CoChat
Sign Up
Cited by 47

The DOI matches its Crossref record; 31 of the 31 references it cites were found in a registry or an index.

Fetal‐derived immune cells at the roots of lifelong pathophysiology

Mass, Elvira, Gentek, Rebecca·2021·Frontiers in Cell and Developmental Biology
DOI 10.3389/fcell.2021.648313PMC PMC7940384
Open this paper in CoChat — free account

Abstract

Tissue-resident innate immune cells exert a wide range of functions in both adult homeostasis and pathology. Our understanding of when and how these cellular networks are established has dramatically changed with the recognition that many lineages originate at least in part from fetal sources and self-maintain independently from hematopoietic stem cells. Indeed, fetal-derived immune cells are found in most organs and serous cavities of our body, where they reside throughout the entire lifespan. At the same time, there is a growing appreciation that pathologies manifesting in adulthood may be caused by adverse early life events, a concept known as “developmental origins of health and disease” (DOHaD). Yet, whether fetal-derived immune cells are mechanistically involved in DOHaD remains elusive. In this review, we summarize our knowledge of fetal hematopoiesis and its contribution to adult immune compartments, which results in a “layered immune system.” Based on their ontogeny, we argue that fetal-derived immune cells are prime transmitters of long-term consequences of prenatal adversities. In addition to increasing disease susceptibility, these may also directly cause inflammatory, degenerative, and metabolic disorders. We explore this notion for cells generated from erythro-myeloid progenitors (EMP) produced in the extra-embryonic yolk sac. Focusing on macrophages and mast cells, we present emerging evidence implicating them in lifelong disease by either somatic mutations or developmental programming events resulting from maternal and early environmental perturbations.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fcell.2021.648313

Cites

31 of 31 references verified0 citation errors · 0 not checkable

Statistics

Figures

FIGURE 1 Layered hematopoiesis. The primitive and transient-definitive waves in the yolk sac (YS) give rise to erythro-myeloid progenitors (EMP) that will colonize the fetal liver (FL) consecutively. EMP arising at early stages will differentiate into macrophages and probably mast cells in tissues developing early during embryogenesis (brain, liver), while EMPs at later stages remain in the FL and will give rise to the same cell types driven by the demand of later developing tissues, such as the lung and skin. Hematopoietic stem cells (HSC) develop in the aorta-gonad-mesonephros (AGM) region before colonizing the FL. After the formation of the bone marrow (BM), HSC migrate to the BM cavity where they will constantly give rise to short-lived macrophages and mast cells. The cell of origin for mast cells and macrophages is color-indicated. For simplicity, blood-circulating intermediate precursor stages between EMP and macrophages are not depicted. Created with BioRender.com.
FIGURE 1 Layered hematopoiesis. The primitive and transient-definitive waves in the yolk sac (YS) give rise to erythro-myeloid progenitors (EMP) that will colonize the fetal liver (FL) consecutively. EMP arising at early stages will differentiate into macrophages and probably mast cells in tissues developing early during embryogenesis (brain, liver), while EMPs at later stages remain in the FL and will give rise to the same cell types driven by the demand of later developing tissues, such as the lung and skin. Hematopoietic stem cells (HSC) develop in the aorta-gonad-mesonephros (AGM) region before colonizing the FL. After the formation of the bone marrow (BM), HSC migrate to the BM cavity where they will constantly give rise to short-lived macrophages and mast cells. The cell of origin for mast cells and macrophages is color-indicated. For simplicity, blood-circulating intermediate precursor stages between EMP and macrophages are not depicted. Created with BioRender.com.CC BY · PubMed Central
FIGURE 2 Genetic and developmental programming of fetal-derived immune cells. Perturbation of the maternal environment e.g., by nutrition, smoking, and infection, leads to the production of mediators such as cytokines and lipids that will lead to epigenetic alterations in EMP and thereby, chronic activation of EMP-derived immune cells after birth. This switch from a homeostatic to a pro-inflammatory state due to developmental programming may cause or contribute to different diseases. In addition to naturally occurring somatic mutations in proliferating EMP and their progeny, maternal-derived hazardous materials may lead to DNA damage, which could eventually lead to a change in transcriptional programs and chronic activation of tissue-resident immune cells. Created with BioRender.com.
FIGURE 2 Genetic and developmental programming of fetal-derived immune cells. Perturbation of the maternal environment e.g., by nutrition, smoking, and infection, leads to the production of mediators such as cytokines and lipids that will lead to epigenetic alterations in EMP and thereby, chronic activation of EMP-derived immune cells after birth. This switch from a homeostatic to a pro-inflammatory state due to developmental programming may cause or contribute to different diseases. In addition to naturally occurring somatic mutations in proliferating EMP and their progeny, maternal-derived hazardous materials may lead to DNA damage, which could eventually lead to a change in transcriptional programs and chronic activation of tissue-resident immune cells. Created with BioRender.com.CC BY · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 190

  1. Aberg, 1993, Familial occurrence of atopic disease: genetic versus environmental factors., Clin. Exp. Allergy, 23, 829, 10.1111/j.1365-2222.1993.tb00260.x · DOI
  2. Afonja, 1998, Multilineage involvement and erythropoietin-’independent’ erythroid progenitor cells in a patient with systemic mastocytosis., Ann. Hematol., 77, 183, 10.1007/s002770050439 · DOI
  3. Akin, 2004, A novel form of mastocytosis associated with a transmembrane c-kit mutation and response to imatinib., Blood, 103, 3222, 10.1182/blood-2003-11-3816 · DOI · Paper page
  4. Alliot, 1999, Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain., Dev. Brain Res., 117, 145, 10.1016/S0165-3806(99)00113-3 · DOI · Paper page
  5. Aloi, 2015, The p53 transcriptional network influences microglia behavior and neuroinflammation., Crit. Rev. Immunol., 35, 401, 10.1615/CritRevImmunol.v35.i5.40 · DOI
  6. Alvarez-Silva, 2003, Mouse placenta is a major hematopoietic organ., Development, 130, 5437, 10.1242/dev.00755 · DOI · Paper page
  7. Anandan, 2010, Is the prevalence of asthma declining? Systematic review of epidemiological studies., Allergy Eur. J. Allergy Clin. Immunol., 65, 152, 10.1111/j.1398-9995.2009.02244.x · DOI
  8. Andersson, 2016, Prenatal maternal stress and atopic diseases in the child: a systematic review of observational human studies., Allergy Eur. J. Allergy Clin. Immunol., 71, 15, 10.1111/all.12762 · DOI
  9. Apostol, 2020, Training the fetal immune system through maternal inflammation—a layered hygiene hypothesis., Front. Immunol., 11, 10.3389/fimmu.2020.00123 · DOI · Paper page
  10. Asher, 2006, Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC phases one and three repeat multicountry cross-sectional surveys., Lancet, 368, 733, 10.1016/S0140-6736(06)69283-0 · DOI · Paper page
  11. Ayyadurai, 2017, Frontline science: corticotropin-releasing factor receptor subtype 1 is a critical modulator of mast cell degranulation and stress-induced pathophysiology., J. Leukoc. Biol., 102, 1299, 10.1189/jlb.2hi0317-088rr · DOI · Paper page
  12. Backman, 2017, Increased prevalence of allergic asthma from 1996 to 2006 and further to 2016—results from three population surveys., Clin. Exp. Allergy, 47, 1426, 10.1111/cea.12963 · DOI
  13. Badalian-Very, 2010, Recurrent BRAF mutations in Langerhans cell histiocytosis., Blood, 116, 1919, 10.1182/blood-2010-04-279083 · DOI
  14. Balistreri, 2019, Developmental programming of adult haematopoiesis system., Ageing Res. Rev., 54, 10.1016/j.arr.2019.100918 · DOI · Paper page
  15. Barbara, 2007, Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome., Gastroenterology, 132, 26, 10.1053/j.gastro.2006.11.039 · DOI · Paper page
  16. Barker, 2009, Growth and chronic disease: findings in the Helsinki birth cohort., Ann. Hum. Biol., 36, 445, 10.1080/03014460902980295 · DOI
  17. Bayon, 1996, Role of Kupffer cells in arresting circulating tumor cells and controlling metastatic growth in the liver., Hepatology, 23, 1224, 10.1002/hep.510230542 · DOI
  18. Beaudin, 2016, A transient developmental hematopoietic stem cell gives rise to innate-like B and T cells., Cell Stem Cell, 19, 768, 10.1016/j.stem.2016.08.013 · DOI · Paper page
  19. Beghini, 2001, Germline mutation in the juxtamembrane domain of the kit gene in a family with gastrointestinal stromal tumors and urticaria pigmentosa., Cancer, 92, 657, 10.1002/1097-0142(20010801)92:3<657::aid-cncr1367<3.0.co;2-d · DOI
  20. Berezowska, 2014, Adult-onset mastocytosis in the skin is highly suggestive of systemic mastocytosis., Mod. Pathol., 27, 19, 10.1038/modpathol.2013.117 · DOI · Paper page
  21. Berres, 2014, BRAF-V600E expression in precursor versus differentiated dendritic cells defines clinically distinct LCH risk groups., J. Exp. Med., 211, 669, 10.1084/jem.20130977 · DOI
  22. Berres, 2015, Progress in understanding the pathogenesis of Langerhans cell histiocytosis: back to histiocytosis X?, Br. J. Haematol., 169, 3, 10.1111/bjh.13247 · DOI
  23. Bian, 2020, Deciphering human macrophage development at single-cell resolution., Nature, 582, 571, 10.1038/s41586-020-2316-7 · DOI
  24. Biswas, 2014, Mast cells in cutaneous tumors: innocent bystander or maestro conductor?, Int. J. Dermatol., 53, 806, 10.1111/j.1365-4632.2012.05745.x · DOI
  25. Boeckxstaens, 2018, The emerging role of mast cells in irritable bowel syndrome., Gastroenterol. Hepatol., 14, 250
  26. Böiers, 2013, Lymphomyeloid contribution of an immune-restricted progenitor emerging prior to definitive hematopoietic stem cells., Cell Stem Cell, 13, 535, 10.1016/j.stem.2013.08.012 · DOI
  27. Boisset, 2010, In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium., Nature, 464, 116, 10.1038/nature08764 · DOI · Paper page
  28. Bowling, 2019, Cell competition: the winners and losers of fitness selection., Development, 146, 10.1242/dev.167486 · DOI
  29. Boyle, 2006, Can allergic diseases be prevented prenatally?, Allergy Eur. J. Allergy Clin. Immunol., 61, 1423, 10.1111/j.1398-9995.2006.01113.x · DOI · Paper page
  30. Bracken, 2002, Genetic and perinatal risk factors for asthma onset and severity: a review and theoretical analysis., Epidemiol. Rev., 24, 176, 10.1093/epirev/mxf012 · DOI
  31. Bradford, 2012, Association between early adverse life events and irritable bowel syndrome., Clin. Gastroenterol. Hepatol., 10, 385, 10.1016/j.cgh.2011.12.018 · DOI
  32. Brumby, 2003, Scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila., EMBO J., 22, 5769, 10.1093/emboj/cdg548 · DOI · Paper page
  33. Chang, 2016, Prenatal maternal distress affects atopic dermatitis in offspring mediated by oxidative stress., J. Allergy Clin. Immunol., 138, 468, 10.1016/j.jaci.2016.01.020 · DOI
  34. Coëffier, 2005, Epsilon germ-line and IL-4 transcripts are expressed in human intestinal mucosa and enhanced in patients with food allergy., Allergy Eur. J. Allergy Clin. Immunol., 60, 822, 10.1111/j.1398-9995.2005.00782.x · DOI
  35. Cohen-Aubart, 2018, Phenotypes and survival in Erdheim-Chester disease: results from a 165-patient cohort., Am. J. Hematol., 93, E114, 10.1002/ajh.25055 · DOI
  36. Contu, 2017, A review of the impact of maternal obesity on the cognitive function and mental health of the offspring., Int. J. Mol. Sci., 18, 10.3390/ijms18051093 · DOI
  37. Cordner, 2015, Effects of high-fat diet exposure on learning & memory., Physiol. Behav., 152, 363, 10.1016/j.physbeh.2015.06.008 · DOI
  38. Cunningham, 2013, Microglia regulate the number of neural precursor cells in the developing cerebral cortex., J. Neurosci., 33, 4216, 10.1523/JNEUROSCI.3441-12.2013 · DOI · Paper page
  39. Davies, 2002, Mutations of the BRAF gene in human cancer., Nature, 417, 949, 10.1038/nature00766 · DOI · Paper page
  40. De, 2018, Two distinct ontogenies confer heterogeneity to mouse brain microglia., Development, 145, 10.1242/dev.152306 · DOI
  41. De Bruijn, 2002, Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta., Immunity, 16, 673, 10.1016/S1074-7613(02)00313-8 · DOI
  42. Dege, 2020, Potently cytotoxic natural killer cells initially emerge from erythro-myeloid progenitors during Mammalian development., Dev. Cell, 53, 229, 10.1016/j.devcel.2020.02.016 · DOI · Paper page
  43. Deng, 2016, Early life exposure to traffic-related air pollution and allergic rhinitis in preschool children., Respir. Med., 121, 67, 10.1016/j.rmed.2016.10.016 · DOI
  44. Diamond, 2016, Diverse and targetable kinase alterations drive histiocytic neoplasms., Cancer Discov., 6, 154, 10.1158/2159-8290.CD-15-0913 · DOI
  45. Eguíluz-Gracia, 2016, Long-term persistence of human donor alveolar macrophages in lung transplant recipients., Thorax, 71, 1006, 10.1136/thoraxjnl-2016-208292 · DOI
  46. Ekström, 2015, Maternal body mass index in early pregnancy and offspring asthma, rhinitis and eczema up to 16 years of age., Clin. Exp. Allergy, 45, 283, 10.1111/cea.12340 · DOI
  47. Elsaid, 2020, A wave of bipotent T/ILC-restricted progenitors shapes the embryonic thymus microenvironment in a time-dependent manner., Blood, 45, 283, 10.1182/blood.2020006779 · DOI
  48. Fagiani, 2020, Targeting dementias through cancer kinases inhibition., Alzheimers Dement., 6, 10.1002/trc2.12044 · DOI · Paper page
  49. Fantin, 2010, Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction., Blood, 116, 829, 10.1182/blood-2009-12-257832 · DOI · Paper page
  50. Ferner, 2007, Guidelines for the diagnosis and management of individuals with neurofibromatosis., J. Med. Genet., 44, 81, 10.1136/jmg.2006.045906 · DOI
  51. Frieri, 2013, Pediatric mastocytosis: a review of the literature., Pediatr. Allergy Immunol. Pulmonol., 26, 175, 10.1089/ped.2013.0275 · DOI · Paper page
  52. Fuller-Thomson, 2009, Making a link between childhood physical abuse and cancer: results from a regional representative survey., Cancer, 115, 3341, 10.1002/cncr.24372 · DOI
  53. Geissmann, 2015, A stratified myeloid system, the challenge of understanding macrophage diversity., Semin. Immunol., 27, 353, 10.1016/j.smim.2016.03.016 · DOI
  54. Gekas, 2005, The placenta is a niche for hematopoietic stem cells., Dev. Cell, 8, 365, 10.1016/j.devcel.2004.12.016 · DOI · Paper page
  55. Gentek, Hemogenic endothelial fate mapping reveals dual developmental origin of mast cells., Immunity, 48, 1160, 10.1016/j.immuni.2018.04.025 · DOI · Paper page
  56. Gentek, Epidermal γδ T cells originate from yolk sac hematopoiesis and clonally self-renew in the adult., J. Exp. Med., 215, 2994, 10.1084/jem.20181206 · DOI
  57. Georgin-Lavialle, 2013, Mast cell leukemia., Blood, 121, 1285, 10.1182/blood-2012-07-442400 · DOI
  58. Ginhoux, 2010, Fate mapping analysis reveals that adult microglia derive from primitive macrophages., Science, 330, 841, 10.1126/science.1194637 · DOI · Paper page
  59. Ginhoux, 2016, Tissue-resident macrophage ontogeny and homeostasis., Immunity, 44, 439, 10.1016/j.immuni.2016.02.024 · DOI · Paper page
  60. Godin, 1995, Emergence of multipotent hemopoietic cells in the yolk sac and paraaortic splanchnopleura in mouse embryos, beginning at 8.5 days postcoitus., Proc. Natl. Acad. Sci. U.S.A., 92, 773, 10.1073/pnas.92.3.773 · DOI
  61. Gold, 2015, Macrophages and cellular immunity in Drosophila melanogaster., Semin. Immunol., 27, 357, 10.1016/j.smim.2016.03.010 · DOI
  62. Goldmann, 2013, A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation., Nat. Neurosci., 16, 1618, 10.1038/nn.3531 · DOI · Paper page
  63. Gordon-Keylock, 2013, Mouse extraembryonic arterial vessels harbor precursors capable of maturing into definitive HSCs., Blood, 122, 2338, 10.1182/blood-2012-12-470971 · DOI
  64. Grootens, 2019, Single-cell analysis reveals the KIT D816V mutation in haematopoietic stem and progenitor cells in systemic mastocytosis., EBioMedicine, 43, 150, 10.1016/j.ebiom.2019.03.089 · DOI
  65. Guilliams, 2017, Does niche competition determine the origin of tissue-resident macrophages?, Nat. Rev. Immunol., 17, 451, 10.1038/nri.2017.42 · DOI · Paper page
  66. Hanahan, 2011, Hallmarks of cancer: the next generation., Cell, 144, 646, 10.1016/j.cell.2011.02.013 · DOI · Paper page
  67. Haroche, 2015, Reproducible and sustained efficacy of targeted therapy with vemurafenib in patients with BRAF(V600E)-mutated Erdheim-Chester disease., J. Clin. Oncol., 33, 411, 10.1200/JCO.2014.57.1950 · DOI
  68. Hartmann, 2005, Novel germline mutation of KIT associated with familial gastrointestinal stromal tumors and mastocytosis., Gastroenterology, 129, 1042, 10.1053/j.gastro.2005.06.060 · DOI · Paper page
  69. Hatanaka, 2017, Disturbance in maternal environment leads to abnormal synaptic instability during neuronal circuitry development., Front. Neurosci., 11, 10.3389/fnins.2017.00035 · DOI
  70. Hayakawa, 1985, Progenitors for Ly-1 b cells are distinct from progenitors for other b cells., J. Exp. Med., 161, 1554, 10.1084/jem.161.6.1554 · DOI
  71. Héritier, 2018, Incidence and risk factors for clinical neurodegenerative Langerhans cell histiocytosis: a longitudinal cohort study., Br. J. Haematol., 183, 608, 10.1111/bjh.15577 · DOI
  72. Herzenberg, 2015, Layered evolution in the immune system: a view from history., Ann. N. Y. Acad. Sci., 1362, 1, 10.1111/nyas.12795 · DOI
  73. Herzenberg, 1989, Toward a layered immune system., Cell, 59, 953, 10.1016/0092-8674(89)90748-4 · DOI
  74. Hong, 2020, Long-term programming of CD8 T cell immunity by perinatal exposure to glucocorticoids., Cell, 180, 847, 10.1016/j.cell.2020.02.018 · DOI
  75. Hsieh, 2018, Gastrointestinal involvement in mast cell activation disorders., Immunol. Allergy Clin. North Am., 38, 429, 10.1016/j.iac.2018.04.008 · DOI
  76. Hsu, 2015, Prenatal particulate air pollution and asthma onset in urban children: identifying sensitive windows and sex differences., Am. J. Respir. Crit. Care Med., 192, 1052, 10.1164/rccm.201504-0658OC · DOI
  77. Hsu, 2014, Emerging interactions between skin stem cells and their niches., Nat. Med., 20, 847, 10.1038/nm.3643 · DOI
  78. Huang, 1994, In vitro differentiation of B cells and myeloid cells from the early mouse embryo and its extraembryonic yolk sac., Exp. Hematol., 22, 19
  79. Huang, 2018, S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense., Science, 359, 114, 10.1126/science.aam5809 · DOI
  80. Indinnimeo, 2016, Prevalence and risk factors for atopic disease in a population of preschool children in Rome: challenges to early intervention., Int. J. Immunopathol. Pharmacol., 29, 308, 10.1177/0394632016635656 · DOI
  81. Jawhar, 2015, Molecular profiling of myeloid progenitor cells in multi-mutated advanced systemic mastocytosis identifies KIT D816V as a distinct and late event., Leukemia, 29, 1115, 10.1038/leu.2015.4 · DOI
  82. Johnson, 2002, Environmental epidemiology of pediatric asthma and allergy., Epidemiol. Rev., 24, 154, 10.1093/epirev/mxf013 · DOI
  83. Julien, 2016, Origin of the hematopoietic system in the human embryo., FEBS Lett., 590, 3987, 10.1002/1873-3468.12389 · DOI
  84. Kanitakis, 2011, Self-renewal capacity of human epidermal Langerhans cells: observations made on a composite tissue allograft., Exp. Dermatol., 20, 145, 10.1111/j.1600-0625.2010.01146.x · DOI
  85. Keirsse, 2018, The role of hepatic macrophages in liver metastasis., Cell. Immunol., 330, 202, 10.1016/j.cellimm.2018.03.010 · DOI
  86. Kelly-Irving, 2013, Childhood adversity as a risk for cancer: findings from the 1958 British birth cohort study., BMC Public Health, 13, 10.1186/1471-2458-13-767 · DOI
  87. Kihlström, 2003, Exposure to high doses of birch pollen during pregnancy, and risk of sensitization and atopic disease in the child., Allergy Eur. J. Allergy Clin. Immunol., 58, 871, 10.1034/j.1398-9995.2003.00232.x · DOI · Paper page
  88. Kimura, 2016, The innate immune receptor Dectin-2 mediates the phagocytosis of cancer cells by Kupffer cells for the suppression of liver metastasis., Proc. Natl. Acad. Sci. U.S.A., 113, 14097, 10.1073/pnas.1617903113 · DOI
  89. Klooker, 2010, The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome., Gut, 59, 1213, 10.1136/gut.2010.213108 · DOI
  90. Kolter, 2019, A subset of skin macrophages contributes to the surveillance and regeneration of local nerves., Immunity, 50, 1482, 10.1016/J.IMMUNI.2019.05.009 · DOI
  91. Krämer, 2004, The effect of environmental tobacco smoke on eczema and allergic sensitization in children., Br. J. Dermatol., 150, 111, 10.1111/j.1365-2133.2004.05710.x · DOI
  92. Lee, 2018, Somatic APP gene recombination in Alzheimer’s disease and normal neurons., Nature, 563, 639, 10.1038/s41586-018-0718-6 · DOI · Paper page
  93. Leyva-Castillo, 2019, Mechanical skin injury promotes food anaphylaxis by driving intestinal mast cell expansion., Immunity, 50, 1262, 10.1016/j.immuni.2019.03.023 · DOI
  94. Li, 2012, Mouse embryonic head as a site for hematopoietic stem cell development., Cell Stem Cell, 11, 663, 10.1016/j.stem.2012.07.004 · DOI
  95. Li, 2018, Adult connective tissue-resident mast cells originate from late erythro-myeloid progenitors., Immunity, 49, 640, 10.1016/j.immuni.2018.09.023 · DOI · Paper page
  96. Li, 2016, Subregional localization and characterization of Ly6aGFP-expressing hematopoietic cells in the mouse embryonic head., Dev. Biol., 416, 34, 10.1016/j.ydbio.2016.05.031 · DOI
  97. Lilla, 2010, Mast cells contribute to the stromal microenvironment in mammary gland branching morphogenesis., Dev. Biol., 337, 124, 10.1016/j.ydbio.2009.10.021 · DOI · Paper page
  98. Lin, 2014, Lymphoid progenitor emergence in the murine embryo and yolk sac precedes stem cell detection., Stem Cells Dev., 23, 1168, 10.1089/scd.2013.0536 · DOI
  99. Litonjua, 1998, Parental history and the risk for childhood asthma: does mother confer more risk than father?, Am. J. Respir. Crit. Care Med., 158, 176, 10.1164/ajrccm.158.1.9710014 · DOI
  100. Liu, 2003, Prenatal prediction of infant atopy by maternal but not paternal total IgE levels., J. Allergy Clin. Immunol., 112, 899, 10.1016/j.jaci.2003.08.030 · DOI · Paper page
  101. Liu, 1991, In vitro development of murine T cells from prethymic and preliver embryonic yolk sac hematopoietic stem cells., Development, 113, 1315, 10.1242/dev.113.4.1315 · DOI
  102. Liu, 2015, Mast cells participate in corneal development in mice., Sci. Rep., 5, 10.1038/srep17569 · DOI · Paper page
  103. Liu, 2019, Fate mapping via Ms4a3 expression history traces monocyte-derived cells., bioRxiv, 10.1101/652032 · DOI
  104. Loyher, 2018, Macrophages of distinct origins contribute to tumor development in the lung., J. Exp. Med., 215, 2536, 10.1084/jem.20180534 · DOI · Paper page
  105. Luis, 2016, Initial seeding of the embryonic thymus by immune-restricted lympho-myeloid progenitors., Nat. Immunol., 17, 1424, 10.1038/ni.3576 · DOI
  106. Magnus, 2018, Association of maternal psychosocial stress with increased risk of asthma development in offspring., Am. J. Epidemiol., 187, 1199, 10.1093/aje/kwx366 · DOI
  107. Martincorena, 2018, Somatic mutant clones colonize the human esophagus with age., Science, 362, 911, 10.1126/science.aau3879 · DOI · Paper page
  108. Martinez, 1992, Increased incidence of asthma in children of smoking mothers., Pediatrics, 89, 21, 10.1542/peds.89.1.21 · DOI
  109. Mass, 2018, Delineating the origins, developmental programs and homeostatic functions of tissue-resident macrophages., Int. Immunol., 30, 493, 10.1093/intimm/dxy044 · DOI
  110. McClain, 2020, Histamine-dependent interactions between mast cells, glia, and neurons are altered following early-life adversity in mice and humans., Am. J. Physiol. Liver Physiol., 319, G655, 10.1152/ajpgi.00041.2020 · DOI · Paper page
  111. McGrath, 2015, Distinct sources of hematopoietic progenitors emerge before HSCs and provide functional blood cells in the mammalian embryo., Cell Rep., 11, 1892, 10.1016/j.celrep.2015.05.036 · DOI · Paper page
  112. Metchnikoff, 1905, Immunity in Infective Diseases., 10.5962/bhl.title.29861 · DOI
  113. Molderings, 2017, Risk of solid cancer in patients with mast cell activation syndrome: results from Germany and USA., F1000Research, 6, 10.12688/f1000research.12730.1 · DOI · Paper page
  114. Moore, 1970, Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo., Br. J. Haematol., 18, 279, 10.1111/j.1365-2141.1970.tb01443.x · DOI
  115. Moriuchi, 2020, RasV12 expression in microglia initiates retinal inflammation and induces photoreceptor degeneration., Invest. Ophthalmol. Vis. Sci., 61, 10.1167/iovs.61.13.34 · DOI
  116. Msallam, 2020, Fetal mast cells mediate postnatal allergic responses dependent on maternal IgE., Science, 370, 941, 10.1126/science.aba0864 · DOI · Paper page
  117. Naik, 2018, Review two to tango: dialog between immunity and stem cells in health and disease., Cell, 175, 908, 10.1016/j.cell.2018.08.071 · DOI
  118. Nardone, 2016, The interaction between the immune system and epigenetics in the etiology of autism spectrum disorders., Front. Neurosci., 10, 10.3389/fnins.2016.00329 · DOI
  119. Nayak, 2016, Long-term persistence of donor alveolar macrophages in human lung transplant recipients that influences donor specific immune responses., Am. J. Transplant., 16, 2300, 10.1111/AJT.13819 · DOI
  120. Pagliarini, 2003, A genetic screen in Drosophila for metastatic behavior., Science, 302, 1227, 10.1126/science.1088474 · DOI · Paper page
  121. Palis, 2017, Interaction of the macrophage and primitive erythroid lineages in the mammalian embryo., Front. Immunol., 7, 10.3389/fimmu.2016.00669 · DOI
  122. Palis, 1999, Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse., Development, 126, 5073, 10.1242/dev.126.22.5073 · DOI · Paper page
  123. Paolicelli, 2011, Synaptic pruning by microglia is necessary for normal brain development., Science, 333, 1456, 10.1126/science.1202529 · DOI · Paper page
  124. Park, 2003, Activated mast cells infiltrate in close proximity to enteric nerves in diarrhea-predominant irritable bowel syndrome., J. Korean Med. Sci., 18, 204, 10.3346/jkms.2003.18.2.204 · DOI
  125. Parkhurst, 2013, Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor., Cell, 155, 1596, 10.1016/j.cell.2013.11.030 · DOI · Paper page
  126. Parsons, 2016, Cellular immune defenses of Drosophila melanogaster., Dev. Comp. Immunol., 58, 95, 10.1016/j.dci.2015.12.019 · DOI
  127. Pascual, 2012, Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission., Proc. Natl. Acad. Sci. U.S.A., 109, E197, 10.1073/pnas.1111098109 · DOI · Paper page
  128. Payer, 1991, Circulating CD3+/T cell receptor V gamma 3+ fetal murine thymocytes home to the skin and give rise to proliferating dendritic epidermal T cells., J. Immunol., 146, 2536, 10.4049/jimmunol.146.8.2536 · DOI
  129. Pedersen, 2011, Global strategy for the diagnosis and management of asthma in children 5 years and younger., Pediatr. Pulmonol., 46, 1, 10.1002/ppul.21321 · DOI
  130. Pei, 2017, Polylox barcoding reveals haematopoietic stem cell fates realized in vivo., Nature, 548, 456, 10.1038/nature23653 · DOI
  131. Perdiguero, 2016, The development and maintenance of resident macrophages., Nat. Immunol., 17, 2, 10.1038/ni.3341 · DOI
  132. Perdiguero, 2015, The origin of tissue-resident macrophages: when an erythro-myeloid progenitor is an erythro-myeloid progenitor., Immunity, 43, 1023, 10.1016/j.immuni.2015.11.022 · DOI · Paper page
  133. Piccinni, 1993, Aeroallergen sensitization can occur during fetal life., Int. Arch. Allergy Immunol., 102, 301, 10.1159/000236541 · DOI
  134. Poh, 2017, Inhibition of hematopoietic cell kinase activity suppresses myeloid cell-mediated colon cancer progression., Cancer Cell, 31, 563, 10.1016/j.ccell.2017.03.006 · DOI
  135. Pohl, 2017, Early weaning stress induces chronic functional diarrhea, intestinal barrier defects, and increased mast cell activity in a porcine model of early life adversity., Neurogastroenterol. Motil., 29, 10.1111/nmo.13118 · DOI · Paper page
  136. Presumey, 2017, “Complement system in neural synapse elimination in development and disease,” in, Advances in Immunology, 53, 10.1016/bs.ai.2017.06.004 · DOI
  137. Raherison, 2007, In utero and childhood exposure to parental tobacco smoke, and allergies in schoolchildren., Respir. Med., 101, 107, 10.1016/j.rmed.2006.04.010 · DOI
  138. Reber, 2012, New models for analyzing mast cell functions in vivo., Trends Immunol., 33, 613, 10.1016/j.it.2012.09.008 · DOI · Paper page
  139. Reichman, 2008, Maternal pre-pregnancy obesity and diagnosis of asthma in offspring at age 3 years., Matern. Child Health J., 12, 725, 10.1007/s10995-007-0292-2 · DOI
  140. Ribatti, Tumor vascularity and tryptase-positive mast cells correlate with a poor prognosis in melanoma., Eur. J. Clin. Invest., 33, 420, 10.1046/j.1365-2362.2003.01152.x · DOI
  141. Ribatti, Neovascularisation, expression of fibroblast growth factor-2, and mast cells with tryptase activity increase simultaneously with pathological progression in human malignant melanoma., Eur. J. Cancer, 39, 666, 10.1016/s0959-8049(02)00150-8 · DOI
  142. Roseboom, 2001, Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview., Mol. Cell. Endocrinol., 185, 93, 10.1016/s0303-7207(01)00721-3 · DOI
  143. Satoh, 2012, B-RAF mutant alleles associated with Langerhans cell histiocytosis, a granulomatous pediatric disease., PLoS One, 7, 10.1371/journal.pone.0033891 · DOI
  144. Schneider, 2019, Tissue-resident group 2 innate lymphoid cells differentiate by layered ontogeny and in situ perinatal priming., Immunity, 50, 1425, 10.1016/j.immuni.2019.04.019 · DOI
  145. Schultze, 2019, Emerging principles in myelopoiesis at homeostasis and during infection and inflammation., Immunity, 50, 288, 10.1016/j.immuni.2019.01.019 · DOI
  146. Schürch, 2020, Coordinated cellular neighborhoods orchestrate antitumoral immunity at the colorectal cancer invasive front., Cell, 182, 1341, 10.1016/j.cell.2020.07.005 · DOI
  147. Scrimshaw, 1968, Interactions of nutrition and infection., Monogr. Ser. World Health Organ., 57, 3
  148. Sharma, 2020, Onco-fetal reprogramming of endothelial cells drives immunosuppressive macrophages in hepatocellular carcinoma., Cell, 183, 377, 10.1016/j.cell.2020.08.040 · DOI · Paper page
  149. Sheng, 2015, Fetal HSCs versus EMP2s., Immunity, 43, 10.1016/j.immuni.2015.11.023 · DOI
  150. Shigemoto-Mogami, 2014, Microglia enhance neurogenesis and oligodendrogenesis in the early postnatal subventricular zone., J. Neurosci., 34, 2231, 10.1523/JNEUROSCI.1619-13.2014 · DOI
  151. Shigeta, 2019, Endocardially derived macrophages are essential for valvular remodeling., Dev. Cell, 48, 617, 10.1016/j.devcel.2019.01.021 · DOI
  152. Siiskonen, 2015, Low numbers of tryptase+ and chymase+ mast cells associated with reduced survival and advanced tumor stage in melanoma., Melanoma Res., 25, 479, 10.1097/CMR.0000000000000192 · DOI
  153. Simic, 2020, Distinct waves from the hemogenic endothelium give rise to layered lymphoid tissue inducer cell ontogeny., Cell Rep., 32, 10.1016/j.celrep.2020.108004 · DOI · Paper page
  154. Simon, 2008, The role of oxygen availability in embryonic development and stem cell function., Nat. Rev. Mol. Cell Biol., 9, 285, 10.1038/nrm2354 · DOI
  155. Solano, 2014, Advancing the detection of maternal haematopoietic microchimeric cells in fetal immune organs in mice by flow cytometry., Chimerism, 5, 99, 10.4161/19381956.2014.959827 · DOI
  156. Song, 2018, The microglial response to neurodegenerative disease., Adv. Immunol., 139, 1, 10.1016/BS.AI.2018.04.002 · DOI
  157. Speight, 2013, Rare, germline mutation of KIT with imatinib-resistant multiple GI stromal tumors and mastocytosis., J. Clin. Oncol., 31, 10.1200/JCO.2012.42.0133 · DOI · Paper page
  158. Squarzoni, 2014, Microglia modulate wiring of the embryonic forebrain., Cell Rep., 8, 1271, 10.1016/j.celrep.2014.07.042 · DOI
  159. Stinson, 2019, The not-so-sterile womb: evidence that the human fetus is exposed to bacteria prior to birth., Front. Microbiol., 10, 10.3389/fmicb.2019.01124 · DOI
  160. Stremmel, 2018, Yolk sac macrophage progenitors traffic to the embryo during defined stages of development., Nat. Commun., 9, 10.1038/s41467-017-02492-2 · DOI
  161. Su, 2014, The p53 transcription factor modulates microglia behavior through microRNA-dependent regulation of c-Maf., J. Immunol., 192, 358, 10.4049/jimmunol.1301397 · DOI · Paper page
  162. Sugiyama, 2007, Early-life risk factors for occurrence of atopic dermatitis during the first year., Pediatrics, 119, 10.1542/peds.2006-0893 · DOI
  163. Susser, 2009, Timing in prenatal nutrition: a reprise of the dutch famine study., Nutr. Rev., 52, 84, 10.1111/j.1753-4887.1994.tb01395.x · DOI
  164. Takhar, 2007, Class switch recombination to IgE in the bronchial mucosa of atopic and nonatopic patients with asthma., J. Allergy Clin. Immunol., 119, 213, 10.1016/j.jaci.2006.09.045 · DOI
  165. Talley, 1994, Gastrointestinal tract symptoms and self-reported abuse: a population-based study., Gastroenterology, 107, 1040, 10.1016/0016-5085(94)90228-3 · DOI
  166. Tang, 2004, A germline mutation in KIT in familial diffuse cutaneous mastocytosis., J. Med. Genet., 41, 10.1136/jmg.2003.015156 · DOI · Paper page
  167. Tariq, 1998, The prevalence of and risk factors for atopy in early childhood: a whole population birth cohort study., J. Allergy Clin. Immunol., 101, 587, 10.1016/S0091-6749(98)70164-2 · DOI
  168. Tober, 2007, The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis., Blood, 109, 1433, 10.1182/blood-2006-06-031898 · DOI
  169. Tóth-Jakatics, 2000, Cutaneous malignant melanoma: correlation between neovascularization and peritumor accumulation of mast cells overexpressing vascular endothelial growth factor., Hum. Pathol., 31, 955, 10.1053/hupa.2000.16658 · DOI
  170. Valent, 2017, Mastocytosis: 2016 updated WHO classification and novel emerging treatment concepts., Blood, 129, 1420, 10.1182/blood-2016-09-731893 · DOI · Paper page
  171. Veru, 2014, Prenatal maternal stress exposure and immune function in the offspring., Stress, 17, 133, 10.3109/10253890.2013.876404 · DOI
  172. Wasag, 2011, Novel, activating KIT-N822I mutation in familial cutaneous mastocytosis., Exp. Hematol., 39, 859, 10.1016/j.exphem.2011.05.009 · DOI · Paper page
  173. Weinberger, 1987, Implications of normal brain development for the pathogenesis of schizophrenia., Arch. Gen. Psychiatry, 44, 660, 10.1001/archpsyc.1987.01800190080012 · DOI · Paper page
  174. Werner, 2020, Cxcr4 distinguishes HSC-derived monocytes from microglia and reveals monocyte immune responses to experimental stroke., Nat. Neurosci., 23, 351, 10.1038/s41593-020-0585-y · DOI · Paper page
  175. Wlodarczyk, 2017, A novel microglial subset plays a key role in myelinogenesis in developing brain., EMBO J., 36, 3292, 10.15252/embj.201696056 · DOI · Paper page
  176. Wong, 1986, Properties of the earliest clonogenic hemopoietic precursors to appear in the developing murine yolk sac., Proc. Natl. Acad. Sci. U.S.A., 83, 3851, 10.1073/pnas.83.11.3851 · DOI
  177. Wu, 2012, Different implications of paternal and maternal atopy for perinatal IgE production and asthma development., Clin. Dev. Immunol., 2012, 10.1155/2012/132142 · DOI
  178. Yang, 2008, Nf1-dependent tumors require a microenvironment containing Nf1+/– and c-kit-dependent bone marrow., Cell, 135, 437, 10.1016/j.cell.2008.08.041 · DOI
  179. Yokota, 2006, Tracing the first waves of lymphopoiesis in mice., Development, 133, 2041, 10.1242/dev.02349 · DOI
  180. Yoshimoto, 2011, Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential., Proc. Natl. Acad. Sci. U.S.A., 108, 1468, 10.1073/pnas.1015841108 · DOI
  181. Yvernogeau, 2019, In vivo generation of haematopoietic stem/progenitor cells from bone marrow-derived haemogenic endothelium., Nat. Cell Biol., 21, 1334, 10.1038/s41556-019-0410-6 · DOI
  182. Zamenhof, 1966, Stimulation of the proliferation of cortical neurons by prenatal treatment with growth hormone., Science, 152, 1396, 10.1126/science.152.3727.1396 · DOI
  183. Zasłona, 2014, Resident alveolar macrophages suppress, whereas recruited monocytes promote, allergic lung inflammation in murine models of asthma., J. Immunol., 193, 4245, 10.4049/jimmunol.1400580 · DOI
  184. Zeigler, 2006, The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential., Development, 133, 4183, 10.1242/dev.02596 · DOI
  185. Zhang, 2016, Mast cells and irritable bowel syndrome: from the bench to the bedside., J. Neurogastroenterol. Motil., 22, 181, 10.5056/jnm15137 · DOI
  186. Zhang, 2006, A novel K509I mutation of KIT identified in familial mastocytosis-in vitro and in vivo responsiveness to imatinib therapy., Leuk. Res., 30, 373, 10.1016/j.leukres.2005.08.015 · DOI · Paper page
  187. Zhou, 2018, Circuit design features of a stable two-cell system circuit design features of a stable two-cell system., Cell, 172, 744, 10.1016/j.cell.2018.01.015 · DOI · Paper page
  188. Zhu, 2020, Developmental trajectory of prehematopoietic stem cell formation from endothelium., Blood, 136, 845, 10.1182/blood.2020004801 · DOI
  189. Zhu, 2002, Neurofibromas in NF1: schwann cell origin and role of tumor environment., Science, 296, 920, 10.1126/science.1068452 · DOI
  190. Zhu, 2017, Tissue-resident macrophages in pancreatic ductal adenocarcinoma originate from embryonic hematopoiesis and promote tumor progression., Immunity, 47, 323, 10.1016/J.IMMUNI.2017.07.014 · DOI

Cited by

Sorted by citations

See all 47

Metadata

Authors
Mass, E., & Gentek, R.
Venue
Frontiers in Cell and Developmental Biology
Publisher
Frontiers Media SA
Published
2021-02-23
Volume
9
ISSN
2296-634X
DOI
10.3389/fcell.2021.648313
PMC
PMC7940384
Cited by
47
References
31
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Deutsche Forschungsgemeinschaft (EXC2151-390873048)
  • Fritz Thyssen Stiftung
  • Daimler und Benz Stiftung
  • Kennedy Trust for Rheumatology Research

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review