Skip to main content
bioRxiv
  • Home
  • About
  • Submit
  • ALERTS / RSS
Advanced Search
New Results

Immune and malignant cell phenotypes of ovarian cancer are determined by distinct mutational processes

View ORCID ProfileIgnacio Vázquez-García, View ORCID ProfileFlorian Uhlitz, Nicholas Ceglia, View ORCID ProfileJamie L.P. Lim, View ORCID ProfileMichelle Wu, Neeman Mohibullah, View ORCID ProfileArvin Eric B. Ruiz, View ORCID ProfileKevin M. Boehm, Viktoria Bojilova, Christopher J. Fong, View ORCID ProfileTyler Funnell, Diljot Grewal, Eliyahu Havasov, Samantha Leung, Arfath Pasha, View ORCID ProfileDruv M. Patel, Maryam Pourmaleki, Nicole Rusk, View ORCID ProfileHongyu Shi, Rami Vanguri, View ORCID ProfileMarc J. Williams, View ORCID ProfileAllen W. Zhang, Vance Broach, Dennis Chi, Arnaud Da Cruz Paula, Ginger J. Gardner, Sarah H. Kim, View ORCID ProfileMatthew Lennon, View ORCID ProfileKara Long Roche, Yukio Sonoda, Oliver Zivanovic, View ORCID ProfileRitika Kundra, Agnes Viale, View ORCID ProfileFatemeh N. Derakhshan, View ORCID ProfileLuke Geneslaw, Ana Maroldi, Rahelly Nunez, Fresia Pareja, Anthe Stylianou, View ORCID ProfileMahsa Vahdatinia, Yonina Bykov, View ORCID ProfileRachel N. Grisham, Ying L. Liu, View ORCID ProfileYulia Lakhman, View ORCID ProfileInes Nikolovski, Daniel Kelly, View ORCID ProfileJianjiong Gao, Andrea Schietinger, View ORCID ProfileTravis J. Hollmann, Samuel F. Bakhoum, Robert A. Soslow, Lora H. Ellenson, Nadeem R. Abu-Rustum, Carol Aghajanian, View ORCID ProfileClaire F. Friedman, View ORCID ProfileAndrew McPherson, Britta Weigelt, View ORCID ProfileDmitriy Zamarin, View ORCID ProfileSohrab P. Shah
doi: https://doi.org/10.1101/2021.08.24.454519
Ignacio Vázquez-García
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Ignacio Vázquez-García
Florian Uhlitz
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Florian Uhlitz
Nicholas Ceglia
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jamie L.P. Lim
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Jamie L.P. Lim
Michelle Wu
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Michelle Wu
Neeman Mohibullah
3Integrated Genomics Operation, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Arvin Eric B. Ruiz
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Arvin Eric B. Ruiz
Kevin M. Boehm
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Kevin M. Boehm
Viktoria Bojilova
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Christopher J. Fong
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tyler Funnell
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Tyler Funnell
Diljot Grewal
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Eliyahu Havasov
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Samantha Leung
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Arfath Pasha
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Druv M. Patel
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Druv M. Patel
Maryam Pourmaleki
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nicole Rusk
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hongyu Shi
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Hongyu Shi
Rami Vanguri
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Marc J. Williams
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Marc J. Williams
Allen W. Zhang
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Allen W. Zhang
Vance Broach
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Dennis Chi
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Arnaud Da Cruz Paula
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ginger J. Gardner
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sarah H. Kim
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Matthew Lennon
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Matthew Lennon
Kara Long Roche
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Kara Long Roche
Yukio Sonoda
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Oliver Zivanovic
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ritika Kundra
5Marie-Josée and Henry R. Kravis Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Ritika Kundra
Agnes Viale
5Marie-Josée and Henry R. Kravis Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Fatemeh N. Derakhshan
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Fatemeh N. Derakhshan
Luke Geneslaw
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Luke Geneslaw
Ana Maroldi
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rahelly Nunez
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Fresia Pareja
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Anthe Stylianou
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Mahsa Vahdatinia
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Mahsa Vahdatinia
Yonina Bykov
6Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rachel N. Grisham
6Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
12Weill Cornell Medical Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Rachel N. Grisham
Ying L. Liu
6Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yulia Lakhman
7Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Yulia Lakhman
Ines Nikolovski
7Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Ines Nikolovski
Daniel Kelly
8Department of Information Systems, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jianjiong Gao
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
5Marie-Josée and Henry R. Kravis Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Jianjiong Gao
Andrea Schietinger
9Immunology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Travis J. Hollmann
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Travis J. Hollmann
Samuel F. Bakhoum
10Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
11Department of Radiation Oncology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert A. Soslow
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lora H. Ellenson
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nadeem R. Abu-Rustum
2Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
12Weill Cornell Medical Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Carol Aghajanian
6Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Claire F. Friedman
6Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
12Weill Cornell Medical Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Claire F. Friedman
Andrew McPherson
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Andrew McPherson
Britta Weigelt
4Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Dmitriy Zamarin
6Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
12Weill Cornell Medical Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Dmitriy Zamarin
  • For correspondence: shahs3@mskcc.org zamarind@mskcc.org
Sohrab P. Shah
1Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Sohrab P. Shah
  • For correspondence: shahs3@mskcc.org zamarind@mskcc.org
  • Abstract
  • Full Text
  • Info/History
  • Metrics
  • Supplementary material
  • Preview PDF
Loading

ABSTRACT

High-grade serous ovarian cancer (HGSOC) is an archetypal cancer of genomic instability patterned by distinct mutational processes, intratumoral heterogeneity and intraperitoneal spread. We investigated determinants of immune recognition and evasion in HGSOC to elucidate co- evolutionary processes underlying malignant progression and tumor immunity. Mutational processes and anatomic sites of tumor foci were key determinants of tumor microenvironment cellular phenotypes, inferred from whole genome sequencing, single-cell RNA sequencing, digital histopathology and multiplexed immunofluorescence of 160 tumor sites from 42 treatment-naive HGSOC patients. Homologous recombination-deficient (HRD)-Dup (BRCA1 mutant-like) and HRD- Del (BRCA2 mutant-like) tumors harbored increased neoantigen burden, inflammatory signaling and ongoing immunoediting, reflected in loss of HLA diversity and tumor infiltration with highly- differentiated dysfunctional CD8+ T cells. Foldback inversion (FBI, non-HRD) tumors exhibited elevated TGFβ signaling and immune exclusion, with predominantly naive/stem-like and memory T cells. Our findings implicate distinct immune resistance mechanisms across HGSOC subtypes which can inform future immunotherapeutic strategies.

HIGHLIGHTS

  • Multi-region, multi-modal profiling of malignant and immune cell phenotypes in ovarian cancer

  • Anatomic site specificity is a determinant of cancer cell and intratumoral immune phenotypes

  • Tumor mutational processes impact mechanisms of immune control and immune evasion

  • Spatial topology of HR-deficient tumors is defined by immune interactions absent from immune inert HR-proficient subtypes

Competing Interest Statement

SPS is a consultant and shareholder of Canexia Health Inc. DZ reports research funding to MSK from AstraZeneca, Genentech, and Plexxikon; personal fees from Synlogic Therapeutics, Hookipa Biotech, Agenus, Synthekine, Memgen, Mana Therapeutics, Tessa Therapeutics, and Xencor; stock options from Accurius, Calidi Biotherapeutics, and Immunos. DZ is an inventor on a patent concerning the use of Newcastle Disease Virus as a cancer therapeutic, licensed to Merck. CFF reports research funding to the institution from Merck, AstraZeneca, Genentech, Bristol Myer Squibb, Taiho and Seattle Genetics; uncompensated membership of a scientific advisory board for Merck and Genentech; and is a consultant for OncLive, Aptitude Health, and Seattle Genetics, all outside the scope of this manuscript. CA reports grants from Clovis, Genentech, AbbVie and AstraZeneca, personal fees from Tesaro, Eisai/Merck, Mersana Therapeutics, Roche/Genentech, Abbvie, AstraZeneca/Merck and Repare Therapeutics, outside the submitted work. NRAR reports grants to MSK from Stryker/Novadaq and GRAIL, outside the submitted work. DSC is on the medical advisory board of Apyx Medical Co, Verthermia Acquio Inc and Biom'up, and is a stockholder of Intuitive Surgical Inc and TransEnterix Inc. RNG reports funding from GSK, Mateon Therapeutics, Regeneron, Clovis, Context Therapeutics, EMD Serono, MCM Education, OncLive, Aptitude Health and Prime Oncology, outside this work. YLL reports research funding from AstraZeneca and GSK/Tesaro outside this work. YL is a shareholder of Y-mAbs Therapeutics Inc. TJH receives research funding from Bristol Myers Squibb, Calico Labs and the Parker Institute for Cancer Immunotherapy. SFB owns equity in, receives compensation from, and serves as a consultant and the Scientific Advisory Board and Board of Directors of Volastra Therapeutics Inc. SFB has also consulted for Sanofi, received sponsored travel from the Prostate Cancer Foundation, and both travel and compensation from Cancer Research UK. BW reports ad hoc membership of the scientific advisory board of Repare Therapeutics, outside the submitted work.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
Back to top
PreviousNext
Posted August 25, 2021.
Download PDF

Supplementary Material

Email

Thank you for your interest in spreading the word about bioRxiv.

NOTE: Your email address is requested solely to identify you as the sender of this article.

Enter multiple addresses on separate lines or separate them with commas.
Immune and malignant cell phenotypes of ovarian cancer are determined by distinct mutational processes
(Your Name) has forwarded a page to you from bioRxiv
(Your Name) thought you would like to see this page from the bioRxiv website.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Immune and malignant cell phenotypes of ovarian cancer are determined by distinct mutational processes
Ignacio Vázquez-García, Florian Uhlitz, Nicholas Ceglia, Jamie L.P. Lim, Michelle Wu, Neeman Mohibullah, Arvin Eric B. Ruiz, Kevin M. Boehm, Viktoria Bojilova, Christopher J. Fong, Tyler Funnell, Diljot Grewal, Eliyahu Havasov, Samantha Leung, Arfath Pasha, Druv M. Patel, Maryam Pourmaleki, Nicole Rusk, Hongyu Shi, Rami Vanguri, Marc J. Williams, Allen W. Zhang, Vance Broach, Dennis Chi, Arnaud Da Cruz Paula, Ginger J. Gardner, Sarah H. Kim, Matthew Lennon, Kara Long Roche, Yukio Sonoda, Oliver Zivanovic, Ritika Kundra, Agnes Viale, Fatemeh N. Derakhshan, Luke Geneslaw, Ana Maroldi, Rahelly Nunez, Fresia Pareja, Anthe Stylianou, Mahsa Vahdatinia, Yonina Bykov, Rachel N. Grisham, Ying L. Liu, Yulia Lakhman, Ines Nikolovski, Daniel Kelly, Jianjiong Gao, Andrea Schietinger, Travis J. Hollmann, Samuel F. Bakhoum, Robert A. Soslow, Lora H. Ellenson, Nadeem R. Abu-Rustum, Carol Aghajanian, Claire F. Friedman, Andrew McPherson, Britta Weigelt, Dmitriy Zamarin, Sohrab P. Shah
bioRxiv 2021.08.24.454519; doi: https://doi.org/10.1101/2021.08.24.454519
Digg logo Reddit logo Twitter logo Facebook logo Google logo LinkedIn logo Mendeley logo
Citation Tools
Immune and malignant cell phenotypes of ovarian cancer are determined by distinct mutational processes
Ignacio Vázquez-García, Florian Uhlitz, Nicholas Ceglia, Jamie L.P. Lim, Michelle Wu, Neeman Mohibullah, Arvin Eric B. Ruiz, Kevin M. Boehm, Viktoria Bojilova, Christopher J. Fong, Tyler Funnell, Diljot Grewal, Eliyahu Havasov, Samantha Leung, Arfath Pasha, Druv M. Patel, Maryam Pourmaleki, Nicole Rusk, Hongyu Shi, Rami Vanguri, Marc J. Williams, Allen W. Zhang, Vance Broach, Dennis Chi, Arnaud Da Cruz Paula, Ginger J. Gardner, Sarah H. Kim, Matthew Lennon, Kara Long Roche, Yukio Sonoda, Oliver Zivanovic, Ritika Kundra, Agnes Viale, Fatemeh N. Derakhshan, Luke Geneslaw, Ana Maroldi, Rahelly Nunez, Fresia Pareja, Anthe Stylianou, Mahsa Vahdatinia, Yonina Bykov, Rachel N. Grisham, Ying L. Liu, Yulia Lakhman, Ines Nikolovski, Daniel Kelly, Jianjiong Gao, Andrea Schietinger, Travis J. Hollmann, Samuel F. Bakhoum, Robert A. Soslow, Lora H. Ellenson, Nadeem R. Abu-Rustum, Carol Aghajanian, Claire F. Friedman, Andrew McPherson, Britta Weigelt, Dmitriy Zamarin, Sohrab P. Shah
bioRxiv 2021.08.24.454519; doi: https://doi.org/10.1101/2021.08.24.454519

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Subject Area

  • Cancer Biology
Subject Areas
All Articles
  • Animal Behavior and Cognition (3514)
  • Biochemistry (7365)
  • Bioengineering (5342)
  • Bioinformatics (20318)
  • Biophysics (10041)
  • Cancer Biology (7773)
  • Cell Biology (11348)
  • Clinical Trials (138)
  • Developmental Biology (6450)
  • Ecology (9979)
  • Epidemiology (2065)
  • Evolutionary Biology (13354)
  • Genetics (9370)
  • Genomics (12607)
  • Immunology (7724)
  • Microbiology (19087)
  • Molecular Biology (7459)
  • Neuroscience (41134)
  • Paleontology (300)
  • Pathology (1235)
  • Pharmacology and Toxicology (2142)
  • Physiology (3177)
  • Plant Biology (6878)
  • Scientific Communication and Education (1276)
  • Synthetic Biology (1900)
  • Systems Biology (5328)
  • Zoology (1091)