Human interpretable grammar encodes multicellular systems biology models to democratize virtual cell laboratories

Jeanette A I Johnson¹, Daniel R Bergman², Heber L Rocha³, David L Zhou⁴, Eric Cramer⁵, Ian C Mclean⁵, Yoseph W Dance⁶, Max Booth⁷, Zachary Nicholas⁸, Tamara Lopez-Vidal⁷, Atul Deshpande⁹, Randy Heiland³, Elmar Bucher³, Fatemeh Shojaeian¹⁰, Matthew Dunworth¹¹, André Forjaz¹², Michael Getz³, Inês Godet¹³, Furkan Kurtoglu³, Melissa Lyman¹⁴, John Metzcar¹⁵, Jacob T Mitchell¹⁶, Andrew Raddatz¹⁷, Jacobo Solorzano¹⁸, Aneequa Sundus³, Yafei Wang³, David G DeNardo¹⁹, Andrew J Ewald²⁰, Daniele M Gilkes²¹, Luciane T Kagohara¹⁴, Ashley L Kiemen²², Elizabeth D Thompson¹⁰, Denis Wirtz²³, Laura D Wood²⁴, Pei-Hsun Wu²⁵, Neeha Zaidi¹⁴, Lei Zheng²⁶, Jacquelyn W Zimmerman¹⁴, Jude M Phillip²⁷, Elizabeth M Jaffee¹⁴, Joe W Gray²⁸, Lisa M Coussens²⁹, Young Hwan Chang²⁸, Laura M Heiser²⁸, Genevieve L Stein-O'Brien³⁰, Elana J Fertig³¹, Paul Macklin³²

Affiliations

¹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA; Marlene & Stuart Greenbaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, USA.
² Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Pharmacology, Physiology, and Drug Development, University of Maryland School of Medicine, Baltimore, MD, USA; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA; Marlene & Stuart Greenbaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, USA; University of Maryland Institute of Health Computing, University of Maryland School of Medicine, Baltimore, MD, USA.
³ Department of Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA.
⁴ Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA.
⁵ Department of Biomedical Engineering, Oregon Health & Science University, Portland, OR, USA.
⁶ Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA.
⁷ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA.
⁸ Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA.
⁹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Electrical and Computer Engineering, Johns Hopkins University, Baltimore, MD, USA; Data Science and AI Institute, Johns Hopkins University, Baltimore, MD, USA.
¹⁰ Department of Pathology, Johns Hopkins University, Baltimore, MD, USA.
¹¹ Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
¹² Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA.
¹³ Memorial Sloan Kettering Cancer Center, New York, NY, USA.
¹⁴ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA.
¹⁵ Department of Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA; Department of Informatics, Indiana University, Bloomington, IN, USA.
¹⁶ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA.
¹⁷ Department of Biomedical Engineering, Georgia Institute of Technology, Emory University, Atlanta, GA, USA.
¹⁸ Centre de Recherches en Cancerologie de Toulouse, Toulouse, France.
¹⁹ Department of Medicine, Washington University Saint Louis, St. Louis, MO, USA.
²⁰ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Giovannis Institute for Translational Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²¹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA.
²² Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Pathology, Johns Hopkins University, Baltimore, MD, USA.
²³ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Pathology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA; Department of Materials Science and Engineering, Johns Hopkins University, Baltimore, MD, USA.
²⁴ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Department of Pathology, Johns Hopkins University, Baltimore, MD, USA.
²⁵ Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA.
²⁶ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Mays Cancer Center, University of Texas Health, San Antonio, TX, USA; MD Anderson Cancer Center, San Antonio, TX, USA.
²⁷ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA; Translational Tissue Engineering Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²⁸ Department of Biomedical Engineering, Oregon Health & Science University, Portland, OR, USA; Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA.
²⁹ Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA; Department of Cell, Developmental and Cancer Biology, Oregon Health & Science University, Portland, OR, USA.
³⁰ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA; Data Science and AI Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, USA. Electronic address: gsteinobrien@jmhi.edu.
³¹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA; Marlene & Stuart Greenbaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, USA; University of Maryland Institute of Health Computing, University of Maryland School of Medicine, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Data Science and AI Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Applied Mathematics and Statistics, Johns Hopkins University, Baltimore, MD, USA; Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, USA. Electronic address: ejfertig@som.umaryland.edu.
³² Department of Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA. Electronic address: macklinp@iu.edu.

PMID: 40713951
DOI: 10.1016/j.cell.2025.06.048

Free article

Human interpretable grammar encodes multicellular systems biology models to democratize virtual cell laboratories

Jeanette A I Johnson et al. Cell. 2025.

Free article

. 2025 Aug 21;188(17):4711-4733.e37.

doi: 10.1016/j.cell.2025.06.048. Epub 2025 Jul 26.

Authors

Affiliations

¹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA; Marlene & Stuart Greenbaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, USA.
² Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Pharmacology, Physiology, and Drug Development, University of Maryland School of Medicine, Baltimore, MD, USA; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA; Marlene & Stuart Greenbaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, USA; University of Maryland Institute of Health Computing, University of Maryland School of Medicine, Baltimore, MD, USA.
³ Department of Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA.
⁴ Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA.
⁵ Department of Biomedical Engineering, Oregon Health & Science University, Portland, OR, USA.
⁶ Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA.
⁷ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA.
⁸ Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA.
⁹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Electrical and Computer Engineering, Johns Hopkins University, Baltimore, MD, USA; Data Science and AI Institute, Johns Hopkins University, Baltimore, MD, USA.
¹⁰ Department of Pathology, Johns Hopkins University, Baltimore, MD, USA.
¹¹ Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
¹² Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA.
¹³ Memorial Sloan Kettering Cancer Center, New York, NY, USA.
¹⁴ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA.
¹⁵ Department of Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA; Department of Informatics, Indiana University, Bloomington, IN, USA.
¹⁶ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA.
¹⁷ Department of Biomedical Engineering, Georgia Institute of Technology, Emory University, Atlanta, GA, USA.
¹⁸ Centre de Recherches en Cancerologie de Toulouse, Toulouse, France.
¹⁹ Department of Medicine, Washington University Saint Louis, St. Louis, MO, USA.
²⁰ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Giovannis Institute for Translational Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²¹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA.
²² Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Pathology, Johns Hopkins University, Baltimore, MD, USA.
²³ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Pathology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA; Department of Materials Science and Engineering, Johns Hopkins University, Baltimore, MD, USA.
²⁴ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Department of Pathology, Johns Hopkins University, Baltimore, MD, USA.
²⁵ Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA.
²⁶ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Mays Cancer Center, University of Texas Health, San Antonio, TX, USA; MD Anderson Cancer Center, San Antonio, TX, USA.
²⁷ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Institute for NanoBioTechnology, Johns Hopkins University, Baltimore, MD, USA; Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD, USA; Translational Tissue Engineering Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²⁸ Department of Biomedical Engineering, Oregon Health & Science University, Portland, OR, USA; Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA.
²⁹ Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA; Department of Cell, Developmental and Cancer Biology, Oregon Health & Science University, Portland, OR, USA.
³⁰ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA; Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA; Data Science and AI Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, USA. Electronic address: gsteinobrien@jmhi.edu.
³¹ Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USA; Convergence Institute, Johns Hopkins University, Baltimore, MD, USA; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA; Marlene & Stuart Greenbaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, USA; University of Maryland Institute of Health Computing, University of Maryland School of Medicine, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Data Science and AI Institute, Johns Hopkins University, Baltimore, MD, USA; Department of Applied Mathematics and Statistics, Johns Hopkins University, Baltimore, MD, USA; Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, USA. Electronic address: ejfertig@som.umaryland.edu.
³² Department of Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA. Electronic address: macklinp@iu.edu.

PMID: 40713951
DOI: 10.1016/j.cell.2025.06.048

Abstract

Cells interact as dynamically evolving ecosystems. While recent single-cell and spatial multi-omics technologies quantify individual cell characteristics, predicting their evolution requires mathematical modeling. We propose a conceptual framework-a cell behavior hypothesis grammar-that uses natural language statements (cell rules) to create mathematical models. This enables systematic integration of biological knowledge and multi-omics data to generate in silico models, enabling virtual "thought experiments" that test and expand our understanding of multicellular systems and generate new testable hypotheses. This paper motivates and describes the grammar, offers a reference implementation, and demonstrates its use in developing both de novo mechanistic models and those informed by multi-omics data. We show its potential through examples in cancer and its broader applicability in simulating brain development. This approach bridges biological, clinical, and systems biology research for mathematical modeling at scale, allowing the community to predict emergent multicellular behavior.

Keywords: agent-based modeling; cancer biology; cell behavior hypothesis grammar; cell behaviors; cell interactions; immunology; immunotherapy; mathematical biology; mathematical modeling; modeling language; multi-omics; multicellular systems; multicellular systems biology; physics of multicellular biology; simulation; spatial transcriptomics; tissue dynamics.

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Conflict of interest statement

Declaration of interests J.W.Z. receives other support from Roche/Genentech and honoraria from Sermo and ZoomRx. L.Z. receives grant support from Bristol-Myers Squibb, Merck, AstraZeneca, iTeos, Amgen, NovaRock, Inxmed, and Halozyme. L.Z. is a paid consultant/advisory board member at Biosion, Alphamab, NovaRock, Ambrx, Akrevia/Xilio, QED, Tempus, Pfizer, Novagenesis, Snow Lake Capitals, Amberstone, Tavotek Lab, ClinicalTrial Options, LLC, and Mingruizhiyao. L.Z. holds shares at Amberstone, Alphamab, Cellaration, and Mingruizhiyao. E.M.J. reports other support from Abmeta and Adventris; personal fees from Dragonfly, Neuvogen, Surge Tx, Mestag, and HDTbio; and grants from Lustgarten, Genentech, BMS, NeoTx, and Break Through Cancer. E.M.J. is a founder of and holds equity in Adventris Pharmaceuticals. She also serves as a consultant to the entity. Further, Adventris Pharmaceuticals has licensed a technology described in this study from the Johns Hopkins University. As a result of that agreement, E.M.J. and the University are entitled to royalty distributions related to technology described in the study discussed in this publication. This arrangement has been reviewed and approved by Johns Hopkins University in accordance with its conflict-of-interest policies. A.J.E.’s spouse is an employee of Immunocore. A.J.E. has unlicensed patents and patent applications in cancer and autoimmunity, and none of them closely relate to the topic of this paper. N.Z. is a consultant for Genentech and Adventris Pharmaceuticals and receives other support from Adventris Pharmaceuticals. L.M.C. has received reagent support from Cell Signaling Technologies, Syndax Pharmaceuticals, Inc., ZielBio, Inc., and Hibercell, Inc.; holds sponsored research agreements with Prospect Creek Foundation; receives grant support from Susan G. Komen Foundation, National Foundation for Cancer Research, and the National Cancer Institute; and is on the advisory board of Carisma Therapeutics, Inc., CytomX Therapeutics, Inc., Kineta, Inc., Hibercell, Inc., Cell Signaling Technologies, Inc, Alkermes, Inc., NextCure, Guardian Bio, Dispatch Biotherapeutics, AstraZeneca Partner of Choice Network (OHSU Site Leader), Genenta Sciences, Pio Therapeutics Pty Ltd., and Lustgarten Foundation for Pancreatic Cancer Research Therapeutics Working Group. E.J.F. was on the scientific advisory board of Resistance Bio/Viosera Therapeutics, a paid consultant for Merck and Mestag, and received research funds from Abbvie Inc. and Roche/Genetech outside the submitted work.

Update of

Digitize your Biology! Modeling multicellular systems through interpretable cell behavior.
Johnson JAI, Stein-O'Brien GL, Booth M, Heiland R, Kurtoglu F, Bergman DR, Bucher E, Deshpande A, Forjaz A, Getz M, Godet I, Lyman M, Metzcar J, Mitchell J, Raddatz A, Rocha H, Solorzano J, Sundus A, Wang Y, Gilkes D, Kagohara LT, Kiemen AL, Thompson ED, Wirtz D, Wu PH, Zaidi N, Zheng L, Zimmerman JW, Jaffee EM, Hwan Chang Y, Coussens LM, Gray JW, Heiser LM, Fertig EJ, Macklin P. Johnson JAI, et al. bioRxiv [Preprint]. 2023 Nov 5:2023.09.17.557982. doi: 10.1101/2023.09.17.557982. bioRxiv. 2023. Update in: Cell. 2025 Aug 21;188(17):4711-4733.e37. doi: 10.1016/j.cell.2025.06.048. PMID: 37745323 Free PMC article. Updated. Preprint.

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Human interpretable grammar encodes multicellular systems biology models to democratize virtual cell laboratories

Affiliations

Human interpretable grammar encodes multicellular systems biology models to democratize virtual cell laboratories

Authors

Affiliations

Abstract

Conflict of interest statement

Update of

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Molecular Biology Databases