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Ultrastructural localization of fibronectin in bone marrow of the embryonic chick and its relationship to granulopoiesis

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Summary

Fibronectin was immunolocated in embryonic chick bone marrow by the use of both a direct peroxidase conjugated antiserum and an indirect Streptavidin bridge technique. Fibronectin is located in the extravascular granulopoietic compartment and, to a lesser extent, in the vascular, erythropoietic compartment. There is no evidence of fibronectin being associated with blood-stromal cell interactions involving either erythropoiesis or thrombopoiesis. However, mature thrombocytes display a substantial surface coat containing fibronectin. Much of the fibronectin appears to be situated on surfaces of those fibroblastic stromal cells which support granulopoiesis. Fibronectin containing extracellular material connects surfaces of developing granulocytes with surfaces of stromal cells. Fibronectin is a surface component of granulocytes as well as nearby stromal cells. However, there appear to be fewer ferritin particles per unit of surface on granulocytic cells. Many of the ferritin particles are not clearly associated with amorphous matrix material at cell surfaces. Immunocytochemical attempts to identify laminin were unsuccessful. These studies indicate that fibronectin is situated at sites where it could mediate adhesive interaction between granulopoietic cells and their stromal cells. Furthermore, cell surface-matrix interaction involving fibronectin could mediate migration of blood cells within the extravascular spaces.

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References

  • Ainsworth SK, Karnovsky MJ (1972) An ultrastructural staining method for enhancing the size and electron opacity of ferritin in thin sections. J Histochem Cytochem 20:225–229

    Google Scholar 

  • Akiyama SK, Yamada SS, Yamada KM (1986) Characterization of a 140-kD avian cell surface antigen as a fibronectin-binding molecule. J Cell Biol 102:442–448

    Google Scholar 

  • Ali IU, Hynes RO (1978) Effects of LETS glycoprotein on cell motility. Cell 14:439–446

    Google Scholar 

  • Bentley SA, Foidart J-M (1980) Some properties of marrow derived adherent cells in tissue culture. Blood 56:1006–1012

    Google Scholar 

  • Bentley SA, Tralka TS (1983) Fibronectin-mediated attachment of hematopoietic cells to stromal elements in continuous bone marrow culture. Exp Hematol 11:129–138

    Google Scholar 

  • Bentley SA, Foidart J-M, Kleinman HK (1984) Connective tissue elements in rat bone marrow: immunofluorescent visualization of the hematopoietic microenvironment. J Histochem Cytochem 32:114–116

    Google Scholar 

  • Bonnard C, Papermaster DS, Kraehenbuhl J-P (1984) The streptavidin-biotin bridge technique: application in light and electron microscope immunocytochemistry. In: Polak JM, Varndell IM (eds) Immunolabelling for electron microscopy. Elsevier, Amsterdam, pp 95–121

    Google Scholar 

  • Boucaut J-C, Darribere T (1983) Fibronectin in early amphibian embryos. Migrating mesodermal cells contact fibronectin established prior to gastrulation. Cell Tissue Res 234:135–145

    Google Scholar 

  • Campbell A, Wicha MS, Long M (1985) Extracellular matrix promotes the growth and differentiation of murine hematopoietic cells in vitro. J Clin Invest 75:2085–2090

    Google Scholar 

  • Cardarelli PM, Pierschbacher MD (1986) T-lymphocyte differentiation and the extracellular matrix: identification of a thymocyte subset that attaches specifically to fibronectin. Proc Natl Acad Sci USA 83:2647–2651

    Google Scholar 

  • Castro-Malaspina H, Gay RE, Resnick G, Kapoor N, Meyers P, Chiarieri D, McKenzie S, Broxmeyer HE, Moore MAS (1980) Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood 56:289–301

    Google Scholar 

  • Chen W-T, Greve JM, Gottlieb DI, Singer SJ (1985) Immunocytochemical localization of 140 kD cell adhesion molecules in cultured chicken fibroblasts, and in chicken smooth muscle and intestinal epithelial tissues. J Histochem Cytochem 33:576–586

    Google Scholar 

  • Curry JL, Trentin JJ (1967) Hemopoietic spleen colony studies. I. Growth and differentiation. Dev Biol 15:395–413

    Google Scholar 

  • Curry JL, Trentin JJ, Wolf N (1967) Hemopoietic spleen colony studies. II. Erythropoiesis. J Exp Med 125:703–725

    Google Scholar 

  • Dexter TM (1982) Stromal cell associated haemopoiesis. J Cell Physiol [Suppl] 1:87–94

    Google Scholar 

  • Duband JL, Thiery JP (1982a) Distribution of fibronectin in the early phase of avian cephalic neural crest cell migration. Dev Biol 93:308–323

    Google Scholar 

  • Duband JL, Theiry JP (1982b) Appearance and distribution of fibronectin during chick embryo gastrulation and neurulation. Dev Biol 94:337–350

    Google Scholar 

  • Duband JL, Rocher S, Chen W-T, Yamada KM (1986) Cell adhesion and migration in the early vertebrate embryo: location and possible role of the putative fibronectin receptor complex. J Cell Biol 102:160–178

    Google Scholar 

  • Fujimoto T, Yoshinaga K, Kono I (1985) Distribution of fibronectin on the migratory pathway of primordial germ cells in mice. Anat Rec 211:271–178

    Google Scholar 

  • Gardner JM, Hynes RO (1985) Interaction of fibronectin with its receptor on platelets. Cell 42:439–448

    Google Scholar 

  • Giancotti FG, Comoglia PM, Tarone G (1986) Fibronectin-plasma membrane interaction in the adhesion of hematopoietic cells. J Cell Biol 103:429–437

    Google Scholar 

  • Gualtieri RJ, Shadduck RK, Baker DG, Quesenberry PJ (1984) Hematopoietic regulatory factors produced in long-term murine bone marrow cultures and the effect of in vitro irradiation. Blood 64:516–525

    Google Scholar 

  • Harrison B, Reineke U, Smith M, Hellman S (1984) The morphology of hematopoietic layers in long-term mouse bone marrow. Blood Cells 10:451–466

    Google Scholar 

  • Hoffstein ST, Weissmann G, Pearlstein E (1981) Fibronectin is a component of the surface coat of human neutrophils. J Cell Sci 50:315–327

    Google Scholar 

  • Kamenov B, Longemecker BM (1985) Further evidence for the existence of ‘homing’ receptors on murine leukemia cells which mediate adherence to normal bone marrow stromal cells. Leuk Res 9:1529–1537

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137a

    Google Scholar 

  • Lause DB, Doran JE, Houston JA, Beezhold DH (1983) Modulation of rat lymphocyte transformation by plasma fibronectin. J Reticuloendo Soc 34:437–448

    Google Scholar 

  • Marino JA, Pensky J, Culp LA, Spagnuolo PJ (1985) Fibronectin mediates chemotactic factor-stimulated neutrophil substrate adhesion. J Lab Clin Med 105:725–730

    Google Scholar 

  • McCarthy JB, Furcht LT (1984) Laminin and fibronectin promote the heptotactic migration of B16 mouse melanoma cells in vitro. J Cell Biol 98:1474–1480

    Google Scholar 

  • Mollenhauer HH (1964) Plastic embedding mixtures for use in electron microscopy. Stain Technol 39:111–114

    Google Scholar 

  • Mosesson MW, Amrani DL (1980) The structure and biologic activities of plasma fibronectin. Blood 56:145–158

    Google Scholar 

  • Patel VP, Lodish HF (1984) Loss of adhesion of murine erythroleukemia cells to fibronectin during erythroid differentiation. Science 224:996–998

    Google Scholar 

  • Pierschbacher MD, Ruoslahti E (1984) Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309:30–33

    Google Scholar 

  • Piersma AH, Brockband KGM, Ploemacher RE, van Vliet E, Brakel-van Peer KMJ, Visser PJ (1985) Characterization of fibroblastic stromal cells from murine bone marrow. Exp Hematol 13:237–243

    Google Scholar 

  • Piotrowicz RS, Nugent SM, Kristopeit SM, Yamada KM, Kunicki TJ (1986) Chicken thrombocyte glycoprotein (GP) IIb-IIIa and the fibronectin receptor. J Cell Biol 103:5 32 a

    Google Scholar 

  • Pommier CG, O'shea J, Chused T, Yancey K, Frank MM, Takahashi T, Brown EJ (1984) Studies on the fibronectin receptors of human peripheral blood leukocytes. Morphologic and functional characterization. J Exp Med 159:137–151

    Google Scholar 

  • Reineke U, Hsieh P, Mauch P, Hellman S, Chen LB (1982) Cell types associated with fibronectin in long-term mouse bone marrow cultures. J Histochem Cytochem 30:235–244

    Google Scholar 

  • Sorrell JM, Weiss L (1980) Cell interactions between hematopoietic and stromal cells in the chick embryonic bone marrow. Anat Rec 197:1–19

    Google Scholar 

  • Sorrell JM, Weiss L (1982) Intercellular junctions in the hematopoietic compartments of embryonic chick bone marrow. Am J Anat 164:57–66

    Google Scholar 

  • Tavassoli M, Takahashi K (1982) Morphological studies on long-term culture of marrow cells: characterization of the adherent stromal cells and their interactions in maintaining the proliferation of hematopoietic stem cells. Am J Anat 164:91–111

    Google Scholar 

  • Turksen K, Aubin JE, Sodek J, Kalnins VI (1985) Localization of laminin, type IV collagen, fibronectin, and heparan sulfate proteoglycan in chick retinal pigment epithelium basement membrane during embryonic development. J Histochem Cytochem 33:665–671

    Google Scholar 

  • Waterhouse EJ, Quesenberry PJ, Balian G (1986) Collagen synthesis by murine bone marrow cell culture. J Cell Physiol 127:397–402

    Google Scholar 

  • Weiss RE, Reddi AH (1980) Synthesis and localization of fibronectin during collagenous matrix-mesenchymal cell interaction and differentiation of cartilage and bone in vivo. Proc Natl Acad Sci USA 77:2074–2078

    Google Scholar 

  • Wencel-Drake JD, Plow EF, Zimmerman TS, Painter RG, Ginsberg MH (1984) Immunofluorescent localization of adhesive glycoproteins in resting and thrombin-stimulated platelets. Am J Pathol 115:156–164

    Google Scholar 

  • Yamada KM (1981) Fibronectin and other structural proteins. In: Hay ED (ed) Cell biology of the extracellular matrix. Plenum, New York, pp 95–114

    Google Scholar 

  • Zipori D, Friedman A, Tamir M, Silverberg D, Malik Z (1984) Cultured mouse marrow cell lines: interactions between fibroblastoid cells and monocytes. J Cell Physiol 118:143–152

    Google Scholar 

  • Zipori D, Duksin D, Tamir M, Argaman A, Toledo J, Malik Z (1985) Cultured mouse marrow stromal cell lines. II. Distinct subtypes differing in morphology, collagen types, myelopoietic factors, and leukemic cell growth modulating activities. J Cell Physiol 122:81–90

    Google Scholar 

  • Zuckerman KS, Wicha MS (1983) Extracellular matrix production by the adherent cells of long-term murine bone marrow cultures. Blood 61:540–547

    Google Scholar 

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Sorrell, J.M. Ultrastructural localization of fibronectin in bone marrow of the embryonic chick and its relationship to granulopoiesis. Cell Tissue Res. 252, 565–571 (1988). https://doi.org/10.1007/BF00216643

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