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1. A proteogenomic portrait of lung squamous cell carcinoma

Author

Shuang Cai, Elizabeth R. Duffy, Felipe da Veiga Leprevost, D. R. Mani, Antonio Colaprico, Jiayi Ji, Mehdi Mesri, Alicia Francis, Peter B. McGarvey, Myvizhi Esai Selvan, Corbin D. Jones, Michael J. Birrer, Robert J. Welsh, Lori Bernard, Shankha Satpathy, Li Ding, Sara R. Savage, Eugene S. Fedorov, Fernanda Martins Rodrigues, Marcin J. Domagalski, Jennifer M. Eschbacher, Shayan C. Avanessian, Boris Reva, Harsh Batra, Suhas Vasaikar, Nathan Edwards, Michael A. Gillette, Chet Birger, Scott D. Jewell, Kei Suzuki, William Bocik, Shilpi Singh, Meenakshi Anurag, Karen E. Christianson, Namrata D. Udeshi, Vasileios Stathias, Warren G. Tourtellotte, Karl R. Clauser, Shutack, Andrii Karnuta, Dana R. Valley, Kelly V. Ruggles, Qing Kay Li, Amanda G. Paulovich, MacIntosh Cornwell, Shankara Anand, Bartosz Kubisa, Pierre M. Jean Beltran, James Suh, Gilbert S. Omenn, Azra Krek, Wohaib Hasan, Yongchao Dou, David Fenyö, Henry Rodriguez, Samuel H. Payne, Małgorzata Wojtyś, Daniel W. Chan, Bo Wen, Nicollette Maunganidze, Özgün Babur, Renganayaki Pandurengan, Karen A. Ketchum, Nikolay Gabrovski, Pankaj Vats, Saravana M. Dhanasekaran, Richard D. Smith, Gad Getz, Sailaja Mareedu, Yuxing Liao, Mikhail Krotevich, Hui Zhang, Eric J. Jaehnig, Charles A. Goldthwaite, Alexey I. Nesvizhskii, Katherine A. Hoadley, Alexander A. Green, Francesca Petralia, Chandan Kumar-Sinha, Karsten Krug, Eunkyung An, Elena V. Ponomareva, Ximing Tang, Nancy Roche, Daniel C. Rohrer, David I. Heiman, Arul M. Chinnaiyan, Pamela Grady, Rebecca I. Montgomery, Galen Hostetter, Liqun Qi, Stephan C. Schürer, George D. Wilson, Pushpa Hariharan, Zhen Zhang, Yvonne, David Chesla, Chia-Kuei Mo, Maria Gabriela Raso, Negin Vatanian, Paul K. Paik, Fei Ding, Thomas L. Bauer, Barbara Hindenach, Matthew J. Ellis, Chen Huang, Karin D. Rodland, Oluwole Fadare, Ramaswamy Govindan, Eric E. Schadt, Sandra Cottingham, Barbara Pruetz, Sendurai A. Mani, Shirley Tsang, Carissa Huynh, Weiping Ma, Jennifer E. Maas, Tobias Schraink, Stacey Gabriel, Bing Zhang, Tara Hiltke, Rama Soundararajan, Tatiana Omelchenko, Brian J. Druker, Matthew A. Wyczalkowski, Neil R. Mucci, Ziad Hanhan, Donna E. Hansel, Yifat Geffen, Mathangi Thiagarajan, Xiaojun Jing, Pei Wang, Alfredo Molinolo, Tanmayi Vashist, Ratna R. Thangudu, Maciej Wiznerowicz, Edwin R. Parra, Tanvi H. Visal, Maureen Dyer, Melissa Borucki, Ki Sung Um, Jonathan T. Lei, Marcin Cieslik, Christopher R. Kinsinger, M. Harry Kane, Houxiang Zhu, Chelsea J. Newton, Steven A. Carr, Tao Liu, Wenke Liu, Volodymyr Sovenko, Olga Potapova, Eric J. Burks, Song Cao, Ana I. Robles, Yuping Zhang, Yize Li, Midie Xu, Erik J. Bergstrom, Zeynep H. Gümüş, Kai Li, and Xiaoyu Song

Subjects
Adult, Male, Epithelial-Mesenchymal Transition, Lung Neoplasms, Biology, Proteomics, Receptor Tyrosine Kinase-like Orphan Receptors, General Biochemistry, Genetics and Molecular Biology, Article, SOX2, CDKN2A, Survivin, medicine, Cluster Analysis, Humans, Receptors, Platelet-Derived Growth Factor, Phosphorylation, Lung cancer, Aged, Proteogenomics, Aged, 80 and over, EZH2, Ubiquitination, Cyclin-Dependent Kinase 4, Acetylation, Cyclin-Dependent Kinase 6, Middle Aged, medicine.disease, Chromatin, Neoplasm Proteins, Gene Expression Regulation, Neoplastic, Mutation, Cancer research, Carcinoma, Squamous Cell, Female, Protein Binding, Signal Transduction
Abstract

Lung squamous cell carcinoma (LSCC) remains a leading cause of cancer death with few therapeutic options. We characterized the proteogenomic landscape of LSCC, providing a deeper exposition of LSCC biology with potential therapeutic implications. We identify NSD3 as an alternative driver in FGFR1-amplified tumors and low-p63 tumors overexpressing the therapeutic target survivin. SOX2 is considered undruggable, but our analyses provide rationale for exploring chromatin modifiers such as LSD1 and EZH2 to target SOX2-overexpressing tumors. Our data support complex regulation of metabolic pathways by crosstalk between post-translational modifications including ubiquitylation. Numerous immune-related proteogenomic observations suggest directions for further investigation. Proteogenomic dissection of CDKN2A mutations argue for more nuanced assessment of RB1 protein expression and phosphorylation before declaring CDK4/6 inhibition unsuccessful. Finally, triangulation between LSCC, LUAD, and HNSCC identified both unique and common therapeutic vulnerabilities. These observations and proteogenomics data resources may guide research into the biology and treatment of LSCC.

Published
2020

2. Integrated Proteogenomic Characterization across Major Histological Types of Pediatric Brain Cancer

Author

Matthew E. Monroe, Saravana M. Dhanasekaran, Brian R. Rood, Zeynep H. Gümüş, Jena Lilly, Samuel G. Winebrake, Richard G. Ivey, William Bocik, Mahdi Sarmady, Alicia Francis, Lamiya Tauhid, Nathan Edwards, Lizabeth Katsnelson, Rui Zhao, Matilda Broberg, Jo Lynne Rokita, Mateusz Koptyra, Henry Rodriguez, Cassie Kline, Shrabanti Chowdhury, Nicole Tignor, Ying Wang, Christopher R. Kinsinger, Antonio Colaprico, Amanda G. Paulovich, Weiping Ma, Emily S. Boja, Tara Hiltke, Sabine Mueller, Liang-Bo Wang, Javad Nazarian, Marcin J. Domagalski, Karl K. Weitz, Jessica B. Foster, Robert Lober, Carina A. Leonard, Bo Zhang, Gerald A. Grant, Anna Calinawan, Gonzalo Lopez, Shuang Cai, Joanna J. Phillips, Guo Ci Teo, July E. Palma, Felipe da Veiga Leprevost, Yiran Guo, Angela Waanders, Xiaoyu Song, Li Ding, Allison Heath, Steven P. Gygi, Rosalie K. Chu, Vasileios Stathias, Bailey Farrow, Oren J. Becher, Dmitry Rykunov, Nithin D. Adappa, Ron Firestein, Adam C. Resnick, Marcin Cieślik, Jennifer Mason, D. R. Mani, Selim Kalayci, Boris Reva, Antonio Iavarone, MacIntosh Cornwell, Uliana J. Voytovich, Gabrielle S. Stone, Miguel A. Brown, Jacob J. Kennedy, Tao Liu, Ronald J. Moore, Emily Kawaler, Eric H. Raabe, Marina A. Gritsenko, Valerie Baubet, Francesca Petralia, Maciej Wiznerowicz, Olena Morozova Vaske, Eric E. Schadt, Ian F. Pollack, Arul M. Chinnaiyan, Meghan Connors, Jason E. Cain, Lei Zhao, Matthew A. Wyczalkowski, Nalin Gupta, Bing Zhang, Jiayi Ji, Marilyn M. Li, Samuel Rivero-Hinojosa, Mariarita Santi, Wenke Liu, John Szpyt, Brian Ennis, Alexey I. Nesvizhskii, Joshua M. Wang, Jeffrey P. Greenfield, Sanjukta Guha Thakurta, Hui Yin Chang, Peter B. McGarvey, Xi Chen, Karen A. Ketchum, Stephan C. Schürer, Sarah Leary, Lili Blumenberg, Matthew J. Ellis, Pei Wang, Anna Maria Buccoliero, Karsten Krug, Chiara Caporalini, Gad Getz, David E. Kram, Pichai Raman, Eric M. Jackson, James N. Palmer, Mehdi Mesri, Kelly V. Ruggles, Chunde Li, Jun Zhu, Sonia Partap, Jeffrey R. Whiteaker, Mirko Scagnet, Krutika S. Gaonkar, Azra Krek, Allison M. Morgan, Tatiana Omelchenko, Richard D. Smith, Elizabeth Appert, Karin D. Rodland, Derek Hanson, Phillip B. Storm, Jamie Moon, Vladislav A. Petyuk, Nathan Young, Travis D. Lorentzen, David Fenyö, Angela N. Viaene, Seungyeul Yoo, Yuankun Zhu, Nicholas A Vitanza, Toan Le, Tatiana Patton, and Ana I. Robles

Subjects
DNA Copy Number Variations, Computational biology, Biology, Proteomics, Article, General Biochemistry, Genetics and Molecular Biology, Ganglioglioma, 03 medical and health sciences, Lymphocytes, Tumor-Infiltrating, 0302 clinical medicine, Glioma, medicine, Humans, Gene Regulatory Networks, RNA, Messenger, Copy-number variation, Phosphorylation, Child, Proteogenomics, 030304 developmental biology, Medulloblastoma, 0303 health sciences, Brain Neoplasms, Genome, Human, Phosphoproteomics, Phosphoproteins, medicine.disease, Gene Expression Regulation, Neoplastic, Mutation, Atypical teratoid rhabdoid tumor, Neoplasm Grading, Neoplasm Recurrence, Local, Transcriptome, 030217 neurology & neurosurgery
Abstract

We report a comprehensive proteogenomics analysis, including whole-genome sequencing, RNA sequencing, and proteomics and phosphoproteomics profiling, of 218 tumors across 7 histological types of childhood brain cancer: low-grade glioma (n = 93), ependymoma (32), high-grade glioma (25), medulloblastoma (22), ganglioglioma (18), craniopharyngioma (16), and atypical teratoid rhabdoid tumor (12). Proteomics data identify common biological themes that span histological boundaries, suggesting that treatments used for one histological type may be applied effectively to other tumors sharing similar proteomics features. Immune landscape characterization reveals diverse tumor microenvironments across and within diagnoses. Proteomics data further reveal functional effects of somatic mutations and copy number variations (CNVs) not evident in transcriptomics data. Kinase-substrate association and co-expression network analysis identify important biological mechanisms of tumorigenesis. This is the first large-scale proteogenomics analysis across traditional histological boundaries to uncover foundational pediatric brain tumor biology and inform rational treatment selection.

Published
2020
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3. Proteogenomic Characterization Reveals Therapeutic Vulnerabilities in Lung Adenocarcinoma

Author

Yuxing Liao, Meghan C. Burke, Donghui Tan, Xiaoyu Song, Lauren C. Tang, Elizabeth R. Duffy, Shayan C. Avanessian, Daniel Cui Zhou, Maureen Dyer, Sara R. Savage, Jennifer M. Eschbacher, Shaleigh Smith, Alex Webster, Alicia Francis, Kelly V. Ruggles, Christopher R. Kinsinger, Shirley Tsang, Melissa Borucki, Nancy Roche, Pei Wang, Qing Kay Li, David Chesla, Ronald Matteotti, Zeynep H. Gümüş, Kai Li, Kei Suzuki, Thomas L. Bauer, Lori J. Sokoll, John McGee, Marcin J. Domagalski, Ki Sung Um, Tara Hiltke, Hai-Quan Chen, Hongwei Liu, Eric E. Schadt, Antonio Colaprico, Alyssa Charamut, Lijun Chen, Emily Kawaler, Ramani B. Kothadia, Mehdi Mesri, Jiayi Ji, Simina M. Boca, Myvizhi Esai Selvan, Emily S. Boja, Xi Chen, Shuang Cai, Kim Elburn, Samuel H. Payne, George D. Wilson, Peter B. McGarvey, Chelsea J. Newton, Felipe da Veiga Leprevost, Uma Velvulou, Tara Skelly, Corbin D. Jones, Michael J. Birrer, Steven A. Carr, Erik J. Bergstrom, Jeffrey R. Whiteaker, Michael H.A. Roehrl, Gad Getz, Tanya Krubit, Zhen Zhang, Yan Shi, Lili Blumenberg, Melanie A. MacMullan, Song Cao, Zhiao Shi, Weiping Ma, Chet Birger, Karl R. Clauser, Runyu Hong, Shankha Satpathy, Andrii Karnuta, Boris Reva, Barbara Hindenach, Matthew J. Ellis, Amanda G. Paulovich, Michael C. Wendl, Bing Zhang, Marina A. Gritsenko, Matthew A. Wyczalkowski, Stacey Gabriel, Michael A. Gillette, Jacob J. Day, Maciej Wiznerowicz, Stephen E. Stein, Ewa P. Malc, Robert J. Welsh, Sunita Shankar, Brian J. Druker, Li Ding, Lijun Yao, David J. Clark, Małgorzata Wojtyś, Dmitry Rykunov, Eugene S. Fedorov, Linda Hannick, Andrew K. Godwin, Sailaja Mareedu, Pushpa Hariharan, Mary Beth Beasley, Stephanie De Young, Arul M. Chinnaiyan, Robert Zelt, Mathangi Thiagarajan, Munziba Khan, Suhas Vasaikar, Tao Liu, Karin D. Rodland, Katherine A. Hoadley, Wen-Wei Liang, Ana I. Robles, Dana R. Valley, Sanford P. Markey, Mikhail Krotevich, David I. Heiman, Piotr A. Mieczkowski, Galen Hostetter, Liqun Qi, Yige Wu, Hui Zhang, Liang-Bo Wang, Nathan Edwards, Ramaswamy Govindan, Yifat Geffen, Seema Chugh, Alexey I. Nesvizhskii, Karen A. Ketchum, Pankaj Vats, Matthew E. Monroe, Marcin Cieslik, Yingwei Hu, Karsten Krug, Yosef E. Maruvka, Yize Li, Ratna R. Thangudu, William W. Maggio, Sandra Cottingham, Saravana M. Dhanasekaran, Wenke Liu, Hua Sun, Sonya Carter, Volodymyr Sovenko, M. Harry Kane, Annette Marrero-Oliveras, Barbara Pruetz, Amy M. Perou, Gilbert S. Omenn, Azra Krek, Olga Potapova, Michael S. Noble, Daniel W. Chan, Seungyeul Yoo, Eric J. Burks, Bo Wen, William Bocik, Michael Vernon, Henry Rodriguez, James Suh, Scott D. Jewell, MacIntosh Cornwell, Richard D. Smith, Chandan Kumar-Sinha, Halina M. Krzystek, Daniel C. Rohrer, Tatiana Omelchenko, D. R. Mani, Houston Culpepper, Vladislav A. Petyuk, Meng-Hong Sun, Michelle Chaikin, David Fenyö, Rahul Mannan, Bartosz Kubisa, Rohit Mehra, Rajwanth R. Veluswamy, Umut Ozbek, Michael Schnaubelt, Francesca Petralia, Elena V. Ponomareva, Rashna Madan, Pamela Grady, Karna Robinson, and Negin Vatanian

Subjects
0303 health sciences, Phosphoproteomics, Genomics, Environmental exposure, Computational biology, Biology, Proteomics, Proteogenomics, medicine.disease_cause, Article, General Biochemistry, Genetics and Molecular Biology, 03 medical and health sciences, 0302 clinical medicine, Neutrophil degranulation, medicine, KRAS, 030217 neurology & neurosurgery, 030304 developmental biology, Epigenomics
Abstract

To explore the biology of lung adenocarcinoma (LUAD) and identify new therapeutic opportunities, we performed comprehensive proteogenomic characterization of 110 tumors and 101 matched normal adjacent tissues (NATs) incorporating genomics, epigenomics, deep-scale proteomics, phosphoproteomics, and acetylproteomics. Multi-omics clustering revealed four subgroups defined by key driver mutations, country, and gender. Proteomic and phosphoproteomic data illuminated biology downstream of copy number aberrations, somatic mutations, and fusions and identified therapeutic vulnerabilities associated with driver events involving KRAS, EGFR, and ALK. Immune subtyping revealed a complex landscape, reinforced the association of STK11 with immune-cold behavior, and underscored a potential immunosuppressive role of neutrophil degranulation. Smoking-associated LUADs showed correlation with other environmental exposure signatures and a field effect in NATs. Matched NATs allowed identification of differentially expressed proteins with potential diagnostic and therapeutic utility. This proteogenomics dataset represents a unique public resource for researchers and clinicians seeking to better understand and treat lung adenocarcinomas.

Published
2020
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4. Integrated Proteogenomic Characterization of Clear Cell Renal Cell Carcinoma

Author

David J. Clark, Jianbo Pan, Gerald W. Hart, Katherine A. Hoadley, Negin Vatanian, Shuang Cai, Yige Wu, Felipe da Veiga Leprevost, A. Ari Hakimi, Sanford P. Markey, Thomas F. Westbrook, Maciej Wiznerowicz, Nathan Edwards, Alla Y. Karpova, Sohini Sengupta, Marcin Cieslik, Samuel H. Payne, Xi Steven Chen, Guo Ci Teo, Jin Chen, Boris Reva, Corbin D. Jones, Michael J. Birrer, Ying Wang, Kelly V. Ruggles, Doug W. Chan, John McGee, Marcin J. Domagalski, Song Cao, Linda Hannick, Christopher R. Kinsinger, David I. Heiman, Jennifer M. Eschbacher, Munziba Khan, Jason E. McDermott, Dmitry M. Avtonomov, Sue Hilsenbeck, Qing Kay Li, Jiayi Ji, Emek Demir, Rebecca I. Montgomery, Qingsong Gao, Beom-Jun Kim, Xiaoyu Song, Karl R. Clauser, Christian P. Pavlovich, Richard D. Smith, Maureen Dyer, Jeffrey W. Tyner, Amy M. Perou, Yuping Zhang, Dana R. Valley, George D. Wilson, Shiyong Ma, Minghui Ao, Jiang Qian, Umut Ozbek, Melissa Borucki, Zhi Li, Michael Schnaubelt, Chen Huang, Piotr A. Mieczkowski, Francesca Petralia, Abdul Samad Hashimi, Hui Yin Chang, Liang-Bo Wang, Matthew E. Monroe, Peter B. McGarvey, Tao Liu, Karen A. Ketchum, Hui Zhang, Bing Zhang, D. R. Mani, Houston Culpepper, Hua Zhou, Saravana M. Dhanasekaran, Paul D. Piehowski, Zhidong Tu, Brian J. Druker, Ki Sung Um, Zhiao Shi, Uma Borate, Uma Velvulou, Michael Ittmann, Weiping Ma, Steven M. Foltz, Heng Zhu, Stacey Gabriel, Hongwei Liu, Ramani B. Kothadia, Lin Chen, Ewa P. Malc, Marina A. Gritsenko, Jun Zhu, David Chesla, Lori J. Sokoll, Stephen E. Stein, Andrzej Antczak, Matthew L. Anderson, Alyssa Charamut, Pamela Grady, Michael T. Lewis, Shannon Richey, Tanya Krubit, Alexander R. Pico, Kyung-Cho Cho, Daniel C. Rohrer, Francesmary Modugno, Stephanie De Young, Li Ding, Michael Smith, Mathangi Thiagarajan, Alexey I. Nesvizhskii, Shrabanti Chowdhury, Noam D. Beckmann, Kimberly R. Holloway, Ratna R. Thangudu, Sherri R. Davies, Tung-Shing M. Lih, Nicole Tignor, Anna Calinawan, Meghan C. Burke, Karna Robinson, Chet Birger, Shalin Patel, Antonio Colaprico, Sarah Keegan, Daniel J. Geiszler, Scott D. Jewell, William Bocik, Snehal Patil, Pei Wang, MacIntosh Cornwell, Emily Kawaler, Seungyeul Yoo, Jasmine Huang, Vladislav A. Petyuk, Ross Bremner, Donghui Tan, Stefani N. Thomas, Emily S. Boja, Anna Malovannaya, Xi Chen, Wenke Liu, Eric E. Schadt, Shankha Satpathy, Nancy Roche, Rajiv Dhir, Cristina E. Tognon, Michelle Chaikin, Gabriel Bromiński, Daniel C. Zhou, Yifat Geffen, Tara Skelly, Jacob J. Day, Sunantha Sethuraman, Sonya Carter, Zhen Zhang, Selim Kalayci, Michael Vernon, Zeynep H. Gümüş, Kai Li, Barbara Hindenach, Matthew J. Ellis, Meenakshi Anurag, David C. Wheeler, Sailaja Mareedu, Andy T. Kong, Arul M. Chinnaiyan, Robert Zelt, Annette Marrero-Oliveras, Henry Rodriguez, James Suh, Anupriya Agarwal, David Fenyö, Galen Hostetter, Liqun Qi, Matthew A. Wyczalkowski, W. Marston Linehan, Tara Hiltke, Feng Chen, Lijun Chen, Jan Lubinski, Chelsea J. Newton, Steven A. Carr, Tatiana Omelchenko, Gilbert S. Omenn, Karsten Krug, Ana I. Robles, Azra Krek, Runyu Hong, Milan G. Chheda, Yize Li, Yan Shi, Lili Blumenberg, Ruiyang Liu, Karin D. Rodland, Hua Sun, Kim Elburn, Jeffrey R. Whiteaker, Christopher J. Ricketts, Gaddy Getz, Daniel W. Chan, Bo Wen, Robert Edwards, Patricia Castro, Yingwei Hu, Pushpa Hariharan, Simina M. Boca, Darlene Tansil, Phillip M. Pierorazio, Yosef E. Maruvka, Sandra Cottingham, James J. Hsieh, Amanda G. Paulovich, Barbara Pruetz, Michael A. Gillette, Yihao Lu, Dmitry Rykunov, Mehdi Mesri, Marc M. Loriaux, Reyka G Jayasinghe, and Suhas Vasaikar

Subjects
Adult, Male, Cell, Computational biology, Biology, Proteomics, Disease-Free Survival, Oxidative Phosphorylation, Article, General Biochemistry, Genetics and Molecular Biology, Transcriptome, 03 medical and health sciences, 0302 clinical medicine, Exome Sequencing, medicine, Biomarkers, Tumor, Tumor Microenvironment, Humans, Exome, Phosphorylation, Carcinoma, Renal Cell, 030304 developmental biology, Epigenomics, Aged, Proteogenomics, Aged, 80 and over, 0303 health sciences, Tumor microenvironment, Genome, Human, Phosphoproteomics, Middle Aged, medicine.disease, Neoplasm Proteins, Gene Expression Regulation, Neoplastic, Clear cell renal cell carcinoma, medicine.anatomical_structure, Female, 030217 neurology & neurosurgery, Signal Transduction
Abstract

SUMMARY To elucidate the deregulated functional modules that drive clear cell renal cell carcinoma (ccRCC), we performed comprehensive genomic, epigenomic, transcriptomic, proteomic, and phosphoproteomic characterization of treatment-naive ccRCC and paired normal adjacent tissue samples. Genomic analyses identified a distinct molecular subgroup associated with genomic instability. Integration of proteogenomic measurements uniquely identified protein dysregulation of cellular mechanisms impacted by genomic alterations, including oxidative phosphorylation-related metabolism, protein translation processes, and phospho-signaling modules. To assess the degree of immune infiltration in individual tumors, we identified microenvironment cell signatures that delineated four immune-based ccRCC subtypes characterized by distinct cellular pathways. This study reports a large-scale proteogenomic analysis of ccRCC to discern the functional impact of genomic alterations and provides evidence for rational treatment selection stemming from ccRCC pathobiology., Graphical Abstract, In Brief Comprehensive proteogenomic characterization in 103 treatment-naive clear cell renal cell carcinoma patient samples highlights tumor-specific alterations at the proteomic level that are unrevealed by transcriptomic profiling and proposes a revised subtyping scheme based on integrated omics analysis.

Published
2020
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