Newborn

Register      Login

VOLUME 1 , ISSUE 4 ( October-December, 2022 ) > List of Articles

REVIEW ARTICLE

The Phylogeny, Ontogeny, and Organ-specific Differentiation of Macrophages in the Developing Intestine

Keywords : Blood counts, Inflammation, Macrophages, Monocytes, Organ injury, Signaling

Citation Information : The Phylogeny, Ontogeny, and Organ-specific Differentiation of Macrophages in the Developing Intestine. 2022; 1 (4):340-355.

DOI: 10.5005/jp-journals-11002-0044

License: CC BY-NC 4.0

Published Online: 23-12-2022

Copyright Statement:  Copyright © 2022; The Author(s).


Abstract

Macrophages are large highly motile phagocytic leukocytes that appear early during embryonic development and have been conserved during evolution. The developmental roles of macrophages were first described nearly a century ago, at about the time these cells were being identified as central effectors in phagocytosis and elimination of microbes. Since then, we have made considerable progress in understanding the development of various subsets of macrophages and the diverse roles these cells play in both physiology and disease. This article reviews the phylogeny and the ontogeny of macrophages with a particular focus on the gastrointestinal tract, and the role of these mucosal macrophages in immune surveillance, innate immunity, homeostasis, tissue remodeling, angiogenesis, and repair of damaged tissues. We also discuss the importance of these macrophages in the inflammatory changes in neonatal necrotizing enterocolitis (NEC). This article presents a combination of our own peer-reviewed clinical and preclinical studies, with an extensive review of the literature using the databases PubMed, EMBASE, and Scopus.


HTML PDF Share
  1. Cavaillon J-M. The historical milestones in the understanding of leukocyte biology initiated by Elie Metchnikoff. J Leukoc Biol 2011;90(3):413–424. DOI: 10.1189/jlb.0211094.
  2. Weigert A, Olesch C, Brune B. Sphingosine-1-phosphate and macrophage biology – How the sphinx tames the big eater. Front Immunol 2019;10:1706. DOI: 10.3389/fimmu.2019.01706.
  3. Bain CC, Schridde A. Origin, differentiation, and function of intestinal macrophages. Front Immunol 2018;9:2733. DOI: 10.3389/fimmu.2018.02733.
  4. Yao Y, Xu XH, Jin L. Macrophage polarization in physiological and pathological pregnancy. Front Immunol 2019;10:792. DOI: 10.3389/fimmu.2019.00792.
  5. Geissmann F, Manz MG, Jung S, et al. Development of monocytes, macrophages, and dendritic cells. Science 2010;327(5966):656–661. DOI: 10.1126/science.1178331.
  6. Jaumouille V, Waterman CM. Physical constraints and forces involved in phagocytosis. Front Immunol 2020;11:1097. DOI: 10.3389/fimmu.2020.01097.
  7. Suckale J, Sim RB, Dodds AW. Evolution of innate immune systems. Biochem Mol Biol Educ 2005;33(3):177–183. DOI: 10.1002/bmb.2005.494033032466.
  8. Richards DM, Endres RG. The mechanism of phagocytosis: Two stages of engulfment. Biophys J 2014;107(7):1542–1553. DOI: 10.1016/j.bpj.2014.07.070.
  9. Stuart LM, Ezekowitz RA. Phagocytosis and comparative innate immunity: Learning on the fly. Nat Rev Immunol 2008;8(2):131–141. DOI: 10.1038/nri2240.
  10. Arroyo Portilla C, Tomas J, Gorvel J-P, et al. From species to regional and local specialization of intestinal macrophages. Front Cell Dev Biol 2020;8:624213. DOI: 10.3389/fcell.2020.624213.
  11. Lanna E. Evo-devo of non-bilaterian animals. Genet Mol Biol 2015;38(3):284–300. DOI: 10.1590/S1415-475738320150005.
  12. Yap NV, Whelan FJ, Bowdish DM, et al. The evolution of the scavenger receptor cysteine-rich domain of the class A scavenger receptors. Front Immunol 2015;6:342. DOI: 10.3389/fimmu.2015.00342.
  13. Benard EL, Racz PI, Rougeot J, et al. Macrophage-expressed perforins mpeg1 and mpeg1.2 have an anti-bacterial function in zebrafish. J Innate Immun 2015;7:136–152. DOI: 10.1159/000366103.
  14. Salinas-Saavedra M, Rock AQ, Martindale MQ. Germ layer-specific regulation of cell polarity and adhesion gives insight into the evolution of mesoderm. Elife 2018;7:e36740. DOI: 10.7554/eLife.36740.
  15. Muller WE, Schwertner H, Muller IM. Porifera a reference phylum for evolution and bioprospecting: The power of marine genomics. Keio J Med 2004;53(3):159–165. DOI: 10.2302/kjm.53.159.
  16. Martindale MQ, Pang K, Finnerty JR. Investigating the origins of triploblasty: ‘Mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 2004;131(10):2463–2474. DOI: 10.1242/dev.01119.
  17. Monahan-Earley R, Dvorak AM, Aird WC. Evolutionary origins of the blood vascular system and endothelium. J Thromb Haemost 2013;11(Suppl 1):46–66. DOI: 10.1111/jth.12253.
  18. Wolf MJ, Rockman HA. Drosophila, genetic screens, and cardiac function. Circ Res 2011;109(7):794–806. DOI: 10.1161/CIRCRESAHA.111.244897.
  19. Prochazkova P, Roubalova R, Dvorak J, et al. Pattern recognition receptors in annelids. Dev Comp Immunol 2020;102:103493. DOI: 10.1016/j.dci.2019.103493.
  20. Engelmann P, Hayashi Y, Bodo K, et al. Phenotypic and functional characterization of earthworm coelomocyte subsets: Linking light scatter-based cell typing and imaging of the sorted populations. Dev Comp Immunol 2016;65:41–52. DOI: 10.1016/j.dci.2016.06.017.
  21. Buchmann, K. Evolution of innate immunity: Clues from invertebrates via fish to mammals. Front Immunol 2014;5:459. DOI: 10.3389/fimmu.2014.00459.
  22. Dvorak J, Roubalová R, Procházková P, et al. Sensing microorganisms in the gut triggers the immune response in Eisenia andrei earthworms. Dev Comp Immunol 2016;57:67–74. DOI: 10.1016/j.dci.2015.12.001.
  23. Cameron CB, Garey JR, Swalla BJ. Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 2000;97(9):4469–4474. DOI: 10.1073/pnas.97.9.4469.
  24. Guilliams M, Mildner A, Yona S. Developmental and functional heterogeneity of monocytes. Immunity 2018;49(4):595–613. DOI: 10.1016/j.immuni.2018.10.005.
  25. Cooper MD, Alder MN. The evolution of adaptive immune systems. Cell 2006;124(4):815–822. DOI: 10.1016/j.cell.2006.02.001.
  26. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392(6673):245–252. DOI: 10.1038/32588.
  27. Golconda P, Buckley KM, Reynolds CR, et al. The axial organ and the pharynx are sites of hematopoiesis in the Sea Urchin. Front Immunol 2019;10:870. DOI: 10.3389/fimmu.2019.00870.
  28. Ch Ho E, Buckley KM, Schrankel CS, et al. Perturbation of gut bacteria induces a coordinated cellular immune response in the purple sea urchin larva. Immunol Cell Biol 2016;94(9):861–874. DOI: 10.1038/icb.2016.51.
  29. Buckley KM, Rast JP. Immune activity at the gut epithelium in the larval sea urchin. Cell Tissue Res 2019;377(3):469–474. DOI: 10.1007/s00441-019-03095-7.
  30. Coates CJ, McCulloch C, Betts J, et al. Echinochrome A release by red spherule cells is an iron-withholding strategy of sea urchin innate immunity. J Innate Immun 2018;10(2):119–130. DOI: 10.1159/000484722.
  31. Buckley KM, Ho ECH, Hibino T, et al. IL17 factors are early regulators in the gut epithelium during inflammatory response to Vibrio in the sea urchin larva. Elife 2017;6:e23481. DOI: 10.7554/eLife.23481.
  32. Stachura DL, Svoboda O, Lau RP, et al. Clonal analysis of hematopoietic progenitor cells in the zebrafish. Blood 2011;118(5):1274–1282. DOI: 10.1182/blood-2011-01-331199.
  33. Wittamer V, Bertrand JY, Gutschow PW, et al. Characterization of the mononuclear phagocyte system in zebrafish. Blood 2011;117(26):7126–7135. DOI: 10.1182/blood-2010-11-321448.
  34. Grayfer L, Robert J. Amphibian macrophage development and antiviral defenses. Dev Comp Immunol 2016;58:60–67. DOI: 10.1016/j.dci.2015.12.008.
  35. Yaparla A, Reeves P, Grayfer L. Myelopoiesis of the amphibian Xenopus laevis is segregated to the bone marrow, away from their hematopoietic peripheral liver. Front Immunol 2019;10:3015. DOI: 10.3389/fimmu.2019.03015.
  36. Chin KN, Wong WC. Some ultrastructural observations on the intestinal mucosa of the toad (Bufo melanostictus). J Anat 1977;123 (Pt 2):331–339. PMID: 870472.
  37. Nochi T, Jansen CA, Toyomizu M, et al. The well-developed mucosal immune systems of birds and mammals allow for similar approaches of mucosal vaccination in both types of animals. Front Nutr 2018;5:60. DOI: 10.3389/fnut.2018.00060.
  38. de Geus ED, Vervelde L. Regulation of macrophage and dendritic cell function by pathogens and through immunomodulation in the avian mucosa. Dev Comp Immunol 2013;41(3):341–351. DOI: 10.1016/j.dci.2013.03.008.
  39. Wigley P. Salmonella enterica in the chicken: How it has helped our understanding of immunology in a non-biomedical model species. Front Immunol 2014;5:482. DOI: 10.3389/fimmu.2014.00482.
  40. Stremmel C, Schuchert R, Wagner F, et al. Yolk sac macrophage progenitors traffic to the embryo during defined stages of development. Nat Commun 2018;9:75. DOI: 10.1038/s41467-017-02492-2.
  41. Takashina T. Haemopoiesis in the human yolk sac. J Anat 1987;151: 125–135. PMCID: PMC1261706.
  42. Smythies LE, Maheshwari A, Clements R, et al. Mucosal IL-8 and TGF-beta recruit blood monocytes: Evidence for cross-talk between the lamina propria stroma and myeloid cells. J Leukoc Biol 2006;80(3):492–499. DOI: 10.1189/jlb.1005566.
  43. Shepard JL, Zon LI. Developmental derivation of embryonic and adult macrophages. Curr Opin Hematol 2000;7(1):3–8. DOI: 10.1097/00062752-200001000-00002.
  44. Maheshwari A, Kurundkar AR, Shaik SS, et al. Epithelial cells in fetal intestine produce chemerin to recruit macrophages. Am J Physiol Gastrointest Liver Physiol 2009;297(1):G1–G10. DOI: 10.1152/ajpgi.90730.2008.
  45. Janossy G, Bofill M, Poulter LW, et al. Separate ontogeny of two macrophage-like accessory cell populations in the human fetus. J Immunol 1986;136(12):4354–4361. PMID: 3711660.
  46. MacDonald TT, Weinel A, Spencer J. HLA-DR expression in human fetal intestinal epithelium. Gut 1988;29(10):1342–1348. DOI: 10.1136/gut.29.10.1342.
  47. Celada A, Borràs FE, Soler C, et al. The transcription factor PU.1 is involved in macrophage proliferation. J Exp Med 1996;184(1):61–69. DOI: 10.1084/jem.184.1.61.
  48. Kasaai B, Caolo V, Peacock HM, et al. Erythro-myeloid progenitors can differentiate from endothelial cells and modulate embryonic vascular remodeling. Sci Rep 2017;7:43817. DOI: 10.1038/srep 43817.
  49. Sinka L, Biasch K, Khazaal I, et al. Angiotensin-converting enzyme (CD143) specifies emerging lympho-hematopoietic progenitors in the human embryo. Blood 2012;119(16):3712–3723. DOI: 10.1182/blood-2010-11-314781.
  50. Mariani SA, Li Z, Rice S, et al. Pro-inflammatory aorta-associated macrophages are involved in embryonic development of hematopoietic stem cells. Immunity 2019;50(6):1439–1452.e5. DOI: 10.1016/j.immuni.2019.05.003.
  51. McGrath KE, Frame JM, Fegan KH, et al. Distinct sources of hematopoietic progenitors emerge before HSCs and provide functional blood cells in the mammalian embryo. Cell Rep 2015;11(12):1892–1904. DOI: 10.1016/j.celrep.2015.05.036.
  52. Ginhoux F, Greter M, Leboeuf M, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010;330(6005):841–845. DOI: 10.1126/science.1194637.
  53. Elchaninov AV, Fatkhudinov TKh, Vishnyakova PA, et al. Phenotypical and functional polymorphism of liver resident macrophages. Cells 2019;8(9):1032. DOI: 10.3390/cells8091032.
  54. Kelemen E, Janossa M. Macrophages are the first differentiated blood cells formed in human embryonic liver. Exp Hematol 1980;8(8): 996–1000. PMID: 7202591.
  55. Zhu YP, Thomas GD, Hedrick CC. 2014 Jeffrey M. Hoeg Award Lecture: Transcriptional control of monocyte development. Arterioscler Thromb Vasc Biol 2016;36(9):1722–1733. DOI: 10.1161/ATVBAHA.116.304054.
  56. Palis J, Yoder MC. Yolk-sac hematopoiesis: The first blood cells of mouse and man. Exp Hematol 2001;29(8):927–936. DOI: 10.1016/s0301-472x(01)00669-5.
  57. Perdiguero EG, Geissmann F. The development and maintenance of resident macrophages. Nat Immunol 2016;17(1):2–8. DOI: 10.1038/ni.3341.
  58. Italiani P, Boraschi D. From monocytes to M1/M2 macrophages: Phenotypical vs. functional differentiation. Front Immunol 2014;5:514. DOI: 10.3389/fimmu.2014.00514.
  59. Jakubzick C, Gautier EL, Gibbings SL, et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 2013;39(3):599–610. DOI: 10.1016/j.immuni.2013.08.007.
  60. Nguyen KD, Fenstress SJ, Qiu Y, et al. Circadian gene Bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science 2013;341(6153):1483–1488. DOI: 10.1126/science.1240636.
  61. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003;19(1):71–82. DOI: 10.1016/s1074-7613(03)00174-2.
  62. Prata L, Ovsyannikova IG, Tchkonia T, et al. Senescent cell clearance by the immune system: Emerging therapeutic opportunities. Semin Immunol 2018;40:101275. DOI: 10.1016/j.smim.2019.04.003.
  63. Grage-Griebenow E, Flad HD, Ernst M. Heterogeneity of human peripheral blood monocyte subsets. J Leukoc Biol 2001;69(1):11–20. PMID: 11200054.
  64. Zhang C, Zhang B, Zhang X, et al. Targeting orphan nuclear receptors NR4As for energy homeostasis and diabetes. Front Pharmacol 2020;11:587457. DOI: 10.3389/fphar.2020.587457.
  65. Tamura A, Hirai H, Yokota A, et al. C/EBPbeta is required for survival of Ly6C(-) monocytes. Blood 2017;130(16):1809–1818. DOI: 10.1182/blood-2017-03-772962.
  66. Auffray C, Fogg D, Garfa M, et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007;317(5838):666–670. DOI: 10.1126/science. 1142883.
  67. Garré JM, Yang G. Contributions of monocytes to nervous system disorders. J Mol Med (Berl) 2018;96(9):873–883. DOI: 10.1007/s00109-018-1672-3.
  68. Yona S, Kim K-W, Wolf Y, et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013;38(1):79–91. DOI: 10.1016/j.immuni.2012.12.001.
  69. Porcellini A, Manna A, Manna M, et al. Ontogeny of granulocyte-macrophage progenitor cells in the human fetus. Int J Cell Cloning 1983;1(2):92–104. DOI: 10.1002/stem.5530010204.
  70. Linch DC, Knott LJ, Rodeck CH, et al. Studies of circulating hemopoietic progenitor cells in human fetal blood. Blood 1982;59(5):976–979. PMID: 7074222.
  71. Christensen RD, Jensen J, Maheshwari A, et al. Reference ranges for blood concentrations of eosinophils and monocytes during the neonatal period defined from over 63,000 records in a multihospital health-care system. J Perinatol 2010;30(8):540–545. DOI: 10.1038/jp.2009.196.
  72. Xanthou M. Leucocyte blood picture in healthy full-term and premature babies during neonatal period. Arch Dis Child 1970;45(240):242–249. DOI: 10.1136/adc.45.240.242.
  73. Weinberg AG, Rosenfeld CR, Manroe BL, et al. Neonatal blood cell count in health and disease. II. Values for lymphocytes, monocytes, and eosinophils. J Pediatr 1985;106(3):462–466. DOI: 10.1016/s0022-3476(85)80681-8.
  74. Germic N, Frangez Z, Yousefi S, et al. Regulation of the innate immune system by autophagy: Monocytes, macrophages, dendritic cells and antigen presentation. Cell Death Differ 2019;26(4):715–727. DOI: 10.1038/s41418-019-0297-6.
  75. Martino DJ, Tulic MK, Gordon L, et al. Evidence for age-related and individual-specific changes in DNA methylation profile of mononuclear cells during early immune development in humans. Epigenetics 2011;6(9):1085–1094. DOI: 10.4161/epi.6.9.16401.
  76. Bermick JR, Lambrecht NJ, denDekker AD, et al. Neonatal monocytes exhibit a unique histone modification landscape. Clin Epigenetics 2016;8:99. DOI: 10.1186/s13148-016-0265-7.
  77. Kobayashi SD, DeLeo FR. Role of neutrophils in innate immunity: A systems biology-level approach. Wiley Interdiscip Rev Syst Biol Med 2009;1(3):309–333. DOI: 10.1002/wsbm.32.
  78. Speer CP, Ambruso DR, Grimsley J, et al. Oxidative metabolism in cord blood monocytes and monocyte-derived macrophages. Infect Immun 1985;50(3):919–921. DOI: 10.1128/iai.50.3.919-921.1985.
  79. Speer CP, Wieland M, Ulbrich R, et al. Phagocytic activities in neonatal monocytes. Eur J Pediatr 1986;145(5):418–421. DOI: 10.1007/BF00439252.
  80. Weston WL, Carson BS, Barkin RM, et al. Monocyte-macrophage function in the newborn. Am J Dis Child 1977;131(11):1241–1242. DOI: 10.1001/archpedi.1977.02120240059011.
  81. D'Ambola JB, Sherman MP, Tashkin DP, et al. Human and rabbit newborn lung macrophages have reduced anti-Candida activity. Pediatr Res 1988;24(3):285–290. DOI: 10.1203/00006450-198809000-00001.
  82. Bryson YJ, Winter HS, Gard SE, et al. Deficiency of immune interferon production by leukocytes of normal newborns. Cell Immunol 1980;55(1):191–200. DOI: 10.1016/0008-8749(80)90150-1.
  83. Weatherstone KB, Rich EA. Tumor necrosis factor/cachectin and interleukin-1 secretion by cord blood monocytes from premature and term neonates. Pediatr Res 1989;25(4):342–346. DOI: 10.1203/00006450-198904000-00006.
  84. Wilson CB. Immunologic basis for increased susceptibility of the neonate to infection. J Pediatr 1986;108(1):1–12. DOI: 10.1016/s0022-3476(86)80761-2.
  85. Bessler H, Sirota L, Dulitzky F, et al. Production of interleukin-1 by mononuclear cells of newborns and their mothers. Clin Exp Immunol 1987;68(3):655–661. PMCID: PMC1542750.
  86. Kesson AM, Bryson YJ. Induction of interferon-gamma by cord blood mononuclear cells is calcium dependent. Cell Immunol 1991;133(1):138–146. DOI: 10.1016/0008-8749(91)90186-f.
  87. Bencheikh L, Diop MK, Rivière J, et al. Dynamic gene regulation by nuclear colony-stimulating factor 1 receptor in human monocytes and macrophages. Nat Commun 2019;10(1):1935. DOI: 10.1038/s41467-019-09970-9.
  88. Wang Y, Colonna M. Interkeukin-34, a cytokine crucial for the differentiation and maintenance of tissue resident macrophages and Langerhans cells. Eur J Immunol 2014;44(6):1575–1581. DOI: 10.1002/eji.201344365.
  89. Orecchioni M, Ghosheh Y, Pramod AB, et al. Macrophage polarization: Different gene signatures in M1(LPS+) vs. classically and M2(LPS-) vs. alternatively activated macrophages. Front Immunol 2019;10:1084. DOI: 10.3389/fimmu.2019.01084.
  90. Kapellos TS, Bonaguro L, Gemünd I, et al. Human monocyte subsets and phenotypes in major chronic inflammatory diseases. Front Immunol 2019;10:2035. DOI: 10.3389/fimmu.2019.02035.
  91. Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 2014;6:13. DOI: 10.12703/P6-13.
  92. Wang N, Liang H, Zen K. Molecular mechanisms that influence the macrophage M1–M2 polarization balance. Front Immunol 2014;5:614. DOI: 10.3389/fimmu.2014.00614.
  93. Mills CD, Ley K. M1 and M2 macrophages: The chicken and the egg of immunity. J Innate Immun 2014;6(6):716–726. DOI: 10.1159/000364945.
  94. Gschwandtner M, Derler R, Midwood KS. More than just attractive: How CCL2 influences myeloid cell behavior beyond chemotaxis. Front Immunol 2019;10:2759. DOI: 10.3389/fimmu.2019.02759.
  95. Mills CD. Macrophage arginine metabolism to ornithine/urea or nitric oxide/citrulline: a life or death issue. Crit Rev Immunol 2001;21(5): 399–425. PMID: 11942557.
  96. Liu SX, Gustafson HH, Jackson DL, et al. Trajectory analysis quantifies transcriptional plasticity during macrophage polarization. Sci Rep 2020;10(1):12273. DOI: 10.1038/s41598-020-68766-w.
  97. Lee M, Lee Y, Song J, et al. Tissue-specific role of CX3CR1 expressing immune cells and their relationships with human disease. Immune Netw 2018;18(1):e5. DOI: 10.4110/in.2018.18.e5.
  98. Zhang J, Patel L, Pienta KJ. Targeting chemokine (C-C motif) ligand 2 (CCL2) as an example of translation of cancer molecular biology to the clinic. Prog Mol Biol Transl Sci 2010;95:31–53. DOI: 10.1016/B978-0-12-385071-3.00003-4.
  99. Graney PL, Ben-Shaul S, Landau S, et al. Macrophages of diverse phenotypes drive vascularization of engineered tissues. Sci Adv 2020;6(18):eaay6391. DOI: 10.1126/sciadv.aay6391.
  100. Roszer T. Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediators Inflamm 2015;2015:816460. DOI: 10.1155/2015/816460.
  101. Muraille E, Leo O, Moser M. TH1/TH2 paradigm extended: Macrophage polarization as an unappreciated pathogen-driven escape mechanism? Front Immunol 2014;5:603. DOI: 10.3389/fimmu.2014.00603.
  102. Hashimoto D, Chow A, Noizat C, et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 2013;38(4):792–804. DOI: 10.1016/j.immuni.2013.04.004.
  103. Davies LC, Jenkins SJ, Allen JE, et al. Tissue-resident macrophages. Nat Immunol 2013;14(10):986–995. DOI: 10.1038/ni.2705.
  104. Boulakirba S, Pfeifer A, Mhaidly R, et al. IL-34 and CSF-1 display an equivalent macrophage differentiation ability but a different polarization potential. Sci Rep 2018;8(1):256. DOI: 10.1038/s41598-017-18433-4.
  105. Rettenmier CW, Roussel MF, Sherr CJ. The colony-stimulating factor 1 (CSF-1) receptor (c-fms proto-oncogene product) and its ligand. J Cell Sci Suppl 1988;9:27–44. DOI: 10.1242/jcs.1988.supplement_9.2.
  106. Jaguin M, Houlbert N, Fardel O, et al. Polarization profiles of human M-CSF-generated macrophages and comparison of M1-markers in classically activated macrophages from GM-CSF and M-CSF origin. Cell Immunol 2013;281(1):51–61. DOI: 10.1016/j.cellimm.2013.01.010.
  107. Jaffe R. Review of human dendritic cells: Isolation and culture from precursors. Pediatr Pathol 1993;13:821–837. DOI: 10.3109/15513819309048268.
  108. Foster CA, Holbrook KA, Farr AG. Ontogeny of langerhans cells in human embryonic and fetal skin: Expression of HLA-DR and OKT-6 determinants. J Invest Dermatol 1986;86(3):240–243. DOI: 10.1111/1523-1747.ep12285201.
  109. Grouard G, Rissoan MC, Filgueira L, et al. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997;185(6):1101–1111. DOI: 10.1084/jem.185.6.1101.
  110. O'Doherty U, Peng M, Gezelter S, et al. Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 1994;82(3):487–493. PMID: 7525461.
  111. Liu Y-J, Kanzler H, Soumelis V, et al. Dendritic cell lineage, plasticity and cross-regulation. Nat Immunol 2001;2(7):585–589. DOI: 10.1038/89726.
  112. Denning TL, Wang YC, Patel SR, et al. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 2007;8(10):1086–1094. DOI: 10.1038/ni1511.
  113. Velilla PA, Rugeles MT, Chougnet CA. Defective antigen-presenting cell function in human neonates. Clin Immunol 2006;121(3):251–259. DOI: 10.1016/j.clim.2006.08.010.
  114. Petty RE, Hunt DW. Neonatal dendritic cells. Vaccine 1998;16 (14–15):1378–1382. DOI: 10.1016/s0264-410x(98)00095-4.
  115. Bondada S, Wu H, Robertson DA. Accessory cell defect in unresponsiveness of neonates and aged to polysaccharide vaccines. Vaccine 2000;19(4–5):557–565. DOI: 10.1016/S0264-410X(00)00161-4.
  116. Guilliams M, Svedberg FR. Does tissue imprinting restrict macrophage plasticity? Nat Immunol 2021;22:118–127. DOI: 10.1038/s41590-020-00849-2.
  117. Yang J, Zhang L, Yu C, et al. Monocyte and macrophage differentiation: Circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark Res 2014;2:1. DOI: 10.1186/2050-7771-2-1.
  118. Nahrendorf M, Swirski FK, Aikawa E, et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007;204(12):3037–3047. DOI: 10.1084/jem.20070885.
  119. Das A, Sinha M, Datta S, et al. Monocyte and macrophage plasticity in tissue repair and regeneration. Am J Pathol 2015;185(10):2596–2606. DOI: 10.1016/j.ajpath.2015.06.001.
  120. Avraham-Davidi I, Yona S, Grunewald M, et al. On-site education of VEGF-recruited monocytes improves their performance as angiogenic and arteriogenic accessory cells. J Exp Med 2013;210(12):2611–2625. DOI: 10.1084/jem.20120690.
  121. Maheshwari A, Kelly DR, Nicola T, et al. TGF-β2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 2011;140(1):242–253. DOI: 10.1053/j.gastro.2010.09.043.
  122. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008;8(12):958–969. DOI: 10.1038/nri2448.
  123. Parisi L, Gini E, Baci D, et al. Macrophage polarization in chronic inflammatory diseases: Killers or builders? J Immunol Res 2018; 2018:8917804. DOI: 10.1155/2018/8917804.
  124. Van Belleghem JD, Bollyky PL. Macrophages and innate immune memory against Staphylococcus skin infections. Proc Natl Acad Sci USA 2018;115(47):11865–11867. DOI: 10.1073/pnas.1816935115.
  125. Hampton HR, Chtanova T. Lymphatic migration of immune cells. Front Immunol 2019;10:1168. DOI: 10.3389/fimmu.2019.01168.
  126. Watanabe S, Alexander M, Misharin AV. The role of macrophages in the resolution of inflammation. J Clin Invest 2019;129(7):2619–2628. DOI: 10.1172/JCI124615.
  127. Bezsonov EE, Gratchev A, Orekhov AN. Macrophages in health and non-infectious disease. Biomedicines 2021;9(5):460. DOI: 10.3390/biomedicines9050460.
  128. Italiani P, Della Camera G, Boraschi D. Induction of innate immune memory by engineered nanoparticles in monocytes/macrophages: From hypothesis to reality. Front Immunol 2020;11:566309. DOI: 10.3389/fimmu.2020.566309.
  129. Jakubzick CV, Randolph GJ, Henson PM. Monocyte differentiation and antigen-presenting functions. Nat Rev Immunol 2017;17(6):349–362. DOI: 10.1038/nri.2017.28.
  130. Netea MG, Domínguez-Andrés J, Barreiro LB, et al. Defining trained immunity and its role in health and disease. Nat Rev Immunol 2020;20(6):375–388. DOI: 10.1038/s41577-020-0285-6.
  131. Lee SH, Starkey PM, Gordon S. Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J Exp Med 1985;161(3): 475–489. DOI: 10.1084/jem.161.3.475.
  132. Maheshwari A, Zemlin M. Ontogeny of the intestinal immune system. Haematol Rep 2006;10:18–26.
  133. MacDonald TT, Spencer J. Ontogeny of the mucosal immune response. Springer Semin Immunopathol 1990;12:129–137. DOI: 10.1007/BF00 197501.
  134. Rognum TO, Thrane S, Stoltenberg L, et al. Development of intestinal mucosal immunity in fetal life and the first postnatal months. Pediatr Res 1992;32(2):145–149. DOI: 10.1203/00006450-199208000-00003.
  135. Braegger CP, Spencer J, MacDonald TT. Ontogenetic aspects of the intestinal immune system in man. Int J Clin Lab Res 1992;22(1):1–4. PMID: 1633313.
  136. Harvey J, Jones DB, Wright DH. Differential expression of MHC- and macrophage-associated antigens in human fetal and postnatal small intestine. Immunology 1990;69(3):409–415. PMCID: PMC1385960.
  137. Spencer J, MacDonald TT, Isaacson PG. Heterogeneity of non-lymphoid cells expressing HLA-D region antigens in human fetal gut. Clin Exp Immunol 1987;67(2):415–424. PMCID: PMC1542580.
  138. Smythies LE, Maheshwari A, Clements R, et al. Mucosal IL-8 and TGF-beta recruit blood monocytes: Evidence for cross-talk between the lamina propria stroma and myeloid cells. J Leukoc Biol 2006;80(3):492–499. DOI: 10.1189/jlb.1005566.
  139. Smythies LE, Sellers M, Clements RH, et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 2005;115(1):66–75. DOI: 10.1172/JCI19229.
  140. Mayrhofer G, Pugh CW, Barclay AN. The distribution, ontogeny and origin in the rat of Ia-positive cells with dendritic morphology and of Ia antigen in epithelia, with special reference to the intestine. Eur J Immunol 1983;13(2):112–122. DOI: 10.1002/eji.1830130206.
  141. Alenghat E, Esterly JR. Alveolar macrophages in perinatal infants. Pediatrics 1984;74(2):221–223. PMID: 6540435.
  142. Jacobs RF, Wilson CB, Palmer S, et al. Factors related to the appearance of alveolar macrophages in the developing lung. Am Rev Respir Dis 1985;131(4):548–553. DOI: 10.1164/arrd.1985.131.4.548.
  143. Kurland G, Cheung ATW, Miller ME, et al. The ontogeny of pulmonary defenses: Alveolar macrophage function in neonatal and juvenile rhesus monkeys. Pediatr Res 1988;23:293–297. DOI: 10.1203/00006450- 198803000-00013.
  144. Johnston RB, Jr. Current concepts: Immunology. Monocytes macrophages. N Engl J Med 1988;318(12):747–752. DOI: 10.1056/NEJM198803243181205.
  145. Yoder MC, Lanker TA, Engle WA. Culture medium oxygen tension affects fibronectin production in human adult and cord blood macrophages. Immunol Lett 1988;19(1):1–6. DOI: 10.1016/0165-2478(88)90111-3.
  146. Santiago-Schwarz F, Fleit HB. Identification of nonadherent mononuclear cells in human cord blood that differentiate into macrophages. J Leukoc Biol 1988;43(1):51–59. DOI: 10.1002/jlb.43.1.51.
  147. Stiehm ER, Sztein MB, Steeg PS, et al. Deficient DR antigen expression on human cord blood monocytes: Reversal with lymphokines. Clin Immunol Immunopathol 1984;30(3):430–436. DOI: 10.1016/0090-1229(84)90028-x.
  148. Morris RB, Nichols BA, Bainton DF. Ultrastructure and peroxidase cytochemistry of normal human leukocytes at birth. Dev Biol 1975;44(2):223–238. DOI: 10.1016/0012-1606(75)90394-2.
  149. Bhoopat L, Taylor CR, Hofman FM. The differentiation antigens of macrophages in human fetal liver. Clin Immunol Immunopathol 1986;41(2):184–192. DOI: 10.1016/0090-1229(86)90102-9.
  150. Bulmer JN, Morrison L, Smith JC. Expression of class II MHC gene products by macrophages in human uteroplacental tissue. Immunology 1988;63(4):707–714. PMCID: PMC1454811.
  151. Glover DM, Brownstein D, Burchett S, et al. Expression of HLA class II antigens and secretion of interleukin-1 by monocytes and macrophages from adults and neonates. Immunology 1987;61(2): 195–201. PMID: 3496273.
  152. Stiehm ER, Sztein MB, Steeg PS, et al. Deficient DR antigen expression on human neonatal monocytes: Reversal with lymphokines. Birth Defects Orig Artic Ser 1983;19:295–298. PMID: 6197111.
  153. Kelsall B. Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunol 2008;1(6):460–469. DOI: 10.1038/mi.2008.61.
  154. Maheshwari A, Voitenok NN, Akalovich S, et al. Developmental changes in circulating IL-8/CXCL8 isoforms in neonates. Cytokine 2009;46(1):12–16. DOI: 10.1016/j.cyto.2008.12.022.
  155. Maheshwari A, Kelly DR, Nicola T, et al. TGF-β2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 2011;140(1):242–253.
  156. Fox SE, Lu W, Maheshwari A, et al. The effects and comparative differences of neutrophil specific chemokines on neutrophil chemotaxis of the neonate. Cytokine 2005;29(3):135–140. DOI: 10.1016/j.cyto.2004.10.007.
  157. Adams DH, Hathaway M, Shaw J, et al. Transforming growth factor-beta induces human T lymphocyte migration in vitro. J Immunol 1991;147(2):609–612. PMID: 2071897.
  158. Kitagawa Y, Sano Y, Ueda M, et al. N-glycosylation of erythropoietin is critical for apical secretion by Madin-Darby canine kidney cells. Exp Cell Res 1994;213(2):449–457. DOI: 10.1006/excr.1994.1222.
  159. Vagin O, Kraut JA, Sachs G. The role of N-glycosylation in trafficking of apical membrane proteins in epithelia. Am J Physiol Renal Physiol 2009;296(3):F459–F469. DOI: 10.1152/ajprenal.90340.2008.
  160. Trowbridge IS, Collawn JF, Hopkins CR. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu Rev Cell Biol 1993;9:129–161. DOI: 10.1146/annurev.cb.09.110193.001021.
  161. Yeaman C, Grindstaff KK, Nelson WJ. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol Rev 1999;79(1):73–98. DOI: 10.1152/physrev.1999.79.1.73.
  162. Murakami K, Kojima T, Sakaki Y. Assessment of clusters of transcription factor binding sites in relationship to human promoter, CpG islands and gene expression. BMC Genomics 2004;5(1):16. DOI: 10.1186/1471-2164-5-16.
  163. Chandraratna RA. Tazarotene--first of a new generation of receptor-selective retinoids. Br J Dermatol 1996;135(Suppl 49):18–25. DOI: 10.1111/j.1365-2133.1996.tb15662.x.
  164. Swift ME, Wallden B, Wayner EA, et al. Truncated RAR beta isoform enhances proliferation and retinoid resistance. J Cell Physiol 2006;209(3):718–725. DOI: 10.1002/jcp.20788.
  165. Kutzleb C, Busmann A, Wendland M, et al. Discovery of novel regulatory peptides by reverse pharmacology: Spotlight on chemerin and the RF-amide peptides metastin and QRFP. Curr Protein Pept Sci 2005;6(3):265–278. DOI: 0.2174/1389203054065419.
  166. Wittamer V, Franssen J-D, Vulcano M, et al. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J Exp Med 2003;198(7):977–985. DOI: 10.1084/jem.20030382.
  167. Miller MD, Krangel MS. Biology and biochemistry of the chemokines: A family of chemotactic and inflammatory cytokines. Crit Rev Immunol 1992;12(1–2):17–46. PMID: 1418604.
  168. MohanKumar K, Kaza N, Jagadeeswaran R, et al. Gut mucosal injury in neonates is marked by macrophage infiltration in contrast to pleomorphic infiltrates in adult: Evidence from an animal model. Am J Physiol Gastrointest Liver Physiol 2012;303(1):G93–G102. DOI: 10.1152/ajpgi.00016.2012.
  169. MohanKumar K, Namachivayam K, Chapalamadugu KC, et al. Smad7 interrupts TGF-β signaling in intestinal macrophages and promotes inflammatory activation of these cells during necrotizing enterocolitis. Pediatr Res 2016;79(6):951–961. DOI: 10.1038/pr. 2016.18.
  170. MohanKumar K, Namachivayam K, Cheng F, et al. Trinitrobenzene sulfonic acid-induced intestinal injury in neonatal mice activates transcriptional networks similar to those seen in human necrotizing enterocolitis. Pediatr Res 2016;81(1–1):99–112. DOI: 10.1038/pr.2016.189.
  171. MohanKumar K, Namachivayam K, Ho TTB, et al. Cytokines and growth factors in the developing intestine and during necrotizing enterocolitis. Semin Perinatol 2017;41(1):52–60. DOI: 10.1053/j.semperi.2016.09.018.
  172. MohanKumar K, Namachivayam K, Song T, et al. A murine neonatal model of necrotizing enterocolitis caused by anemia and red blood cell transfusions. Nat Commun 2019;10(1):3494. DOI: 10.1038/s41467-019-11199-5.
  173. Namachivayam K, Blanco CL, MohanKumar K, et al. Smad7 inhibits autocrine expression of TGF-beta2 in intestinal epithelial cells in baboon necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2013;304(2):G167–G180. DOI: 10.1152/ajpgi.00141.2012.
  174. Smith PD, S
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.