. 2020 Feb 20;180(4):729-748.e26.

doi: 10.1016/j.cell.2020.01.026. Epub 2020 Feb 13.

Proteogenomic Characterization of Endometrial Carcinoma

Yongchao Dou¹, Emily A Kawaler², Daniel Cui Zhou³, Marina A Gritsenko⁴, Chen Huang¹, Lili Blumenberg⁵, Alla Karpova³, Vladislav A Petyuk⁴, Sara R Savage¹, Shankha Satpathy⁶, Wenke Liu², Yige Wu³, Chia-Feng Tsai⁴, Bo Wen¹, Zhi Li², Song Cao³, Jamie Moon⁴, Zhiao Shi¹, MacIntosh Cornwell², Matthew A Wyczalkowski³, Rosalie K Chu⁴, Suhas Vasaikar⁷, Hua Zhou², Qingsong Gao³, Ronald J Moore⁴, Kai Li¹, Sunantha Sethuraman³, Matthew E Monroe⁴, Rui Zhao⁴, David Heiman⁶, Karsten Krug⁶, Karl Clauser⁶, Ramani Kothadia⁶, Yosef Maruvka⁶, Alexander R Pico⁸, Amanda E Oliphant⁹, Emily L Hoskins⁹, Samuel L Pugh⁹, Sean J I Beecroft⁹, David W Adams⁹, Jonathan C Jarman⁹, Andy Kong¹⁰, Hui-Yin Chang¹⁰, Boris Reva¹¹, Yuxing Liao¹, Dmitry Rykunov¹¹, Antonio Colaprico¹², Xi Steven Chen¹², Andrzej Czekański¹³, Marcin Jędryka¹³, Rafał Matkowski¹³, Maciej Wiznerowicz¹⁴, Tara Hiltke¹⁵, Emily Boja¹⁵, Christopher R Kinsinger¹⁵, Mehdi Mesri¹⁵, Ana I Robles¹⁵, Henry Rodriguez¹⁵, David Mutch¹⁶, Katherine Fuh¹⁶, Matthew J Ellis¹, Deborah DeLair¹⁷, Mathangi Thiagarajan¹⁸, D R Mani⁶, Gad Getz⁶, Michael Noble⁶, Alexey I Nesvizhskii¹⁹, Pei Wang¹¹, Matthew L Anderson²⁰, Douglas A Levine²¹, Richard D Smith⁴, Samuel H Payne⁹, Kelly V Ruggles⁵, Karin D Rodland²², Li Ding²³, Bing Zhang²⁴, Tao Liu²⁵, David Fenyö²⁶; Clinical Proteomic Tumor Analysis Consortium

Collaborators, Affiliations

Collaborators

Clinical Proteomic Tumor Analysis Consortium:
Anupriya Agarwal, Meenakshi Anurag, Dmitry Avtonomov, Chet Birger, Michael J Birrer, Simina M Boca, William E Bocik, Uma Borate, Melissa Borucki, Meghan C Burke, Shuang Cai, Anna Calinawan, Steven A Carr, Sonya Carter, Patricia Castro, Sandra Cerda, Michelle Chaikin, Daniel W Chan, Doug Chan, Alyssa Charamut, Feng Chen, Jin Chen, Lijun Chen, Lin S Chen, David Chesla, Milan G Chheda, Arul M Chinnaiyan, Shrabanti Chowdhury, Marcin P Cieslik, David J Clark, Sandra Cottingham, Houston Culpepper, Jacob Day, Stephanie De Young, Emek Demir, Saravana Mohan Dhanasekaran, Rajiv Dhir, Marcin J Domagalski, Peter Dottino, Brian Druker, Elizabeth Duffy, Maureen Dyer, Nathan J Edwards, Robert Edwards, Kim Elburn, Jayson B Field, Alicia Francis, Stacey Gabriel, Yifat Geffen, Daniel Geiszler, Michael A Gillette, Andrew K Godwin, Pamela Grady, Linda Hannick, Pushpa Hariharan, Sue Hilsenbeck, Barbara Hindenach, Katherine A Hoadley, Runyu Hong, Galen Hostetter, James J Hsieh, Yingwei Hu, Michael M Ittmann, Eric Jaehnig, Scott D Jewell, Jiayi Ji, Corbin D Jones, Renee Karabon, Karen A Ketchum, Munziba Khan, Beom-Jun Kim, Azra Krek, Tanya Krubit, Chandan Kumar-Sinha, Felipe D Leprevost, Michael Lewis, Qing Kay Li, Yize Li, Hongwei Liu, Jan Lubinski, Weiping Ma, Rashna Madan, Ewa Malc, Anna Malovannaya, Sailaja Mareedu, Sanford P Markey, Annette Marrero-Oliveras, John Martignetti, Jason McDermott, Peter B McGarvey, John McGee, Piotr Mieczkowski, Francesmary Modugno, Rebecca Montgomery, Chelsea J Newton, Gilbert S Omenn, Amanda G Paulovich, Amy M Perou, Francesca Petralia, Paul Piehowski, Larisa Polonskaya, Liqun Qi, Shannon Richey, Karna Robinson, Nancy Roche, Daniel C Rohrer, Eric E Schadt, Michael Schnaubelt, Yan Shi, Tara Skelly, Lori J Sokoll, Xiaoyu Song, Stephen E Stein, James Suh, Donghui Tan, Darlene Tansil, Guo Ci Teo, Ratna R Thangudu, Cristina Tognon, Elie Traer, Jeffrey Tyner, Ki Sung Um, Dana R Valley, Negin Vatanian, Pankaj Vats, Uma Velvulou, Michael Vernon, Liang-Bo Wang, Ying Wang, Alex Webster, Thomas Westbrook, David Wheeler, Jeffrey R Whiteaker, George D Wilson, Yuriy Zakhartsev, Robert Zelt, Hui Zhang, Yuping Zhang, Zhen Zhang, Grace Zhao

Affiliations

¹ Lester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA.
² Institute for Systems Genetics, NYU School of Medicine, New York, NY 10016, USA; Department of Biochemistry and Molecular Pharmacology, NYU School of Medicine, New York, NY 10016, USA.
³ Department of Medicine and Genetics, Siteman Cancer Center, Washington University in St. Louis, St. Louis, MO 63110, USA; McDonnell Genome Institute, Washington University in St. Louis, St. Louis, MO 63108, USA.
⁴ Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99354, USA.
⁵ Department of Medicine, NYU School of Medicine, New York, NY 10016, USA.
⁶ The Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
⁷ Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
⁸ Institute of Data Science and Biotechnology, Gladstone Institutes, San Francisco, CA 94158, USA.
⁹ Department of Biology, Brigham Young University, Provo, UT 84602, USA.
¹⁰ Department of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
¹¹ Department of Genetics and Genomic Sciences, Icahn Institute of Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
¹² Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA; Division of Biostatistics, Department of Public Health Science, University of Miami Miller School of Medicine, Miami, FL 33136, USA.
¹³ Department of Oncology, Wroclaw Medical University, 50-367 Wrocław, Poland; Wroclaw Comprehensive Cancer Center, 53-413 Wrocław, Poland.
¹⁴ Poznan University of Medical Sciences, 61-701 Poznań, Poland; University Hospital of Lord's Transfiguration, 60-569 Poznań, Poland; International Institute for Molecular Oncology, 60-203 Poznań, Poland.
¹⁵ Office of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
¹⁶ Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹⁷ Department of Pathology, NYU Langone Health, New York, NY 10016, USA.
¹⁸ Leidos Biomedical Research Inc., Frederick National Laboratory for Cancer Research, Frederick, MD 21702, USA.
¹⁹ Department of Pathology, University of Michigan, Ann Arbor, MI 48109, USA; Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48109, USA.
²⁰ College of Medicine Obstetrics & Gynecology, University of South Florida Health, Tampa, FL 33620, USA.
²¹ Gynecologic Oncology, Laura and Isaac Perlmutter Cancer Center, NYU Langone Health, New York, NY 10016, USA.
²² Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99354, USA; Department of Cell, Developmental, and Cancer Biology, Oregon Health & Science University, Portland, OR 97221, USA. Electronic address: karin.rodland@pnnl.gov.
²³ Department of Medicine and Genetics, Siteman Cancer Center, Washington University in St. Louis, St. Louis, MO 63110, USA; McDonnell Genome Institute, Washington University in St. Louis, St. Louis, MO 63108, USA. Electronic address: lding@wustl.edu.
²⁴ Lester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA. Electronic address: bing.zhang@bcm.edu.
²⁵ Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99354, USA. Electronic address: tao.liu@pnnl.gov.
²⁶ Institute for Systems Genetics, NYU School of Medicine, New York, NY 10016, USA; Department of Biochemistry and Molecular Pharmacology, NYU School of Medicine, New York, NY 10016, USA. Electronic address: david@fenyolab.org.

PMID: 32059776
PMCID: PMC7233456
DOI: 10.1016/j.cell.2020.01.026

Proteogenomic Characterization of Endometrial Carcinoma

Yongchao Dou et al. Cell. 2020.

. 2020 Feb 20;180(4):729-748.e26.

doi: 10.1016/j.cell.2020.01.026. Epub 2020 Feb 13.

Authors

Collaborators

Clinical Proteomic Tumor Analysis Consortium:
Anupriya Agarwal, Meenakshi Anurag, Dmitry Avtonomov, Chet Birger, Michael J Birrer, Simina M Boca, William E Bocik, Uma Borate, Melissa Borucki, Meghan C Burke, Shuang Cai, Anna Calinawan, Steven A Carr, Sonya Carter, Patricia Castro, Sandra Cerda, Michelle Chaikin, Daniel W Chan, Doug Chan, Alyssa Charamut, Feng Chen, Jin Chen, Lijun Chen, Lin S Chen, David Chesla, Milan G Chheda, Arul M Chinnaiyan, Shrabanti Chowdhury, Marcin P Cieslik, David J Clark, Sandra Cottingham, Houston Culpepper, Jacob Day, Stephanie De Young, Emek Demir, Saravana Mohan Dhanasekaran, Rajiv Dhir, Marcin J Domagalski, Peter Dottino, Brian Druker, Elizabeth Duffy, Maureen Dyer, Nathan J Edwards, Robert Edwards, Kim Elburn, Jayson B Field, Alicia Francis, Stacey Gabriel, Yifat Geffen, Daniel Geiszler, Michael A Gillette, Andrew K Godwin, Pamela Grady, Linda Hannick, Pushpa Hariharan, Sue Hilsenbeck, Barbara Hindenach, Katherine A Hoadley, Runyu Hong, Galen Hostetter, James J Hsieh, Yingwei Hu, Michael M Ittmann, Eric Jaehnig, Scott D Jewell, Jiayi Ji, Corbin D Jones, Renee Karabon, Karen A Ketchum, Munziba Khan, Beom-Jun Kim, Azra Krek, Tanya Krubit, Chandan Kumar-Sinha, Felipe D Leprevost, Michael Lewis, Qing Kay Li, Yize Li, Hongwei Liu, Jan Lubinski, Weiping Ma, Rashna Madan, Ewa Malc, Anna Malovannaya, Sailaja Mareedu, Sanford P Markey, Annette Marrero-Oliveras, John Martignetti, Jason McDermott, Peter B McGarvey, John McGee, Piotr Mieczkowski, Francesmary Modugno, Rebecca Montgomery, Chelsea J Newton, Gilbert S Omenn, Amanda G Paulovich, Amy M Perou, Francesca Petralia, Paul Piehowski, Larisa Polonskaya, Liqun Qi, Shannon Richey, Karna Robinson, Nancy Roche, Daniel C Rohrer, Eric E Schadt, Michael Schnaubelt, Yan Shi, Tara Skelly, Lori J Sokoll, Xiaoyu Song, Stephen E Stein, James Suh, Donghui Tan, Darlene Tansil, Guo Ci Teo, Ratna R Thangudu, Cristina Tognon, Elie Traer, Jeffrey Tyner, Ki Sung Um, Dana R Valley, Negin Vatanian, Pankaj Vats, Uma Velvulou, Michael Vernon, Liang-Bo Wang, Ying Wang, Alex Webster, Thomas Westbrook, David Wheeler, Jeffrey R Whiteaker, George D Wilson, Yuriy Zakhartsev, Robert Zelt, Hui Zhang, Yuping Zhang, Zhen Zhang, Grace Zhao

Affiliations

¹ Lester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA.
² Institute for Systems Genetics, NYU School of Medicine, New York, NY 10016, USA; Department of Biochemistry and Molecular Pharmacology, NYU School of Medicine, New York, NY 10016, USA.
³ Department of Medicine and Genetics, Siteman Cancer Center, Washington University in St. Louis, St. Louis, MO 63110, USA; McDonnell Genome Institute, Washington University in St. Louis, St. Louis, MO 63108, USA.
⁴ Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99354, USA.
⁵ Department of Medicine, NYU School of Medicine, New York, NY 10016, USA.
⁶ The Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
⁷ Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
⁸ Institute of Data Science and Biotechnology, Gladstone Institutes, San Francisco, CA 94158, USA.
⁹ Department of Biology, Brigham Young University, Provo, UT 84602, USA.
¹⁰ Department of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
¹¹ Department of Genetics and Genomic Sciences, Icahn Institute of Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
¹² Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA; Division of Biostatistics, Department of Public Health Science, University of Miami Miller School of Medicine, Miami, FL 33136, USA.
¹³ Department of Oncology, Wroclaw Medical University, 50-367 Wrocław, Poland; Wroclaw Comprehensive Cancer Center, 53-413 Wrocław, Poland.
¹⁴ Poznan University of Medical Sciences, 61-701 Poznań, Poland; University Hospital of Lord's Transfiguration, 60-569 Poznań, Poland; International Institute for Molecular Oncology, 60-203 Poznań, Poland.
¹⁵ Office of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
¹⁶ Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹⁷ Department of Pathology, NYU Langone Health, New York, NY 10016, USA.
¹⁸ Leidos Biomedical Research Inc., Frederick National Laboratory for Cancer Research, Frederick, MD 21702, USA.
¹⁹ Department of Pathology, University of Michigan, Ann Arbor, MI 48109, USA; Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48109, USA.
²⁰ College of Medicine Obstetrics & Gynecology, University of South Florida Health, Tampa, FL 33620, USA.
²¹ Gynecologic Oncology, Laura and Isaac Perlmutter Cancer Center, NYU Langone Health, New York, NY 10016, USA.
²² Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99354, USA; Department of Cell, Developmental, and Cancer Biology, Oregon Health & Science University, Portland, OR 97221, USA. Electronic address: karin.rodland@pnnl.gov.
²³ Department of Medicine and Genetics, Siteman Cancer Center, Washington University in St. Louis, St. Louis, MO 63110, USA; McDonnell Genome Institute, Washington University in St. Louis, St. Louis, MO 63108, USA. Electronic address: lding@wustl.edu.
²⁴ Lester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA. Electronic address: bing.zhang@bcm.edu.
²⁵ Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99354, USA. Electronic address: tao.liu@pnnl.gov.
²⁶ Institute for Systems Genetics, NYU School of Medicine, New York, NY 10016, USA; Department of Biochemistry and Molecular Pharmacology, NYU School of Medicine, New York, NY 10016, USA. Electronic address: david@fenyolab.org.

PMID: 32059776
PMCID: PMC7233456
DOI: 10.1016/j.cell.2020.01.026

Abstract

We undertook a comprehensive proteogenomic characterization of 95 prospectively collected endometrial carcinomas, comprising 83 endometrioid and 12 serous tumors. This analysis revealed possible new consequences of perturbations to the p53 and Wnt/β-catenin pathways, identified a potential role for circRNAs in the epithelial-mesenchymal transition, and provided new information about proteomic markers of clinical and genomic tumor subgroups, including relationships to known druggable pathways. An extensive genome-wide acetylation survey yielded insights into regulatory mechanisms linking Wnt signaling and histone acetylation. We also characterized aspects of the tumor immune landscape, including immunogenic alterations, neoantigens, common cancer/testis antigens, and the immune microenvironment, all of which can inform immunotherapy decisions. Collectively, our multi-omic analyses provide a valuable resource for researchers and clinicians, identify new molecular associations of potential mechanistic significance in the development of endometrial cancers, and suggest novel approaches for identifying potential therapeutic targets.

Keywords: CTNNB1; TP53; acetylation; circular RNA; endometrial cancer; endometrioid endometrial cancer; immune evasion; proteogenomics; proteomics; serous endometrial cancer.

PubMed Disclaimer

Conflict of interest statement

Declaration Of Interests The authors declare no competing interests.

Figures

**Figure 1.. Proteogenomic Summary of the Cohort**
Samples are ordered by genomic subtype and then by histology. Representative pathways are shown for genes with the greatest variation between subtypes. For each sample, we display mutation load, copy number indices (at both global and arm levels), and mutation status in SMGs. See also Figure S2; Table S3.

**Figure 2.. Effects of Somatic Mutations**
(A) *Cis* and *trans* effects of mutations in EC SMGs. Affected proteins and phosphoproteins are grouped by pathway. (B) Effects of missense and truncation mutations. (C) Effects of *CTNNB1* mutations. (D) p53 binds DNA as a tetramer. Highlighted in red is a mutation-phosphosite cluster that directly affects the DNA binding domain of p53. (E) Effects of *TP53* mutations. See also Figure S3.

**Figure 3.. Acetylation**
(A) Associations of the levels of key acetylation enzymes with histone acetylation sites. (B) Change in acetylation levels between tumor samples and normal endometrium samples. The horizontal line denotes an FDR cutoff of 0.05, and the vertical lines denote a fold change of 0.4. Grey points represent sites whose acetylation change is explained by a change in protein levels. (C) Association between histone acetylation sites and mutated SMGs. The acetylation change is shown for the most significant site in each histone protein. (D-F) Acetylation-level changes in specific histone sites in WT and mutated samples for *CTNNB1* (D), *ARID1A* (E), and *KRAS* (F). See also Figure S4.

**Figure 4.. Proteomics Data Reveal SCNA and DNA Methylation Drivers of Tumor Progression**
(A) MLH1 and HOX family genes are directly affected by DNA methylation. Samples are ranked from lowest (left) to highest (right) DNA methylation levels. (B) Effects of SCNA on mRNA and protein levels. Top: copy number correlation with mRNA (left) and protein (right). Positive and negative correlations are indicated in red and blue, respectively. Bottom: the frequency of correlations. Blue bars represent copy number correlation with mRNA (left) and protein (right), and black bars represent copy number correlation to both mRNA and protein. (C) 1q amplification is anticorrelated with p53 pathway activity. The samples are ranked based on their inferred p53 pathway activity. The triangles denote recurrent TP53 mutations across multiple cancer types. (D) Identifying novel p53 inhibitors encoded on 1q. On the top, all quantifiable genes in proteomics, transcriptomics, and copy number alterations are ranked based on the correlation between the protein level and p53 activity. On the bottom, from top to bottom, 1q genes, 1q genes with SCNA *cis* effects, and 1q histone modifiers with SCNA *cis* effects are highlighted. (E) The correlation between SCNAs, mRNA level, and protein levelsfor1q histone modifiers. Samples are ranked from lowest (left) to highest (right) copy number values. (F) SETDB1 protein levels showed anticorrelation with *CDKN1A* RNA. See also Figure S5; Table S5.

**Figure 5.. Discovery of circRNAs and Their Potential Roles in EMT Regulation**
(A) Distributions of correlations between pairs of circRNAs and between circRNAs and their host genes. (B) Numbers of circRNAs correlated to RBPs. (C) Positive correlation is found between QKI protein level and EMT score. (D) Negative correlation is found between QKI and ESRP2 protein levels. (E) Correlation between QKI protein level and miRNA expression/activity. (F) Schematic of our model shows QKI, circRNAs, and miRNAs forming a positive feedback loop to promote EMT in EC. See also Figure S6; Table S5.

**Figure 6.. Proteomics-Driven Clinical Utility**
(A) Differential levels of protein (green), phosphorylation sites (maroon), and acetylation sites (yellow) between MSI and MSS tumors. (B) Comparison of RPL22L1 protein levels between MSI tumors with and without *RPL22* indel and MSS tumors. (C) Differential levels of protein (green), phosphorylation sites (maroon), and acetylation sites (yellow) between serous and endometrioid tumors. (D-F) Correlation between PLK1 level and the levels of its substrates TP53BP1-S1763 (D) and CHEK2-S163 (E) and G2M checkpoint protein level (F). (G) Dependence of PLK1 level on DNA damage signaling. * indicates p < 0.05 (H) Proteins with drug interactions that are enriched in DDR-high endometrioid and/or DDR-high serous samples (outlier analysis FDR < 0.05). (I) Proteins with drug interactions that are enriched in serous or endometrioid CNV-high samples (outlier analysis FDR < 0.05). See also Figure S7; Table S6.

**Figure 7.. Immune Landscape of EC**
(A) Putative neoantigens and CT antigens. (B) Tumor samples are divided into four immune subtypes by TMB and APM efficiency. (C) Immune profiles of each immune subtype. (D) Comparison of the JAK/STAT pathway between TMB-H/APM-H and TMB-H/APM-L groups. * indicates p < 0.05; *** indicates p < 0.001. See also Table S7.

See this image and copyright information in PMC

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Proteogenomic Characterization of Endometrial Carcinoma

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Proteogenomic Characterization of Endometrial Carcinoma

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