The Human Tumor Atlas Network: Charting Tumor Transitions across Space and Time at Single-Cell Resolution

Orit Rozenblatt-Rosen; Aviv Regev; Philipp Oberdoerffer; Tal Nawy; Anna Hupalowska; Jennifer E Rood; Orr Ashenberg; Ethan Cerami; Robert J Coffey; Emek Demir; Li Ding; Edward D Esplin; James M Ford; Jeremy Goecks; Sharmistha Ghosh; Joe W Gray; Justin Guinney; Sean E Hanlon; Shannon K Hughes; E Shelley Hwang; Christine A Iacobuzio-Donahue; Judit Jané-Valbuena; Bruce E Johnson; Ken S Lau; Tracy Lively; Sarah A Mazzilli; Dana Pe'er; Sandro Santagata; Alex K Shalek; Denis Schapiro; Michael P Snyder; Peter K Sorger; Avrum E Spira; Sudhir Srivastava; Kai Tan; Robert B West; Elizabeth H Williams; Human Tumor Atlas Network

doi:10.1016/j.cell.2020.03.053

The Human Tumor Atlas Network: Charting Tumor Transitions across Space and Time at Single-Cell Resolution

Cell. 2020 Apr 16;181(2):236-249. doi: 10.1016/j.cell.2020.03.053.

Authors

Orit Rozenblatt-Rosen¹, Aviv Regev², Philipp Oberdoerffer³, Tal Nawy⁴, Anna Hupalowska¹, Jennifer E Rood¹, Orr Ashenberg¹, Ethan Cerami⁵, Robert J Coffey⁶, Emek Demir⁷, Li Ding⁸, Edward D Esplin⁹, James M Ford¹⁰, Jeremy Goecks¹¹, Sharmistha Ghosh¹², Joe W Gray¹³, Justin Guinney¹⁴, Sean E Hanlon¹⁵, Shannon K Hughes³, E Shelley Hwang¹⁶, Christine A Iacobuzio-Donahue¹⁷, Judit Jané-Valbuena¹, Bruce E Johnson¹⁸, Ken S Lau⁶, Tracy Lively¹⁹, Sarah A Mazzilli²⁰, Dana Pe'er⁴, Sandro Santagata²¹, Alex K Shalek²², Denis Schapiro²³, Michael P Snyder⁹, Peter K Sorger²⁴, Avrum E Spira²⁵, Sudhir Srivastava¹², Kai Tan²⁶, Robert B West²⁷, Elizabeth H Williams²⁸; Human Tumor Atlas Network

Collaborators

Human Tumor Atlas Network:
Denise Aberle, Samuel I Achilefu, Foluso O Ademuyiwa, Andrew C Adey, Rebecca L Aft, Rachana Agarwal, Ruben A Aguilar, Fatemeh Alikarami, Viola Allaj, Christopher Amos, Robert A Anders, Michael R Angelo, Kristen Anton, Orr Ashenberg, Jon C Aster, Ozgun Babur, Amir Bahmani, Akshay Balsubramani, David Barrett, Jennifer Beane, Diane E Bender, Kathrin Bernt, Lynne Berry, Courtney B Betts, Julie Bletz, Katie Blise, Adrienne Boire, Genevieve Boland, Alexander Borowsky, Kristopher Bosse, Matthew Bott, Ed Boyden, James Brooks, Raphael Bueno, Erik A Burlingame, Qiuyin Cai, Joshua Campbell, Wagma Caravan, Ethan Cerami, Hassan Chaib, Joseph M Chan, Young Hwan Chang, Deyali Chatterjee, Ojasvi Chaudhary, Alyce A Chen, Bob Chen, Changya Chen, Chia-Hui Chen, Feng Chen, Yu-An Chen, Milan G Chheda, Koei Chin, Roxanne Chiu, Shih-Kai Chu, Rodrigo Chuaqui, Jaeyoung Chun, Luis Cisneros, Robert J Coffey, Graham A Colditz, Kristina Cole, Natalie Collins, Kevin Contrepois, Lisa M Coussens, Allison L Creason, Daniel Crichton, Christina Curtis, Tanja Davidsen, Sherri R Davies, Ino de Bruijn, Laura Dellostritto, Angelo De Marzo, Emek Demir, David G DeNardo, Dinh Diep, Li Ding, Sharon Diskin, Xengie Doan, Julia Drewes, Stephen Dubinett, Michael Dyer, Jacklynn Egger, Jennifer Eng, Barbara Engelhardt, Graham Erwin, Edward D Esplin, Laura Esserman, Alex Felmeister, Heidi S Feiler, Ryan C Fields, Stephen Fisher, Keith Flaherty, Jennifer Flournoy, James M Ford, Angelo Fortunato, Allison Frangieh, Jennifer L Frye, Robert S Fulton, Danielle Galipeau, Siting Gan, Jianjiong Gao, Long Gao, Peng Gao, Vianne R Gao, Tim Geiger, Ajit George, Gad Getz, Sharmistha Ghosh, Marios Giannakis, David L Gibbs, William E Gillanders, Jeremy Goecks, Simon P Goedegebuure, Alanna Gould, Kate Gowers, Joe W Gray, William Greenleaf, Jeremy Gresham, Jennifer L Guerriero, Tuhin K Guha, Alexander R Guimaraes, Justin Guinney, David Gutman, Nir Hacohen, Sean Hanlon, Casey R Hansen, Olivier Harismendy, Kathleen A Harris, Aaron Hata, Akimasa Hayashi, Cody Heiser, Karla Helvie, John M Herndon, Gilliam Hirst, Frank Hodi, Travis Hollmann, Aaron Horning, James J Hsieh, Shannon Hughes, Won Jae Huh, Stephen Hunger, Shelley E Hwang, Christine A Iacobuzio-Donahue, Heba Ijaz, Benjamin Izar, Connor A Jacobson, Samuel Janes, Judit Jané-Valbuena, Reyka G Jayasinghe, Lihua Jiang, Brett E Johnson, Bruce Johnson, Tao Ju, Humam Kadara, Klaus Kaestner, Jacob Kagan, Lukas Kalinke, Robert Keith, Aziz Khan, Warren Kibbe, Albert H Kim, Erika Kim, Junhyong Kim, Annette Kolodzie, Mateusz Kopytra, Eran Kotler, Robert Krueger, Kostyantyn Krysan, Anshul Kundaje, Uri Ladabaum, Blue B Lake, Huy Lam, Rozelle Laquindanum, Ken S Lau, Ashley M Laughney, Hayan Lee, Marc Lenburg, Carina Leonard, Ignaty Leshchiner, Rochelle Levy, Jerry Li, Christine G Lian, Kian-Huat Lim, Jia-Ren Lin, Yiyun Lin, Qi Liu, Ruiyang Liu, Tracy Lively, William J R Longabaugh, Teri Longacre, Cynthia X Ma, Mary Catherine Macedonia, Tyler Madison, Christopher A Maher, Anirban Maitra, Netta Makinen, Danika Makowski, Carlo Maley, Zoltan Maliga, Diego Mallo, John Maris, Nick Markham, Jeffrey Marks, Daniel Martinez, Robert J Mashl, Ignas Masilionais, Jennifer Mason, Joan Massagué, Pierre Massion, Marissa Mattar, Richard Mazurchuk, Linas Mazutis, Sarah A Mazzilli, Eliot T McKinley, Joshua F McMichael, Daniel Merrick, Matthew Meyerson, Julia R Miessner, Gordon B Mills, Meredith Mills, Suman B Mondal, Motomi Mori, Yuriko Mori, Elizabeth Moses, Yael Mosse, Jeremy L Muhlich, George F Murphy, Nicholas E Navin, Tal Nawy, Michel Nederlof, Reid Ness, Stephanie Nevins, Milen Nikolov, Ajit Johnson Nirmal, Garry Nolan, Edward Novikov, Philipp Oberdoerffer, Brendan O'Connell, Michael Offin, Stephen T Oh, Anastasiya Olson, Alex Ooms, Miguel Ossandon, Kouros Owzar, Swapnil Parmar, Tasleema Patel, Gary J Patti, Dana Pe'er, Itsik Pe'er, Tao Peng, Daniel Persson, Marvin Petty, Hanspeter Pfister, Kornelia Polyak, Kamyar Pourfarhangi, Sidharth V Puram, Qi Qiu, Álvaro Quintanal-Villalonga, Arjun Raj, Marisol Ramirez-Solano, Rumana Rashid, Ashley N Reeb, Aviv Regev, Mary Reid, Adam Resnick, Sheila M Reynolds, Jessica L Riesterer, Scott Rodig, Joseph T Roland, Sonia Rosenfield, Asaf Rotem, Sudipta Roy, Orit Rozenblatt-Rosen, Charles M Rudin, Marc D Ryser, Sandro Santagata, Maria Santi-Vicini, Kazuhito Sato, Denis Schapiro, Deborah Schrag, Nikolaus Schultz, Cynthia L Sears, Rosalie C Sears, Subrata Sen, Triparna Sen, Alex Shalek, Jeff Sheng, Quanhu Sheng, Kooresh I Shoghi, Martha J Shrubsole, Yu Shyr, Alexander B Sibley, Kiara Siex, Alan J Simmons, Dinah S Singer, Shamilene Sivagnanam, Michal Slyper, Michael P Snyder, Artem Sokolov, Sheng-Kwei Song, Peter K Sorger, Austin Southard-Smith, Avrum Spira, Sudhir Srivastava, Janet Stein, Phillip Storm, Elizabeth Stover, Siri H Strand, Timothy Su, Damir Sudar, Ryan Sullivan, Lea Surrey, Mario Suvà, Kai Tan, Nadezhda V Terekhanova, Luke Ternes, Lisa Thammavong, Guillaume Thibault, George V Thomas, Vésteinn Thorsson, Ellen Todres, Linh Tran, Madison Tyler, Yasin Uzun, Anil Vachani, Eliezer Van Allen, Simon Vandekar, Deborah J Veis, Sébastien Vigneau, Arastoo Vossough, Angela Waanders, Nikhil Wagle, Liang-Bo Wang, Michael C Wendl, Robert West, Elizabeth H Williams, Chi-Yun Wu, Hao Wu, Hung-Yi Wu, Matthew A Wyczalkowski, Yubin Xie, Xiaolu Yang, Clarence Yapp, Wenbao Yu, Yinyin Yuan, Dadong Zhang, Kun Zhang, Mianlei Zhang, Nancy Zhang, Yantian Zhang, Yanyan Zhao, Daniel Cui Zhou, Zilu Zhou, Houxiang Zhu, Qin Zhu, Xiangzhu Zhu, Yuankun Zhu, Xiaowei Zhuang

Affiliations

¹ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
² Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA; Koch Institute for Integrative Cancer Research, Department of Biology, MIT, Cambridge, MA 02139, USA. Electronic address: [email protected].
³ Division of Cancer Biology, National Cancer Institute, NIH, Rockville, MD 20850, USA.
⁴ Computational and Systems Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
⁵ Department of Data Sciences, Dana-Farber Cancer Institute, Boston, MA 02215, USA.
⁶ Department of Medicine, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
⁷ Department of Molecular and Medical Genetics, School of Medicine, Oregon Health & Science University, Portland, OR 97239, USA.
⁸ Department of Medicine, McDonnell Genome Institute, and Siteman Cancer Center, Washington University in St. Louis, Saint Louis, MO 63108, USA.
⁹ Department of Genetics, Stanford School of Medicine, Stanford, CA 94305, USA.
¹⁰ Department of Genetics, Stanford School of Medicine, Stanford, CA 94305, USA; Department of Medicine, Oncology Division, Stanford University School of Medicine, Stanford, CA 94305, USA.
¹¹ Computational Biology Program, Oregon Health and Science University, OR 97201, USA.
¹² Division of Cancer Prevention, National Cancer Institute, NIH, Rockville, MD 20850, USA.
¹³ Center for Spatial Systems Biomedicine, Department of Biomedical Engineering, Oregon Health & Science University, Portland, OR 97201, USA.
¹⁴ Sage Bionetworks, Seattle, WA 98121, USA; Biomedical Informatics and Medical Education, University of Washington, Seattle, WA 98195, USA.
¹⁵ Center for Strategic Scientific Initiatives, National Cancer Institute, NIH, Bethesda, MD 20892, USA.
¹⁶ Department of Surgery, Duke University School of Medicine, Durham, NC 27710, USA; Women's Cancer Program, Duke Cancer Institute, Duke University, Durham, NC 27710, USA.
¹⁷ David M. Rubenstein Center for Pancreatic Cancer Research, Human Oncology and Pathogenesis Program, and Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
¹⁸ Department of Medical Oncology and Department of Medicine, Dana-Farber Cancer Institute and Brigham and Women's Hospital, 450 Brookline Avenue, Boston, MA 02215, USA.
¹⁹ Division of Cancer Treatment and Diagnosis, National Cancer Institute, NIH, Rockville, MD 20850, USA.
²⁰ Department of Medicine, Division of Computational Biomedicine, Boston University School of Medicine, Boston, MA 02118, USA.
²¹ Ludwig Center for Cancer Research and Laboratory of Systems Pharmacology, Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA; Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
²² Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Institute for Medical Engineering and Science, Department of Chemistry, and Koch Institute for Integrative Cancer Research, MIT, Cambridge, MA 02139, USA; Ragon Institute of Massachusetts General Hospital, MIT and Harvard University, Cambridge, MA 02139, USA; Division of Health Sciences and Technology, Harvard Medical School, Boston, MA 02115, USA; Department of Immunology, Massachusetts General Hospital, Boston, MA 02114, USA.
²³ Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Ludwig Center for Cancer Research and Laboratory of Systems Pharmacology, Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA.
²⁴ Ludwig Center for Cancer Research and Laboratory of Systems Pharmacology, Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA.
²⁵ Department of Medicine, Division of Computational Biomedicine, Boston University School of Medicine, Boston, MA 02118, USA; Johnson & Johnson, Cambridge, MA 02142, USA.
²⁶ Division of Oncology and Center for Childhood Cancer Research, 4004 CTRB, Children's Hospital of Philadelphia, 3501 Civic Center Boulevard, Philadelphia, PA 19104, USA; Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
²⁷ Department of Pathology, Stanford School of Medicine, Stanford, CA 94305, USA.
²⁸ Department of Data Sciences, Dana-Farber Cancer Institute, Boston, MA 02215, USA; Present address: Foundation Medicine, Cambridge, MA 02141, USA.

Abstract

Crucial transitions in cancer-including tumor initiation, local expansion, metastasis, and therapeutic resistance-involve complex interactions between cells within the dynamic tumor ecosystem. Transformative single-cell genomics technologies and spatial multiplex in situ methods now provide an opportunity to interrogate this complexity at unprecedented resolution. The Human Tumor Atlas Network (HTAN), part of the National Cancer Institute (NCI) Cancer Moonshot Initiative, will establish a clinical, experimental, computational, and organizational framework to generate informative and accessible three-dimensional atlases of cancer transitions for a diverse set of tumor types. This effort complements both ongoing efforts to map healthy organs and previous large-scale cancer genomics approaches focused on bulk sequencing at a single point in time. Generating single-cell, multiparametric, longitudinal atlases and integrating them with clinical outcomes should help identify novel predictive biomarkers and features as well as therapeutically relevant cell types, cell states, and cellular interactions across transitions. The resulting tumor atlases should have a profound impact on our understanding of cancer biology and have the potential to improve cancer detection, prevention, and therapeutic discovery for better precision-medicine treatments of cancer patients and those at risk for cancer.

Keywords: AI; Cancer Moonshot; Human Tumor Atlas; cancer transitions; data integration; data visualization; metastasis; pre-cancer; resistance; single-cell genomics; spatial genomics; spatial imaging; tumor.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Review

MeSH terms

Atlases as Topic
Cell Transformation, Neoplastic / metabolism*
Cell Transformation, Neoplastic / pathology
Genomics / methods
Humans
Neoplasms / metabolism*
Precision Medicine / methods
Single-Cell Analysis / methods
Tumor Microenvironment / physiology*

Abstract

Publication types

MeSH terms

Grants and funding