Taking a basic science research approach to understanding cancer
Our research aims to define the mechanisms that control normal cell proliferation, differentiation, survival and genome maintenance to identify the aberrations in these processes that drive cancer. Our research focus areas include: Cellular and Molecular Mechanisms of Carcinogenesis; Cancer Genetics and Epigenetics; Genome Integrity - DNA Replication, Recombination and Repair; and Cancer Stem Cells, Apoptosis and Autophagy. Our department has laboratories and resources located on both the North and South MD Anderson Campuses in Houston, Texas.
The overall goal of our carcinogenesis research is to understand the basic cellular and molecular mechanisms that allow the transformation of normal cells into cancer cells. Defining these mechanisms will help identify new cancer targets and novel strategies for identifying, treating, and preventing cancer.
Departmental carcinogenesis research includes:
- Discovering new genetic contributors and drivers of cancers
- Identifying genetic and/or therapeutic vulnerabilities in cancers (e.g. synthetic lethality)
- Defining genetic, epigenetic, immunologic, and transcriptional alterations accompanying cancer initiation and progression
- Investigating cell signaling pathways involved in cancer induction and progression
Developing novel computational approaches for cancer research
Enormous amounts of data have been generated from high-throughput, genome-wide experimental approaches, thus creating a pressing need for novel computational approaches to mine and interpret complex "-omics" data sets. Understanding these data sets will help define both the players in biological interaction networks and their functions. Research in the department is combining in-silico approaches with wet-lab experiments to identify drivers and attenuators of cancer. Likewise, the development of CRISPR technology has led to new high-throughput approaches such as genome-wide synthetic lethal screens that also benefit from computational approaches, like those being developed in the department to aid the design and interpretation of high-throughput screens.
Implementing cutting-edge animal models
Our research relies on the development of genetically engineered animal models for investigating the stepwise molecular changes that occur during carcinogenesis, the function of key genes and gene variants in cancer development, and preclinical prevention and therapeutic studies. A number of existing models are being used for these mechanistic studies, including models for skin, mammary gland, prostate, thymus and blood cancers, but we are also creating novel mouse models using modern knockout/knock-in technologies (e.g. CRISPR-Cas9) to study specific genes and pathways involved in cancer induction and progression.
Making discoveries at the intersection of immunology and systems biology
Immunotherapy has been hailed as the fourth pillar of cancer therapy joining surgery, chemotherapy, and radiation treatment. Yet, this treatment approach does not work for all patients. Collaborative departmental research has revealed that patients who respond to immunotherapy have antibody responses against their tumors and that the presence of B cells within a tumor may serve as a marker to predict patient immunotherapy response. These findings are leading to new questions about the role of B cells in immunotherapy response. Other departmental research combining systems-level approaches and wet-lab experiments has revealed that specific mismatch repair-deficient (dMMR) tumors rely on neddylation to remove misfolded or otherwise aberrant proteins, and this mechanism can be exploited by blocking neddylation-mediated protein degradation, which leads to in an increase in immunogenic cell death. These findings suggest that blocking neddylation may benefit patients with dMMR tumors who do not respond to treatment with immunotherapy alone.
Examples of faculty members who are defining the Cellular and Molecular Mechanisms of Carcinogenesis:
C. Marcelo Aldaz - Role of WWOX in cancer and disease; genomic determinants contolling development and progression of pre-invasive breast lesions
Shawn Bratton - Autophagy and prostate cancer; caspase-activating complexes
Sharon Dent - Chromatin remodeling and epigenetics in normal cell growth and in development of cancer and disease
David Johnson - Transcription factor responses in DNA damage and tumor development
Ellen Richie - Regulation of thymus development and homeostasis; role of thymic epithelial cells in regulating T-cell development and T-cell receptor repertoire selection
Kevin McBride - B cell function and antibody repertoire; B cell lymphoma; role of B cells in immunotherapy response
Nidhi Sahni - Systems-level functional and computational genomics, genetic and epigenetic influncing susceptibility and reistance to human cancer and immune system heterogeneity
Margarida Almeida Santos - Tumor promoting roles of genome guardians in leukemia
Richard Wood - Role of DNA polymerase zeta in skin and mammary carcinogenesis
Han Xu - Global view of transcriptional and epigenetic regulation using CRISPR screens; machine-learning and statistical algorithms for high-throughput experiments
Epigenetic factors that regulate DNA methylation, histone modification and chromatin organization can act as either oncogenes or tumor suppressors. Departmental epigenetics research seeks to define both the normal functions of these factors as well as their roles in cancer formation or suppression.
Readers, Writers and Erasers of Epigenetic Marks
Epigenetic marks include cytosine methylation and hydroxymethylation of DNA and methylation, acetylation, phosphorylation, and ubiquitination of histones. These marks are created by enzymes called "writers." Epigenetic "readers" are effector proteins that bear domains that recognize the specific marks left by the "writers," and epigenetic "erasers" can remove these marks. Thus, multiple epigenomes can be created from a single genome.
Uncovering how epigenetic changes and mutations in epigenetic proteins alter gene expression
The major outcome of epigenetic change is alterations in gene expression. Some epigenetic changes are required for normal development and stem cell differentiation, whereas others are aberrant and can lead to diseases, including immunodeficiency, centromeric region instability and facial anomalies syndrome (ICF) and leukemia and other cancers. Importantly, many epigenetic proteins are mutated in human disease, and epigenetic alterations may be just as important as DNA mutations in driving cancer. In addition to controlling gene transcription, these chromatin-modifying enzymes regulate other processes that require access to DNA, including DNA replication and repair.
Departmental epigenetic research areas include:
- Uncovering epigenetic factors controlling developmental reprogramming
- Discovering biological roles of histone lysine and arginine methylation
- Defining the structure and function of epigenetic proteins and epigenetic marks
- Revealing the cellular functions of ATP-dependent chromatin remodelers
- Identifiying and characterizing “readers” of epigenetic marks
- Understanding the role of histone modifications in DNA repair
- Deciphering crosstalk between: histone modifications; histone modifications and DNA methylation; and histone modifications and post-translational modifications of non-histone substrates
Epigenetics-based research provides new avenues for cancer treatment
Epimutations, unlike genetic mutations, can be reversed by chemotherapeutic intervention, which makes epigenetic therapy conceptually appealing. Researchers in the department are screening and identifying small-molecule regulators of epigenetic modifiers and evaluating their potential as anti-cancer drugs, providing clear translational relevance to this research.
As an example, mutliple departmental research teams combined their expertise to use cell culture experiments, computational approaches evaluating cancer cell line RNAi screens, and animal xenograft models to show that small molecule inhibition of an arginine methyltransferase (CARM1) in CREBBP/EP300-mutated diffuse large B-cell lymphomas (DLBCLs) reduces histone acetyltransferase activity and causes synthetic lethality through downregulation of CBP-target genes. This synthetic interaction reveals the possibility that combination therapy using CARM1 inhibitors with CBP/p300 inhibitors may be useful for treating DLBCLs and other cancers with non-mutated CREBBP/EP300.
Examples of faculty engaged in epigenetics research:
Blaine Bartholomew - ATP-dependent chromatin remodelers influence on chromatin dynamics and non-coding RNA transcription
Mark Bedford - Arginine methylation in cellular processes; development of technologies to identify readers of proteins bearing specific epigenetic marks
Taiping Chen - Biological function of histone methylases and demethylases in development and disease
Xiaodong Cheng - Structure and function of readers, writers, and erasers of DNA modifications and their associated histone modifications
Francesca Cole - Epigenetic regulation of meiotic chromosome organization & pairing
Sharon Dent - Histone modifying proteins in development and disease
David Johnson - Recruitment of histone modifying enzymes by E2F1
Margarida Almeida Santos - Epigenetic regulators affecting hematopoietic stem cells
Understanding the mechanisms that damage and repair DNA is fundamental to cancer research
DNA breaks can result from molecularly programmed, intentional DNA damage or non-programmed, incidental DNA damage. Intentional breaks results from specialized cellular processes such as those needed for accurate segregation of chromosomes during meiosis and for creating immune system diversity. In contrast, incidental DNA damage results from exposure to DNA damaging agents from both external and internal sources. External sources include ultraviolet radiation from the sun and chemicals in the environment. Internal sources include reactive chemical species, such as oxygen and water as well as accidental DNA breaks formed during DNA replication. Moreover, many cancer therapies induce irreparable DNA damage leading to cell death. Therefore, investigating how cells respond to and repair DNA damage is important for understanding the causes of cancer and developing new treatments. Research in this area employs a broad range of approaches including studies using protein biochemistry, single-cell genomics, high-resolution microscopy, and genetically engineered mouse models.
Departmental research related to genomic stability includes:
- Defining molecular mechanisms of DNA double-strand break repair
- Discovering new DNA repair pathways and proteins
- Defining the functions of DNA polymerases in DNA repair
- Characterizing DNA damage and repair processes in normal cell function and in carcinogenesis
- Learning how DNA damage and repair contribute to immune system diversity
- Unraveling the relationships between DNA damage, chromatin remodeling, and DNA repair
- Understanding how DNA methylation influences DNA mutation and repair
When DNA damage causes cells to go awry
Department investigators are studying the protein machinery involved in several DNA repair pathways, including homologous recombination and DNA end-joining proccesses for the repair of DNA double-strand breaks, and nucleotide excision repair for the repair of ultraviolet radiation-induced DNA damage and other strand-distorting lesions.
Faculty are also uncovering how programmed DNA damage and repair are involved in normal cellular processes, such as meiosis and immune system B cell development, as well as how these normal processes go awry and contribute to cancer and disease.
Other active areas of research include investigations into the actions of DNA polymerases at repair sites, how chromatin-modifying proteins cooperate with the DNA repair machinery to facilitate repair in the context of chromatin, the mechanisms underlying the conversion of DNA damage into the mutations that cause cancer, and the mechanisms that allow cells to tolerate and survive DNA damage.
Examples of faculty members leading the way in DNA Replication, Recombination, and Repair :
Xiaodong Cheng - Role of DNA methylation in DNA mutation and repair
Francesca Cole - DSB repair by homologous recombination during meiosis
Kevin McBride - Role of programmed DNA damage in creating antibody diversity and leading to lymphomagenesis
Margarida Almeida Santos - DNA damage-induced differentiation of stem-like cancer cells
Richard Wood - Nucleotide excision repair, DNA crosslink repair, role of polymerases in DNA damage tolerance
Stem cells are undifferentiated cells that are unique in their ability to self-renew to create more stem cells while also being able to create daughter cells that can differentiate into other cell types. Most, if not all, cancerous states reflect inappropriate or incomplete cellular differentiation. Aggressive, therapy resistant cancer cells often resemble stem cells in terms of their transcription profiles and self-renewal capacities. Likewise, unregulated growth, abnormal cell division, and defective apoptotic cell death pathways are hallmark features of tumors.
The goal of research in this area is to define normal stem cell biology and developmental pathways as well as to define genetic, molecular, and biochemical mechanisms that regulate cell proliferation, apoptosis and autophagy and relate these pathways to carcinogenesis.
Specific research in this area includes:
- Defining pathways that govern stem cell biology and embryo development
- Understanding DNA damage response in cancer stem cells
- Epigenetic modifications in embyronic, adult, and cancer stem cells
- Epigenetic mechanisms in early embryos and germ cells
- Role of caspases in apoptosis
- Apoptosis and autophagy in normal and disease processes
Using stem cells to learn about cancer
Our research using mouse embryonic and adult stem cells has led to several foundational discoveries. For example, research centered on GCN5, a histone acetyltransferase component of the SAGA complex, uncovered a Myc-SAGA axis that is critical for driving stem cells to pluripotency and is essential for the expression of cell-cycle genes driven by MYC overexpression in a mouse model of B cell lymphoma. Studies of SETDB1, a lysine methyltransferase that deposits the repressive H3K9me3 mark, revealed that SETDB1-dependent gene repression is essential for preserving intestinal stem cell identity by modulating the Wnt and Notch signaling pathways. Other research using mouse models of MLL-rearranged acute myeloid leukemia showed that protein arginine methyltransferase 5 (PRMT5) is essential for the initiation and maintenance of MLL-AF9-mediated leukemia and that inhibiting PRMT5 restores normal differentiation to hematopoietic stem cells.
Apoptosis and autophagy: cancer inhibitors and facilitators
Autophagy (self-cannibalism) and apoptosis (programmed cell death) are fundamental cellular processes that provide mechanisms for cell survival (autophagy) and cell death (apoptosis). Autophagy provides cells with means not only to survive cellular stress and to recycle cellular materials and organelles but also to rid themselves of damaged, malformed, or foreign material. Although autophagy helps suppress carcinogenesis, it can also promote tumor progression, metastasis, and cancer therapy resistance. Apoptosis is required for normal organismal development, but also provides a mechanism to stop cells with DNA damage from dividing. Many chemotherapeutics work by causing DNA damage and inducing apoptosis; however, defects in apoptosis contribute to both tumorigenesis and resistance to cancer treatment. Therefore, defining the molecular mechanisms guiding autophagy and apoptosis, and the pathways allowing cross-talk between them, will provide insights into how cells evade and succumb to cancer treatments.
Faculty with research interests in Cancer Stem Cells and Programmed Cell Death:
Blaine Bartholomew - Chromatin remodelers in pluripotency and development
Shawn Bratton - Heat shock- and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)- induced apoptosis; caspase-activating complexes and the apoptosome; structure and function of autophagosomes; role of autophagy in prostate cancer
Taiping Chen - Epigenetic regulation of embryonic and adult stem cell behavior and function
Sharon Dent - Chromatin modifiers in embryonic stem cells and somatic cell reprogramming
Margarida Almeida Santos - Epigenetic regulation of cancer stem cells
Basu S, Dong Y, Kumar R, Jeter C, Tang DG. Slow-cycling (dormant) cancer cells in therapy resistance, cancer relapse and metastasis. Semin Cancer Biol. 2022 Jan;78:90-103.
Carvajal-Maldonado D, Drogalis Beckham L, Wood RD, Doublié S. When DNA Polymerases Multitask: Functions Beyond Nucleotidyl Transfer. Front Mol Biosci. 2022 Jan 7;8:815845
Chen YC, Koutelou E, Dent SYR. Now open: Evolving insights to the roles of lysine acetylation in chromatin organization and function. Mol Cell. 2022 Feb 17;82(4):716-727.
Fedoriw A*, Shi L*, O'Brien S, Smitheman KN, Wang Y, Hou J, Sherk C, Rajapurkar S, Laraio J, Williams LJ, Xu C, Han G, Feng Q, Bedford MT, Wang L, Barbash O, Kruger RG, Hwu P, Mohammad HP, Peng W. Inhibiting Type I arginine methyltransferase activity promotes the T cell mediated antitumor immune response. Cancer Immunol Res. 2022 Apr 1;10(4):420-436. (*equal contribution)
Fontes F, Rocha S, Sánchez R, Pessina P, Sebastian M, Benavides F, Breijo M. Detection of high antibodies titers against rat leukemia virus in an outbreak of reproductive disorders and lymphomas in Wistar rats. Lab Anim. 2022 Mar 31:236772221085356. doi: 10.1177/00236772221085356. Online ahead of print.
Fu* R, He W*, Dou J, Villarreal OD, Bedford E, Wang H, Hou C, Zhang L, Wang Y, Ma D, Chen Y, Gao X, Depken M, Xu H. Systematic decomposition of sequence determinants governing CRISPR/Cas9 specificity. Nat Commun. 2022 Jan 25;13(1):474. (*equal contribution)
Horton JR, Pathuri S, Wong K, Ren R, Rueda L, Fosbenner DT, Heerding DA, McCabe MT, Pappalardi MB, Zhang X, King BW, Cheng X. Structural characterization of dicyanopyridine containing DNMT1-selective, non-nucleoside inhibitors. Structure. 2022 Mar 28:S0969-2126(22)00090-9. doi: 10.1016/j.str.2022.03.009. Online ahead of print.
Huang YH, Chen CW, Sundaramurthy V, Słabicki M, Hao D, Watson CJ, Tovy A, Reyes JM, Dakhova O, Crovetti BR, Galonska C, Lee M, Brunetti L, Zhou Y, Tatton-Brown K, Huang Y, Cheng X, Meissner A, Valk PJM, Van Maldergem L, Sanders MA, Blundell JR, Li W, Ebert BL, Goodell MA. Systematic Profiling of DNMT3A Variants Reveals Protein Instability Mediated by the DCAF8 E3 Ubiquitin Ligase Adaptor. Cancer Discov. 2022 Jan;12(1):220-235.
Iannelli G, Milite C, Marechal N, Cura V, Bonnefond L, Troffer-Charlier N, Feoli A, Rescigno D, Wang Y, Cipriano A, Viviano M, Bedford MT, Cavarelli J, Castellano S, Sbardella G. Turning Nonselective Inhibitors of Type I Protein Arginine Methyltransferases into Potent and Selective Inhibitors of Protein Arginine Methyltransferase 4 through a Deconstruction-Reconstruction and Fragment-Growing Approach. J Med Chem. 2022 Apr 28. doi: 10.1021/acs.jmedchem.2c00252. Online ahead of print.
Kannan S, Irwin ME, Herbrich SM, Cheng T, Patterson LL, Aitken MJL, Bhalla K, You MJ, Konopleva M, Zweidler-McKay PA, Chandra J. Targeting the NRF2/HO-1 Antioxidant Pathway in FLT3-ITD-Positive AML Enhances Therapy Efficacy. Antioxidants (Basel). 2022 Apr 5;11(4):717.
Khan FI, Rehman T, Sameena F, Hussain T*, AlAjmi MF, Lai D, Khan MKA. Investigating the binding mechanism of topiramate with bovine serum albumin using spectroscopic and computational methods. J Mol Recognit. 2022 Mar 29:e2958. doi: 10.1002/jmr.2958. Online ahead of print. (*postdoctoral fellow with C.M. Aldaz)
Kim KB, Kabra A, Kim DW, Xue Y*, Huang Y, Hou PC, Zhou Y, Miranda LJ, Park JI, Shi X, Bender TP, Bushweller JH, Park KS. KIX domain determines a selective tumor-promoting role for EP300 and its vulnerability in small cell lung cancer. Sci Adv. 2022 Feb 18;8(7):eabl4618. (*graduate student with X. Shi)
Koutelou E, Dent SYR. Navigating EMT with COMPASS and PRC2. Nat Cell Biol. 2022 Apr;24(4):412-414. (News & Views article)
Li J, Lu H, Ng PK, Pantazi A, Ip CKM, Jeong KJ, Amador B, Tran R, Tsang YH, Yang L, Song X, Dogruluk T, Ren X, Hadjipanayis A, Bristow CA, Lee S, Kucherlapati M, Parfenov M, Tang J, Seth S, Mahadeshwar HS, Mojumdar K, Zeng D, Zhang J, Protopopov A, Seidman JG, Creighton CJ, Lu Y, Sahni N, Shaw KR, Meric-Bernstam F, Futreal A, Chin L, Scott KL, Kucherlapati R, Mills GB, Liang H. A functional genomic approach to actionable gene fusions for precision oncology. Sci Adv. 2022 Feb 11;8(6):eabm2382.
Liao Y, Chen CH, Xiao T, de la Peña Avalos B, Dray EV, Cai C, Gao S, Shah N, Zhang Z, Feit A, Xue P, Liu Z, Yang M, Lee JH, Xu H, Li W, Mei S, Pierre RS, Shu S, Fei T, Duarte M, Zhao J, Bradner JE, Polyak K, Kantoff PW, Long H, Balk SP, Liu XS, Brown M, Xu K. Inhibition of EZH2 transactivation function sensitizes solid tumors to genotoxic stress. Proc Natl Acad Sci U S A. 2022 Jan 18;119(3):e2105898119.
Meng H, Gonzales NM, Jung SY, Lu Y, Putluri N, Zhu B, Dacso CC, Lonard DM, O'Malley BW. Defining the mammalian coactivation of hepatic 12-h clock and lipid metabolism. Cell Rep. 2022 Mar 8;38(10):110491.
Mustachio LM, Roszik J . Single-Cell Sequencing: Current Applications in Precision Onco-Genomics and Cancer Therapeutics. Cancers (Basel). 2022 Jan 28;14(3):657.
Ozirmak Lermi N, Gray SB, Bowen CM, Reyes-Uribe L, Dray BK, Deng N, Harris RA, Raveendran M, Benavides F, Hodo CL, Taggart MW, Colbert Maresso K, Sinha KM, Rogers J, Vilar E. Comparative molecular genomic analyses of a spontaneous rhesus macaque model of mismatch repair-deficient colorectal cancer. PLoS Genet. 2022 Apr 21;18(4):e1010163.
Park D, Gharghabi M, Reczek CR, Plow R, Yungvirt C, Aldaz CM, Huebner K. Wwox Binding to the Murine Brca1-BRCT Domain Regulates Timing of Brip1 and CtIP Phospho-Protein Interactions with This Domain at DNA Double-Strand Breaks, and Repair Pathway Choice. Int J Mol Sci. 2022 Mar 28;23(7):3729.
Perez CJ, Mecklenburg L, Fernandez A, Cantero M, de Souza T, Lin K, Dent SYR, Montoliu L, Awgulewitsch A, Benavides, F. Naked (N) mutant mice carry a nonsense mutation in the homeobox of Hoxc13. Exp Dermatol. 2022 Mar;31(3):330-340.
Piya S, Yang Y, Bhattacharya S, Sharma P, Ma H, Mu H, He H, Ruvolo V, Baran N, Davis RE, Jain AK, Konopleava M, Kantarjian H, Andreeff M, You MJ, Borthakur G. Targeting the NOTCH1-MYC-CD44 axis in leukemia-initiating cells in T-ALL. Leukemia. 2022 May;36(5):1261-1273.
Srour N, Villarreal OD, Hardikar S, Yu Z, Preston S, Miller WH Jr, Szewczyk MM, Barsyte-Lovejoy D, Xu H, Chen T, del Rincón SV, Richard S. PRMT7 ablation stimulates anti-tumor immunity and sensitizes melanoma to immune checkpoint blockade. Cell Rep. 2022 Mar 29;38(13):110582.
Tu SM, Estecio MR, Lin SH, Zacharias NM. Stem Cell Theory of Cancer: Rude Awakening or Bad Dream from Cancer Dormancy? Cancers (Basel). 2022 Jan 27;14(3):655.
Van HT, Harkins PR, Patel A, Jain AK, Lu Y, Bedford MT, Santos MA. Methyl-lysine readers PHF20 and PHF20L1 define two distinct gene expression-regulating NSL complexes. J Biol Chem. 2022 Mar;298(3):101588.
Wang Z, Lu Y, Fornage M, Jiao L, Shen J, Li D, Wei P. Identification of novel susceptibility methylation loci for pancreatic cancer in a two-phase epigenome-wide association study. Epigenetics. 2022 Jan 14:1-16. Online ahead of print.
Yang J*, Gupta E*, Horton JR, Blumenthal RM, Zhang X, Cheng X. DNA Repair. Differential ETS1 binding to T:G mismatches within a CpG dinucleotide contributes to C-to-T somatic mutation rate of the IDH2 hotspot at codon Arg140. DNA Repair DNA Repair (Amst). 2022 Apr;298(4):101751. (*equal contribution)
Yu D, Dai N, Wolf EJ, Corrêa IR Jr, Zhou J, Wu T, Blumenthal RM, Zhang X, Cheng X. Enzymatic characterization of mRNA cap adenosine-N6 methyltransferase PCIF1 activity on uncapped RNAs. J Biol Chem. 2022 Feb 18:101751. Online ahead of print.
Zhao S, Habib SL, Senejani AG, Sebastian M, Kidane D. Role of Base Excision Repair in Innate Immune Cells and Its Relevance for Cancer Therapy. Biomedicines. 2022 Feb 26;10(3):557.
Zhang Y, Li Y, Chachad D, Liu B, Godavarthi JD, Williams-Villalobo A, Lasisi L, Xiong S, Matin A. In silico analysis of DND1 and its co-expressed genes in human cancers. Biochem Biophys Rep. 2022 Jan 13;29:101206.
Abba MC, Fabre ML, Lee J, Tatineni P, Kil H, Aldaz CM. HOTAIR Modulated Pathways in Early-Stage Breast Cancer Progression. Front Oncol. 2021 Nov 17;11:783211.
Chen J, Horton J, Sagum C, Zhou J, Cheng X, Bedford MT. Histone H3 N-terminal mimicry drives a novel network of methyl-effector interactions. Biochem J. 2021 May 10:BCJ20210203. doi: 10.1042/BCJ20210203. Online ahead of print.
Genois MM, Gagné JP, Yasuhara T, Jackson J, Saxena S, Langelier MF, Ahel I, Bedford MT, Pascal JM, Vindigni A, Poirier GG, Zou L. CARM1 regulates replication fork speed and stress response by stimulating PARP1. Mol Cell. 2021 Feb 18;81(4):784-800.e8
Guo L, Li Y, Cirillo KM, Marick RA, Su Z, Yin X, Hua X, Mills GB, Sahni N*, Yi SS*. mi-IsoNet: systems-scale microRNA landscape reveals rampant isoform-mediated gain of target interaction diversity and signaling specificity. Brief Bioinform. 2021 Sep 2;22(5):bbab091. (*co-corresponding authors)
Hu X, Estecio MR, Chen R, Reuben A, Wang L, Fujimoto J, Carrot-Zhang J, McGranahan N, Ying L, Fukuoka J, Chow CW, Pham HHN, Godoy MCB, Carter BW, Behrens C, Zhang J, Antonoff MB, Sepesi B, Lu Y, Pass HI, Kadara H, Scheet P, Vaporciyan AA, Heymach JV, Wistuba II, Lee JJ, Futreal PA, Su D, Issa JJ, Zhang J. Evolution of DNA methylome from precancerous lesions to invasive lung adenocarcinomas. Nat Commun. 2021 Jan 29;12(1):687.
Jung YS, Stratton SA, Lee SH, Kim MJ, Jun S, Zhang J, Zheng B, Cervantes CL, Cha JH, Barton MC, Park JI. TMEM9-v-ATPase Activates Wnt/β-Catenin Signaling via APC Lysosomal Degradation for Liver Regeneration and Tumorigenesis. Hepatology. 2021 Feb;73(2):776-794.
Koutelou E, Farria AT, Dent SYR. Complex functions of Gcn5 and Pcaf in development and disease. Biochim Biophys Acta Gene Regul Mech. 2021 Feb;1864(2):194609.
Kuang X, McAndrew MJ, Mustachio LM, Chen YC, Atanassov BS, Lin K, Lu Y, Shen J, Salinger A, Macatee T, Dent SYR*, Koutelou E*. Usp22 Overexpression Leads to Aberrant Signal Transduction of Cancer-Related Pathways but Is Not Sufficient to Drive Tumor Formation in Mice. Cancers (Basel). 2021 Aug 25;13(17):4276. (*co-corresponding authors)
Li Y, Burgman B, Khatri IS, Pentaparthi SR, Su Z, McGrail DJ, Li Y, Wu E, Eckhardt SG, Sahni N*, Yi SS. e-MutPath: computational modeling reveals the functional landscape of genetic mutations rewiring interactome networks. Nucleic Acids Res. 2021 Jan 11;49(1):e2 (*co-corresponding author)
Llorens-Agost M, Ensminger M, Le HP, Gawai A, Liu J, Cruz-García A, Bhetawal S, Wood RD, Heyer WD, Löbrich M. POLθ-mediated end joining is restricted by RAD52 and BRCA2 until the onset of mitosis. Nat Cell Biol. 2021 Oct;23(10):1095-1104.
Martin SK, Tomida J, Wood RD. Disruption of DNA polymerase ζ engages an innate immune response. Cell Rep. 2021 Feb 23;34(8):108775.
Shah VV*, Duncan AD*, Jiang S*, Stratton SA, Allton KL, Yam C, Jain A, Krause PM, Lu Y, Cai S, Tu Y, Zhou X, Zhang X, Jiang Y, Carroll CL, Kang Z, Liu B, Shen J, Gagea M, Manu SM, Huo L, Gilcrease M, Powell RT, Guo L, Stephan C, Davies PJ, Parker-Thornburg J, Lozano G, Behringer RR, Piwnica-Worms H, Chang JT, Moulder SL, Barton MC. Mammary-specific expression of Trim24 establishes a mouse model of human metaplastic breast cancer. Nat Commun. 2021 Sep 10;12(1):5389. (*co-first authors)
Srinivasan J, Lancaster JN, Singarapu N, Hale LP, Ehrlich LIR, Richie ER. Age-Related Changes in Thymic Central Tolerance. Front Immunol. 2021 Apr 22;12:676236. (Review)
Toraason E, Horacek A, Clark C, Glover ML, Adler VL, Premkumar T, Salagean A, Cole F, Libuda DE. Meiotic DNA break repair can utilize homolog-independent chromatid templates in C. elegans. Curr Biol. 2021 Apr 12;31(7):1508-1514.e5.
Trinh A, Gil Del Alcazar CR, Shukla SA, Chin K, Chang YH, Thibault G, Eng J, Jovanović B, Aldaz CM, Park SY, Jeong J, Wu C, Gray J, Polyak K. Genomic Alterations during the In Situ to Invasive Ductal Breast Carcinoma Transition Shaped by the Immune System. Mol Cancer Res. 2021 Apr;19(4):623-635.
Wang Y, Person MD, Bedford MT. Pan-methylarginine antibody generation using PEG linked GAR motifs as antigens. Methods. 2021 Jun 6:S1046-2023(21)00157-2.
Wright T, Wang Y, Bedford MT. The Role of the PRMT5-SND1 Axis in Hepatocellular Carcinoma. Epigenomes. 2021 Mar;5(1):2. (Review)
Yang F, Chen J, Liu B, Gao G, Sebastian M, Jeter C, Shen J, Person MD, Bedford MT. SPINDOC binds PARP1 to facilitate PARylation. Nat Commun. 2021 Nov 4;12(1):6362.
Yang J, Horton JR, Akdemir KC, Li J, Huang Y, Kumar J, Blumenthal RM, Zhang X, Cheng X. Preferential CEBP binding to T:G mismatches and increased C-to-T human somatic mutations. Nucleic Acids Res. 2021 May 21;49(9):5084-5094.
Zahn KE, Jensen RB, Wood RD, Doublié S. Human DNA polymerase θ harbors DNA end-trimming activity critical for DNA repair. Mol Cell. 2021 Apr 1;81(7):1534-1547.e4.
Abba MC, Canzoneri R, Gurruchaga A, Lee J, Tatineni P, Kil H, Lacunza E, Aldaz CM. LINC00885 a Novel Oncogenic Long Non-Coding RNA Associated with Early Stage Breast Cancer Progression. Int J Mol Sci. 2020 Oct 8;21(19):7407.
Benavides F, Rülicke T, Prins JB, Bussell J, Scavizzi F, Cinelli P, Herault Y, Wedekind D. Genetic quality assurance and genetic monitoring of laboratory mice and rats: FELASA Working Group Report. Lab Anim. 2020 Apr;54(2):135-148.
Bhardwaj SK, Hailu SG, Olufemi L, Brahma S, Kundu S, Hota SK, Persinger J, Bartholomew B. Dinucleosome specificity and allosteric switch of the ISW1a ATP-dependent chromatin remodeler in transcription regulation. Nat Commun. 2020 Nov 20;11(1):5913.
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