Lactation-associated macrophages exist in murine mammary tissue and human milk.
Journal
Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
received:
11
05
2021
accepted:
08
05
2023
medline:
30
6
2023
pubmed:
20
6
2023
entrez:
19
6
2023
Statut:
ppublish
Résumé
Macrophages are involved in immune defense, organogenesis and tissue homeostasis. Macrophages contribute to the different phases of mammary gland remodeling during development, pregnancy and involution postlactation. Less is known about the dynamics of mammary gland macrophages in the lactation stage. Here, we describe a macrophage population present during lactation in mice. By multiparameter flow cytometry and single-cell RNA sequencing, we identified a lactation-induced CD11c
Identifiants
pubmed: 37337103
doi: 10.1038/s41590-023-01530-0
pii: 10.1038/s41590-023-01530-0
pmc: PMC10307629
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1098-1109Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023. The Author(s).
Références
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
Blériot, C., Chakarov, S. & Ginhoux, F. Determinants of resident tissue macrophage identity and function. Immunity 52, 957–970 (2020).
pubmed: 32553181
doi: 10.1016/j.immuni.2020.05.014
Ingman, V. W., Wyckoff, J., Gouon-Evans, V., Condeelis, J. & Pollard, J. W. Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Dev. Dyn. 235, 3222–3229 (2006).
pubmed: 17029292
doi: 10.1002/dvdy.20972
Dawson, C. A. et al. Tissue-resident ductal macrophages survey the mammary epithelium and facilitate tissue remodelling. Nat. Cell Biol. 22, 546–558 (2020).
pubmed: 32341550
doi: 10.1038/s41556-020-0505-0
Gouon-Evans, V., Rothenberg, M. E. & Pollard, J. W. Postnatal mammary gland development requires macrophages and eosinophils. Development 127, 2269–2282 (2000).
pubmed: 10804170
doi: 10.1242/dev.127.11.2269
O’Brien, J., Martinson, H., Durand-Rougely, C. & Schedin, P. Macrophages are crucial for epithelial cell death and adipocyte repopulation during mammary gland involution. Development 139, 269–275 (2012).
pubmed: 22129827
doi: 10.1242/dev.071696
Pollard, J. W. & Hennighausen, L. Colony stimulating factor 1 is required for mammary gland development during pregnancy. Proc. Natl Acad. Sci. USA 91, 9312–9316 (1994).
pubmed: 7937762
pmcid: 44802
doi: 10.1073/pnas.91.20.9312
Laouar, A. Maternal leukocytes and infant immune programming during breastfeeding. Trends Immunol. 41, 225–239 (2020).
pubmed: 32057705
doi: 10.1016/j.it.2020.01.005
Boorman, K. E., Dodd, B. E. & Gunther, M. A consideration of colostrum and milk as sources of antibodies which may be transferred to the newborn baby. Arch. Dis. Child. 33, 24–29 (1958).
pubmed: 13509739
pmcid: 2012183
doi: 10.1136/adc.33.167.24
Cabinian, A. et al. Transfer of maternal immune cells by breastfeeding: maternal cytotoxic T lymphocytes present in breast milk localize in the Peyer’s patches of the nursed infant. PLoS ONE 11, e0156762 (2016).
doi: 10.1371/journal.pone.0156762
Zhou, L. et al. Two independent pathways of maternal cell transmission to offspring: through placenta during pregnancy and by breast-feeding after birth. Immunology 101, 570–580 (2000).
pubmed: 11122462
pmcid: 2327113
doi: 10.1046/j.1365-2567.2000.00144.x
Trend, S. et al. Leukocyte populations in human preterm and term breast milk identified by multicolour flow cytometry. PLoS ONE 10, e0135580 (2015).
pubmed: 26288195
pmcid: 4545889
doi: 10.1371/journal.pone.0135580
Nyquist, S. K. et al. Cellular and transcriptional diversity over the course of human lactation. Proc. Natl Acad. Sci. USA 119, e2121720119 (2022).
pubmed: 35377806
pmcid: 9169737
doi: 10.1073/pnas.2121720119
Hassiotou, F. et al. Maternal and infant infections stimulate a rapid leukocyte response in breastmilk. Clin. Transl. Immunol. 2, e3 (2013).
doi: 10.1038/cti.2013.1
Lazar, K. et al. Immunomonitoring of human breast milk cells during HCMV-reactivation. Front. Immunol. 12, 723010 (2021).
pubmed: 34566980
pmcid: 8462275
doi: 10.3389/fimmu.2021.723010
Jäppinen, N. et al. Fetal-derived macrophages dominate in adult mammary glands. Nat. Commun. 10, 281 (2019).
pubmed: 30655530
pmcid: 6336770
doi: 10.1038/s41467-018-08065-1
Hassel, C., Gausserès, B., Guzylack-Piriou, L. & Foucras, G. Ductal macrophages predominate in the immune landscape of the lactating mammary gland. Front. Immunol. 12, 754661 (2021).
pubmed: 34745127
pmcid: 8564477
doi: 10.3389/fimmu.2021.754661
Watson, C. J. & Khaled, W. T. Mammary development in the embryo and adult: a journey of morphogenesis and commitment. Development 135, 995–1003 (2008).
pubmed: 18296651
doi: 10.1242/dev.005439
Stewart, T. A., Hughes, K., Hume, D. A., Davis, F. M. & Davis, F. M. Developmental stage-specific distribution of macrophages in mouse mammary gland. Front. Cell Dev. Biol. 7, 250 (2019).
pubmed: 31709255
pmcid: 6821639
doi: 10.3389/fcell.2019.00250
Gibbings, S. L. et al. Three unique interstitial macrophages in the murine lung at steady state. Am. J. Respir. Cell Mol. Biol. 57, 66–76 (2017).
pubmed: 28257233
pmcid: 5516280
doi: 10.1165/rcmb.2016-0361OC
Chakarov, S. et al. Two distinct interstitial macrophage populations coexist across tissues in specific subtissular niches. Science 363, eaau0964 (2019).
pubmed: 30872492
doi: 10.1126/science.aau0964
Ramos, R. N. et al. Tissue-resident FOLR2
Utz, S. G. et al. Early fate defines microglia and non-parenchymal brain macrophage development. Cell 181, 557–573.e18 (2020).
pubmed: 32259484
doi: 10.1016/j.cell.2020.03.021
Masuda, T. et al. Novel Hexb-based tools for studying microglia in the CNS. Nat. Immunol. 21, 802–815 (2020).
pubmed: 32541832
doi: 10.1038/s41590-020-0707-4
Bennett, M. L. et al. New tools for studying microglia in the mouse and human CNS. Proc. Natl Acad. Sci. USA 113, E1738–E1746 (2016).
pubmed: 26884166
pmcid: 4812770
doi: 10.1073/pnas.1525528113
Liu, Z. et al. Fate mapping via Ms4a3-expression history traces monocyte-derived cells. Cell 178, 1509–1525.e19 (2019).
pubmed: 31491389
doi: 10.1016/j.cell.2019.08.009
Croxford, A. L. et al. The cytokine GM-CSF drives the inflammatory signature of CCR2
pubmed: 26341401
doi: 10.1016/j.immuni.2015.08.010
Amorim, A. et al. IFNγ and GM-CSF control complementary differentiation programs in the monocyte-to-phagocyte transition during neuroinflammation. Nat. Immunol. 23, 217–228 (2022).
Serbina, V. N. & Pamer, E. G. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311–317 (2006).
pubmed: 16462739
doi: 10.1038/ni1309
Dai, X. M. et al. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99, 111–120 (2002).
pubmed: 11756160
doi: 10.1182/blood.V99.1.111
Erblich, B., Zhu, L., Etgen, A. M., Dobrenis, K. & Pollard, J. W. Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS ONE 6, e26317 (2011).
pubmed: 22046273
pmcid: 3203114
doi: 10.1371/journal.pone.0026317
Lelios, I. et al. Emerging roles of IL-34 in health and disease. J. Exp. Med. 217, e20190290 (2020).
pubmed: 31940023
pmcid: 7062519
doi: 10.1084/jem.20190290
Greter, M. et al. Stroma-derived interleukin-34 controls the development and maintenance of Langerhans cells and the maintenance of microglia. Immunity 37, 1050–1060 (2012).
pubmed: 23177320
pmcid: 4291117
doi: 10.1016/j.immuni.2012.11.001
De Agüero, M. G. et al. The maternal microbiota drives early postnatal innate immune development. Science 351, 1296–1302 (2016).
doi: 10.1126/science.aad2571
Erny, D. et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18, 965–977 (2015).
pubmed: 26030851
pmcid: 5528863
doi: 10.1038/nn.4030
Thion, M. S. et al. Microbiome influences prenatal and adult microglia in a sex-specific manner. Cell 172, 500–516.e16 (2018).
pubmed: 29275859
pmcid: 5786503
doi: 10.1016/j.cell.2017.11.042
Honda, M. et al. Perivascular localization of macrophages in the intestinal mucosa is regulated by Nr4a1 and the microbiome. Nat. Commun. 11, 4 (2020).
doi: 10.1038/s41467-020-15068-4
Porcherie, A. et al. IL-17A is an important effector of the immune response of the mammary gland to Escherichia coli infection. J. Immunol. 196, 803–812 (2016).
pubmed: 26685206
doi: 10.4049/jimmunol.1500705
Elazar, S., Gonen, E., Livneh-Kol, A., Rosenshine, I. & Shpigel, N. Y. Essential role of neutrophils but not mammary alveolar macrophages in a murine model of acute Escherichia coli mastitis. Vet. Res. 41, 53 (2010).
pubmed: 20416261
pmcid: 2881416
doi: 10.1051/vetres/2010025
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
Elazar, S., Gonen, E., Livneh-Kol, A., Rosenshine, I. & Shpigel, N. Y. Neutrophil recruitment in endotoxin-induced murine mastitis is strictly dependent on mammary alveolar macrophages. Vet. Res. 41, 10 (2010).
pubmed: 19828114
doi: 10.1051/vetres/2009058
Mulder, K. et al. Cross-tissue single-cell landscape of human monocytes and macrophages in health and disease. Immunity 54, 1883–1900.e5 (2021).
pubmed: 34331874
doi: 10.1016/j.immuni.2021.07.007
Molgora, M. et al. TREM2 modulation remodels the tumor myeloid landscape enhancing anti-PD-1 immunotherapy. Cell 182, 886–900.e17 (2020).
pubmed: 32783918
pmcid: 7485282
doi: 10.1016/j.cell.2020.07.013
Katzenelenbogen, Y. et al. Coupled scRNA-seq and intracellular protein activity reveal an immunosuppressive role of TREM2 in cancer. Cell 182, 872–885.e19 (2020).
pubmed: 32783915
doi: 10.1016/j.cell.2020.06.032
Jaitin, D. A. et al. Lipid-associated macrophages control metabolic homeostasis in a Trem2-dependent manner. Cell 178, 686–698.e14 (2019).
pubmed: 31257031
pmcid: 7068689
doi: 10.1016/j.cell.2019.05.054
Dai, H., Wang, L., Li, L., Huang, Z. & Ye, L. Metallothionein 1: a new spotlight on inflammatory diseases. Front. Immunol. 12, 739918 (2021).
pubmed: 34804020
pmcid: 8602684
doi: 10.3389/fimmu.2021.739918
Zheng, Y. et al. Macrophage profile and homing into breast milk in response to ongoing respiratory infections in the nursing infant. Cytokine 129, 155045 (2020).
pubmed: 32109721
doi: 10.1016/j.cyto.2020.155045
Li, J., Chen, K. & Pollard, J. W. Conditional deletion of the colony stimulating factor-1 receptor (c-fms proto-oncogene) in mice. Genesis 44, 328–335 (2006).
pubmed: 16823860
doi: 10.1002/dvg.20219
Caton, M. L., Smith-Raska, M. R. & Reizis, B. Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J. Exp. Med. 204, 1653–1664 (2007).
pubmed: 17591855
pmcid: 2118632
doi: 10.1084/jem.20062648
Boring, L. et al. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100, 2552–2561 (1997).
pubmed: 9366570
pmcid: 508456
doi: 10.1172/JCI119798
Jung, S. et al. Analysis of Fractalkine Receptor CX(3)CR1 Function by Targeted Deletion and Green Fluorescent Protein Reporter Gene Insertion. Mol. Cell. Biol. 20, 4106–4114 (2000).
Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).
pubmed: 20023653
doi: 10.1038/nn.2467
McInnes, L., Healy, J., Saul, N. & Grossberger, L. UMAP: Uniform Manifold Approximation and Projection. J. Open Source Softw. 3, 861 (2018).
Van Gassen, S. et al. FlowSOM: using self-organizing maps for visualization and interpretation of cytometry data. Cytometry A 87, 636–645 (2015).
pubmed: 25573116
doi: 10.1002/cyto.a.22625
Hartmann, F. J. et al. High-dimensional single-cell analysis reveals the immune signature of narcolepsy. J. Exp. Med. 213, 2621–2633 (2016).
pubmed: 27821550
pmcid: 5110028
doi: 10.1084/jem.20160897
Mrdjen, D. et al. High-dimensional single-cell mapping of central nervous system immune cells reveals distinct myeloid subsets in health, aging, and disease. Immunity 48, 380–395.e6 (2018).
pubmed: 29426702
doi: 10.1016/j.immuni.2018.01.011
Brummelman, J. et al. Development, application and computational analysis of high-dimensional fluorescent antibody panels for single-cell flow cytometry. Nat. Protoc. 14, 1946–1969 (2019).
pubmed: 31160786
doi: 10.1038/s41596-019-0166-2
Berg, S. et al. Ilastik: interactive machine learning for (bio)image analysis. Nat. Methods 16, 1226–1232 (2019).
pubmed: 31570887
doi: 10.1038/s41592-019-0582-9
Germain, P. L., Robinson, M. D., Lun, A., Garcia Meixide, C. & Macnair, W. Doublet identification in single-cell sequencing data using scDblFinder. F1000Research 10, 979 (2022).
pmcid: 9204188
doi: 10.12688/f1000research.73600.2
Scialdone, A. et al. Computational assignment of cell-cycle stage from single-cell transcriptome data. Methods 85, 54–61 (2015).
pubmed: 26142758
doi: 10.1016/j.ymeth.2015.06.021
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
Hafemeister, C., Satija, R. Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. Genome Biol 20, 296 (2019).
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902.e21 (2019).
pubmed: 31178118
pmcid: 6687398
doi: 10.1016/j.cell.2019.05.031
Wiśniewski, J. R., Zougman, A., Nagaraj, N. & Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 6, 359–362 (2009).
pubmed: 19377485
doi: 10.1038/nmeth.1322
Türker, C. et al. B-fabric: the Swiss army knife for life sciences. In Proceedings of the 13th International Conference on Extending Database Technology 717–720 (2010).
Perez-Riverol, Y. et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2022).
pubmed: 34723319
doi: 10.1093/nar/gkab1038
Miller, J. C. et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13, 888–899 (2012).
Gautier, E. L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118–1128 (2012).