1932

Abstract

Myeloid cells are a significant proportion of leukocytes within tissues, comprising granulocytes, monocytes, dendritic cells, and macrophages. With the identification of various myeloid cells that perform separate but complementary functions during homeostasis and disease, our understanding of tissue myeloid cells has evolved significantly. Exciting findings from transcriptomics profiling and fate-mapping mouse models have facilitated the identification of their developmental origins, maturation, and tissue-specific specializations. This review highlights the current understanding of tissue myeloid cells and the contributing factors of functional heterogeneity to better comprehend the complex and dynamic immune interactions within the healthy or inflamed tissue. Specifically, we discuss the new understanding of the contributions of granulocyte-monocyte progenitor–derived phagocytes to tissue myeloid cell heterogeneity as well as the impact of niche-specific factors on monocyte and neutrophil phenotype and function. Lastly, we explore the developing paradigm of myeloid cell heterogeneity during inflammation and disease.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-immunol-081022-113627
2023-04-26
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/immunol/41/1/annurev-immunol-081022-113627.html?itemId=/content/journals/10.1146/annurev-immunol-081022-113627&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Brinkmann V, Zychlinsky A. 2007. Beneficial suicide: why neutrophils die to make NETs. Nat. Rev. Microbiol. 5:8577–82
    [Google Scholar]
  2. 2.
    Lämmermann T, Afonso PV, Angermann BR, Wang JM, Kastenmüller W et al. 2013. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498:7454371–75
    [Google Scholar]
  3. 3.
    Ley K, Hoffman HM, Kubes P, Cassatella MA, Zychlinsky A et al. 2018. Neutrophils: new insights and open questions. Sci. Immunol. 3:30eaat4579
    [Google Scholar]
  4. 4.
    Zhang Y, Wang Q, Mackay CR, Ng LG, Kwok I. 2022. Neutrophil subsets and their differential roles in viral respiratory diseases. J. Leukoc. Biol. 111:61159–73
    [Google Scholar]
  5. 5.
    St. John AL, Rathore APS, Ginhoux F 2023. New perspectives on the origins and heterogeneity of mast cells. Nat. Rev. Immunol. 23:55–68
    [Google Scholar]
  6. 6.
    Ginhoux F, Guilliams M. 2016. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44:3439–49
    [Google Scholar]
  7. 7.
    Guilliams M, Scott CL. 2017. Does niche competition determine the origin of tissue-resident macrophages?. Nat. Rev. Immunol. 17:7451–60
    [Google Scholar]
  8. 8.
    Bain CC, Bravo-Blas A, Scott CL, Perdiguero EG, Geissmann F et al. 2014. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15:10929–37
    [Google Scholar]
  9. 9.
    Ginhoux F, Greter M, Leboeuf M, Nandi S, See P et al. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:6005841–45
    [Google Scholar]
  10. 10.
    Hoeffel G, Wang Y, Greter M, See P, Teo P et al. 2012. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J. Exp. Med. 209:61167–81
    [Google Scholar]
  11. 11.
    Lee CZW, Ginhoux F. 2022. Biology of resident tissue macrophages. Development 149:8dev200270
    [Google Scholar]
  12. 12.
    Schulz C, Perdiguero EG, Chorro L, Szabo-Rogers H, Cagnard N et al. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 335:607786–90
    [Google Scholar]
  13. 13.
    Tamoutounour S, Guilliams M, Sanchis FM, Liu H, Terhorst D et al. 2013. Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39:5925–38
    [Google Scholar]
  14. 14.
    Calzetti F, Finotti G, Tamassia N, Bianchetto-Aguilera F, Castellucci M et al. 2022. CD66bCD64dimCD115 cells in the human bone marrow represent neutrophil-committed progenitors. Nat. Immunol. 23:5679–91
    [Google Scholar]
  15. 15.
    Dinh HQ, Eggert T, Meyer MA, Zhu YP, Olingy CE et al. 2020. Coexpression of CD71 and CD117 identifies an early unipotent neutrophil progenitor population in human bone marrow. Immunity 53:2319–34.e6
    [Google Scholar]
  16. 16.
    Kim M-H, Yang D, Kim M, Kim S-Y, Kim D, Kang S-J 2017. A late-lineage murine neutrophil precursor population exhibits dynamic changes during demand-adapted granulopoiesis. Sci. Rep. 7:139804
    [Google Scholar]
  17. 17.
    Kwok I, Becht E, Xia Y, Ng M, Teh YC et al. 2020. Combinatorial single-cell analyses of granulocyte-monocyte progenitor heterogeneity reveals an early uni-potent neutrophil progenitor. Immunity 53:2303–18.e5
    [Google Scholar]
  18. 18.
    Muench DE, Olsson A, Ferchen K, Pham G, Serafin RA et al. 2020. Mouse models of neutropenia reveal progenitor-stage-specific defects. Nature 582:7810109–14
    [Google Scholar]
  19. 19.
    Theilgaard-Mönch K, Pundhir S, Reckzeh K, Su J, Tapia M et al. 2022. Transcription factor-driven coordination of cell cycle exit and lineage-specification in vivo during granulocytic differentiation: in memoriam Professor Niels Borregaard. Nat. Commun. 13:13595
    [Google Scholar]
  20. 20.
    Xie X, Shi Q, Wu P, Zhang X, Kambara H et al. 2020. Single-cell transcriptome profiling reveals neutrophil heterogeneity in homeostasis and infection. Nat. Immunol. 21:91119–33
    [Google Scholar]
  21. 21.
    Zhu YP, Padgett L, Dinh HQ, Marcovecchio P, Blatchley A et al. 2018. Identification of an early unipotent neutrophil progenitor with pro-tumoral activity in mouse and human bone marrow. Cell Rep. 24:92329–41.e8
    [Google Scholar]
  22. 22.
    Deniset JF, Kubes P. 2018. Neutrophil heterogeneity: bona fide subsets or polarization states?. J. Leukoc. Biol. 103:5829–38
    [Google Scholar]
  23. 23.
    Silvestre-Roig C, Fridlender ZG, Glogauer M, Scapini P. 2019. Neutrophil diversity in health and disease. Trends Immunol. 40:7565–83
    [Google Scholar]
  24. 24.
    Ballesteros I, Rubio-Ponce A, Genua M, Lusito E, Kwok I et al. 2020. Co-option of neutrophil fates by tissue environments. Cell 183:51282–97.e18
    [Google Scholar]
  25. 25.
    Hedrick CC, Malanchi I. 2022. Neutrophils in cancer: heterogeneous and multifaceted. Nat. Rev. Immunol. 22:3173–87
    [Google Scholar]
  26. 26.
    Jaillon S, Ponzetta A, Di Mitri D, Santoni A, Bonecchi R, Mantovani A. 2020. Neutrophil diversity and plasticity in tumour progression and therapy. Nat. Rev. Cancer 20:9485–503
    [Google Scholar]
  27. 27.
    Ng LG, Ostuni R, Hidalgo A. 2019. Heterogeneity of neutrophils. Nat. Rev. Immunol. 19:4255–65
    [Google Scholar]
  28. 28.
    Quail DF, Amulic B, Aziz M, Barnes BJ, Eruslanov E et al. 2022. Neutrophil phenotypes and functions in cancer: a consensus statement. J. Exp. Med. 219:6e20220011
    [Google Scholar]
  29. 29.
    Hoeffel G, Chen J, Lavin Y, Low D, Almeida FF et al. 2015. C-Myb+ erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42:4665–78
    [Google Scholar]
  30. 30.
    McGrath KE, Frame JM, Fegan KH, Bowen JR, Conway SJ et al. 2015. Distinct sources of hematopoietic progenitors emerge before HSCs and provide functional blood cells in the mammalian embryo. Cell Rep. 11:121892–904
    [Google Scholar]
  31. 31.
    Palis J, Robertson S, Kennedy M, Wall C, Keller G. 1999. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Dev. Camb. Engl. 126:225073–84
    [Google Scholar]
  32. 32.
    Perdiguero EG, Klapproth K, Schulz C, Busch K, Azzoni E et al. 2015. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518:7540547–51
    [Google Scholar]
  33. 33.
    Hoeffel G, Ginhoux F. 2018. Fetal monocytes and the origins of tissue-resident macrophages. Cell. Immunol. 330:5–15
    [Google Scholar]
  34. 34.
    Cumano A, Godin I. 2007. Ontogeny of the hematopoietic system. Annu. Rev. Immunol. 25:1745–85
    [Google Scholar]
  35. 35.
    Sheng J, Ruedl C, Karjalainen K. 2015. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 43:2382–93
    [Google Scholar]
  36. 36.
    Traver D, Miyamoto T, Christensen JL, Iwasaki-Arai J, Akashi K, Weissman IL. 2001. Fetal liver myelopoiesis occurs through distinct, prospectively isolatable progenitor subsets. Blood 98:3627–35
    [Google Scholar]
  37. 37.
    Ito K, Frenette PS. 2016. HSC contribution in making steady-state blood. Immunity 45:3464–66
    [Google Scholar]
  38. 38.
    Sawai CM, Babovic S, Upadhaya S, Knapp DJHF, Lavin Y et al. 2016. Hematopoietic stem cells are the major source of multilineage hematopoiesis in adult animals. Immunity 45:3597–609
    [Google Scholar]
  39. 39.
    Busch K, Klapproth K, Barile M, Flossdorf M, Holland-Letz T et al. 2015. Fundamental properties of unperturbed haematopoiesis from stem cells in vivo. Nature 518:7540542–46
    [Google Scholar]
  40. 40.
    Sun J, Ramos A, Chapman B, Johnnidis JB, Le L et al. 2014. Clonal dynamics of native haematopoiesis. Nature 514:7522322–27
    [Google Scholar]
  41. 41.
    Pietras EM, Reynaud D, Kang Y-A, Carlin D, Calero-Nieto FJ et al. 2015. Functionally distinct subsets of lineage-biased multipotent progenitors control blood production in normal and regenerative conditions. Cell Stem Cell 17:135–46
    [Google Scholar]
  42. 42.
    Akashi K, Traver D, Miyamoto T, Weissman IL. 2000. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404:6774193–97
    [Google Scholar]
  43. 43.
    Iwasaki H, Mizuno S, Arinobu Y, Ozawa H, Mori Y et al. 2006. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev. 20:213010–21
    [Google Scholar]
  44. 44.
    Zhang P, Iwasaki-Arai J, Iwasaki H, Fenyus ML, Dayaram T et al. 2004. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBPα. Immunity 21:6853–63
    [Google Scholar]
  45. 45.
    Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P et al. 2006. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311:575783–87
    [Google Scholar]
  46. 46.
    Auffray C, Fogg DK, Narni-Mancinelli E, Senechal B, Trouillet C et al. 2009. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 206:3595–606
    [Google Scholar]
  47. 47.
    Hettinger J, Richards DM, Hansson J, Barra MM, Joschko A-C et al. 2013. Origin of monocytes and macrophages in a committed progenitor. Nat. Immunol. 14:8821–30
    [Google Scholar]
  48. 48.
    Yáñez A, Ng MY, Hassanzadeh-Kiabi N, Goodridge HS. 2015. IRF8 acts in lineage-committed rather than oligopotent progenitors to control neutrophil versus monocyte production. Blood 125:91452–59
    [Google Scholar]
  49. 49.
    Sathe P, Metcalf D, Vremec D, Naik SH, Langdon WY et al. 2014. Lymphoid tissue and plasmacytoid dendritic cells and macrophages do not share a common macrophage-dendritic cell-restricted progenitor. Immunity 41:1104–15
    [Google Scholar]
  50. 50.
    Ginhoux F, Jung S 2014. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14:6392–404
    [Google Scholar]
  51. 51.
    Zhu YP, Thomas GD, Hedrick CC. 2016. Transcriptional control of monocyte development. Arterioscler. Thromb. Vasc. Biol. 36:91722–33
    [Google Scholar]
  52. 52.
    Guilliams M, Mildner A, Yona S. 2018. Developmental and functional heterogeneity of monocytes. Immunity 49:4595–613
    [Google Scholar]
  53. 53.
    Giladi A, Paul F, Herzog Y, Lubling Y, Weiner A et al. 2018. Single-cell characterization of haematopoietic progenitors and their trajectories in homeostasis and perturbed haematopoiesis. Nat. Cell Biol. 20:7836–46
    [Google Scholar]
  54. 54.
    Notta F, Zandi S, Takayama N, Dobson S, Gan OI et al. 2016. Distinct routes of lineage development reshape the human blood hierarchy across ontogeny. Science 351:6269aab2116
    [Google Scholar]
  55. 55.
    Paul F, Arkin Y, Giladi A, Jaitin DA, Kenigsberg E et al. 2015. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163:71663–77
    [Google Scholar]
  56. 56.
    Yáñez A, Coetzee SG, Olsson A, Muench DE, Berman BP et al. 2017. Granulocyte-monocyte progenitors and monocyte-dendritic cell progenitors independently produce functionally distinct monocytes. Immunity 47:5890–902.e4
    [Google Scholar]
  57. 57.
    Liu Z, Gu Y, Chakarov S, Bleriot C, Kwok I et al. 2019. Fate mapping via Ms4a3-expression history traces monocyte-derived cells. Cell 178:61509–25.e19
    [Google Scholar]
  58. 58.
    Menezes S, Melandri D, Anselmi G, Perchet T, Loschko J et al. 2016. The heterogeneity of Ly6Chi monocytes controls their differentiation into iNOS+ macrophages or monocyte-derived dendritic cells. Immunity 45:61205–18
    [Google Scholar]
  59. 59.
    Mildner A, Schönheit J, Giladi A, David E, Lara-Astiaso D et al. 2017. Genomic characterization of murine monocytes reveals C/EBPβ transcription factor dependence of Ly6C cells. Immunity 46:5849–62.e7
    [Google Scholar]
  60. 60.
    Ikeda N, Asano K, Kikuchi K, Uchida Y, Ikegami H et al. 2018. Emergence of immunoregulatory Ym1+Ly6Chi monocytes during recovery phase of tissue injury. Sci. Immunol. 3:28eaat0207
    [Google Scholar]
  61. 61.
    Shibuya T, Kamiyama A, Sawada H, Kikuchi K, Maruyama M et al. 2021. Immunoregulatory monocyte subset promotes metastasis associated with therapeutic intervention for primary tumor. Front. Immunol. 12:663115
    [Google Scholar]
  62. 62.
    Drissen R, Buza-Vidas N, Woll P, Thongjuea S, Gambardella A et al. 2016. Distinct myeloid progenitor-differentiation pathways identified through single-cell RNA sequencing. Nat. Immunol. 17:6666–76
    [Google Scholar]
  63. 63.
    Olsson A, Venkatasubramanian M, Chaudhri VK, Aronow BJ, Salomonis N et al. 2016. Single-cell analysis of mixed-lineage states leading to a binary cell fate choice. Nature 537:7622698–702
    [Google Scholar]
  64. 64.
    Bourdely P, Anselmi G, Vaivode K, Ramos RN, Missolo-Koussou Y et al. 2020. Transcriptional and functional analysis of CD1c+ human dendritic cells identifies a CD163+ subset priming CD8+CD103+ T cells. Immunity 53:2335–52.e8
    [Google Scholar]
  65. 65.
    Cytlak U, Resteu A, Pagan S, Green K, Milne P et al. 2020. Differential IRF8 transcription factor requirement defines two pathways of dendritic cell development in humans. Immunity 53:2353–70.e8
    [Google Scholar]
  66. 66.
    Dutertre CA, Becht E, Irac SE, Khalilnezhad A, Narang V et al. 2019. Single-cell analysis of human mononuclear phagocytes reveals subset-defining markers and identifies circulating inflammatory dendritic cells. Immunity 51:3573–89.e8
    [Google Scholar]
  67. 67.
    Rieger MA, Hoppe PS, Smejkal BM, Eitelhuber AC, Schroeder T. 2009. Hematopoietic cytokines can instruct lineage choice. Science 325:5937217–18
    [Google Scholar]
  68. 68.
    Askenase MH, Han SJ, Byrd AL, Morais da Fonseca D, Bouladoux N et al. 2015. Bone-marrow-resident NK cells prime monocytes for regulatory function during infection. Immunity 42:61130–42
    [Google Scholar]
  69. 69.
    Buchmeier NA, Schreiber RD. 1985. Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. PNAS 82:217404–8
    [Google Scholar]
  70. 70.
    de Bruin AM, Libregts SF, Valkhof M, Boon L, Touw IP, Nolte MA. 2012. IFNγ induces monopoiesis and inhibits neutrophil development during inflammation. Blood 119:61543–54
    [Google Scholar]
  71. 71.
    Gore AV, Pillay LM, Galanternik MV, Weinstein BM. 2018. The zebrafish: a fintastic model for hematopoietic development and disease. Wiley Interdiscip. Rev. Dev. Biol. 7:3e312
    [Google Scholar]
  72. 72.
    Wittamer V, Bertrand JY, Gutschow PW, Traver D 2011. Characterization of the mononuclear phagocyte system in zebrafish. Blood 117:267126–35
    [Google Scholar]
  73. 73.
    Tong R, Pan L, Zhang X, Li Y. 2022. Neuroendocrine-immune regulation mechanism in crustaceans: a review. Rev. Aquaculture 14:1378–98
    [Google Scholar]
  74. 74.
    Hérault A, Binnewies M, Leong S, Calero-Nieto FJ, Zhang SY et al. 2017. Myeloid progenitor cluster formation drives emergency and leukaemic myelopoiesis. Nature 544:764853–58
    [Google Scholar]
  75. 75.
    Chavakis T, Mitroulis I, Hajishengallis G. 2019. Hematopoietic progenitor cells as integrative hubs for adaptation to and fine-tuning of inflammation. Nat. Immunol. 20:7802–11
    [Google Scholar]
  76. 76.
    Christensen JL, Wright DE, Wagers AJ, Weissman IL. 2004. Circulation and chemotaxis of fetal hematopoietic stem cells. PLOS Biol. 2:3e75
    [Google Scholar]
  77. 77.
    Liu Y, Chen Q, Jeong H-W, Koh BI, Watson EC et al. 2022. A specialized bone marrow microenvironment for fetal haematopoiesis. Nat. Commun. 13:11327
    [Google Scholar]
  78. 78.
    Cordeiro Gomes A, Hara T, Lim VY, Herndler-Brandstetter D, Nevius E et al. 2016. Hematopoietic stem cell niches produce lineage-instructive signals to control multipotent progenitor differentiation. Immunity 45:61219–31
    [Google Scholar]
  79. 79.
    Greenbaum A, Hsu YMS, Day RB, Schuettpelz LG, Christopher MJ et al. 2013. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495:7440227–30
    [Google Scholar]
  80. 80.
    Zhou BO, Yu H, Yue R, Zhao Z, Rios JJ et al. 2017. Bone marrow adipocytes promote the regeneration of stem cells and haematopoiesis by secreting SCF. Nat. Cell Biol. 19:8891–903
    [Google Scholar]
  81. 81.
    Arinobu Y, Iwasaki H, Gurish MF, Mizuno SI, Shigematsu H et al. 2005. Developmental checkpoints of the basophil/mast cell lineages in adult murine hematopoiesis. PNAS 102:5018105–10
    [Google Scholar]
  82. 82.
    Dress RJ, Dutertre CA, Giladi A, Schlitzer A, Low I et al. 2019. Plasmacytoid dendritic cells develop from Ly6D+ lymphoid progenitors distinct from the myeloid lineage. Nat. Immunol. 20:7852–64
    [Google Scholar]
  83. 83.
    Iwasaki H, Mizuno SI, Mayfield R, Shigematsu H, Arinobu Y et al. 2005. Identification of eosinophil lineage-committed progenitors in the murine bone marrow. J. Exp. Med. 201:121891–97
    [Google Scholar]
  84. 84.
    See P, Dutertre CA, Chen J, Günther P, McGovern N et al. 2017. Mapping the human DC lineage through the integration of high-dimensional techniques. Science 356:6342eaag3009
    [Google Scholar]
  85. 85.
    Wanet A, Bassal MA, Patel SB, Marchi F, Mariani SA et al. 2021. E-cadherin is regulated by GATA-2 and marks the early commitment of mouse hematopoietic progenitors to the basophil and mast cell fates. Sci. Immunol. 6:56eaba0178
    [Google Scholar]
  86. 86.
    McAlpine CS, Kiss MG, Rattik S, He S, Vassalli A et al. 2019. Sleep modulates haematopoiesis and protects against atherosclerosis. Nature 566:7744383–87
    [Google Scholar]
  87. 87.
    Evrard M, Kwok IWH, Chong SZ, Teng KWW, Becht E et al. 2018. Developmental analysis of bone marrow neutrophils reveals populations specialized in expansion, trafficking, and effector functions. Immunity 48:2364–79.e8
    [Google Scholar]
  88. 88.
    Zhang J, Wu Q, Johnson CB, Pham G, Kinder JM et al. 2021. In situ mapping identifies distinct vascular niches for myelopoiesis. Nature 590:7846457–62
    [Google Scholar]
  89. 89.
    Teh YC, Chooi MY, Liu D, Kwok I, Lai GC et al. 2022. Transitional premonocytes emerge in the periphery for host defense against bacterial infections. Sci. Adv. 8:9eabj4641
    [Google Scholar]
  90. 90.
    Schulte-Schrepping J, Reusch N, Paclik D, Baßler K, Schlickeiser S et al. 2020. Severe COVID-19 is marked by a dysregulated myeloid cell compartment. Cell 182:61419–40.e23
    [Google Scholar]
  91. 91.
    Silvin A, Chapuis N, Dunsmore G, Goubet A-G, Dubuisson A et al. 2020. Elevated calprotectin and abnormal myeloid cell subsets discriminate severe from mild COVID-19. Cell 182:61401–18.e18
    [Google Scholar]
  92. 92.
    Short C, Lim HK, Tan J, O'Neill HC. 2019. Targeting the spleen as an alternative site for hematopoiesis. BioEssays 41:51800234
    [Google Scholar]
  93. 93.
    Dias S, Silva H, Cumano A, Vieira P. 2005. Interleukin-7 is necessary to maintain the B cell potential in common lymphoid progenitors. J. Exp. Med. 201:6971–79
    [Google Scholar]
  94. 94.
    Dutta P, Hoyer FF, Grigoryeva LS, Sager HB, Leuschner F et al. 2015. Macrophages retain hematopoietic stem cells in the spleen via VCAM-1. J. Exp. Med. 212:4497–512
    [Google Scholar]
  95. 95.
    Oda A, Tezuka T, Ueno Y, Hosoda S, Amemiya Y et al. 2018. Niche-induced extramedullary hematopoiesis in the spleen is regulated by the transcription factor Tlx1. Sci. Rep. 8:18308
    [Google Scholar]
  96. 96.
    Vasamsetti SB, Florentin J, Coppin E, Stiekema LCA, Zheng KH et al. 2018. Sympathetic neuronal activation triggers myeloid progenitor proliferation and differentiation. Immunity 49:193–106.e7
    [Google Scholar]
  97. 97.
    Acar M, Kocherlakota KS, Murphy MM, Peyer JG, Oguro H et al. 2015. Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal. Nature 526:7571126–30
    [Google Scholar]
  98. 98.
    Baccin C, Al-Sabah J, Velten L, Helbling PM, Grünschläger F et al. 2020. Combined single-cell and spatial transcriptomics reveal the molecular, cellular and spatial bone marrow niche organization. Nat. Cell Biol. 22:138–48
    [Google Scholar]
  99. 99.
    Inra CN, Zhou BO, Acar M, Murphy MM, Richardson J et al. 2015. A perisinusoidal niche for extramedullary haematopoiesis in the spleen. Nature 527:7579466–71
    [Google Scholar]
  100. 100.
    Veglia F, Perego M, Gabrilovich D. 2018. Myeloid-derived suppressor cells coming of age. Nat. Immunol. 19:2108–19
    [Google Scholar]
  101. 101.
    Wu C, Ning H, Liu M, Lin J, Luo S et al. 2018. Spleen mediates a distinct hematopoietic progenitor response supporting tumor-promoting myelopoiesis. J. Clin. Investig. 128:83425–38
    [Google Scholar]
  102. 102.
    Liu M, Wu C, Luo S, Hua Q, Chen H-T et al. 2022. PERK reprograms hematopoietic progenitor cells to direct tumor-promoting myelopoiesis in the spleen. J. Exp. Med. 219:4e20211498 Erratum 2022. J. Exp. Med. 219:7jem.2021149805312022c
    [Google Scholar]
  103. 103.
    Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V et al. 2009. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325:5940612–16
    [Google Scholar]
  104. 104.
    Robbins CS, Chudnovskiy A, Rauch PJ, Figueiredo J-L, Iwamoto Y et al. 2012. Extramedullary hematopoiesis generates Ly-6Chigh monocytes that infiltrate atherosclerotic lesions. Circulation 125:2364–74
    [Google Scholar]
  105. 105.
    Sabatel C, Radermecker C, Fievez L, Paulissen G, Chakarov S et al. 2017. Exposure to bacterial CpG DNA protects from airway allergic inflammation by expanding regulatory lung interstitial macrophages. Immunity 46:3457–73
    [Google Scholar]
  106. 106.
    Deniset JF, Surewaard BG, Lee W-Y, Kubes P. 2017. Splenic Ly6Ghigh mature and Ly6Gint immature neutrophils contribute to eradication of S. pneumoniae. J. Exp. Med. 214:51333–50
    [Google Scholar]
  107. 107.
    Puga I, Cols M, Barra CM, He B, Cassis L et al. 2011. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat. Immunol. 13:2170–80
    [Google Scholar]
  108. 108.
    Chorny A, Casas-Recasens S, Sintes J, Shan M, Polentarutti N et al. 2016. The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells. J. Exp. Med. 213:102167–85
    [Google Scholar]
  109. 109.
    Magri G, Miyajima M, Bascones S, Mortha A, Puga I et al. 2014. Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat. Immunol. 15:4354–64
    [Google Scholar]
  110. 110.
    Scapini P, Cassatella MA. 2017. Location in the spleen dictates the function of murine neutrophils. J. Exp. Med. 214:51207–9
    [Google Scholar]
  111. 111.
    Hägglöf T, Sedimbi SK, Yates JL, Parsa R, Salas BH et al. 2016. Neutrophils license iNKT cells to regulate self-reactive mouse B cell responses. Nat. Immunol. 17:121407–14
    [Google Scholar]
  112. 112.
    Ince LM, Weber J, Scheiermann C. 2019. Control of leukocyte trafficking by stress-associated hormones. Front. Immunol. 9:3143
    [Google Scholar]
  113. 113.
    Devi S, Wang Y, Chew WK, Lima R, A-González N et al. 2013. Neutrophil mobilization via plerixafor-mediated CXCR4 inhibition arises from lung demargination and blockade of neutrophil homing to the bone marrow. J. Exp. Med. 210:112321–36
    [Google Scholar]
  114. 114.
    Ricci E, Ronchetti S, Gabrielli E, Pericolini E, Gentili M et al. 2019. GILZ restrains neutrophil activation by inhibiting the MAPK pathway. J. Leukoc. Biol. 105:187–94
    [Google Scholar]
  115. 115.
    Bajrami B, Zhu H, Kwak H-J, Mondal S, Hou Q et al. 2016. G-CSF maintains controlled neutrophil mobilization during acute inflammation by negatively regulating CXCR2 signaling. J. Exp. Med. 213:101999–2018
    [Google Scholar]
  116. 116.
    Adrover JM, del Fresno C, Crainiciuc G, Cuartero MI, Casanova-Acebes M et al. 2019. A neutrophil timer coordinates immune defense and vascular protection. Immunity 50:2390–402.e10
    [Google Scholar]
  117. 117.
    Casanova-Acebes M, Pitaval C, Weiss LA, Nombela-Arrieta C, Chèvre R et al. 2013. Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell 153:51025–35
    [Google Scholar]
  118. 118.
    Zhang D, Chen G, Manwani D, Mortha A, Xu C et al. 2015. Neutrophil ageing is regulated by the microbiome. Nature 525:7570528–32
    [Google Scholar]
  119. 119.
    van Furth R, Cohn Z, Hirsch J, Humphrey J, Spector W, Langevoort H. 1972. The mononuclear phagocyte system: a new classification of macrophages, monocytes, and their precursor cells. Bull. World Health Organ. 46:6845–52
    [Google Scholar]
  120. 120.
    van Furth R, Cohn ZA. 1968. The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 128:3415–35
    [Google Scholar]
  121. 121.
    Geissmann F, Jung S, Littman DR 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:171–82
    [Google Scholar]
  122. 122.
    Yona S, Kim KW, Wolf Y, Mildner A, Varol D et al. 2013. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38:51073–79
    [Google Scholar]
  123. 123.
    Hanna RN, Carlin LM, Hubbeling HG, Nackiewicz D, Green AM et al. 2011. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C monocytes. Nat. Immunol. 12:8778–85
    [Google Scholar]
  124. 124.
    Carlin LM, Stamatiades EG, Auffray C, Hanna RN, Glover L et al. 2013. Nr4a1-dependent Ly6Clow monocytes monitor endothelial cells and orchestrate their disposal. Cell 153:2362–75
    [Google Scholar]
  125. 125.
    Hamers AAJ, Vos M, Rassam F, Marinković G, Kurakula K et al. 2012. Bone marrow-specific deficiency of nuclear receptor Nur77 enhances atherosclerosis. Circ. Res. 110:3428–38
    [Google Scholar]
  126. 126.
    Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T et al. 2007. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204:123037–47
    [Google Scholar]
  127. 127.
    Amorim A, De Feo D, Friebel E, Ingelfinger F, Anderfuhren CD et al. 2022. IFNγ and GM-CSF control complementary differentiation programs in the monocyte-to-phagocyte transition during neuroinflammation. Nat. Immunol. 23:2217–28
    [Google Scholar]
  128. 128.
    Hoffman D, Tevet Y, Trzebanski S, Rosenberg G, Vainman L et al. 2021. A non-classical monocyte-derived macrophage subset provides a splenic replication niche for intracellular Salmonella. Immunity 54:122712–2723.e6
    [Google Scholar]
  129. 129.
    Olingy CE, San Emeterio CL, Ogle ME, Krieger JR, Bruce AC et al. 2017. Non-classical monocytes are biased progenitors of wound healing macrophages during soft tissue injury. Sci. Rep. 7:1447
    [Google Scholar]
  130. 130.
    Wright DE, Wagers AJ, Gulati AP, Johnson FL, Weissman IL. 2001. Physiological migration of hematopoietic stem and progenitor cells. Science 294:55481933–36
    [Google Scholar]
  131. 131.
    Wright DE, Bowman EP, Wagers AJ, Butcher EC, Weissman IL. 2002. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J. Exp. Med. 195:91145–54
    [Google Scholar]
  132. 132.
    Massberg S, Schaerli P, Knezevic-Maramica I, Köllnberger M, Tubo N et al. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131:5994–1008
    [Google Scholar]
  133. 133.
    Chong SZ, Evrard M, Devi S, Chen J, Lim JY et al. 2016. CXCR4 identifies transitional bone marrow premonocytes that replenish the mature monocyte pool for peripheral responses. J. Exp. Med. 213:112293–314
    [Google Scholar]
  134. 134.
    Serrano-Lopez J, Hegde S, Kumar S, Serrano J, Fang J et al. 2021. Inflammation rapidly recruits mammalian GMP and MDP from bone marrow into regional lymphatics. eLife 10:e66190
    [Google Scholar]
  135. 135.
    Mass E, Ballesteros I, Farlik M, Halbritter F, Günther P et al. 2016. Specification of tissue-resident macrophages during organogenesis. Science 353:6304aaf4238
    [Google Scholar]
  136. 136.
    Park MD, Silvin A, Ginhoux F, Merad M. 2022. Macrophages in health and disease. Cell 185:234259–79
    [Google Scholar]
  137. 137.
    Epelman S, Lavine KJ, Randolph GJ. 2014. Origin and functions of tissue macrophages. Immunity 41:121–35
    [Google Scholar]
  138. 138.
    Gautier EL, Shay T, Miller J, Greter M, Jakubzick C et al. 2012. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13:111118–28
    [Google Scholar]
  139. 139.
    Lavin Y, Winter DR, Blecher-Gonen R, David E, Keren-Shaul H et al. 2014. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159:61312–26
    [Google Scholar]
  140. 140.
    Blériot C, Chakarov S, Ginhoux F. 2020. Determinants of resident tissue macrophage identity and function. Immunity 52:6957–70
    [Google Scholar]
  141. 141.
    Kornberg TB. 2017. Macrophages help cells connect to pattern zebrafish stripes. Dev. Cell 40:6520–21
    [Google Scholar]
  142. 142.
    Baranska A, Shawket A, Jouve M, Baratin M, Malosse C et al. 2018. Unveiling skin macrophage dynamics explains both tattoo persistence and strenuous removal. J. Exp. Med. 215:41115–33
    [Google Scholar]
  143. 143.
    Schyns J, Bureau F, Marichal T. 2018. Lung interstitial macrophages: past, present, and future. Clin. Dev. Immunol. 2018:5160794
    [Google Scholar]
  144. 144.
    Kohyama M, Ise W, Edelson BT, Wilker PR, Hildner K et al. 2009. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457:7227318–21
    [Google Scholar]
  145. 145.
    DeFalco T, Potter SJ, Williams AV, Waller B, Kan MJ, Capel B. 2015. Macrophages contribute to the spermatogonial niche in the adult testis. Cell Rep. 12:71107–19
    [Google Scholar]
  146. 146.
    Squarzoni P, Oller G, Hoeffel G, Pont-Lezica L, Rostaing P et al. 2014. Microglia modulate wiring of the embryonic forebrain. Cell Rep. 8:51271–79
    [Google Scholar]
  147. 147.
    Casanova-Acebes M, Nicolás-Ávila , Li JL, García-Silva S, Balachander A et al. 2018. Neutrophils instruct homeostatic and pathological states in naive tissues. J. Exp. Med. 215:112778–95
    [Google Scholar]
  148. 148.
    Kolaczkowska E, Kubes P. 2013. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13:3159–75
    [Google Scholar]
  149. 149.
    Aegerter H, Kulikauskaite J, Crotta S, Patel H, Kelly G et al. 2020. Influenza-induced monocyte-derived alveolar macrophages confer prolonged antibacterial protection. Nat. Immunol. 21:2145–57
    [Google Scholar]
  150. 150.
    Lambrecht BN. 2006. Alveolar macrophage in the driver's seat. Immunity 24:4366–68
    [Google Scholar]
  151. 151.
    Schneider C, Nobs SP, Heer AK, Kurrer M, Klinke G et al. 2014. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLOS Pathog. 10:4e1004053
    [Google Scholar]
  152. 152.
    Machiels B, Dourcy M, Xiao X, Javaux J, Mesnil C et al. 2017. A gammaherpesvirus provides protection against allergic asthma by inducing the replacement of resident alveolar macrophages with regulatory monocytes. Nat. Immunol. 18:121310–20
    [Google Scholar]
  153. 153.
    Yao Y, Jeyanathan M, Haddadi S, Barra NG, Vaseghi-Shanjani M et al. 2018. Induction of autonomous memory alveolar macrophages requires T cell help and is critical to trained immunity. Cell 175:61634–50
    [Google Scholar]
  154. 154.
    Chakarov S, Lim HY, Tan L, Lim SY, See P et al. 2019. Two distinct interstitial macrophage populations coexist across tissues in specific subtissular niches. Science 363:6432eaau0964
    [Google Scholar]
  155. 155.
    Chen Q, Ruedl C. 2020. Obesity retunes turnover kinetics of tissue-resident macrophages in fat. J. Leukoc. Biol. 107:5773–82
    [Google Scholar]
  156. 156.
    Cox N, Crozet L, Holtman IR, Loyher P-L, Lazarov T et al. 2021. Diet-regulated production of PDGFcc by macrophages controls energy storage. Science 373:6550eabe9383
    [Google Scholar]
  157. 157.
    Ichimura H, Parthasarathi K, Issekutz AC, Bhattacharya J. 2005. Pressure-induced leukocyte margination in lung postcapillary venules. Am. J. Physiol. Lung Cell. Mol. Physiol. 289:3L407–12
    [Google Scholar]
  158. 158.
    Kuebler WM, Goetz AE. 2002. The marginated pool. Eur. Surg. Res. 34:92–100
    [Google Scholar]
  159. 159.
    Peters AM, Allsop P, Stuttle AWJ, Arnot RN, Gwilliam ME, Hall GM. 1992. Granulocyte margination in the human lung and its response to strenuous exercise. Clin. Sci. 82:2237–44
    [Google Scholar]
  160. 160.
    Doerschuk CM. 2000. Leukocyte trafficking in alveoli and airway passages. Respir. Res. 1:3136–40
    [Google Scholar]
  161. 161.
    Yipp BG, Kim JH, Lima R, Zbytnuik LD, Petri B et al. 2017. The lung is a host defense niche for immediate neutrophil-mediated vascular protection. Sci. Immunol. 2:10eaam8929
    [Google Scholar]
  162. 162.
    Kim JH, Podstawka J, Lou Y, Li L, Lee EKS et al. 2018. Aged polymorphonuclear leukocytes cause fibrotic interstitial lung disease in the absence of regulation by B cells. Nat. Immunol. 19:2192–201
    [Google Scholar]
  163. 163.
    Uhl B, Vadlau Y, Zuchtriegel G, Nekolla K, Sharaf K et al. 2016. Aged neutrophils contribute to the first line of defense in the acute inflammatory response. Blood 128:192327–37
    [Google Scholar]
  164. 164.
    von Kupffer C. 1876. Ueber Sternzellen der leber. Arch. Für Mikrosk. Anat. 12:1353–58
    [Google Scholar]
  165. 165.
    Krenkel O, Tacke F. 2017. Liver macrophages in tissue homeostasis and disease. Nat. Rev. Immunol. 17:5306–21
    [Google Scholar]
  166. 166.
    Gola A, Dorrington MG, Speranza E, Sala C, Shih RM et al. 2021. Commensal-driven immune zonation of the liver promotes host defence. Nature 589:7840131–36
    [Google Scholar]
  167. 167.
    Scott CL, Zheng F, De Baetselier P, Martens L, Saeys Y et al. 2016. Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells. Nat. Commun. 7:110321
    [Google Scholar]
  168. 168.
    Bonnardel J, T'Jonck W, Gaublomme D, Browaeys R, Scott CL et al. 2019. Stellate cells, hepatocytes, and endothelial cells imprint the Kupffer cell identity on monocytes colonizing the liver macrophage niche. Immunity 51:4638–54
    [Google Scholar]
  169. 169.
    Scott CL, T'Jonck W, Martens L, Todorov H, Sichien D et al. 2018. The transcription factor ZEB2 is required to maintain the tissue-specific identities of macrophages. Immunity 49:2312–25
    [Google Scholar]
  170. 170.
    Sakai M, Troutman TD, Seidman JS, Ouyang Z, Spann NJ et al. 2019. Liver-derived signals sequentially reprogram myeloid enhancers to initiate and maintain Kupffer cell identity. Immunity 51:4655–70.e8
    [Google Scholar]
  171. 171.
    Beattie L, Sawtell A, Mann JL, Frame TCM, Teal BE et al. 2016. Bone marrow-derived and resident liver macrophages display unique transcriptomic signatures but similar biological functions. J. Hepatol. 65:4758–68
    [Google Scholar]
  172. 172.
    Misharin AV, Morales-Nebreda L, Reyfman PA, Cuda CM, Walter JM et al. 2017. Monocyte-derived alveolar macrophages drive lung fibrosis and persist in the lung over the life span. J. Exp. Med. 214:82387–404
    [Google Scholar]
  173. 173.
    Heymann F, Peusquens J, Ludwig-Portugall I, Kohlhepp M, Ergen C et al. 2015. Liver inflammation abrogates immunological tolerance induced by Kupffer cells. Hepatology 62:1279–91
    [Google Scholar]
  174. 174.
    Tran S, Baba I, Poupel L, Dussaud S, Moreau M et al. 2020. Impaired Kupffer cell self-renewal alters the liver response to lipid overload during non-alcoholic steatohepatitis. Immunity 53:3627–40.e5
    [Google Scholar]
  175. 175.
    Remmerie A, Martens L, Thoné T, Castoldi A, Seurinck R et al. 2020. Osteopontin expression identifies a subset of recruited macrophages distinct from Kupffer cells in the fatty liver. Immunity 53:3641–57.e14
    [Google Scholar]
  176. 176.
    Jaitin D, Adlung L, Thaiss CA, Weiner A, Li B et al. 2019. Lipid-associated macrophages control metabolic homeostasis in a Trem2-dependent manner. Cell 178:3686–98.e14
    [Google Scholar]
  177. 177.
    Zigmond E, Samia-Grinberg S, Pasmanik-Chor M, Brazowski E, Shibolet O et al. 2014. Infiltrating monocyte-derived macrophages and resident Kupffer cells display different ontogeny and functions in acute liver injury. J. Immunol. 193:1344–53
    [Google Scholar]
  178. 178.
    David BA, Rezende RM, Antunes MM, Santos MM, Lopes MAF et al. 2016. Combination of mass cytometry and imaging analysis reveals origin, location, and functional repopulation of liver myeloid cells in mice. Gastroenterology 151:61176–91
    [Google Scholar]
  179. 179.
    Blériot C, Barreby E, Dunsmore G, Ballaire R, Chakarov S et al. 2021. A subset of Kupffer cells regulates metabolism through the expression of CD36. Immunity 54:92101–16.e6
    [Google Scholar]
  180. 180.
    De Simone G, Andreata F, Bleriot C, Fumagalli V, Laura C et al. 2021. Identification of a Kupffer cell subset capable of reverting the T cell dysfunction induced by hepatocellular priming. Immunity 54:92089–100.e8
    [Google Scholar]
  181. 181.
    MacParland SA, Liu JC, Zhong X, Innes BT, Bartczak A et al. 2018. Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations. Nat. Commun. 9:14383
    [Google Scholar]
  182. 182.
    Sierro F, Evrard M, Rizzetto S, Melino M, Mitchell AJ et al. 2017. A liver capsular network of monocyte-derived macrophages restricts hepatic dissemination of intraperitoneal bacteria by neutrophil recruitment. Immunity 47:2374–88.e6
    [Google Scholar]
  183. 183.
    Prickett TCR, Mckenzie JL, Hart DNJ. 1988. Characterization of interstitial dendritic cells in human liver. Transplantation 46:5754–61
    [Google Scholar]
  184. 184.
    Wang J, Kubes P. 2016. A reservoir of mature cavity macrophages that can rapidly invade visceral organs to affect tissue repair. Cell 165:3668–78
    [Google Scholar]
  185. 185.
    Jin H, Liu K, Tang J, Huang X, Wang H et al. 2021. Genetic fate-mapping reveals surface accumulation but not deep organ invasion of pleural and peritoneal cavity macrophages following injury. Nat. Commun. 12:12863
    [Google Scholar]
  186. 186.
    McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I et al. 2010. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330:6002362–66
    [Google Scholar]
  187. 187.
    Wang J, Hossain M, Thanabalasuriar A, Gunzer M, Meininger C, Kubes P. 2017. Visualizing the function and fate of neutrophils in sterile injury and repair. Science 358:6359111–16
    [Google Scholar]
  188. 188.
    Merad M, Manz MG, Karsunky H, Wagers AJ, Peters W et al. 2002. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3:121135–41
    [Google Scholar]
  189. 189.
    Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB et al. 2013. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38:4792–804
    [Google Scholar]
  190. 190.
    Doebel T, Voisin B, Nagao K. 2017. Langerhans cells—the macrophage in dendritic cell clothing. Trends Immunol. 38:11817–28
    [Google Scholar]
  191. 191.
    Malissen B, Tamoutounour S, Henri S 2014. The origins and functions of dendritic cells and macrophages in the skin. Nat. Rev. Immunol. 14:6417–28
    [Google Scholar]
  192. 192.
    Ginhoux F, Tacke F, Angeli V, Bogunovic M, Loubeau M et al. 2006. Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7:3265–73
    [Google Scholar]
  193. 193.
    Jakubzick C, Gautier EL, Gibbings SL, Sojka DK, Schlitzer A et al. 2013. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39:3599–610
    [Google Scholar]
  194. 194.
    Kolter J, Feuerstein R, Zeis P, Hagemeyer N, Paterson N et al. 2019. A subset of skin macrophages contributes to the surveillance and regeneration of local nerves. Immunity 50:61482–97.e7
    [Google Scholar]
  195. 195.
    Goh CC, Evrard M, Chong SZ, Tan Y, Tan LDL et al. 2018. The impact of ischemia-reperfusion injuries on skin resident murine dendritic cells. Eur. J. Immunol. 48:61014–19
    [Google Scholar]
  196. 196.
    Bigley V, Haniffa M, Doulatov S, Wang X-N, Dickinson R et al. 2011. The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. J. Exp. Med. 208:2227–34
    [Google Scholar]
  197. 197.
    Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S et al. 2011. IRF8 mutations and human dendritic-cell immunodeficiency. N. Engl. J. Med. 365:2127–38
    [Google Scholar]
  198. 198.
    Ng LG, Qin JS, Roediger B, Wang Y, Jain R et al. 2011. Visualizing the neutrophil response to sterile tissue injury in mouse dermis reveals a three-phase cascade of events. J. Investig. Dermatol. 131:102058–68
    [Google Scholar]
  199. 199.
    Kienle K, Glaser KM, Eickhoff S, Mihlan M, Knöpper K et al. 2021. Neutrophils self-limit swarming to contain bacterial growth in vivo. Science 372:6548eabe7729
    [Google Scholar]
  200. 200.
    Uderhardt S, Martins AJ, Tsang JS, Lämmermann T, Germain RN. 2019. Resident macrophages cloak tissue microlesions to prevent neutrophil-driven inflammatory damage. Cell 177:3541–55.e17
    [Google Scholar]
  201. 201.
    Dal-Secco D, Wang J, Zeng Z, Kolaczkowska E, Wong CHY et al. 2015. A dynamic spectrum of monocytes arising from the in situ reprogramming of CCR2+ monocytes at a site of sterile injury. J. Exp. Med. 212:4447–56
    [Google Scholar]
  202. 202.
    Kratofil RM, Shim HB, Shim R, Lee WY, Labit E et al. 2022. A monocyte–leptin–angiogenesis pathway critical for repair post-infection. Nature 609:166–173
    [Google Scholar]
  203. 203.
    Prinz M, Jung S, Priller J 2019. Microglia biology: one century of evolving concepts. Cell 179:2292–311
    [Google Scholar]
  204. 204.
    Kierdorf K, Masuda T, Jordão MJC, Prinz M. 2019. Macrophages at CNS interfaces: ontogeny and function in health and disease. Nat. Rev. Neurosci. 20:9547–62
    [Google Scholar]
  205. 205.
    Mrdjen D, Pavlovic A, Hartmann FJ, Schreiner B, Utz SG et al. 2018. High-dimensional single-cell mapping of central nervous system immune cells reveals distinct myeloid subsets in health, aging, and disease. Immunity 48:2599
    [Google Scholar]
  206. 206.
    Prinz M, Masuda T, Wheeler MA, Quintana FJ. 2021. Microglia and central nervous system-associated macrophages—from origin to disease modulation. Annu. Rev. Immunol. 39:1251–77
    [Google Scholar]
  207. 207.
    Alvez de Lima K, Rustenhoven J, Kipnis J 2020. Meningeal immunity and its function in maintenance of the central nervous system in health and disease. Annu. Rev. Immunol. 38:1597–620
    [Google Scholar]
  208. 208.
    Herz J, Filiano AJ, Smith AT, Yogev N, Kipnis J. 2017. Myeloid cells in the central nervous system. Immunity 46:6943–56
    [Google Scholar]
  209. 209.
    Van Hove H, Martens L, Scheyltjens I, De Vlaminck K, Antunes ARP et al. 2019. A single-cell atlas of mouse brain macrophages reveals unique transcriptional identities shaped by ontogeny and tissue environment. Nat. Neurosci. 22:61021–35
    [Google Scholar]
  210. 210.
    Elmore MRP, Najafi AR, Koike MA, Dagher NN, Spangenberg EE et al. 2014. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82:2380–97
    [Google Scholar]
  211. 211.
    Bruttger J, Karram K, Wörtge S, Regen T, Marini F et al. 2015. Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity 43:192–106
    [Google Scholar]
  212. 212.
    Rogers JT, Morganti JM, Bachstetter AD, Hudson C, Peters MM et al. 2011. CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J. Neurosci. 31:4516241–50
    [Google Scholar]
  213. 213.
    Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G et al. 2014. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17:3400–6
    [Google Scholar]
  214. 214.
    Easley-Neal C, Foreman O, Sharma N, Zarrin AA, Weimer RM. 2019. CSF1R ligands IL-34 and CSF1 are differentially required for microglia development and maintenance in white and gray matter brain regions. Front. Immunol. 10:2199
    [Google Scholar]
  215. 215.
    Wang Y, Szretter KJ, Vermi W, Gilfillan S, Rossini C et al. 2012. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13:8753–60
    [Google Scholar]
  216. 216.
    Kana V, Desland FA, Casanova-Acebes M, Ayata P, Badimon A et al. 2019. CSF-1 controls cerebellar microglia and is required for motor function and social interaction. J. Exp. Med. 216:102265–81
    [Google Scholar]
  217. 217.
    Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C et al. 2013. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 16:3273–80
    [Google Scholar]
  218. 218.
    Cronk JC, Filiano AJ, Louveau A, Marin I, Marsh R et al. 2018. Peripherally derived macrophages can engraft the brain independent of irradiation and maintain an identity distinct from microglia. J. Exp. Med. 215:61627–47
    [Google Scholar]
  219. 219.
    Goldmann T, Wieghofer P, Jordão MJC, Prutek F, Hagemeyer N et al. 2016. Origin, fate and dynamics of macrophages at central nervous system interfaces. Nat. Immunol. 17:7797–805
    [Google Scholar]
  220. 220.
    Masuda T, Amann L, Monaco G, Sankowski R, Staszewski O et al. 2022. Specification of CNS macrophage subsets occurs postnatally in defined niches. Nature 604:7907740–48
    [Google Scholar]
  221. 221.
    Utz SG, See P, Mildenberger W, Thion MS, Silvin A et al. 2020. Early fate defines microglia and non-parenchymal brain macrophage development. Cell 181:3557–73.e18
    [Google Scholar]
  222. 222.
    Silvin A, Uderhardt S, Piot C, Da Mesquita S, Yang K et al. 2022. Dual ontogeny of disease-associated microglia and disease inflammatory macrophages in aging and neurodegeneration. Immunity 55:81448–65.e6
    [Google Scholar]
  223. 223.
    Cugurra A, Mamuladze T, Rustenhoven J, Dykstra T, Beroshvili G et al. 2021. Skull and vertebral bone marrow are myeloid cell reservoirs for the meninges and CNS parenchyma. Science 373:6553eabf7844
    [Google Scholar]
  224. 224.
    Herisson F, Frodermann V, Courties G, Rohde D, Sun Y et al. 2018. Direct vascular channels connect skull bone marrow and the brain surface enabling myeloid cell migration. Nat. Neurosci. 21:91209–17
    [Google Scholar]
  225. 225.
    Mazzitelli JA, Smyth LCD, Cross KA, Dykstra T, Sun J et al. 2022. Cerebrospinal fluid regulates skull bone marrow niches via direct access through dural channels. Nat. Neurosci. 25:5555–60
    [Google Scholar]
  226. 226.
    Pulous FE, Cruz-Hernández JC, Yang C, Kaya Ζ, Paccalet A et al. 2022. Cerebrospinal fluid can exit into the skull bone marrow and instruct cranial hematopoiesis in mice with bacterial meningitis. Nat. Neurosci. 25:5567–76
    [Google Scholar]
  227. 227.
    Li X, Qi L, Yang D, Hao S, Zhang F et al. 2022. Meningeal lymphatic vessels mediate neurotropic viral drainage from the central nervous system. Nat. Neurosci. 25:5577–87
    [Google Scholar]
  228. 228.
    Krishnan S, Wemyss K, Prise IE, McClure FA, O'Boyle C et al. 2021. Hematopoietic stem and progenitor cells are present in healthy gingiva tissue. J. Exp. Med. 218:4e20200737
    [Google Scholar]
  229. 229.
    Bain CC, Schridde A. 2018. Origin, differentiation, and function of intestinal macrophages. Front. Immunol. 9:2733
    [Google Scholar]
  230. 230.
    Chikina AS, Nadalin F, Maurin M, San-Roman M, Thomas-Bonafos T et al. 2020. Macrophages maintain epithelium integrity by limiting fungal product absorption. Cell 183:2411–28.e16
    [Google Scholar]
  231. 231.
    Kim K-W, Vallon-Eberhard A, Zigmond E, Farache J, Shezen E et al. 2011. In vivo structure/function and expression analysis of the CX3C chemokine fractalkine. Blood 118:22e156–67
    [Google Scholar]
  232. 232.
    Niess JH, Brand S, Gu X, Landsman L, Jung S et al. 2005. CX 3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307:5707254–58
    [Google Scholar]
  233. 233.
    Kang B, Alvarado LJ, Kim T, Lehmann ML, Cho H et al. 2020. Commensal microbiota drive the functional diversification of colon macrophages. Mucosal Immunol. 13:2216–29
    [Google Scholar]
  234. 234.
    De Schepper S, Verheijden S, Aguilera-Lizarraga J, Viola MF, Boesmans W et al. 2018. Self-maintaining gut macrophages are essential for intestinal homeostasis. Cell 175:2676–76
    [Google Scholar]
  235. 235.
    Shaw TN, Houston S, Wemyss K, Bridgeman HM, Barbera TA et al. 2018. Tissue-resident macrophages in the intestine are long lived and defined by Tim-4 and CD4 expression. J. Exp. Med. 215:61507–18
    [Google Scholar]
  236. 236.
    Christ A, Günther P, Lauterbach MAR, Duewell P, Biswas D et al. 2018. Western diet triggers NLRP3-dependent innate immune reprogramming. Cell 172:1162–75
    [Google Scholar]
  237. 237.
    Barman PK, Urao N, Koh TJ. 2019. Diabetes induces myeloid bias in bone marrow progenitors associated with enhanced wound macrophage accumulation and impaired healing. J. Pathol. 249:4435–46
    [Google Scholar]
  238. 238.
    Murphy AJ, Akhtari M, Tolani S, Pagler T, Bijl N et al. 2011. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J. Clin. Investig. 121:104138–49
    [Google Scholar]
  239. 239.
    Liu A, Chen M, Kumar R, Stefanovic-Racic M, O'Doherty RM et al. 2018. Bone marrow lympho-myeloid malfunction in obesity requires precursor cell-autonomous TLR4. Nat. Commun. 9:1708
    [Google Scholar]
  240. 240.
    Pietras EM, Mirantes-Barbeito C, Fong S, Loeffler D, Kovtonyuk LV et al. 2016. Chronic interleukin-1 exposure drives haematopoietic stem cells towards precocious myeloid differentiation at the expense of self-renewal. Nat. Cell Biol. 18:6607–18
    [Google Scholar]
  241. 241.
    Engblom C, Pfirschke C, Zilionis R, Da Silva Martins J, Bos SA et al. 2017. Osteoblasts remotely supply lung tumors with cancer-promoting SiglecFhigh neutrophils. Science 358:6367eaal5081
    [Google Scholar]
  242. 242.
    Pfirschke C, Engblom C, Gungabeesoon J, Lin Y, Rickelt S et al. 2020. Tumor-promoting Ly-6G+ SiglecFhigh cells are mature and long-lived neutrophils. Cell Rep. 32:12108164
    [Google Scholar]
  243. 243.
    Long H, Jia Q, Wang L, Fang W, Wang Z et al. 2022. Tumor-induced erythroid precursor-differentiated myeloid cells mediate immunosuppression and curtail anti-PD-1/PD-L1 treatment efficacy. Cancer Cell 40:6674–93.e7
    [Google Scholar]
  244. 244.
    Carissimo G, Xu W, Kwok I, Abdad MY, Chan Y-H et al. 2020. Whole blood immunophenotyping uncovers immature neutrophil-to-VD2 T-cell ratio as an early marker for severe COVID-19. Nat. Commun. 11:15243
    [Google Scholar]
  245. 245.
    Combadière B, Adam L, Guillou N, Quentric P, Rosenbaum P et al. 2021. LOX-1-expressing immature neutrophils identify critically-ill COVID-19 patients at risk of thrombotic complications. Front. Immunol. 12:752612
    [Google Scholar]
  246. 246.
    Sinha S, Rosin NL, Arora R, Labit E, Jaffer A et al. 2022. Dexamethasone modulates immature neutrophils and interferon programming in severe COVID-19. Nat. Med. 28:1201–11
    [Google Scholar]
  247. 247.
    Liao M, Liu Y, Yuan J, Wen Y, Xu G et al. 2020. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat. Med. 26:6842–44
    [Google Scholar]
  248. 248.
    Szabo PA, Dogra P, Gray JI, Wells SB, Connors TJ et al. 2021. Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19. Immunity 54:4797–814.e6
    [Google Scholar]
  249. 249.
    Wendisch D, Dietrich O, Mari T, von Stillfried S, Ibarra IL et al. 2021. SARS-CoV-2 infection triggers profibrotic macrophage responses and lung fibrosis. Cell 184:266243–61.e27
    [Google Scholar]
  250. 250.
    Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. 2012. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12:4253–68
    [Google Scholar]
  251. 251.
    Ma R-Y, Black A, Qian B-Z. 2022. Macrophage diversity in cancer revisited in the era of single-cell omics. Trends Immunol 43:7546–63
    [Google Scholar]
  252. 252.
    Ringel AE, Drijvers JM, Baker GJ, Catozzi A, García-Cañaveras JC et al. 2020. Obesity shapes metabolism in the tumor microenvironment to suppress anti-tumor immunity. Cell 183:71848–66.e26
    [Google Scholar]
  253. 253.
    Veglia F, Tyurin VA, Blasi M, De Leo A, Kossenkov AV et al. 2019. Fatty acid transport protein 2 reprograms neutrophils in cancer. Nature 569:775473–78
    [Google Scholar]
/content/journals/10.1146/annurev-immunol-081022-113627
Loading
/content/journals/10.1146/annurev-immunol-081022-113627
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error