Skip to main content

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 184))

Abstract

Thymus colonization during embryogenesis starts with the accumulation of basophilic cells in the jugular vein, in capillaries and in the mesenchyme surrounding the thymus. In birds the extrinsic origin of these basophilic cells, which are considered to be hematopoietic precursors, was established by the construction of quail-chick chimaeras (Le Douarin 1978; Le Douarin and Jotereau 1980). Using this technique the group of Le Douarin demonstrated that the thymus of birds is colonized mainly in three waves during embryogenesis and the first few days following hatching (Jotereau and Le Douarin 1982; Coltey et al. 1987). In mice, the thymus is colonized by hematopoietic precursors at days 10 and 13 of embryogenesis (Jotereau et al. 1987). A similar process, albeit at a lower level, may occur throughout life (Scollay et al. 1986; Donskoy and Goldschneider 1992). The major cellular events of thymus homing are illustrated in Fig. 1.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Adachi S, Ebi Y, Nishikawa S, Hayashi S, Yamazaki M, Kasugai T, Yamamura T, Nomura S, Kitamura Y (1992) Necessity of extracellular domain of W (c-kit) receptors for attachment of murine cultured mast cells to fibroblasts. Blood 79: 650–656.

    PubMed  CAS  Google Scholar 

  • Ben Slimane S, Houllier F, Tucker G, Thiery JP (1983) In vitro migration of avian hemopoietic cells to the thymus. Cell Diff 13: 1–24

    Article  CAS  Google Scholar 

  • Champion S, Imhof BA, Savagner P, Thiery JP (1986) The embryonic thymus produces chemotactic peptides involved in the homing of hemopoietic precursors. Cell 44: 781–790

    Article  PubMed  CAS  Google Scholar 

  • Coltey M, Jotereau FV, Le Douarin NM(1987) Evidence for a cyclic renewal of lymphocyte precursor cells in the intraembryonic chick thymus. Cell Diff 22: 71–82

    Google Scholar 

  • Dargemont C, Dunon D, Deugnier MA, Denoyelle M, Girault JM, Lederer F, Le KHD, Godeau F, Thiery JP, Imhof BA (1989) Thymotaxin, a chemotactic protein, is identical to β2–microglobulin. Science 246: 803–806

    Article  PubMed  CAS  Google Scholar 

  • Dargemont C, Dunon D, Salamero J, Deugnier M-A, Davoust J, Thiery JP (1991) Overproduction and secretion of β2–microglobulin by a rat thymic epithelial cell line that expresses MHC class heavy chain. J Cell Sei 98: 559–565

    CAS  Google Scholar 

  • de Vries P, Brasel KA, McKenna HJ, Williams DE, Watson JD (1992) Thymus reconstitution by c-kit-expressing hematopoietic stem cells purified from adult mouse bone marrow. J Exp Med 176: 1503–1509

    Article  PubMed  Google Scholar 

  • Deugnier MA, Imhof BA, Bauvois B, Dunon D, Denoyelle M, Thiery J P (1989) Characterization of rat T cell precursors sorted by chemotactic migration toward thymotaxin. Cell 56: 1073–1083

    Article  PubMed  CAS  Google Scholar 

  • Dieterlen-Lièvre F (1984) Blood in chimeras. In: Le Douarin NM, McLaren A (eds) Chimeras in developmental biology. Academic, London, pp 133–163

    Google Scholar 

  • Donskoy E, Goldschneider I (1992) Thymocytopoiesis is maintained by blood-borne precursors throughout posnatal life. J Immunol 148: 1604–1612

    PubMed  CAS  Google Scholar 

  • Dunon D, Imhof BA (1991) Migration of hemopoietic precursors toward β2–microglobulin is involved in thymus colonization of chicken embryos. In: Imhof BA, Berrih-Aknin S, Ezine S (eds) Lymphatic tissues and in vivo immune responses. Dekker, New York, pp 953–957

    Google Scholar 

  • Dunon D, Kaufman J, Salomonsen J, Skjoedt K, Vainio O, Thiery JP, Imhof, BA (1990) T cell precursor migration towards β2–microglobulin is involved in thymus colonization of chicken embryos. EM BO J 9: 3315–3322

    PubMed  CAS  Google Scholar 

  • Fleischman RA, Custer RP, Mintz B (1982)Totipotent hematopoietic stem cells: normal self renewal and differentiation after transplantation between mouse fetuses. Cell 30: 351–359

    Google Scholar 

  • Günthert U, Hofman M, Rudy W, Reber S, Zoller M, Haussmann I, Matzku S, Wenzel A, Ponta H, Herrlich P (1991) A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cell. Cell 65: 13–24

    Article  PubMed  Google Scholar 

  • Haar JL, Loor F (1981) Selective migration of ‘null’ cells towards a thymus factor in vitro. Thymus 3: 187–194

    PubMed  CAS  Google Scholar 

  • He Q, Hyman R, Ishihara K, Kincade PW (1992) Molecular isoforms of murine CD44 and evidence that the membrane proximal domain is not critical for hyaluronate recognition. J Cell Biol 119: 1711–1719

    Article  PubMed  CAS  Google Scholar 

  • Horst E, Meijer CJLM, Duijvestjin AM, Hartwig N, Van der Harten HJ, Pals S (1990) The ontogeny of human lymphocyte recirculation: high endothelial cell antigen (HECA-452) and CD44 homing receptor expression in the development of the immune system. Eur J Immunol 20: 1483–1489

    Article  PubMed  CAS  Google Scholar 

  • Huber AR, Kunkel SL, Todd RF III, Weiss SJ (1991) Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 254: 99–102

    Article  PubMed  CAS  Google Scholar 

  • Imaizumi A, Torisu M, Yoshida T (1987) A chemotactic factor for rat thymocytes may regulate T-lymphocyte migration toward the thymic microenvironment. Cell Immunol 108: 53–63

    Article  PubMed  CAS  Google Scholar 

  • Imaizumi A, Torisu M, Watanabe H, Yoshida T (1989) Migration of putative progenitor T cells in response to thymus-derived chemotactic factors. Cell Immunol 120: 301–313

    Article  PubMed  CAS  Google Scholar 

  • Imhof BA, Deugnier MA, Girault JM, Champion S, Damais C, Itoh T, Thiery JP (1988) Thymotaxin: a thymic epithelial peptide chemotactic for T-cell precursors. Proc Natl Acad Sei USA 85: 7699–7703

    Article  CAS  Google Scholar 

  • Imhof BA, Deugnier MA, Bauvois B, Dunon D, Thiery JP (1989) Properties of pre-T cells and their chemotactic migration to the thymus. In: Kendall MD, Ritter MA (eds) Thymus update, vol 2. Harwood Academic, Chur, Switzerland pp 3–19

    Google Scholar 

  • Imhof BA, Skjoedt K, Thiery J P, Dunon D (1990) Chemotaxis: a molecular mechanism involved in thymus colonization. In: Le Douarin NM, Dieterlen-Lièvre F, Smith J (eds) The avian model in developmental biology: from organism to genes. CNRS, pp 251–259

    Google Scholar 

  • Imhof BA, Ruiz P, Hesse B, Palacios R, Dunon D (1991) EA-1, a novel adhesion molecule involved in the homing of progenitor T lymphocytes to the thymus. J Cell Biol 114: 1069–1078

    Article  PubMed  CAS  Google Scholar 

  • Jotereau FV, Le Douarin NM (1982) Demonstration of a cyclic renewal of the lymphocyte precursor cells n the quail thymus during embryonic and perinatal life. J Immunol 129: 1869–1877

    PubMed  CAS  Google Scholar 

  • Jotereau FV, Houssaint E, Le Douarin NM (1980) Lymphoid stem cell homing to the early thymic primordium of the avian embryo. Eur J Immunol 10: 620–627

    Article  PubMed  CAS  Google Scholar 

  • Jotereau F, Heuze F, Salomon-Vie V, Gascan H (1987) Cell kinetics in the fetal mouse thymus: precursor cell input, proliferation, and emigration. J Immunol 138: 1026–1030

    PubMed  CAS  Google Scholar 

  • Kaplan HS, Brown MB (1952) Effect of peripheral shieldings on lymphoid tissue response to irradiation in C57 Black mice. Science 116: 195

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto TK, Jutila MA, Berg EL, Butcher EC (1989) Neutrophil Mac-1 and Mel-14 adhesion proteins inversely regulated by chemotactic factors. Science 245: 1238–1241

    Article  PubMed  CAS  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York

    Google Scholar 

  • Kudo C, Araki A, Matsushima K, Sendo F (1991) Inhibition of IL-8-induced W3/25 + (CD4 +) T lymphocyte recruitment into subcutaneous tissues of rats by selective depletion of in vivo neutrophils with a monoclonal antibody. J Immunol 147: 2196–2201

    PubMed  CAS  Google Scholar 

  • Kyewski BA (1987) Seeding of thymic microenvironments defined by distinct thymocyte-stromal interactions is developmentally controlled. J Exp Med 166: 520–538

    Article  PubMed  CAS  Google Scholar 

  • Le Douarin NM (1978) Ontogeny of hematopoietic organs studied in avian embryo interspecific chimeras. In: Differentiation of normal and neoplastic hematopoietic cells. Cold Spring Harbor, New York, pp 5–31

    Google Scholar 

  • Le Douarin NM, Jotereau FV (1980) Homing of lymphoid stem cells to the thymus and bursa of Fabricius studied in avian embryo chimaeras. In Fangerean M, Daurret J (eds) Immunology 80. Academic, London, pp 285–302

    Google Scholar 

  • Le Douarin NM, Jotereau FV, Houssaint E, Thiery JP (1984) Primary lymphoid organ ontogeny in birds. In: Le Douarin NM, McLaren A (eds) Chimeras in developmental biology. Academic, London, pp 179–216

    Google Scholar 

  • Lepault F, Coffman RL, Weissman IL (1983) Characteristics of thymus homing bone marrow cells. J Immunol 131: 64–69

    PubMed  CAS  Google Scholar 

  • Lotz MM, Korzelius CA, Mercurio AM (1990) Human colon carcinoma cells use multiple receptors to adhere to laminin: involvement of α6β4 and α6β1 integrins. Cell Regul 1: 249–257

    PubMed  CAS  Google Scholar 

  • Moore MAS, Metcalf D (1970) Ontogeny of the hematopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 18: 279–296

    Article  PubMed  CAS  Google Scholar 

  • Moore MAS, Owen JJT (1967) Experimental studies on the development of the thymus. J Exp Med 126: 715–726

    Article  PubMed  CAS  Google Scholar 

  • Nagel MD, Nagel J, Jacquot R (1981) Early erythropoiesis in foetal rat bone marrow: evidence for a liver-to-bone marrow relay. J Embryol Exp Morphol 64: 275–293

    PubMed  CAS  Google Scholar 

  • O’Neill HC (1987) Isolation of a thymus homing lyt-2-,L3T4-T-Cell line from mouse spleen. Cell Immunol 109: 222–230

    Article  PubMed  Google Scholar 

  • O’Neill HC (1989) Antibody which defines a subset of bone marrow cells that can migrate to the thymus. Immunology 68: 59–65

    PubMed  Google Scholar 

  • O’Neill HC, Ni K, O’Neill TJ (1992) Lymphoid precursor cell lines have capacity to migrate to multiple lymphoid sites. Immunology 76: 631–635

    PubMed  Google Scholar 

  • Owen JJ, Raff M (1970) Studies on the differentiation of thymus-derived lymphocytes. J Exp Med 132: 1216

    Article  PubMed  CAS  Google Scholar 

  • Palacios R, Samaridis J (1991) Thymus colonization in the developing mouse embryo. Eur J Immunol 21: 109–113

    Article  PubMed  CAS  Google Scholar 

  • Palacios R, Samaridis J, Thorpe D, Leu T (1990) Identification and characterization of pro-T lymphocytes and lineage uncommitted lymphocyte precursors from mice with three novel surface markers. J Exp Med 172: 219–230

    Article  PubMed  CAS  Google Scholar 

  • Potorowski EF, Pyke KW (1985) Thymic microenvironmental factor: a possible chemoattractant for hemopoietic stem cells. Thymus 7: 345–356

    Google Scholar 

  • Pyke KW, Bach J-F (1981) In vitro migration of potential hemopoietic precursor from the murine fetus. Thymus 3: 1–7

    PubMed  CAS  Google Scholar 

  • Ruiz P, Imhof BA (1992) Embryonic colonization of the thymus by T cell progenitors as a model for metastasis. In: Zabes HM, Peters PE, Munk K (eds) Contributions to oncology. Karger, Basel, pp 318–331

    Google Scholar 

  • Ruiz P, Dunon D, Hesse B, Imhof BA (1991) T lymphocyte precursors adhere to thymic endothelium. In: Imhof BA, Berrih-Aknin S, Ezine S (eds) Lymphocyte reaction and in vivo immunology. Dekker, New York, pp 963–968

    Google Scholar 

  • Ruiz P, Dunon D, Sonnenberg A, Imhof BA (1993) Prevention of mouse melanoma metastasis by EA-1, a monoclonal antibody specific for α-integrins. Cell Adhesion Commun 1: 67–81

    Article  CAS  Google Scholar 

  • Savagner P, Imhof BA, Yamada KM, Thiery JP (1986) Homing of hemopoietic precursor cells to the embryonic thymus: characterization of an invasive mechanism induced by chemotactic peptides. J Cell Biol 103: 2715–2727

    Article  PubMed  CAS  Google Scholar 

  • Scollay R, Smith J, Stauffer V (1986) Dynamics of early T cells: Prothymocyte migration and proliferation in the adult mouse thymus. Immunol Rev 91: 129–157

    Google Scholar 

  • Shimamura M, Oku M, Ohta S, Yamagata T (1992) Haematopoietic cell lines capable of colonizing the thymus following in vivo transfer expressed T-cell receptor delta-gene immature mRNA. Immunology 77: 369–376

    PubMed  CAS  Google Scholar 

  • Smith WB, Gamble JR, Clark-Lewis I, Vadas MA (1991a) lnterleukin-8 induces neutrophil transendothelial migration. Immunology 72: 65–72

    Google Scholar 

  • Smith CW, Kishimoto TK, Abbass O, Hughes B, Rothlein R, Mclntire LV, Butcher E, Anderson DC (1991b) Chemotactic factors regulate lectin adhesion molecule 1 (LECAM-1)- dependent neutrophil adhesion to cytokine-stimulated endothelial cells in vitro. J Clin Invest 87: 609–618

    Article  PubMed  CAS  Google Scholar 

  • Sonnenberg A, Linders CJT, Modderman PW, Damsky CH, Aumailley M, Timpl R (1990) Integrin recognition of different cell-binding fragments of laminin (P1, E3, E8) and evidence that α6β1 but not α6β4 functions as a major receptor for fragment E8. J Cell Biol 110: 2145–2155

    Article  PubMed  CAS  Google Scholar 

  • Sy MS, Guo Y, Stamenkovic I (1991) Distinct effects of two CD44 isoforms on tumor growth in vivo J Exp Med 174: 859–866

    CAS  Google Scholar 

  • Terstappen LWMM, Huang S, Picker LJ (1992) Flow cytometric assessment of human T-cell differentiation in thymus and bone marrow. Blood 79: 666–677

    PubMed  CAS  Google Scholar 

  • Wadsworth S, Halvorson MJ, Coligan JE (1992) Developmentally regulated expression of the β4 integrin on immature mouse thymocytes. J Immunol 149: 421–428

    PubMed  CAS  Google Scholar 

  • Zigmond SH (1977) The ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol 75: 606–616

    Article  PubMed  CAS  Google Scholar 

  • Zijlstra M, Bix M, Simister NE, Loring JM, Raulet DH, Jaenisch R (1990) β2-macroglobulin deficient mice lack CD4–CD8 + cytolytic cells. Nature 344: 742–746

    Google Scholar 

  • Zimmerman GA, Prescott SM, Mclntyre TM (1992) Endothelial cell interactions with granulocytes: tethering and signaling molecules. Immunol Today 13: 93–99

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Springer-Verlag Berlin · Heidelberg

About this chapter

Cite this chapter

Dunon, D., Ruiz, P., Imhof, B.A. (1993). Pro-T Cell Homing to the Thymus. In: Dunon, D., Mackay, C.R., Imhof, B.A. (eds) Adhesion in Leukocyte Homing and Differentiation. Current Topics in Microbiology and Immunology, vol 184. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-78253-4_11

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-78253-4_11

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-78255-8

  • Online ISBN: 978-3-642-78253-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics