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Citations to this article

Fragile TIM-4–expressing tissue resident macrophages are migratory and immunoregulatory
Thomas B. Thornley, … , Vijay K. Kuchroo, Terry B. Strom
Thomas B. Thornley, … , Vijay K. Kuchroo, Terry B. Strom
Published July 1, 2014
Citation Information: J Clin Invest. 2014;124(8):3443-3454. https://doi.org/10.1172/JCI73527.
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Research Article Immunology Article has an altmetric score of 1

Fragile TIM-4–expressing tissue resident macrophages are migratory and immunoregulatory

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Abstract

Macrophages characterized as M2 and M2-like regulate immune responses associated with immune suppression and healing; however, the relationship of this macrophage subset to CD169+ tissue-resident macrophages and their contribution to shaping alloimmune responses is unknown. Here we identified a population of M2-like tissue-resident macrophages that express high levels of the phosphatidylserine receptor TIM-4 and CD169 (TIM-4hiCD169+). Labeling and tracking of TIM-4hiCD169+ macrophages in mice revealed that this population is a major subset of tissue-resident macrophages, homes to draining LNs following oxidative stress, exhibits an immunoregulatory and hypostimulatory phenotype that is maintained after migration to secondary lymphoid organs, favors preferential induction of antigen-stimulated Tregs, and is highly susceptible to apoptosis. Moreover, CD169+ tissue-resident macrophages were resistant to oxidative stress–induced apoptosis in mice lacking TIM-4. Compared with heart allografts from WT mice, Tim4–/– heart allografts survived much longer and were more easily tolerized by non-immunosuppressed recipients. Furthermore, Tim4–/– allograft survival was associated with the infiltration of Tregs into the graft. Together, our data provide evidence that M2-like TIM-4hiCD169+ tissue-resident macrophages are immunoregulatory and promote engraftment of cardiac allografts, but their influence is diminished by TIM-4–dependent programmed cell death.

Authors

Thomas B. Thornley, Zemin Fang, Savithri Balasubramanian, Rafael A. Larocca, Weihua Gong, Shipra Gupta, Eva Csizmadia, Nicolas Degauque, Beom Seok Kim, Maria Koulmanda, Vijay K. Kuchroo, Terry B. Strom

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Total citations by year

Year: 2024 2023 2022 2021 2020 2019 2017 2016 2015 Total
Citations: 5 5 3 2 5 3 8 5 3 39
Citation information
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Citations to this article (39)

Title and authors Publication Year
CD169+ Skin Macrophages Function as a Specialized Subpopulation in Promoting Psoriasis-like Skin Disease in Mice
Li M, Yu W, Liu Z, Liu S
International journal of molecular sciences 2024
Modulating Lipid-Polymer Nanoparticles’ Physicochemical Properties to Alter Macrophage Uptake
Bender EC, Sircar AJ, Taubenfeld EK, Suggs LJ
ACS Biomaterials Science & Engineering 2024
Targeting Macrophages in Organ Transplantation: A Step Toward Personalized Medicine.
Owen MC, Kopecky BJ
Transplantation 2024
Retention of ES cell-derived 129S genome drives NLRP1 hypersensitivity and transcriptional deregulation in Nlrp3(tm1Flv) mice.
Weiss FD, Alvarez Y, Shakeri F, Sahu A, Leka P, Dernst A, Rollheiser J, Vasconcelos M, Geraci A, Duthie F, Stahl R, Lee HE, Gellner AK, Buness A, Latz E, Meissner F
Cell death and differentiation 2024
TIM proteins and microRNAs: distinct impact and promising interactions on transplantation immunity
Tao J, Shen X, Qian H, Ding Q, Wang L
Frontiers in Immunology 2024
Multiple Shades of Gray—Macrophages in Acute Allograft Rejection
Lackner K, Ebner S, Watschinger K, Maglione M
International journal of molecular sciences 2023
Macrophages in cardiac remodelling after myocardial infarction.
Yap J, Irei J, Lozano-Gerona J, Vanapruks S, Bishop T, Boisvert WA
Nature reviews. Cardiology 2023
Apoptosis recognition receptors regulate skin tissue repair in mice
Justynski O, Bridges K, Krause W, Forni MF, Phan QM, Sandoval-Schaefer T, Carter K, King DE, Hsia HC, Gazes MI, Vyce SD, Driskell RR, Miller-Jensen K, Horsley V
eLife 2023
Recipient TIM4 signaling regulates ischemia reperfusion-induced ER stress and metabolic responses in liver transplantation: from mouse-to-human
Hirao H, Kageyama S, Nakamura K, Kadono K, Kojima H, Siyuan Y, Farmer DG, Kaldas FM, Dery KJ, Kupiec-Weglinski JW
2023
Single-nucleus RNA sequencing reveals heterogeneity among multiple white adipose tissue depots
Xie L, Hu W, Zhang H, Ding Y, Zeng Q, Liao X, Wang D, Xie W, Hui HX, Deng T
Life Metabolism 2023
The role of efferocytosis in neuro-degenerative diseases
F Taheri, E Taghizadeh, J Navashenaq, M Rezaee, S Gheibihayat
Neurological Sciences 2022
A Microbiota-Dependent Subset of Skin Macrophages Protects Against Cutaneous Bacterial Infection
Park YJ, Kang BH, Kim HJ, Oh JE, Lee HK
Frontiers in immunology 2022
Function and characteristics of TIM‑4 in immune regulation and disease (Review).
Wang Z, Chen C, Su Y, Ke N
International journal of molecular medicine 2022
The Evolving Roles of Cardiac Macrophages in Homeostasis, Regeneration, and Repair
S Alvarez-Argote, CC OMeara
International journal of molecular sciences 2021
Innovative Systems to Deliver Allergen Powder for Epicutaneous Immunotherapy
Y Wang, Y Kong, MX Wu
Frontiers in immunology 2021
Autophagic adaptation to oxidative stress alters peritoneal residential macrophage survival and ovarian cancer metastasis
Houjun Xia, Shasha Li, Xiong Li, Weichao Wang, Yingjie Bian, Shuang Wei, Sara Grove, Weimin Wang, Linda Vatan, J. Rebecca Liu, Karen McLean, Ramandeep Rattan, Adnan R. Munkarah, Jun-Lin Guan, Ilona Kryczek, Weiping Zou
JCI Insight 2020
The role of phosphatidylserine recognition receptors in multiple biological functions
MB Naeini, V Bianconi, M Pirro, A Sahebkar
Cellular & Molecular Biology Letters 2020
Role of donor macrophages after heart and lung transplantation
BJ Kopecky, C Frye, Y Terada, KR Balsara, D Kreisel, KJ Lavine
American Journal of Transplantation 2020
Macrophages in Organ Transplantation
F Ordikhani, V Pothula, R Sanchez-Tarjuelo, S Jordan, J Ochando
Frontiers in immunology 2020
Tim-4 in Health and Disease: Friend or Foe?
W Liu, L Xu, X Liang, X Liu, Y Zhao, C Ma, L Gao
Frontiers in immunology 2020
CCL2/MCP-1 signaling drives extracellular matrix turnover by diverse macrophage subsets
HJ Jürgensen, LM Silva, O Krigslund, S van Putten, DH Madsen, N Behrendt, LH Engelholm, TH Bugge
2019
IL-4/IL-13 polarization of macrophages enhances Ebola virus glycoprotein-dependent infection
KJ Rogers, B Brunton, L Mallinger, D Bohan, KM Sevcik, J Chen, N Ruggio, W Maury, T Geisbert
PLoS neglected tropical diseases 2019
Adaptive features of innate immune cells and their relevance to graft rejection
G Wang, G Kong, XC Li
Current Opinion in Organ Transplantation 2019
CRIg, a tissue-resident macrophage specific immune checkpoint molecule, promotes immunological tolerance in NOD mice, via a dual role in effector and regulatory T cells
X Yuan, BH Yang, Y Dong, A Yamamura, W Fu
eLife 2017
Therapeutic application of T regulatory cells in composite tissue allotransplantation
JH Yang, SC Eun
Journal of Translational Medicine 2017
Efferocytosis Signaling in the Regulation of Macrophage Inflammatory Responses
MR Elliott, KM Koster, PS Murphy
Journal of immunology (Baltimore, Md. : 1950) 2017
Macrophage subpopulations and their impact on chronic allograft rejection versus graft acceptance in a mouse heart transplant model
Y Zhao, S Chen, P Lan, C Wu, Y Dou, X Xiao, Z Zhang, L Minze, X He, W Chen, XC Li
American Journal of Transplantation 2017
Sex Differences in Macrophage Functions in Middle-Aged Rats: Relevance of Estradiol Level and Macrophage Estrogen Receptor Expression
I Ćuruvija, S Stanojević, N Arsenović-Ranin, V Blagojević, M Dimitrijević, B Vidić-Danković, V Vujić
Inflammation 2017
Mouse macrophages show different requirements for phosphatidylserine receptor Tim4 in efferocytosis
Y Yanagihashi, K Segawa, R Maeda, Y Nabeshima, S Nagata
Proceedings of the National Academy of Sciences 2017
Comparison of the characteristics of macrophages derived from murine spleen, peritoneal cavity, and bone marrow
Y Zhao, P Tian, F Han, J Zheng, X Xia, W Xue, X Ding, C Ding
Journal of Zhejiang University SCIENCE B 2017
Mannose receptor high, M2 dermal macrophages mediate nonhealing Leishmania major infection in a Th1 immune environment
SH Lee, M Charmoy, A Romano, A Paun, MM Chaves, FO Cope, DA Ralph, DL Sacks
Journal of Experimental Medicine 2017
Macrophages as Effectors of Acute and Chronic Allograft Injury
Y Liu, M Kloc, XC Li
Current Transplantation Reports 2016
T Cell Cosignaling Molecules in Transplantation
ML Ford
Immunity 2016
The transcriptional signature of human ovarian carcinoma macrophages is associated with extracellular matrix reorganization
F Finkernagel, S Reinartz, S Lieber, T Adhikary, A Wortmann, N Hoffmann, T Bieringer, A Nist, T Stiewe, JM Jansen, U Wagner, S Müller-Brüsselbach, R Müller
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Blockade of Tim-1 and Tim-4 Enhances Atherosclerosis in Low-Density Lipoprotein Receptor–Deficient MiceSignificance
AC Foks, D Engelbertsen, F Kuperwaser, N Alberts-Grill, A Gonen, JL Witztum, J Lederer, P Jarolim, RH DeKruyff, GJ Freeman, AH Lichtman
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Contrasting Roles of Islet Resident Immunoregulatory Macrophages and Dendritic Cells in Experimental Autoimmune Type 1 Diabetes
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F Ginhoux, JL Schultze, PJ Murray, J Ochando, SK Biswas
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Innate immunity for better or worse govern the allograft response:
LE Otterbein, Z Fan, M Koulmanda, T Thronley, TB Strom
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Tim-4 Inhibits NO Generation by Murine Macrophages
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