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Author Mats Ljungman

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Deletion of Glutathione S-Transferase Omega 1 Activates Type I Interferon Genes and Downregulates Tissue Factor.

Yibin Xu, Armand Bankhead, Xiaoli Tian, Jianming Tang, Mats Ljungman, Nouri Neamati,

Glutathione S-transferase omega 1 (GSTO1) is an atypical GST isoform that is overexpressed in several cancers and has been implicated in drug resistance. Currently, no small-molecule drug targeting GSTO1 is under clinical development. Here we have validated GSTO1 as an impactful target in oncology. Transcriptional profiling coupled with proteomics uncovered ... Read more >>

Cancer Res. (Cancer research)
[2020, :]

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UAE1 inhibition mediates the unfolded protein response, DNA damage and caspase-dependent cell death in pancreatic cancer.

Yajing Liu, Sahezeel Awadia, Amy Delaney, Merna Sitto, Carl G Engelke, Heli Patel, Andrew Calcaterra, Sylvia Zelenka-Wang, Hojin Lee, Joseph Contessa, Nouri Neamati, Mats Ljungman, Theodore S Lawrence, Meredith A Morgan, Alnawaz Rehemtulla,

The Unfolded Protein Response (UPR) plays a key role in the adaptive response to loss of protein homeostasis within the endoplasmic reticulum (ER). The UPR has an adaptive function in protein homeostasis, however, sustained activation of the UPR due to hypoxia, nutrient deprivation, and increased demand for protein synthesis, alters ... Read more >>

Transl Oncol (Translational oncology)
[2020, 13(11):100834]

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Up-regulation of hypoxia-inducible factor antisense as a novel approach to treat ovarian cancer.

Tiangong Lu, Jianming Tang, Binita Shrestha, Blake R Heath, Li Hong, Yu L Lei, Mats Ljungman, Nouri Neamati,

Ovarian cancer (OC) is estimated to kill ~14,000 women in the United States in 2019. Current chemotherapies to treat OC initially show therapeutic efficacy but frequently drug resistance develops, at which point therapies with alternative targets are needed. Herein, we are describing a novel approach to sensitize these tumors to ... Read more >>

Theranostics (Theranostics)
[2020, 10(15):6959-6976]

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Principles of mRNA control by human PUM proteins elucidated from multi-modal experiments and integrative data analysis

Michael Wolfe, Trista Schagat, Michelle Paulsen, Brian Magnuson, Mats Ljungman, Daeyoon Park, Chi Zhang, Zachary Campbell, Aaron Goldstrohm, Peter Freddolino,

Abstract The human PUF-family proteins, PUM1 and PUM2, post-transcriptionally regulate gene expression by binding to a PUM recognition element (PRE) in the 3’ UTR of target mRNAs. Hundreds of PUM1/2 targets have been identified from changes in steady state RNA levels; however, prior studies could not differentiate between the contributions ... Read more >>

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KMT2D links TGF-β Signalling to Non-Canonical Activin Pathway and Regulates Pancreatic Cancer Cell Plasticity

Shuang Lu, Hong Sun Kim, Yubo Cao, Karan Bedi, Krista Chain, Lili Zhao, Ishwarya Venkata Narayanan, Zhujun Yi, Jing Yang, Yumei Gu, Michelle Paulsen, Mats Ljungman, Sivakumar Jeyarajan, Dafydd Thomas, Yali Dou, Howard Crawford, Marina Pasca di Magliano, Jiaqi Shi,

Abstract Although KMT2D, also known as MLL2, is known to play an essential role in development, differentiation, and tumor suppression, its role in pancreatic cancer development is not well understood. Here, we discovered a novel signaling axis mediated by KMT2D, which links TGF-β to the activin A pathway. We found ... Read more >>

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Nascent Transcriptomics Reveal Cellular Prolytic Factors Upregulated Upstream of the Latent-to-Lytic Switch Protein of Epstein-Barr Virus.

Tiffany R Frey, Jozan Brathwaite, Xiaofan Li, Sandeepta Burgula, Ibukun A Akinyemi, Saurabh Agarwal, Eric M Burton, Mats Ljungman, Michael T McIntosh, Sumita Bhaduri-McIntosh,

Lytic activation from latency is a key transition point in the life cycle of herpesviruses. Epstein-Barr virus (EBV) is a human herpesvirus that can cause lymphomas, epithelial cancers, and other diseases, most of which require the lytic cycle. While the lytic cycle of EBV can be triggered by chemicals and ... Read more >>

J. Virol. (Journal of virology)
[2020, 94(7):]

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A CSB-PAF1C axis restores processive transcription elongation after DNA damage repair

Diana van den Heuvel, Cornelia Spruijt, Román González-Prieto, Angela Kragten, Michelle Paulsen, Di Zhou, Haoyu Wu, Katja Apelt, Yana van der Weegen, Kevin Yang, Madelon Dijk, Lucia Daxinger, Jurgen Marteijn, Alfred C.O. Vertegaal, Mats Ljungman, Michiel Vermeulen, Martijn Luijsterburg,

Abstract The coordinated transcription of genes involves the regulated release of RNA polymerase II (RNAPII) from promoter-proximal sites into active elongation. DNA lesions in transcribed strands block elongation and induce a strong transcriptional arrest. The transcription-coupled repair (TCR) pathway efficiently removes transcription-blocking DNA lesions, but this is not sufficient to ... Read more >>

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Characterization of novel primary miRNA transcription units in human cells using Bru-seq nascent RNA sequencing.

Karan Bedi, Michelle T Paulsen, Thomas E Wilson, Mats Ljungman,

MicroRNAs (miRNAs) are key contributors to gene regulatory networks. Because miRNAs are processed from RNA polymerase II transcripts, insight into miRNA regulation requires a comprehensive understanding of the regulation of primary miRNA transcripts. We used Bru-seq nascent RNA sequencing and hidden Markov model segmentation to map primary miRNA transcription units ... Read more >>

NAR Genom Bioinform (NAR genomics and bioinformatics)
[2020, 2(1):lqz014]

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Multi-omics profiling reveals key signaling pathways in ovarian cancer controlled by STAT3.

Tiangong Lu, Armand Bankhead, Mats Ljungman, Nouri Neamati,

Inhibiting STAT3 signaling reduces tumor progression, metastasis and chemoresistance, however the precise molecular mechanism has not been fully delineated in ovarian cancer. METHODS:In this study, we generated STAT3 knockout (KO) ovarian cancer cell lines. Effects of STAT3 KO on cell proliferation, migration and spheroid formation were assessed in vitro and ... Read more >>

Theranostics (Theranostics)
[2019, 9(19):5478-5496]

Cited: 3 times

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Multivalent proteins rapidly and reversibly phase-separate upon osmotic cell volume change

Ameya Jalihal, Sethuramasundaram Pitchiaya, Lanbo Xiao, Pushpinder Bawa, Xia Jiang, Karan Bedi, Abhijit Parolia, Marcin Cieslik, Mats Ljungman, Arul Chinnaiyan, Nils Walter,

SUMMARY Processing bodies (PBs) and stress granules (SGs) are prominent examples of sub-cellular, membrane-less compartments that are observed under physiological and stress conditions, respectively. We observe that the trimeric PB protein DCP1A rapidly (within ∼10 s) phase-separates in mammalian cells during hyperosmotic stress and dissolves upon isosmotic rescue (over ∼100 ... Read more >>

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Inhibition of protein disulfide isomerase in glioblastoma causes marked downregulation of DNA repair and DNA damage response genes.

Shili Xu, Yajing Liu, Kai Yang, Hanxiao Wang, Andrea Shergalis, Anahita Kyani, Armand Bankhead, Shuzo Tamura, Suhui Yang, Xi Wang, Chih-Chen Wang, Alnawaz Rehemtulla, Mats Ljungman, Nouri Neamati,

Aberrant overexpression of endoplasmic reticulum (ER)-resident oxidoreductase protein disulfide isomerase (PDI) plays an important role in cancer progression. In this study, we demonstrate that PDI promotes glioblastoma (GBM) cell growth and describe a class of allosteric PDI inhibitors that are selective for PDI over other PDI family members. Methods: We ... Read more >>

Theranostics (Theranostics)
[2019, 9(8):2282-2298]

Cited: 5 times

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ATDC is required for the initiation of KRAS-induced pancreatic tumorigenesis.

Lidong Wang, Huibin Yang, Andrea Zamperone, Daniel Diolaiti, Phillip L Palmbos, Ethan V Abel, Vinee Purohit, Igor Dolgalev, Andrew D Rhim, Mats Ljungman, Christina H Hadju, Christopher J Halbrook, Dafna Bar-Sagi, Marina Pasca di Magliano, Howard C Crawford, Diane M Simeone,

Pancreatic adenocarcinoma (PDA) is an aggressive disease driven by oncogenic KRAS and characterized by late diagnosis and therapeutic resistance. Here we show that deletion of the ataxia-telangiectasia group D-complementing (Atdc) gene, whose human homolog is up-regulated in the majority of pancreatic adenocarcinoma, completely prevents PDA development in the context of ... Read more >>

Genes Dev. (Genes & development)
[2019, 33(11-12):641-655]

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Activation of the Unfolded Protein Response via Inhibition of Protein Disulfide Isomerase Decreases the Capacity for DNA Repair to Sensitize Glioblastoma to Radiotherapy.

Yajing Liu, Wenbin Ji, Andrea Shergalis, Jiaqi Xu, Amy M Delaney, Andrew Calcaterra, Anupama Pal, Mats Ljungman, Nouri Neamati, Alnawaz Rehemtulla,

Patients with glioblastoma multiforme (GBM) survive on average 12 to 14 months after diagnosis despite surgical resection followed by radiotheraphy and temozolomide therapy. Intrinsic or acquired resistance to chemo- and radiotherapy is common and contributes to a high rate of recurrence. To investigate the therapeutic potential of protein disulfide isomerase ... Read more >>

Cancer Res. (Cancer research)
[2019, 79(11):2923-2932]

Cited: 3 times

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Design, Synthesis, and Biological Evaluation of Novel Allosteric Protein Disulfide Isomerase Inhibitors.

Suhui Yang, Andrea Shergalis, Dan Lu, Anahita Kyani, Ziwei Liu, Mats Ljungman, Nouri Neamati,

Protein disulfide isomerase (PDI) is responsible for nascent protein folding in the endoplasmic reticulum (ER) and is critical for glioblastoma survival. To improve the potency of lead PDI inhibitor BAP2 (( E)-3-(3-(4-hydroxyphenyl)-3-oxoprop-1-en-1-yl)benzonitrile), we designed and synthesized 67 analogues. We determined that PDI inhibition relied on the A ring hydroxyl group ... Read more >>

J. Med. Chem. (Journal of medicinal chemistry)
[2019, 62(7):3447-3474]

Cited: 3 times

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Genome-wide de novo L1 Retrotransposition Connects Endonuclease Activity with Replication.

Diane A Flasch, Ángela Macia, Laura Sánchez, Mats Ljungman, Sara R Heras, José L García-Pérez, Thomas E Wilson, John V Moran,

L1 retrotransposon-derived sequences comprise approximately 17% of the human genome. Darwinian selective pressures alter L1 genomic distributions during evolution, confounding the ability to determine initial L1 integration preferences. Here, we generated high-confidence datasets of greater than 88,000 engineered L1 insertions in human cell lines that act as proxies for cells ... Read more >>

Cell (Cell)
[2019, 177(4):837-851.e28]

Cited: 5 times

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IDH1-R132H acts as a tumor suppressor in glioma via epigenetic up-regulation of the DNA damage response.

Felipe J Núñez, Flor M Mendez, Padma Kadiyala, Mahmoud S Alghamri, Masha G Savelieff, Maria B Garcia-Fabiani, Santiago Haase, Carl Koschmann, Anda-Alexandra Calinescu, Neha Kamran, Meghna Saxena, Rohin Patel, Stephen Carney, Marissa Z Guo, Marta Edwards, Mats Ljungman, Tingting Qin, Maureen A Sartor, Rebecca Tagett, Sriram Venneti, Jacqueline Brosnan-Cashman, Alan Meeker, Vera Gorbunova, Lili Zhao, Daniel M Kremer, Li Zhang, Costas A Lyssiotis, Lindsey Jones, Cameron J Herting, James L Ross, Dolores Hambardzumyan, Shawn Hervey-Jumper, Maria E Figueroa, Pedro R Lowenstein, Maria G Castro,

Patients with glioma whose tumors carry a mutation in isocitrate dehydrogenase 1 (IDH1R132H) are younger at diagnosis and live longer. IDH1 mutations co-occur with other molecular lesions, such as 1p/19q codeletion, inactivating mutations in the tumor suppressor protein 53 (TP53) gene, and loss-of-function mutations in alpha thalassemia/mental retardation syndrome X-linked ... Read more >>

Sci Transl Med (Science translational medicine)
[2019, 11(479):]

Cited: 12 times

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Identifying cis Elements for Spatiotemporal Control of Mammalian DNA Replication.

Jiao Sima, Abhijit Chakraborty, Vishnu Dileep, Marco Michalski, Kyle N Klein, Nicolas P Holcomb, Jesse L Turner, Michelle T Paulsen, Juan Carlos Rivera-Mulia, Claudia Trevilla-Garcia, Daniel A Bartlett, Peiyao A Zhao, Brian K Washburn, Elphège P Nora, Katerina Kraft, Stefan Mundlos, Benoit G Bruneau, Mats Ljungman, Peter Fraser, Ferhat Ay, David M Gilbert,

The temporal order of DNA replication (replication timing [RT]) is highly coupled with genome architecture, but cis-elements regulating either remain elusive. We created a series of CRISPR-mediated deletions and inversions of a pluripotency-associated topologically associating domain (TAD) in mouse ESCs. CTCF-associated domain boundaries were dispensable for RT. CTCF protein depletion ... Read more >>

Cell (Cell)
[2019, 176(4):816-830.e18]

Cited: 11 times

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GENE-35. IDH1-R132H INDUCES AN EPIGENETIC REPROGRAMMING IN GLIOMA IMPACTING MEDIAN SURVIVAL, DNA-DAMAGE RESPONSE AND RADIO-SENSITIVITY.

Felipe Nunez, Flor Mendez, Padma Kadiyala, Mahmoud Alghamri, Stephen Carney, Mats Ljungman, Tingting Qin, Maureen Sartor, Sriram Venneti, Costas Lyssiotis, Joseph Costello, Cameron Herting, Dolores Hambardzumyan, Maria Figueroa, Pedro Lowenstein, Maria Castro,

AbstractIDH1-R132H is the most common mutation in lower-grade glioma and secondary glioblastoma. It is expressed in combination with ATRX and p53 inactivation in a mIDH1 glioma subtype which has been associated with better prognosis. We hypothesized that this is mediated by the impact of epigenetic changes on DNA-repair and DNA ... Read more >>

Neuro-oncology (Neuro-oncology)
[2018, 20(Suppl 6):vi111-vi111]

Cited: 0 times

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Synthesis and mechanistic studies of quinolin-chlorobenzothioate derivatives with proteasome inhibitory activity in pancreatic cancer cell lines.

Shuai Hu, Yi Jin, Yanghan Liu, Mats Ljungman, Nouri Neamati,

Inhibition of proteasome activity blocks the degradation of dysfunctional proteins and induces cancer cell death due to cellular stress. Thus, proteasome inhibitors represent an attractive class of anticancer agents, and bortezomib, carfilzomib and ixazomib have been FDA-approved to treat multiple myeloma. However, cancer cells acquire resistance to these inhibitors through ... Read more >>

Eur J Med Chem (European journal of medicinal chemistry)
[2018, 158:884-895]

Cited: 1 time

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HNF1A is a novel oncogene that regulates human pancreatic cancer stem cell properties.

Ethan V Abel, Masashi Goto, Brian Magnuson, Saji Abraham, Nikita Ramanathan, Emily Hotaling, Anthony A Alaniz, Chandan Kumar-Sinha, Michele L Dziubinski, Sumithra Urs, Lidong Wang, Jiaqi Shi, Meghna Waghray, Mats Ljungman, Howard C Crawford, Diane M Simeone,

The biological properties of pancreatic cancer stem cells (PCSCs) remain incompletely defined and the central regulators are unknown. By bioinformatic analysis of a human PCSC-enriched gene signature, we identified the transcription factor HNF1A as a putative central regulator of PCSC function. Levels of HNF1A and its target genes were found ... Read more >>

Elife (eLife)
[2018, 7:]

Cited: 8 times

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IDH1R132H acts as a tumor suppressor in glioma via epigenetic upregulation of the DNA damage response

Felipe Núñez, Flor Mendez, Padma Kadiyala, Mahmoud Alghamri, Masha Savelieff, Carl Koschmann, Anda-Alexandra Calinescu, Neha Kamran, Rohin Patel, Stephen Carney, Marissa Guo, Maria Garcia-Fabiani, Santiago Haase, Marta Edwards, Mats Ljungman, Tingting Qin, Maureen Sartor, Rebecca Tagett, Sriram Venneti, Jacqueline Brosnan-Cashman, Alan Meeker, Vera Gorbunova, Lili Zhao, Daniel Kremer, Li Zhang, Costas Lyssiotis, Lindsey Jones, Cameron Herting, James Ross, Dolores Hambardzumyan, Shawn Hervey-Jumper, Maria Figueroa, Pedro Lowenstein, Maria Castro,

One sentence summary Mutant IDH1 acts as a tumor suppressor when co-expressed together with TP53 and ATRX inactivating mutations in glioma, inducing genomic stability, DNA repair and resistance to genotoxic therapies. Abstract Glioma patients whose tumors carry a mutation in the Isocitrate Dehydrogenase 1 (IDH1 R132H ) gene are younger ... Read more >>

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Menin regulates the serine biosynthetic pathway in Ewing sarcoma.

Laurie K Svoboda, Selina Shiqing K Teh, Sudha Sud, Samuel Kerk, Aaron Zebolsky, Sydney Treichel, Dafydd Thomas, Christopher J Halbrook, Ho-Joon Lee, Daniel Kremer, Li Zhang, Szymon Klossowski, Armand R Bankhead, Brian Magnuson, Mats Ljungman, Tomasz Cierpicki, Jolanta Grembecka, Costas A Lyssiotis, Elizabeth R Lawlor,

Developmental transcription programs are epigenetically regulated by multi-protein complexes, including the menin- and MLL-containing trithorax (TrxG) complexes, which promote gene transcription by depositing the H3K4me3 activating mark at target gene promoters. We recently reported that in Ewing sarcoma, MLL1 (lysine methyltransferase 2A, KMT2A) and menin are overexpressed and function as ... Read more >>

J. Pathol. (The Journal of pathology)
[2018, 245(3):324-336]

Cited: 4 times

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Mutant p53R270H drives altered metabolism and increased invasion in pancreatic ductal adenocarcinoma.

Heather K Schofield, Jörg Zeller, Carlos Espinoza, Christopher J Halbrook, Annachiara Del Vecchio, Brian Magnuson, Tania Fabo, Ayse Ece Cali Daylan, Ilya Kovalenko, Ho-Joon Lee, Wei Yan, Ying Feng, Saadia A Karim, Daniel M Kremer, Chandan Kumar-Sinha, Costas A Lyssiotis, Mats Ljungman, Jennifer P Morton, Stefanie Galbán, Eric R Fearon, Marina Pasca di Magliano,

Pancreatic cancer is characterized by nearly universal activating mutations in KRAS. Among other somatic mutations, TP53 is mutated in more than 75% of human pancreatic tumors. Genetically engineered mice have proven instrumental in studies of the contribution of individual genes to carcinogenesis. Oncogenic Kras mutations occur early during pancreatic carcinogenesis ... Read more >>

JCI Insight (JCI insight)
[2018, 3(2):]

Cited: 6 times

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Identification of cis elements for spatio-temporal control of DNA replication

Jiao Sima, Abhijit Chakraborty, Vishnu Dileep, Marco Michalski, Juan Carlos Rivera-Mulia, Claudia Trevilla-Garcia, Kyle Klein, Daniel Bartlett, Brian Washburn, Michelle Paulsen, Daniel Vera, Elphège Nora, Katerina Kraft, Stefan Mundlos, Benoit Bruneau, Mats Ljungman, Peter Fraser, Ferhat Ay, David Gilbert,

SUMMARY The temporal order of DNA replication (replication timing, RT) is highly coupled with genome architecture, but cis -elements regulating spatio-temporal control of replication have remained elusive. We performed an extensive series of CRISPR mediated deletions and inversions and high-resolution capture Hi-C of a pluripotency associated domain (DppA2/4) in mouse ... Read more >>

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Design and Synthesis of Novel Reactive Oxygen Species Inducers for the Treatment of Pancreatic Ductal Adenocarcinoma.

Yuting Kuang, Mario Sechi, Salvatore Nurra, Mats Ljungman, Nouri Neamati,

Altering redox homeostasis provides distinctive therapeutic opportunities for the treatment of pancreatic cancer. Quinazolinediones (QDs) are novel redox modulators that we previously showed to induce potent growth inhibition in pancreatic ductal adenocarcinoma (PDAC) cell lines. Our lead optimization campaign yielded QD325 as the most potent redox modulator candidate inducing substantial ... Read more >>

J. Med. Chem. (Journal of medicinal chemistry)
[2018, 61(4):1576-1594]

Cited: 5 times

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