DPPIV
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
13 Dec 2023
13 Dec 2023
Historique:
received:
21
12
2022
accepted:
14
11
2023
medline:
14
12
2023
pubmed:
14
12
2023
entrez:
13
12
2023
Statut:
epublish
Résumé
Adult tissue-resident macrophages (RMs) are either maintained by blood monocytes or through self-renewal. While the presence of a nurturing niche is likely crucial to support the survival and function of self-renewing RMs, evidence regarding its nature is limited. Here, we identify fibro-adipogenic progenitors (FAPs) as the main source of colony-stimulating factor 1 (CSF1) in resting skeletal muscle. Using parabiosis in combination with FAP-deficient transgenic mice (Pdgfrα
Identifiants
pubmed: 38092736
doi: 10.1038/s41467-023-43579-3
pii: 10.1038/s41467-023-43579-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8273Subventions
Organisme : Gouvernement du Canada | Instituts de Recherche en Santé du Canada | CIHR Skin Research Training Centre (Skin Research Training Centre)
ID : 159908
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : AG045040
Organisme : Welch Foundation
ID : AQ-1507
Informations de copyright
© 2023. The Author(s).
Références
Wu, Y. & Hirschi, K. K. Tissue-resident macrophage development and function. Front Cell Dev. Biol. 8, 617879 (2020).
pubmed: 33490082
doi: 10.3389/fcell.2020.617879
Davies, L. C., Jenkins, S. J., Allen, J. E. & Taylor, P. R. Tissue-resident macrophages. Nat. Immunol. 14, 986–95 (2013).
pubmed: 24048120
pmcid: 4045180
doi: 10.1038/ni.2705
Paolicelli, R. C. et al. Synaptic pruning by microglia is necessary for normal brain development. Science 333, 1456–1458 (2011).
pubmed: 21778362
doi: 10.1126/science.1202529
Kohyama, M. et al. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457, 318–321 (2009).
pubmed: 19037245
doi: 10.1038/nature07472
Rosen, A. & Casciola-Rosen, L. Clearing the way to mechanisms of autoimmunity. Nat. Med. 7, 664–665 (2001).
pubmed: 11385500
doi: 10.1038/89034
Carrero, J. A. et al. Resident macrophages of pancreatic islets have a seminal role in the initiation of autoimmune diabetes of NOD mice. Proc. Natl Acad. Sci. USA 114, E10418–E10427 (2017).
pubmed: 29133420
pmcid: 5715775
doi: 10.1073/pnas.1713543114
Ying, W. et al. Expansion of islet-resident macrophages leads to inflammation affecting β cell proliferation and function in obesity. Cell Metab. 29, 457–474.e5 (2019).
pubmed: 30595478
doi: 10.1016/j.cmet.2018.12.003
Halevy, O. & Velleman, S. G. Chapter 23 - Skeletal muscle. in Sturkie’s Avian Physiology (Seventh Edition) (eds. Scanes, C. G. & Dridi, S.) 565–589 (Academic Press, 2022). https://doi.org/10.1016/B978-0-12-819770-7.00024-4 .
Michele, D. E. Mechanisms of skeletal muscle repair and regeneration in health and disease. FEBS J. 289, 6460–6462 (2022).
doi: 10.1111/febs.16577
pubmed: 35929418
Lemos, D. R. et al. Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors. Nat. Med. 21, 786–794 (2015).
pubmed: 26053624
doi: 10.1038/nm.3869
Babaeijandaghi, F. et al. TNFα and IFNγ cooperate for efficient pro- to anti-inflammatory transition of macrophages during muscle regeneration. Proc. Natl Acad. Sci. USA 119, e2209976119 (2022).
pubmed: 36279473
pmcid: 9636974
doi: 10.1073/pnas.2209976119
Babaeijandaghi, F. et al. Metabolic reprogramming of skeletal muscle by resident macrophages points to CSF1R inhibitors as muscular dystrophy therapeutics. Sci. Transl. Med. 14, eabg7504 (2022).
pubmed: 35767650
doi: 10.1126/scitranslmed.abg7504
Wang, X. et al. Heterogeneous origins and functions of mouse skeletal muscle-resident macrophages. Proc. Natl Acad. Sci. 117, 20729–20740 (2020).
pubmed: 32796104
pmcid: 7456122
doi: 10.1073/pnas.1915950117
Krasniewski, L. K. et al. Single-cell analysis of skeletal muscle macrophages reveals age-associated functional subpopulations. Elife 11, e77974 (2022).
pubmed: 36259488
pmcid: 9629833
doi: 10.7554/eLife.77974
Ferraro, F., Celso, C. L. & Scadden, D. Adult stem cels and their niches. Adv. Exp. Med. Biol. 695, 155–168 (2010).
pubmed: 21222205
pmcid: 4020242
doi: 10.1007/978-1-4419-7037-4_11
Guilliams, M. & Scott, C. L. Does niche competition determine the origin of tissue-resident macrophages? Nat. Rev. Immunol. 17, 451–460 (2017).
pubmed: 28461703
doi: 10.1038/nri.2017.42
Crane, G. M., Jeffery, E. & Morrison, S. J. Adult haematopoietic stem cell niches. Nat. Rev. Immunol. 17, 573–590 (2017).
pubmed: 28604734
doi: 10.1038/nri.2017.53
McCarthy, N., Kraiczy, J. & Shivdasani, R. A. Cellular and molecular architecture of the intestinal stem cell niche. Nat. Cell Biol. 22, 1033–1041 (2020).
pubmed: 32884148
doi: 10.1038/s41556-020-0567-z
Yin, H., Price, F. & Rudnicki, M. A. Satellite cells and the muscle stem cell niche. Physiol. Rev. 93, 23–67 (2013).
pubmed: 23303905
pmcid: 4073943
doi: 10.1152/physrev.00043.2011
Judson, R. N., Zhang, R. H. & Rossi, F. M. A. Tissue-resident mesenchymal stem/progenitor cells in skeletal muscle: Collaborators or saboteurs? FEBS J. 280, 4100–4108 (2013).
pubmed: 23763717
pmcid: 4880469
doi: 10.1111/febs.12370
Joe, A. W. B. et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12, 153–163 (2010).
pubmed: 20081841
pmcid: 4580288
doi: 10.1038/ncb2015
Uezumi, A., Fukada, S. I., Yamamoto, N., Takeda, S. & Tsuchida, K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 12, 143–152 (2010).
pubmed: 20081842
doi: 10.1038/ncb2014
Roberts, E. W. et al. Depletion of stromal cells expressing fibroblast activation protein-α from skeletal muscle and bone marrow results in cachexia and anemia. J. Exp. Med. 210, 1137–1151 (2013).
pubmed: 23712428
pmcid: 3674708
doi: 10.1084/jem.20122344
Uezumi, A. et al. Mesenchymal Bmp3b expression maintains skeletal muscle integrity and decreases in age-related sarcopenia. J. Clin. Invest. 131, e139617 (2021).
pubmed: 33170806
pmcid: 7773381
doi: 10.1172/JCI139617
Wosczyna, M. N. et al. Mesenchymal stromal cells are required for regeneration and homeostatic maintenance of skeletal muscle. Cell Rep. 27, 2029–2035.e5 (2019).
pubmed: 31091443
pmcid: 7034941
doi: 10.1016/j.celrep.2019.04.074
Kajabadi, N. et al. Activation of β-catenin in mesenchymal progenitors leads to muscle mass loss. Dev. Cell 58, 489–505.e7 (2023).
pubmed: 36898377
doi: 10.1016/j.devcel.2023.02.009
Naito, M. et al. Abnormal differentiation of tissue macrophage populations in ‘osteopetrosis’ (op) mice defective in the production of macrophage colony-stimulating factor. Am. J. Pathol. 139, 657–667 (1991).
pubmed: 1887865
pmcid: 1886220
Zhou, X. et al. Microenvironmental sensing by fibroblasts controls macrophage population size. bioRxiv https://doi.org/10.1101/2022.01.18.476683 (2022).
Zhou, X. et al. Microenvironmental sensing by fibroblasts controls macrophage population size. https://doi.org/10.1073/pnas (2022).
Elmore, M. R. P. et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82, 380–397 (2014).
pubmed: 24742461
pmcid: 4161285
doi: 10.1016/j.neuron.2014.02.040
Guilliams, M., Thierry, G. R., Bonnardel, J. & Bajenoff, M. Establishment and maintenance of the macrophage niche. Immunity 52, 434–451 (2020).
pubmed: 32187515
doi: 10.1016/j.immuni.2020.02.015
Dick, S. A. et al. Three tissue resident macrophage subsets coexist across organs with conserved origins and life cycles. Sci. Immunol. 7, eabf7777 (2022).
pubmed: 34995099
doi: 10.1126/sciimmunol.abf7777
Bonnardel, J. et al. Stellate cells, hepatocytes, and endothelial cells imprint the kupffer cell identity on monocytes colonizing the liver macrophage niche. Immunity 51, 638–654.e9 (2019).
pubmed: 31561945
pmcid: 6876284
doi: 10.1016/j.immuni.2019.08.017
Muller, P. A. et al. Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 158, 1210. Preprint at https://doi.org/10.1016/j.cell.2014.08.002 (2014).
Ryan, G. R. et al. Rescue of the colony-stimulating factor 1 (CSF-1)-nullizygous mouse (Csf1op/Csf1op) phenotype with a CSF-1 transgene and identification of sites of local CSF-1 synthesis. Blood 98, 74–84 (2001).
pubmed: 11418465
doi: 10.1182/blood.V98.1.74
Mondor, I. et al. Lymphatic endothelial cells are essential components of the subcapsular sinus macrophage niche. Immunity 50, 1453–1466.e4 (2019).
pubmed: 31053503
pmcid: 6697131
doi: 10.1016/j.immuni.2019.04.002
Bellomo, A. et al. Reticular fibroblasts expressing the transcription factor WT1 define a stromal niche that maintains and replenishes splenic red pulp macrophages. Immunity 53, 127–142.e7 (2020).
pubmed: 32562599
doi: 10.1016/j.immuni.2020.06.008
Tanaka, S. et al. Macrophage colony-stimulating factor is indispensable for both proliferation and differentiation of osteoclast progenitors. J. Clin. Invest. 91, 257–263 (1993).
pubmed: 8423223
pmcid: 330022
doi: 10.1172/JCI116179
Schaum, N. et al. Single-cell transcriptomics of 20 mouse organs creates a Tabula Muris. Nature 562, 367–372 (2018).
pmcid: 6642641
doi: 10.1038/s41586-018-0590-4
De Micheli, A. J. et al. Single-cell analysis of the muscle stem cell hierarchy identifies heterotypic communication signals involved in skeletal muscle regeneration. Cell Rep. 30, 3583–3595.e5 (2020).
pubmed: 32160558
pmcid: 7091476
doi: 10.1016/j.celrep.2020.02.067
Fukada, S. et al. Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25, 2448–2459 (2007).
pubmed: 17600112
doi: 10.1634/stemcells.2007-0019
Low, M., Eisner, C. & Rossi, F. Fibro/Adipogenic Progenitors (FAPs): Isolation by FACS and Culture. in Muscle Stem Cells: Methods and Protocols (eds. Perdiguero, E. & Cornelison, D. D. W.) 179–189 (Springer New York, 2017). https://doi.org/10.1007/978-1-4939-6771-1_9 .
Ding, L., Saunders, T. L., Enikolopov, G. & Morrison, S. J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481, 457–462 (2012).
pubmed: 22281595
pmcid: 3270376
doi: 10.1038/nature10783
Woo, H.-H., László, C. F., Greco, S. & Chambers, S. K. Regulation of colony stimulating factor-1 expression and ovarian cancer cell behavior in vitro by miR-128 and miR-152. Mol. Cancer 11, 58 (2012).
pubmed: 22909061
pmcid: 3706266
doi: 10.1186/1476-4598-11-58
Wu, Z. et al. Regulation and function of macrophage colony-stimulating factor (CSF1) in the chicken immune system. Dev. Comp. Immunol. 105, 103586 (2020).
pubmed: 31870792
pmcid: 6996135
doi: 10.1016/j.dci.2019.103586
Scadden, D. T. The stem-cell niche as an entity of action. Nature 441, 1075–1079 (2006).
pubmed: 16810242
doi: 10.1038/nature04957
Totey, S. & Deb, K. D. Stem Cell Technologies: Basics and Applications. (McGraw-Hill Education, 2010).
Scott, R. W., Arostegui, M., Schweitzer, R., Rossi, F. M. V. & Underhill, T. M. Hic1 defines quiescent mesenchymal progenitor subpopulations with distinct functions and fates in skeletal muscle regeneration. Stem Cell 25, 797–813.e9 (2019).
Oprescu, S. N., Yue, F., Qiu, J., Brito, L. F. & Kuang, S. Temporal dynamics and heterogeneity of cell populations during skeletal muscle regeneration. iScience 23, 100993 (2020).
pubmed: 32248062
pmcid: 7125354
doi: 10.1016/j.isci.2020.100993
Capucha, T. et al. Sequential BMP7/TGF-β1 signaling and microbiota instruct mucosal Langerhans cell differentiation. J. Exp. Med. 215, 481–500 (2018).
pubmed: 29343501
pmcid: 5789418
doi: 10.1084/jem.20171508
Malsin, E. S., Kim, S., Lam, A. P. & Gottardi, C. J. Macrophages as a source and recipient of Wnt signals. Front. Immunol. 10, 1813 (2019).
pubmed: 31417574
pmcid: 6685136
doi: 10.3389/fimmu.2019.01813
Kanth, S. M., Gairhe, S. & Torabi-Parizi, P. The role of semaphorins and their receptors in innate immune responses and clinical diseases of acute inflammation. Front. Immunol. 12, 672441 (2021).
pubmed: 34012455
pmcid: 8126651
doi: 10.3389/fimmu.2021.672441
Buechler, M. B., Fu, W. & Turley, S. J. Fibroblast-macrophage reciprocal interactions in health, fibrosis, and cancer. Immunity 54, 903–915 (2021).
Voehringer, D., Liang, H.-E. & Locksley, R. M. Homeostasis and effector function of lymphopenia-induced ‘memory-like’ T cells in constitutively T cell-depleted mice. J. Immunol. 180, 4742–4753 (2008).
pubmed: 18354198
doi: 10.4049/jimmunol.180.7.4742
Hamilton, T. G., Klinghoffer, R. A., Corrin, P. D. & Soriano, P. Evolutionary divergence of platelet-derived growth factor alpha receptor signaling mechanisms. Mol. Cell Biol. 23, 4013–4025 (2003).
pubmed: 12748302
pmcid: 155222
doi: 10.1128/MCB.23.11.4013-4025.2003
Wright, D. E. et al. Cyclophosphamide/granulocyte colony-stimulating factor causes selective mobilization of bone marrow hematopoietic stem cells into the blood after M phase of the cell cycle. http://ashpublications.org/blood/article-pdf/97/8/2278/1673319/h8080102278.pdf (2001).
Kisanuki, Y. Y. et al. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230–242 (2001).
pubmed: 11161575
doi: 10.1006/dbio.2000.0106
Harris, S. E. et al. Meox2Cre-mediated disruption of CSF-1 leads to osteopetrosis and osteocyte defects. Bone 50, 42–53 (2012).
pubmed: 21958845
doi: 10.1016/j.bone.2011.09.038
Chung, M.-I., Bujnis, M., Barkauskas, C. E., Kobayashi, Y. & Hogan, B. L. M. Niche-mediated BMP/SMAD signaling regulates lung alveolar stem cell proliferation and differentiation. Development 145, dev163014 (2018).
pubmed: 29752282
pmcid: 5992594
doi: 10.1242/dev.163014
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587.e29 (2021).
pubmed: 34062119
pmcid: 8238499
doi: 10.1016/j.cell.2021.04.048