	Life Sciences	2020
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Ligand-based design identifies a potent NUPR1 inhibitor exerting anticancer activity via necroptosis Patricia Santofimia-Castaño, Yi Xia, Wenjun Lan, Zhengwei Zhou, Can Huang, Ling Peng, Philippe Soubeyran, Adrian Velazquez-Campoy, Olga Abian, Bruno Rizzuti, Jose Luis Neira, Juan L Iovanna	Journal of Clinical Investigation	2019
NF-κB/Rel Transcription Factors in Pancreatic Cancer: Focusing on RelA, c-Rel, and RelB D Kabacaoglu, DA Ruess, J Ai, H Algül	Cancers	2019
Systems biology reveals how altered TGFβ signalling with age reduces protection against pro-inflammatory stimuli D Hodgson, AD Rowan, F Falciani, CJ Proctor, JJ Saucerman	PLoS computational biology	2019
Utility of Circulating Cell-Free RNA Analysis for the Characterization of Global Transcriptome Profiles of Multiple Myeloma Patients M Chen, S Mithraprabhu, M Ramachandran, K Choi, T Khong, A Spencer	Cancers	2019
Targeting intrinsically disordered proteins involved in cancer P Santofimia-Castaño, B Rizzuti, Y Xia, O Abian, L Peng, A Velázquez-Campoy, JL Neira, J Iovanna	Cellular and Molecular Life Sciences	2019
Targeting the Stress-Induced Protein NUPR1 to Treat Pancreatic Adenocarcinoma SC, Xia, Peng, VC, Abián, Lan, Lomberk, Urrutia, Rizzuti, Soubeyran, Neira, Iovanna	Cells	2019
Cell-in-Cell Phenomenon and Its Relationship With Tumor Microenvironment and Tumor Progression: A Review X Wang, Y Li, J Li, L Li, H Zhu, H Chen, R Kong, G Wang, Y Wang, J Hu, B Sun	Frontiers in Cell and Developmental Biology	2019
Inactivation of NUPR1 promotes cell death by coupling ER-stress responses with necrosis P Santofimia-Castaño, W Lan, J Bintz, O Gayet, A Carrier, G Lomberk, JL Neira, A González, R Urrutia, P Soubeyran, J Iovanna	Scientific Reports	2018
Systems Analysis of the Liver Transcriptome in Adult Male Zebrafish Exposed to the Plasticizer (2-Ethylhexyl) Phthalate (DEHP) M Huff, WA da Silveira, O Carnevali, L Renaud, G Hardiman	Scientific Reports	2018
Evolutionary routes and KRAS dosage define pancreatic cancer phenotypes S Mueller, T Engleitner, R Maresch, M Zukowska, S Lange, T Kaltenbacher, B Konukiewitz, R Öllinger, M Zwiebel, A Strong, HY Yen, R Banerjee, S Louzada, B Fu, B Seidler, J Götzfried, K Schuck, Z Hassan, A Arbeiter, N Schönhuber, S Klein, C Veltkamp, M Friedrich, L Rad, M Barenboim, C Ziegenhain, J Hess, OM Dovey, S Eser, S Parekh, F Constantino-Casas, J de la Rosa, MI Sierra, M Fraga, J Mayerle, G Klöppel, J Cadiñanos, P Liu, G Vassiliou, W Weichert, K Steiger, W Enard, RM Schmid, F Yang, K Unger, G Schneider, I Varela, A Bradley, D Saur, R Rad	Nature	2018
RNA-Seq Analysis of Islets to Characterise the Dedifferentiation in Type 2 Diabetes Model Mice db/db AN John, R Ram, FX Jiang	Endocrine Pathology	2018
Glucose restriction combined with autophagy inhibition and chemotherapy in HCT 116 spheroids decreases cell clonogenicity and viability regulated by tumor suppressor genes MM Schroll, GJ LaBonia, KR Ludwig, AB Hummon	Journal of Proteome Research	2017
NUPR1 maintains autolysosomal efflux by activating SNAP25 transcription in cancer cells Y Mu, X Yan, D Li, D Zhao, L Wang, X Wang, D Gao, J Yang, H Zhang, Y Li, Y Sun, Y Wei, Z Zhang, X Chang, Z Yao, S Tian, K Zhang, LS Terada, Z Ma, Z Liu	Autophagy	2017
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Intrinsically disordered chromatin protein NUPR1 binds to the C-terminal region of Polycomb RING1B P Santofimia-Castaño, B Rizzuti, ÁL Pey, P Soubeyran, M Vidal, R Urrutia, JL Iovanna, JL Neira	Proceedings of the National Academy of Sciences	2017
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Pancreatic Cancer: Molecular Characterization, Clonal Evolution and Cancer Stem Cells Pelosi E, Castelli G, Testa U	Biomedicines	2017
MET signaling in keratinocytes activates EGFR and initiates squamous carcinogenesis C Cataisson, AM Michalowski, K Shibuya, A Ryscavage, M Klosterman, L Wright, W Dubois, F Liu, A Zhuang, KB Rodrigues, S Hoover, J Dwyer, MR Simpson, G Merlino, SH Yuspa	Science signaling	2016
The Receptor for Advanced Glycation Endproducts Drives T Cell Survival and Inflammation in Type 1 Diabetes Mellitus SP Durning, P Preston-Hurlburt, PR Clark, D Xu, KC Herold	Journal of immunology (Baltimore, Md. : 1950)	2016
Dual PI3K/ERK inhibition induces necroptotic cell death of Hodgkin Lymphoma cells through IER3 downregulation SL Locatelli, G Careddu, GG Stirparo, L Castagna, A Santoro, C Carlo-Stella	Scientific Reports	2016
The pancreatitis-associated protein VMP1, a key regulator of inducible autophagy, promotes KrasG12D-mediated pancreatic cancer initiation C Loncle, MI Molejon, S Lac, JI Tellechea, G Lomberk, L Gramatica, MF Zapico, N Dusetti, R Urrutia, JL Iovanna	Cell Death and Disease	2016
Selective single cell isolation for genomics using microraft arrays JD Welch, LA Williams, M DiSalvo, AT Brandt, R Marayati, CE Sims, NL Allbritton, JF Prins, JJ Yeh, CD Jones	Nucleic Acids Research	2016
Nupr1/Chop signal axis is involved in mitochondrion-related endothelial cell apoptosis induced by methamphetamine D Cai, E Huang, B Luo, Y Yang, F Zhang, C Liu, Z Lin, WB Xie, H Wang	Cell Death and Disease	2016
NUPR1, a new target in liver cancer: implication in controlling cell growth, migration, invasion and sorafenib resistance MR Emma, JL Iovanna, D Bachvarov, R Puleio, GR Loria, G Augello, S Candido, M Libra, A Gulino, V Cancila, JA McCubrey, G Montalto, M Cervello	Cell Death and Disease	2016
Hexavalent Chromium (Cr(VI)) Down-Regulates Acetylation of Histone H4 at Lysine 16 through Induction of Stressor Protein Nupr1 D Chen, T Kluz, L Fang, X Zhang, H Sun, C Jin, M Costa, WG Zhu	PloS one	2016
p8 attenuates the apoptosis induced by dihydroartemisinin in cancer cells through promoting autophagy SS Chen, W Hu, Z Wang, XE Lou, HJ Zhou	Cancer biology & therapy	2015
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Identification of a mitochondrial defect gene signature reveals NUPR1 as a key regulator of liver cancer progression YK Lee, BA Jee, SM Kwon, YS Yoon, WG Xu, HJ Wang, XW Wang, SS Thorgeirsson, JS Lee, HG Woo, G Yoon	Hepatology	2015
Functional Characterization of Nupr1L, A Novel p53-Regulated Isoform of the High-Mobility Group (HMG)-Related Protumoral Protein Nupr1: NUPR1L IS REGULATED BY P53 MB Lopez, MN Garcia, D Grasso, J Bintz, MI Molejon, G Velez, G Lomberk, JL Neira, R Urrutia, J Iovanna	Journal of Cellular Physiology	2015
Integrated stress response is critical for gemcitabine resistance in pancreatic ductal adenocarcinoma LR Palam, J Gore, KE Craven, JL Wilson, M Korc	Cell Death and Disease	2015
Pivotal Role of the Chromatin Protein Nupr1 in Kras-Induced Senescence and Transformation D Grasso, J Bintz, G Lomberk, MI Molejon, C Loncle, MN Garcia, MB Lopez, R Urrutia, JL Iovanna	Scientific Reports	2015
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IER3 in pancreatic carcinogenesis Molejon MI, Iovanna JL	Oncotarget	2015
Genetic inactivation of IER3 delays KrasG12D-dependent pancreatic cancer development Maria Noé Grasso, Daniel Grasso, Maria Belen Lopez-Millan, Tewfik Hamidi, Celine Loncle, Richard Tomasini, Gwen Lomberk, Françoise Porteu, Raul Urrutia, Juan L Iovanna	Journal of Clinical Investigation	2014
Dicer regulates differentiation and viability during mouse pancreatic cancer initiation JP 4th, R Greer, HA Russ, G Figura, GE Kim, A Busch, J Lee, KJ Hertel, S Kim, M McManus, M Hebrok	PloS one	2014
c-Rel is a critical mediator of NF-κB-dependent TRAIL resistance of pancreatic cancer cells C Geismann, F Grohmann, S Sebens, G Wirths, A Dreher, R Häsler, P Rosenstiel, C Hauser, JH Egberts, A Trauzold, G Schneider, B Sipos, S Zeissig, S Schreiber, H Schäfer, A Arlt	Cell Death and Disease	2014
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Genetic inactivation of the pancreatitis-inducible gene Nupr1 impairs PanIN formation by modulating KrasG12D-induced senescence D Grasso, MN Garcia, T Hamidi, C Cano, E Calvo, G Lomberk, R Urrutia, JL Iovanna	Cell Death and Differentiation	2014
Dermal wound transcriptomic responses to Infection with Pseudomonas aeruginosa versus Klebsiella pneumoniae in a rabbit ear wound model KP Leung, P D’Arpa, AK Seth, MR Geringer, M Jett, W Xu, SJ Hong, RD Galiano, T Chen, TA Mustoe	BMC clinical pathology	2014
Pancreatitis promotes oncogenic KrasG12D-induced pancreatic transformation through activation of Nupr1 D Grasso, MN Garcia, H Tewfik, C Cano, E Calvo, G Lomberk, R Urrutia, JL Iovanna	Molecular & Cellular Oncology	2014
Evidence supporting the existence of a NUPR1-like family of helix-loop-helix chromatin proteins related to, yet distinct from, AT hook-containing HMG proteins R Urrutia, G Velez, M Lin, G Lomberk, JL Neira, J Iovanna	Journal of Molecular Modeling	2014
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A subgroup of pancreatic adenocarcinoma is sensitive to the 5-aza-dC DNA methyltransferase inhibitor Gayet O, Loncle C, Duconseil P, Gilabert M, Lopez MB, Moutardier V, Turrini O, Calvo E, Ewald J, Giovannini M, Gasmi M, Bories E, Barthet M, Ouaissi M, Goncalves A, Poizat F, Raoul JL, Secq V, Garcia S, Viens P, Dusetti N, Iovanna J	Oncotarget	2014
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Deciphering the binding between Nupr1 and MSL1 and their DNA-repairing activity D Aguado-Llera, T Hamidi, R Doménech, D Pantoja-Uceda, M Gironella, J Santoro, A Velázquez-Campoy, JL Neira, JL Iovanna	PloS one	2013
Homotypic cell cannibalism, a cell-death process regulated by the nuclear protein 1, opposes to metastasis in pancreatic cancer CE Cano, MJ Sandí, T Hamidi, EL Calvo, O Turrini, L Bartholin, C Loncle, V Secq, S Garcia, G Lomberk, G Kroemer, R Urrutia, JL Iovanna	EMBO Molecular Medicine	2012
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