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

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

Human Tumor Atlas Network

Pediatrics

Research output: Contribution to journal › Review article › peer-review

321 Scopus citations

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. The Human Tumor Atlas Network outlines their ambitious plan to generate 3D, single-cell, multiparametric, and longitudinal maps of diverse tumor types.

Original language	English (US)
Pages (from-to)	236-249
Number of pages	14
Journal	Cell
Volume	181
Issue number	2
DOIs	https://doi.org/10.1016/j.cell.2020.03.053
State	Published - Apr 16 2020

Funding

We thank Jennifer Beane-Ebel for critical reading of the manuscript. This work is supported by the National Cancer Institute Cancer Moonshot under awards U24 CA233243 , U2C CA233195 , U2C CA233238 , U2C CA233254 , U2C CA233262 , U2C CA233280 , U2C CA233284 , U2C CA233285 , U2C CA233291 , U2C CA233303 , and U2C CA233311 . The Lung Pre-Cancer Atlas is partly supported by funding from Janssen Research & Development LLC (principal investigator [PI]: S.A.M.), Johnson & Johnson (PI: S.A.M.), and a Stand Up To Cancer (SU2C)-LUNGevity-American Lung Association Lung Cancer Interception Dream Team Translational Cancer Research Grant ( SU2C-AACR-DT23-17 to S.M.D. and A.E.S.). SU2C is a division of the Entertainment Industry Foundation. Research grants are administered by the American Association for Cancer Research, the scientific partner of SU2C. The Human Tumor Atlas Pilot Project is supported by federal funds from the NIH National Cancer Institute (task order no. HHSN261100039 under contract no. HHSN261201500003I ). A.R. is an investigator of the Howard Hughes Medical Institute. A.R. and O.R.R. are supported by the Klarman Cell Observatory at the Broad Institute . D.S. is funded by an Early Postdoc Mobility fellowship (no. P2ZHP3_181475 ) from the Swiss National Science Foundation . We thank Jennifer Beane-Ebel for critical reading of the manuscript. This work is supported by the National Cancer Institute Cancer Moonshot under awards U24 CA233243, U2C CA233195, U2C CA233238, U2C CA233254, U2C CA233262, U2C CA233280, U2C CA233284, U2C CA233285, U2C CA233291, U2C CA233303, and U2C CA233311. The Lung Pre-Cancer Atlas is partly supported by funding from Janssen Research & Development LLC (principal investigator [PI]: S.A.M.), Johnson & Johnson (PI: S.A.M.), and a Stand Up To Cancer (SU2C)-LUNGevity-American Lung Association Lung Cancer Interception Dream Team Translational Cancer Research Grant (SU2C-AACR-DT23-17 to S.M.D. and A.E.S.). SU2C is a division of the Entertainment Industry Foundation. Research grants are administered by the American Association for Cancer Research, the scientific partner of SU2C. The Human Tumor Atlas Pilot Project is supported by federal funds from the NIH National Cancer Institute (task order no. HHSN261100039 under contract no. HHSN261201500003I). A.R. is an investigator of the Howard Hughes Medical Institute. A.R. and O.R.R. are supported by the Klarman Cell Observatory at the Broad Institute. D.S. is funded by an Early Postdoc Mobility fellowship (no. P2ZHP3_181475) from the Swiss National Science Foundation. A.R. is a founder of and equity holder in Celsius Therapeutics, an equity holder in Immunitas Therapeutics, and a scientific advisory board (SAB) member of Syros Pharmaceuticals, ThermoFisher Scientific, Asimov, and NeoGene Therapeutics. A.K.S. has received compensation for consulting for and being on the SAB of Honeycomb Biotechnologies, Cellarity, Cogen Therapeutics, and Dahlia Biosciences. O.R.R. A.K.S. and A.R. are co-inventors on patent applications filed by the Broad Institute to inventions relating to single-cell genomics, such as in PCT/US2018/060860 and US provisional application no. 62/745,259. J.W.G. has licensed technologies to Abbott Diagnostics and Danaher and has ownership positions in PDX Pharmaceuticals and Convergent Genomics. He serves as an advisor to New Leaf Ventures and receives private-sector research support from Zeiss, ThermoFisher, Danaher, Micron, PDX Pharmaceuticals, and Quantitative Imaging. C.I.D. receives research support from Bristol-Myers Squibb. S.S. is a consultant for RareCyte, Inc. A.S. is an employee of Johnson & Johnson. S.A.M. has commercial research grants from Johnson & Johnson. P.K.S. is a member of the SAB or board of directors of and has equity in Glencoe Software and RareCyte Inc. which create software and instruments for tissue imaging.

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

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.cell.2020.03.053

Cite this

@article{37e892961f8e43dab4479b7fbe9338e7,

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

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. The Human Tumor Atlas Network outlines their ambitious plan to generate 3D, single-cell, multiparametric, and longitudinal maps of diverse tumor types.",

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",

author = "{Human Tumor Atlas Network} and Orit Rozenblatt-Rosen and Aviv Regev and Philipp Oberdoerffer and Tal Nawy and Anna Hupalowska and Rood, {Jennifer E.} and Orr Ashenberg and Ethan Cerami and Coffey, {Robert J.} and Emek Demir and Li Ding and Esplin, {Edward D.} and Ford, {James M.} and Jeremy Goecks and Sharmistha Ghosh and Gray, {Joe W.} and Justin Guinney and Hanlon, {Sean E.} and Hughes, {Shannon K.} and Hwang, {E. Shelley} and Iacobuzio-Donahue, {Christine A.} and Judit Jan{\'e}-Valbuena and Johnson, {Bruce E.} and Lau, {Ken S.} and Tracy Lively and Mazzilli, {Sarah A.} and Dana Pe'er and Sandro Santagata and Shalek, {Alex K.} and Denis Schapiro and Snyder, {Michael P.} and Sorger, {Peter K.} and Spira, {Avrum E.} and Sudhir Srivastava and Kai Tan and West, {Robert B.} and Williams, {Elizabeth H.} and Denise Aberle and Achilefu, {Samuel I.} and Ademuyiwa, {Foluso O.} and Adey, {Andrew C.} and Aft, {Rebecca L.} and Rachana Agarwal and Aguilar, {Ruben A.} and Fatemeh Alikarami and Viola Allaj and Christopher Amos and Anders, {Robert A.} and Angelo, {Michael R.} and Angela Waanders",

note = "Publisher Copyright: {\textcopyright} 2020",

year = "2020",

month = apr,

day = "16",

doi = "10.1016/j.cell.2020.03.053",

language = "English (US)",

volume = "181",

pages = "236--249",

journal = "Cell",

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T1 - The Human Tumor Atlas Network

T2 - Charting Tumor Transitions across Space and Time at Single-Cell Resolution

AU - Human Tumor Atlas Network

AU - Rozenblatt-Rosen, Orit

AU - Regev, Aviv

AU - Oberdoerffer, Philipp

AU - Nawy, Tal

AU - Hupalowska, Anna

AU - Rood, Jennifer E.

AU - Ashenberg, Orr

AU - Cerami, Ethan

AU - Coffey, Robert J.

AU - Demir, Emek

AU - Ding, Li

AU - Esplin, Edward D.

AU - Ford, James M.

AU - Goecks, Jeremy

AU - Ghosh, Sharmistha

AU - Gray, Joe W.

AU - Guinney, Justin

AU - Hanlon, Sean E.

AU - Hughes, Shannon K.

AU - Hwang, E. Shelley

AU - Iacobuzio-Donahue, Christine A.

AU - Jané-Valbuena, Judit

AU - Johnson, Bruce E.

AU - Lau, Ken S.

AU - Lively, Tracy

AU - Mazzilli, Sarah A.

AU - Pe'er, Dana

AU - Santagata, Sandro

AU - Shalek, Alex K.

AU - Schapiro, Denis

AU - Snyder, Michael P.

AU - Sorger, Peter K.

AU - Spira, Avrum E.

AU - Srivastava, Sudhir

AU - Tan, Kai

AU - West, Robert B.

AU - Williams, Elizabeth H.

AU - Aberle, Denise

AU - Achilefu, Samuel I.

AU - Ademuyiwa, Foluso O.

AU - Adey, Andrew C.

AU - Aft, Rebecca L.

AU - Agarwal, Rachana

AU - Aguilar, Ruben A.

AU - Alikarami, Fatemeh

AU - Allaj, Viola

AU - Amos, Christopher

AU - Anders, Robert A.

AU - Angelo, Michael R.

AU - Waanders, Angela

PY - 2020/4/16

Y1 - 2020/4/16

N2 - 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. The Human Tumor Atlas Network outlines their ambitious plan to generate 3D, single-cell, multiparametric, and longitudinal maps of diverse tumor types.

AB - 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. The Human Tumor Atlas Network outlines their ambitious plan to generate 3D, single-cell, multiparametric, and longitudinal maps of diverse tumor types.

KW - AI

KW - Cancer Moonshot

KW - Human Tumor Atlas

KW - cancer transitions

KW - data integration

KW - data visualization

KW - metastasis

KW - pre-cancer

KW - resistance

KW - single-cell genomics

KW - spatial genomics

KW - spatial imaging

KW - tumor

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DO - 10.1016/j.cell.2020.03.053

M3 - Review article

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AN - SCOPUS:85083116634

SN - 0092-8674

VL - 181

SP - 236

EP - 249

JO - Cell

JF - Cell

IS - 2

ER -

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

Abstract

Funding

Keywords

ASJC Scopus subject areas

UN SDGs

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