Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytes

Summary: The diversity of mononuclear phagocyte (MNP) subpopulations across tissues is one of the key physiological characteristics of the immune system. Here, we focus on understanding the metabolic variability of MNPs through metabolic network analysis applied to three large-scale transcriptional...

Full description

Bibliographic Details
Main Authors: Anastasiia Gainullina, Denis A. Mogilenko, Li-Hao Huang, Helena Todorov, Vipin Narang, Ki-Wook Kim, Lim Sheau Yng, Andrew Kent, Baosen Jia, Kumba Seddu, Karen Krchma, Jun Wu, Karine Crozat, Elena Tomasello, Regine Dress, Peter See, Charlotte Scott, Sophie Gibbings, Geetika Bajpai, Jigar V. Desai, Barbara Maier, Sébastien This, Peter Wang, Stephanie Vargas Aguilar, Lucie Poupel, Sébastien Dussaud, Tyng-An Zhou, Veronique Angeli, J. Magarian Blander, Kyunghee Choi, Marc Dalod, Ivan Dzhagalov, Emmanuel L. Gautier, Claudia Jakubzick, Kory Lavine, Michail S. Lionakis, Helena Paidassi, Michael H. Sieweke, Florent Ginhoux, Martin Guilliams, Christophe Benoist, Miriam Merad, Gwendalyn J. Randolph, Alexey Sergushichev, Maxim N. Artyomov
Format: Article
Language:English
Published: Elsevier 2023-02-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723000578
_version_ 1828052323712106496
author Anastasiia Gainullina
Denis A. Mogilenko
Li-Hao Huang
Helena Todorov
Vipin Narang
Ki-Wook Kim
Lim Sheau Yng
Andrew Kent
Baosen Jia
Kumba Seddu
Karen Krchma
Jun Wu
Karine Crozat
Elena Tomasello
Regine Dress
Peter See
Charlotte Scott
Sophie Gibbings
Geetika Bajpai
Jigar V. Desai
Barbara Maier
Sébastien This
Peter Wang
Stephanie Vargas Aguilar
Lucie Poupel
Sébastien Dussaud
Tyng-An Zhou
Veronique Angeli
J. Magarian Blander
Kyunghee Choi
Marc Dalod
Ivan Dzhagalov
Emmanuel L. Gautier
Claudia Jakubzick
Kory Lavine
Michail S. Lionakis
Helena Paidassi
Michael H. Sieweke
Florent Ginhoux
Martin Guilliams
Christophe Benoist
Miriam Merad
Gwendalyn J. Randolph
Alexey Sergushichev
Maxim N. Artyomov
author_facet Anastasiia Gainullina
Denis A. Mogilenko
Li-Hao Huang
Helena Todorov
Vipin Narang
Ki-Wook Kim
Lim Sheau Yng
Andrew Kent
Baosen Jia
Kumba Seddu
Karen Krchma
Jun Wu
Karine Crozat
Elena Tomasello
Regine Dress
Peter See
Charlotte Scott
Sophie Gibbings
Geetika Bajpai
Jigar V. Desai
Barbara Maier
Sébastien This
Peter Wang
Stephanie Vargas Aguilar
Lucie Poupel
Sébastien Dussaud
Tyng-An Zhou
Veronique Angeli
J. Magarian Blander
Kyunghee Choi
Marc Dalod
Ivan Dzhagalov
Emmanuel L. Gautier
Claudia Jakubzick
Kory Lavine
Michail S. Lionakis
Helena Paidassi
Michael H. Sieweke
Florent Ginhoux
Martin Guilliams
Christophe Benoist
Miriam Merad
Gwendalyn J. Randolph
Alexey Sergushichev
Maxim N. Artyomov
author_sort Anastasiia Gainullina
collection DOAJ
description Summary: The diversity of mononuclear phagocyte (MNP) subpopulations across tissues is one of the key physiological characteristics of the immune system. Here, we focus on understanding the metabolic variability of MNPs through metabolic network analysis applied to three large-scale transcriptional datasets: we introduce (1) an ImmGen MNP open-source dataset of 337 samples across 26 tissues; (2) a myeloid subset of ImmGen Phase I dataset (202 MNP samples); and (3) a myeloid mouse single-cell RNA sequencing (scRNA-seq) dataset (51,364 cells) assembled based on Tabula Muris Senis. To analyze such large-scale datasets, we develop a network-based computational approach, genes and metabolites (GAM) clustering, for unbiased identification of the key metabolic subnetworks based on transcriptional profiles. We define 9 metabolic subnetworks that encapsulate the metabolic differences within MNP from 38 different tissues. Obtained modules reveal that cholesterol synthesis appears particularly active within the migratory dendritic cells, while glutathione synthesis is essential for cysteinyl leukotriene production by peritoneal and lung macrophages.
first_indexed 2024-04-10T19:51:51Z
format Article
id doaj.art-8a6a390493e44f40a7321fccee2cd51c
institution Directory Open Access Journal
issn 2211-1247
language English
last_indexed 2024-04-10T19:51:51Z
publishDate 2023-02-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj.art-8a6a390493e44f40a7321fccee2cd51c2023-01-28T04:07:41ZengElsevierCell Reports2211-12472023-02-01422112046Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytesAnastasiia Gainullina0Denis A. Mogilenko1Li-Hao Huang2Helena Todorov3Vipin Narang4Ki-Wook Kim5Lim Sheau Yng6Andrew Kent7Baosen Jia8Kumba Seddu9Karen Krchma10Jun Wu11Karine Crozat12Elena Tomasello13Regine Dress14Peter See15Charlotte Scott16Sophie Gibbings17Geetika Bajpai18Jigar V. Desai19Barbara Maier20Sébastien This21Peter Wang22Stephanie Vargas Aguilar23Lucie Poupel24Sébastien Dussaud25Tyng-An Zhou26Veronique Angeli27J. Magarian Blander28Kyunghee Choi29Marc Dalod30Ivan Dzhagalov31Emmanuel L. Gautier32Claudia Jakubzick33Kory Lavine34Michail S. Lionakis35Helena Paidassi36Michael H. Sieweke37Florent Ginhoux38Martin Guilliams39Christophe Benoist40Miriam Merad41Gwendalyn J. Randolph42Alexey Sergushichev43Maxim N. Artyomov44Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA; Computer Technologies Department, ITMO University, St. Petersburg 197101, Russia; Laboratory of Bioinformatics and Molecular Genetics, Koltzov Institute of Developmental Biology of the Russian Academy of Sciences, Moscow 119334, RussiaDepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Medicine, Department of Pathology, Microbiology, and Immunology, Vanderbilt Center for Immunobiology, Vanderbilt University Medical Center, Nashville, TN 37232, USADepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USALaboratory of Immunoregulation, Inflammation Research Centre, VIB Ghent University, 9052 Ghent, BelgiumSingapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Singapore 138648, SingaporeDepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USAImmunology Translational Research Programme, Yong Loo Lin School of Medicine, Department of Microbiology and Immunology, National University of Singapore, Singapore 117545, Singapore; Immunology Programme, Life Sciences Institute, National University of Singapore, Singapore 117545, SingaporeThe Jill Roberts Institute for Research in Inflammatory Bowel Disease, Joan and Sanford I. Weill Department of Medicine, Department of Microbiology and Immunology, Weill Cornell Medicine, Cornell University, New York, NY 10021, USAThe Jill Roberts Institute for Research in Inflammatory Bowel Disease, Joan and Sanford I. Weill Department of Medicine, Department of Microbiology and Immunology, Weill Cornell Medicine, Cornell University, New York, NY 10021, USADepartment of Immunology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USAAix Marseille University, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille-Luminy, Turing Center for Living Systems, 13288 Marseille, FranceAix Marseille University, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille-Luminy, Turing Center for Living Systems, 13288 Marseille, FranceSingapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Singapore 138648, SingaporeSingapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Singapore 138648, SingaporeLaboratory of Immunoregulation, Inflammation Research Centre, VIB Ghent University, 9052 Ghent, BelgiumDepartment of Pediatrics, National Jewish Health, Denver, CO 80206, USACenter for Cardiovascular Research, Division of Cardiology, Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USAFungal Pathogenesis Section, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USAImmunology Institute and Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USACentre International de Recherche en Infectiologie (CIRI), University Lyon, Inserm, U1111, Université Claude Bernard Lyon ,1, CNRS, UMR5308, ENS de Lyon, 69007 Lyon, FranceDepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USAAix Marseille University, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille-Luminy, Turing Center for Living Systems, 13288 Marseille, France; Center for Regenerative Therapies (CRTD), TU Dresden, 01307 Dresden, Germany; Max-Delbrück-Centrum für Molekulare Medizin in der Helmholtzgemeinschaft (MDC), 13125 Berlin, GermanyINSERM UMR-S 1166, Sorbonne Université, Hôpital de la Pitié-Salpêtrière, 75013 Paris, FranceINSERM UMR-S 1166, Sorbonne Université, Hôpital de la Pitié-Salpêtrière, 75013 Paris, FranceInstitute of Microbiology and Immunology, National Yang-Ming University, Taipei 112, TaiwanImmunology Translational Research Programme, Yong Loo Lin School of Medicine, Department of Microbiology and Immunology, National University of Singapore, Singapore 117545, Singapore; Immunology Programme, Life Sciences Institute, National University of Singapore, Singapore 117545, SingaporeThe Jill Roberts Institute for Research in Inflammatory Bowel Disease, Joan and Sanford I. Weill Department of Medicine, Department of Microbiology and Immunology, Weill Cornell Medicine, Cornell University, New York, NY 10021, USADepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USAAix Marseille University, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille-Luminy, Turing Center for Living Systems, 13288 Marseille, FranceInstitute of Microbiology and Immunology, National Yang-Ming University, Taipei 112, TaiwanINSERM UMR-S 1166, Sorbonne Université, Hôpital de la Pitié-Salpêtrière, 75013 Paris, FranceDepartment of Pediatrics, National Jewish Health, Denver, CO 80206, USACenter for Cardiovascular Research, Division of Cardiology, Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USAFungal Pathogenesis Section, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USACentre International de Recherche en Infectiologie (CIRI), University Lyon, Inserm, U1111, Université Claude Bernard Lyon ,1, CNRS, UMR5308, ENS de Lyon, 69007 Lyon, FranceAix Marseille University, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille-Luminy, Turing Center for Living Systems, 13288 Marseille, France; Center for Regenerative Therapies (CRTD), TU Dresden, 01307 Dresden, Germany; Max-Delbrück-Centrum für Molekulare Medizin in der Helmholtzgemeinschaft (MDC), 13125 Berlin, GermanySingapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), Singapore 138648, SingaporeLaboratory of Immunoregulation, Inflammation Research Centre, VIB Ghent University, 9052 Ghent, BelgiumDepartment of Immunology, Harvard Medical School, Boston, MA 02115, USAImmunology Institute and Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USADepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA; Computer Technologies Department, ITMO University, St. Petersburg 197101, Russia; Corresponding authorDepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA; Corresponding authorSummary: The diversity of mononuclear phagocyte (MNP) subpopulations across tissues is one of the key physiological characteristics of the immune system. Here, we focus on understanding the metabolic variability of MNPs through metabolic network analysis applied to three large-scale transcriptional datasets: we introduce (1) an ImmGen MNP open-source dataset of 337 samples across 26 tissues; (2) a myeloid subset of ImmGen Phase I dataset (202 MNP samples); and (3) a myeloid mouse single-cell RNA sequencing (scRNA-seq) dataset (51,364 cells) assembled based on Tabula Muris Senis. To analyze such large-scale datasets, we develop a network-based computational approach, genes and metabolites (GAM) clustering, for unbiased identification of the key metabolic subnetworks based on transcriptional profiles. We define 9 metabolic subnetworks that encapsulate the metabolic differences within MNP from 38 different tissues. Obtained modules reveal that cholesterol synthesis appears particularly active within the migratory dendritic cells, while glutathione synthesis is essential for cysteinyl leukotriene production by peritoneal and lung macrophages.http://www.sciencedirect.com/science/article/pii/S2211124723000578CP: ImmunologyCP: Metabolism
spellingShingle Anastasiia Gainullina
Denis A. Mogilenko
Li-Hao Huang
Helena Todorov
Vipin Narang
Ki-Wook Kim
Lim Sheau Yng
Andrew Kent
Baosen Jia
Kumba Seddu
Karen Krchma
Jun Wu
Karine Crozat
Elena Tomasello
Regine Dress
Peter See
Charlotte Scott
Sophie Gibbings
Geetika Bajpai
Jigar V. Desai
Barbara Maier
Sébastien This
Peter Wang
Stephanie Vargas Aguilar
Lucie Poupel
Sébastien Dussaud
Tyng-An Zhou
Veronique Angeli
J. Magarian Blander
Kyunghee Choi
Marc Dalod
Ivan Dzhagalov
Emmanuel L. Gautier
Claudia Jakubzick
Kory Lavine
Michail S. Lionakis
Helena Paidassi
Michael H. Sieweke
Florent Ginhoux
Martin Guilliams
Christophe Benoist
Miriam Merad
Gwendalyn J. Randolph
Alexey Sergushichev
Maxim N. Artyomov
Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytes
Cell Reports
CP: Immunology
CP: Metabolism
title Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytes
title_full Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytes
title_fullStr Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytes
title_full_unstemmed Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytes
title_short Network analysis of large-scale ImmGen and Tabula Muris datasets highlights metabolic diversity of tissue mononuclear phagocytes
title_sort network analysis of large scale immgen and tabula muris datasets highlights metabolic diversity of tissue mononuclear phagocytes
topic CP: Immunology
CP: Metabolism
url http://www.sciencedirect.com/science/article/pii/S2211124723000578
work_keys_str_mv AT anastasiiagainullina networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT denisamogilenko networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT lihaohuang networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT helenatodorov networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT vipinnarang networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT kiwookkim networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT limsheauyng networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT andrewkent networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT baosenjia networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT kumbaseddu networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT karenkrchma networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT junwu networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT karinecrozat networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT elenatomasello networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT reginedress networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT petersee networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT charlottescott networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT sophiegibbings networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT geetikabajpai networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT jigarvdesai networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT barbaramaier networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT sebastienthis networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT peterwang networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT stephanievargasaguilar networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT luciepoupel networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT sebastiendussaud networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT tynganzhou networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT veroniqueangeli networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT jmagarianblander networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT kyungheechoi networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT marcdalod networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT ivandzhagalov networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT emmanuellgautier networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT claudiajakubzick networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT korylavine networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT michailslionakis networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT helenapaidassi networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT michaelhsieweke networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT florentginhoux networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT martinguilliams networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT christophebenoist networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT miriammerad networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT gwendalynjrandolph networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT alexeysergushichev networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes
AT maximnartyomov networkanalysisoflargescaleimmgenandtabulamurisdatasetshighlightsmetabolicdiversityoftissuemononuclearphagocytes